Blocking transforming growth factor β signaling in transgenic epidermis accelerates chemical carcinogenesis: A mechanism associated with increased angiogenesis

Cancer Research

Volumn 59, Issue 12, 1999, Pages 2861-2868

  Go, Cindy ^a   Li, Ping ^a   Wang, Xiao Jing ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LORICRIN; PHORBOL 13 ACETATE 12 MYRISTATE; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER SUSCEPTIBILITY; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; EPIDERMIS; GENE MUTATION; IMMUNOFLUORESCENCE; METASTASIS; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PAPILLOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; TRANSGENIC MOUSE;

ANIMALS; CARCINOGENS; EPIDERMIS; GENES, RAS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE; MICE, TRANSGENIC; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; PAPILLOMA; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0033564547     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Bottinger, E. P., Letterio, J. J., and Roberts, A. B. Biology of TGF-β in knockout and transgenic mouse models. Kidney Int., 51: 1355-1360, 1997.
2. Roberts, A. B., and Sporn, M. B. Physiological actions and clinical applications of transforming growth factor-β (TGF-β). Growth Factors, 8: 1-9, 1993.
3. Sellheyer, K., Bickenbach, J. R., Rothnagel, J. A., Bundman, D., Longley, M. A., Krieg, 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. Sci. USA, 90: 5237-5241, 1993.
4. Cui, W., Fowlis, D. J., Cousins, F. M., Duffie, E., Bryson, S., Balmain, A., and Akhurst, R. J. Concerted action of TGF-β1 and its type II receptor in control of epidermal homeostasis in transgenic mice. Genes Dev., 9: 945-955, 1995.
5. Filmus, J., and Kerbel, R. S. Development of resistance mechanisms to the growth-inhibitory effects of transforming growth factor-β during tumor progression. Curr. Opin. Oncol., 8: 123-129, 1993.
6. Fynan, T. M., and Reiss, M. Resistance to inhibition of cell growth by transforming growth factor-β and its role in oncogenesis. Crit. Rev. Oncog., 4: 493-540, 1993.
7. Satterwhite, D. J., and Moses, H. L. Mechanisms of transforming growth factor-β1-induced cell cycle arrest. Invasion Metastasis, 14: 309-318, 1994.
8. 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.
9. 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.
10. Pierce, D. F. J., Gorska, A. E., Chytil, A., Meise, K. S., Page, D. L., Coffey, R. J. J., and Moses, H. L. Mammary tumor suppression by transforming growth factor β1 transgene expression. Proc. Natl. Acad. Sci. USA, 92: 4254-4258, 1995.
11. Tang, B., Bottinger, E. P., Jakowlew, S. B., Bagnall, K. M., Mariano, J., Anver, M. R., Letterio, J. J., and Wakefield, L. M. Transforming growth factor-β-1 is a new form of tumor suppressor with true haploid insufficiency. Nat. Med., 4: 802-807, 1998.
12. Cui, W., Fowlis, D. J., Bryson, S., Duffie, E., Ireland, H., Balmain, A., and Akhurst, R. J. TGF-β1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell, 86: 531-542, 1996.
13. Factor, V. M., Kao, C-Y., Santoni-Rugiu, E., Woitach, J. T., Jensen, M.R., and Thorgeirsson, S. S. Constitutive expression of mature transforming growth factor β1 in the liver accelerates hepatocarcinogenesis in transgenic mice. Cancer Res., 57: 2089-2095, 1997.
14. Wright, J. A., Turley, E. A., and Greenberg, A. H. Transforming growth factor β and fibroblast growth factor as promoters of tumor progression to malignancy. Crit. Rev. Oncog., 4: 473-492, 1993.
15. Derynck, R. TGF-β-receptor-mediated signaling. Trends Biochem. Sci., 19: 548-553, 1994.
16. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F., and Massague, J. Mechanism of activation of the TGF-β receptor. Nature (Lond.), 370: 341-347, 1994.
17. Chen, F., and Weinberg, R. A. Biochemical evidence for the autophosphorylation and transphosphorylation of transforming growth factor β receptor kinases. Proc. Natl. Acad. Sci. USA, 92: 1565-1569, 1995.
18. Feng, X. H., Filvaroff, E. H., and Derynck, R. Transforming growth factor-β (TGF-β)-induced down-regulation of cyclin A expression requires a functional TGF-β receptor complex. Characterization of chimeric and truncated type I and type II receptors. J. Biol. Chem., 270: 24237-24245, 1995.
19. Chen, R. H., Ebner, R., and Derynck, R. Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science (Washington DC), 260: 1335-1338, 1993.
20. Wieser, R., Attisano, L., Wrana, J. L., and Massague, J. Signaling activity of transforming growth factor β type II receptors lacking specific domains in the cytoplasmic region. Mol. Cell. Biol., 13: 7239-7247, 1993.
21. Wang, X. J., Greenhalgh, D. A., Bickenbach, J. R., Jiang, A., Bundman, D. S., Krieg, T., Derynck, R., and Roop, D. R. Expression of a dominant-negative type II transforming growth factor β (TGF-β) receptor in the epidermis of transgenic mice blocks TGF-β-mediated growth inhibition. Proc. Natl. Acad. Sci. USA, 94: 2386-2391, 1997.
22. Bottinger, E. P., Jakubczak, J. L., Roberts, I. S., Mumy, M., Hemmati, P., Bagnall, K., Merlino, G., and Wakefield, L. M. Expression of a dominant-negative mutant TGF-β type II receptor in transgenic mice reveals essential roles for TGF-β in regulation of growth and differentiation in the exocrine pancreas. EMBO J., 16: 2621-2633, 1997.
23. Gorska, A. E., Joseph, H., Derynck, R., Moses, H. L., and Serra, R. Dominant-negative interference of the transforming growth factor β type II receptor in mammary gland epithelium results in alveolar hyperplasia and differentiation in virgin mice. Cell Growth Differ., 9: 229-238, 1998.
24. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Fan, R. S., Zborowska, E., Kinzler, K. W., and Vogelstein, B. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science (Washington DC), 268: 1336-1338, 1995.
25. Myeroff, L. L., Parsons, R., Kim, S-J., Hedrick, L., Cho, K. R., Orth, K., Mathis, M., Kinzler, K. W., Lutterbaugh, J., Park, K., Bang, Y-J., Lee, H. W., Park, J-G., Lynch, H. T., Roberts, A. R., Vogelstein, B., and Markowitz, S. D. A transforming growth factor β receptor type II gene mutation common in colon and gastric but rare in endometrial cancers with microsatellite instability. Cancer Res., 55: 5545-5547, 1995.
26. Carcamo, J., Zentella, A., and Massague, J. Disruption of transforming growth factor β signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol. Cell. Biol., 15: 1573-1581, 1995.
27. Takenoshita, S., Tani, M., Nagashima, M., Hagiwara, K., Bennett, W. P., Yokota, J., and Harris, C. C. Mutation analysis of coding sequences of the entire transforming growth factor β type II receptor gene in sporadic human colon cancer using genomic DNA and intron primers. Oncogene, 14: 1255-1258, 1997.
28. Iacopetta, B. J., Welch, J., Soong, R., House, A. K., Zhou, X. P., and Hamelin, R. Mutation of the transforming growth factor-β type II receptor gene in right-sided colorectal cancer: relationship to clinicopathological features and genetic alterations. J. Pathol., 184: 390-395, 1998.
29. Lu, S. L., Kawabata, M., Imamura, T., Akiyama, Y., Nomizu, T., Miyazono, K., and Yuasa, Y. HNPCC associated with germline mutation in the TGF-β type II receptor gene. Nat. Genet., 19: 17-18, 1998.
30. Lu, S. L., Akiyama, Y., Nagasaki, H., Saitoh, K., and Yuasa, Y. Mutations of the transforming growth factor-β type II receptor gene and genomic instability in hereditary nonpolyposis colorectal cancer. Biochem. Biophys. Res. Commun., 216: 452-457, 1995.
31. Wang, D., Song, H., Evans, J. A., Lang, J. C., Schuller, D. E., and Weghorst, C. M. Mutation and down-regulation of the transforming growth factor β type II receptor gene in primary squamous cell carcinomas of the head and neck. Carcinogenesis (Lond.), 18: 2285-2290, 1997.
32. Imai, Y., Tsurutani, N., Oda, H., Inoue, T., and Ishikawa, T. Genetic instability and mutation of the TGF-β-receptor-II gene in ampullary carcinomas. Int. J. Cancer, 76: 407-411, 1998.
33. Venkatasubbarao, K., Ahmed, M. M., Swiderski, C., Harp, C., Lee, E. Y., McGrath, P., Mohiuddin, M., Strodel, W., and Freeman, J. W. Novel mutations in the polyadenine tract of the transforming growth factor β type II receptor gene are found in a subpopulation of human pancreatic adenocarcinomas. Genes Chromosomes Cancer, 22: 138-144, 1998.
34. Wang, X. J., Greenhalgh, D. A., Jiang, A. B., He, D. C., Zhong, L., Medina, D., Brinkley, B. R., and Roop, D. R. Expression of a p53 mutant in the epidermis of transgenic mice accelerates chemical carcinogenesis. Oncogene, 17: 35-45, 1998.
35. Bolontrade, M. F., Stern, M. C., Binder, R. L., Zenklusen, J. C., Gimenez-Conti, I. B., and Conti, C. J. Angiogenesis is an early event in the development of chemically induced skin tumors. Carcinogenesis (Lond.), 19: 2107-2113, 1998.
36. 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 1 47-kDa keratin, K13, normally associated with terminal differentiation of internal stratified epithelia. Mol. Carcinog., 1: 96-108, 1988.
37. DiGiovanni, J. Multistage carcinogenesis in mouse skin. Pharmacol. Ther., 54: 63-128, 1992.
38. Jhappan, C., Takayama, H., Dickson, R. B., and Merlino, G. Transgenic mice provide genetic evidence that transforming growth factor α promotes skin tumorigenesis via H-Ras-dependent and H-Ras-independent pathways. Cell Growth Differ., 5: 385-394, 1994.
39. 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 tumours of interspecific hybrid mice. Oncogene, 6: 2363-2369, 1991.
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. Charpin, C., Devictor, B., Bergeret, D., Andrac, L., Boulat, J., Horschowski, N., Lavaut, M. N., and Piana, L. CD31 quantitative immunocytochemical assays in breast carcinomas: correlation with current prognostic factors. Am. J. Clin. Pathol., 103: 443-448, 1995.
42. Claffey, K. P., and Robinson, G. S. Regulation of VEGF/VPF expression in tumor cells: consequences for tumor growth and metastasis. Cancer Metastasis Rev., 15: 165-176, 1996.
43. Dameron, K. M., Volpert, O. V., Tainsky, M. A., and Bouck, N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science (Washington DC), 265: 1582-1584, 1994.
44. Akhurst, R. J., Fee, F., and Balmain, A. Localized production of TGF-β mRNA in tumour promoter-stimulated mouse epidermis. Nature (Lond.), 331: 363-365, 1988.
45. Amendt, C., Schirmacher, P., Weber, H., and Blessing, M. Expression of a dominant negative type II TGF-β receptor in mouse skin results in an increase in carcinoma incidence and an acceleration of carcinoma development. Oncogene, 17: 25-34, 1998.
46. 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.
47. Bottinger, E. P., Jakubczak, J. L., Haines, D. C., Bagnall, K., and Wakefield, L. M. Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor β receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res., 57: 5564-5570, 1997.
48. Wang, X. J., Greenhalgh, D. A., Eckhardt, J. N., Rothnagel, J. A., and Roop, D. R. Epidermal expression of transforming growth factor-α in transgenic mice: induction of spontaneous and 12-O-tetradecanoylphorbol-13-acetate-induced papillomas via a mechanism independent of Ha-ras activation or overexpression. Mol. Carcinog., 10: 15-22, 1994.
49. Ha, v-fos, or human transforming growth factor α. Cancer Res., 56: 4413-4423, 1996.
50. Pepper, M. S. Transforming growth factor-β: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev., 8: 21-43, 1997.
51. Frank, S., Hubner, G., Breier, G., Longaker, M. T., Greenhalgh, D. G., and Wemer, S. Regulation of vascular endothelial growth factor expression in cultured keratinocytes: implications for normal and impaired wound healing. J. Biol. Chem., 270: 12607-12613, 1995.
52. Pertovaara, L., Kaipainen, A., Mustonen, T., Orpana, A., Ferrara, N., Saksela, O., and Alitalo, K. Vascular endothelial growth factor is induced in response to transforming growth factor-β in fibroblastic and epithelial cells. J. Biol. Chem., 269: 6271-6274, 1994.
53. Sankar, S., Mahooti-Brooks, N., Bensen, L., McCarthy, T. L., Centrella, M., and Madri, J. A. Modulation of transforming growth factor β receptor levels on microvascular endothelial cells during in vitro angiogenesis. J. Clin. Invest., 97: 1436-1446, 1996.
54. Kieser, A., Weich, H. A., Brandner, G., Marme, D., and Kolch, W. Mutant p53 potentiates protein kinase C induction of vascular endothelial growth factor expression. Oncogene, 9: 963-969, 1994.
55. 172H mutant or p53 knockout transgenic mice following chemical carcinogenesis: evidence for a gain-of-function. Mol. Carcinog., 23: 185-192, 1998.