Role of TGFβ signaling in skin carcinogenesis

Microscopy Research and Technique

Volumn 52, Issue 4, 2001, Pages 420-429

  Wang, Xiao Jing ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Smads; TGF receptor; Tumor promoter; Tumor suppressor

Indexed keywords

DISEASES; PATHOLOGY; SIGNALING;

CANCER DEVELOPMENT; CARCINOGENESES; EPITHELIAL CELLS; HOMOEOSTASIS; SIGNALLING PATHWAYS; SKIN CARCINOGENESIS; SMADS; TGFΒ RECEPTOR; TUMOR PROMOTERS; TUMOUR SUPPRESSOR;

TUMORS;

SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

CANCER INVASION; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; PATHOPHYSIOLOGY; SKIN TUMOR;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0035864356     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-0029(20010215)52:4<420::AID-JEMT1027>3.0.CO;2-7     Document Type: Review

References (130)

1. Abdollah S, Macias-Silva M, Tsukazaki T, Hayashi H, Attisano L, Wrana JL. 1997. TbetaRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling. J Biol Chem 272:27678-27685.
2. Akhurst RJ, Fee F, Balmain A. 1988. Localized production of TGF-beta mRNA in tumour promoter-stimulated mouse epidermis. Nature 331:363-365.
3. Amendt C, Schirmacher P, Weber H, Blessing M. 1998. Expression of a dominant negative type ii tgf-beta receptor in mouse skin results in an increase in carcinoma incidence and an acceleration of carcinoma development. Oncogene 17:25-34.
4. Barrett MT, Schutte M, Kern SE, Reid BJ. 1996. Allelic loss and mutational analysis of the DPC4 gene in esophageal adenocarcinoma. Cancer Res 56:4351-4353.
5. Benassi L, Ottani D, Fantini F, Marconi A, Chiodino C, Giannetti A, Pincelli C. 1997. 1,25-dihydroxyvitamin D3, transforming growth factor beta1, calcium, and ultraviolet B radiation induce apoptosis in cultured human keratinocytes. J Invest Dermatol 109:276-282.
6. Bottinger EP, Letterio JJ, Roberts AB. 1997. Biology of TGF-beta in knockout and transgenic mouse models. [Review] [69 refs]. Kidney Int 51:1355-1360.
7. Brodin G, ten Dijke P, Funa K, Heldin CH, Landstrom M. 1999. Increased smad expression and activation are associated with apoptosis in normal and malignant prostate after castration [in process citation]. Cancer Res 59:2731-2738.
8. Brunner AM, Marquardt H, Malacko AR, Lioubin MN, Purchio AF. 1989. Site-directed mutagenesis of cysteine residues in the pro region of the transforming growth factor beta 1 precursor. Expression and characterization of mutant proteins. J Biol Chem 264: 13660-13664.
9. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JV, Markowitz SD, Kinzler KW, Vogelstein B. 1998. Mutations of mitotic checkpoint genes in human cancers. Nature 392:300-303.
10. Carcamo J, Zentella A, Massagué J. 1995. Disruption of transforming growth factor beta signaling by a mutation that prevents transphosphorylation within the receptor complex. Mol Cell Biol 15:1573-1581.
11. Caulin C, Scholl FG, Frontelo P, Gamallo C, Quintanilla M. 1995. Chronic exposure of cultured transformed mouse epidermal cells to transforming growth factor-beta 1 induces an epithelial-mesenchymal transdifferentiation and a spindle tumoral phenotype. Cell Growth Differ 6:1027-1035.
12. Chen F, Weinberg RA. 1995. Biochemical evidence for the autophosphorylation and transphosphorylation of transforming growth factor beta receptor kinases. Proc Natl Acad Sci USA 92:1565-1569.
13. Cui W, Kemp CJ, Duffie E, Balmain A, Akhurst RJ. 1994. Lack of transforming growth factor-beta 1 expression in benign skin tumors of p53null mice is prognostic for a high risk of malignant conversion. Cancer Res 54:5831-5836.
14. Cui W, Fowlis DJ, Cousins FM, Duffie E, Bryson S, Balmain A, Akhurst RJ. 1995. Concerted action of TGF-beta 1 and its type II receptor in control of epidermal homeostasis in transgenic mice. Genes Dev 9:945-955.
15. Cui W, Fowlis DJ, Bryson S, Duffie E, Ireland H, Balmain A, Akhurst RJ. 1996. TGFβeta1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell 86:531-542.
16. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92:5545-5549.
17. Derynck R. 1994. TGF-beta-receptor-mediated signaling. [Review] [50 refs]. Trends Biochem Sci 19:548-553.
18. Derynck R, Zhang Y, Feng XH. 1998. Smads: transcriptional activators of TGF-beta responses. Cell 95:737-740.
19. Devereux TR, Anna CH, Patel AC, White CM, Festing MF, You M. 1997. Smad4 (homolog of human DPC4) and Smad2 (homolog of human JV18-1): candidates for murine lung tumor resistance and suppressor genes. Carcinogenesis 18:1751-1755.
20. DiGiovanni J. 1992. Multistage carcinogenesis in mouse skin. [Review] [761 refs]. PharmacolTher 54:63-128.
21. Eppert K, Scherer SW, Ozcelik H, Pirone R, Hoodless P, Kim H, Tsui LC, Bapat B, Gallinger S, Andrulis IL, Thomsen GH, Wrana JL, Attisano L. 1996. MADR2 maps to 18q21 and encodes a TGFβeta-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86:543-552.
22. Factor VM, Kao CY, Santoni-Rugiu E, Woitach JT, Jensen MR, Thorgeirsson SS. 1997. Constitutive expression of mature transforming growth factor beta1 in the liver accelerates hepatocarcinogenesis in transgenic mice. Cancer Res 57:2089-2095.
23. Feng XH, Filvaroff EH, Derynck R. 1995. Transforming growth factor-beta (TGF-beta)-induced down-regulation of cyclin A expression requires a functional TGF-beta receptor complex. Characterization of chimeric and truncated type I and type II receptors. JBiolChem 270:24237-24245.
24. Filmus J, Kerbel RS. 1993. Development of resistance mechanisms to the growth-inhibitory effects of transforming growth factor-beta during tumor progression. [Review] [56 refs]. Curr Opin Oncol 5:123-129.
25. Fowlis DJ, Flanders KC, Duffie E, Balmain A, Akhurst RJ. 1992. Discordant transforming growth factor beta 1 RNA and protein localization during chemical carcinogenesis of the skin. Cell Growth Differ 3:81-91.
26. Fowlis DJ, Cui W, Johnson SA, Balmain A, Akhurst RJ. 1996. Altered epidermal cell growth control in vivo by inducible expression of transforming growth factor beta 1 in the skin of transgenic mice. Cell Growth Differ 7:679-687.
27. Frank S, Hubner G, Breier G, Longaker MT, Greenhalgh DG, Werner S. 1995. Regulation of vascular endothelial growth factor expression in cultured keratinocytes. Implications for normal and impaired wound healing. J Biol Chem 270:12607-12613.
28. Furue M, Kato M, Nakamura K, Nashiro K, Kikuchi K, Okochi H, Miyazono K, Tamaki K. 1997. Dysregulated expression of transforming growth factor beta and its type-1 and type-II receptors in basal-cell carcinoma. Int J Cancer 71:505-509.
29. Fynan TM, Reiss M. 1993. Resistance to inhibition of cell growth by transforming growth factor-beta and its role in oncogenesis. [Review] [211 refs]. Crit Rev Oncog 4:493-540.
30. Glick AB, Sporn MB, Yuspa SH. 1991. Altered regulation of TGF-beta 1 and TGF-alpha in primary keratinocytes and papillomas expressing v-Ha-ras. Mol Carcinog 4:210-219.
31. Glick AB, Kulkarni AB, Tennenbaum T, Hennings H, Flanders KC, O'Reilly M, Sporn MB, Karlsson S, Yuspa SH. 1993. Loss of expression of transforming growth factor beta in skin and skin tumors is associated with hyperproliferation and a high risk for malignant conversion. Proc Natl Acad Sci USA 90:6076-6080.
32. Glick AB, Lee MM, Darwiche N, Kulkarni AB, Karlsson S, Yuspa SH. 1994. Targeted deletion of the TGF-beta 1 gene causes rapid progression to squamous cell carcinoma. Genes Dev 8:2429-2440.
33. Glick AB, Weinberg WC, Wu IH, Quan W, Yuspa SH. 1996. Transforming growth factor beta 1 suppresses genomic instability independent of a G1 arrest, p53, and Rb [published erratum appears in Cancer Res 1997 May 15;5710.:2079]. Cancer Res 56: 3645-3650.
34. Glick A, Popescu N, Alexander V, Ueno H, Bottinger E, Yuspa SH. 1999. Defects in transforming growth factor-beta signaling cooperate with a Ras oncogene to cause rapid aneuploidy and malignant transformation of mouse keratinocytes. Proc Natl Acad Sci USA 96:14949-14954.
35. Go C, Li P, Wang XJ. 1999. Blocking transforming growth factor beta signaling in transgenic epidermis accelerates chemical carcinogenesis: a mechanism associated with increased angiogenesis [In Process Citation]. Cancer Res 59:2861-2868.
36. Go C, He W, Zhong L, Li P, Huang J, Brinkley BR, Wang XJ. 2000. Aberrant cell cycle progression contributes to the early-stage accelerated carcinogenesis in transgenic epidermis expressing the dominant negative TGFβRII. Oncogene (in press).
37. Greenhalgh DA, Wang XJ, Donehower LA, Roop DR. 1996. Paradoxical tumor inhibitory effect of p53 loss in transgenic mice expressing epidermal-targeted v-rasHa, v-fos, or human transforming growth factor alpha. Cancer Res 56:4413-4423.
38. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE. 1996. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. [see comments]. Science 271:350-353.
39. Hannon GJ, Beach D. 1994. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest [see comments]. Nature 371: 257-261.
40. He W, Cao T, Smith DA, Myers TE, Wang XJ. 2001. Smads mediate signaling of the TGFβ superfamily in normal keratinocytes but are lost during skin chemical carcinogenesis. Oncogene, in press.
41. Heckmann M, Aumailley M, Chu ML, Timpl R, Krieg T. 1992. Effect of transforming growth factor-beta on collagen type VI expression in human dermal fibroblasts. FEBS Lett 310:79-82.
42. Hejlik DP, Kottickal LV, Liang H, Fairman J, Davis T, Janecki T, Sexton D, Perry W, Tavtigian SV, Teng DH, Nagarajan L. 1997. Localization of SMAD5 and its evaluation as a candidate myeloid tumor suppressor. Cancer Res 57:3779-3783.
43. Hoodless PA, Wrana JL. 1998. Mechanism and function of signaling by the TGF beta superfamily. [Review] [160 refs]. Curr Top Microbiol Immunol 228:235-272.
44. Hoque AT, Hahn SA, Schutte M, Kern SE. 1997. DPC4 gene mutation in colitis associated neoplasia. Gut 40:120-122.
45. Hsu S, Huang F, Hafez M, Winawer S, Friedman E. 1994. Colon carcinoma cells switch their response to transforming growth factor beta 1 with tumor progression. Cell Growth Differ 5:267-275.
46. Iacopetta BJ, Welch J, Soong R, House AK, Zhou XP, Hamelin R. 1998. Mutation of the transforming growth factor-beta type II receptor gene in right-sided colorectal cancer: relationship to clinicopathological features and genetic alterations. J Pathol 184:390-395.
47. Imai Y, Tsurutani N, Oda H, Inoue T, Ishikawa T. 1998. Genetic instability and mutation of the TGF-beta-receptor-II gene in ampullary carcinomas. Int J Cancer 76:407-411.
48. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. 1997. Smad6 inhibits signalling by the TGF-beta superfamily [see comments]. Nature 389:622-626.
49. Iozzo RV. 1995. Tumor stroma as a regulator of neoplastic behavior. Agonistic and antagonistic elements embedded in the same connective tissue [editorial]. Lab Invest 73:157-160.
50. Ishisaki A, Yamato K, Nakao A, Nonaka K, Ohguchi M, ten Dijke P, Nishihara T. 1998. Smad7 is an activin-inducible inhibitor of activin-induced growth arrest and apoptosis in mouse B cells. J Biol Chem 273:24293-24296.
51. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H, Nishihara T. 1999. Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem 274:13637-13642.
52. Jonson T, Gorunova L, Dawiskiba S, Andren-Sandberg A, Stenman G, ten Dijke P, Johansson B, Hoglund M. 1999. Molecular analyses of the 15q and 18q SMAD genes in pancreatic cancer [In Process Citation]. Genes Chromosomes Cancer 24:62-71.
53. Kawabata M, Miyazono K. 1999. Signal transduction of the TGF-beta superfamily by Smad proteins. J Biochem (Tokyo) 125:9-16.
54. Kong XT, Choi SH, Inoue A, Xu F, Chen T, Takita J, Yokota J, Bessho F, Yanagisawa M, Hanada R, Yamamoto K, Hayashi Y. 1997. Expression and mutational analysis of the DCC, DPC4, and MADR2/JV18-1 genes in neuroblastoma. Cancer Res 57:3772-3778.
55. Kordon EC, McKnight RA, Jhappan C, Hennighausen L, Merlino G, Smith GH. 1995. Ectopic TGF beta 1 expression in the secretory mammary epithelium induces early senescence of the epithelial stem cell population. Dev Biol 168:47-61.
56. Krieg P, Schnapke R, Furstenberger G, Vogt I, Marks F. 1991. TGF-beta 1 and skin carcinogenesis: antiproliferative effect in vitro and TGF-beta 1 mRNA expression during epidermal hyperproliferation and multistage tumorigenesis. Mol Carcinog 4:129-137.
57. Lange D, Persson U, Wollina U, ten Dijke P, Castelli E, Heldin CH, Funa K. 1999. Expression of TGF-beta related smad proteins in human epithelial skin tumors [In Process Citation]. Int J Oncol 14:1049-1056.
58. Letterio JJ, Roberts AB. 1997. TGF-beta: a critical modulator of immune cell function. [Review] [61 refs]. Clin ImmunolImmunopathol 84:244-250.
59. Li CY, Suardet L, Little JB. 1995. Potential role of WAF1/Cip1/p21 as a mediator of TGF-beta cytoinhibitory effect. J Biol Chem 270: 4971-4974.
60. Li JM, Nichols MA, Chandrasekharan S, Xiong Y, Wang XF. 1995. Transforming growth factor beta activates the promoter of cyclin-dependent kinase inhibitor p15INK4B through an Sp1 consensus site. J Biol Chem 270:26750-26753.
61. Li JM, Datto MB, Shen X, Hu PC, Yu Y, Wang XF. 1998. SP1, but not SP3, functions to mediate promoter activation by TGF-beta through canonical SP1 binding sites. Nucleic Acids Res 26:2449-2456.
62. Liu F, Hata A, Baker JC, Doody J, Carcamo J, Harland RM, Massagué J. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator [see comments]. Nature 381:620-623.
63. Liu X, Sun Y, Constantinescu SN, Karam E, Weinberg RA, Lodish HF. 1997. Transforming growth factor beta-induced phosphorylation of Smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc Natl Acad Sci U S A 94:10669-10674.
64. Lu SL, Akiyama Y, Nagasaki H, Saitoh K, Yuasa Y. 1995. Mutations of the transforming growth factor-beta type II receptor gene and genomic instability in hereditary nonpolyposis colorectal cancer. Biochem Biophys Res Commun 216:452-457.
65. Lu SL, Kawabata M, Imamura T, Akiyama Y, Nomizu T, Miyazono K, Yuasa Y. 1998. HNPCC associated with germline mutation in the TGF-beta type II receptor gene [letter]. Nat Genet 19:17-18.
66. MacDougall JR, Matrisian LM. 1995. Contributions of tumor and stromal matrix metalloproteinases to tumor progression, invasion and metastasis. Cancer Metast Rev 14:351-362.
67. Markowitz S, Wang J, Myeroff L, Parsons R, Sun L, Lutterbaugh J, Fan RS, Zborowska E, Kinzler KW, Vogelstein B. 1995. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability [see comments]. Science 268:1336-1338.
68. Massagué J. 1998. TGF-beta signal transduction. Annu Rev Biochem 67:753-791.
69. Miyaki M, Iijima T, Konishi M, Sakai K, Ishii A, Yasuno M, Hishima T, Koike M, Shitara N, Iwama T, Utsunomiya J, Kuroki T, Mori T. 1999. Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis. Oncogene 18:3098-3103.
70. Moskaluk CA, Kern SE. 1996. Cancer gets Mad: DPC4 and other TGFβeta pathway genes in human cancer. Biochim Biophys Acta 1288:M31-M33.
71. Moskaluk CA, Hruban RH, Schutte M, Lietman AS, Smyrk T, Fusaro L, Fusaro R, Lynch J, Yeo CJ, Jackson CE, Lynch HT, Kern SE. 1997. Genomic sequencing of DPC4 in the analysis of familial pancreatic carcinoma. Diagn Mol Pathol 6:85-90.
72. Myeroff LL, Parsons R, Kim SJ, Hedrick L, Cho KR, Orth K, Mathis M, Kinzler KW, Lutterbaugh J, Park K. 1995. A transforming growth factor beta receptor type II gene mutation common in colon and gastric but rare in endometrial cancers with microsatellite instability. Cancer Res 55:5545-5547.
73. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. 1997a. Identification of Smad7, a TGFβeta-inducible antagonist of TGF-beta signalling [see comments]. Nature 389:631-635.
74. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P. 1997b. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362.
75. Nakayama T, Snyder MA, Grewal SS, Tsuneizumi K, Tabata T, Christian JL. 1998. Xenopus smad8 acts downstream of bmp-4 to modulate its activity during vertebrate embryonic patterning. Development 125:857-867.
76. Navarro P, Gomez M, Pizarro A, Gamallo C, Quintanilla M, Cano A. 1991. A role for the E-cadherin cell-cell adhesion molecule during tumor progression of mouse epidermal carcinogenesis. J Cell Biol 115:517-533.
77. Newman MJ. 1993. Transforming growth factor beta and the cell surface in tumor progression. Cancer Metast Rev 12:239-254.
78. Padgett RW, Cho SH, Evangelista C. 1998. Smads are the central-component in transforming growth factor-beta signaling [Review]. Pharmacol Ther 78:47-52.
79. Patamalai B, Burow DL, Gimenez-Conti I, Zenklusen JC, Conti CJ, Klein-Szanto AJ, Fischer SM. 1994. Altered expression of transforming growth factor-beta 1 mRNA and protein in mouse skin carcinogenesis. Mol Carcinog 9:220-229.
80. Pepper MS. 1997. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. [Review] [242 refs]. Cytokine Growth Factor Rev 8:21-43.
81. Pierce DFJ, Gorska AE, Chytil A, Meise KS, Page DL, Coffey RJJ, Moses HL. 1995. Mammary tumor suppression by transforming growth factor beta 1 transgene expression. Proc Natl Acad Sci USA 92:4254-4258.
82. Pietenpol JA, Holt JT, Stein RW, Moses HL. 1990a. Transforming growth factor beta 1 suppression of c-myc gene transcription: role in inhibition of keratinocyte proliferation. Proc Natl Acad Sci USA 87:3758-3762.
83. Pietenpol JA, Stein RW, Moran E, Yaciuk P, Schlegel R, Lyons RM, Pittelkow MR, Munger K, Howley PM, Moses HL. 1990b. TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 61:777-785.
84. Pittelkow MR, Coffey RJJ, Moses HJ. 1988. Keratinocytes produce and are regulated by transforming growth factors. [Review] [83 refs]. Ann NY Acad Sci 548:211-224.
85. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massagué J, Roberts JM, Koff A. 1994. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8:9-22.
86. Portella G, Cumming SA, Liddell J, Cui W, Ireland H, Akhurst RJ, Balmain A. 1998. Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion. Cell Growth Differ 9:393-404.
87. Reynisdottir I, Polyak K, Iavarone A, Massagué J. 1995. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev 9:1831-1845.
88. Roberts AB, Sporn MB. 1989. Regulation of endothelial cell growth, architecture, and matrix synthesis by TGF-beta. Am Rev Respir Dis 140:1126-1128.
89. Roberts AB, Sporn MB. 1993. Physiological actions and clinical applications of transforming growth factor-beta (TGF-beta). [Review] [990 refs]. Growth Factors 8:1-9.
90. Roberts AB, McCune BK, Sporn MB. 1992. TGF-beta: regulation of extracellular matrix. [Review] [23 refs]. Kidney Int 41:557-559.
91. Rozenblum E, Schutte M, Goggins M, Hahn SA, Panzer S, Zahurak M, Goodman SN, Sohn TA, Hruban RH, Yeo CJ, Kern SE. 1997. Tumor-suppressive pathways in pancreatic carcinoma. Cancer Res 57:1731-1734.
92. Rundhaug JE, Park J, Fischer SM. 1997a. Uncoordinated regulation of mRNA expression of the three isoforms of transforming growth factor-beta in the mouse skin carcinogenesis model. Mol Carcinog 18:115-126.
93. Rundhaug JE, Park J, Pavone A, Opdenakker G, Fischer SM. 1997b. Opposite effect of stable transfection of bioactive transforming growth factor-beta 1 (TGF beta 1) versus exogenous TGF beta 1 treatment on expression of 92-kDa type IV collagenase in mouse skin squamous cell carcinoma CH72 cells. Mol Carcinog 19:122-136.
94. Satterwhite DJ, Moses HL. 1994. Mechanisms of transforming growth factor-beta 1-induced cell cycle arrest. [Review] [69 refs]. Invas Metast 14:309-318.
95. Schmid P, Itin P, Rufli T. 1996. In situ analysis of transforming growth factors-beta (TGF-beta 1, TGF- beta 2, TGF-beta 3. and TGF-beta type II receptor expression in basal cell carcinomas. Br J Dermatol 134:1044-1051.
96. Schutte M, Hruban RH, Hedrick L, Cho KR, Nadasdy GM, Weinstein CL, Bova GS, Isaacs WB, Cairns P, Nawroz H, Sidransky D, Casero RAJ, Meltzer PS, Hahn SA, Kern SE. 1996. DPC4 gene in various tumor types. Cancer Res 56:2527-2530.
97. Sehgal I, Baley PA, Thompson TC. 1996. Transforming growth factor beta1 stimulates contrasting responses in metastatic versus primary mouse prostate cancer-derived cell lines in vitro. Cancer Res 56:3359-3365.
98. Sellheyer K, Bickenbach JR, Rothnagel JA, Bundman D, Longley MA, Krieg, Roche NS, Roberts AB, Roop DR. 1993. Inhibition of skin development by overexpression of transforming growth factor beta 1 in the epidermis of transgenic mice. Proc Natl Acad Sci U S A 90:5237-5241.
99. Shaw LM, Rabinovitz I, Wang HH, Toker A, Mercurio AM. 1997. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell 91:949-960.
100. Sherman JH, Miller ML, Albert RE, Baxter CS. 1993. Dose- and time-dependent expression of transforming growth factor-beta 1 mRNA and protein in mouse epidermis and papillomas after repeated topical application of benzo[a]pyrene. Mol Carcinog 8:264-271.
101. Shi Y, Hata A, Lo RS, Massagué J, Pavletich NP. 1997. A structural basis for mutational inactivation of the tumour suppressor Smad4 [see comments]. Nature 388:87-93.
102. Souchelnytskyi S, Nakayama T, Nakao A, Moren A, Heldin CH, Christian JL, ten Dijke P. 1998. Physical and functional interaction of murine and Xenopus Smad7 with bone morphogenetic protein receptors and transforming growth factor- beta receptors. J Biol Chem 273:25364-25370.
103. Sporn MB, Roberts AB. 1992. Transforming growth factor-beta: recent progress and new challenges. [Review] [50 refs]. J Cell Biol 119:1017-1021.
104. Tada H, Hatoko M, Muramatsu T, Shirai T. 1996. Expression of E-cadherin in skin carcinomas. J Dermatol 23:104-110.
105. Takagi Y, Kohmura H, Futamura M, Kida H, Tanemura H, Shimokawa K, Saji S. 1996. Somatic alterations of the DPC4 gene in human colorectal cancers in vivo [see comments]. Gastroenterology 111:1369-1372.
106. Takenoshita S, Tani M, Nagashima M, Hagiwara K, Bennett WP, Yokota J, Harris CC. 1997. Mutation analysis of coding sequences of the entire transforming growth factor beta type II receptor gene in sporadic human colon cancer using genomic DNA and intron primers. Oncogene 14:1255-1258.
107. Talts JF, Weller A, Timpl R, Ekblom M, Ekblom P. 1995. Regulation of mesenchymal extracellular matrix protein synthesis by transforming growth factor-beta and glucocorticoids in tumor stroma. J Cell Sci 108:2153-2162.
108. Tang B, Bottinger EP, Jakowlew SB, Bagnall KM, Mariano J, Anver MR, Letterio JJ, Wakefield LM. 1998. Transforming growth factor-β-1 is a new form of tumor suppressor with true haploid insufficiency. Nat Med 4:802-807.
109. Tennenbaum T, Yuspa SH, Grover A, Castronovo V, Sobel ME, Yamada Y, De Luca LM. 1992. Extracellular matrix receptors and mouse skin carcinogenesis: altered expression linked to appearance of early markers of tumor progression. Cancer Res 52:2966-2976.
110. Tennenbaum T, Weiner AK, Belanger AJ, Glick AB, Hennings H, Yuspa SH. 1993. The suprabasal expression of alpha 6 beta 4 integrin is associated with a high risk for malignant progression in mouse skin carcinogenesis. Cancer Res 53:4803-4810.
111. Topley GI, Okuyama R, Gonzales JG, Conti C, Dotto GP. 1999. p21(WAF1/Cip1) functions as a suppressor of malignant skin tumor formation and a determinant of keratinocyte stem-cell potential. Proc Natl Acad Sci USA 96:9089-9094.
112. Uchida K, Nagatake M, Osada H, Yatabe Y, Hondo M, Mitsudomi T, Masuda A, Takahashi T. 1996. Somatic in vivo alterations of the JV18-1 gene at 18q21 in human lung cancers. Cancer Res 56:5583-5585.
113. Ueda T, Komiya A, Emi M, Suzuki H, Shiraishi T, Yatani R, Masai M, Yasuda K, Ito H. 1997. Allelic losses on 18q21 are associated with progression and metastasis in human prostate cancer. Genes Chromosomes Cancer 20:140-147.
114. Varga J, Jimenez SA. 1986. Stimulation of normal human fibroblast collagen production and processing by transforming growth factor-beta. Biochem Biophys Res Commun 138:974-980.
115. Venkatasubbarao K, Ahmed MM, Swiderski C, Harp C, Lee EY, McGrath P, Mohiuddin M, Strodel W, Freeman JW. 1998. Novel mutations in the polyadenine tract of the transforming growth factor beta type II receptor gene are found in a subpopulation of human pancreatic adenocarcinomas. Genes Chromosomes Cancer 22:138-144.
116. Waikel RL, Wang XJ, Roop DR. 1999. Targeted expression of c-Myc in the epidermis alters normal proliferation, differentiation and UV-B induced apoptosis. Oncogene 18:4870-4878.
117. Wang D, Song H, Evans JA, Lang JC, Schuller DE, Weghorst CM. 1997a. Mutation and downregulation of the transforming growth factor beta type II receptor gene in primary squamous cell carcinomas of the head and neck. Carcinogenesis 18:2285-2290.
118. Wang XJ, Greenhalgh DA, Bickenbach JR, Jiang A, Bundman DS, Krieg T, Derynck R, Roop DR. 1997b. Expression of a dominant-negative type II transforming growth factor beta (TGF-beta) receptor in the epidermis of transgenic mice blocks TGF-beta-mediated growth inhibition. Proc Natl Acad Sci USA 94:2386-2391.
119. Wang XJ, Greenhalgh DA, Jiang AB, He DC, Zhong L, Medina D, Brinkley BR, Roop DR. 1998. Expression of a p53 mutant in the epidermis of transgenic mice accelerates chemical carcinogenesis. Oncogene 17:35-45.
120. Wang XJ, Liefer KM, Tsai SY, O'Malley BW, Roop DR. 1999. Development of gene-switch transgenic mice that inducibly express transforming growth factor β1 in the epidermis. Proc Natl Acad Sci USA 96:8483-8488.
121. Wang Y, O'Malley BWJ, Tsai SY, O'Malley BW. 1994. A regulatory system for use in gene transfer. Proc Natl Acad Sci USA 91:8180-8184.
122. Wang Y, DeMayo FJ, Tsai SY, O'Malley BW. 1997a. Ligand-inducible and liver-specific target gene expression in transgenic mice. Nat Biotechnol 15:239-243.
123. Wang Y, Xu J, Pierson T, O'Malley BW, Tsai SY. 1997b. Positive and negative regulation of gene expression in eukaryotic cells with an inducible transcriptional regulator. Gene Ther 4:432-441.
124. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. 1994. Mechanism of activation of the TGF-beta receptor. Nature 370:341-347.
125. Wright JA, Turley EA, Greenberg AH. 1993. Transforming growth factor beta and fibroblast growth factor as promoters of tumor progression to malignancy. [Review] [192 refs]. Crit Rev Oncog 4:473-492.
126. Yanagisawa K, Osada H, Masuda A, Kondo M, Saito T, Yatabe Y, Takagi K, Takahashi T. 1998. Induction of apoptosis by Smad3 and down-regulation of Smad3 expression in response to TGF-beta in human normal lung epithelial cells. Oncogene 17:1743-1747.
127. Yingling JM, Datto MB, Wong C, Frederick JP, Liberati NT, Wang XF. 1997. Tumor suppressor Smad4 is a transforming growth factor beta-inducible DNA binding protein. Mol Cell Biol 17:7019-7028.
128. Zavadil J, Brezinova J, Svoboda P, Zemanova Z, Michalova K. 1997. Smad5, a tumor suppressor candidate at 5q31.1, is hemizygously lost and not mutated in the retained allele in human leukemia cell line HL60. Leukemia 11:1187-1192.
129. Zhang Y, Feng X, We R, Derynck R. 1996. Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383:168-172.
130. Zhu Y, Richardson JA, Parada LF, Graff JM. 1998. Smad3 mutant mice develop metastatic colorectal cancer. Cell 94:703-714.