Enhanced sensitivity to tumor growth and development in multistage skin carcinogenesis by transforming growth factor-α-induced epidermal growth factor receptor activation but not p53 inactivation

Molecular Carcinogenesis

Volumn 18, Issue 3, 1997, Pages 160-170

  Shibata, Masa Aki ^a   Ward, Jerrold M ^a   Green, Jeffrey E ^a   Merlino, Glenn ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Epidermal growth factor receptor; Ha ras; p53; Transforming growth factor ; Tyrosine phosphorylation

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; EPIDERMAL GROWTH FACTOR RECEPTOR; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN P53; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; NONHUMAN; PAPILLOMA; PHOSPHORYLATION; PRIORITY JOURNAL; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; TUMOR GROWTH;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CLONING, MOLECULAR; EXONS; GENES, P53; HUMANS; MICE; MICE, TRANSGENIC; PAPILLOMA; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT PROTEINS; SKIN; SKIN NEOPLASMS; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMALIA; MUS MUSCULUS;

EID: 0030932620     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2744(199703)18:3<160::AID-MC5>3.0.CO;2-J     Document Type: Article

References (43)

1. Marquardt H, Hunkapiller MW, Hood LE, Todaro GJ. Rat transforming growth factor type 1 structure and relation to epidermal growth factor. Science 223:1079-1082, 1984.
2. Massagué J. Transforming growth factor-α: A model for membrane-anchored growth factors. J Biol Chem 265:21393-21396, 1990.
3. Brachmann R, Lindquist PB, Nagashima M, et al. Transmembrane TGF-α precursors activate EGF/TGF-α receptors. Cell 56:691-700, 1989.
4. Wong ST, Winchell LF, McCune BK, et al. The TGF-α precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 56:495-506, 1989.
5. Cohen S, Carpenter G, King L. Epidermal growth factor receptor protein kinase interactions. J Biol Chem 255:4834-4842, 1980.
6. Ushiro H, Cohen S. Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A431 cell membranes. J Biol Chem 255:8363-8365, 1980.
7. Cohen S, Ushiro H, Stoscheck C, Gill GN. Regulation of the epidermal growth factor by phosphorylation. J Cell Biochem 29:195-208, 1985.
8. Yamamoto T, Nishida T, Miyajima M, Kawai S, Ooi T, Toyoshima K. The erb B gene of avian erythroblastosis virus is a member of the src gene family. Cell 35:71-78, 1983.
9. DiGiovanni J. Multistage carcinogenesis in mouse skin. Pharmacol Ther 54:63-128, 1992.
10. Yuspa SH. 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, 1994.
11. Pittelkow MR, Lindquist PB, Abraham RT, Graves-Deal R, Derynck R, Coffey RJ. Induction of transforming growth factor-α expression in human keratmocytes by phorbol esters. J Biol Chem 264:5164-5171, 1989.
12. Imamoto A, Beltrán LM, DiGiovanni J. Evidence for autocrine/paracrine growth stimulation by transforming growth factor-α during the process of skin tumor promotion. Mol Carcinog 4:52-60, 1991.
13. Finzi E, Kilkenny A, Strickland JE, et al. TGFα stimulates growth of skin papillomas by autocrine and paracrine mechanisms but does not cause neoplastic progression. Mol Carcinog 1:7-12, 1988.
14. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGFα overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61:1137-1146, 1990.
15. Takagi H, Jhappan C, Sharp R, Merlino G. Hypertrophic gastropathy resembling Menetrier's disease in transgenic mice overexpressing transforming growth factor α in the stomach. J Clin Invest 90:1161-1167, 1992.
16. Lee G-H, Merlino G, Fausto N. Development of liver tumors in transforming growth factor α transgenic mice. Cancer Res 52:5162-5170, 1992.
17. Jhappan C, Takayama H, Dickson RB, Merlino G. Transgenic mice provide genetic evidence that transforming growth factor α promotes skin tumorigenesis via Ha-Ras-dependent and H-Ras-independent pathway. Cell Growth Differ 5:385-394, 1994.
18. Matsui Y, Halter SA, Holt JT, Hogan BLM, Coffey RJ. Development of mammary hyperplasia and neoplasia in MMTV-TGFα transgenic mice. Cell 61:1147-1155, 1990.
19. Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF-α in transgenic mice: Induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61:1121-1135, 1990.
20. Sandgren EP, Luetteke NC, Qiu TH, Palmiter RD, Brinster RL, Lee DC. Transforming growth factor α dramatically enhances oncogene-induced carcinogenesis in transgenic mouse pancreas and liver. Mol Cell Biol 13:320-330, 1993.
21. Vassar R, Hutton ME, Fuchs E. Transgenic overexpression of transforming growth factor α bypasses the need for c-Ha-ras mutations in mouse skin tumorigenesis. Mol Cell Biol 12:4643-4653, 1992.
22. Wang X-J, Greenhalgh DA, Eckhardt JN, Rothnagel JA, Roop DR. 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.
23. Tamano S, Merlino GT, Ward JM. Rapid development of hepatic tumors in transforming growth factor α transgenic mice associated with increased cell proliferation in precancerous hepatocellular lesions initiated by N-nitrosodiethylamine and promoted by phenobarbital. Carcinogenesis 15:1791-1798, 1994.
24. Quintanilla M, Brown K, Ramsden M, Balmain A. Carcinogenspecific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322:78-80, 1986.
25. Bizub D, Wood AW, Skalka AM. Mutagenesis of the Ha-ras oncogene in mouse skin tumors induced by polycyclic aromatic hydrocarbons. Proc Natl Acad Sci USA 83:6048-6052, 1986.
26. Roop DR, Lowy DR, Tambourin PE, et al. An activated Harvey ras oncogene produces benign tumors on mouse epidermal tissue. Nature 323:822-824, 1986.
27. Ha gene into keratinocytes derived from carcinogen-induced mouse papillomas causes malignant progression. Mol Cell Biol 6:3144-3149, 1986.
28. Glick AB, Sporn MB, Yuspa SH. Altered regulation of TGFβ1 and TGFα in primary keratinocytes and papillomas expressing v-Ha-ras. Mol Carcinog 4:210-219, 1991.
29. Burns PA, Kemp CJ, Gannon JV, Lane DP, Bremner R, Balmain A. Loss of heterozygosity and mutational alterations of the p53 gene in the skin tumours of interspecific hybrid mice. Oncogene 6:2363-2369, 1991.
30. Ruggeri B, Caamano J, Goodrow T, et al. Alterations of the p53 tumor suppressor gene during mouse skin tumor progression. Cancer Res 51:6615-6621, 1991.
31. Guide for Care and Use of Laboratory Animals. NIH Publication No. 82-23, National Institutes of Health, Bethesda, MD, 1985.
32. Onta M, Youichi S, Sekiya T, Hayashi K. Rapid sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics 5:874-879, 1989.
33. Aldaz CM, Conti CJ, Klein-Szanto AJP, Slaga TJ. Progressive dysplasia and aneuploidy are hallmarks of mouse skin papillomas: Relevance to malignancy. Proc Natl Acad Sci USA 84:2029-2032, 1987.
34. Gentry LE, Twardzik DR, Lim GJ, Ranchalis JE, Lee DC. Expression and characterization of transforming growth factor α precursor protein in transfected mammalian cells. Mol Cell Biol 7:1585-1591, 1987.
35. Rho O, Beltrán LM, Gimenez-Conti IB, DiGiovanni J. Altered expression of the epidermal growth factor receptor and transforming growth factor-α during multistage skin carcinogenesis in SENCAR mice. Mol Carcinog 11:19-28, 1994.
36. Ha-induced epidermal neoplasia: Potential involvement of alternate epidermal growth factor receptor ligands. Cancer Res 55:1883-1893, 1995.
37. Anklesaria P, Texidó J, Laiho M, Pierce JH, Greenberger JS, Massagué J. Cell-cell adhesion mediated by binding of membrane-anchored transforming growth factor α to epidermal growth factor receptors promotes cell proliferation. Proc Natl Acad Sci USA 87:3289-3293, 1990.
38. Bertrics PJ, Gill GN. Self-phosphorylation enhances the protein-tyrosine kinase activity by the epidermal growth factor receptor. J Biol Chem 260:14642-14647, 1985.
39. Gerwin BI, Spillare E, Forrester K, et al. Mutant p53 can induce tumorigenic conversion of human bronchial epithelial cells and reduce their responsiveness to a negative growth factor β1. Proc Natl Acad Sci USA 89:2759-2763, 1992
40. Reiss M, Sartorelli AC. Regulation of growth and differentiation of human keratinocytes by type β transforming factor and epidermal growth factor. Cancer Res 47: 6705-6709, 1987.
41. Kemp CJ, Donehower LA, Bradley A, 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.
42. Mitsunaga SI, Zhang SY, Ruggeri BA, Gimenez-Conti I, Robles AI. Positive immunohistochemical staining of p53 and cyclin D in advanced mouse skin tumors, but not in precancerous lesions produced by benzo[a]pyrene. Carcinogenesis 16:1629-1635, 1995.
43. Ruggen B, DiRado M, Zhang SY, Bauer B, Goodrow T. Benzo[a]pyrene-induced murine skin tumors exhibit frequent and characteristic G to T mutations in the p53 gene. Proc Natl Acad Sci USA 90:1013-1017, 1993.