Ink4a/Arf deficiency promotes ultraviolet radiation-induced melanomagenesis

Cancer Research

Volumn 62, Issue 22, 2002, Pages 6724-6730

  Recio, Juan A ^a   Noonan, Frances P ^b   Takayama, Hisashi ^a,g   Anver, Miriam R ^c   Duray, Paul ^a   Rush, Walter L ^d   Lindner, Gerd ^e   De Fabo, Edward C ^b   DePinho, Ronald A ^f   Merlino, Glenn ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c SAIC FREDERICK INC   (United States)

^d ARMED FORCES INSTITUTE OF PATHOLOGY   (United States)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^f HARVARD MEDICAL SCHOOL   (United States)

^g Fujioka General Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SCATTER FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARF GENE; ARTICLE; CANCER INHIBITION; CANCER RISK; CARCINOGENESIS; CONTROLLED STUDY; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; INK4A GENE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RADIATION DOSE; RISK FACTOR; SKIN CANCER; SUNBURN; TRANSGENE; TUMOR SUPPRESSOR GENE; ULTRAVIOLET RADIATION;

ANIMALS; COCARCINOGENESIS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DISEASE MODELS, ANIMAL; HEPATOCYTE GROWTH FACTOR; HUMANS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ULTRAVIOLET RAYS;

EID: 0037112371     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Howe, H. L., Wingo, P. A., Thun, M. J., Ries, L. A., Rosenberg, H. M., Feigal, E. G., and Edwards, B. K. Annual report to the nation on the status of cancer (1973 Through 1998). Featuring cancers with recent increasing trends. J. Natl. Cancer Inst. (Bethesda), 93: 824-842, 2001
2. Jemal, A., Devesa, S. S., Hartge, P., and Tucker, M. A. Recent trends in cutaneous melanoma incidence among whites in the United States. J. Natl. Cancer Inst. (Bethesda), 93: 678-683, 2001
3. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Solar and Ultraviolet Radiation, Vol. 55. Lyon, France: IARC, 1992
4. Chin, L., Merlino, G., and DePinho, R. A. Malignant melanoma: Modern black plague and genetic black box. Genes Dev., 12: 3467-3481, 1998
5. Herlyn, M. Molecular and cellular biology of melanoma, pp. 1-102, Austin, TX: R. G. Landes Co., 1993
6. Pollock, P. M., and Trent, J. M. The genetics of cutaneous melanoma. Clin. Lab. Med., 20: 667-690, 2000
7. Quelle, D. E., Zindy, F., Ashmun, R. A., and Sherr, C. J. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell, 83: 993-1000, 1995
8. Chin, L., Pomerantz, J., and DePinho, R. A. The INK4a/ARF tumor suppressor: One gene-two products-two pathways. Trends Biochem. Sci., 23: 291-296, 1998
9. Gonzalgo, M. L., Bender, C. M., You, E. H., Glendening, J. M., Flores, J. F., Walker, G. J., Hayward, N. K., Jones, P. A., and Fountain, J. W. Low frequency of p16/CDKN2A methylation in sporadic melanoma: Comparative approaches for methylation analysis of primary tumors. Cancer Res., 57: 5336-5347, 1997
10. Funk, J. O., Schiller, P. I., Barrett, M. T., Wong, D. J., Kind, P., and Sander, C. A. p16INK4a expression is frequently decreased and associated with 9p21 loss of heterozygosity in sporadic melanoma. J. Cutan. Pathol., 25: 291-296, 1998
11. INK4a binding domain of CDK4 in familial melanoma. Nat. Genet., 12: 97-99, 1996
12. Serrano, M., Lee, H., Chin, L., Cordon-Cardo, C., Beach, D., and DePinho, R. A. Role of the INK4a locus in tumor suppression and cell mortality. Cell, 85: 27-37, 1996
13. Chin, L., Pomerantz, J., Polsky, D., Jacobson, M., Cohen, C., Cordon-Cardo, C., Horner, J. W., and DePinho, R. A. Cooperative effects of INK4a and ras in melanoma susceptibility in vivo. Genes Dev., 11: 2822-2834, 1997
14. Sharpless, N. E., Bardeesy, N., Lee, K. H., Carrasco, D., Castrillon, D. H., Aguirre, A. J., Wu, E. A., Horner, J. W., and DePinho, R. A. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature (Lond.), 413: 86-91, 2001
15. Krimpenfort, P., Quon, K. C., Mooi, W. J., Loonstra, A., and Berns, A. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature (Lond.), 413: 83-86, 2001
16. Sotillo, R., Garcia, J. F., Ortega, S., Martin, J., Dubus, P., Barbacid, M., and Malumbres M. Invasive melanoma in Cdk4-targeted mice. Proc. Natl. Acad. Sci. USA, 98: 13312-13317, 2001
17. Rane, S. G., Cosenza, S. C., Mettus, R. V., and Reddy, E. P. Germ line transmission of the Cdk4(R24C) mutation facilitates tumorigenesis and escape from cellular senescence. Mol. Cell. Biol., 22: 644-656, 2002
18. Bennett, D. C. Genetics, development, and malignancy of melanocytes. Int. Rev. Cytol., 146: 191-260, 1993
19. Shih, I. M., and Herlyn, M. Autocrine and paracrine roles for growth factors in melanoma. In Vivo, 8: 113-123, 1994
20. Halaban, R. Growth factors and melanomas. Semin. Oncol., 23: 673-681, 1996
21. Jeffers, M., Rong, S., and Vande Woude, G. F. Hepatocyte growth factor/scatter factor-Met signaling in tumorigenicity and invasion/metastasis. J. Mol. Med., 74: 505-513, 1996
22. Matsumoto, K., and Nakamura, T. Emerging multipotent aspects of hepatocyte growth factor. J. Biochem. (Tokyo), 119: 591-600, 1996
23. Schmidt, C., Bladt, F., Goedecke, S., Brinkman, V., Zschiesche, W., Sharpe, M., Gherardi, E., and Birchmeier, C. Scatter factor/hepatocyte growth factor is essential for liver development. Nature (Lond.), 373: 699-702, 1995
24. Uehara, Y., Minowa, O., Mori, C., Shiota, K., Kuno, J., Noda, T., and Kitamura, N. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature (Lond.), 373: 702-705, 1995
25. Bladt, F., Rlethmacher, D., Isenmann, S., Aguzzi, A., and Birchmeier, C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature (Lond.), 376: 768-771, 1995
26. Rosen, E. M., Lamszus, K., Laterra, J., Polverini, P. J., Rubin, J. S., and Goldberg, I. D. HGF/SF in angiogenesis. Ciba Found. Symp., 212: 215-226, 1997
27. Comoglio, P. M., and Boccaccio, C. Scatter factors and invasive growth. Semin. Cancer Biol., 11: 153-165, 2001
28. Li, G., Schaider, H., Satyamoorthy, K., Hanakawa, Y., Hashimoto, K., and Herlyn, M. Down-regulation of E-cadherin and desmoglein 1 by autocrine hepatocyte growth factor during melanoma development. Oncogene, 20: 8125-8135, 2001
29. Wiltshire, R. N., Duray, P., Bittner, M. L., Visakorpi, T., Meltzer, P. S., Tuthill, R. J., Liotta, L. A., and Trent, J. M. Direct visualization of the clonal progression of primary cutaneous melanoma: Application of tissue microdissection and comparative genomic hybridization. Cancer Res., 55: 3954-3957, 1995
30. Bastian, B. C., LeBoit, P. E., Hamm, H., Brocker, E. B., and Pinkel, D. Chromosomal gains and losses in primary cutaneous melanomas detected by comparative genomic hybridization. Cancer Res., 58: 2170-2175, 1998
31. Natali, P. G., Nicotra, M. R., Di Renzo, M. F., Prat, M., Bigotti, A., Cavaliere, R., and Comoglio, P. M. Expression of the c-Met/HGF receptor in human melanocytic neoplasms: Demonstration of the relationship to malignant melanoma tumour progression. Br. J. Cancer, 68: 746-750, 1993
32. Hendrix, M. J., Seftor, E. A., Seftor, R. E., Kirschmann, D. A., Gardner, L. M., Boldt, H. C., Meyer, M., Pe’er, J., and Folberg, R. Regulation of uveal melanoma interconverted phenotype by hepatocyte growth factor/scatter factor (HGF/SF). Am. J. Pathol., 152: 855-863, 1998
33. Takayama, H., LaRochelle, W. J., Sharp, R., Otsuka, T., Kriebel, P., Anver, M., Aaronson, S. A., and Merlino, G. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc. Natl. Acad. Sci. USA, 94: 701-706, 1997
34. Otsuka, T., Takayama, H., Sharp, R., Celli, G., LaRochelle, W. J., Bottaro, D. P., Ellmore, N., Vieira, W., Owens, J. W., Anver, M., and Merlino, G. c-Met autocrine activation induces development of malignant melanoma and acquisition of the metastatic phenotype. Cancer Res., 58: 5157-5167, 1998
35. Armstrong, B. K., Kricker, A., and English, D. R. Sun exposure and skin cancer. Australas., J. Dermatol., 38 (Suppl.) 1: S1-S6, 1997
36. MacKie, R. M. Incidence, risk factors and prevention of melanoma. Eur. J. Cancer, 34 (Suppl.) 3: S3-S6, 1998
37. Holman, C. D. J., Armstrong, B. K., and Heenan, P. J. A theory of the etiology and pathogenesis of human cutaneous malignant melanoma. J. Natl. Cancer Inst. (Bethesda), 71: 651-656, 1983
38. Whiteman, D. C., Whiteman, C. A., and Green, A. C. Childhood sun exposure as a risk factor for melanoma: A systematic review of epidemiologic studies. Cancer Causes Control, 12: 69-82, 2001
39. Tietze, M. K., and Chin, L. Murine models of malignant melanoma. Mol. Med. Today, 6: 408-410. 2000
40. Kelsall, S. R., and Mintz, B. Metastatic cutaneous melanoma promoted by ultraviolet radiation in mice with transgene-initiated low melanoma susceptibility. Cancer Res., 58: 4061-4065, 1998
41. Broome Powell, M., Gause, P. R., Hyman, P., Gregus, J., Lluria-Prevatt, M., Nagle, R., and Bowden, G. T. Induction of melanoma in TPras transgenic mice. Carcinogenesis (Lond.), 20: 1747-1753, 1999
42. Kos, L., Aronzon, A., Takayama, H., Maina, F., Ponzetto, C., Merlino, G., and Pavan, W. Hepatocyte growth factor/scatter factor-Met signaling in neural crest-derived melanocyte development. Pigm. Cell Res., 12: 13-21, 1999
43. Kunisada, T., Yamazaki, H., Hirobe, T., Kamei, S., Omoteno, M., Tagaya, H., Hemmi, H., Koshimizu, U., Nakamura, T., and Hayashi, S-1. Keratinocyte expression of transgenic hepatocyte growth factor affects melanocyte development, leading to dermal melanocytosis. Mech. Dev., 94: 67-78, 2000
44. Noonan, F. P., Otsuka, T., Bang, S., Anver, M. R., and Merlino, G. Accelerated ultraviolet radiation-induced carcinogenesis in hepatocyte growth factor/scatter factor transgenic mice. Cancer Res., 60: 3738-3743, 2000
45. Noonan, F, P., Recio, J. A., Takayama, H., Duray, P., Anver, M. R., Rush, W. L., De Fabo, E. C., and Merlino, G. Neonatal sunburn and melanoma in mice. Nature (Lond.), 413: 271-272, 2001
46. Takayama, H., LaRochelle, W. J., Anver, M., Bockman, D. E., and Merlino, G. Scatter factor/hepatocyte growth factor as a regulator of skeletal muscle and neural crest development. Proc. Natl. Acad. Sci. USA, 93: 5866-5871, 1996
47. Noonan, F. P., and De Fabo, E. C. Ultraviolet-B dose response curves for local and systemic immunosuppression are identical. Photochem. Photobiol., 52: 801-810, 1990
48. Lindner, G., Menrad, A., Gherardi, E., Merlino, G., Welker, P., Handjiski, B., Roloff, B., and Paus, R. Involvement of hepatocyte growth factor/scatter factor and Met receptor signaling in hair follicle morphogenesis and cycling. FASEB J., 14: 319-332, 2000
49. Iyer, A., Kmiecik, T. E., Park, M., Daar, I., Blair, D., Dunn, K. J., Sutrave, P., Ihle, J. N., Bodescot, M., and Vande Woude, G. F. Structure, tissue-specific expression, and transforming activity of the mouse met proto-oncogene. Cell Growth Diff., 1: 87-95, 1990
50. Zhuang, S. M., Schippert, A., Haugen-Strano, A., Wiseman, R. W., and Soderkvist, P. Inactivations of p16INK4a-α, p16INK4a-β, and p15INK4b genes in 2′, 3′-dideoxycytidine- and 1, 3-butadiene-induced murine lymphomas. Oncogene, 16: 803-808, 1998
51. Scott, G., Stoler, M., Sarkar, S., and Halaban, R. Localization of basic fibroblast growth factor mRNA in melanocytic lesions by in situ hybridization. J. Investig. Dermatol., 96: 318-322, 1991
52. Sharp, R., Recio, J. A., Jhappan, C., Otsuka, T., Liu, S., Yu, Y., Liu, W., Anver, M., Navid, F., Helman, L. J., DePinho, R. A., and Merlino, G. Synergism between INK4a/ARF inactivation and aberrant HGF/SF signaling in rhabdomyosarcomagenesis. Nature Medicine, 8: in press, 2002
53. Hirobe, T. Histochemical survey of the distribution of the epidermal melanoblasts and melanocytes in the mouse during fetal and postnatal periods. Anat. Rec., 208: 589-594, 1984
54. Rosdahl, I. K., and Szabo, G. Mitotic activity of epidermal melanocytes in UV-irradiated mouse skin. J. Investig. Dermatol., 70: 143-148, 1978
55. Hirobe, T. Developmental changes of the proliferative response of mouse epidermal melanocytes to skin wounding. Development (Camb.), 102: 567-574, 1988
56. Noonan, F. P., and De Fabo, E. C. Immunosuppression by ultraviolet B radiation: Initiation by urocanic acid. Immunol. Today, 13: 250-254, 1992
57. Kripke, M. L. Effects of UV radiation on tumor immunity. J. Natl. Cancer Inst. (Bethesda), 82: 1392-1396, 1990
58. Bishop, D. T., Demenais, F., Goldstein, A. M., Bergman, W., Newton Bishop, J., Bressac-de Paillerets, B., Chompret, A., Ghiorzo, P., Gruis, N., Hansson, J., Harland, M., Hayward, N., Holland, E. A., Mann, G. J., Mantelli, M., Nancarrow, D., Platz, A., Tucker, M. A., and the Melanoma Genetics Consortium. Geographical Variation in the penetrance of CDKN2A mutations for melanoma. J. Natl. Cancer Inst. (Bethesda), 94: 894-903, 2002
59. Maestro, R., and Boiocchi, M. Sunlight and melanoma: An answer from MTS1 (p16). Science (Wash. DC), 267: 15-16, 1995
60. Pollock, P. M., Yu, F., Qiu, L., Parsons, P. G., and Hayward, N. K. Evidence for u. v. induction of CDKN2 mutations in melanoma cell lines. Oncogene, 11: 663-668, 1995
61. Pavey, S., Conroy, S., Russell, T., and Gabrielli, B. Ultraviolet radiation induces p16CDKN2A expression in human skin. Cancer Res., 59: 4185-4189, 1999
62. Rizos, H., Puig, S., Badenas, C., Malvehy, J., Darmanian, A. P., Jimenez, L., Mila, M., and Kefford, R. F. A melanoma-associated germline mutation in exon 1β inactivates p14ARF. Oncogene, 20: 5543-5547, 2001