A CDK4/6-dependent epigenetic mechanism protects cancer cells from PML-induced senescence

Cancer Research

Volumn 76, Issue 11, 2016, Pages 3252-3264

  Acevedo, Mariana ^a   Vernier, Mathieu ^a   Mignacca, Lian ^a   Lessard, Frederic ^a   Huot, Genevieve ^a   Moiseeva, Olga ^a   Bourdeau, Veronique ^a   Ferbeyre, Gerardo ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; PALBOCICLIB; RNA; TRANSCRIPTION FACTOR E2F; CDK4 PROTEIN, HUMAN; CDK6 PROTEIN, HUMAN; MESSENGER RNA; PML PROTEIN, HUMAN; PROMYELOCYTIC LEUKEMIA PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; CANCER CELL; CARCINOGENICITY; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE TARGETING; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; RNA INTERFERENCE; SENESCENCE; TUMOR CELL; TUMOR GROWTH; XENOGRAFT; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL AGING; CELL CYCLE; CELL PROLIFERATION; DRUG SCREENING; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; MALE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL AGING; CELL CYCLE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE 6; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; PHOSPHORYLATION; PROMYELOCYTIC LEUKEMIA PROTEIN; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84975073463     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2347     Document Type: Article

References (51)

1. Ferbeyre G. PML a target of translocations in APL is a regulator of cellular senescence. Leukemia 2002;16:1918-26.
2. Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW. PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 2000;14:2015-27.
3. Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, Saito S, et al. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 2000;406:207-10.
4. Bischof O, Kirsh O, Pearson M, Itahana K, Pelicci PG, Dejean A. Deconstructing PML-induced premature senescence. EMBO J 2002;21:3358-69.
5. Ablain J, Rice K, Soilihi H, de Reynies A, Minucci S, de The H. Activation of a promyelocytic leukemia-tumor protein 53 axis underlies acute promyelocytic leukemia cure. Nat Med 2014;20:167-74.
6. Trotman LC, Alimonti A, Scaglioni PP, Koutcher JA, Cordon-Cardo C, Pandolfi PP. Identification of a tumour suppressor network opposing nuclear Akt function. Nature 2006;441:523-7.
7. Mallette FA, Goumard S, Gaumont-Leclerc MF, Moiseeva O, Ferbeyre G. Human fibroblasts require the Rb family of tumor suppressors, but not p53, for PML-induced senescence. Oncogene 2004;23:91-9.
8. Vernier M, Bourdeau V, Gaumont-Leclerc MF, Moiseeva O, Begin V, Saad F, et al. Regulation of E2Fs and senescence by PML nuclear bodies. Genes Dev 2011;25:41-50.
9. Bischof O, Nacerddine K, Dejean A. Human papillomavirus oncoprotein E7 targets the promyelocytic leukemia protein and circumvents cellular senescence via the Rb and p53 tumor suppressor pathways. Mol Cell Biol 2005;25:1013-24.
10. Burton DG, Krizhanovsky V. Physiological and pathological consequences of cellular senescence. Cell Mol Life Sci 2014;71:4373-86.
11. Schmitt CA. Senescence, apoptosis and therapy-cutting the lifelines of cancer. Nat Rev Cancer 2003;3:286-95.
12. Lee BY, Han JA, Im JS, Morrone A, Johung K, Goodwin EC, et al. Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 2006;5:187-95.
13. Young AR, Narita M, Ferreira M, Kirschner K, Sadaie M, Darot JF, et al. Autophagy mediates the mitotic senescence transition. Genes Dev 2009;23:798-803.
14. Kang C, Xu Q, Martin TD, Li MZ, Demaria M, Aron L, et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 2015;349:aaa5612.
15. Sherman MY, Meng L, Stampfer M, Gabai VL, Yaglom JA. Oncogenes induce senescence with incomplete growth arrest and suppress the DNA damage response in immortalized cells. Aging Cell 2011;10:949-61.
16. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005;436:720-4.
17. Talluri S, Dick FA. The retinoblastoma protein and PML collaborate to organize heterochromatin and silence E2F-responsive genes during senescence. Cell Cycle 2014;13:641-51.
18. Chicas A, Wang X, Zhang C, McCurrach M, Zhao Z, Mert O, et al. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell 2010;17:376-87.
19. Vernier M, Ferbeyre G. Complete senescence: RB and PML share the task. Cell Cycle 2014;13:696.
20. Narita M, Nunez S, Heard E, Lin AW, Hearn SA, Spector DL, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003;113:703-16.
21. Narita M, Narita M, Krizhanovsky V, Nunez S, Chicas A, Hearn SA, et al. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006;126:503-14.
22. Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AH, Schlegelberger B, et al. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 2005;436:660-5.
23. Di Micco R, Sulli G, Dobreva M, Liontos M, Botrugno OA, Gargiulo G, et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 2011;13:292-302.
24. Deschenes-Simard X, Gaumont-Leclerc MF, Bourdeau V, Lessard F, Moiseeva O, Forest V, et al. Tumor suppressor activity of the ERK/MAPK pathway by promoting selective protein degradation. Genes Dev 2013; 27:900-15.
25. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50.
26. Moiseeva O, Deschenes-Simard X, St-Germain E, Igelmann S, Huot G, Cadar AE, et al. Metformin inhibits the senescence-associated secretory phenotype by interfering with IKK/NF-kappaB activation. Aging Cell 2013;12:489-98.
27. Chao SH, Price DH. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J Biol Chem 2001;276:31793-9.
28. Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, et al. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 2004;3:1427-38.
29. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008;6:2853-68.
30. Missiaglia E, Donadelli M, Palmieri M, Crnogorac-Jurcevic T, Scarpa A, Lemoine NR. Growth delay of human pancreatic cancer cells by methylase inhibitor 5-aza-2′-deoxycytidine treatment is associated with activation of the interferon signalling pathway. Oncogene 2005;24:199-211.
31. Wiesmann F, Veeck J, Galm O, Hartmann A, Esteller M, Knuchel R, et al. Frequent loss of endothelin-3 (EDN3) expression due to epigenetic inactivation in human breast cancer. Breast Cancer Res 2009;11:R34.
32. Bulavin DV, Kovalsky O, Hollander MC, Fornace AJJr. Loss of oncogenic H-ras-induced cell cycle arrest and p38 mitogen-activated protein kinase activation by disruption of Gadd45a. Mol Cell Biol 2003;23:3859-71.
33. Coit P, Jeffries M, Altorok N, Dozmorov MG, Koelsch KA, Wren JD, et al. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naive CD4+ T cells from lupus patients. J Autoimmun 2013;43:78-84.
34. Lin Z, Hegarty JP, Yu W, Cappel JA, Chen X, Faber PW, et al. Identification of disease-associated DNA methylation in B cells from Crohn's disease and ulcerative colitis patients. Dig Dis Sci 2012;57:3145-53.
35. Lavoie G, St-Pierre Y. Phosphorylation of human DNMT1: implication of cyclin-dependent kinases. Biochem Biophys Res Commun 2011;409:187-92.
36. Hervouet E, Lalier L, Debien E, Cheray M, Geairon A, Rogniaux H, et al. Disruption of Dnmt1/PCNA/UHRF1 interactions promotes tumorigenesis from human and mice glial cells. PLoS One 2010;5:e11333.
37. Peng L, Yuan Z, Ling H, Fukasawa K, Robertson K, Olashaw N, et al. SIRT1 deacetylates the DNA methyltransferase 1 (DNMT1) protein and alters its activities. Mol Cell Biol 2011;31:4720-34.
38. Patel N, Black J, Chen X, Marcondes AM, Grady WM, Lawlor ER, et al. DNA methylation and gene expression profiling of ewing sarcoma primary tumors reveal genes that are potential targets of epigenetic inactivation. Sarcoma 2012;2012:498472.
39. Lu F, Tempera I, Lee HT, Dewispelaere K, Lieberman PM. EBNA1 binding and epigenetic regulation of gastrokine tumor suppressor genes in gastric carcinoma cells. Virol J 2014;11:12.
40. Tomii K, Tsukuda K, Toyooka S, Dote H, Hanafusa T, Asano H, et al. Aberrant promoter methylation of insulin-like growth factor binding protein-3 gene in human cancers. Int J Cancer 2007;120:566-73.
41. Chanudet E, Huang Y, Ichimura K, Dong G, Hamoudi RA, Radford J, et al. A20 is targeted by promoter methylation, deletion and inactivating mutation in MALT lymphoma. Leukemia 2010;24:483-7.
42. Dubovsky JA, McNeel DG. Inducible expression of a prostate cancer-testis antigen, SSX-2, following treatment with a DNA methylation inhibitor. Prostate 2007;67:1781-90.
43. Wang W, Huper G, Guo Y, Murphy SK, Olson JAJr., Marks JR. Analysis of methylation-sensitive transcriptome identifies GADD45a as a frequently methylated gene in breast cancer. Oncogene 2005;24:2705-14.
44. Moiseeva O, Mallette FA, Mukhopadhyay UK, Moores A, Ferbeyre G. DNA Damage Signaling and p53-dependent Senescence after Prolonged beta-Interferon Stimulation. Mol Biol Cell 2006;17:1583-92.
45. Campanero MR, Armstrong MI, Flemington EK. CpG methylation as a mechanism for the regulation of E2F activity. Proc Natl Acad Sci U S A 2000;97:6481-6.
46. Rhee I, Jair KW, Yen RW, Lengauer C, Herman JG, Kinzler KW, et al. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature 2000;404:1003-7.
47. Cruickshanks HA, McBryan T, Nelson DM, Vanderkraats ND, Shah PP, van Tuyn J, et al. Senescent cells harbour features of the cancer epigenome. Nat Cell Biol 2013;15:1495-506.
48. Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, et al. Autophagy mediates degradation of nuclear lamina. Nature 2015;527:105-9.
49. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev 2009;10:805-11.
50. Sen GL, Reuter JA, Webster DE, Zhu L, Khavari PA. DNMT1 maintains progenitor function in self-renewing somatic tissue. Nature 2010;463:563-7.
51. Law ME, Corsino PE, Narayan S, Law BK. Cyclin-dependent kinase inhibitors as anticancer therapeutics. Mol Pharmacol 2015;88:846-52.