p16INK4a deficiency promotes DNA hyper-replication and genetic instability in melanocytes

Pigment Cell and Melanoma Research

Volumn 26, Issue 2, 2013, Pages 236-246

  Fung, Carina ^a   Pupo, Gulietta M ^a   Scolyer, Richard A ^b,c,d   Kefford, Richard F ^a,b   Rizos, Helen ^a  

^a WESTMEAD HOSPITAL   (Australia)

^b MELANOMA INSTITUTE AUSTRALIA   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

DNA damage; Melanoma; P16INK4a; P53

Indexed keywords

CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 2A; LENTIVIRUS VECTOR; SHORT HAIRPIN RNA;

ARTICLE; CELL PROLIFERATION; DNA DAMAGE; DNA REPLICATION; GENE INACTIVATION; GENOMIC INSTABILITY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MELANOCYTE; MELANOMA; NEVUS; NUCLEOTIDE SEQUENCE; ONCOGENE; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA EXTRACTION; TUMOR SUPPRESSOR GENE;

CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; DNA REPLICATION; GENOMIC INSTABILITY; HEK293 CELLS; HISTONES; HUMANS; MELANOCYTES; NEVUS; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84874394983     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12062     Document Type: Article

References (48)

1. Alcorta, D.A., Xiong, Y., Phelps, D., Hannon, G., Beach, D., and Barrett, J.C. (1996). Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl Acad. Sci. U S A 93, 13742-13747.
2. Bartkova, J., Horejsi, Z., Koed, K. et al. (2005). DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870.
3. Bartkova, J., Rezaei, N., Liontos, M. et al. (2006). Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637.
4. Beck, H., Nahse, V., Larsen, M.S., Groth, P., Clancy, T., Lees, M., Jorgensen, M., Helleday, T., Syljuasen, R.G., and Sorensen, C.S. (2010). Regulators of cyclin-dependent kinases are crucial for maintaining genome integrity in S phase. J. Cell Biol. 188, 629-638.
5. Blomberg, I., and Hoffmann, I. (1999). Ectopic expression of Cdc25A accelerates the G(1)/S transition and leads to premature activation of cyclin E- and cyclin A-dependent kinases. Mol. Cell Biol. 19, 6183-6194.
6. Bond, J., Jones, C., Haughton, M., Demicco, C., Kipling, D., and Wynford-Thomas, D. (2004). Direct evidence from siRNA-directed "knock down" that p16(INK4a) is required for human fibroblast senescence and for limiting ras-induced epithelial cell proliferation. Exp. Cell Res. 292, 151-156.
7. Bracken, A.P., Ciro, M., Cocito, A., and Helin, K. (2004). E2F target genes: unraveling the biology. Trends Biochem. Sci. 29, 409-417.
8. Braden, W.A., Mcclendon, A.K., and Knudsen, E.S. (2008). Cyclin-dependent kinase 4/6 activity is a critical determinant of pre-replication complex assembly. Oncogene 27, 7083-7093.
9. Brenner, A.J., Stampfer, M.R., and Aldaz, C.M. (1998). Increased p16 expression with first senescence arrest in human mammary epithelial cells and extended growth capacity with p16 inactivation. Oncogene 17, 199-205.
10. Brookes, S., Rowe, J., Ruas, M. et al. (2002). INK4a-deficient human diploid fibroblasts are resistant to RAS-induced senescence. EMBO J. 21, 2936-2945.
11. Brookes, S., Rowe, J., Gutierrez Del Arroyo, A., Bond, J., and Peters, G. (2004). Contribution of p16(INK4a) to replicative senescence of human fibroblasts. Exp. Cell Res. 298, 549-559.
12. Cerqueira, A., Santamaria, D., Martinez-Pastor, B., Cuadrado, M., Fernandez-Capetillo, O., and Barbacid, M. (2009). Overall Cdk activity modulates the DNA damage response in mammalian cells. J. Cell Biol. 187, 773-780.
13. Curtin, J.A., Fridlyand, J., Kageshita, T. et al. (2005). Distinct sets of genetic alterations in melanoma. N. Engl. J. Med. 353, 2135-2147.
14. Denoyelle, C., Abou-Rjaily, G., Bezrookove, V. et al. (2006). Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat. Cell Biol. 8, 1053-1063.
15. Di Micco, R., Fumagalli, M., Cicalese, A. et al. (2006). Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-642.
16. Diffley, J.F., and Labib, K. (2002). The chromosome replication cycle. J. Cell Sci. 115, 869-872.
17. Forbes, S., Clements, J., Dawson, E. et al. (2006). COSMIC 2005. Br. J. Cancer 94, 318-322.
18. Fry, D.W., Harvey, P.J., Keller, P.R. et al. (2004). Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol. Cancer Ther. 3, 1427-1438.
19. Gladden, A.B., and Diehl, J.A. (2003). The cyclin D1-dependent kinase associates with the pre-replication complex and modulates RB.MCM7 binding. J. Biol. Chem. 278, 9754-9760.
20. Goldstein, A.M., Chan, M., Harland, M. et al. (2006). High-risk melanoma susceptibility genes and pancreatic cancer, neural system tumors, and uveal melanoma across GenoMEL. Cancer Res. 66, 9818-9828.
21. Gorgoulis, V.G., Vassiliou, L.V., Karakaidos, P. et al. (2005). Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913.
22. Haferkamp, S., Scurr, L.L., Becker, T.M., Frausto, M., Kefford, R.F., and Rizos, H. (2009). Oncogene-induced senescence does not require the p16(INK4a) or p14ARF melanoma tumor suppressors. J. Invest. Dermatol. 129, 1983-1991.
23. Halazonetis, T.D., Gorgoulis, V.G., and Bartek, J. (2008). An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355.
24. Huot, T.J., Rowe, J., Harland, M. et al. (2002). Biallelic mutations in p16(INK4a) confer resistance to Ras- and Ets-induced senescence in human diploid fibroblasts. Mol. Cell. Biol. 22, 8135-8143.
25. Jones, R., Ruas, M., Gregory, F., Moulin, S., Delia, D., Manoukian, S., Rowe, J., Brookes, S., and Peters, G. (2007). A CDKN2A mutation in familial melanoma that abrogates binding of p16INK4a to CDK4 but not CDK6. Cancer Res. 67, 9134-9141.
26. Kishimoto, H., Hamada, K., Saunders, M., Backman, S., Sasaki, T., Nakano, T., Mak, T.W., and Suzuki, A. (2003). Physiological functions of Pten in mouse tissues. Cell Struct. Funct. 28, 11-21.
27. Lam, M.H., and Rosen, J.M. (2004). Chk1 versus Cdc25: checking one's levels of cellular proliferation. Cell Cycle 3, 1355-1357.
28. Lambert, S., and Carr, A.M. (2005). Checkpoint responses to replication fork barriers. Biochimie 87, 591-602.
29. Mailand, N., and Diffley, J.F. (2005). CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 122, 915-926.
30. Mayo, L.D., Dixon, J.E., Durden, D.L., Tonks, N.K., and Donner, D.B. (2002). PTEN protects p53 from Mdm2 and sensitizes cancer cells to chemotherapy. J. Biol. Chem. 277, 5484-5489.
31. Michaloglou, C., Vredeveld, L.C., Soengas, M.S., Denoyelle, C., Kuilman, T., Van Der Horst, C.M., Majoor, D.M., Shay, J.W., Mooi, W.J., and Peeper, D.S. (2005). BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436, 720-724.
32. Planas-Silva, M.D., and Weinberg, R.A. (1997). Estrogen-dependent cyclin E-cdk2 activation through p21 redistribution. Mol. Cell. Biol. 17, 4059-4069.
33. Puc, J., Keniry, M., Li, H.S. et al. (2005). Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 7, 193-204.
34. Raderschall, E., Golub, E.I., and Haaf, T. (1999). Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl Acad. Sci. USA. 96, 1921-1926.
35. Sarkisian, C.J., Keister, B.A., Stairs, D.B., Boxer, R.B., Moody, S.E., and Chodosh, L.A. (2007). Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat. Cell Biol. 9, 493-505.
36. Scurr, L.L., Pupo, G.M., Becker, T.M. et al. (2010). IGFBP7 is not required for B-RAF-induced melanocyte senescence. Cell 141, 717-727.
37. Serrano, M., Hannon, G.J., and Beach, D. (1993). A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366, 704-707.
38. Serrano, M., Lin, A.W., Mccurrach, M.E., Beach, D., and Lowe, S.W. (1997). Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 85, 593-602.
39. Spruck, C.H., Won, K.A., and Reed, S.I. (1999). Deregulated cyclin E induces chromosome instability. Nature 401, 297-300.
40. Sviderskaya, E.V., Gray-Schopfer, V.C., Hill, S.P. et al. (2003). p16/Cyclin-dependent kinase inhibitor 2A deficiency in human melanocyte senescence, apoptosis, and immortalization: possible implications for melanoma progression. J. Natl Cancer Inst. 95, 723-732.
41. Tort, F., Bartkova, J., Sehested, M., Orntoft, T., Lukas, J., and Bartek, J. (2006). Retinoblastoma pathway defects show differential ability to activate the constitutive DNA damage response in human tumorigenesis. Cancer Res. 66, 10258-10263.
42. Tran, S.L., Haferkamp, S., Scurr, L.L., Gowrishankar, K., Becker, T.M., Desilva, C., Thompson, J.F., Scolyer, R.A., Kefford, R.F., and Rizos, H. (2012). Absence of distinguishing senescence traits in human melanocytic nevi. J. Invest. Dermatol. 19, 126.
43. Vafa, O., Wade, M., Kern, S., Beeche, M., Pandita, T.K., Hampton, G.M., and Wahl, G.M. (2002). c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol. Cell 9, 1031-1044.
44. Vassilev, L.T., Vu, B.T., Graves, B. et al. (2004). In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303, 844-848.
45. Voorhoeve, P.M., and Agami, R. (2003). The tumor-suppressive functions of the human INK4A locus. Cancer Cell 4, 311-319.
46. Voorhoeve, P.M., and Agami, R. (2004). Unraveling human tumor suppressor pathways: a tale of the INK4A locus. Cell Cycle 3, 616-620.
47. Wolfel, T., Hauer, M., Schneider, J., Serrano, M., Wolfel, C., Klehmannhieb, E., Deplaen, E., Hankeln, T., Zumbuschenfelde, K.H.M., and Beach, D. (1995). A p16(INK4a)-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269, 1281-1284.
48. Zuo, L., Weger, J., Yang, Q., Goldstein, A.M., Tucker, M.A., Walker, G.J., Hayward, N., and Dracopoli, N.C. (1996). Germline mutations in the p16ink4a binding domain of CDK4 in familial melanoma. Nat. Genet. 12, 97-99.