Autophagy Modulated by Inorganic Nanomaterials
Identifieur interne : 000B12 ( Pmc/Corpus ); précédent : 000B11; suivant : 000B13Autophagy Modulated by Inorganic Nanomaterials
Auteurs : Lingling Guo ; Nongyue He ; Yongxiang Zhao ; Tonghua Liu ; Yan DengSource :
- Theranostics [ 1838-7640 ] ; 2020.
Abstract
With the rapid development of nanotechnology, inorganic nanomaterials (NMs) have been widely applied in modern society. As human exposure to inorganic NMs is inevitable, comprehensive assessment of the safety of inorganic NMs is required. It is well known that autophagy plays dual roles in cell survival and cell death. Moreover, inorganic NMs have been proven to induce autophagy perturbation in cells. Therefore, an in-depth understanding of inorganic NMs-modulated autophagy is required for the safety assessment of inorganic NMs. This review presents an overview of a set of inorganic NMs, consisting of iron oxide NMs, silver NMs, gold NMs, carbon-based NMs, silica NMs, quantum dots, rare earth oxide NMs, zinc oxide NMs, alumina NMs, and titanium dioxide NMs, as well as how each modulates autophagy. This review emphasizes the potential mechanisms underlying NMs-induced autophagy perturbation, as well as the role of autophagy perturbation in cell fate determination. Furthermore, we also briefly review the potential roles of inorganic NMs-modulated autophagy in diagnosis and treatment of disease.
Url:
DOI: 10.7150/thno.40414
PubMed: 32194863
PubMed Central: 7053187
Links to Exploration step
PMC:7053187Le document en format XML
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<author><name sortKey="He, Nongyue" sort="He, Nongyue" uniqKey="He N" first="Nongyue" last="He">Nongyue He</name>
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<front><div type="abstract" xml:lang="en"><p>With the rapid development of nanotechnology, inorganic nanomaterials (NMs) have been widely applied in modern society. As human exposure to inorganic NMs is inevitable, comprehensive assessment of the safety of inorganic NMs is required. It is well known that autophagy plays dual roles in cell survival and cell death. Moreover, inorganic NMs have been proven to induce autophagy perturbation in cells. Therefore, an in-depth understanding of inorganic NMs-modulated autophagy is required for the safety assessment of inorganic NMs. This review presents an overview of a set of inorganic NMs, consisting of iron oxide NMs, silver NMs, gold NMs, carbon-based NMs, silica NMs, quantum dots, rare earth oxide NMs, zinc oxide NMs, alumina NMs, and titanium dioxide NMs, as well as how each modulates autophagy. This review emphasizes the potential mechanisms underlying NMs-induced autophagy perturbation, as well as the role of autophagy perturbation in cell fate determination. Furthermore, we also briefly review the potential roles of inorganic NMs-modulated autophagy in diagnosis and treatment of disease.</p>
</div>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Theranostics</journal-id>
<journal-id journal-id-type="iso-abbrev">Theranostics</journal-id>
<journal-id journal-id-type="publisher-id">thno</journal-id>
<journal-title-group><journal-title>Theranostics</journal-title>
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<issn pub-type="epub">1838-7640</issn>
<publisher><publisher-name>Ivyspring International Publisher</publisher-name>
<publisher-loc>Sydney</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32194863</article-id>
<article-id pub-id-type="pmc">7053187</article-id>
<article-id pub-id-type="doi">10.7150/thno.40414</article-id>
<article-id pub-id-type="publisher-id">thnov10p3206</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
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</article-categories>
<title-group><article-title>Autophagy Modulated by Inorganic Nanomaterials</article-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Guo</surname>
<given-names>Lingling</given-names>
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<xref ref-type="aff" rid="A1">1</xref>
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<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A3">3</xref>
<xref ref-type="aff" rid="A4">4</xref>
<xref ref-type="corresp" rid="FNA_envelop">✉</xref>
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<given-names>Yongxiang</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Tonghua</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Deng</surname>
<given-names>Yan</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="corresp" rid="FNA_envelop">✉</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
State Key Laboratory of Bioelectronics, National Demonstration Center for Experimental Biomedical Engineering Education, School of Biological Science and Medical Engineering, Southeast University, Nanjing 210096, China</aff>
<aff id="A2"><label>2</label>
Hunan Key Laboratory of Biological Nanomaterials and Devices, College of life sciences and chemistry, Hunan University of Technology, Zhuzhou 412007, Hunan, China</aff>
<aff id="A3"><label>3</label>
Tibetan University of Tibetan Traditional Medicine, Lasa 850000, Tibetan, China</aff>
<aff id="A4"><label>4</label>
National Center for International Bio-targeting Theranostics, Guangxi Key Laboratory of Bio-targeting Theranostics, Collaborative Innovation Center for Targeting Tumor Theranostics, Guangxi Medical University, Guangxi 530021, China</aff>
<author-notes><corresp id="FNA_envelop">✉ Corresponding authors: <email>nyhe@seu.edu.cn</email>
(N. He), and <email>hndengyan@126.com</email>
(Y. Deng).</corresp>
<fn fn-type="COI-statement"><p>Competing Interests: The authors have declared that no competing interest exists.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2020</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>2</month>
<year>2020</year>
</pub-date>
<volume>10</volume>
<issue>7</issue>
<fpage>3206</fpage>
<lpage>3222</lpage>
<history><date date-type="received"><day>17</day>
<month>9</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>6</day>
<month>1</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© The author(s)</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link>
). See <ext-link ext-link-type="uri" xlink:href="http://ivyspring.com/terms">http://ivyspring.com/terms</ext-link>
for full terms and conditions.</license-p>
</license>
</permissions>
<abstract><p>With the rapid development of nanotechnology, inorganic nanomaterials (NMs) have been widely applied in modern society. As human exposure to inorganic NMs is inevitable, comprehensive assessment of the safety of inorganic NMs is required. It is well known that autophagy plays dual roles in cell survival and cell death. Moreover, inorganic NMs have been proven to induce autophagy perturbation in cells. Therefore, an in-depth understanding of inorganic NMs-modulated autophagy is required for the safety assessment of inorganic NMs. This review presents an overview of a set of inorganic NMs, consisting of iron oxide NMs, silver NMs, gold NMs, carbon-based NMs, silica NMs, quantum dots, rare earth oxide NMs, zinc oxide NMs, alumina NMs, and titanium dioxide NMs, as well as how each modulates autophagy. This review emphasizes the potential mechanisms underlying NMs-induced autophagy perturbation, as well as the role of autophagy perturbation in cell fate determination. Furthermore, we also briefly review the potential roles of inorganic NMs-modulated autophagy in diagnosis and treatment of disease.</p>
</abstract>
<kwd-group><kwd>inorganic nanomaterials</kwd>
<kwd>nanotechnology</kwd>
<kwd>nanotoxicity</kwd>
<kwd>autophagy perturbation</kwd>
<kwd>disease therapy</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec sec-type="intro"><title>Introduction</title>
<p>Nanomaterials are particulate materials with 50% or more of the constituent particles having one or more external dimensions in the size range of 1 to 100 nanometers <xref rid="B1" ref-type="bibr">1</xref>
. Among the engineered nanomaterials, the majority of inorganic nanomaterials (NMs) exhibit unique physicochemical and optical properties, such as that exhibited by superparamagnetic iron oxide nanoparticles (SPIONs) <xref rid="B2" ref-type="bibr">2</xref>
, the localized surface plasmon resonance (LSPR) effect of silver and gold nanoparticles <xref rid="B3" ref-type="bibr">3</xref>
, the antioxidant and free-radical scavenging capabilities of fullerenol <xref rid="B4" ref-type="bibr">4</xref>
, and the very high fluorescent brightness and excellent photostability of colloidal quantum dots <xref rid="B5" ref-type="bibr">5</xref>
. Various inorganic nanomaterials have been developed for advanced theranostics to incorporate with therapeutic and diagnostic agents in order to achieve stimuli-responsive drug release, synergetic and combinatory therapy, and multimodality therapies <xref rid="B6" ref-type="bibr">6</xref>
. Nanotechnology, which is generally described as the manipulation of nanoscale materials, now has a prominent role in industrial applications as well as in biomedical applications <xref rid="B7" ref-type="bibr">7</xref>
,<xref rid="B8" ref-type="bibr">8</xref>
. With the rapid development of nanotechnology, NMs have been comprehensively applied in modern society. Figure <xref ref-type="fig" rid="F1">1</xref>
shows various applications of inorganic NMs in the biomedical field.</p>
<p>Autophagy is a natural regulated mechanism that disassembles unnecessary or dysfunctional components, thus allowing the orderly degradation and recycling of cellular components. It is well known that autophagy plays dual role in cell survival and cell death <xref rid="B9" ref-type="bibr">9</xref>
,<xref rid="B10" ref-type="bibr">10</xref>
. A growing body of research has reported the ability of NMs to induce autophagy activation <xref rid="B11" ref-type="bibr">11</xref>
-<xref rid="B14" ref-type="bibr">14</xref>
. It has been reported that intracellular nanoparticles are not only degraded through the endo-lysosomal pathway, but also sequestered by autophagosomes and degraded through the auto-lysosomal pathway <xref rid="B15" ref-type="bibr">15</xref>
,<xref rid="B16" ref-type="bibr">16</xref>
. NMs-induced autophagy may be a cellular defensive mechanism against nanotoxicity <xref rid="B17" ref-type="bibr">17</xref>
, though it may also be a potential mechanism of nanotoxicity <xref rid="B18" ref-type="bibr">18</xref>
. Furthermore, both autophagy inhibition and activation have been reported as potent anticancer therapeutic strategies <xref rid="B19" ref-type="bibr">19</xref>
-<xref rid="B27" ref-type="bibr">27</xref>
. It should be noted that in cancer therapy, autophagy has a dual-opposite role, either opposing cell transformation and progression or facilitating survival under harsh conditions and in response to chemotherapeutics.</p>
<p>An in-depth understanding of inorganic NMs-modulated autophagy is required for the safety assessment of inorganic NMs. This review presents an overview of a set of inorganic NMs, consisting of iron oxide NMs, silver NMs, gold NMs, carbon-based NMs, silica NMs, quantum dots, rare earth oxide NMs, zinc oxide NMs, alumina NMs, and titanium dioxide NMs, and discusses how they modulate autophagy. Special emphasis is given on the mechanism underlying the current NMs induced-autophagy perturbation and the role of autophagy perturbation in cell-fate determination. Furthermore, we also briefly review the potential roles of inorganic NMs-modulated autophagy in diagnosis and treatment of disease.</p>
</sec>
<sec sec-type="materials"><title>Iron oxide nanomaterials</title>
<p>Iron oxide nanoparticles (IONPs) are promising materials for theranostic applications such as magnetic resonance imaging (MRI), hyperthermia, and drug delivery <xref rid="B28" ref-type="bibr">28</xref>
-<xref rid="B30" ref-type="bibr">30</xref>
.</p>
<p>As shown in Table <xref rid="T1" ref-type="table">1</xref>
, an elevated level of autophagy is frequently observed in cells treated with IONPs. It is well known that iron ions leached from intracellular IONPs might be involved in the generation of the extremely reactive hydroxyl radical (•OH) <italic>via</italic>
Harber-Weiss type reactions, increasing the intracellular reactive oxygen species (ROS) <xref rid="B31" ref-type="bibr">31</xref>
. Moreover, intracellular IONPs might also impair the function of mitochondria, enhancing the production of ROS. It has been reported that IONPs-induced increase of intracellular ROS might be a principle initiator of autophagy <xref rid="B32" ref-type="bibr">32</xref>
-<xref rid="B34" ref-type="bibr">34</xref>
. Increased production of ROS can result in the damage of not only macromolecules (proteins, lipids, and nucleic acids), but also of cell organelles (e.g. mitochondria and endoplasmic reticulum) <xref rid="B35" ref-type="bibr">35</xref>
. One possible reason for underlying IONPs-induced autophagy is to protect cells from oxidative stress through eliminating damaged macromolecules and cell organelles caused by excessive ROS. In such a scenario, IONPs-induced autophagy can be efficiently alleviated by addition of ROS scavengers, such as N-acetyl cysteine (NAC) and natural catalase <xref rid="B32" ref-type="bibr">32</xref>
,<xref rid="B34" ref-type="bibr">34</xref>
. Activation of autophagy in IONPs-treated cells might also be an attempt by cells to degrade internalized IONPs regarded as foreign materials and autophagic cargos by cells. Huang et al. <xref rid="B36" ref-type="bibr">36</xref>
reported that aggregated citrate-coated IONPs induced autophagy activation in HeLa cells while no elevation of cellular ROS was observed; moreover, blocking the uptake of IONPs by dynasore, which itself does not block autophagy, led to dramatically diminished autophagic effects. Xu et al <xref rid="B37" ref-type="bibr">37</xref>
reported that γ-Fe<sub>2</sub>
O<sub>3</sub>
modified with polydextrose sorbitol carboxymethyl ether upregulated the expression of caveolin-1 (Cav1) in RAW264.7 cells in a time-dependent manner. Moreover, overexpression of Cav1 significantly increased LC3Ⅱ expression in macrophages and also the uptake of SPIONs by macrophages. Similarly, knockdown of Cav1 using specific siRNA markedly reduced both the uptake of SPIONs and LC3Ⅱ expression. Results demonstrated the close correlation between increased cellular uptake of IONPs and elevated autophagic activity in cells, and also indicated that enhancing degradation activity in cells in order to eliminate the internalized IONPs might be a mechanism underlying IONPs-induced autophagy activation.</p>
<p>Many researchers have found that the molecular mechanism underlying IONPs-induced autophagy is determined by multiple factors including cell type and physicochemical properties of IONPs. Khan et al. <xref rid="B32" ref-type="bibr">32</xref>
reported that phosphorylation levels of mTOR and Akt significantly decreased while the phosphorylated AMPK significantly increased in Fe<sub>2</sub>
O<sub>3</sub>
-treated A549 cells, suggesting that the AMPK-mTOR-AKT signaling pathway might be involved in Fe<sub>2</sub>
O<sub>3</sub>
-induced autophagy. In this case, Fe<sub>2</sub>
O<sub>3</sub>
NPs might affect the early phase of autophagy through initiating phagophore nucleation. However, Shi et al. <xref rid="B38" ref-type="bibr">38</xref>
demonstrated that mTOR activation was not affected in OPM2 cells treated with Fe<sub>3</sub>
O<sub>4</sub>
NPs, whereas expression levels of Beclin 1, Atg14, and VSP34 were increased while Bcl-2 decreased in a dose- and time-dependent manner. These results indicated that Fe<sub>3</sub>
O<sub>4</sub>
NPs induced autophagy in OPM2 cells by modulating the Beclin l/Bcl-2/VPS34 complex, which plays a key role in modulating the elongation of autophagosomes. Jin et al <xref rid="B39" ref-type="bibr">39</xref>
reported that two commercially available IONPs (Resovist and Feraheme, 100 μg·mL<sup>-1</sup>
), upregulate p62 (an autophagy adapter protein that binds to ubiquitinated protein aggregates and LC3-Ⅱ) through activation of TLR4 signaling pathways, followed by phosphorylation of p38 and nuclear translocation of Nrf2. Then, p62 accumulation promotes autophagosome formation through factors necessary for aggresome-like induced structures (ALIS) formation and subsequent autophagic degradation. In this case, IONPs affected the later stage of autophagosome formation through upregulating expression of the autophagic adapter protein p62.</p>
<p>IONPs-modulated autophagy plays important roles in cell fate determination, as shown in Table <xref rid="T2" ref-type="table">2</xref>
. It has been reported that IONPs-modulated autophagy might play a pro-death role in cell fate <xref rid="B32" ref-type="bibr">32</xref>
-<xref rid="B34" ref-type="bibr">34</xref>
. Wang et al. <xref rid="B34" ref-type="bibr">34</xref>
demonstrated that carboxylate-modified α-Fe<sub>2</sub>
O<sub>3</sub>
NPs (150 μg·mL<sup>-1</sup>
) with a core size of 17 nm induced autophagic activity and cell death in PC12 cells through significantly elevating intracellular ROS in a relatively short time. However, cytotoxicity of α-Fe<sub>2</sub>
O<sub>3</sub>
NPs was remarkably relieved by inhibiting autophagy at an early stage with 3-MA. A similar phenomenon was observed by Khan et al. <xref rid="B32" ref-type="bibr">32</xref>
, demonstrating that bare Fe<sub>2</sub>
O<sub>3</sub>
NPs (100 μg·mL<sup>-1</sup>
) with a core size of 51 nm induced autophagy and significant necrotic cell death in A549 cells through remarkable elevation of intracellular ROS. However, pre-treatment of A549 cells with 3-MA was shown to reduce the conversion of LC3-I to LC3-II and promote cellular viability. The above results imply that the pro-death role of IONPs induced autophagic activity in cell fate. However, exact mechanisms underlying IONPs-induced autophagic cell death remain unknown. While “excessive” autophagy induced by IONPs through elevating intracellular ROS over a threshold may in principle be more likely to lead to a cell death outcome, definitive experimental demonstration is lacking, and no detailed information is available on the characteristics of this so-called “excessive autophagy”. Otherwise, the disrupted autophagic process may also be an explanation of IONPs-induced pro-death autophagy, as it has been reported that Fe<sub>3</sub>
O<sub>4</sub>
NPs extensively impair lysosomes, which would lead to the blockage of fusion of the autophagosome with the lysosome <xref rid="B40" ref-type="bibr">40</xref>
.</p>
<p>There are also many studies that suggest a pro-survival role of IONPs-induced autophagy in cell fate determination <xref rid="B37" ref-type="bibr">37</xref>
-<xref rid="B39" ref-type="bibr">39</xref>
,<xref rid="B41" ref-type="bibr">41</xref>
. It has been reported that polydextrose sorbitol carboxymethyl ether coated γ-Fe<sub>2</sub>
O<sub>3</sub>
(200 μg·mL<sup>-1</sup>
) with a core size of 6.5 nm induces autophagy activation in RAW264.7 cells, promoting the production of immunoregulatory cytokine IL-10 in macrophages through activation of Cav1-Notch1/HES1 signaling, leading to inhibition of inflammation in lipopolysaccharide (LPS)-induced sepsis and liver injury <xref rid="B37" ref-type="bibr">37</xref>
. Results indicate that the autophagic process generates pro-survival factors or activates pro-survival signaling pathways, and it is likely that IONPs induce pro-survival autophagy.</p>
<p>It should be noted that the effects of IONPs on autophagic activity and its role in cell fate determination should be considered together with the physicochemical properties of IONPs as well as the cell types (Table <xref rid="T2" ref-type="table">2</xref>
). It has been reported that surface modification <xref rid="B42" ref-type="bibr">42</xref>
, dispersity <xref rid="B36" ref-type="bibr">36</xref>
,<xref rid="B43" ref-type="bibr">43</xref>
, and composition <xref rid="B34" ref-type="bibr">34</xref>
of IONPs might all be important factors in IONPs-induced autophagy perturbation. In addition to physicochemical properties of IONPs, cell type is also a critical factor impacting IONPs-induced autophagy and cytotoxicity. Khan et al. <xref rid="B32" ref-type="bibr">32</xref>
found that bare IONPs synthesized by themselves selectively induced autophagy in cancer cells (A549), but not in normal cells (IMR-90). Park et al. <xref rid="B33" ref-type="bibr">33</xref>
,<xref rid="B44" ref-type="bibr">44</xref>
found that γ-Fe<sub>2</sub>
O<sub>3</sub>
NPs induced autophagic cell death in a murine peritoneal macrophage cell line, but not in murine alveolar macrophage cells.</p>
<p>IONPs-modulated autophagy exhibits a potential mechanism for anticancer therapeutics. It has been reported that IONPs exhibit anticancer effects through selectively inducing pro-death autophagy in cancer cells, but not in normal cells <xref rid="B32" ref-type="bibr">32</xref>
,<xref rid="B45" ref-type="bibr">45</xref>
. It has also been reported that IONPs-induced autophagy activation exhibits a synergistic effect with chemotherapeutics to enhance cancer therapy <xref rid="B46" ref-type="bibr">46</xref>
.</p>
<p>In summary, IONPs-induced elevation of intracellular ROS may be a major initiator responsible for IONPs-induced autophagy activity. Molecular mechanisms of IONPs-modulated autophagy, as well as the role of IONPs-modulated autophagy on cell fate, should be considered together with physicochemical properties of IONPs themselves, in addition to the model cell lines. As IONPs-modulated autophagy demonstrates promise for disease treatment, comprehensive studies describing the mechanisms of IONPs-modulated autophagy are required.</p>
</sec>
<sec sec-type="materials"><title>Silver nanomaterials</title>
<p>Sliver nanomaterials (AgNMs) not only possess broad-spectrum anti-microbial activities, but also exhibit desirable electronic, electrical, mechanical, and optical properties, and therefore have been used extensively in consumer applications <xref rid="B50" ref-type="bibr">50</xref>
-<xref rid="B52" ref-type="bibr">52</xref>
. AgNMs have also been suggested as potential sensitizers for cancer radiotherapy <xref rid="B53" ref-type="bibr">53</xref>
,<xref rid="B54" ref-type="bibr">54</xref>
.</p>
<p>AgNMs-induced autophagy perturbation has been frequently observed in a variety of cell lines, as shown in Table <xref rid="T1" ref-type="table">1</xref>
. Previous studies have shown that ROS can be generated by AgNMs owing to local surface plasmon resonance (SPR) <xref rid="B55" ref-type="bibr">55</xref>
. It has also been reported that AgNMs exposure caused an increase in cellular ROS, possibly due to the release of ionic silver <xref rid="B17" ref-type="bibr">17</xref>
. AgNMs-induced ROS increase was reported to initiate autophagy <xref rid="B56" ref-type="bibr">56</xref>
,<xref rid="B57" ref-type="bibr">57</xref>
. In this case, AgNPs-induced autophagy could be efficiently inhibited by antioxidants vitamin C (Vit C) and N-acetylcysteine (NAC) <xref rid="B57" ref-type="bibr">57</xref>
. AgNPs might also block fusion between autophagosomes and lysosomes <xref rid="B58" ref-type="bibr">58</xref>
. Possible mechanisms underlying AgNPs-induced autophagic flux blockage might be AgNPs-induced lysosome dysfunction <xref rid="B17" ref-type="bibr">17</xref>
,<xref rid="B58" ref-type="bibr">58</xref>
,<xref rid="B59" ref-type="bibr">59</xref>
, disorganization of the mitochondrial network <xref rid="B60" ref-type="bibr">60</xref>
, and ubiquitination interference <xref rid="B17" ref-type="bibr">17</xref>
. Villeret et al. <xref rid="B60" ref-type="bibr">60</xref>
showed that AgNPs altered mitochondrial organization and membrane potential, accompanied by increased expression of cargo-associated protein p62 and LC3-I, along with its conversion to LC3-II. Xu et al. <xref rid="B58" ref-type="bibr">58</xref>
reported that AgNPs block degradation of the autophagy substrate p62 and induce autophagosome accumulation in THP-1 cells. Moreover, lysosomal impairments including alkalization and decreased membrane stability were also observed in AgNP-treated THP-1 cells. Miyayama et al. <xref rid="B59" ref-type="bibr">59</xref>
reported that AgNPs induces autophagosome accumulation in A549 cells, accompanied by lysosomal pH alkalization. Moreover, p62 expression increases in a dose-dependent manner in AgNPs-treated A549 cells. The above results indicate that AgNPs treatment might result in a blockage of autophagic flux in cells; furthermore, lysosome dysfunction seems to be a primary mechanism.</p>
<p>Researchers have uncovered important details regarding the molecular mechanism of AgNMs-induced autophagic activity. It has been reported that levels of phosphorylated mTOR were significantly inhibited by AgNPs in Ba/F3 cells and were then restored by treatment with the antioxidants vitamin C (Vit C) and N-acetylcysteine (NAC). Results indicate that the ROS-mediated mTOR signaling pathway may be responsible for the autophagy activation induced by PVP-coated AgNPs <xref rid="B57" ref-type="bibr">57</xref>
. Wu et al. <xref rid="B61" ref-type="bibr">61</xref>
demonstrated that specifically inhibiting ERK and JNK significantly blocks AgNPs-induced autophagy activity in U251 cells. Results indicated that PVP-coated AgNPs induced autophagy in U251 cells through modulating extracellular-signal-regulated kinase (ERK) and the c-Jun N-terminal kinase (JNK). Lin et al. <xref rid="B62" ref-type="bibr">62</xref>
reported that AgNPs induced autophagy activation in Hela cells but did not alter the phosphorylation level of mTOR or its substrate, RPS6KB. Moreover, AgNPs-induced autophagy was significantly inhibited by wortmannin, an inhibitor of the PI3K pathway, suggesting that AgNPs-induced autophagy is PI3K-dependent and mTOR-independent.</p>
<p>AgNPs-modulated autophagy plays an important role in cell fate determination, as shown in Table <xref rid="T2" ref-type="table">2</xref>
. AgNPs-induced autophagy has been reported to be an anti-toxicity and a pro-survival process <xref rid="B61" ref-type="bibr">61</xref>
-<xref rid="B64" ref-type="bibr">64</xref>
. However, mechanisms underlying the AgNPs-induced cytoprotective autophagy have rarely been studied. Lin et al. <xref rid="B62" ref-type="bibr">62</xref>
reported that negatively charged, PVP-coated AgNPs (20 μg·mL<sup>-1</sup>
) with a near spherical shape and 26 nm core size increase both the expression of LC3-I and its conversion to LC3-Ⅱ in HeLa cells through activating autophagy. Moreover, inhibition of autophagy either by chemical inhibitors or ATG5 siRNA enhances AgNPs-elicited cancer cell killing. Therefore, it was suggested that PVP-coated AgNPs induce cytoprotective autophagy in HeLa cells. Recently, it was shown that PVP-coated AgNPs activate autophagy in HeLa cells through inducing nuclear translocation of TFEB, enhancing expression of autophagy-related genes. Furthermore, the same study demonstrated that knocking down the expression of TFEB attenuates autophagy induction while enhancing cell killing in HeLa cells treated with AgNPs <xref rid="B64" ref-type="bibr">64</xref>
. Results indicated that TFEB was a key mediator for AgNPs-induced cytoprotective autophagy.</p>
<p>It has also been reported that AgNPs-induced autophagic perturbation played a pro-death role in cell fate determination <xref rid="B57" ref-type="bibr">57</xref>
,<xref rid="B59" ref-type="bibr">59</xref>
,<xref rid="B65" ref-type="bibr">65</xref>
. It has furthermore been suggested that autophagy may serve as a trigger of apoptosis <xref rid="B66" ref-type="bibr">66</xref>
. One possible outcome of AgNPs-induced pro-death autophagy is the activation of apoptosis. Zhu et al. <xref rid="B57" ref-type="bibr">57</xref>
reported that PVP-coated AgNPs (8 μg·mL<sup>-1</sup>
) with a near-spherical shape and core size of 11 nm induce autophagy activation in normal hematopoietic cells (Ba/F3), accompanied by DNA damage and apoptosis. Moreover, inhibiting autophagy with either a chemical inhibitor or via Atg5 silencing significantly attenuated the autophagy of AgNPs in Ba/F3 cells, as well as apoptosis and DNA damage. Results indicated that AgNPs-induced autophagy contributes to apoptosis and DNA damage, which may be the mechanism underlying AgNPs-induced pro-death autophagy. It is well known that autophagy plays a crucial role in selective removal of stress-mediated protein aggregates and injured organelles, thereby protecting cells from stress. AgNPs-induced autophagy activation may also serve as a cellular defense mechanism against nanotoxicity. However, the subsequent autophagosome-lysosome fusion defect, which leads to autophagic flux blockage, was also frequently observed in cells treated with AgNPs <xref rid="B58" ref-type="bibr">58</xref>
,<xref rid="B59" ref-type="bibr">59</xref>
,<xref rid="B65" ref-type="bibr">65</xref>
. Moreover, AgNPs-induced autophagic flux blockage was suggested as a mechanism underlying AgNPs-induced pro-death autophagy <xref rid="B17" ref-type="bibr">17</xref>
.</p>
<p>As shown in Table <xref rid="T2" ref-type="table">2</xref>
, AgNMs with different physicochemical properties can have different effects on autophagy. The documented factors that may affect AgNMs-induced autophagy include physicochemical properties of AgNMs (e.g. concentration, size, shape) and cell types. Mishra AR et al. <xref rid="B65" ref-type="bibr">65</xref>
reported that PVP-coated AgNPs modulated autophagy in HepG2 cells in a concentration- and size-dependent manner. Villeret B et al. <xref rid="B60" ref-type="bibr">60</xref>
reported that AgNPs-induced autophagy in BEAS-2B cells was Rab9-dependent, whereas AgNPs induced ATG-5-dependent classical autophagy in NCI-H292 cells. AgNMs-modulated autophagy also seems to be shape-dependent, as it has been reported that silver nanowires (5 <italic>μ</italic>
g·mL<sup>-1</sup>
) induced cytoprotective autophagy in human monocytes <xref rid="B67" ref-type="bibr">67</xref>
, whereas silver nanoparticles (5 <italic>μ</italic>
g·mL<sup>-1</sup>
) interfered with the autophagic flux in human monocytes <xref rid="B58" ref-type="bibr">58</xref>
.</p>
<p>AgNMs-modulated autophagy provides a new target for cancer therapy, as it has been observed that autophagy and apoptosis are tightly connected by common upstream signaling components <xref rid="B61" ref-type="bibr">61</xref>
,<xref rid="B64" ref-type="bibr">64</xref>
. It has been reported that inhibiting AgNPs-induced autophagy leads to significantly increased cell death and effectively enhances the tumor-shrinking effect of AgNPs <xref rid="B62" ref-type="bibr">62</xref>
. AgNPs-induced autophagy has been reported to involve the radiosensitivity-enhancing effect of AgNPs, which may provide a useful strategy for improving the efficacy of AgNMs in cancer radiotherapy <xref rid="B61" ref-type="bibr">61</xref>
.</p>
<p>Since accumulation of AgNMs in the environment and subsequent entry into biological systems is inevitable, there are increasing bio-safety concerns related to AgNMs <xref rid="B68" ref-type="bibr">68</xref>
,<xref rid="B69" ref-type="bibr">69</xref>
. Thorough investigations are still required to elucidate the mechanisms underlying AgNMs-induced autophagy perturbation and its important role in cytotoxicity.</p>
</sec>
<sec sec-type="materials"><title>Gold nanomaterials</title>
<p>Because of their attractive physicochemical properties such as localized surface plasmon resonance, photothermal conversion, and biocompatibility <xref rid="B72" ref-type="bibr">72</xref>
, gold nanomaterials (AuNMs) appear to be a promising material for clinical diagnosis and treatment, including cancer cell near-infrared imaging and photothermal therapy <xref rid="B73" ref-type="bibr">73</xref>
, Raman signaling enhancement <xref rid="B74" ref-type="bibr">74</xref>
, and gene delivery <xref rid="B75" ref-type="bibr">75</xref>
.</p>
<p>AuNMs significantly increase the level of LC3-II, an autophagosome-building protein, in a variety of cell lines, as shown in Table <xref rid="T1" ref-type="table">1</xref>
. This indicates that AuNMs may induce autophagy perturbation in cells. It has been reported that AuNMs can induce autophagy, as well <xref rid="B76" ref-type="bibr">76</xref>
-<xref rid="B80" ref-type="bibr">80</xref>
. Mitochondrial damage and excessive ROS generation have been suggested as possible mechanisms underlying AuNMs-induced autophagy activation. Lu et al. <xref rid="B78" ref-type="bibr">78</xref>
fabricated gold nanoparticles and mesoporous silica nanoparticles into a nanohybrid (denoted GCMSNs), and they demonstrated that the presence of gold nanoparticles causes oxidative damage and mitochondrial dysfunction in A549 cells through the suppression of oxidative metabolism. Wan et al. <xref rid="B77" ref-type="bibr">77</xref>
demonstrated that cetyltrimethylammonium bromide-coated gold nanorods (CTAB-GNRs) induced autophagy activation in HCT116 cells, accompanied by decreased mitochondrial membrane potential and ROS accumulation. Furthermore, CTAB-GNRs-induced autophagy activation was partially abrogated by treatment with a mitochondrial membrane potential stabilizer (cyclosporine A) or ROS scavenger (NAC). Results indicate that gold nanorods induce autophagy activation through decreasing mitochondrial membrane potential and increasing ROS generation. AuNMs can also cause impairment of autophagosome/lysosome fusion, resulting in autophagic flux blockage. Lysosome impairment caused by AuNMs treatment was reported to be a principle mechanism underlying AuNMs-induced autophagic flux blockage. Ma et al. <xref rid="B81" ref-type="bibr">81</xref>
demonstrated that citrate-coated AuNPs (1 nM) were taken up into normal rat kidney cells through endocytosis, and the internalized AuNPs eventually accumulated in lysosomes and caused impairment of lysosome degradation capacity through alkalinization of lysosomal pH. Lysosome impairment made autophagosome/lysosome fusion defective, leading to autophagic flux blockage.</p>
<p>AuNPs-modulated autophagy can play a pro-survival role in cell fate determination. It is likely that the AuNPs-induced autophagic process generates pro-survival factors. Li et al. <xref rid="B82" ref-type="bibr">82</xref>
reported that negatively charged fetal bovine serum stabilized AuNPs (1 nM) with near-spherical shape and hydrodynamic diameter of 36nm, inducing autophagosome accumulation in MRC-5 cells, accompanied by upregulation of antioxidants and stress-response proteins. Results indicate that AuNPs-induced autophagy activation might serve as a defense pathway. AuNPs-induced autophagy activation can also lead to cell death <xref rid="B78" ref-type="bibr">78</xref>
; however, the underlying mechanism remains unknown. AuNPs may block autophagic flux subsequently, which usually leads to cell death. It has been reported that citrate-coated AuNPs with near-spherical shape and core size of 10-50 nm cause autophagic flux blockage in normal murine kidney cells through lysosomal impairment, ultimately leading to cell death <xref rid="B81" ref-type="bibr">81</xref>
.</p>
<p>Documented factors impacting AuNMs-modulated autophagy include surface chemistry <xref rid="B76" ref-type="bibr">76</xref>
,<xref rid="B77" ref-type="bibr">77</xref>
and particle size <xref rid="B81" ref-type="bibr">81</xref>
,<xref rid="B79" ref-type="bibr">79</xref>
. Zhang et al. <xref rid="B79" ref-type="bibr">79</xref>
reported that autophagy is activated in human periodontal ligament progenitor cells (PDLPs) by 13 and 45 nm AuNPs; however, autophagy is blocked by 5 nm AuNPs, and results indicate that AuNPs-modulated autophagy is size-dependent (Figure <xref ref-type="fig" rid="F2">2</xref>
A-C). Furthermore, 13 and 45 nm AuNPs not only activate autophagy in PDLPs, but also induce osteogenesis, whereas 5 nm AuNPs reduce osteogenic markers (Figure <xref ref-type="fig" rid="F2">2</xref>
D). Osteogenesis induced by 45 nm AuNPs can be reversed by autophagy inhibitors (3-MA and chloroquine) (Figure <xref ref-type="fig" rid="F2">2</xref>
E). Results indicate that AuNPs-modulated autophagy might be a mechanism underlying the osteogenic differentiation of PDLPs induced by AuNPs.</p>
<p>AuNMs-modulated autophagy appears to be a potential mechanism for cancer therapy. It has been reported that gold-silica nanohybrid-induced autophagy activation exhibits synergistic therapeutic effects with chemotherapy in A549 lung cancer xenografted nude mice <xref rid="B78" ref-type="bibr">78</xref>
. It has also been reported that AuNPs-modulated autophagy intensifies the TRAIL-induced apoptosis in non-small-cell lung cancer cells both <italic>in vitro</italic>
and <italic>in vivo</italic>
, indicating that the combination of TRAIL with AuNPs can be a potential therapeutic strategy for the treatment of non-small-cell lung cancer <xref rid="B80" ref-type="bibr">80</xref>
. Currently, the molecular mechanisms of AuNMs-modulated autophagy are poorly understood, and thus more investigations are required.</p>
</sec>
<sec sec-type="materials"><title>Carbon-based nanomaterials</title>
<p>“Carbon-based nanomaterials” mainly refers to fullerene and its derivative (fullerenol), carbon nanotube (CNT), graphene oxide (GO), and nanodiamond (ND). As shown in Figure <xref ref-type="fig" rid="F3">3</xref>
, carbon-based NMs possess unique physicochemical properties and have potential applications in many fields, especially biomedicine. Water-soluble fullerene derivative (fullerenol) possesses significant <italic>in vitro</italic>
and <italic>in vivo</italic>
antioxidant and free-radical scavenging capabilities, and it exhibits therapeutic potential against oxidative stress-associated diseases <xref rid="B83" ref-type="bibr">83</xref>
,<xref rid="B84" ref-type="bibr">84</xref>
. Single-walled carbon nanotubes (SWCNT) have been widely utilized in the field of Raman and photoacoustic imaging, and drug delivery benefits from their unique structure and physicochemical properties <xref rid="B85" ref-type="bibr">85</xref>
,<xref rid="B86" ref-type="bibr">86</xref>
. GO possesses unique electronic and mechanical properties as well as abundant oxygen functional groups; it demonstrates potential use in sensors, alternative energy, and biomedical applications such as bioimaging, cellular probing, drug delivery, and photothermal therapy <xref rid="B87" ref-type="bibr">87</xref>
-<xref rid="B92" ref-type="bibr">92</xref>
. ND has excellent mechanical and optical properties, high surface areas, tunable surface structures, chemical stability, and biocompatibility, which make it well suited for biomedical applications such as drug delivery, tissue scaffolds, and surgical implants <xref rid="B93" ref-type="bibr">93</xref>
. Although carbon-based NMs appear to be promising candidates for many biomedical applications, there is a growing body of literature detailing their cytotoxic effects.</p>
<p>Carbon-based NMs can induce autophagy perturbation in a variety of cells, as shown in Table <xref rid="T1" ref-type="table">1</xref>
. It has been reported that carbon-based NMs can induce autophagy activation <xref rid="B94" ref-type="bibr">94</xref>
. Proposed mechanisms underlying carbon-based NMs-induced autophagy activation include mitochondrial dysfunction and ER stress <xref rid="B95" ref-type="bibr">95</xref>
, accumulation of polyubiquitinated proteins <xref rid="B96" ref-type="bibr">96</xref>
, and/or increased ROS generation <xref rid="B97" ref-type="bibr">97</xref>
. Ubiquitination of nanomaterials could also be a mechanism underlying autophagy induction by carbon-based NMs, as it has been observed that ubiquitin coats NDs involved in selective autophagy through binding to autophagy receptors <xref rid="B98" ref-type="bibr">98</xref>
. Carbon-based NMs can also block autophagic flux. Carbon-based NMs-induced lysosomal dysfunction and cytoskeleton disruption have been suggested as the prominent mechanism of autophagic flux blockage <xref rid="B85" ref-type="bibr">85</xref>
,<xref rid="B99" ref-type="bibr">99</xref>
,<xref rid="B100" ref-type="bibr">100</xref>
.</p>
<p>Exploring molecular links between carbon-based NMs and autophagy perturbation is critically important in autophagy modulation. It has been reported that the AKT-TSC2-mTOR signaling pathway is responsible for the induction of autophagy by carboxylic acid-modified CNTs in A549 cells <xref rid="B101" ref-type="bibr">101</xref>
. Activation of class III PI3K and MEK/ERK1/2 signaling pathways was involved in autophagy induction by GO in PC12 cells <xref rid="B102" ref-type="bibr">102</xref>
. Another study showed that increasing intracellular calcium ion (Ca<sup>2+</sup>
) levels activates c-Jun N-terminal kinase (JNK), and subsequently leads to phosphorylation of Bcl-2 and dissociation of Beclin-1 from the Beclin-1-Bcl-2 complex, which was responsible for the autophagy induction by GO in HUVECs <xref rid="B103" ref-type="bibr">103</xref>
.</p>
<p>In addition to the signaling pathways mentioned above, Toll-like receptors have also been reported to play an important role in autophagy induction <xref rid="B104" ref-type="bibr">104</xref>
. Chen et al. <xref rid="B90" ref-type="bibr">90</xref>
reported that GO treatment of RAW 264.7 cells simultaneously triggered autophagy and Toll-like receptor 4 and 9 (TLR4/TLR9)-regulated inflammatory responses, and they further demonstrated that autophagy was at least partially regulated by the TLRs pathway. Small GTPase Rab26, which regulates receptor trafficking in the cytoplasm, may be a link between TLRs and autophagy. Binotti B et al. <xref rid="B105" ref-type="bibr">105</xref>
reported that Rab26 selectively localizes to presynaptic membrane vesicles and recruits both Atg16L1 and Rab33B, two components of the pre-autophagosomes. Moreover, overexpression of EGFP-tagged Rab26 induces the formation of autophagosomes in the cell bodies of hippocampal neurons. Li H et al. <xref rid="B106" ref-type="bibr">106</xref>
reported that Rab26 silencing activated the TLR4 signal pathway, but that overexpression of Rab26 partially inactivated lipopolysaccharide-induced TLR4 signaling pathway. Additional research is required to clarify the role of Rab26 in TLRs-dependent autophagy.</p>
<p>Carbon-based NMs-modulated autophagy plays an important role in cell fate determination. It has been reported that carbon-based NMs can be a pro-survival mechanism in cells <xref rid="B94" ref-type="bibr">94</xref>
. A likely possibility is that carbon-based NMs-induced autophagy enhances the degradation of toxic aggregate-prone proteins (e.g. mutant huntingtin <xref rid="B102" ref-type="bibr">102</xref>
). However, carbon-based NMs-induced autophagy can also lead to cell death <xref rid="B84" ref-type="bibr">84</xref>
,<xref rid="B95" ref-type="bibr">95</xref>
,<xref rid="B107" ref-type="bibr">107</xref>
,<xref rid="B96" ref-type="bibr">96</xref>
. It has been reported that PLCβ3/IP<sub>3</sub>
/Ca<sup>2+</sup>
/JNK signaling pathway was involved in sub-micrometer-sized GO- (SGO; 390.2 ± 51.4 nm) and nanometer-sized GO (NGO; 65.5 ± 51.4 nm)-induced autophagic cell death in endothelial cells <xref rid="B103" ref-type="bibr">103</xref>
. Factors affecting carbon-based NMs-modulated autophagy include surface coatings <xref rid="B101" ref-type="bibr">101</xref>
,<xref rid="B108" ref-type="bibr">108</xref>
, particle size <xref rid="B103" ref-type="bibr">103</xref>
, and shapes <xref rid="B100" ref-type="bibr">100</xref>
.</p>
<p>Carbon-based NMs-modulated autophagy has also been exploited for disease therapy. Fullerene nanocrystals have been reported to enhance the chemotherapeutic killing of cancer cells through autophagy modulation in HeLa cells <xref rid="B97" ref-type="bibr">97</xref>
. Xu et al. <xref rid="B109" ref-type="bibr">109</xref>
explored CaMKIIα as a regulator of fullerene C60 nanocrystals (nano-C60)-induced autophagy. They demonstrated that inhibition of CaMKIIα activity suppresses the degradation of nano-C60-induced autophagy by causing lysosomal alkalinization and enlargement, leading to enhanced cancer cell death. This investigation presented a promising strategy for improving the antitumor efficacy of nano-C60. GO effectively enhanced the clearance of mutant huntingtin (Htt), the aggregate-prone protein underlying the pathogenesis of Huntington's disease, through the activation of autophagy in GFP-Htt(Q74)/PC12 cells stably expressing green fluorescent protein-tagged Htt protein <xref rid="B102" ref-type="bibr">102</xref>
. Autophagic flux blockage by NDs has been reported to allosterically improve the therapeutic efficacy of arsenic trioxide (AOT)-based treatment in solid tumors <xref rid="B110" ref-type="bibr">110</xref>
. However, there is a lack of mechanistic data concerning the molecular links between carbon-based NMs-modulated autophagy and enhanced therapeutic effects, and thus more related studies are required.</p>
</sec>
<sec sec-type="materials"><title>Silica nanomaterials</title>
<p>Silica nanomaterials (SiNMs) are among the most abundantly manufactured engineered nanomaterials, serving as an additive to cosmetics, drugs, printer toners, varnishes, and even food <xref rid="B111" ref-type="bibr">111</xref>
. Mesoporous silica nanoparticles (SiNPs) have been exploited for drug delivery, diagnosis, and bioimaging due to their high specific surface area and pore volume, tunable pore structures, and excellent physicochemical stability <xref rid="B112" ref-type="bibr">112</xref>
-<xref rid="B116" ref-type="bibr">116</xref>
. With the growing applications of SiNMs, there are growing concerns about their potential hazards to human health. It has been reported that autophagy induction may attenuate cytotoxicity caused by SiNPs, as it has been reported that dioscin promoting autophagy in alveolar macrophages relieved crystalline-silica-stimulated ROS stress and facilitated cell survival <xref rid="B117" ref-type="bibr">117</xref>
.</p>
<p>As shown in Table <xref rid="T1" ref-type="table">1</xref>
, SiNPs induces autophagy perturbation in a variety of cell lines. SiNPs can also induce autophagy activation. Mechanisms underlying SiNPs-induced autophagy activation include cytoskeleton disruption <xref rid="B118" ref-type="bibr">118</xref>
, oxidative stress <xref rid="B119" ref-type="bibr">119</xref>
, ER stress <xref rid="B120" ref-type="bibr">120</xref>
, and mitochondrial damage <xref rid="B121" ref-type="bibr">121</xref>
. It has also been reported that SiNPs can block autophagic flux through lysosome impairment <xref rid="B122" ref-type="bibr">122</xref>
.</p>
<p>The PI3K/AKT/mTOR pathway was reported to be involved in surface negatively charged silica NPs-induced autophagy activation in HUVECs <xref rid="B123" ref-type="bibr">123</xref>
. It has also been reported that activation of the EIF2AK3 and ATF6 UPR pathways is responsible for autophagosome accumulation by silica NPs in L-02 cells <xref rid="B120" ref-type="bibr">120</xref>
. In another case, it was reported that autophagy induction by PEGylated silica-based NPs in MC3T3-E1 cells was dependent on the mitogen activated protein kinase ERK1/2 <xref rid="B124" ref-type="bibr">124</xref>
.</p>
<p>SiNMs-modulated autophagy plays dual roles in cell survival and cell death. One study showed that autophagy induction by bioactive SiNPs promoted <italic>in vitro</italic>
differentiation and mineralization of murine pre-osteoblasts (MC3T3-E1) <xref rid="B124" ref-type="bibr">124</xref>
. It was reported that SiNPs enhanced autophagic activity in HUVECs, accompanied by cellular homeostasis disruption and angiogenesis impairment <xref rid="B118" ref-type="bibr">118</xref>
. It has also been reported that SiNPs can block autophagic flux, which usually leads to cell death. Wang et al. <xref rid="B122" ref-type="bibr">122</xref>
reported that SiNPs induce increased LC3B-Ⅱ expression in hepatocytes in a dose- and time-dependent manner, in accordance with SiNPs-induced cytotoxicity in hepatocytes. However, p62 degradation was not observed in hepatocytes at any dose of SiNPs at any time. After treating with bafilomycin A1 (BafA1), which suppresses fusion between autophagosomes and lysosomes, LC3B-Ⅱ expression increases in hepatocytes treated with lower doses of SiNPs, whereas p62 expression increases only in cells exposed to lower doses of SiNPs. Furthermore, higher-dose SiNPs treatment caused lysosomal destruction, lysosomal cathepsin expression downregulation, and increased lysosomal membrane permeability. Results indicate that high-dose SiNPs inhibits autophagosome degradation via lysosomal impairment in hepatocytes, resulting in autophagy dysfunction.</p>
<p>Mesoporous silica NPs significantly sensitize doxorubicin for killing cancer cells by increasing ROS generation and triggering the mitochondria-related autophagic lysosome pathway <xref rid="B125" ref-type="bibr">125</xref>
. Results indicate that silica NMs-modulated autophagy may also be exploited for cancer therapy.</p>
</sec>
<sec><title>Quantum dots</title>
<p>Quantum dots (QDs) are nanoscale (2-10 nm) fluorescent colloids composed of semiconductor materials, commonly used as fluorescent probes for bioimaging fixed cells and tissues <xref rid="B5" ref-type="bibr">5</xref>
. It has also been reported that QDs have the potential to be used as multimodal contrast agents during drug delivery <xref rid="B126" ref-type="bibr">126</xref>
and in bioimaging <xref rid="B127" ref-type="bibr">127</xref>
. However, precautions should be taken when QDs are used <italic>in vivo</italic>
, as leaking of toxic core metals from QDs is able to generate ROS, which damage cellular membrane integrity, and inflict oxidative damage on intracellular DNA, proteins, and lipids <xref rid="B128" ref-type="bibr">128</xref>
,<xref rid="B129" ref-type="bibr">129</xref>
.</p>
<p>QDs can induce autophagy perturbation in cells, as shown in Table <xref rid="T1" ref-type="table">1</xref>
. QDs-caused oxidative stress has been reported to be responsible for QDs-induced autophagy <xref rid="B121" ref-type="bibr">121</xref>
,<xref rid="B130" ref-type="bibr">130</xref>
. QDs-modulated autophagy plays important roles in cell fate determination. It was reported that QDs-induced autophagy activation in a murine renal adenocarcinoma cell line is a defensive/survival mechanism against nanotoxicity <xref rid="B130" ref-type="bibr">130</xref>
. QDs-induced autophagy can also play a pro-death role in cell fate determination <xref rid="B5" ref-type="bibr">5</xref>
,<xref rid="B121" ref-type="bibr">121</xref>
. It has been reported that elevated autophagy is at least partially responsible for the <italic>in vivo</italic>
synaptic dysfunction induced by CdSe/ZnS QDs <xref rid="B131" ref-type="bibr">131</xref>
.</p>
</sec>
<sec sec-type="materials"><title>Rare earth oxide nanomaterials</title>
<p>Rare earth elements are a category of materials including 17 different members with similar chemical properties. Cerium is one of the rare earth elements that belongs to the lanthanide series. Cerium oxide (CeO<sub>2</sub>
) is routinely used in polishing glass and jewelry, and it is also used in catalytic converters for automobile exhaust systems and other commercial applications <xref rid="B132" ref-type="bibr">132</xref>
. Cerium oxide nanoparticles (NPs) are promising for therapeutic applications including antioxidant therapy, neuroprotection, radioprotection, and ocular protection <xref rid="B132" ref-type="bibr">132</xref>
-<xref rid="B135" ref-type="bibr">135</xref>
. Because of their clinical application prospects, the biosafety of rare earth oxide nanomaterials (REO NMs) is drawing increased attention. Cerium oxide NPs at relatively low doses have been reported to cause mitochondrial damage, overexpression of apoptosis-inducing factor, and autophagy induction in human peripheral blood monocytes <xref rid="B136" ref-type="bibr">136</xref>
. REO NMs can induce autophagy perturbation in a variety of cell lines, as shown in Table <xref rid="T1" ref-type="table">1</xref>
.</p>
<p>Neodymium is one of the rare earth elements that belong to the lanthanide series, as well. Autophagy induction by neodymium oxide NPs is accompanied by cell cycle arrest in S-phase, mild disruption of mitochondrial membrane potential, and inhibition of proteasome activity, as observed in non-small cell lung cancer cells (NCI-H460) <xref rid="B137" ref-type="bibr">137</xref>
. Another study reported that autophagy, induced by cerium oxide NPs through promoting activation of the transcription factor EB, promotes clearance of proteolipid aggregates in fibroblasts derived from a patient with late infantile neuronal ceroid lipofuscinosis <xref rid="B138" ref-type="bibr">138</xref>
. Zhang et al. <xref rid="B139" ref-type="bibr">139</xref>
reported that lanthanide-based upconversion nanoparticles (UCNs) are able to induce obvious autophagy and hepatotoxicity in mouse liver; furthermore, they demonstrated that coating with specific peptide RE-1 reduced autophagy and hepatotoxicity of UCNs. Zhu et al. <xref rid="B140" ref-type="bibr">140</xref>
demonstrated that UCNs induced pro-death autophagy in Kupffer cells and liver injury. Furthermore, inhibition of autophagy enhances Kupffer survival and further abrogates UCN-induced liver toxicity. Recently, Zhang et al. <xref rid="B141" ref-type="bibr">141</xref>
revealed the detailed mechanisms of UCNs-induced liver damage: insufficient PIP5K1B on the autolysosome membrane after treatment with UCNs causes disrupted phospholipid transition from PI(4)P to PI(4,5)P2 on the enlarged autolysosome membrane. This subsequently leads to clathrin recruitment failure and causes persistent, large autolysosomes in hepatocytes, which finally lead to hepatotoxicity.</p>
<p>Autophagic flux defect is caused by a series of rare-earth oxide NPs including La<sub>2</sub>
O<sub>3</sub>
, Gd<sub>2</sub>
O<sub>3</sub>
, Sm<sub>2</sub>
O<sub>3</sub>
, and Yb<sub>2</sub>
O<sub>3</sub>
through lysosomal dysfunction, which disrupts homeostatic regulation of activated NLRP3 complexes, as has been observed in a myeloid cell line (THP-1) <xref rid="B142" ref-type="bibr">142</xref>
. Wei et al. <xref rid="B143" ref-type="bibr">143</xref>
demonstrated that europium hydroxide nanorods (EHNs)-induced autophagy enhances the degradation of mutant huntingtin protein aggregation in Neuro2a cells. Afterwards, they revealed that EHNs-induced autophagy does not follow the classical AKT-mTOR and AMPK signaling pathways, but instead the MEK/ERK1/2 signaling pathway. Furthermore, they demonstrated that the combined treatment of EHNs and the autophagy inducer trehalose led to more degradation of mutant huntingtin protein aggregation, suggesting that enhanced clearance of intracellular protein aggregates may be achieved through combined treatment with two or more autophagy inducers. This information is vital for the treatment of diverse neurogenerative diseases <xref rid="B144" ref-type="bibr">144</xref>
.</p>
</sec>
<sec sec-type="materials"><title>Zinc oxide nanomaterials</title>
<p>Zinc oxide nanomaterials (ZnO-NMs) have been extensively used in many dental materials, cosmetic products, and textiles because of their antibacterial performance and ultraviolet light-absorbing properties. Zinc oxide nanoparticles (ZnO-NPs) are also versatile platforms for biomedical applications and therapeutic intervention <xref rid="B145" ref-type="bibr">145</xref>
,<xref rid="B146" ref-type="bibr">146</xref>
. However, biosafety concerns have been raised over the wide applications of ZnO-NPs. Cellular zinc homeostasis disruption, ROS generation, mitochondrial damage, and autophagy induction have been reported to be caused by zinc oxide nanoparticles <xref rid="B147" ref-type="bibr">147</xref>
-<xref rid="B149" ref-type="bibr">149</xref>
.</p>
<p>Recently, Hu et al. <xref rid="B150" ref-type="bibr">150</xref>
investigated the subcellular mechanism of pro-death autophagy elicited by ZnO-NPs. The group demonstrated that the acceleration of zinc ion release by autophagy and the sequentially increasing intracellular ROS generation in cancer cells contributed to cell death. Furthermore, they demonstrated that combinatory use of ZnO-NPs and doxorubicin results in sensitizing the chemotherapeutic killing of both normal cancer cells and drug-resistant cells through autophagy-mediated intracellular dissolution of ZnO-NPs. These results indicate that the modulation of autophagy holds great promise for improving the efficacy of tumor chemotherapy.</p>
<p>ZnO-NMs-modulated autophagy is closely correlated with cytotoxicity. It has been reported that autophagy induction by ZnO-NPs ultimately leads to autophagic flux blockage in A549 cells through lysosomal impairment, which is caused by the enhanced dissolution of zinc oxide NPs and release of zinc ions, decreasing cell viability and causing cell death <xref rid="B151" ref-type="bibr">151</xref>
. Autophagy modulated by ZnO-NPs may be dependent on particle size, as it has been reported that 50 nm ZnO-NPs interfered with the autophagic flux in A549 cells and led to cell death, whereas 200 nm ZnO-NPs failed to induce autophagy-mediated toxicity <xref rid="B152" ref-type="bibr">152</xref>
.</p>
</sec>
<sec sec-type="materials"><title>Alumina and titanium dioxide nanomaterials</title>
<p>Nano-sized alumina (Al<sub>2</sub>
O<sub>3</sub>
) and titanium dioxide (TiO<sub>2</sub>
) are among the most abundantly manufactured engineered nanomaterials. Titanium dioxide is a common additive in food, personal care items, and other consumer products <xref rid="B153" ref-type="bibr">153</xref>
. Therefore, one can predict that many workers around the world will encounter Al<sub>2</sub>
O<sub>3</sub>
and TiO<sub>2</sub>
NMs, and thus occupational exposures can be anticipated. Cellular exposure to TiO<sub>2</sub>
NPs resulted in ROS production, DNA damage, and autophagy induction, as has been observed in human cerebral endothelial cells (HCECs) <xref rid="B47" ref-type="bibr">47</xref>
. Prolonged exposure (72 h) to TiO<sub>2</sub>
NPs was found to cause autophagic flux blockage in H4/a-syn-GFP cells, whereas short exposure (24 h) to TiO<sub>2</sub>
NPs promoted autophagic flux <xref rid="B154" ref-type="bibr">154</xref>
. Autophagy induction seems to be an important mechanism involved in Al<sub>2</sub>
O<sub>3</sub>
NMs-induced toxicity, as has been observed in human cerebral microvascular endothelial cells (HCMECs) <xref rid="B155" ref-type="bibr">155</xref>
and RAW 264.7 cells <xref rid="B156" ref-type="bibr">156</xref>
.</p>
<p>Besides its adverse effects, autophagy induction by nanosized Al<sub>2</sub>
O<sub>3</sub>
also exhibits potential applications in the biomedical field. Autophagy induction by Al<sub>2</sub>
O<sub>3</sub>
NPs inhibits the activation of osteoclasts and thus reduces osteolysis and aseptic loosening by decreasing the expression of RANKL <xref rid="B157" ref-type="bibr">157</xref>
. α-Al<sub>2</sub>
O<sub>3</sub>
NPs-modulated autophagy efficiently enhances antigen cross-presentation, a key step for the successful development of therapeutic cancer vaccines, through delivering significant amounts of antigens into autophagosomes in dendritic cells, which then present the antigens to T cells through autophagy <xref rid="B158" ref-type="bibr">158</xref>
.</p>
</sec>
<sec sec-type="conclusions"><title>Conclusion and perspective</title>
<p>This review presents an overview of a set of inorganic nanomaterials (NMs) including iron oxide nanomaterials, silver NMs, gold NMs, carbon-based NMs, silica NMs, quantum dots, rare earth oxide NMs, zinc oxide NMs, alumina NMs, and titanium dioxide NMs, and discusses how each modulates autophagy and of their role in cell fate determination. As shown in Figure <xref ref-type="fig" rid="F4">4</xref>
, inorganic nanomaterials including AgNMs, AuNMs, and quantum dots, are frequently observed to elevate intracellular ROS generation, accompanied by autophagy activation. Furthermore, ROS scavengers (e.g. NAC) can efficiently suppress inorganic nanomaterials-induced autophagy. Therefore, inorganic NMs-induced increased ROS generation may be a prominent mechanism underlying IONPs-induced autophagy activation. In addition to excessive ROS generation, there are several other mechanisms responsible for inorganic NMs-modulated autophagy, including mitochondria damage, endoplasmic reticulum (ER) stress, polyubiquitinated protein accumulation, cytoskeleton disruption, mitochondrial network disorganization, lysosome dysfunction, and ubiquitination interference. Several possible mechanisms underlying inorganic nanomaterials-modulated autophagy are summarized in Figure <xref ref-type="fig" rid="F5">5</xref>
. As shown in Figure <xref ref-type="fig" rid="F5">5</xref>
, inorganic NMs causing excessive ROS generation, mitochondrial damage, ER stress, and polyubiquitinated protein accumulation are more likely to induce autophagy activation, while mitochondrial network disorganization, lysosome dysfunction, cytoskeleton disruption, and ubiquitination interference tend to block autophagic flux, resulting in autophagy disruption. Furthermore, Figure <xref ref-type="fig" rid="F5">5</xref>
summarizes the possible roles of inorganic NMs-modulated autophagy in cell fate determination. Inorganic NMs-induced autophagy activation may promote cell survival by decreasing intracellular ROS, generating pro-survival factors, degrading toxic proteins, or activating pro-survival pathways. Inorganic NMs-induced autophagy activation may also lead to cell death through promoting apoptosis. However, inorganic NMs-induced autophagy disruption usually results in cell death through toxic protein accumulation and excessive ROS. It should be noted that the effects of IONPs on autophagic activity and their role in cell fate determination should be considered together with the physicochemical properties of IONPs, as well as the cell types.</p>
<p>Inorganic NMs-modulated autophagy provides a new target for therapy. Inorganic NMs-modulated autophagy has been reported to play an important role in radiotherapy and chemotherapy sensitization, and in promoting the clearance of huntingtin protein aggregation in neurons, indicating that it can be a potential tool for therapy. However, as the research on autophagy modulation by nanomaterial is still at a rudimentary stage, many scientific questions remain largely unanswered. Molecular links between inorganic NMs-modulated autophagy and enhanced therapeutic effects remain murky. Therefore, comprehensive investigations are still required to fully explore the values of inorganic NMs-modulated autophagy for theranostic application.</p>
</sec>
</body>
<back><ack><p>This work was supported by the National Key Research and Development Program of China (2017YFA0205301), the NSF of China (61527806, 61871180, 61901168, 61971187, 81902153 and 81430055), Programs for Changjiang Scholars and Innovative Research Team in University (No. IRT_15R13) and open Funding of State Key Laboratory of Oral Diseases (SKLOD2019OF03).</p>
</ack>
<glossary><title>Abbreviations</title>
<def-list><def-item><term id="GL1">AKT</term>
<def><p>protein kinase B</p>
</def>
</def-item>
<def-item><term id="GL2">AMPK</term>
<def><p>AMP-activated protein kinase</p>
</def>
</def-item>
<def-item><term id="GL3">ATF6</term>
<def><p>transcription factor 6</p>
</def>
</def-item>
<def-item><term id="GL4">Atg14</term>
<def><p>autophagy-related protein14</p>
</def>
</def-item>
<def-item><term id="GL5">Bcl-2</term>
<def><p>B-cell lymphoma 2</p>
</def>
</def-item>
<def-item><term id="GL6">CTAB</term>
<def><p>cetyltrimethylammonium bromide</p>
</def>
</def-item>
<def-item><term id="GL7">DA</term>
<def><p>dopamine</p>
</def>
</def-item>
<def-item><term id="GL8">DA-PAA-PEG</term>
<def><p>dopamine-polyacrylic acid- polyethylene glycol</p>
</def>
</def-item>
<def-item><term id="GL9">DMSA</term>
<def><p>dimercaptosuccinic acid</p>
</def>
</def-item>
<def-item><term id="GL10">EIF2AK3</term>
<def><p>eukaryotic translation initiation factor 2 alpha kinase 3</p>
</def>
</def-item>
<def-item><term id="GL11">ERK</term>
<def><p>extracellular signal-regulated kinase</p>
</def>
</def-item>
<def-item><term id="GL12">GlcNAc</term>
<def><p>N-acetyl-glucosamine</p>
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</def-item>
<def-item><term id="GL13">JNK</term>
<def><p>c-jun N-terminal kinase</p>
</def>
</def-item>
<def-item><term id="GL14">LC3</term>
<def><p>microtubule-associated protein 1 light chain3</p>
</def>
</def-item>
<def-item><term id="GL15">MEK</term>
<def><p>mitogen-activated protein kinase</p>
</def>
</def-item>
<def-item><term id="GL16">mTOR</term>
<def><p>mammalian target of rapamycin</p>
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</def-item>
<def-item><term id="GL17">MWCNT</term>
<def><p>multi-walled carbon nanotube</p>
</def>
</def-item>
<def-item><term id="GL18">NO</term>
<def><p>nitric oxide</p>
</def>
</def-item>
<def-item><term id="GL19">NOS</term>
<def><p>nitric oxide synthase</p>
</def>
</def-item>
<def-item><term id="GL20">PEG</term>
<def><p>polyethylene glycol</p>
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</def-item>
<def-item><term id="GL21">PI3K</term>
<def><p>phosphoinositide 3-kinase</p>
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</def-item>
<def-item><term id="GL22">PtdIns3K</term>
<def><p>phosphatidylinositol 3-kinase</p>
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</def-item>
<def-item><term id="GL23">PVP</term>
<def><p>polyvinylpyrrolidone</p>
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</def-item>
<def-item><term id="GL24">RANKL</term>
<def><p>receptor activation of nuclear factor (NF)-κB</p>
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</def-item>
<def-item><term id="GL25">RPS6KB</term>
<def><p>ribosomal protein S6 kinase</p>
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</def-item>
<def-item><term id="GL26">TRAIL</term>
<def><p>tumor necrosis factor-related apoptosis-inducing ligand</p>
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</def-item>
<def-item><term id="GL27">TSC2</term>
<def><p>tuberous Sclerosis Complex 2</p>
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</def-item>
<def-item><term id="GL28">UPR</term>
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</def-item>
<def-item><term id="GL29">VPS34</term>
<def><p>phosphatidylinositol 3-kinase</p>
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<floats-group><fig id="F1" position="float"><label>Figure 1</label>
<caption><p>Potential applications of various inorganic nanomaterials (NMs) in the biomedical field. MRI: magnetic resonance imaging; NIR: near-infrared; PPT: photothermal therapy; PA: photoacoustic.</p>
</caption>
<graphic xlink:href="thnov10p3206g001"></graphic>
</fig>
<fig id="F2" position="float"><label>Figure 2</label>
<caption><p>AuNPs-induced autophagy and osteogenesis is size-dependent. (A) TEM images of AuNPs of different sizes. (B-C) AuNPs-induce autophagy in PDLPs in a size-dependent manner. AP: autophagosome; AL: autolysosome. (D) AuNPs-induced osteogenesis of PDLPs in a size-dependent manner. (E) Effects of autophagy inhibitors on 45 nm AuNP-induced osteogenic differentiation. Reprinted with permission from reference <xref rid="B79" ref-type="bibr">79</xref>
, copyright 2017 Ivyspring International Publisher.</p>
</caption>
<graphic xlink:href="thnov10p3206g002"></graphic>
</fig>
<fig id="F3" position="float"><label>Figure 3</label>
<caption><p>Major properties of carbon-based nanomaterials and their potential applications in biomedicine. SWCNT: single-walled carbon nanotube; GO: graphene oxide; NIR: near-infrared.</p>
</caption>
<graphic xlink:href="thnov10p3206g003"></graphic>
</fig>
<fig id="F4" position="float"><label>Figure 4</label>
<caption><p>Increased intracellular ROS generation and its role in inorganic nanomaterials-modulated autophagy. (A) Effect of AgNPs on the production of ROS, and (B) effect of the ROS scavengers Vit C and NAC on reduction in cell autophagy induced by AgNPs detected by LysoTracker Red assay. Reprinted with permission from reference <xref rid="B57" ref-type="bibr">57</xref>
, copyright 2017 Royal Society of Chemistry. (C) Effect of gold nanorods (CTAB) on the production of ROS, and (D) effect of NAC on the reduction in cell autophagy induced by gold nanorods (CTAB-GNRs) detected by western blot assay. Reprinted with permission from reference <xref rid="B77" ref-type="bibr">77</xref>
, copyright 2015 Springer Nature. (E) Effect of quantum dots (QD-COOH) on intracellular ROS determined using 2,7-dichlorofluorescein diacetate, and (F) effect of NAC on the reduction of cell autophagy induced by QD-COOH, detected by western blot. Reprinted with permission from reference <xref rid="B130" ref-type="bibr">130</xref>
, copyright 2013 American Chemical Society.</p>
</caption>
<graphic xlink:href="thnov10p3206g004"></graphic>
</fig>
<fig id="F5" position="float"><label>Figure 5</label>
<caption><p>A summary of possible mechanisms underlying inorganic nanomaterials-modulated autophagy, and important roles of autophagy in cytotoxicity. IO NMs: iron oxide nanomaterials; Ag NMs: silver nanomaterials; Au NMs: gold nanomaterials.</p>
</caption>
<graphic xlink:href="thnov10p3206g005"></graphic>
</fig>
<table-wrap id="T1" position="float"><label>Table 1</label>
<caption><p>Inorganic NMs-modulated autophagy was frequently observed in a variety of cell lines.</p>
</caption>
<table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="1" colspan="1">NMs</th>
<th rowspan="1" colspan="1">Cell line</th>
</tr>
</thead>
<tbody valign="top"><tr><td rowspan="1" colspan="1">IO NMs</td>
<td rowspan="1" colspan="1">A549 <xref rid="B32" ref-type="bibr">32</xref>
, RAW264.7 <xref rid="B33" ref-type="bibr">33</xref>
,<xref rid="B37" ref-type="bibr">37</xref>
,<xref rid="B39" ref-type="bibr">39</xref>
, PC12 <xref rid="B34" ref-type="bibr">34</xref>
, HeLa <xref rid="B36" ref-type="bibr">36</xref>
, OPM2 <xref rid="B38" ref-type="bibr">38</xref>
, MCF-7 <xref rid="B40" ref-type="bibr">40</xref>
, human monocytes <xref rid="B41" ref-type="bibr">41</xref>
, SKOV-3 <xref rid="B42" ref-type="bibr">42</xref>
, OECM1 <xref rid="B45" ref-type="bibr">45</xref>
, HepG2 <xref rid="B46" ref-type="bibr">46</xref>
, Human cerebral endothelial cells <xref rid="B47" ref-type="bibr">47</xref>
, U2OS <xref rid="B48" ref-type="bibr">48</xref>
, Mouse dendritic cells <xref rid="B49" ref-type="bibr">49</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Ag NMs</td>
<td rowspan="1" colspan="1">NIH 3T3 <xref rid="B70" ref-type="bibr">70</xref>
, U251 <xref rid="B56" ref-type="bibr">56</xref>
, <xref rid="B61" ref-type="bibr">61</xref>
, T24 <xref rid="B71" ref-type="bibr">71</xref>
, NCI-H292 <xref rid="B60" ref-type="bibr">60</xref>
, THP-1 monocyte <xref rid="B58" ref-type="bibr">58</xref>
,<xref rid="B67" ref-type="bibr">67</xref>
, HepG2 <xref rid="B65" ref-type="bibr">65</xref>
, A549 <xref rid="B59" ref-type="bibr">59</xref>
, HeLa <xref rid="B62" ref-type="bibr">62</xref>
, <xref rid="B64" ref-type="bibr">64</xref>
, Ba/F3 <xref rid="B57" ref-type="bibr">57</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Au NMs</td>
<td rowspan="1" colspan="1">HUVECs <xref rid="B76" ref-type="bibr">76</xref>
, HEK293T <xref rid="B77" ref-type="bibr">77</xref>
, L02 <xref rid="B77" ref-type="bibr">77</xref>
, HFF <xref rid="B77" ref-type="bibr">77</xref>
, HCT116 <xref rid="B77" ref-type="bibr">77</xref>
, BEL7402 <xref rid="B77" ref-type="bibr">77</xref>
, PC3 <xref rid="B77" ref-type="bibr">77</xref>
, A549 <xref rid="B78" ref-type="bibr">78</xref>
, NRK <xref rid="B81" ref-type="bibr">81</xref>
, MRC-5 <xref rid="B82" ref-type="bibr">82</xref>
, human periodontal ligament progenitor cells <xref rid="B79" ref-type="bibr">79</xref>
, Calu-1 <xref rid="B80" ref-type="bibr">80</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Carbon-based NMs</td>
<td rowspan="1" colspan="1">LLC-PK1 <xref rid="B84" ref-type="bibr">84</xref>
, HUVECs <xref rid="B85" ref-type="bibr">85</xref>
,<xref rid="B96" ref-type="bibr">96</xref>
,<xref rid="B103" ref-type="bibr">103</xref>
, RAW264.7 <xref rid="B90" ref-type="bibr">90</xref>
,<xref rid="B100" ref-type="bibr">100</xref>
,<xref rid="B95" ref-type="bibr">95</xref>
, A549 <xref rid="B99" ref-type="bibr">99</xref>
,<xref rid="B101" ref-type="bibr">101</xref>
, BEAS-2B <xref rid="B100" ref-type="bibr">100</xref>
, SK-N-SH <xref rid="B94" ref-type="bibr">94</xref>
, HeLa <xref rid="B97" ref-type="bibr">97</xref>
, PC12 <xref rid="B102" ref-type="bibr">102</xref>
, HEK 293 <xref rid="B108" ref-type="bibr">108</xref>
, U87 <xref rid="B108" ref-type="bibr">108</xref>
, 143B <xref rid="B109" ref-type="bibr">109</xref>
, MG63 <xref rid="B109" ref-type="bibr">109</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Silica NMs</td>
<td rowspan="1" colspan="1">HUVECs <xref rid="B118" ref-type="bibr">118</xref>
,<xref rid="B123" ref-type="bibr">123</xref>
,<xref rid="B119" ref-type="bibr">119</xref>
, L-02 <xref rid="B122" ref-type="bibr">122</xref>
,<xref rid="B120" ref-type="bibr">120</xref>
, HepG2 <xref rid="B122" ref-type="bibr">122</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Quantum dots</td>
<td rowspan="1" colspan="1">LLC-PK1 <xref rid="B5" ref-type="bibr">5</xref>
, murine embryonic fibroblast <xref rid="B121" ref-type="bibr">121</xref>
, RAG <xref rid="B130" ref-type="bibr">130</xref>
, hippocampal neurons <xref rid="B131" ref-type="bibr">131</xref>
, HeLa <xref rid="B131" ref-type="bibr">131</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Rare earth oxide NMs</td>
<td rowspan="1" colspan="1">NCI-H460 <xref rid="B137" ref-type="bibr">137</xref>
, late infinite neuronal ceroid lipofuscinosis fibroblasts <xref rid="B138" ref-type="bibr">138</xref>
, HeLa <xref rid="B139" ref-type="bibr">139</xref>
, Kupffer <xref rid="B140" ref-type="bibr">140</xref>
, primary hepatocytes <xref rid="B141" ref-type="bibr">141</xref>
, THP-1 <xref rid="B142" ref-type="bibr">142</xref>
, Neuro 2a <xref rid="B143" ref-type="bibr">143</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Zinc oxide NMs</td>
<td rowspan="1" colspan="1">HeLa <xref rid="B150" ref-type="bibr">150</xref>
, A549 <xref rid="B151" ref-type="bibr">151</xref>
,<xref rid="B152" ref-type="bibr">152</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Alumina NMs</td>
<td rowspan="1" colspan="1">human cerebral microvascular endothelial cells (HCMECs) <xref rid="B155" ref-type="bibr">155</xref>
, RAW264.7 <xref rid="B156" ref-type="bibr">156</xref>
, T cells <xref rid="B158" ref-type="bibr">158</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Titanium dioxide NMs</td>
<td rowspan="1" colspan="1">human cerebral endothelial cells (HCECs) <xref rid="B47" ref-type="bibr">47</xref>
, H4/a-syn-GFP <xref rid="B154" ref-type="bibr">154</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="T2" position="float"><label>Table 2</label>
<caption><p>Inorganic nanomaterials-modulated autophagy and its effects on cell fate.</p>
</caption>
<table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="1" colspan="1">NMs</th>
<th rowspan="1" colspan="1">Size (characterization method); Zeta Pot.; shape or dispersity</th>
<th rowspan="1" colspan="1">Coating</th>
<th rowspan="1" colspan="1">Concentration</th>
<th rowspan="1" colspan="1">Exposure period </th>
<th rowspan="1" colspan="1">Model cells</th>
<th rowspan="1" colspan="1">Mechanism</th>
<th rowspan="1" colspan="1">Cell fate</th>
<th rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody valign="top"><tr><td rowspan="1" colspan="1">IONPs</td>
<td rowspan="1" colspan="1">51 nm (TEM); -39 mV; aggregates</td>
<td rowspan="1" colspan="1">Bare</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">48 h</td>
<td rowspan="1" colspan="1">A549 cells</td>
<td rowspan="1" colspan="1">ROS upregulation and p-mTOR expression inhibition</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B32" ref-type="bibr">32</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Fe<sub>3</sub>
O<sub>4</sub>
</td>
<td rowspan="1" colspan="1">41 nm (DLS); -51 mV; near spherical</td>
<td rowspan="1" colspan="1">Phospholipid</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">RAW264.7 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Apoptotic cell death</td>
<td rowspan="1" colspan="1"><xref rid="B33" ref-type="bibr">33</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">α-Fe<sub>2</sub>
O<sub>3</sub>
NPs</td>
<td rowspan="1" colspan="1">17 nm (TEM); near spherical</td>
<td rowspan="1" colspan="1">Caboxylate</td>
<td rowspan="1" colspan="1">150 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">PC12 cells</td>
<td rowspan="1" colspan="1">ROS upregulation</td>
<td rowspan="1" colspan="1">Cell death and growth arrest</td>
<td rowspan="1" colspan="1"><xref rid="B34" ref-type="bibr">34</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">γ-Fe<sub>2</sub>
O<sub>3</sub>
</td>
<td rowspan="1" colspan="1">6.5 nm (TEM); --; nano-aggregates</td>
<td rowspan="1" colspan="1">polydextrose sorbitol carboxymethyl ether</td>
<td rowspan="1" colspan="1">200 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">RAW 264.7</td>
<td rowspan="1" colspan="1">Activation Cav1-Notch1/HES1 pathway</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B37" ref-type="bibr">37</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Fe<sub>3</sub>
O<sub>4</sub>
NPs</td>
<td rowspan="1" colspan="1">>10 nm (TEM); 22 mV, -29 mV, or 5 mV; near spherical</td>
<td rowspan="1" colspan="1">Bare, DA, DMSA, or DA-PAA-PEG</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">9 h</td>
<td rowspan="1" colspan="1">OPM2 cells</td>
<td rowspan="1" colspan="1">upregulation of Beclin l/Bcl-2/VPS34 complex</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B38" ref-type="bibr">38</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Resovist and Feraheme</td>
<td rowspan="1" colspan="1">62 nm (DLS), 30 nm (DLS); --; --</td>
<td rowspan="1" colspan="1">Carboxydextran, polyglucose sorbitol carboxymethyl ether</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">RAW 264.7</td>
<td rowspan="1" colspan="1">Activation TLR4-p38-Nrf2-p62 pathway</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B39" ref-type="bibr">39</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">IO-NPs</td>
<td rowspan="1" colspan="1">60 nm (DLS); -11 mV; nano-aggregates</td>
<td rowspan="1" colspan="1">Dextran</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h, 48 h</td>
<td rowspan="1" colspan="1">Human monocytes</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B41" ref-type="bibr">41</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">11 nm (TEM); near spherical</td>
<td rowspan="1" colspan="1">PVP</td>
<td rowspan="1" colspan="1">8 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">Ba/F3 cells</td>
<td rowspan="1" colspan="1">ROS activation and p-mTOR inhibition</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B57" ref-type="bibr">57</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">>30 nm (TEM); -4.3 mV; near spherical shape</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">5 and 10 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">48 h</td>
<td rowspan="1" colspan="1">THP-1 cells</td>
<td rowspan="1" colspan="1">Lysosome dysfunction</td>
<td rowspan="1" colspan="1">Imedence of PMA-induced monocyte differentiation</td>
<td rowspan="1" colspan="1"><xref rid="B58" ref-type="bibr">58</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">70 nm (DLS); -31 mV in culture medium; near spherical</td>
<td rowspan="1" colspan="1">Citrate</td>
<td rowspan="1" colspan="1">50, 100, and 200 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">A549 cells</td>
<td rowspan="1" colspan="1">Lysosome dysfunction</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B59" ref-type="bibr">59</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">27 nm (TEM); -13 mV; near spherical</td>
<td rowspan="1" colspan="1">PVP</td>
<td rowspan="1" colspan="1">20 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">Hela cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Promoted cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B62" ref-type="bibr">62</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">27 nm (TEM); --; near shperical</td>
<td rowspan="1" colspan="1">PVP</td>
<td rowspan="1" colspan="1">10 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">8 h</td>
<td rowspan="1" colspan="1">HeLa cells</td>
<td rowspan="1" colspan="1">nucleus translocation of TFEB</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B64" ref-type="bibr">64</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AgNPs</td>
<td rowspan="1" colspan="1">14 nm, 52 nm, and 102nm (TEM); spherical</td>
<td rowspan="1" colspan="1">PVP</td>
<td rowspan="1" colspan="1">10 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">12 h, 24 h</td>
<td rowspan="1" colspan="1">HepG2 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B65" ref-type="bibr">65</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Au naorods</td>
<td rowspan="1" colspan="1">100 nm length and 4 aspect ratio (TEM); 38 mV; nanorod</td>
<td rowspan="1" colspan="1">CTAB</td>
<td rowspan="1" colspan="1">2 nM</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">HCT116 cells</td>
<td rowspan="1" colspan="1">ROS upregulation</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B77" ref-type="bibr">77</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AuNPs</td>
<td rowspan="1" colspan="1">18 nm, 55 nm, and 84 nm (DLS); negative; near spherical</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">Calu-1 cells</td>
<td rowspan="1" colspan="1">Mitochondrial dysfunction</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B80" ref-type="bibr">80</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AuNPs</td>
<td rowspan="1" colspan="1">10 nm, 25 nm, and 50 nm (TEM); negative; near spherical</td>
<td rowspan="1" colspan="1">Citrate</td>
<td rowspan="1" colspan="1">1 nM</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">NRK cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1"><xref rid="B81" ref-type="bibr">81</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">AuNPs</td>
<td rowspan="1" colspan="1">36 nm (DLS); -11 mV; near spherical</td>
<td rowspan="1" colspan="1">Fetal bovine serum</td>
<td rowspan="1" colspan="1">1 nM</td>
<td rowspan="1" colspan="1">72 h</td>
<td rowspan="1" colspan="1">MRC-5 cells</td>
<td rowspan="1" colspan="1">Oxidative stress</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B82" ref-type="bibr">82</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">C<sub>60</sub>
(OH)<sub>x</sub>
</td>
<td rowspan="1" colspan="1">15.7 nm (DLS); -49 mV; nano-aggregates</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">6 mM</td>
<td rowspan="1" colspan="1">6 h, 24 h</td>
<td rowspan="1" colspan="1">LLC-PK1 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B84" ref-type="bibr">84</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">MWCNT</td>
<td rowspan="1" colspan="1">60 nm diameter; -42 mV; nanotube</td>
<td rowspan="1" colspan="1">Carboxylated</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">HUVECs</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B85" ref-type="bibr">85</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">GO</td>
<td rowspan="1" colspan="1">350 nm diameter, 1.0- 1.2 nm thickness (AFM); nanosheets</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">RAW 264.7 cells</td>
<td rowspan="1" colspan="1">Activation TLR signaling cascades</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B90" ref-type="bibr">90</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">GO</td>
<td rowspan="1" colspan="1">100 nm-2 μm diameter, 1 nm thickness (SEM); negative; nanosheet</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">8 mg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">12 h</td>
<td rowspan="1" colspan="1">SK-N-SH cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Promoted neuro cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B94" ref-type="bibr">94</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Graphite carbon nanofibers</td>
<td rowspan="1" colspan="1">79 nm outer and 7 nm inner diameter (TEM); -30 mV; nanofiber</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">25 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">A549 cells</td>
<td rowspan="1" colspan="1">Lysosomal dysfunction and cytoskeleton disruption</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B99" ref-type="bibr">99</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">MWCNT</td>
<td rowspan="1" colspan="1">24-26 nm diameter, 1.7-6.4 μm length (TEM); 8 mV; nanotube</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">10 and 50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">6 h</td>
<td rowspan="1" colspan="1">RAW 264.7 cells</td>
<td rowspan="1" colspan="1">Lysosomal dysfunction</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B100" ref-type="bibr">100</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">GO</td>
<td rowspan="1" colspan="1">200 nm diameter, 0.6-1.0 nm thickness (AFM); -30 mV; nanosheet</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">60 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24, 48, and 72 h</td>
<td rowspan="1" colspan="1">PC12 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B102" ref-type="bibr">102</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">GO</td>
<td rowspan="1" colspan="1">390 nm or 66 nm diameter, 1 nm thickness (AFM); 30mV; nanosheet</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">25 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">HUVECs</td>
<td rowspan="1" colspan="1">Increasing intracellular calcium ion (Ca<sup>2+</sup>
) level</td>
<td rowspan="1" colspan="1">Apoptosis</td>
<td rowspan="1" colspan="1"><xref rid="B103" ref-type="bibr">103</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">NDs</td>
<td rowspan="1" colspan="1">119 nm (DLS); -25 mV; irregular shape</td>
<td rowspan="1" colspan="1">Ubiquitin K63</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">12, 24, and 48 h</td>
<td rowspan="1" colspan="1">A549 cells</td>
<td rowspan="1" colspan="1">Ubiquitination</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B98" ref-type="bibr">98</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">NDs</td>
<td rowspan="1" colspan="1">2-10 nm (TEM); aggregates (40-200 nm)</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">48 h</td>
<td rowspan="1" colspan="1">HepG2 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B110" ref-type="bibr">110</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">SiNPs</td>
<td rowspan="1" colspan="1">62 nm (TEM); -44 mV; near spherical</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">25, 50, 75, and 100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">HUVECs</td>
<td rowspan="1" colspan="1">upregulation of MAPK/Erk1/2/mTOR signaling and PI3K/Akt/mTOR signaling pathways</td>
<td rowspan="1" colspan="1">Disturb the cell homeostasis and impair angiogenesis</td>
<td rowspan="1" colspan="1"><xref rid="B118" ref-type="bibr">118</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">SiNPs</td>
<td rowspan="1" colspan="1">58 nm (TEM); -39 mV; near spherical</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">50 and 100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">3, 6, 12, and 24 h</td>
<td rowspan="1" colspan="1">L-02 and HepG2 cells</td>
<td rowspan="1" colspan="1">Lysosome impairment</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B122" ref-type="bibr">122</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">CoFe<sub>2</sub>
O<sub>4</sub>
<break></break>
@silica</td>
<td rowspan="1" colspan="1">50 nm; -28 mV; near spherical</td>
<td rowspan="1" colspan="1">Silica caped and PEGylated</td>
<td rowspan="1" colspan="1">60 and 100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">15, 30, 45, and 60 mins, 72 h</td>
<td rowspan="1" colspan="1">MC3T3-E1 cells</td>
<td rowspan="1" colspan="1">ERK1/2 signaling activation</td>
<td rowspan="1" colspan="1">Stimulated <italic>in vitro</italic>
differentiation and mineralization of osteoblasts</td>
<td rowspan="1" colspan="1"><xref rid="B124" ref-type="bibr">124</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Cd-based QDs</td>
<td rowspan="1" colspan="1">10 nm (TEM); --; --</td>
<td rowspan="1" colspan="1">ZnS caped and carboxyl</td>
<td rowspan="1" colspan="1">10 and 20 nM</td>
<td rowspan="1" colspan="1">6h, 24 h</td>
<td rowspan="1" colspan="1">Mouse renal adenocarcinoma cells,</td>
<td rowspan="1" colspan="1">Oxidative stress</td>
<td rowspan="1" colspan="1">Promoted cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B130" ref-type="bibr">130</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">CdSe QDs</td>
<td rowspan="1" colspan="1">5 nm (TEM); --; --</td>
<td rowspan="1" colspan="1">ZnS caped and streptavidin</td>
<td rowspan="1" colspan="1">10 nM (<italic>in vitro</italic>
); 20 nM (<italic>in vivo</italic>
)</td>
<td rowspan="1" colspan="1">24 h (<italic>in vitro</italic>
); 2 h (<italic>in vivo</italic>
)</td>
<td rowspan="1" colspan="1">Primary hippocampal neurons and Wistar rats</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Synaptic dysfunction <italic>in vivo</italic>
</td>
<td rowspan="1" colspan="1"><xref rid="B131" ref-type="bibr">131</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Nd<sub>2</sub>
O<sub>3</sub>
NPs</td>
<td rowspan="1" colspan="1">80 nm; --; --</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">45 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">2 d</td>
<td rowspan="1" colspan="1">NCI-H460 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">S-phase cell cycle arrest, cell death</td>
<td rowspan="1" colspan="1"><xref rid="B137" ref-type="bibr">137</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">CeO<sub>2</sub>
NPs</td>
<td rowspan="1" colspan="1">4.3 nm (TEM); -2 to -14 mV; near spherical</td>
<td rowspan="1" colspan="1">GlcNAc, PEG, and PVP</td>
<td rowspan="1" colspan="1">100 ppm</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">Late infantile neuronal ceroid lipofuscinosis fibroblasts</td>
<td rowspan="1" colspan="1">Activation of TFEB</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B138" ref-type="bibr">138</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">La<sub>2</sub>
O<sub>3</sub>
</td>
<td rowspan="1" colspan="1">26 nm; 28 mV; sub-micro aggregates</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">THP-1 cells</td>
<td rowspan="1" colspan="1">Lysosomal dysfunction</td>
<td rowspan="1" colspan="1">Disrupted homeostatic regulation of activated NLRP3 complexes</td>
<td rowspan="1" colspan="1"><xref rid="B142" ref-type="bibr">142</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Eu<sup>III</sup>
(OH)<sub>3</sub>
nanorods</td>
<td rowspan="1" colspan="1">80-160 nm length, 25-40 nm diameter (TEM); nanorod</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">50 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">GFP-Htt(Q74) Neuro 2a and Htt(Q74) PC12 cells</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Cell survival</td>
<td rowspan="1" colspan="1"><xref rid="B143" ref-type="bibr">143</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">ZnO NPs</td>
<td rowspan="1" colspan="1"><50 nm; -11.5 mV; sub-micro aggregates</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">30 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">24 h</td>
<td rowspan="1" colspan="1">A549 cells</td>
<td rowspan="1" colspan="1">Mitochondria damage, lysosome dysfunction and excessive ROS generation</td>
<td rowspan="1" colspan="1">Cell death</td>
<td rowspan="1" colspan="1"><xref rid="B151" ref-type="bibr">151</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">TiO<sub>2</sub>
NPs</td>
<td rowspan="1" colspan="1">15 nm, 50 nm, and 100nm; < -15 mV; sub-micro aggregates</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">100 μg·mL<sup>-1</sup>
</td>
<td rowspan="1" colspan="1">72 h</td>
<td rowspan="1" colspan="1">H4/a-syn-GFP</td>
<td rowspan="1" colspan="1">Activation of TFEB</td>
<td rowspan="1" colspan="1">Reduced clearance of autophagic cargo (α-synuclein)</td>
<td rowspan="1" colspan="1"><xref rid="B154" ref-type="bibr">154</xref>
</td>
</tr>
<tr><td rowspan="1" colspan="1">Al<sub>2</sub>
O<sub>3</sub>
NPs</td>
<td rowspan="1" colspan="1">8-12 nm; sub-micro aggregates</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">0.01, 0.1, 1, and 10 μg·mL<sup>-1</sup>
(<italic>in vitro</italic>
); 1.25 mg·kg<sup>-1</sup>
(<italic>in vivo</italic>
)</td>
<td rowspan="1" colspan="1">24 h<italic> in vitro</italic>
, 1, 3, 5, and 30 d <italic>in vivo</italic>
</td>
<td rowspan="1" colspan="1">HCMECs/D3 cell and C57BL/6 mice</td>
<td rowspan="1" colspan="1">--</td>
<td rowspan="1" colspan="1">Neurovascular toxicity</td>
<td rowspan="1" colspan="1"><xref rid="B155" ref-type="bibr">155</xref>
</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p><bold>Notes:</bold>
DLS: dynamic light scattering; TEM: transmission electron microscope; AFM: atomic force microscopy; SEM: scanning electron microscopy; TFEB: transcription EB; TLR: toll-like receptor; Zeta Pot.: Zeta Potential; IONPs: iron oxide nanoparticles; LC3-Ⅰ/Ⅱ: LC3-Ⅰ to LC3-Ⅱ conversion; MWCNT: multi-walled carbon nanotube; GO: graphene oxide; NDs: nanodiamonds</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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