ROS-dependent activation of JNK converts p53 into an efficient inhibitor of oncogenes leading to robust apoptosis

Cell Death and Differentiation

Volumn 21, Issue 4, 2014, Pages 612-623

  Shi, Y ^a   Nikulenkov, F ^a   Zawacka Pankau, J ^a,b   Li, H ^a   Gabdoulline, R ^c,d   Xu, J ^a   Eriksson, S ^a   Hedstrom E ^a   Issaeva, N ^a,e   Kel, A ^c,f   Arner E S J ^a   Selivanova, G ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF GDA SK   (Poland)

^c GeneXplain GmbH   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

Author keywords

inhibition of oncogenes; JNK; p53; ROS; TrxR; Wip1

Indexed keywords

FAS ANTIGEN; GROWTH DIFFERENTIATION FACTOR 15; HISTONE H2AX; INITIATION FACTOR 4E; MESSENGER RNA; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN MCL 1; PROTEIN MDMX; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; THIOREDOXIN REDUCTASE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL DEATH; CELL SURVIVAL; DNA DAMAGE; DNA STRAND BREAKAGE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE CLUSTER; GENE EXPRESSION; HISTONE PHOSPHORYLATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; SENESCENCE; TRANSACTIVATION;

APOPTOSIS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; HCT116 CELLS; HUMANS; HYDROGEN PEROXIDE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MCF-7 CELLS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NUCLEAR PROTEINS; OXIDANTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEIN PHOSPHATASES; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; THIOREDOXIN REDUCTASE 1; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84903366271     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.186     Document Type: Article

References (46)

1. Selivanova G. Therapeutic targeting of p53 by small molecules. Semin Cancer Biol 2010; 20: 46-56.
2. Junttila MR, Karnezis AN, Garcia D, Madriles F, Kortlever RM, Rostker F et al. Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 2010; 468: 567-571.
3. Feldser DM, Kostova KK, Winslow MM, Taylor SE, Cashman C, Whittaker CA et al. Stage-specific sensitivity to p53 restoration during lung cancer progression. Nature 2010; 468: 572-575.
4. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445: 656-660.
5. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009; 137: 413-431.
6. Jackson JG, Pant V, Li Q, Chang LL, Quintas-Cardama A, Garza D et al. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell 2012; 21: 793-806.
7. Nikulenkov F, Spinnler C, Li H, Tonelli C, Shi Y, Turunen M et al. Insights into p53 transcriptional function via genome-wide chromatin occupancy and gene expression analysis. Cell Death Differ 2012; 19: 1992-2002.
8. Haigis KM, Sweet-Cordero A. New insights into oncogenic stress. Nat Genet 2011; 43: 177-178.
9. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009; 8: 579-591.
10. Arner ES, Holmgren A. The thioredoxin system in cancer. Semin Cancer Biol 2006; 16: 420-426.
11. Hatfield DL, Yoo MH, Carlson BA, Gladyshev VN. Selenoproteins that function in cancer prevention and promotion. Biochim Biophys Acta 2009; 1790: 1541-1545.
12. Urig S, Becker K. On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin Cancer Biol 2006; 16: 452-465.
13. Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer 2009; 9: 862-873.
14. Enge M, Bao W, Hedstrom E, Jackson SP, Moumen A, Selivanova G. MDM2-dependent downregulation of p21 and hnRNP K provides a switch between apoptosis and growth arrest induced by pharmacologically activated p53. Cancer Cell 2009; 15: 171-183.
15. Grinkevich VV, Nikulenkov F, Shi Y, Enge M, Bao W, Maljukova A et al. Ablation of key oncogenic pathways by RITA-reactivated p53 is required for efficient apoptosis. Cancer Cell 2009; 15: 441-453.
16. Ahmed A, Yang J, Maya-Mendoza A, Jackson DA, Ashcroft M. Pharmacological activation of a novel p53-dependent S-phase checkpoint involving CHK-1. Cell Death Dis 2011; 2: e160.
17. Secchiero P, Bosco R, Celeghini C, Zauli G. Recent advances in the therapeutic perspectives of Nutlin-3. Curr Pharm Des 2011; 17: 569-577.
18. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999; 285: 1733-1737.
19. Nieves-Neira W, Rivera MI, Kohlhagen G, Hursey ML, Pourquier P, Sausville EA et al. DNA protein cross-links produced by NSC 652287, a novel thiophene derivative active against human renal cancer cells. Mol Pharmacol 1999; 56: 478-484.
20. Sedelnikova OA, Redon CE, Dickey JS, Nakamura AJ, Georgakilas AG, Bonner WM. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res 2010; 704: 152-159.
21. Hedstrom E, Eriksson S, Zawacka-Pankau J, Arner ES, Selivanova G. p53-dependent inhibition of TrxR1 contributes to the tumor-specific induction of apoptosis by RITA. Cell Cycle 2009; 8: 3576-3583.
22. Anestal K, Arner ES. Rapid induction of cell death by selenium-compromised thioredoxin reductase 1 but not by the fully active enzyme containing selenocysteine. J Biol Chem 2003; 278: 15966-15972.
23. Anestal K, Prast-Nielsen S, Cenas N, Arner ES. Cell death by SecTRAPs: thioredoxin reductase as a prooxidant killer of cells. PLoS ONE 2008; 3: e1846.
24. He X, Andersson G, Lindgren U, Li Y. Resveratrol prevents RANKL-induced osteoclast differentiation of murine osteoclast progenitor RAW 264.7 cells through inhibition of ROS production. Biochem Biophys Res Commun 2010; 401: 356-362.
25. Floriano-Sanchez E, Villanueva C, Medina-Campos ON, Rocha D, Sanchez-Gonzalez DJ, Cardenas-Rodriguez N et al. Nordihydroguaiaretic acid is a potent in vitro scavenger of peroxynitrite, singlet oxygen, hydroxyl radical, superoxide anion and hypochlorous acid and prevents in vivo ozone-induced tyrosine nitration in lungs. Free Radic Res 2006; 40: 523-533.
26. Marzano C, Gandin V, Folda A, Scutari G, Bindoli A, Rigobello MP. Inhibition of thioredoxin reductase by auranofin induces apoptosis in cisplatin-resistant human ovarian cancer cells. Free Radic Biol Med 2007; 42: 872-881.
27. Bragado P, Armesilla A, Silva A, Porras A. Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 2007; 12: 1733- 1742.
28. Prast-Nielsen S, Cebula M, Pader I, Arner ES. Noble metal targeting of thioredoxin reductase-covalent complexes with thioredoxin and thioredoxin-related protein of 14 kDa triggered by cisplatin. Free Radic Biol Med 2010; 49: 1765-1778.
29. Seyfried J, Wullner U. Inhibition of thioredoxin reductase induces apoptosis in neuronal cell lines: role of glutathione and the MKK4/JNK pathway. Biochem Biophys Res Commun 2007; 359: 759-764.
30. de Feraudy S, Revet I, Bezrookove V, Feeney L, Cleaver JE. A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci USA 2010; 107: 6870-6875.
31. Zawacka-Pankau J, Grinkevich VV, Hunten S, Nikulenkov F, Gluch A, Li H et al. Inhibition of glycolytic enzymes mediated by pharmacologically activated p53: targeting Warburg effect to fight cancer. J Biol Chem 2011; 286: 41600-41615.
32. Le Guezennec X, Bulavin DV. WIP1 phosphatase at the crossroads of cancer and aging. Trends Biochem Sci 2010; 35: 109-114.
33. Macurek L, Lindqvist A, Voets O, Kool J, Vos HR, Medema RH. Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene 2010; 29: 2281-2291.
34. Moon SH, Lin L, Zhang X, Nguyen TA, Darlington Y, Waldman AS et al. Wild-type p53-induced phosphatase 1 dephosphorylates histone variant gamma-H2AX and suppresses DNA double strand break repair. J Biol Chem 2010; 285: 12935-12947.
35. Spinnler C, Hedstrom E, Li H, de Lange J, Nikulenkov F, Teunisse AF et al. Abrogation of Wip1 expression by RITA-activated p53 potentiates apoptosis induction via activation of ATM and inhibition of HdmX. Cell Death Differ 2011; 18: 1736-1745.
36. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9: 402-412.
37. Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 2009; 66: 1326-1336.
38. Gustin JP, Cosgrove DP, Park BH. The PIK3CA gene as a mutated target for cancer therapy. Curr Cancer Drug Targets 2008; 8: 733-740.
39. Blagden SP, Willis AE. The biological and therapeutic relevance of mRNA translation in cancer. Nat Rev Clin Oncol 2011; 8: 280-291.
40. Marine JC, Dyer MA, Jochemsen AG. MDMX: from bench to bedside. J Cell Sci 2007; 120(Pt 3): 371-378.
41. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434: 864-870.
42. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434: 907-913.
43. Schramek D, Kotsinas A, Meixner A, Wada T, Elling U, Pospisilik JA et al. The stress kinase MKK7 couples oncogenic stress to p53 stability and tumor suppression. Nat Genet 2011; 43: 212-219.
44. Carew JS, Nawrocki ST, Reddy VK, Bush D, Rehg JE, Goodwin A et al. The novel polyamine analogue CGC-11093 enhances the antimyeloma activity of bortezomib. Cancer Res 2008; 68: 4783-4790.
45. Imreh G, Norberg HV, Imreh S, Zhivotovsky B. Chromosomal breaks during mitotic catastrophe trigger gammaH2AX-ATM-p53-mediated apoptosis. J Cell Sci 2011; 124(Pt 17): 2951-2963.
46. Qin ZS. Clustering microarray gene expression data using weighted Chinese restaurant process. Bioinformatics 2006; 22: 1988-1997.