Targeted expression of c-Src in epidermal basal cells leads to enhanced skin tumor promotion, malignant progression, and metastasis

Cancer Research

Volumn 63, Issue 16, 2003, Pages 4819-4828

  Matsumoto, Takashi ^a   Jiang, Jianghong ^a   Kiguchi, Kaoru ^a   Ruffino, Lynnsie ^a   Carbajal, Steve ^a   Beltrán, Linda ^a   Bol, David K ^b   Rosenberg, Michael P ^c   DiGiovanni, John ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b Avalon Pharmaceuticals   (United States)

^c Piedmont Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 14; KERATIN; KERATIN 5; PHORBOL 13 ACETATE 12 MYRISTATE; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL CELL; CANCER GROWTH; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS; EPIDERMIS CELL; EPIDERMIS HYPERPLASIA; FEMALE; HYPERKERATOSIS; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; METASTASIS; MOUSE; NONHUMAN; ONCOGENE SRC; PAPILLOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN CARCINOMA; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; SURVIVAL; TUMOR PROMOTION;

9,10-DIMETHYL-1,2-BENZANTHRACENE; AMINO ACID SEQUENCE; ANIMALS; CARCINOMA, SQUAMOUS CELL; FEMALE; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NEOPLASM METASTASIS; PROTEIN-TYROSINE KINASES; SKIN; SKIN NEOPLASMS; TETRADECANOYLPHORBOL ACETATE;

EID: 0041940113     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Brugge, J. S., and Erikson, R. L. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature (Lond.), 269: 346-348, 1977.
2. Collett, M., Erikson, E., Purchio, A. F., Brugge, J. S., and Erikson, R. L. A normal cell protein similar in structure and function to the avian sarcoma virus transforming gene product. Proc. Natl. Acad. Sci. USA, 76: 3159-3163, 1979.
3. Brown, M. T., and Cooper, J. A. Regulation, substrates and functions of src. Biochem. Biophys. Acta., 1287: 121-149, 1996.
4. Okada, M., and Nakagawa, H. Identification of a novel protein tyrosine kinase that phosphorylates pp60c-src and regulates its activity in neonatal rat brain. Biochem. Biophys. Res. Commun., 154: 796-802. 1988.
5. Brickell, P. M. The p60csrc family of protein-tyrosine kinases: structure, regulation, and function. Crit. Rev. Oncog., 3: 401-446, 1992.
6. Stein, P. L., Vogel, H., and Soriano, P. Combined deficiencies of Src, Fyn, and Yes tyrosine kinases in mutant mice. Genes Dev., 8: 1999-2007, 1994.
7. Hirai, H., and Varmus, H. E. Mutations in src homology regions 2 and 3 of activated chicken c-src that result in preferential transformation of mouse of chicken cells. Proc. Natl. Acad. Sci. USA. 87: 8592-8596, 1990.
8. Rosen, N., Bolen, J. B., Schwartz, A. M., Cohen, P., DeSau, V., and Israel, M. A. Analysis of pp60csrc protein kinase activity in human tumor cell lines and tissues. J. Biol. Chem., 261: 13754-13759, 1986.
9. Cartwright, C. A., Kamps, M. P., Meisler, A. I., Pipas, J. M., and Eckhart, W. pp60csrc activation in human colon carcinoma. J. Clin. Investig., 83: 2025-2033. 1989.
10. Ottenhoff-Kalff, A. E., Rijksenm, G., van Beurden, E. A., Hennipman, A., Michels, A. A., and Staal, G. E. Characterization of protein tyrosine kinases from human breast cancer: involvement of the c-src oncogene product. Cancer Res., 52: 4773-4778, 1992.
11. Lutz, M. P., Esser, I. B., Flossmann-Kast, B. B., Vogelmann, R., Luhrs, H., Friess, H., Buchler, M. W., and Adler, G. Overexpression and activation of the tyrosine kinase Src in human pancreatic carcinoma. Biochem. Biophys. Res. Commun., 243: 503-508, 1998.
12. Xian, W., Rosenberg, M. P., and DiGiovanni, J. Activation of erbB2 and c-src in phorbol ester-treated mouse epidermis: possible role in mouse skin tumor promotion. Oncogene, 14: 1435-1444. 1997.
13. Matsumoto, T., Jiang, J., Kiguchi, K., Carbajal, S., Rho, O., Gimenez-Conti, I., Beltran, L., and DiGiovanni. J. Overexpression of a constitutively active form of c-src in skin epidermis increases sensitivity to tumor promotion by 12-O-tetradecanoylphorbol-13-acetate. Mol. Carcinog, 33: 146-155, 2002.
14. Bol, D., Kiguchi, K., Beltrán, L., Rupp, T., Moats, S., Gimenez-Conti, I., Jorcano, J., and DiGiovanni, J. Severe follicular hyperplasia and spontaneous papilloma formation in transgenic mice expressing the Neu oncogene under the control of the bovine keratin 5 promoter. Mol. Carcinog., 21: 2-12, 1998.
15. Hogan, B., Beddington, R., Costantini, F., and Lacy, E. (eds.), Manipulating the Mouse Embryo, A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 1994.
16. Kucera, G., Bortner, D., and Rosenberg, M. Overexpression of an Agouti cDNA in the skin of transgenic mice recapitulates dominant coat color phenotypes of spontaneous mutants. Dev. Biol., 173: 162-173, 1996.
17. Bol, D., Kiguchi, K., Gimenez-Conti, I., Rupp, T., and DiGiovanni. J. Overexpression of insulin-like growth factor-1 induces hyperplasia, dermal abnormalities, and spontaneous tumor formation in transgenic mice. Oncogene, 14: 1725-1734, 1997.
18. Naito, M., Naito, Y., and DiGiovanni, J. Comparison of the histological changes in the skin of DBA/2 and C57BL/6 mice following exposure to various promoting agents. Carcinogenesis (Lond.), 8: 1807-1815, 1987.
19. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227: 680-685, 1970.
20. Mansbridge, J. N., and Knapp, A. M. Changes in keratinocyte maturation during wound healing. J. Investig. Dermatol., 89: 253-263, 1987.
21. Molloy, C. J., and Laskin, J. D. Specific alterations in keratin biosynthesis in mouse epidermis in vivo and in explant culture following a single exposure to the tumor promoter 12-O-tetradecanoylphorbol-13-acetate. Cancer Res., 47: 4674-4680, 1987.
22. Casatorres, J., Navarro, J., Blessing, M., and Jorcano, J. Analysis of the control of expression and tissue specificity of the keratin 5 gene, characteristic of basal keratinocytes. J. Biol. Chem., 32: 20489-20496, 1994.
23. Ramirez, A., Bravo, A., Jorcano, J. L., and Vidal, M. Sequences 5′ of the bovine keratin 5 gene direct tissue- and cell-type-specific expression of a lacZ gene in the adult and during development. Differentiation, 58: 53-64, 1994.
24. Biscardi, J. S., Tice, D. A., and Parsons, S. J. c-Src, receptor tyrosine kinases, and human cancer. Adv. Cancer Res., 76: 61-119, 1999.
25. Irby, R. B., and Yeatman, T. J. Role of Src expression and activation in human cancer. Oncogene, 19: 5636-5642, 2000.
26. DiGiovanni, J. Multistage carcinogenesis in mouse skin. Pharmac. Ther., 48: 63-128, 1992.
27. Kiguchi, K., Beltrán, L. M., You, J., Rho, O., and DiGiovanni, J. Elevation of transforming growth factor-a mRNA and protein expression by diverse tumor promoters in SENCAR mouse epidermis. Mol. Carcinog., 12: 225-235, 1995.
28. Kiguchi, K., Beltrán, L., Rupp, T., and DiGiovanni, J. Altered expression of epidermal growth factor receptor ligands in tumor promoter-treated mouse epidermis and in primary mouse skin tumors by an initiation-promotion protocol. Mol. Carcinog., 22: 73-83, 1998.
29. Muthuswamy, S., and Muller, W. Direct and specific interaction of c-Src with Neu is involved in signaling by the epidermal growth factor receptor. Oncogene, 11: 271-279, 1995.
30. Muthuswamy, S., Siegel, P., Dankort, K., Webster, M., and Muller, W. Mammary tumors expressing the neu proto-oncogene possess elevated c-Src tyrosine kinase activity. Mol. Cell. Biol., 14: 735-743, 1994.
31. Maa, M-C., Leu, T-H., McCarley, D., Schatzman, R., and Parsons, S. Potentiation of epidermal growth factor receptor-mediated oncogenesis by c-Src: implications for the etiology of multiple human cancers. Proc. Natl. Acad. Sci. USA, 92: 6981-6985, 1995.
32. Tice, D. A., Biscardi, J. S., Nickles, A. L., and Parsons, S. J. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl. Acad. Sci. USA, 96: 1415-1420, 1999.
33. Chan, K. S., Carbajal, S., Kiguchi, K., and DiGiovanni, J. Activation of STAT family members in multistage skin carcinogenesis. Proc. Am. Assoc. Cancer Res., 43: 1010, 2002.
34. Park, O. K., Schaefer, T. S., and Nathans, D. In vitro activation of Stat3 by epidermal growth factor receptor kinase. Proc. Natl. Acad. Sci. USA, 93: 13704-13708, 1996.
35. Grandis, J. R., Zeng, Q., and Drenning, S. D. Epidermal growth factor receptor-mediated stat3 signaling blocks apoptosis in head and neck cancer. Laryngoscope, 110: 868-874, 2000.
36. Bao, J., Gur, G., and Yarden, Y. Src promotes destruction of c-Cb1: implications for oncogenic synergy between Src and growth factor receptors. Proc. Natl. Acad. Sci. USA, 100: 2438-2443, 2003.
37. Ewing, W. M., Conti, C., Kruszewski, F. W., Slaga, T. J., and DiGiovanni, J. Tumor progression in SENCAR mouse skin as a function of initiator dose and promoter dose, duration, and type. Cancer Res., 48: 7048-7054, 1988.
38. Fischer, S., O'Connel, F., Conti, C., Tacker, K., Fries, J., Patrick, K., Adams, L., and Slaga, T. Characterization of an inbred strain of the SENCAR mouse that is highly sensitive to phorbol esters, Carcinogenesis (Lond.), 8: 421-424, 1987.
39. Hennings, H., Glick, A. B., Lowry, D. T., Krsmanovic, L. S., Sly, L. M., and Yuspa, S. H. FVB/N mice: an inbred strain sensitive to the chemical induction of squamous cell carcinomas in the skin. Carcinogenesis (Lond.), 14: 2353-2358, 1993.
40. Coghlan, L. G., Gimenez-Conti, I., Kleiner, H. E., Fischer, S. M., Rundhaug, J. E., Conti, C. J., Slaga, T. J., and DiGiovanni, J. Development and initial characterization of several new inbred strains of SENCAR mice for studies of multistage skin carcinogenesis. Carcinogenesis (Lond.), 21: 641-646, 2000.
41. Haas, M., Askari, A., and Xie, Z. Involvement of Src and epidermal growth factor receptor in the signal-transducing function of Na+/K+-ATPase. J. Biol. Chem., 275: 27832-27837, 2000.
42. Yu, C. L., Meyer, D. J., Campbell, G. S., Larner, A. C., Carter-Su, C., Schwartz, J., and Jove, R. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science (Wash. DC), 269. 81-83, 1995.
43. Genda, T., Sakamoto, M., Ichida, T., Asakura, H., and Hirohashi, S. Loss of cell-cell contact is induced by integrin-mediated cell-substratum adhesion in highly-motile and highly-metastatic hepatocellular carcinoma cells. Lab. Investig., 80: 387-394, 2000.
44. Hamaguchi, M., Matsuyoshi, N., Ohnishi, Y., Gotoh, B., Takeichi, M., and Nagai, Y. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO J., 12: 307-314, 1993.
45. Fleming, R. Y., Ellis, L. M., Parikh, N. U., Liu, W., Staley, C. A., and Gallick, G. E. Regulation of vascular endothelial growth factor expression in human colon carcinoma cells by activity of src kinase. Surgery (St. Louis), 122: 501-507, 1997.
46. Munshi, N., Groopman, J. E., Gill, P. S., and Ganju, R. K. c-Src mediates mitogenic signals and associates with cytoskeletal proteins upon vascular endothelial growth factor stimulation in Kaposi's sarcoma cells, J. Immunol., 164: 1169-1174, 2000.
47. Karni, R., Jove, R., and Levitzki, A. Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene, 18: 4654-4662, 1999.
48. Matsumoto, T., Kiguchi, K., Jiang, J., Carbajal, S., Ruffino, L., Beltran, L., Wang, X., Roop, D., and DiGiovanni, J. Development of transgenic mice that inducibly express an active form of c-src in the epidermis. Proc. Am. Assoc. Cancer Res., 43: 1009-1010, 2002.
49. Webster, M. A., Cardiff, R. D., and Muller, W. J. Induction of mammary epithelial hyperplasias and mammary tumors in transgenic mice expressing a murine mammary tumor virus/activated c-src fusion gene. Proc. Natl. Acad. Sci. USA, 92: 7849-7853, 1995.
50. Weissenberger, J., Steinbach, J. P., Malin, G., Spada, S., Rulicke, T., and Aguzzi, A. Development and malignant progression of astrocytomas in GFAP-v-src transgenic mice. Oncogene, 14: 2005-2013, 1997.