Paradoxical tumor inhibitory effect of p53 loss in transgenic mice expressing epidermal-targeted v-ras(Ha), v-fos, or human transforming growth factor α

Cancer Research

Volumn 56, Issue 19, 1996, Pages 4413-4423

  Greenhalgh, David A ^a,b   Wang, Xiao Jing ^a   Donehower, Lawrence A ^a   Roop, Dennis R ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN P53; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPIDERMIS HYPERPLASIA; GENE EXPRESSION REGULATION; GENE TARGETING; HISTOPATHOLOGY; IMMUNOPHENOTYPING; KERATINOCYTE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SKIN CARCINOGENESIS; TUMOR PROMOTION; TUMOR SUPPRESSOR GENE;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; COCARCINOGENESIS; CROSSES, GENETIC; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; EPIDERMIS; GENES, FOS; GENES, P53; GENES, RAS; HYPERPLASIA; KERATINOCYTES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; ONCOGENE PROTEIN P21(RAS); ONCOGENE PROTEINS V-FOS; RECOMBINANT FUSION PROTEINS; TETRADECANOYLPHORBOL ACETATE; TRANSFORMING GROWTH FACTOR ALPHA; TRANSGENES;

EID: 0029782220     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Yuspa, S. H The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis Cancer Res., 54: 1178-1187, 1994
2. Balmain, A., and Brown, K. Oncogene activation in chemical carcinogenesis. Adv Cancer Res , 51, 147-182, 1988.
3. Hanahan, D. Dissecting multistep tumorigenesis in transgenic mice. Annu. Rev Genet., 22 479-519, 1988.
4. Greenhalgh, D. A., and Roop, D. R. Dissecting molecular carcinogenesis, development of transgenic mouse models by epidermal gene targeting. Adv. Cancer Res., 64: 247-296, 1994
5. Bailleul, B., Surani, M. A., White, S., Barton, S. C., Brown, K , Blessing, N., Jorcano, J , and Balmain, A. Skin hyperkeratosis and papilloma formation in transgenic mice expressing a ras oncogene from a suprabasal keratin promoter Cell, 62: 697-708, 1990.
6. Ha mutation in mouse skin tumorigenesis Mol. Cell Biol., 12: 4643-4653, 1992.
7. Ha to the epidermis of transgenic mice induces hyperplasia, hyperkeratosis and papillomas Mol. Carcinog., 7: 99-110, 1993.
8. Greenhalgh, D A , Rothnagel, J A., Wang, X-J , Quintanilla, M. I , Orengo, C. C., Gagne, T A., Bundman, D. S., Longley, M. A., Fisher, C., and Roop, D. R Hyperplasia, hyperkeratosis and benign tumor production in transgenic mice by a targeted v-fos oncogene suggests a role for fos in epidermal differentiation and neoplasia Oncogene, 8: 2145-2157, 1993.
9. Dominey, A. M , Wang, X-J., King, L E , Jr , Nanney, L. B., Gagne, T. A , Sellheyer, K , Bundman, D S., Longley, M A., Rothnagel, J. A., Greenhalgh, D. A., and Roop, D. R Targeted overexpression of transforming growth factor-α in the epidermis of transgenic mice elicits hyperplasia, hyperkeratosis and spontaneous squamous papillomas Cell Growth & Differ., 4 1071-1082, 1993.
10. Ha activation or overexpression. Mol. Carcinog., 10: 5-22, 1994.
11. Jhappan, C , Takayama, H , Dickson, R B., and Merlino, G. Transgenic mice provide genetic evidence that transforming growth factor α promotes skin tumongenesis via H-ras-dependent and H-ras-independent pathways. Cell Growth & Differ., 5: 385-397, 1994.
12. Ha activated papillomas and carcinomas without p53 mutation: association of v-fos expression with promotion and tumor autonomy. Cell Growth & Differ., 6: 579-586, 1995.
13. Ha induces autonomous papillomas in transgenic epidermis but not malignant conversion. Cancer Res., 53: 5071-5075, 1993.
14. Wang, X-J., Greenhalgh, D. A , Lu, X-R., Bickenbach, J., and Roop, D. R. TGFα and v-fos cooperation in transgenic mice epidermis induces aberrant-keratinocyte differentiation and stable autonomous papillomas. Oncogene, 10: 279-289, 1995.
15. Kim, S. H., Roth, K. A , Moser, A., and Gordon, J. I. Transgenic mouse models that explore the multistep hypothesis of intestinal neoplasia J. Cell Biol , 123, 877-887, 1993
16. Greenblatt, M S , Bennett, W. P., Hollstein, M., and Harris, C. C. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis Cancer Res , 54: 4855-4878, 1994.
17. Malkin, D , Li, F P., Stong, L. C , Fraumeni, J. F , Nelson, C E., Kim, D. H , Kassel, J , Gryka, M A , Bischoff, F. Z., Tainsky, M. A , and Friend, S. H. Germline p53 mutations in a familial syndrome of breast cancer, sarcomas and other neoplasms. Science (Washington DC), 250: 1233-1238, 1990.
18. Brash, D. E., Rudolph, J. A , Simon, J. A., Lin, A., McKenna, G. J , Baden, H P., Halperin, A J., and Ponten, J A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. USA, 8 10124-10128, 1991
19. Moles, J. P., Moyret, C., Guillot, B , Jeanteau, P., Guilhous, J. J., Theiller, C , and Basset-Seguin. N p53 gene mutations in human epithelial skin cancers. Oncogene, 8 583-588, 1993.
20. Kastan, M. B., Onykivere, O., Sidransky, D , Vogelstein, B., and Craig, R. W. Participation of the p53 protein in the cellular response to DNA damage. Cancer Res., 51: 6301-6311, 1991.
21. Livingstone, L. R , White, K., Sprouse, J , Livanos, E., Jacks, T., and Tlsty, T D Altered cell cycle arrest and gene amplification potential accompanying loss of wild type p53. Cell, 70: 923-935, 1992.
22. Harper, J. W., Adami, G. R , Wei, N. W . Handon-Keyomarsi, K., and Elledge, S. J. The p21 Cdk-interacting protein, CIP1, is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75. 805-816, 1993.
23. El-Deiry, W. S., Tokino, T., Velculescu, V. E , Levy, D. B , Parson, R , Trent, J. M , Lin, D., Mercer, E. W., Kinzler, K W., and Vogelstein, B WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
24. Morgenbesser, S. D., Williams, B G , Jacks, T., and DePinho, R. A. p53 dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature (Lond.), 371: 72-74, 1994.
25. Kasten, M. B., Zhan, Q., El-Deiry, W. S., Carrier, F , Jacks, T , Welsh, W. V., Plunkett, B. S , Vogelstein, B., and Fornace, A. J., Jr A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in Ataria-Telangiectasia Cell, 71, 587-592, 1992.
26. Werness, B. A., Levine, A. J , and Howley, P. M. The E6 proteins encoded by human papillomavirus types 16 and 18 can complex p53 in vitro. Science (Washington DC), 248: 76-79, 1990.
27. Dittmer, D., Pato, S., Zambetti, G., Chu, S., Tersky, A. K., More, M , Finlay, L., and Levine, A. J. Gain of function p53 mutants. Nat. Genet., 4: 42-49, 1993
28. Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M J , Montgomery, C A., Jr., Butel, J. S., and Bradley, A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature (Lond.), 356: 215-221, 1992.
29. Lu, X , Park, S H , Thompson, T. C., and Lane, D. P. ras-induced hyperplasia occurs with mutation of p53, but activated ras and myc together can induce carcinoma without p53 mutation. Cell, 70: 153-160, 1992.
30. Burns, P. A., Kemp, C. J , Gannon, J. V., Lane, D. P , Bremner, R., and Balmain, A. Loss of heterozygosity and mutational alterations of the p53 gene in skin tumors of interspecific hybrid mice Oncogene, 6: 2363-2369, 1991.
31. Ruggeri, B , Caamano, J., Goodrow, T., DiRado, M., Bianchi, A., Trono, D., Conti, C. J , and Klein-Santo, A. J. P. Alterations of the p53 tumor suppressor gene during mouse skin tumor progression. Cancer Res., 51 6615-6622, 1991.
32. Eliyahu, D , Mechaloritz, D., Eliyahu, S , Pinhasi-Kimhi, O., and Oren, M. Wild-type p53 can inhibit oncogene mediated focus formation. Proc. Natl Acad. Sci. USA, 86: 8763-8769, 1986.
33. Kemp, C J , Donehower, L. A , Bradley, A , and Balmain, A. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically-induced skin tumors Cell, 74 813-822, 1993.
34. Ha oncogene. Cancer Res., 54: 5584-5592, 1994
35. Ziegler, A., Jonason, A. S , Leffett, D. J , Simon, J. A , Sharma, H. S , Kimmelman, J., Remington, L., Jacks, T., and Brash, D. Sunburn and p53 in the onset of skin cancer Nature (Lond.), 372: 773-776, 1994
36. Chomczynski, P., and Sacchi, N Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987
37. Friedberg, T , Grassow, M. A., and Oesch, F Selective detection of mRNA forms encoding the major phenobarbital inducible cytochromes P450 and other members of the P45011B family by the RNases: a protection assay. Arch Biochem. Biophys , 279: 167-173, 1990.
38. Roop, D R., Huitfeld, H , Kilkenny, A , and Yuspa, S. H Regulated expression of differentiation associated keratins in cultured epidermal cells detected by monospecific antibodies to unique peptides of mouse epidermal keratins Differentiation, 35: 143-150, 1987.
39. Huitfeld, H., Heyden, A., Clausen, O. P. F , Thrane, E V., Roop, D. R , and Yuspa, S H. Altered regulation of growth expression of differentiation associated keratins in benign mouse skin tumors. Carcinogenesis (Lond.), 12: 2063-2067, 1991.
40. Mehrel, T , Hohl, D , Rothnagel, J. A , Longley, M A., Bundman, D , Cheng, C., Lichti, U., Bisher, M. E., Steven, A. C , Steinert, P. M , Yuspa, S. H., and Roop, D R Identification of a major keratinocyte cell envelope protein, loricrin. Cell. 61: 1103-1112, 1990.
41. Rothnagel, J. A., Mehrel, T , Idler, W. W , Roop, D R , and Steinert, P. M. The structure and expression of the mouse epidermal filaggrin precursor gene J Biol. Chem, 262. 15643-15648, 1987.
42. Weiss, R. A., Eichner, R A., and Sun, T. T Monoclonal antibody analysis of keratin expression in epidermal diseases. A 48- and 56-kilodalton keratin as molecular markers for hypoproliferative keratinocytes J. Cell Biol , 98: 1397-1406, 1984.
43. Sellheyer, K., Bickenbach, J. R , Rothnagel, J. A., Bundman, D., Longley, M A., Krieg, T., Roche, N. S , Roberts, A. B., and Roop, D R Inhibition of skin development by overexpression of transforming growth factor-β1 in the epidermis of transgenic mice Proc Natl. Acad. Sei USA, 90: 5237-5241, 1993
44. Nischt, R., Roop, D. R., Mehrel, T., Yuspa, S H., Rentrop, M., Winter, H , and Schweizer, J. Aberrant expression during two stage mouse skin carcinogenesis of a type 47 kDa keratin, K13, normally associated with terminal differentiation of internal stratified epithelia. Mol. Carcinog , 1: 96-108, 1988.
45. Harvey, M , McArthur, M. J., Montgomery, C. A , Bradley, A , and Donehower, L. A Genetic background alters the spectrum of tumors that develop in p53 deficient mice. FASEB J., 10, 938-943, 1993.
46. DiGiovanni, J. Further genetic analyses of skin tumor promoter susceptibility using inbred and recombinant inbred mice. Carcinogenesis (Lond.), 13: 525-531, 1992.
47. Kuerbitz, S. J., Plunkett, B. S , Walsh, W. V., and Kastan, M B. Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl Acad. Sci. USA, 39: 7491-7495, 1992.
48. Roop, D. R., Lowy, D R., Tamborm, P. E , Strickland, J. E , Harper, J. R., Balaschak, M., Spangler, E. G., and Yuspa, S. H An activated Harvey ras oncogene produces benign tumors on mouse epidermal tissue. Nature (Lond.), 323: 822-824, 1986.
49. 2. Cell, 79. 329-339, 1994
50. Li, M , Hu, J , Heermeier K., Heemghausen, L , and Furth, P. A. Expression of a viral oncoprotein during mammary gland development alters cell fate and function: induction of p53 independent apoptosis is followed by impaired milk protein production in surviving cells. Cell Growth & Differ., 7: 3-11, 1996.
51. Symonds, H , Krall, L., Remington, L , Saenz-Robles, M , Lowe, S., Jacks, T., and VanDyke, T p53 dependent apoptosis suppresses tumor growth and progression in vivo. Cell, 78: 703-711, 1994.
52. Michiele, P , Chedid, M., Lin, D., Mercer, W. E., and Givol, D. Induction of WAF1/C1P1 by a p53-independent pathway. Cancer Res , 54: 3391-3395, 1994.
53. Johnson, M., Dimitrov, D., Vojta, P. J., Barrett, J. C., Pereira-Smith, O. L., and Smith, J. R Evidence for a p53-independent pathway for up-reguliation of SDI1/CIP1/ WAF1l/p21 RNA in human cells. Mol Carcinog , 11: 59-64, 1994.
54. Cip1 in muscle and other terminally differentiating cells. Science (Washington DC), 267: 1024-1027, 1995
55. Macleod, K F., Sherry, N., Hannon, G , Beach, D , Tokino, T., Kinzler, K., Vogelstein, B , and Jacks, T p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev., 9: 935-944, 1995.
56. Shin, T H., Paterson, A. J , and Kudlow, J. E. p53 stimulates transcription from the human transforming growth factor a promoter: a potential growth stimulatory role for p53. Mol Cell Biol., 15 4694-4701, 1995.
57. Slaga, T. J. Critical events in skin tumor promotion and progression Basic Life Sci., 57: 19-29, 1991.
58. Kastan, M. B., Radin, A. I., Kuerbitz, S. J., Onyekwere, O , Wolkow, C. A., Civin, C. I., Stone, K D , Woo, T , Ravindravath, Y , and Craig, R. W Levels of p53 protein increase with maturation in human hematopoietic cells. Cell Res , 51: 4279-4286, 1991.
59. Klinedinst, D K , and Drinkwater, N R Reduction to homozygosity is the predominant spontaneous mutational event in cultured human lymphoblastoid cells. Mutat. Res., 250 365-374, 1991
60. Vogelstein, B. Cancer, a deadly inheritance. Nature (Lond.), 348, 681-682, 1990.