Redox regulation of p53, redox effectors regulated by p53: A subtle balance

Antioxidants and Redox Signaling

Volumn 16, Issue 11, 2012, Pages 1285-1294

  Maillet, Agnès ^a   Pervaiz, Shazib ^a,b,c,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SINGAPORE MIT ALLIANCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2; GLUTATHIONE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE SYNTHASE; PROLINE DEHYDROGENASE; PROTEIN BAX; PROTEIN P53; REACTIVE OXYGEN METABOLITE; THIOREDOXIN;

CELL FATE; CELL FUNCTION; ENZYME ACTIVITY; GENE CONTROL; GENOMIC INSTABILITY; INTRACELLULAR SIGNALING; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; STRESS;

ANIMALS; HUMANS; OXIDATION-REDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84859855907     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4434     Document Type: Review

References (94)

1. Abbas HA, Maccio DR, Coskun S, Jackson JG, Hazen AL, Sills TM, You MJ, Hirschi KK, and Lozano G. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 7: 606-617, 2010.
2. Achanta G, Sasaki R, Feng L, Carew JS, Lu W, Pelicano H, Keating MJ, and Huang P. Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J 24: 3482-3492, 2005. (Pubitemid 41486785)
3. Ahmad KA, Clement MV, Hanif IM, and Pervaiz S. Resveratrol inhibits drug-induced apoptosis in human leukemia cells by creating an intracellular milieu nonpermissive for death execution. Cancer Res 64: 1452-1459, 2004. (Pubitemid 38235616)
4. Ahmad KA, Clement MV, and Pervaiz S. Pro-oxidant activity of low doses of resveratrol inhibits hydrogen peroxideinduced apoptosis. Ann N Y Acad Sci 1010: 365-373, 2003. (Pubitemid 38265009)
5. Ambs S, Ogunfusika MO, Merriam WG, Bennett WP, Billiar TR, and Harris CC. Up-regulation of inducible nitric oxide synthase expression in cancer-prone p53 knockout mice. Proc Natl Acad Sci USA 95: 8823-8828, 1998.
6. Arner ES and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109, 2000.
7. Arrigo AP. Gene expression and the thiol redox state. Free Radic Biol Med 27: 936-944, 1999.
8. Baker SJ, Fearon ER, Nigro JM, Hamilton SR, Preisinger AC, Jessup JM, vanTuinen P, Ledbetter DH, Barker DF, Nakamura Y, White R, and Vogelstein B. Chromosome 17 deletions and p53 gene mutations in colorectal carcinomas. Science 244: 217-221, 1989. (Pubitemid 19110302)
9. Berglind H, Pawitan Y, Kato S, Ishioka C, and Soussi T. Analysis of p53 mutation status in human cancer cell lines: a paradigm for cell line cross-contamination. Cancer Biol Ther 7: 699-708, 2008.
10. Brynczka C, Labhart P, and Merrick BA. NGF-mediated transcriptional targets of p53 in PC12 neuronal differentiation. BMC Genomics 8: 139, 2007.
11. Cassidy PB, Edes K, Nelson CC, Parsawar K, Fitzpatrick FA, and Moos PJ. Thioredoxin reductase is required for the inactivation of tumor suppressor p53 and for apoptosis induced by endogenous electrophiles. Carcinogenesis 27: 2538-2549, 2006. (Pubitemid 44884113)
12. Cheng NH, Zhang W, Chen WQ, Jin J, Cui X, Butte NF, Chan L, and Hirschi KD. A mammalian monothiol glutaredoxin, Grx3, is critical for cell cycle progression during embryogenesis. FEBS J 278: 2525-2539, 2011.
13. Choi EM, Kim SR, Lee EJ, and Han JA. Cyclooxygenase-2 functionally inactivates p53 through a physical interaction with p53. Biochim Biophys Acta 1793: 1354-1365, 2009.
14. Clement MV, Hirpara JL, and Pervaiz S. Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria. Cell Death Differ 10: 1273-1285, 2003. (Pubitemid 37407129)
15. Clement MV and Pervaiz S. Reactive oxygen intermediates regulate cellular response to apoptotic stimuli: an hypothesis. Free Radic Res 30: 247-252, 1999. (Pubitemid 29213163)
16. Clement MV and Pervaiz S. Intracellular superoxide and hydrogen peroxide concentrations: a critical balance that determines survival or death. Redox Rep 6: 211-214, 2001. (Pubitemid 32962820)
17. Clement MV, Ponton A, and Pervaiz S. Apoptosis induced by hydrogen peroxide is mediated by decreased superoxide anion concentration and reduction of intracellular milieu. FEBS Lett 440: 13-18, 1998. (Pubitemid 28558725)
18. Cobbs CS, Samanta M, Harkins LE, Gillespie GY, and Merrick BA, MacMillan-Crow LA. Evidence for peroxynitritemediated modifications to p53 in human gliomas: possible functional consequences. Arch Biochem Biophys 394: 167-172, 2001. (Pubitemid 32989325)
19. Cobbs CS, Whisenhunt TR, Wesemann DR, Harkins LE, Van Meir EG, and Samanta M. Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res 63: 8670-8673, 2003. (Pubitemid 38064042)
20. 2. J Biol Chem 279: 31157-31163, 2004. (Pubitemid 39037778)
21. Dhar SK, Xu Y, Chen Y, and St. Clair DK. Specificity protein 1-dependent p53-mediated suppression of human manganese superoxide dismutase gene expression. J Biol Chem 281: 21698-21709, 2006. (Pubitemid 44181873)
22. Dhar SK, Xu Y, and St. Clair DK. Nuclear factor kappaB-and specificity protein 1-dependent p53-mediated bi-directional regulation of the human manganese superoxide dismutase gene. J Biol Chem 285: 9835-9846, 2010.
23. Diebold I, Flugel D, Becht S, Belaiba RS, Bonello S, Hess J, Kietzmann T, and Gorlach A. The hypoxia-inducible factor-2alpha is stabilized by oxidative stress involving NOX4. Antioxid Redox Signal 13: 425-436, 2010.
24. Donald SP, Sun XY, Hu CA, Yu J, Mei JM, Valle D, and Phang JM. Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species. Cancer Res 61: 18101815, 2001.
25. Drahota Z, Chowdhury SK, Floryk D, Mracek T, Wilhelm J, Rauchova H, Lenaz G, and Houstek J. Glycerophosphatedependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J Bioenerg Biomembr 34: 105-113, 2002. (Pubitemid 34477973)
26. Drane P, BravardA, Bouvard V, andMay E. Reciprocal downregulation of p53 and SOD2 gene expression-implication in p53 mediated apoptosis. Oncogene 20: 430-439, 2001. (Pubitemid 32158223)
27. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
28. Fernando MR, Nanri H, Yoshitake S, Nagata-Kuno K, and Minakami S. Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells. Eur J Biochem 209: 917-922, 1992.
29. Finkel T and Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247, 2000.
30. Flatt PM, Polyak K, Tang LJ, Scatena CD, Westfall MD, Rubinstein LA, Yu J, Kinzler KW, Vogelstein B, Hill DE, and Pietenpol JA. p53-dependent expression of PIG3 during proliferation, genotoxic stress, and reversible growth arrest. Cancer Lett 156: 63-72, 2000. (Pubitemid 30326769)
31. Forrester K, Ambs S, Lupold SE, Kapust RB, Spillare EA, Weinberg WC, Felley-Bosco E, Wang XW, Geller DA, Tzeng E, Billiar TR, and Harris CC. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc Natl Acad Sci USA 93: 2442-2447, 1996. (Pubitemid 26104369)
32. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, and Pelicci PG. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122: 221-233, 2005. (Pubitemid 41032986)
33. Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, and Del Sal G. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 18: 6462-6471, 1999. (Pubitemid 29533250)
34. Gottlieb E and Vousden KH. p53 regulation of metabolic pathways. Cold Spring Harb Perspect Biol 2: a001040, 2010.
35. Hafsi H and Hainaut P. Redox control and interplay between p53 isoforms: roles in the regulation of basal p53 levels, cell fate, and senescence. Antioxid Redox Signal 15: 1655-1667, 2011.
36. Halliwell B, Gutteridge JM, and Cross CE. Free radicals, antioxidants, and human disease: where are we now? J Lab Clin Med 119: 598-620, 1992.
37. Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev 38: 171-196, 2006. (Pubitemid 43739006)
38. Henry Y, Lepoivre M, Drapier JC, Ducrocq C, Boucher JL, and Guissani A. EPR characterization of molecular targets for NO in mammalian cells and organelles. FASEB J 7: 1124-1134, 1993. (Pubitemid 23271031)
39. Higashimoto Y, Saito S, Tong XH, Hong A, Sakaguchi K, Appella E, and Anderson CW. Human p53 is phosphorylated on serines 6 and 9 in response to DNA damageinducing agents. J Biol Chem 275: 23199-23203, 2000. (Pubitemid 30646216)
40. Hirpara JL, Clement MV, and Pervaiz S. Intracellular acidification triggered by mitochondrial-derived hydrogen peroxide is an effector mechanism for drug-induced apoptosis in tumor cells. J Biol Chem 276: 514-521, 2001. (Pubitemid 32050345)
41. Hussain SP, Amstad P, He P, Robles A, Lupold S, Kaneko I, Ichimiya M, Sengupta S, Mechanic L, Okamura S, Hofseth LJ, Moake M, Nagashima M, Forrester KS, and Harris CC. p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res 64: 2350-2356, 2004. (Pubitemid 38523887)
42. Jayaraman L, Murthy KG, Zhu C, Curran T, Xanthoudakis S, and Prives C. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev 11: 558-570, 1997. (Pubitemid 27133376)
43. Jiang F, Zhang Y, and Dusting GJ. NADPH oxidasemediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 63: 218-242, 2011.
44. Jiang J, Borisenko GG, Osipov A, Martin I, Chen R, Shvedova AA, Sorokin A, Tyurina YY, Potapovich A, Tyurin VA, Graham SH, and Kagan VE. Arachidonic acid-induced carbon-centered radicals and phospholipid peroxidation in cyclo-oxygenase-2-transfected PC12 cells. J Neurochem 90: 1036-1049, 2004. (Pubitemid 39167337)
45. Johnson TM, Yu ZX, Ferrans VJ, Lowenstein RA, and Finkel T. Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proc Natl Acad Sci USA 93: 11848-11852, 1996. (Pubitemid 26347212)
46. Keisari Y, Braun L, and Flescher E. The oxidative burst and related phenomena inmousemacrophages elicited by different sterile inflammatory stimuli. Immunobiology 165: 78-89, 1983. (Pubitemid 13075939)
47. Kontos HA, Wei EP, Povlishock JT, Dietrich WD, Magiera CJ, and Ellis EF. Cerebral arteriolar damage by arachidonic acid and prostaglandin G2. Science 209: 1242-1245, 1980. (Pubitemid 10019752)
48. Lane DP and Crawford LV. T antigen is bound to a host protein in SV40-transformed cells. Nature 278: 261-263, 1979. (Pubitemid 9129076)
49. Lavrovsky Y, Chatterjee B, Clark RA, and Roy AK. Role of redox-regulated transcription factors in inflammation, aging and age-related diseases. Exp Gerontol 35: 521-532, 2000.
50. Lebedeva MA, Eaton JS, and Shadel GS. Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim Biophys Acta 1787: 328-334, 2009.
51. Lee JH, Kang Y, Khare V, Jin ZY, Kang MY, Yoon Y, Hyun JW, Chung MH, Cho SI, Jun JY, Chang IY, and You HJ. The p53-inducible gene 3 (PIG3) contributes to early cellular response to DNA damage. Oncogene 29: 1431-1450, 2010.
52. Legan M, Luzar B, Marolt VF, and Cor A. Expression of cyclooxygenase-2 is associated with p53 accumulation in premalignant and malignant gallbladder lesions. World J Gastroenterol 12: 3425-3429, 2006. (Pubitemid 43933791)
53. Leto TL, Morand S, Hurt D, and Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal 11: 2607-2619, 2009.
54. Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, and Gu W. Mono-versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302: 1972-1975, 2003. (Pubitemid 37523506)
55. Li Z, Shi K, Guan L, Cao T, Jiang Q, Yang Y, and Xu C. ROS leads to MnSOD upregulation through ERK2 translocation and p53 activation in selenite-induced apoptosis of NB4 cells. FEBS Lett 584: 2291-2297, 2010.
56. 2 formation. Free Radic Biol Med 42: 1465-1469, 2007. (Pubitemid 46590616)
57. Liu Z, Lu H, Shi H, Du Y, Yu J, Gu S, Chen X, Liu KJ, and Hu CA. PUMA overexpression induces reactive oxygen species generation and proteasome-mediated stathmin degradation in colorectal cancer cells. Cancer Res 65: 1647-1654, 2005. (Pubitemid 40478588)
58. Los M, Schenk H, Hexel K, Baeuerle PA, Droge W, and Schulze-Osthoff K. IL-2 gene expression and NF-kappa B activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J 14: 3731-3740, 1995.
59. Margis R, Dunand C, Teixeira FK, and Margis-Pinheiro M. Glutathione peroxidase family-an evolutionary overview. FEBS J 275: 3959-3970, 2008. (Pubitemid 351990959)
60. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, Hurley PJ, Bunz F, and Hwang PM. p53 regulates mitochondrial respiration. Science 312: 1650-1653, 2006. (Pubitemid 43902663)
61. Miyashita T and Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80: 293-299, 1995.
62. Moos PJ, Edes K, Cassidy P, Massuda E, and Fitzpatrick FA. Electrophilic prostaglandins and lipid aldehydes repress redox-sensitive transcription factors p53 and hypoxiainducible factor by impairing the selenoprotein thioredoxin reductase. J Biol Chem 278: 745-750, 2003. (Pubitemid 36790745)
63. Nathan CF and Root RK. Hydrogen peroxide release from mouse peritoneal macrophages: dependence on sequential activation and triggering. J Exp Med 146: 1648-1662, 1977. (Pubitemid 8245448)
64. Nigro JM, Baker SJ, Preisinger AC, Jessup JM, Hostetter R, Cleary K, Bigner SH, Davidson N, Baylin S, Devilee P, et al. Mutations in the p53 gene occur in diverse human tumour types. Nature 342: 705-708, 1989. (Pubitemid 20001591)
65. Ostrakhovitch EA and Cherian MG. Role of p53 and reactive oxygen species in apoptotic response to copper and zinc in epithelial breast cancer cells. Apoptosis 10: 111-121, 2005. (Pubitemid 40558119)
66. Pani G, Bedogni B, Anzevino R, Colavitti R, Palazzotti B, Borrello S, and Galeotti T. Deregulated manganese superoxide dismutase expression and resistance to oxidative injury in p53-deficient cells. Cancer Res 60: 4654-4660, 2000. (Pubitemid 32106655)
67. PearsonM, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S, Higashimoto Y, Appella E, Minucci S, Pandolfi PP, and Pelicci PG. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406: 207-210, 2000. (Pubitemid 30469006)
68. Pervaiz S, Cao J, Chao OS, Chin YY, and Clement MV. Activation of the RacGTPase inhibits apoptosis in human tumor cells. Oncogene 20: 6263-6268, 2001. (Pubitemid 32970414)
69. Pervaiz S and Clement MV. Superoxide anion: oncogenic reactive oxygen species? Int J Biochem Cell Biol 39: 1297-1304, 2007. (Pubitemid 47031046)
70. Pietenpol JA, Tokino T, Thiagalingam S, el-Deiry WS, Kinzler KW, and Vogelstein B. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc Natl Acad Sci USA 91: 1998-2002, 1994. (Pubitemid 24092029)
71. Polyak K, Xia Y, Zweier JL, Kinzler KW, and Vogelstein B. A model for p53-induced apoptosis. Nature 389: 300-305, 1997. (Pubitemid 27406646)
72. Powis G, Briehl M, and Oblong J. Redox signalling and the control of cell growth and death. Pharmacol Ther 68: 149-173, 1995.
73. Qu Y, Wang J, Ray PS, Guo H, Huang J, Shin-Sim M, Bukoye BA, Liu B, Lee AV, Lin X, Huang P, Martens JW, Giuliano AE, Zhang N, Cheng NH, and Cui X. Thioredoxin-like 2 regulates human cancer cell growth and metastasis via redox homeostasis and NF-kappaB signaling. J Clin Invest 121: 212-225, 2011.
74. Raha S and Robinson BH. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25: 502-508, 2000.
75. Raha S and Robinson BH. Mitochondria, oxygen free radicals, and apoptosis. Am J Med Genet 106: 62-70, 2001.
76. Ravi D, Muniyappa H, and Das KC. Endogenous thioredoxin is required for redox cycling of anthracyclines and p53-dependent apoptosis in cancer cells. J Biol Chem 280: 40084-40096, 2005. (Pubitemid 41779143)
77. Richie JP, Jr., Komninou D, and Albino AP. Induction of colon tumorigenesis by glutathione depletion in p53-knockout mice. Int J Oncol 30: 1539-1543, 2007.
78. Rivera A and Maxwell SA. The p53-induced gene-6 (proline oxidase) mediates apoptosis through a calcineurin-dependent pathway. J Biol Chem 280: 29346-29354, 2005. (Pubitemid 41161390)
79. Russo T, Zambrano N, Esposito F, Ammendola R, Cimino F, Fiscella M, Jackman J, O'Connor PM, Anderson CW, and Appella E. A p53-independent pathway for activation of WAF1/CIP1 expression following oxidative stress. J Biol Chem 270: 29386-29391, 1995.
80. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, and Chumakov PM. The antioxidant function of the p53 tumor suppressor. Nat Med 11: 1306-1313, 2005. (Pubitemid 41752911)
81. Stoner CS, Pearson GD, Koc A, Merwin JR, Lopez NI, and Merrill GF. Effect of thioredoxin deletion and p53 cysteine replacement on human p53 activity in wild-type and thioredoxin reductase null yeast. Biochemistry 48: 9156-9169, 2009.
82. Subbaramaiah K, Altorki N, Chung WJ, Mestre JR, Sampat A, and Dannenberg AJ. Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 274: 10911-10915, 1999.
83. Tan M, Heizmann CW, Guan K, Schafer BW, and Sun Y. Transcriptional activation of the human S100A2 promoter by wild-type p53. FEBS Lett 445: 265-268, 1999. (Pubitemid 29117224)
84. Tan M, Li S, Swaroop M, Guan K, Oberley LW, and Sun Y. Transcriptional activation of the human glutathione peroxidase promoter by p53. J Biol Chem 274: 12061-12066, 1999.
85. Tanaka K, Abe M, and Shigematsu N. Effects of a 5-lipoxygenase inhibitor, AA861, on lipoxygenase metabolism and superoxide anion generation by human polymorphonuclear leukocytes-potentiation of superoxide anion generation by LTB4. Int Arch Allergy Immunol 98: 361-369, 1992.
86. Tokino T and Nakamura Y. The role of p53-target genes in human cancer. Crit Rev Oncol Hematol 33: 1-6, 2000. (Pubitemid 30064481)
87. Townsend DM and Tew KD. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22: 7369-7375, 2003.
88. Tretter L and Adam-Vizi V. Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J Neurosci 24: 7771-7778, 2004. (Pubitemid 39215680)
89. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, and Yodoi J. Redox control of cell death. Antioxid Redox Signal 4: 405-414, 2002. (Pubitemid 34753380)
90. Velaithan R, Kang J, Hirpara JL, Loh T, Goh BC, Le Bras M, Brenner C, Clement MV, and Pervaiz S. The small GTPase Rac1 is a novel binding partner of Bcl-2 and stabilizes its antiapoptotic activity. Blood 117: 6214-6226, 2011.
91. Velu CS, Niture SK, Doneanu CE, Pattabiraman N, and Srivenugopal KS. Human p53 is inhibited by glutathionylation of cysteines present in the proximal DNA-binding domain during oxidative stress. Biochemistry 46: 7765-7780, 2007. (Pubitemid 47016060)
92. Wynford-Thomas D and Blaydes J. The influence of cell context on the selection pressure for p53 mutation in human cancer. Carcinogenesis 19: 29-36, 1998. (Pubitemid 28376822)
93. Yakovlev VA, Bayden AS, Graves PR, Kellogg GE, and Mikkelsen RB. Nitration of the tumor suppressor protein p53 at tyrosine 327 promotes p53 oligomerization and activation. Biochemistry 49: 5331-5339, 2010.
94. Yusuf MA, Chuang T, Bhat GJ, and Srivenugopal KS. Cys-141 glutathionylation of human p53: studies using specific polyclonal antibodies in cancer samples and cell lines. Free Radic Biol Med 49: 908-917, 2010.