Targeted deletion of the TGF-β1 gene causes rapid progression to squamous cell carcinoma

Genes and Development

Volumn 8, Issue 20, 1994, Pages 2429-2440

  Glick, Adam B ^a   Lee, Margo M ^a   Darwiche, Nadine ^a   Kulkarni, Ashok B ^b   Karlsson, Stefan ^b   Yuspa, Stuart H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

fibroblasts; keratinocytes; squamous cell carcinoma; targeted deletion; TGF 1 gene; tumor cell proliferation

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CANCER GENETICS; CANCER GROWTH; CONTROLLED STUDY; FIBROBLAST; GENE DELETION; KERATINOCYTE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE RAS; PAPILLOMA; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA;

ANIMALIA;

EID: 0028171401     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.8.20.2429     Document Type: Article

References (77)

1. Akhurst, R.J., F. Fee, and A. Balmain. 1988. Localized production of TGF-beta mRNA in tumour promoter-stimulated mouse epidermis. Nature 331: 363-365.
2. Aldaz, C.M., C.J. Conti, A.J.P. Klein-Szanto, and T.J. Slaga. 1987. Progressive dysplasia and aneuploidy are hallmarks of mouse skin papillomas: Relevance to malignancy. Proc. Natl. Acad. Sci. 84: 2029-2032.
3. Aldaz, C.M., D. Trono, F. Larcher, T.J. Slaga, and C.J. Conti. 1989. Sequential trisomization of chromosomes 6 and 7 in mouse skin premalignant lesions. Mol Carcinog. 2: 22-26.
4. Arrick, B.A., A.R. Lopez, F. Elfman, R. Ebner, C.H. Damsky, and R. Derynck. 1992. Altered metabolic and adhesive properties and increased tumorigenesis associated with increased expression of transforming growth factor β1. J. Cell Biol. 118: 715-726.
5. Balmain, A., M. Ramsden, G.T. Bowden, and J. Smith. 1984. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature 307: 658-660.
6. Bianchi, A.B., S.M. Fischer, A.I. Robles, E.M. Rinchik, and C.J. Conti. 1993. Overexpression of cyclin D1 in mouse skin carcinogenesis. Oncogene 8: 1127-1133.
7. Bremner, R. and A. Balmain. 1990. Genetic changes in skin tumor progression: Correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell 61:407-117.
8. Buchmann, A., B. Ruggeri, A.J.P. Klein-Szanto, and A. Balmain. 1991. Progression of squamous carcinoma cells to spindle carcinomas of mouse skin is associated with an imbalance of H-ras alleles on chromosome 7. Cancer Res. 51: 4097-4101.
9. Burns, P.A., C.J. Kemp, J.V. Cannon, D.P. Lane, R. Bremner, and A. Balmain. 1991. Loss of heterozygosity and mutational alterations of the p53 gene in skin tumours of interspecific hybrid mice. Oncogene 6: 2363-2369.
10. Chang, H.L., N. Gillett, I. Figari, A.R. Lopez, M.A. Palladino, and R. Derynck. 1993. Increased transforming growth factor β expression inhibits cell proliferation in vitro, yet increases tumorigenicity and tumor growth of Meth A sarcoma cells. Cancer Res. 53: 4391-4398.
11. Coffey, R.J., N.J. Sipes, C.C. Bascom, R. Graves-Deal, C.Y. Pennington, B.E. Weissman, and H.L. Moses. 1988. Growth modulation of mouse keratinocytes by transforming growth factors. Cancer Res. 48: 1596-1602.
12. Cox, K.H., D.V. DeLeon, L.M. Angerer, and R.C. Angerer. 1984. Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev. Biol. 101:485-502.
13. Danielpour, D., L.L. Dart, K.C. Flanders, A.B. Roberts, and M.B. Sporn. 1989. Immunodetection and quantitation of the two forms of transforming growth factor-beta (TGF-beta 1 and TGF-beta 2) secreted by cells in culture. J. Cell Physiol. 138: 79-86.
14. Dennis, P.A. and D.B. Rifkin. 1991. Cellular activation of latent transforming growth factor beta requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc. Natl. Acad. Sci. 88: 580-584.
15. 3 down-modulation in 12-O-tetradecanoylphorbol-13-acetate-induced skin hyperplasia. Cancer Res. 53: 5517-5522.
16. Ewen, M.E., H.K. Sluss, L.L. Whitehouse, and D.M. Livingston. 1993. TGFβ inhibition of Cdk4 synthesis is linked to cell cycle arrest. Cell 74: 1009-1020.
17. Farber, E. 1984. Cellular biochemistry of the stepwise development of cancer with chemicals: G.H.A. Clowes memorial lecture. Cancer Res. 44: 5463-5474.
18. Fearon, E.R. and B. Vogelstein. 1990. A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
19. Flanders, K.C., N.L. Thompson, D.S. Cissel, E. Van Obberghen-Schilling, C.C. Baker, M.E. Kass, L.R. Ellingsworth, A.B. Roberts, and M.B. Sporn. 1989. Transforming growth factor-beta 1 : Histochemical localization with antibodies to different epitopes. J. Cell Biol 108: 653-660.
20. Fowlis, D.J., K.C. Flanders, E. Duffie, A. Balmain, and R.J. Akhurst. 1992. Discordant transforming growth factor β1 RNA and protein localization during chemical carcinogenesis of the skin. Cell Growth Differ. 3: 81-91.
21. Furstenberger, G., M. Rogers, R. Schnapke, G. Bauer, P. Höfler, and F. Marks. 1989. Stimulatory role of transforming growth factors in multistage skin carcinogenesis: Possible explanation for the tumor-inducing effect of wounding in initiated NMRI mouse skin. Int. J. Cancer 43: 915-921.
22. 1 cyclins and cyclin-dependent protein kinases. Proc. Natl. Acad. Sci. 90: 10315-10319.
23. Glick, A.B., D. Danielpour, D. Morgan, M.B. Sporn, and S.H. Yuspa. 1990. Induction and autocrine receptor binding of transforming growth factor-beta during terminal differenti-ation of primary mouse keratinocytes. Mol Endocrinol. 4: 46-52.
24. Glick, A.B., M.B. Sporn, and S.H. Yuspa. 1991. Altered regulation of TGF-β1 and TGF-α in primary keratinocytes and papillomas expressing v-Ha-ras. Mol Carcinog. 4: 210-219.
25. Glick, A.B., A.B. Kulkarni, T. Tennenbaum, H. Hennings, K.C. Flanders, M. O'Reilly, M.B. Sporn, S. Karlsson, and S.H. Yuspa. 1993. 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. 90: 6076-6080.
26. Gomm, J.J., J. Smith, G.K. Ryall, R. Baillie, L. Turnbull, and R.C. Coombes. 1991. Localization of basic fibroblast growth factor and transforming growth factor beta I in the human mammary gland. Cancer Res. 51: 4685-4692.
27. Gorsch, S.M., V.A. Memoli, T.A. Stukel, L.I. Gold, and B.A. Arrick. 1992. Immunohistochemical staining for transforming growth factor β1 associates with disease progression in human breast cancer. Cancer Res. 52: 6949-6952.
28. Greenhalgh, D.A., D.J. Welty, J.E. Strickland, and S.H. Yuspa. 1989. 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.
29. Haddow, S., D.J. Fowlis, K. Parkinson, R.J. Akhurst, and A. Balmain. 1991. Loss of growth control by TGF-beta occurs at a late stage of mouse skin carcinogenesis and is independent of ras gene activation. Oncogene 6: 1465-1470.
30. Hartwell, L. 1992. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71: 543-546.
31. Heine, U.I., E.F. Munoz, K.C. Flanders, A.B. Roberts, and M.B. Sporn. 1990. Colocalization of TGF-beta 1 and collagen 1 and 111, fibronectin and glycosaminoglycans during lung branching morphogenesis. Development 109: 29-36.
32. Hennings, H., D. Michael, C. Cheng, P. Steinert, K. Holbrook, and S.H. Yuspa. 1980. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19: 245-254.
33. Hennings, H., R. Shores, M.L. Wenk, E.F. Spangler, R. Tarone, and S.H. Yuspa. 1983. Malignant conversion of mouse skin tumors is increased by tumor initiators and unaffected by tumor promoters. Nature 304: 67-69.
34. Hennings, H., R. Shores, P. Mitchell, E.F. Spangler, and S.H. Yuspa. 1985. Induction of papillomas with a high probability of conversion to malignancy. Carcinogenesis 6: 1607-1610.
35. Husain, Z., Q.M. Yang, and D.K. Biswas. 1990. cHa-ras protooncogene. Amplification and overexpression in UV-B-induced mouse skin papillomas and carcinomas. Arch. Dermatol. Res. 126: 324-330.
36. Jirtle, R.L., B.I. Carr, and C.D. Scott. 1991. Modulation of insulin-like growth factor-II/mannose 6-phosphate receptors and transforming growth factor-β1 during liver regeneration. J. Biol. Chem. 266: 22444-22450.
37. Jirtle, R.L., J.D. Haag, E.A. Ariazi, and M.N. Gould. 1993. Increased mannose 6-phosphate/insulin-like growth factor II receptor and transforming growth factor β1 levels during monoterpene-induced regression of mammary tumors. Cancer Res. 53: 3849-3852.
38. Kane, C.J., A.M. Knapp, J.N. Mansbridge, and P.C. Hanawalt. 1990. Transforming growth factor-beta 1 localization in normal and psoriatic epidermal keratinocytes in situ. J. Cell Physiol. 144: 144-150.
39. Kane, C.J., P.A. Hebda, J.N. Mansbridge, and P.C. Hanawalt. 1991. Direct evidence for spatial and temporal regulation of transforming growth factor beta 1 expression during cutaneous wound healing. J. Cell Physiol. 148: 157-173.
40. Kanzaki, T., A. Olofsson, A. Moren, C. Wernstedt, U. Hellman, K. Miyazono, L. Claesson-Welsh, and C. Heldin. 1990. TGF-β1 ßl binding protein: A component of the large latent TGF-β1 with multiple repeat sequences. Cell 61: 1051-1061.
41. Kim, S.J., K. Park, D. Koeller, K.Y. Kim, L.M. Wakefield, M.B. Sporn, and A.B. Roberts. 1992. Post-transcriptional regulation of the human transforming growth factor-β1 gene. J. Biol. Chem. 267: 13702-13707.
42. Klein-Szanto, A.J.P., R.G. Nelson, Y. Shah, and T.J. Slaga. 1983. Keratin modifications and GGT activity as indication of tumor progression in skin papillomas. J. Natl. Cancer Inst. 70: 161-168.
43. Koff, A., M. Ohtsuki, K. Polyak, J.M. Roberts, and J. Massague. 1993. Negative regulation of G1 in mammalian cells: Inhibition of cyclin E-dependent kinase by TGF-beta. Science 260: 536-539.
44. Konig, A. and L. Bruckner-Tuderman. 1992. Transforming growth factor-beta stimulates collagen VII expression by cutaneous cells in vitro. J. Cell Biol. 117: 679-685.
45. Krieg, P., R. Schnapke, G. Furstenberger, I. Vogt, and F. Marks. 1991. TGFβ-1- and skin carcinogenesis: Antiproliferative effect in vitro and TGF-β1 mRNA expression during epidermal hyperproliferation and multistage tumorigenesis. Mol. Carcinog. 4: 129-137.
46. Kulkarni, A.B., G.G. Huh, D. Becker, A. Geiser, M. Lyght, K.C. Flanders, A.B. Roberts, M.B. Sporn, J.M. Ward, and S. Karlsson. 1992. Transforming growth factor-β1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl Acad. Sci. 90: 770-774.
47. Laiho, M., J.A. DeCaprio, J.W. Ludlow, D.M. Livingston, and J. Massague. 1990. Growth inhibition by TGF-β linked to suppression of retinoblastoma protein phosphorylation. Cell 62: 175-185.
48. Lankat-Buttgereit, B., M. Kulozik, N. Hunzelmann, and T. Krieg. 1991. Cytokines alter mRNA steady state levels for basement membrane proteins in human skin fibroblasts. J. Dermatol. Sci. 2: 300-307.
49. Larcher, F., C. Bauluz, M. Diaz-Guerra, M. Quintanilla, C.J. Conti, C. Ballestin, and J.L. Jorcano. 1992. Aberrant expression of the simple epithelial type II keratin 8 by mouse skin carcinomas but not papillomas. Mol. Carcinog. 6: 112-121.
50. Lehnert, S.A. and R.J. Akhurst. 1988. Embryonic expression pattern of TGF beta type-1 RNA suggests both paracrine and autocrine mechanisms of action. Development 104: 263-273.
51. Lopez-Casillas, F., J.L. Wrana, and J. Massague. 1993. Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73: 1435-1444.
52. Manning, A.M., A.C. Williams, S.M. Game, and C. Paraskeva. 1991. Differential sensitivity of human colonic adenoma and carcinoma cells to transforming growth factor beta (TGF-beta): Conversion of an adenoma cell line to a tumorigenic phenotype is accompanied by a reduced response to the inhibitory effects of TGF-beta. Oncogene 6: 1471-1476.
53. Matrisian, L.M., G.T. Bowden, P. Krieg, G. Furstenberger, J.P. Briand, P. Leroy, and R. Breathnach. 1986. The mRNA coding for the secreted protease transin is expressed more abundantly in malignant than in benign tumors. Proc. Natl. Acad. Sci. 83:9413-9417.
54. 1 binding protein in human gastrointestinal carcinomas: Qualitative difference between cancer cells and stromal cells. Cancer Res. 53: 183-190.
55. Mizukami, Y., A. Nonomura, T. Yamada, H. Kurumaya, M. Hayashi, N. Koyasaki, T. Taniya, M. Noguchi, S. Nakamura, and F. Matsubara. 1990. Immunohistochemical demonstration of growth factors, TGF-α, TGF-β, IGF-I and neu oncogene product in benign and malignant human breast tissues. Anticancer Res. 10: 1115-1126.
56. Munger, K., J.A. Pietenpol, M.R. Pittelkow, J.T. Holt, and H.L. Moses. 1992. Transforming growth factor beta 1 regulation of c-myc expression, pRB phosphorylation, and cell cycle progression in keratinocytes. Cell Growth Differ. 3: 291-298.
57. Pelton, R.W., B. Saxena, M. Jones, H.L. Moses, and L.I. Gold. 1991. Immunohistochemical localization of TGFβ1, TGFβ2, and TGFβ3 in the mouse embryo: Expression patterns suggest multiple roles during embryonic development. J. Cell Biol. 115: 1091-1105.
58. Pierce, D.F. Jr., M.D. Johnson, Y. Matsui, S.D. Robinson, L.I. Gold, A.F. Purchio, C.W. Daniel, B.L. Hogan, and H.L. Moses. 1993. Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGFβ1. Genes & Dev. 7: 2308-2317.
59. Quintanilla, M., K. Brown, M. Ramsden, and A. Balmain. 1986. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322: 78-80.
60. Roberts A.B. and M.B. Sporn. 1990. The transforming growth factor-βs. In Handbook of experimental pharmacology, Vol. 95/I peptide growth factors and their receptors I (ed. M.B. Sporn and A.B. Roberts), pp. 419-472. Springer-Verlag, New York.
61. Roberts, A.B., M.B. Sporn, R.K. Assoian, J.M. Smith, N.S. Roche, L.M. Wakefield, U.I. Heine, L.A. Liotta, V. Falanga, J.H. Kehrl, and A.S. Fauci. 1986. Transforming growth factor type-β: Rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. 83: 4167-4171.
62. Roop, D.R., D.R. Lowy, P.E. Tambourin, J. Strickland, J.R. Harper, M. Balaschak, E.F. Spangler, and S.H. Yuspa. 1986. An activated Harvey ras oncogene produces benign tumours on mouse epidermal tissue. Nature 323: 822-824.
63. Sellheyer, K., J.R. Bickenbach, J.A. Rothnagel, D. Bundman, M.A. Longley, T. Krieg, N.S. Roche, A.B. Roberts, and D.R. Roop. 1993. Inhibition of skin development by overexpression of transforming growth factor β1 in the epidermis of transgenic mice. Proc. Natl Acad. Sci. 90: 5237-5241.
64. Shipley, G.D., M.R. Pittelkow, J.J. Wille Jr., R.E. Scott, and H.L. Moses. 1986. Reversible inhibition of normal human prokeratinocyte proliferation by type beta transforming growth factor-growth inhibitor in serum-free medium. Cancer Res. 46: 2068-2071.
65. Stamp, G.W., M. Nasim, M. Cardillo, S.G. Sudhindra, E.N. Lalani, and M. Pignatelli. 1993. Transforming growth factor-beta distribution in basal cell carcinomas: Relationship to proliferation index. Br. J. Dermatol 129: 57-64.
66. Steiner, M.S. and E.R. Barrack. 1992. Transforming growth factor-beta 1 overproduction in prostate cancer: Effects on growth in vivo and in vitro. Mol. Endocrinol. 6: 15-25.
67. Sutler, C., J.E. Strickland, D.J. Welty, S.H. Yuspa, H. Winter, and J. Schweizer. 1991. v-Ha-ras-induced mouse skin papillomas exhibit aberrant expression of keratin K13 as do their 7,12-dimethylbenz[a]anthracene/12-0-tetradecanoylphorbol-13-acetate-induced analogues. Mol. Carcinog. 4: 467-476.
68. Tennenbaum, T., S.H. Yuspa, A. Grover, V. Castronovo, M.E. Sobel, Y. Yamada, and L.M. De Luca. 1992. Extracellular matrix receptors and mouse skin carcinogenesis: Altered expression linked to appearance of early markers of tumor progression. Cancer Res, 52: 2966-2976.
69. Tennenbaum, T., A.K. Weiner, A.J. Belanger, A.B. Glick, H. Hennings, and S.H. Yuspa. 1993. The suprabasal expression of α6β4 integrin is associated with a high risk for malignant progression in mouse skin carcinogenesis. Cancer Res. 53: 4803-4810.
70. Wakefield, L.M. and M.B. Sporn. 1990. Suppression of carcinogenesis: A role for TGF-beta and related molecules in prevention of cancer, Immunol. Ser. 51: 217-243.
71. Wakefield, L.M., D.M. Smith, K.C. Flanders, and M.B. Sporn. 1988. Latent transforming growth factor-beta from human platelets. A high molecular weight complex containing precursor sequences. J. Biol. Chem. 263: 7646-7654.
72. Ha oncogene in mouse skin carcinogenesis. Carcinogenesis 12: 1119-1124.
73. Whitby, D.J. and M.W. Ferguson. 1991. Immunohistochemical localization of growth factors in fetal wound healing. Dev. Biol. 147: 207-215.
74. Young W.S. III. 1990. Handbook of chemical neuroanatomy. In Analysis of neuronal microcircuits and synoptic interactions (ed. A. Bjorklund, T. Horkfelt, F.G. Wouterlood, and A.N. Van den Pol), pp. 481-512. Elsevier Science Publishers, B.V. Amsterdam.
75. Yuspa, S.H. 1994. The pathogenesis of squamous cell cancer: Lessons learned from studies of skin carcinogenesis-Thirty-third G.H.A. Clowes Memorial Award Lecture. Cancer Res. 54: 1178-1189.
76. Yuspa, S.H. and M.C. Poirier. 1988. Chemical carcinogenesis: From animal models to molecular models in one decade. Adv. Cancer. Res. 50: 25-70.
77. Zenklusen, J.C., S.L. Stockman, S.M. Fischer, C.J. Conti, and I.B. Gimenez-Conti. 1994. Transforming growth factor-β1 expression in Syrian hamster cheek pouch carcinogenesis. Mol. Carcinog. 9: 10-16.