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Autophagy Modulated by Inorganic Nanomaterials

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Autophagy Modulated by Inorganic Nanomaterials

Auteurs : Lingling Guo [République populaire de Chine] ; Nongyue He [République populaire de Chine] ; Yongxiang Zhao [République populaire de Chine] ; Tonghua Liu [République populaire de Chine] ; Yan Deng [République populaire de Chine]

Source :

Theranostics [ 1838-7640 ] ; 2020.

RBID : PMC:7053187

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:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7053187

DOI: 10.7150/thno.40414
PubMed: 32194863
PubMed Central: 7053187

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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>
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</TEI>
<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>
</journal-title-group>
<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>
</subj-group>
</article-categories>
<title-group><article-title>Autophagy Modulated by Inorganic Nanomaterials</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Guo</surname>
<given-names>Lingling</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>He</surname>
<given-names>Nongyue</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<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>
</contrib>
<contrib contrib-type="author"><name><surname>Zhao</surname>
<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>
<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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Autophagy Modulated by Inorganic Nanomaterials

Autophagy Modulated by Inorganic Nanomaterials

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