Lack of p53 decreases basal oxidative stress levels in the brain through upregulation of thioredoxin-1, biliverdin reductase-A, manganese superoxide dismutase, and nuclear factor kappa-B

Antioxidants and Redox Signaling

Volumn 16, Issue 12, 2012, Pages 1407-1420

  Barone, Eugenio ^a,b,c   Cenini, Giovanna ^a,b   Sultana, Rukhsana ^a,b   Di Domenico, Fabio ^a,b,d   Fiorini, Ada ^a,b,d   Perluigi, Marzia ^d   Noel, Teresa ^a   Wang, Chi ^a   Mancuso, Cesare ^c   St Clair, Daret K ^a   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c CATHOLIC UNIVERSITY   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; 4 HYDROXYNONENAL; BILIVERDIN; HEME OXYGENASE 1; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; OXIDOREDUCTASE; PROTEIN P53; THIOREDOXIN 1; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOSOL; HOMOGENATE; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; MOUSE MUTANT; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN DEPLETION; UPREGULATION; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; BRAIN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MICE; MICE, KNOCKOUT; NF-KAPPA B; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; SUPEROXIDE DISMUTASE; THIOREDOXINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84860206827     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4124     Document Type: Article

References (70)

1. Ak P and Levine AJ. p53 and NF-kappaB: different strategies for responding to stress lead to a functional antagonism. FASEB J 24: 3643-3652, 2010.
2. 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.
3. Arner ES and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109, 2000.
4. Bakthavatchalu V, Dey S, Xu Y, Noel T, Jungsuwadee P, Holley AK, Dhar SK, Batinic-Haberle I, and St. Clair DK. Manganese superoxide dismutase is a mitochondrial fidelity protein that protects Polgamma against UV-induced inactivation. Oncogene 2011. [Epub ahead of print]; DOI: 10.1038/onc.2011.407
5. Barone E, Trombino S, Cassano R, Sgambato A, De Paola B, Di Stasio E, Picci N, Preziosi P, and Mancuso C. Characterization of the S-denitrosylating activity of bilirubin. J Cell Mol Med 13: 2365-2375, 2009.
6. Bedogni B, Pani G, Colavitti R, Riccio A, Borrello S, Murphy M, Smith R, Eboli ML, and Galeotti T. Redox regulation of cAMP-responsive element-binding protein and induction of manganese superoxide dismutase in nerve growth factordependent cell survival. J Biol Chem 278: 16510-16519, 2003. (Pubitemid 36799511)
7. Bowie A and O'Neill LA. Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 59: 13-23, 2000.
8. Brand KA and Hermfisse U. Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species. FASEB J 11: 388-395, 1997. (Pubitemid 27193945)
9. Butterfield DA and Lauderback CM. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptideassociated free radical oxidative stress. Free Radic Biol Med 32: 1050-1060, 2002. (Pubitemid 34603342)
10. Calabrese V, Cornelius C, Mancuso C, Barone E, Calafato S, Bates T, Rizzarelli E, and Kostova AT. Vitagenes, dietary antioxidants and neuroprotection in neurodegenerative diseases. Front Biosci 14: 376-397, 2009.
11. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, and Stella AM. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8: 766-775, 2007. (Pubitemid 47462116)
12. Calmels S, Hainaut P, and Ohshima H. Nitric oxide induces conformational and functional modifications of wild-type p53 tumor suppressor protein. Cancer Res 57: 3365-3369, 1997. (Pubitemid 27355476)
13. Cenini G, Sultana R, Memo M, and Butterfield DA. Effects of oxidative and nitrosative stress in brain on p53 proapoptotic protein in amnestic mild cognitive impairment and Alzheimer disease. Free Radic Biol Med 45: 81-85, 2008.
14. Cenini G, Sultana R, Memo M, and Butterfield DA. Elevated levels of pro-apoptotic p53 and its oxidative modification by the lipid peroxidation product, HNE, in brain from subjects with amnestic mild cognitive impairment and Alzheimer's disease. J Cell Mol Med 12: 987-994, 2008. (Pubitemid 351718076)
15. Chatoo W, Abdouh M, and Bernier G. p53 Pro-oxidant activity in the central nervous system: implication in aging and neurodegenerative diseases. Antioxid Redox Signal 15: 1729-1737, 2011.
16. Chatoo W, Abdouh M, David J, Champagne MP, Ferreira J, Rodier F, and Bernier G. The polycomb group gene Bmi1 regulates antioxidant defenses in neurons by repressing p53 pro-oxidant activity. J Neurosci 29: 529-542, 2009.
17. Dai C and Gu W. p53 post-translational modification: deregulated in tumorigenesis. Trends Mol Med 16: 528-536, 2010.
18. 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)
19. 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.
20. Di Domenico F, Casalena G, Sultana R, Cai J, Pierce WM, PerluigiM, Cini C, Baracca A, Solaini G, Lenaz G, Jia J, Dziennis S, Murphy SJ, Alkayed NJ, and Butterfield DA. Involvement of Stat3 in mouse brain development and sexual dimorphism: a proteomics approach. Brain Res 1362: 1-12, 2010.
21. Di Domenico F, Cenini G, Sultana R, Perluigi M, Uberti D, Memo M, and Butterfield DA. Glutathionylation of the proapoptotic protein p53 in Alzheimer's disease brain: implications for AD pathogenesis. Neurochem Res 34: 727-733, 2009.
22. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, and Snyder SH. Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450, 1999. (Pubitemid 29117935)
23. Ewing JF, Weber CM, and Maines MD. Biliverdin reductase is heat resistant and coexpressed with constitutive and heat shock forms of heme oxygenase in brain. J Neurochem 61: 1015-1023, 1993. (Pubitemid 23241240)
24. Finkel T. Oxygen radicals and signaling. Curr Opin Cell Biol 10: 248-253, 1998. (Pubitemid 28174767)
25. 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)
26. Franklin EM, Browne S, Horan AM, Inomata K, Hammam MA, Kinoshita H, Lamparter T, Golfis G, and Mantle TJ. The use of synthetic linear tetrapyrroles to probe the verdin sites of human biliverdin-IX alpha reductase and human biliverdin-IX beta reductase. FEBS J 276: 4405-4413, 2009.
27. Gupta R, Rao Gogineni V, Nalla AK, Chetty C, Klopfenstein JD, Tsung AJ, Mohanam S, and Rao JS. Oncogenic role of p53 is suppressed by si-RNA bicistronic construct of uPA, uPAR and cathepsin-B in meningiomas both in vitro and in vivo. Int J Oncol 38: 973-983, 2011.
28. Hadj Amor IY, Smaoui K, Chaabene I, Mabrouk I, Djemal L, Elleuch H, Allouche M, Mokdad-Gargouri R, and Gargouri A. Human p53 induces cell death and downregulates thioredoxin expression in Saccharomyces cerevisiae. FEMS Yeast Res 8: 1254-1262, 2008.
29. 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.
30. Hernlund E, Kutuk O, Basaga H, Linder S, Panaretakis T, and Shoshan M. Cisplatin-induced nitrosylation of p53 prevents its mitochondrial translocation. Free Radic Biol Med 46: 1607-1613, 2009.
31. Hirota K, Nakamura H, Masutani H, and Yodoi J. Thioredoxin superfamily and thioredoxin-inducing agents. Ann N Y Acad Sci 957: 189-199, 2002. (Pubitemid 34721664)
32. Holley AK, Bakthavatchalu V, Velez-Roman JM, and St. Clair DK. Manganese superoxide dismutase: guardian of the powerhouse. Int J Mol Sci 12: 7114-7162, 2011.
33. Holley AK, Dhar SK, and St. Clair DK. Manganese superoxide dismutase versus p53: the mitochondrial center. Ann N Y Acad Sci 1201: 72-78, 2010.
34. Holley AK and St. Clair DK. Preventing Dr. Jekyll from becoming Mr. Hyde: is manganese superoxide dismutase the key to prevent radiation-induced neoplastic transformation? Cancer Biol Ther 8: 1972-1973, 2009.
35. 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)
36. Kapitulnik J and Maines MD. Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol Sci 30: 129-137, 2009.
37. Kim YC, Masutani H, Yamaguchi Y, Itoh K, Yamamoto M, and Yodoi J. Hemin-induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors. J Biol Chem 276: 18399-18406, 2001.
38. Kraus JL, Conti F, Madonna S, Tchoghandjian A, and Beclin C. Alternative responses of primary tumor cells and glioblastoma cell lines to N,N-bis-(8-hydroxyquinoline-5-yl methyl)-benzyl substituted amines: cell death versus P53-independent senescence. Int J Oncol 37: 1463-1470, 2010.
39. Lanni C, Uberti D, Racchi M, Govoni S, and Memo M. Unfolded p53: a potential biomarker for Alzheimer's disease. J Alzheimers Dis 12: 93-99, 2007. (Pubitemid 47396308)
40. 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.
41. Lim YP, Lim TT, Chan YL, Song AC, Yeo BH, Vojtesek B, Coomber D, Rajagopal G, and Lane D. The p53 knowledgebase: an integrated information resource for p53 research. Oncogene 26: 1517-1521, 2007. (Pubitemid 46398738)
42. Liu B, Chen Y, and St. Clair DK. ROS and p53: a versatile partnership. Free Radic Biol Med 44: 1529-1535, 2008.
43. Lozano G. Mouse models of p53 functions. Cold Spring Harb Perspect Biol 2: a001115, 2010.
44. Maines MD. The heme oxygenase system and its functions in the brain. Cell Mol Biol (Noisy-le-grand) 46: 573-585, 2000.
45. Mancuso C and Barone E. The heme oxygenase/biliverdin reductase pathway in drug research and development. Curr Drug Metab 10: 579-594, 2009.
46. Mancuso C, Capone C, Ranieri SC, Fusco S, Calabrese V, Eboli ML, Preziosi P, Galeotti T, and Pani G. Bilirubin as an endogenous modulator of neurotrophin redox signaling. J Neurosci Res 86: 2235-2249, 2008.
47. Mark RJ, Lovell MA, Markesbery WR, Uchida K, and Mattson MP. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J Neurochem 68: 255-264, 1997. (Pubitemid 26427315)
48. Markesbery WR. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23: 134-147, 1997. (Pubitemid 27217017)
49. Matheu A, Maraver A, Klatt P, Flores I, Garcia-Cao I, Borras C, Flores JM, Vina J, Blasco MA, and Serrano M. Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448: 375-379, 2007. (Pubitemid 47080339)
50. Meiller A, Alvarez S, Drane P, Lallemand C, Blanchard B, Tovey M, and May E. p53-dependent stimulation of redoxrelated genes in the lymphoid organs of gamma-irradiated-mice identification of haeme-oxygenase 1 as a direct p53 target gene. Nucleic Acids Res 35: 6924-6934, 2007. (Pubitemid 350201811)
51. Miao L and St. Clair DK. Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med 47: 344-356, 2009.
52. Nam SY and Sabapathy K. p53 promotes cellular survival in a context-dependent manner by directly inducing the expression of haeme-oxygenase-1. Oncogene 30: 4476-4486, 2011.
53. 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)
54. Polyak K, Xia Y, Zweier JL, Kinzler KW, and Vogelstein B. A model for p53-induced apoptosis. Nature 389: 300-305, 1997. (Pubitemid 27406646)
55. 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)
56. 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)
57. Schulze-Osthoff K, Beyaert R, Vandevoorde V, Haegeman G, and Fiers W. Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J 12: 3095-3104, 1993. (Pubitemid 23232740)
58. Simons AL, Mattson DM, Dornfeld K, and Spitz DR. Glucose deprivation-induced metabolic oxidative stress and cancer therapy. J Cancer Res Ther 5 Suppl 1: S2-S6, 2009.
59. Sims NR. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J Neurochem 55: 698-707, 1990. (Pubitemid 120021648)
60. Stambolsky P, Weisz L, Shats I, Klein Y, Goldfinger N, Oren M, and Rotter V. Regulation of AIF expression by p53. Cell Death Differ 13: 2140-2149, 2006. (Pubitemid 44742697)
61. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, and Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046, 1987. (Pubitemid 17049750)
62. Sultana R, Perluigi M, and Butterfield DA. Protein oxidation and lipid peroxidation in brain of subjects with Alzheimer's disease: insights into mechanism of neurodegeneration from redox proteomics. Antioxid Redox Signal 8: 2021-2037, 2006. (Pubitemid 46499264)
63. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo MM, Yamamoto M, and Igarashi K. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 21: 5216-5224, 2002.
64. Tomko RJ, Jr., Bansal P, and Lazo JS. Airing out an antioxidant role for the tumor suppressor p53. Mol Interv 6: 23-25, 2, 2006.
65. Trinei M, Giorgio M, Cicalese A, Barozzi S, Ventura A, Migliaccio E, Milia E, Padura IM, Raker VA, Maccarana M, Petronilli V, Minucci S, Bernardi P, Lanfrancone L, and Pelicci PG. A p53-p66Shc signalling pathway controls intracellular redox status, levels of oxidation-damaged DNA and oxidative stress-induced apoptosis. Oncogene 21: 3872-3878, 2002. (Pubitemid 34620855)
66. Velez JM, Miriyala S, Nithipongvanitch R, Noel T, Plabplueng CD, Oberley T, Jungsuwadee P, Van Remmen H, Vore M, and St. Clair DK. p53 Regulates oxidative stressmediated retrograde signaling: a novel mechanism for chemotherapy-induced cardiac injury. PLoS One 6: e18005, 2011.
67. Vousden KH and Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2: 594-604, 2002. (Pubitemid 37328926)
68. Weisiger RA and Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 248: 4793-4796, 1973.
69. Wenzel P, Schuhmacher S, Kienhofer J, Muller J, Hortmann M, Oelze M, Schulz E, Treiber N, Kawamoto T, Scharffetter-Kochanek K, Munzel T, Burkle A, Bachschmid MM, and Daiber A. Manganese superoxide dismutase and aldehyde dehydrogenase deficiency increase mitochondrial oxidative stress and aggravate age-dependent vascular dysfunction. Cardiovasc Res 80: 280-289, 2008.
70. Zhao Y, Chaiswing L, Velez JM, Batinic-Haberle I, Colburn NH, Oberley TD, and St. Clair DK. p53 translocation to mitochondria precedes its nuclear translocation and targets mitochondrial oxidative defense protein-manganese superoxide dismutase. Cancer Res 65: 3745-3750, 2005. (Pubitemid 40616352)