Loss of retinoic acid receptors in mouse skin and skin tumors is associated with activation of the ras(Ha) oncogene and high risk for premalignant progression

Cancer Research

Volumn 56, Issue 21, 1996, Pages 4942-4949

  Darwiche, Nadine ^a   Scita, Giorgio ^a   Jones, Carol ^a   Rutberg, Susan ^a   Greenwald, Eileen ^a   Tennenbaum, Tamar ^a   Collins, Steven J ^b   De Luca, Luigi M ^a   Yuspa, Stuart H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN; MEZEREIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; RETINOIC ACID; RETINOIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION; KERATINOCYTE; MOUSE; NEWBORN; NONHUMAN; ONCOGENE H RAS; PRIORITY JOURNAL; SKIN CARCINOGENESIS; SKIN TUMOR;

ANIMALS; CELL CYCLE; CELL DIVISION; FEMALE; GENE EXPRESSION REGULATION; GENES, RAS; KERATINOCYTES; MICE; MICE, INBRED BALB C; PRECANCEROUS CONDITIONS; PROTEIN KINASE C; RECEPTORS, RETINOIC ACID; SKIN; SKIN NEOPLASMS; TETRADECANOYLPHORBOL ACETATE; TRANS-ACTIVATION (GENETICS);

EID: 0029956526     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. De Luca, L M. Retinoids and their receptors in differentiation, embryogenesis and neoplasm FASEB J., 5: 2924-2933, 1991.
2. Rosenthal, D., Lancillotti, F., Darwiche, N, Sinha, R, and De Luca, L. M. Retinoids in epithelial differentiation and tumongenesis. In: R. Blomhoff (ed.). Vitamin A in Health and Disease, pp. 425-450. New York: Marcel Dekker, 1994
3. Lippman, S. M, and DiGiovanna, J. J. Retinoids in skin cancer In: W. K Hong and R. Lotan (eds), Retinoids in Oncology, pp 179-202 New York Marcel Dekker, 1993
4. Chen, L. C, and De Luca, L. M. Retinoids and skin cancer. In: H. Mukhtar (ed.), Skin Cancer: Mechanisms and Human Relevance, pp 401-424 Boca Raton, FL: CRC Press, Inc. 1995
5. Kastner, P, Chambon, P., and Leid, M. Role of nuclear retinoic acid receptors in the regulation of gene expression. In R. Blomhoff (ed.), Vitamin A in Health and Disease, pp. 189-238 New York: Marcel Dekker, 1994.
6. Khewer, S A., Umesono, K., Evans, R, and Mangelsdorf, D. J The retinoid X receptors. modulators of multiple hormonal signaling pathways. In: R. Blomhoff (ed.), Vitamin A in Health and Disease, pp. 239-255. New York. Marcel Dekker, 1994.
7. Yuspa, S H., and Poirier, M C. Chemical carcinogenesis: from animal models to molecular models in one decade. Adv. Cancer Res., 50 25-70, 1988.
8. Hennings, H., Shores, R., Mitchell, P, Spangler, E. F., and Yuspa, S H. Induction of papillomas with a high probability of conversion to malignancy. Carcinogenesis (Lond.), 6: 1607-1610, 1985.
9. Tennenbaum, T., Weiner, A. K, Belanger, A. J., Glick, A. B, Hennings, H, and Yuspa, S H. The suprabasal expression of α6β4 integrin is associated with a high risk for malignant progression in mouse skin carcinogenesis Cancer Res., 53: 4803-4810, 1993
10. Glick, A. B., Kulkarni, A B, Tennenbaum, T., Hennings, H., Flanders, K. C, O'Reilly, M., Sporn, M B., Karlsson, S, and Yuspa, S H. Loss of expression of transforming growth factor β in skin and skin tumors is associated with hyperproliferation and a high risk for malignant conversion. Proc Natl Acad Sci. USA, 90: 6076-6080, 1993.
11. Darwiche, N., Celli, G., Tennenbaum, T., Glick, A B., Yuspa, S. H, and De Luca, L. M Mouse skin tumor progression results in differential expression of retinoic acid and retinoid X receptors Cancer Res., 55: 2774-2782, 1995
12. Chen, L. C, Tarone, R, Huynh, M, and De Luca, L M. High dietary retinoic acid inhibits tumor promotion and malignant conversion in a two-stage skin carcinogenesis protocol using 7,12-dimethylbenz(a)anthracene as the initiator and mezerein as the tumor promoter in female SENCAR mice. Cancer Lett, 95: 113-118, 1995
13. Nelson, M A, Futscher, B. W, Kinsella, T, Wymer, J., and Bowden, G. T. Detection of mutant Ha-ras genes in chemically initiated mouse skin epidermis before the development of benign tumors. Proc. Natl Acad. Sci USA, 89 6398-6402, 1992
14. Balmain, A., and Brown, K. Oncogene activation in chemical carcinogenesis Adv Cancer Res, 51: 147-182, 1988.
15. Balmain, A., Ramsden, M, Bowden, G T., and Smith, J Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature (Lond), 307: 658-660, 1984.
16. Yuspa, S H, Kilkenny, A E., Stanley, J., and Lichti, U. Keratinocytes blocked in phorbol ester-responsive early stage of terminal differentiation by sarcoma viruses Nature (Lond), 314 459-462, 1985
17. Ha oncogene and form papillomas in skin grafts on athymic nude mouse hosts. Cancer Res., 48: 165-169, 1988
18. Roop, D R., Lowy, D. R, Tambourin, P E., Strickland, J, Harper, J. R, Balaschak, M, Spangler, E. F. and Yuspa, S H An activated Harvey ras oncogene produces benign tumours on mouse epidermal tissue. Nature (Lond), 323: 822-824, 1986.
19. Dlugosz, A. A, Cheng, C, Williams, E. K., Dharia, A G., Denning, M. F., and Yuspa, S H Alterations in murine keratinocyte differentiation induced by activated ras genes are mediated by protein kinase C-α Cancer Res., 54: 6413-6420, 1994.
20. Ha gene in murine keratinoctyes induces tyrosine phosphorylation and reduced activity of protein kinase C δ J. Biol. Chem, 268: 26079-26081, 1993.
21. Scita, G, Darwiche, N., Greenwald, E., Rosenberg, M, Politi, K., and De Luca, L. M. Retinoic acid downregulation of fibronectin and retinoic acid receptor α proteins in NIH-3T3 cells: block of this response by ras transformation. J. Biol. Chem., 271: 6502-6508, 1996
22. Hennings, H., Michael, D., Cheng, C., Steinen, P., Holbrook, K., and Yuspa, S. H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell, 19: 245-254, 1980.
23. Yuspa, S. H., Kilkenny, A. E., Steinert, P. M, and Roop, D. R. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro. J. Cell Biol., 109: 1207-1217, 1989.
24. Collins, S. J., Robertson, K. A., and Mueller, L Retinoic acid-induced granulocytic differentiation of HL-60 myeloid leukemia cells is mediated directly through the retinoic acid receptor (RAR-α). Mol. Cell. Biol., 10: 2154-2163, 1990.
25. Schreiber, E, Matthias, P., Muller, M. M., and Schaffner, W. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res., 17: 6419, 1989.
26. Gaub, M. P, Rochette-Egly, C, Lutz, Y, Ali, S, Matthes, H, Scheuer, I., and Chambon, P Immunodetection of multiple species of retinoic acid receptor α-1 evidence for phosphorylation Exp. Cell Res., 201: 335-346, 1992.
27. Rochette-Egly, C., Lutz, Y., Saunders, M., Scheuer, I., Gaub, M. P., and Chambon, P. Retinoic acid receptor-π specific immunodetection and phosphorylation. J. Cell Biol., 115, 535-545, 1991.
28. Roop, D. R., Cheng, C. K., Titterington, L, Meyers, C. A., Stanley, J. R., Steinert, P. M, and Yuspa, S. H. Synthetic peptides corresponding to keratin subunits elicit highly specific antibodies. J. Biol. Chem, 259: 8037-8040, 1984.
29. Minucci, S., Zand, D J., Dey, A., Marks, M. S., Nagata, T., Grippo, J. F., and Ozato, K. Dominant negative retinoid X receptor β inhibits retinoic acid-responsive gene regulation in embryonal carcinoma cells Mol Cell Biol., 14: 360-372, 1994.
30. MacGregor, G. R., and Caskey, C T Construction of plasmids that express E coli β-galactosidase in mammalian cells. Nucleic Acids Res, 17: 2365, 1989.
31. Weinberg, W. C, Brown, P. D., Stetler-Stevenson, W. G, and Yuspa, S H. Growth factors specifically alter hair follicle cell proliferation and collagenolytic activity alone or in combination. Differentiation, 45: 168-178, 1990
32. Kumar, R., Shoemaker, A R., and Verma, A. K. Retinoic acid nuclear receptors and tumor promotion: decreased expression of retinoic acid nuclear receptors by the tumor promoter 12-O-tetradecanoylphorbol-13-acetate Carcinogenesis (Lond.), 15: 701-705, 1994.
33. Denning, M. F., Dlugosz, A. A, Williams, E. K, Szallasi, Z., Blumberg, P. M., and Yuspa, S H. Specific protein kinase C isozymes mediate the induction of keratinocyte differentiation markers by calcium. Cell Growth & Differ., 6 149-157, 1995
34. Vollberg, T M., Nervi, C., George, M D., Fujimoto, W., Krust, A, and Jetten, A. M. Retinoic acid receptors as regulators of human epidermal keratinocyte differentiation. Mol Endocrinol, 6: 667-676, 1992
35. Aneskievich, B. J., and Fuchs, E Terminal differentiation in keratinocytes involves positive as well as negative regulation by retinoic acid receptors and retinoid X receptors at retinoid response elements. Mol. Cell Biol., 12: 4862-4871, 1992.
36. Imakado, S., Bickenbach, J R., Bundman, D. S., Rothnagel, J. A., Attar, P. S., Wang, X. J., Walczak, V R, Wisniewski, S, Pole, J, Gordon, J S., Heyman, R. A, Evans, R M., and Roop, D. R. Targeting expression of a dominant-negative retinoic acid receptor mutant in the epidermis of transgenic mice results in loss of barrier function. Genes Dev, 9: 317-329, 1995.
37. Saltou, M., Sugal, S., Tanaka, T., Shimouchi, K, Fuchs, E., Narumiya, S., and Kakizuka, A. Inhibition of skin development by targeted expression of a dominant-negative retinoic acid receptor. Nature (Lond), 374: 159-162, 1995.
38. Yuspa, S H. The pathogenesis of squamous cell cancer lessons learned from studies of skin carcinogenesis Cancer Res., 54: 1178-1189, 1994
39. Glick, A. B, Flanders, K. C., Danielpour, D., Yuspa, S H, and Sporn, M. B. Retinoic acid induces transforming growth factor-β in cultured keratinocytes and mouse epidermis Cell Regul., 1, 87-97, 1989.
40. Fisher, G J, Talwar, H S., Xiao, J. H, Datta, S. C., Reddy, A. P, Gaub, M. P., Rochette-Egly, C, Chambon, P., and Voorhees, J J Immunological identification and functional quantitation of retinoic acid and retinoid X receptor proteins in human skin. J. Biol. Chem., 269: 20629-20635, 1994.
41. Greenhalgh, D A., Welty, D. J., Player, A., and Yuspa, S. H. Two oncogenes, v-fos and v-ras, cooperate to convert normal keratinocytes to squamous cell carcinomas. Proc. Natl. Acad Sci USA, 87: 643-647, 1990.
42. Saez, E., Rutberg, S. E., Mueller, E., Oppenheim, H., Smoluk, J., Yuspa, S. H., and Spiegelman, B. M. c-fos is required for malignant progression of skin tumors. Cell, 82: 721-732, 1995.
43. Curran, T, and Franza, B R. Fos and jun The AP-1 connection. Cell, 55: 395-397, 1988.
44. Domann, F E., Jr., Levy, J. P, Finch, J. S., and Bowden, G T. Constitutive AP-1 DNA binding and transactivating ability of malignant but not benign mouse epidermal cells Mol Carcinog, 9: 61-66, 1994.
45. Dong, Z, Birrer, M. J., Watts, R. G. Matrisian, L M., and Colburn, N. H. Blocking of tumor promoter-induced AP-1 activity inhibits induced transformation in JB6 mouse epidermal cells. Proc. Natl Acad Sci. USA, 91: 609-613, 1994.
46. Schule, R., Rangarajan, P., Yang, N., Kliewer, S, Ransone, L. J, Bolado, J, Verma, I. M, and Evans, R M Retinoic acid is a negative regulator of AP-1-responsive genes. Proc. Natl. Acad. Sci. USA, 88: 6092-6096, 1991
47. Pfahl, M. Nuclear receptor/AP-1 interaction Endocr. Rev., 14 651-658, 1993
48. Nicholson, R. C., Mader, S., Nagpal, S, Leid, M., Rochette-Egly, C., and Chambon, P. Negative regulation of the rat stromelysin gene promoter by retinoic acid is mediated by an API binding site EMBO J, 9 4443-4454, 1990
49. Yang-Yen, H. F., Zhang, X K., Graupner, G, Tzukerman, M, Sakamoto, B., Karin, M., and Pfahl, M. Antagonism between retinoic acid receptors and AP-1. implications for tumor promotion and inflammation New Biol, 3 1206-1219, 1991
50. Nagpal, S., Athanikar, J., and Chandraratna, R. A. Separation of transactivation and API antagonism functions of retinoic acid receptor α. J. Biol Chem., 270: 923-927, 1995
51. Yuspa, S H., Hennings, H., Dlugosz, A., Tennenbaum, T., and Glick, A. B. The role of growth factors in mouse skin tumor promotion and premalignant progression. In: M. McClain, T. Slaga, R. LeBoeuf, and H Pitot (eds.), Growth Factors and Tumor Promotion. Implications for Risk Assessment, pp. 39-48 New York: John Wiley Liss, 1995.
52. De Luca, L. M., Tarone, R, Huynh, M., Jones, C. S, and Chen, L. C. Dietary retinoic acid inhibits mouse skin carcinogenesis irrespective of age at initiation. Nutr. Cancer, 25: 249-257, 1996
53. Greenhalgh, D. A., Welty, D. J, Strickland, J E, and Yuspa, S. H. Spontaneous Ha-ras gene activation in cultured primary murine keratinocytes. consequences of Ha-ras gene activation in malignant conversion and malignant progression. Mol. Carcinog, 2: 199-207, 1989.
54. Bremner, R, and Balmain, A. Genetic changes in skin tumor progression, correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell, 61: 407-417, 1990.
55. Yang, Y., Minucci, S., Zand, D. J., Ozato, K., and Ashwell, J. D. T cell activation and increases in protein kinase C activity enhance retinoic acid-induced gene transcription Mol. Endocrinol., 8: 1370-1376, 1994.
56. Bouzinba-Segard, H., Fan, X. T., Perdenset, M, and Castagna, M. Synergy between phorbol esters and retinoic acid in inducing protein kinase C activation. Biochem. Biophys. Res. Commun., 204: 112-119, 1994.
57. Verma, A K., and Boutwell, R. K. Vitamin A acid (retinoic acid): a potent inhibitor of 12-O-tetradecanoyl-phorbol-13-acetate-induced omithine decarboxylase activity in mouse epidermis. Cancer Res., 37: 2196-2201, 1977
58. Paulsen, J E. Effects of retinoic acid on epidermal DNA synthesis induced by 12-O-tetradecanoylphorbol-13-acetate, mezerein or ethylphenylpropiolate in hairless mice. Carcinogenesis (Lond), 11: 1255-1258, 1990.
59. Sharkey, N A., Hennings, H., Yuspa, S. H., and Blumberg, P. M. Comparison of octahydromezerein and mezerein as protein kinase C activators and as mouse skin tumor promoters. Carcinogenesis (Lond.), 10: 1937-1941, 1989.
60. Klein-Szanto, A. J. P, Major, S K., and Slaga, T. J. Induction of dark keratinocytes by 12-O-ietradecanoyl-phorbol-13-acetate and mezerein as an indicator of tumor-promoting efficiency Carcinogenesis (Lond.), 1: 399-406, 1980
61. Mufson, R. A., Fischer, S. M., Verma, A. K., Gleason, G. L., Slaga, T J., and Boutwell, R K. Effects of 12-O-tetradecanoylphorbol-13-acetate and mezerein on epidermal ornithine decarboxylase activity, isoproterenol-stimulated levels of cyclic adenosine 3′ 5′-monophosphate, and induction of mouse skin tumors in vivo. Cancer Res, 39: 4791-4795, 1979.