Activation of forkhead box O transcription factors by oncogenic BRAF promotes p21cip1-dependent senescence

Cancer Research

Volumn 70, Issue 21, 2010, Pages 8526-8536

  De Keizer, Peter L J ^a,d   Packer, Leisl M ^c   Szypowska, Anna A ^a   Riedl Polderman, Paulien E ^a   Van Den Broek, Niels J F ^a   De Bruin, Alain ^b   Dansen, Tobias B ^a   Marais, Richard ^c   Brenkman, Arjan B ^a   Burgering, Boudewijn M T ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN P16; PROTEIN P27; REACTIVE OXYGEN METABOLITE; SERINE; STRESS ACTIVATED PROTEIN KINASE; THREONINE; TRANSCRIPTION FACTOR FOXO;

ARTICLE; CANCER INHIBITION; CELL ACTIVATION; CELL AGING; CELL CULTURE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOCYTE; MELANOMA CELL; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL AGING; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HUMANS; IN SITU NICK-END LABELING; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MELANOCYTES; MELANOMA; MICE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS B-RAF; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78449289216     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1563     Document Type: Article

References (52)

1. Garnett MJ, Marais R. Guilty as charged: B-RAF is a human oncogene. Cancer Cell 2004;6:313-9.
2. Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-54.
3. Wellbrock C, Karasarides M, Marais R. The RAF proteins take centre stage. Nat Rev Mol Cell Biol 2004;5:875-85.
4. Michaloglou C, Vredeveld LC, Soengas MS, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005;436:720-4.
5. Gray-Schopfer VC, Cheong SC, Chong H, et al. Cellular senescence in naevi and immortalisation in melanoma: a role for p16? Br J Cancer 2006;95:496-505.
6. Chudnovsky Y, Adams AE, Robbins PB, Lin Q, Khavari PA. Use of human tissue to assess the oncogenic activity of melanoma-associated mutations. Nat Genet 2005;37:745-9.
7. Quereda V, Martinalbo J, Dubus P, Carnero A, Malumbres M. Genetic cooperation between p21Cip1 and INK4 inhibitors in cellular senescence and tumor suppression. Oncogene 2007;26:7665-74.
8. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 1997;17:5598-611.
9. Zhu J, Woods D, McMahon M, Bishop JM. Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev 1998;12:2997-3007.
10. Finkel T. Redox-dependent signal transduction. FEBS Lett 2000;476:52-4.
11. Stone JR, Yang S. Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal 2006;8:243-70.
12. 1 arrest but not cell replication. Biochem J 1998;332:43-50.
13. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956;11:298-300.
14. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 2007;8:722-8.
15. Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 1993;366:461-4.
16. Kops GJ, de Ruiter ND, de Vries-Smits AM, Powell DR, Bos JL, Burgering BM. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 1999;398:630-4.
17. Brunet A, Bonni A, Zigmond MJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-68.
18. Paik JH, Kollipara R, Chu G, et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007;128:309-23.
19. Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 2000;404:782-7.
20. Brunet A, Sweeney LB, Sturgill JF, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004;303:2011-5.
21. Essers MA, Weijzen S, Vries-Smits AM, et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 2004;23:4802-12.
22. van der Horst A, Burgering BM. Stressing the role of FoxO proteins in life span and disease. Nat Rev Mol Cell Biol 2007;8:440-50.
23. Dansen TB, Smits LM, van Triest MH, et al. Redox-sensitive cysteines bridge p300/CBP-mediated acetylation and FoxO4 activity. Nat Chem Biol 2009;5:664-72.
24. Kops GJ, Dansen TB, Polderman PE, et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002;419:316-21.
25. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002;295:2450-2.
26. Willcox BJ, Donlon TA, He Q, et al. FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A 2008;105:13987-92.
27. Brenkman AB, de Keizer PL, van den Broek NJ, et al. The peptidyl-isomerase Pin1 regulates p27kip1 expression through inhibition of Forkhead box O tumor suppressors. Cancer Res 2008;68:7597-605.
28. el-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993;75:817-25.
29. Duursma A, Agami R. p53-dependent regulation of Cdc6 protein stability controls cellular proliferation. Mol Cell Biol 2005;25:6937-47.
30. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995;92:9363-7.
31. Collado M, Serrano M. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 2006;6:472-6.
32. Denoyelle C, Abou-Rjaily G, Bezrookove V, et al. Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat Cell Biol 2006;8:1053-63.
33. Leikam C, Hufnagel A, Schartl M, Meierjohann S. Oncogene activation in melanocytes links reactive oxygen to multinucleated phenotype and senescence. Oncogene 2008;27:7070-82.
34. Lee AC, Fenster BE, Ito H, et al. Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J Biol Chem 1999;274:7936-40.
35. Vafa O, Wade M, Kern S, et al. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 2002;9:1031-44.
36. Gray-Schopfer VC, Karasarides M, Hayward R, Marais R. Tumor necrosis factor-α blocks apoptosis in melanoma cells when BRAF signaling is inhibited. Cancer Res 2007;67:122-9.
37. Wellbrock C, Rana S, Paterson H, Pickersgill H, Brummelkamp T, Marais R. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 2008;3:e2734.
38. Wellbrock C, Marais R. Elevated expression of MITF counteracts BRAF-stimulated melanocyte and melanoma cell proliferation. J Cell Biol 2005;170:703-8.
39. Dhomen N, Reis-Filho JS, da Rocha DS, et al. Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009;15:294-303.
40. Dankort D, Curley DP, Cartlidge RA, et al. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009;41:544-52.
41. Ackermann J, Frutschi M, Kaloulis K, McKee T, Trumpp A, Beermann F. Metastasizing melanoma formation caused by expression of activated N-RasQ61K on an INK4a-deficient background. Cancer Res 2005;65:4005-11.
42. Courtois-Cox S, Genther Williams SM, Reczek EE, et al. A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 2006;10:459-72.
43. Ha L, Merlino G, Sviderskaya EV. Melanomagenesis: overcoming the barrier of melanocyte senescence. Cell Cycle 2008;7:1944-8.
44. Gruis NA, van der Velden PA, Sandkuijl LA, et al. Homozygotes for CDKN2 (p16) germline mutation in Dutch familial melanoma kindreds. Nat Genet 1995;10:351-3.
45. Ranade K, Hussussian CJ, Sikorski RS, et al. Mutations associated with familial melanoma impair p16INK4 function. Nat Genet 1995;10:114-6.
46. Li W, Sanki A, Karim RZ, et al. The role of cell cycle regulatory proteins in the pathogenesis of melanoma. Pathology 2006;38:287-301.
47. Pollock PM, Harper UL, Hansen KS, et al. High frequency of BRAF mutations in nevi. Nat Genet 2003;33:19-20.
48. Kuilman T, Michaloglou C, Vredeveld LC, et al. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008;133:1019-31.
49. Nogueira V, Park Y, Chen CC, et al. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 2008;14:458-70.
50. Hedrick SM. The cunning little vixen: Foxo and the cycle of life and death. Nat Immunol 2009;10:1057-63.
51. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007;8:729-40.
52. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell 2007;130:223-33.