Unraveling the Potential Role of Glutathione in Multiple Forms of Cell Death in Cancer Therapy
Identifieur interne : 000256 ( Pmc/Checkpoint ); précédent : 000255; suivant : 000257Unraveling the Potential Role of Glutathione in Multiple Forms of Cell Death in Cancer Therapy
Auteurs : Huanhuan Lv [République populaire de Chine] ; Chenxiao Zhen [République populaire de Chine] ; Junyu Liu [République populaire de Chine] ; Pengfei Yang [République populaire de Chine] ; Lijiang Hu [République populaire de Chine] ; Peng Shang [République populaire de Chine]Source :
- Oxidative Medicine and Cellular Longevity [ 1942-0900 ] ; 2019.
Abstract
Glutathione is the principal intracellular antioxidant buffer against oxidative stress and mainly exists in the forms of reduced glutathione (GSH) and oxidized glutathione (GSSG). The processes of glutathione synthesis, transport, utilization, and metabolism are tightly controlled to maintain intracellular glutathione homeostasis and redox balance. As for cancer cells, they exhibit a greater ROS level than normal cells in order to meet the enhanced metabolism and vicious proliferation; meanwhile, they also have to develop an increased antioxidant defense system to cope with the higher oxidant state. Growing numbers of studies have implicated that altering the glutathione antioxidant system is associated with multiple forms of programmed cell death in cancer cells. In this review, we firstly focus on glutathione homeostasis from the perspectives of glutathione synthesis, distribution, transportation, and metabolism. Then, we discuss the function of glutathione in the antioxidant process. Afterwards, we also summarize the recent advance in the understanding of the mechanism by which glutathione plays a key role in multiple forms of programmed cell death, including apoptosis, necroptosis, ferroptosis, and autophagy. Finally, we highlight the glutathione-targeting therapeutic approaches toward cancers. A comprehensive review on the glutathione homeostasis and the role of glutathione depletion in programmed cell death provide insight into the redox-based research concerning cancer therapeutics.
Url:
DOI: 10.1155/2019/3150145
PubMed: 31281572
PubMed Central: 6590529
Affiliations:
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<author><name sortKey="Liu, Junyu" sort="Liu, Junyu" uniqKey="Liu J" first="Junyu" last="Liu">Junyu Liu</name>
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<author><name sortKey="Yang, Pengfei" sort="Yang, Pengfei" uniqKey="Yang P" first="Pengfei" last="Yang">Pengfei Yang</name>
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<author><name sortKey="Hu, Lijiang" sort="Hu, Lijiang" uniqKey="Hu L" first="Lijiang" last="Hu">Lijiang Hu</name>
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<author><name sortKey="Shang, Peng" sort="Shang, Peng" uniqKey="Shang P" first="Peng" last="Shang">Peng Shang</name>
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<series><title level="j">Oxidative Medicine and Cellular Longevity</title>
<idno type="ISSN">1942-0900</idno>
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<front><div type="abstract" xml:lang="en"><p>Glutathione is the principal intracellular antioxidant buffer against oxidative stress and mainly exists in the forms of reduced glutathione (GSH) and oxidized glutathione (GSSG). The processes of glutathione synthesis, transport, utilization, and metabolism are tightly controlled to maintain intracellular glutathione homeostasis and redox balance. As for cancer cells, they exhibit a greater ROS level than normal cells in order to meet the enhanced metabolism and vicious proliferation; meanwhile, they also have to develop an increased antioxidant defense system to cope with the higher oxidant state. Growing numbers of studies have implicated that altering the glutathione antioxidant system is associated with multiple forms of programmed cell death in cancer cells. In this review, we firstly focus on glutathione homeostasis from the perspectives of glutathione synthesis, distribution, transportation, and metabolism. Then, we discuss the function of glutathione in the antioxidant process. Afterwards, we also summarize the recent advance in the understanding of the mechanism by which glutathione plays a key role in multiple forms of programmed cell death, including apoptosis, necroptosis, ferroptosis, and autophagy. Finally, we highlight the glutathione-targeting therapeutic approaches toward cancers. A comprehensive review on the glutathione homeostasis and the role of glutathione depletion in programmed cell death provide insight into the redox-based research concerning cancer therapeutics.</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">Oxid Med Cell Longev</journal-id>
<journal-id journal-id-type="iso-abbrev">Oxid Med Cell Longev</journal-id>
<journal-id journal-id-type="publisher-id">OMCL</journal-id>
<journal-title-group><journal-title>Oxidative Medicine and Cellular Longevity</journal-title>
</journal-title-group>
<issn pub-type="ppub">1942-0900</issn>
<issn pub-type="epub">1942-0994</issn>
<publisher><publisher-name>Hindawi</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31281572</article-id>
<article-id pub-id-type="pmc">6590529</article-id>
<article-id pub-id-type="doi">10.1155/2019/3150145</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Unraveling the Potential Role of Glutathione in Multiple Forms of Cell Death in Cancer Therapy</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-4869-4908</contrib-id>
<name><surname>Lv</surname>
<given-names>Huanhuan</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="I3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="I4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhen</surname>
<given-names>Chenxiao</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Junyu</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Pengfei</given-names>
</name>
<xref ref-type="aff" rid="I1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="I4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hu</surname>
<given-names>Lijiang</given-names>
</name>
<xref ref-type="aff" rid="I3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-5418-6240</contrib-id>
<name><surname>Shang</surname>
<given-names>Peng</given-names>
</name>
<email>shangpeng@nwpu.edu.cn</email>
<xref ref-type="aff" rid="I2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="I4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="I5"><sup>5</sup>
</xref>
</contrib>
</contrib-group>
<aff id="I1"><sup>1</sup>
School of Life Sciences, Northwestern Polytechnical University, Xi'an, Shaanxi 710072, China</aff>
<aff id="I2"><sup>2</sup>
Research & Development Institute of Northwestern Polytechnical University in Shenzhen, Shenzhen 518057, China</aff>
<aff id="I3"><sup>3</sup>
Zhejiang Heye Health Technology Co. Ltd., Anji, Zhejiang 313300, China</aff>
<aff id="I4"><sup>4</sup>
Research Centre of Microfluidic Chip for Health Care and Environmental Monitoring, Yangtze River Delta Research Institute of Northwestern Polytechnical University in Taicang, Suzhou, Jiangsu 215400, China</aff>
<aff id="I5"><sup>5</sup>
Key Laboratory for Space Bioscience and Biotechnology, Northwestern Polytechnical University, Xi'an, Shaanxi 710072, China</aff>
<author-notes><fn fn-type="other"><p>Guest Editor: Kanhaiya Singh</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>6</month>
<year>2019</year>
</pub-date>
<volume>2019</volume>
<elocation-id>3150145</elocation-id>
<history><date date-type="received"><day>11</day>
<month>4</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>21</day>
<month>5</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2019 Huanhuan Lv et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Glutathione is the principal intracellular antioxidant buffer against oxidative stress and mainly exists in the forms of reduced glutathione (GSH) and oxidized glutathione (GSSG). The processes of glutathione synthesis, transport, utilization, and metabolism are tightly controlled to maintain intracellular glutathione homeostasis and redox balance. As for cancer cells, they exhibit a greater ROS level than normal cells in order to meet the enhanced metabolism and vicious proliferation; meanwhile, they also have to develop an increased antioxidant defense system to cope with the higher oxidant state. Growing numbers of studies have implicated that altering the glutathione antioxidant system is associated with multiple forms of programmed cell death in cancer cells. In this review, we firstly focus on glutathione homeostasis from the perspectives of glutathione synthesis, distribution, transportation, and metabolism. Then, we discuss the function of glutathione in the antioxidant process. Afterwards, we also summarize the recent advance in the understanding of the mechanism by which glutathione plays a key role in multiple forms of programmed cell death, including apoptosis, necroptosis, ferroptosis, and autophagy. Finally, we highlight the glutathione-targeting therapeutic approaches toward cancers. A comprehensive review on the glutathione homeostasis and the role of glutathione depletion in programmed cell death provide insight into the redox-based research concerning cancer therapeutics.</p>
</abstract>
<funding-group><award-group><funding-source>Northwestern Polytechnical University Foundation for Fundamental Research</funding-source>
<award-id>3102018JGC012</award-id>
</award-group>
<award-group><funding-source>Fundamental Research Funds for the Central Universities</funding-source>
<award-id>3102017OQD111</award-id>
</award-group>
<award-group><funding-source>National Natural Science Foundation of China</funding-source>
<award-id>51777171</award-id>
<award-id>11872316</award-id>
<award-id>81803032</award-id>
</award-group>
</funding-group>
</article-meta>
</front>
<floats-group><fig id="fig1" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Two-step enzymatic reaction of glutathione synthesis. The first step is the coupling of L-glutamate and cysteine to produce <italic>γ</italic>
-glutamylcysteine under the catalysis of glutamate-cysteine ligase (GCL). The second step is the coupling of <italic>γ</italic>
-glutamylcysteine to glycine catalyzing by glutathione synthetase (GS). Each reaction consumes one ATP molecule. Glutathione exists in the forms of reduced GSH and oxidized GSSG.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.001"></graphic>
</fig>
<fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Distribution of intracellular GSH. GSH is distributed in the cytosol, nucleus, mitochondria, and ER.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.002"></graphic>
</fig>
<fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Transport of GSH. The liver is the main source of GSH, the kidney is the main organ that ingests and degrades GSH, and the small intestine participates in the GSH enterohepatic circulation. The renal proximal tubule is the place where the whole process of GSH transport, synthesis, and degradation is completed.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.003"></graphic>
</fig>
<fig id="fig4" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Two degradation pathways of GSH. One way occurs outside the cell where GSH is degraded by <italic>γ</italic>
-glutamyltransferase (GGT) which is expressed only on the outer surface of particular cell; the other newly discovered pathway occurs in the cytoplasm where GSH is degraded through ChaC1 and ChaC2.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.004"></graphic>
</fig>
<fig id="fig5" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>The antioxidant role of cellular GSH. Glutathione peroxidase (GPX) converts H<sub>2</sub>
O<sub>2</sub>
and Lipid-OOH to H<sub>2</sub>
O and Lipid-OH where GSH is oxidized to GSSG, and glutathione reductase (GR) reduced GSSG to GSH dependent on NADPH, thereby forming a redox cycle to prevent oxidative damage.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.005"></graphic>
</fig>
<fig id="fig6" orientation="portrait" position="float"><label>Figure 6</label>
<caption><p>The role of cellular GSH in apoptosis and necroptosis. GSH depletion through nutrition starvation or GSH synthesis inhibition or conjugation with GSH or GSH efflux or GSH degradation induces ROS generation which results in the occurrence of proapoptotic signals, such as the disruption of MMP, increased bax, decreased bcl2, cytochrome c release, and caspase activation. Excess ROS accumulation induces necroptosis.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.006"></graphic>
</fig>
<fig id="fig7" orientation="portrait" position="float"><label>Figure 7</label>
<caption><p>The mechanism of GSH depletion in induction of ferroptosis. Lipid-OOHs can be formed by autoxidation via Fenton reaction or by enzymatic reaction via lipoxygenases (LOXs). Lipid-OOHs are regulated by the balance between the activities of GPX4 and LOXs or Fenton reaction. System X<sub>c</sub>
<sup>−</sup>
impairment or GPX4 inactivation leads to Lipid-OOH accumulation which cannot be effectively cleared under the loss of GPX4 activity. Ultimately, the accumulation of Lipid-OOH triggers ferroptosis. Ferroptosis can be inhibited by DFO, liproxstatin-1 (Lip-1), and ferrostatin-1 (Fer-1).</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.007"></graphic>
</fig>
<fig id="fig8" orientation="portrait" position="float"><label>Figure 8</label>
<caption><p>The role of cellular GSH in autophagy. GSH depletion through nutrition starvation or GSH synthesis inhibition or conjugation with GSH or GSH efflux induces ROS generation. ROS accumulation promotes changes in autophagy-related proteins, such as LC3 I/II conversion, p62 degradation, and autophagic vacuole formation. Additionally, ROS induce NCOA4-mediated ferritin degradation in an autophagy process, called ferritinophagy, which is promoting free iron release and accelerating ROS generation.</p>
</caption>
<graphic xlink:href="OMCL2019-3150145.008"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
<region><li>Guangdong</li>
</region>
<settlement><li>Shenzhen</li>
</settlement>
</list>
<tree><country name="République populaire de Chine"><noRegion><name sortKey="Lv, Huanhuan" sort="Lv, Huanhuan" uniqKey="Lv H" first="Huanhuan" last="Lv">Huanhuan Lv</name>
</noRegion>
<name sortKey="Hu, Lijiang" sort="Hu, Lijiang" uniqKey="Hu L" first="Lijiang" last="Hu">Lijiang Hu</name>
<name sortKey="Liu, Junyu" sort="Liu, Junyu" uniqKey="Liu J" first="Junyu" last="Liu">Junyu Liu</name>
<name sortKey="Liu, Junyu" sort="Liu, Junyu" uniqKey="Liu J" first="Junyu" last="Liu">Junyu Liu</name>
<name sortKey="Liu, Junyu" sort="Liu, Junyu" uniqKey="Liu J" first="Junyu" last="Liu">Junyu Liu</name>
<name sortKey="Lv, Huanhuan" sort="Lv, Huanhuan" uniqKey="Lv H" first="Huanhuan" last="Lv">Huanhuan Lv</name>
<name sortKey="Lv, Huanhuan" sort="Lv, Huanhuan" uniqKey="Lv H" first="Huanhuan" last="Lv">Huanhuan Lv</name>
<name sortKey="Lv, Huanhuan" sort="Lv, Huanhuan" uniqKey="Lv H" first="Huanhuan" last="Lv">Huanhuan Lv</name>
<name sortKey="Lv, Huanhuan" sort="Lv, Huanhuan" uniqKey="Lv H" first="Huanhuan" last="Lv">Huanhuan Lv</name>
<name sortKey="Shang, Peng" sort="Shang, Peng" uniqKey="Shang P" first="Peng" last="Shang">Peng Shang</name>
<name sortKey="Shang, Peng" sort="Shang, Peng" uniqKey="Shang P" first="Peng" last="Shang">Peng Shang</name>
<name sortKey="Shang, Peng" sort="Shang, Peng" uniqKey="Shang P" first="Peng" last="Shang">Peng Shang</name>
<name sortKey="Yang, Pengfei" sort="Yang, Pengfei" uniqKey="Yang P" first="Pengfei" last="Yang">Pengfei Yang</name>
<name sortKey="Yang, Pengfei" sort="Yang, Pengfei" uniqKey="Yang P" first="Pengfei" last="Yang">Pengfei Yang</name>
<name sortKey="Yang, Pengfei" sort="Yang, Pengfei" uniqKey="Yang P" first="Pengfei" last="Yang">Pengfei Yang</name>
<name sortKey="Yang, Pengfei" sort="Yang, Pengfei" uniqKey="Yang P" first="Pengfei" last="Yang">Pengfei Yang</name>
<name sortKey="Zhen, Chenxiao" sort="Zhen, Chenxiao" uniqKey="Zhen C" first="Chenxiao" last="Zhen">Chenxiao Zhen</name>
<name sortKey="Zhen, Chenxiao" sort="Zhen, Chenxiao" uniqKey="Zhen C" first="Chenxiao" last="Zhen">Chenxiao Zhen</name>
<name sortKey="Zhen, Chenxiao" sort="Zhen, Chenxiao" uniqKey="Zhen C" first="Chenxiao" last="Zhen">Chenxiao Zhen</name>
</country>
</tree>
</affiliations>
</record>
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