Transgenic coexpression of v-Ha-ras and transforming growth factor α increases epidermal hyperproliferation and tumorigenesis and predisposes to malignant conversion via endogenous c-Ha-ras activation

Molecular Carcinogenesis

Volumn 27, Issue 3, 2000, Pages 200-209

  Wang, Xiao Jing ^a   Greenhalgh, David A ^b   Roop, Dennis R ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Carcinogenesis; Growth factor; Oncogene; Skin; Transgenic

Indexed keywords

COMPLEMENTARY DNA; GROWTH FACTOR; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN P53; RNA; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; EPIDERMIS CELL; GENE EXPRESSION; GENE MUTATION; GENOTYPE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE C H RAS; PAPILLOMA; PHENOTYPE; PRIORITY JOURNAL; SKIN CANCER; SKIN CARCINOGENESIS; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; DNA PRIMERS; EPIDERMIS; GENE EXPRESSION REGULATION; GENES, P53; GENES, RAS; MICE; MICE, TRANSGENIC; MUTATION; PAPILLOMA; SKIN NEOPLASMS; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMALIA; MUS MUSCULUS; UNIDENTIFIED AGENTS;

EID: 0034017757     PISSN: 08991987     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2744(200003)27:3<200::AID-MC7>3.0.CO;2-9     Document Type: Article

References (46)

1. Greenhalgh DA, Roop DR. Dissecting molecular carcinogenesis: Development of transgenic mouse models by epidermal gene targeting. Adv Cancer Res 1994;64:247-296.
2. Greenhalgh DA, Rothnagel JA, Quintanilla MI, et al. Induction of epidermal hyperplasia, hyperkeratosis, and papillomas in transgenic mice by a targeted v-Ha-ras oncogene. Mol Carcinog 1993;7:99-110.
3. Dominey AM, Wang XJ, King LEJ, et al Targeted over-expression of transforming growth factor alpha in the epidermis of transgenic mice elicits hyperplasia, hyperkeratosis, and spontaneous, squamous papillomas. Cell Growth Differ 1993;4:1071-1082.
4. Greenhalgh DA, Rothnagel JA, Wang XJ, et al. 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 1993;8: 2145-2157.
5. 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 1994;54:1178-1189.
6. Greenhalgh DA, Quintanilla Ml, Orengo CC, et al. Cooperation between v-fos and v-rasHA induces autonomous papillomas in transgenic epidermis but not malignant conversion. Cancer Res 1993;53:5071-5075.
7. Wang XJ, Greenhalgh DA, Lu XR, Bickenbach JR, Roop DR. TGF alpha and v-fos cooperation in transgenic mouse epidermis induces aberrant keratinocyte differentiation and stable, autonomous papillomas. Oncogene 1995;10: 279-289.
8. Wang XJ, Greenhalgh DA, Eckhardt JN, Rothnagel JA, Roop DR. Epidermal expression of transforming growth factor-alpha 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 1994;10:15-22.
9. Vassar R, Fuchs E. Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation. Genes Dev 1991;5:714-727.
10. Vassar R, Hutton ME, Fuchs E. Transgenic overexpression of transforming growth factor alpha bypasses the need for c-Ha-ras mutations in mouse skin tumorigenesis. Mol Cell Biol 1992;12:4643-4653.
11. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGF alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990;61: 1137-1146.
12. Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC. Overexpression of TGF alpha in transgenic mice: Induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 1990;61:1121-1135.
13. Matsui Y, Halter SA, Holt JT, Hogan BL, Coffey RJ. Development of mammary hyperplasia and neoplasia in MMTV-TGF alpha transgenic mice. Cell 1990;61:1147-1155.
14. Harper JR, Roop DR, Yuspa SH. Transfection of the EJ rasHa gene into keratinocytes derived from carcinogen-induced mouse papillomas causes malignant progression. Mol Cell Biol 1986;6:3144-3149.
15. Brissette JL, Missero C, Yuspa SH, Dotto GP. Different levels of v-Ha-ras p21 expression in primary keratinocytes transformed with Harvey sarcoma virus correlate with benign versus malignant behavior. Mol Carcinog 1993;7: 21-25.
16. Greenhalgh DA, Welty DJ, Strickland JE, Yuspa SH. Spontaneous Ha-ras gene activation in cultured primary murine keratinocytes: Consequences of Ha-ras gene activation in malignant conversion and malignant progression. Mol Carcinog 1989;2:199-207.
17. Bremner R, Balmam A. Genetic changes in skin tumor progression: Correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell 1990;61:407-417.
18. Bianchi AB, Aldaz CM, Conti CJ. Nonrandom duplication of the chromosome bearing a mutated Ha-ras-1 allele in mouse skin tumors. Proc Natl Acad Sci USA 1990:87: 6902-6906.
19. DiGiovanni J. Multistage carcinogenesis in mouse skin. Pharmacol Ther 1992;54:63-128.
20. Pittelkow MR, Lindquist PB, Abraham RT, Graves-Deal R, Derynck R, Coffey RJ, Jr. Induction of transforming growth factor-alpha expression in human keratinocytes by phorbol esters. J Biol Chem 1989;264:5164-5171.
21. Imamoto A, Beltran LM, DiGiovanni J. Evidence for autocrine/paracrine growth stimulation by transforming growth factor-alpha during the process of skin tumor promotion. Mol Carcinog 1991;4:52-60.
22. Furstenberger G, Rogers M, Schnapke R, Bauer G, Hofler, Marks F. 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 1989;43:915-921.
23. Finzi E, Kilkenny A, Strickland JE, et al. TGF alpha stimulates growth of skin papillomas by autocrine and paracrine mechanisms but does not cause neoplastic progression. Mol Carcinog 1988;1:7-12.
24. Glick AB, Sporn MB, Yuspa SH. Altered regulation of TGF-beta 1 and TGF-alpha in primary keratinocytes and papillomas expressing v-Ha-ras. Mol Carcinog 1991;4: 210-219.
25. Jhappan C, Takayama H, Dickson RB, Merlino G. Transgenic mice provide genetic evidence that transforming growth factor alpha promotes skin tumorigenesis via H-ras-dependent and H-ras-independent pathways. Cell Growth Differ 1994;5:385-394.
26. Quintanilla M, Brown K, Ramsden M, Balmain A. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 1986;322:78-80.
27. Wong ST, Winchell LF, McCune BK, et al. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 1989;56:495-506.
28. Buday L, Downward J. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor. Cell 1993;73:611-620.
29. Gale NW, Kaplan S, Lowenstein EJ, Schlessinger J, Bar-Sagi D. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 1993;363:88-92.
30. Dlugosz AA, Cheng C, Williams EK, et al. Autocrine transforming growth factor alpha is dispensible for v-ras-Ha-induced epidermal neoplasia: potential involvement of alternate epidermal growth factor receptor ligands. Cancer Res 1995;55:1883-1893.
31. Yuspa SH, Hawley-Nelson P, Stanley JR, Hennings H. Epidermal cell culture. Transplant Proc 1980;12:114-122.
32. Aldaz CM, Conti CJ, Klein-Szanto AJ, Slaga TJ. Progressive dysplasia and aneuploidy are hallmarks of mouse skin papillomas: Relevance to malignancy. Proc Natl Acad Sci USA 1987;84:2029-2032.
33. Greenhalgh DA, Wang XJ, Eckhardt JN, Roop DR. 12-o-tetradecanoylphorbol-13-acetate promotion of transgenic mice expressing epidermal-targeted v-fos induces rasHA-activated papillomas and carcinomas without p53 mutation: association of v-fos expression with promotion and tumor autonomy. Cell Growth Differ 1995; 6:579-586.
34. Roop DR, Huitfeldt H, Kilkenny A, Yuspa SH. Regulated expression of differentiation-associated keratins in cultured epidermal cells detected by monospecific antibodies to unique peptides of mouse epidermal keratins. Differentiation 1987;35:143-150.
35. Huitfeldt HS, Heyden A, Clausen OP, Thrane EV, Roop D, Yuspa SH. Altered regulation of growth and expression of differentiation-associated keratins in benign mouse skin tumors. Carcinogenesis 1991;12:2063-2067.
36. Mehrel T, Hohl D, Rothnagel JA, et al. Identification of a major keratinocyte cell envelope protein, loricrin. Cell 1990;61:1103-1112.
37. Rothnagel JA, Mehrel T, Idler WW, Roop DR, Steinert PM. The gene for mouse epidermal filaggrin precursor. Its partial characterization, expression, and sequence of a repeating filaggrin unit. J Biol Chem 1987;262:15643-15648.
38. Weiss RA, Eichner R, Sun TT. Monoclonal antibody analysis of keratin expression in epidermal diseases: A 48-and 56-kdalton keratin as molecular markers for hyperproliferative keratinocytes. J Cell Biol 1984;98:1397-1406.
39. Nischt R, Roop DR, Mehrel T, et al. 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 1988;1:96-108.
40. Pelling JC, Neades R, Strawhecker J. Epidermal papillomas and carcinomas induced in uninitiated mouse skin by tumor promoters alone contain a point mutation in the 61st codon of the Ha-ras oncogene. Carcinogenesis 1988;9:665-667.
41. Sutter C, Greenhalgh DA, Ueda M, et al. SENCAR mouse skin tumors produced by promotion alone have A to G mutations in codon 61 of the c-rasHa gene. Carcinogenesis 1994;15:1975-1978.
42. Lowy DR, Willumsen BM. Function and regulation of ras. Annu Rev Biochem 1993;62:851-891.
43. Lange-Carter CA, Pleiman CM, Gardner AM, Blumer KJ, Johnson GL. A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf. Science 1993;260:315-319.
44. Shuai K, Stark GR, Kerr IM, Darnell JE, Jr. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma. Science 1993;261:1744-1746.
45. Fu XY, Zhang JJ. Transcription factor p91 interacts with the epidermal growth factor receptor and mediates activation of the c-fos gene promoter. Cell 1993;74:1135-1145.
46. Dlugosz AA, Hansen L, Cheng C, et al. Targeted disruption of the epidermal growth factor receptor impairs growth of squamous papillomas expressing the v-ras(Ha) oncogene but does not block in vitro keratinocyte responses to oncogenic ras. Cancer Res 1997;57:3180-3188.