Transgenic mice overexpressing protein kinase Cε in their epidermis exhibit reduced papilloma burden but enhanced carcinoma formation after tumor promotion

Cancer Research

Volumn 60, Issue 3, 2000, Pages 595-602

  Reddig, Peter J ^a   Dreckschmidt, Nancy E ^a   Zou, Jun ^a   Bourguignon, Sarah E ^a   Oberley, Terry D ^a   Verma, Ajit K ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Health   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; FEMALE; GENE OVEREXPRESSION; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; PAPILLOMA; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SKIN CARCINOMA; TRANSGENIC MOUSE; TUMOR PROMOTION;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; EPIDERMIS; FEMALE; HUMANS; ISOENZYMES; MALE; MICE; MICE, TRANSGENIC; PAPILLOMA; PHENOTYPE; PROTEIN KINASE C; SKIN NEOPLASMS; TETRADECANOYLPHORBOL ACETATE;

EID: 0033951214     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Mellor, H., and Parker, P. J. The extended protein kinase C superfamily. Biochem. J., 332: 281-292, 1998.
2. Newton, A. C. Protein kinase C: structure, function, and regulation. J. Biol. Chem., 270: 28495-28498, 1995.
3. Nishizuka, Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J., 9: 484-496, 1995.
4. Lozano, J., Berra, E., Municio, M. M., Diaz-Meco, M. T., Dominguez, I., Sanz, L., and Moscat, J. Protein kinase Cζ isoform is critical for κB-dependent promoter activation by sphingomyelinase. J. Biol. Chem., 269: 19200-19202, 1994.
5. Baxter, G., Oto, E., Daniel-Issakani, S., and Strulovici, B. Constitutive presence of a catalytic fragment of protein kinase C∈ in a small cell lung carcinoma cell line. J. Biol. Chem., 267: 1910-1917, 1992.
6. Cacace, A. M., Guadagno, S. N., Krauss, R. S., Fabbro, D., and Weinstein, I. B. The ∈ isoform of protein kinase C is an oncogene when overexpressed in rat fibroblasts. Oncogene, 8: 2095-2104, 1993.
7. Mischak, H., Goodnight, J. A., Kolch, W., Martiny-Baron, G., Schaechtle, C., Kazanietz, M. G., Blumberg, P. M., Pierce, J. H., and Mushinski, J. F. Overexpression of protein kinase C-δ and -∈ in NIH 3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J. Biol. Chem., 268: 6090-6096, 1993.
8. Perletti, G. P., Folini, M., Lin, H. C., Mischak, H., Piccinini, F., and Tashjian, A. H., Jr. Overexpression of protein kinase C ∈ is oncogenic in rat colonic epithelial cells. Oncogene, 12: 847-854, 1996.
9. Gubina, E., Rinaudo, M. S., Szallasi, Z., Blumberg, P. M., and Mufson, R. A. Overexpression of protein kinase C isoform ∈ but not δ in human interleukin-3-dependent cells suppresses apoptosis and induces bcl-2 expression. Blood, 91: 823-829, 1998.
10. Ono, Y., Fujii, T., Ogita, K., Kikkawa, U., Igarashi, K., and Nishizuka, Y. The structure, expression, and properties of additional members of the protein kinase C family. J. Biol. Chem., 263: 6927-6932, 1988.
11. DiGiovanni, J. Multistage carcinogenesis in mouse skin. Pharmacol. Ther., 54: 63-128, 1992.
12. Marks, F., and Gschwendt, M. Protein kinase C and skin tumor promotion. Mutat. Res., 333: 161-172, 1995.
13. Fournier, A., and Murray, A. W. Application of phorbol ester to mouse skin causes a rapid and sustained loss of protein kinase C. Nature (Lond.), 350: 767-769, 1987.
14. Hansen, L. A., Monteiro-Riviere, N. A., and Smart, R. C. Differential down-regulation of epidermal protein kinase C by 12-O-tetradecanoylphorbol-13-acetate and diacylglycerol: association with epidermal hyperplasia and tumor promotion. Cancer Res., 50: 5740-5745, 1990.
15. Wang, X. J., Warren, B. S., Rupp, T., Beltran, L. M. and DiGiovanni, J. Loss of mouse epidermal protein kinase C isozyme activities following treatment with phorbol ester and non-phorbol ester tumor promoters. Carcinogenesis (Lond.). 15: 2795-2803, 1994.
16. [6. Verma, A. K., Hsiao, K. M., Ahrens, H., Suganuma, M., Fujiki, H., Matsufuji, S., and Hayashi, H. Superinduction of mouse epidermal ornithine decarboxylase activity by repeated 12-O-tetradecanoylphorbol-13-acetate treatments. Mol. Cell. Biochem., 155: 139-151, 1996.
17. Mills, K. J., Bocckino, S. B., Bums, D. J., Loomis, C. R., and Smart, R. C. Alterations in protein kinase C isozymes α and β II in activated Ha-ras-containing papillomas in the absence of an increase in diacylglycerol. Carcinogenesis (Lond.), 13: 1113-1120, 1992.
18. 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.
19. Vassar, R., Rosenberg, M., Ross, S., Tyner, A., and Fuchs, E. Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice. Proc. Natl. Acad. Sci. USA, 86: 1563-1567, 1989.
20. Kampfer, S., Hellbert, K., Villunger, A., Doppler, W., Baier, G., Grunicke, H. H., and Uberall, F. Transcriptional activation of c-fos by oncogenic Ha-Ras in mouse mammary epithelial cells requires the combined activities of PKC-λ, ∈, and ζ. EMBO J., 17: 4046-4055, 1998.
21. Romanova, L. Y., Alexandrov, I. A., Nordan, R. P., Blagosklonny, M. V., and Mushinski, J. F. Cross-talk between protein kinase C-α (PKC-α) and -δ (PKC-δ): PKC-α elevates the PKC-δ protein level, altering its mRNA transcription and degradation. Biochemistry, 37: 5558-5565, 1998.
22. Bailleul, B., Surani, M. A., White, S., Barton, S. C., Brown, K., Blessing, M., 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.
23. Vassar, R., and Fuchs, E. Transgenic mice provide new insights into the role of TGF-α during epidermal development and differentiation. Genes Dev., 5: 714-727, 1991.
24. Xie, W., Wu, X., Chow, L. T., Chin, E., Paterson, A. J., and Kudlow, J. E. Targeted expression of activated erbB-2 to the epidermis of transgenic mice elicits striking developmental abnormalities in the epidermis and hair follicles. Cell Growth Differ., 9: 313-325, 1998.
25. Arbeit, J. M., Munger, K., Howley, P. M., and Hanahan, D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J. Virol., 68: 4358-4368, 1994.
26. 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 suggest a role for fos in epidermal differentiation and neoplasia. Oncogene, 8: 2145-2157, 1993.
27. Guo, L., Yu, Q. C., and Fuchs, E. Targeting expression of keratinocyte growth factor to keratinocytes elicits striking changes in epithelial differentiation in transgenic mice. EMBO J., 12: 973-986, 1993.
28. Cacace, A. M., Ueffing, M., Philipp, A., Han, E. K., Kolch, W., and Weinstein, I. B. PKC∈ functions as an oncogene by enhancing activation of the Raf kinase. Oncogene, 13: 2517-2526, 1996.
29. Perletti, G. P., Concari, P., Brusaferri, S., Marras, E., Piccinini, F., and Tashjian, A. H., Jr. Protein kinase C∈ is oncogenic in colon epithelial cells by interaction with the ras signal transduction pathway. Oncogene, 16: 3345-3348, 1998.
30. Cai, H., Smola, U., Wixler, V., Eisenmann-Tappe, I., Diaz-Meco, M. T., Moscat, J., Rapp, U., and Cooper, G. M. Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the Raf-1 protein kinase. Mol. Cell. Biol., 17: 732-741, 1997.
31. Han, E. K., Cacace, A. M., Sgambato, A., and Weinstein, I. B. Altered expression of cyclins and c-fos in R6 cells that overproduce PKC∈. Carcinogenesis (Lond.), 16: 2423-2428, 1995.
32. Glick, A. B., Sporn, M. B., and Yuspa, S. H. Altered regulation of TGF-β1 and TGF-α in primary keratinocytes and papillomas expressing v-Ha-ras. Mol. Carcinog., 4: 210-219, 1991.
33. 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.
34. Yamasaki, L., Jacks, T., Bronson, R., Goillot, E., Harlow, E., and Dyson, N. J. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell, 85: 537-548, 1996.
35. Field, S. J., Tsai, F. Y., Kuo, F., Zubiaga, A. M., Kaelin, W. G., Jr., Livingston, D. M., Orkin, S. H., and Greenberg, M. E. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell, 85: 549-561, 1996.
36. Verma, A. K., Conrad, E. A., and Boutwell, R. K. Differential effects of retinoic acid and 7,8-benzoflavone on the induction of mouse skin tumors by the complete carcinogencsis process and by the initiation-promotion regimen. Cancer Res., 42: 3519-3525, 1982.
37. 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 carcinoma. Proc. Natl. Acad. Sci. USA, 87: 643-647, 1990.
38. Ohno, S., Mizuno, K., Adachi, Y., Hata, A., Akita, Y., Akimoto, K., Osada, S., Hirai, S., and Suzuki, K. Activation of novel protein kinases Cδ and C∈ upon mitogenic stimulation of quiescent rat 3Y1 fibroblasts. J. Biol. Chem., 269: 17495-17501, 1994.
39. Hirai, S., Izumi, Y., Higa, K., Kaibuchi, K., Mizuno, K., Osada, S., Suzuki, K., and Ohno, S. Ras-dependent signal transduction is indispensable but not sufficient for the activation of AP1/Jun by PKCδ. EMBO J., 13: 2331-2340, 1994.
40. Ruggeri, B., Caamano, J., Goodrow, T., DiRado, M., Bianchi, A., Trono, D., Conti, C. J., and Klein-Szanto, A. J. Alterations of the p53 tumor suppressor gene during mouse skin tumor progression. Cancer Res., 51: 6615-6621, 1991.
41. Bums, 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 tumours of interspecific hybrid mice. Oncogene, 6: 2363-2369, 1991.
42. 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.
43. Delphin, C. and Baudier, J. The protein kinase C activator, phorbol ester, cooperates with the wild-type p53 species of Ras-transformed embryo fibroblasts growth arrest. J. Biol. Chem., 269: 29579-29587, 1994.
44. Hupp, T. R., and Lane, D. P. Allosteric activation of latent p53 tetramers. Curr. Biol., 4: 865-875, 1994.
45. Yuspa, S, H., Dlugosz, A. A., Cheng, C. K., Denning, M. F., Tennenbaum, T., Glick, A. B., and Weinberg, W. C. Role of oncogenes and tumor suppressor genes in multistage carcinogenesis. J. Investig. Dermatol., 103: 90S-95S, 1994.
46. Glick, A. B., Lee, M. M., Darwiche, N., Kulkarni, A. B., Karlsson, S., and Yuspa, S. H. Targeted deletion of the TGF-β1 gene causes rapid progression to squamous cell carcinoma. Genes Dev., 8: 2429-2440, 1994.
47. Cacace, A. M., Ueffing, M., Han, E. K., Marme, D., and Weinstein, I. B. Overexpression of PKC∈ in R6 fibroblasts causes increased production of active TGFβ. J. Cell. Physiol., 175: 314-322, 1998.