322
Views
4
CrossRef citations to date
0
Altmetric
Original Articles

Deficiency of Grx1 leads to high sensitivity of HeLaS3 cells to oxidative stress via excessive accumulation of intracellular oxidants including ROS

&
Pages 585-605 | Received 08 Apr 2020, Accepted 31 Aug 2020, Published online: 21 Sep 2020

References

  • Devasagayam TPA, Tilak JC, Boloor KK, et al. Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicians India. 2004;52:794–804.
  • Banerjee Mustafi S, Chakraborty PK, Dey RS, et al. Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperones. 2009;14(6):579–589.
  • Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci Usa. 1993;90(17):7915–7922.
  • Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science. 2006;312(5782):1882–1883.
  • Choi JY, Cho H-J, Hwang S-G, et al. Podophyllotoxin acetate enhances γ-ionizing radiation-induced apoptotic cell death by stimulating the ROS/p38/caspase pathway. Biomed Pharmacother. 2015;70:111–118.
  • Shelton MD, Chock PB, Mieyal JJ. Glutaredoxin: role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid Redox Signal. 2005;7(3-4):348–366. (
  • Ho Y-S, Xiong Y, Ho DS, et al. Targeted disruption of the glutaredoxin 1 gene does not sensitize adult mice to tissue injury induced by ischemia/reperfusion and hyperoxia. Free Radical Biol Med. 2007;43(9):1299–1312.
  • Yoshikawa Y, Yamasaki A, Takatori K, et al. Excess processing of oxidative damaged bases causes hypersensitivity to oxidative stress and low dose rate irradiation. Free Radic Res. 2015;49(10):1239–1248.
  • Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med. 1991;11(1):81–128.
  • Bohr VA. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic Biol Med. 2002;32(9):804–812.
  • Starke-Reed PE, Oliver CN. Protein oxidation and proteolysis during aging and oxidative stress. Arch Biochem Biophys. 1989;275(2):559–567.
  • Stadtman ER, Oliver CN. Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem. 1991;266(4):2005–2008.
  • Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007;47:143–183.
  • Beckman KB, Ames BN. The free radical theory of aging matures. Physiological reviews, 1998.
  • Sohal RS. Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med. 2002;33(1):37–44.
  • Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem. 1989;264(24):13963–13966.
  • Yoshitake S, Nanri H, Fernando MR, et al. Possible differences in the regenerative roles played by thioltransferase and thioredoxin for oxidatively damaged proteins. J Biochem. 1994;116(1):42–46.
  • Sadhu SS, Callegari E, Zhao Y, et al. Evaluation of a dithiocarbamate derivative as an inhibitor of human glutaredoxin-1. J Enzyme Inhib Med Chem. 2013;28(3):456–462.
  • Allen EM, Mieyal JJ. Protein-thiol oxidation and cell death: regulatory role of glutaredoxins. Antioxid Redox Signal. 2012;17(12):1748–1763.
  • Pai HV, Starke DW, Lesnefsky EJ, et al. What is the functional significance of the unique location of glutaredoxin 1 (GRx1) in the intermembrane space of mitochondria? Antioxid Redox Signal. 2007;9(11):2027–2034.
  • Gladyshev VN, Liu A, Novoselov SV, et al. Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J Biol Chem. 2001;276(32):30374–30380.
  • Lundberg M, Johansson C, Chandra J, et al. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem. 2001;276(28):26269–26275.
  • Lillig CH, et al. Characterization of human glutaredoxin 2 as iron–sulfur protein: a possible role as redox sensor Proceedings of the National Academy of Sciences, 2005. 102(23):8168–8173.
  • Enoksson M, Fernandes AP, Prast S, et al. Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem Biophys Res Commun. 2005;327(3):774–779.
  • Cheng N-H, Zhang W, Chen W-Q, et al. A mammalian monothiol glutaredoxin, Grx3, is critical for cell cycle progression during embryogenesis. Febs J. 2011;278(14):2525–2539.
  • Wingert RA, Galloway JL, Barut B, Tübingen 2000 Screen Consortium, et al. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis. Nature. 2005;436(7053):1035–1039.
  • Ye H, Jeong SY, Ghosh MC, et al. Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts. J Clin Invest. 2010;120(5):1749–1761.
  • Ouyang Y, Peng Y, Li J, et al. Modulation of thiol-dependent redox system by metal ions via thioredoxin and glutaredoxin systems. Metallomics. 2018;10(2):218–228.
  • Song JJ, Lee YJ. Differential role of glutaredoxin and thioredoxin in metabolic oxidative stress-induced activation of apoptosis signal-regulating kinase 1. Biochem J. 2003;373(Pt 3):845–853.
  • Gallogly MM, Shelton MD, Qanungo S, et al. Glutaredoxin regulates apoptosis in cardiomyocytes via NFkappaB targets Bcl-2 and Bcl-xL: implications for cardiac aging. Antioxid Redox Signal. 2010;12(12):1339–1353.
  • Pan S, Berk BC. Glutathiolation regulates tumor necrosis factor-alpha-induced caspase-3 cleavage and apoptosis: key role for glutaredoxin in the death pathway. Circ Res. 2007;100(2):213–219.
  • Sun J, Wei X, Lu Y, et al. Glutaredoxin 1 (GRX1) inhibits oxidative stress and apoptosis of chondrocytes by regulating CREB/HO-1 in osteoarthritis. Mol Immunol. 2017;90:211–218.
  • Liu X, Jann J, Xavier C, et al. Glutaredoxin 1 (Grx1) protects human retinal pigment epithelial cells from oxidative damage by preventing AKT glutathionylation. Invest Ophthalmol Vis Sci. 2015;56(5):2821–2832.
  • Li Y, et al. Glutaredoxin 1 mediates the protective effect of steady laminar flow on endothelial cells against oxidative stress-induced apoptosis via inhibiting Bim. Sci Rep. 2017;7(1):1–11.
  • Hosoki A, Yonekura S-I, Zhao Q-L, et al. Mitochondria-targeted superoxide dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J Radiat Res. 2012;53(1):58–71.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281–2308.
  • Sanada Y, Sasanuma H, Takeda S, et al. Disruption of Hif-1α enhances cytotoxic effects of metformin in murine squamous cell carcinoma. Int J Radiat Biol. 2018;94(1):88–96.
  • Yan Y, Sabharwal P, Rao M, et al. The antioxidant enzyme Prdx1 controls neuronal differentiation by thiol-redox-dependent activation of GDE2. Cell. 2009;138(6):1209–1221.
  • Shi D-Y, Liu H-L, Stern JS, et al. Alpha-lipoic acid induces apoptosis in hepatoma cells via the PTEN/Akt pathway. FEBS Lett. 2008;582(12):1667–1671.
  • Hardy M, Zielonka J, Karoui H, et al. Detection and characterization of reactive oxygen and nitrogen species in biological systems by monitoring species-specific products. Antioxid Redox Signal. 2018;28(15):1416–1432.
  • Rajavel T, Packiyaraj P, Suryanarayanan V, et al. β-Sitosterol targets Trx/Trx1 reductase to induce apoptosis in A549 cells via ROS mediated mitochondrial dysregulation and p53 activation. Sci Rep. 2018;8(1):1–15.
  • Peskin AV, Low FM, Paton LN, et al. The high reactivity of peroxiredoxin 2 with H2O2 is not reflected in its reaction with other oxidants and thiol reagents. J Biol Chem. 2007;282(16):11885–11892.
  • Peskin AV, Pace PE, Behring JB, et al. Glutathionylation of the active site cysteines of peroxiredoxin 2 and recycling by glutaredoxin. J Biol Chem. 2016;291(6):3053–3062.
  • Kalyanaraman B, Darley-Usmar V, Davies KJA, et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med. 2012;52(1):1–6.
  • Thornton TM, Rincon M. Non-classical p38 map kinase functions: cell cycle checkpoints and survival. Int J Biol Sci. 2009;5(1):44–51.
  • Chen Y-R, Chen C-L, Pfeiffer DR, et al. Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem. 2007;282(45):32640–32654.
  • Wang J, Boja ES, Tan W, et al. Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem. 2001;276(51):47763–47766.
  • Chen FC, Ogut O. Decline of contractility during ischemia-reperfusion injury: actin glutathionylation and its effect on allosteric interaction with tropomyosin. Am J Physiol, Cell Physiol. 2006;290(3):C719–C727.
  • Eaton P, Wright N, Hearse DJ, et al. Glyceraldehyde phosphate dehydrogenase oxidation during cardiac ischemia and reperfusion. J Mol Cell Cardiol. 2002;34(11):1549–1560.
  • Hurd TR, Requejo R, Filipovska A, et al. Complex I within Oxidatively Stressed Bovine Heart Mitochondria Is Glutathionylated on Cys-531 and Cys-704 of the 75-kDa subunit: potential role of CYS residues in decreasing oxidative damage. J Biol Chem. 2008;283(36):24801–24815.
  • Dalle-Donne I, Milzani A, Gagliano N, et al. Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal. 2008;10(3):445–474.
  • Mieyal JJ, Gallogly MM, Qanungo S, et al. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal. 2008;10(11):1941–1988.
  • Pineda-Molina E, Klatt P, Vázquez J, et al. Glutathionylation of the p50 subunit of NF-kappaB: a mechanism for redox-induced inhibition of DNA binding . Biochemistry. 2001;40(47):14134–14142.
  • Adachi T, Pimentel DR, Heibeck T, et al. S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem. 2004;279(28):29857–29862.
  • Yang F, Yi M, Liu Y, et al. Glutaredoxin-1 silencing induces cell senescence via p53/p21/p16 signaling axis. J Proteome Res. 2018;17(3):1091–1100.
  • Sharma P, Jha AB, Dubey RS, et al. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany. 2012;2012:1–26.,
  • Ray PD, Huang B-W, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012;24(5):981–990.
  • Manta B, Hugo M, Ortiz C, et al. The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch Biochem Biophys. 2009;484(2):146–154.
  • Rhee SG, Woo HA. Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H2O2, and protein chaperones. Antioxid Redox Signaling. 2011;15(3):781–794.
  • Scherz-Shouval R, Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 2007;17(9):422–427.
  • Taylor ER, Hurrell F, Shannon RJ, et al. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J Biol Chem. 2003;278(22):19603–19610.
  • Suski JM, et al. Relation between mitochondrial membrane potential and ROS formation, in Mitochondrial bioenergetics. Springer; 2012. p. 183–205.
  • Lau LF. CCN1/CYR61: the very model of a modern matricellular protein. Cell Mol Life Sci. 2011;68(19):3149–3163.
  • Stavreus-Evers A, et al. Immunohistochemical localization of glutaredoxin and thioredoxin in human endometrium: a possible association with pinopodes. MHR: Basic Science of Reproductive Medicine. 2002;8(6):546–551.
  • Gallogly MM, Starke DW, Mieyal JJ. Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal. 2009;11(5):1059–1081.
  • Kwon J, Lee S-R, Yang K-S, et al. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. ProcNatl Acad Sci. 2004;101(47):16419–16424.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.