Use of a TGFβ type I receptor inhibitor in mouse skin carcinogenesis reveals a dual role for TGFβ signaling in tumor promotion and progression

Carcinogenesis

Volumn 31, Issue 12, 2010, Pages 2127-2135

  Markell, Lauren Mordasky ^a   Pérez Lorenzo, Rolando ^a,b   Masiuk, Katelyn E ^a   Kennett, Mary J ^a   Glick, Adam B ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; CYTOKERATIN 1; CYTOKERATIN 18; PHORBOL 13 ACETATE 12 MYRISTATE; RAS PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; 1,3 DIOXOLANE DERIVATIVE; 4 (5 BENZO(1,3)DIOXOL 5 YL 4 PYRIDIN 2 YL 1H IMIDAZOL 2 YL)BENZAMIDE; 4-(5-BENZO(1,3)DIOXOL-5-YL-4-PYRIDIN-2-YL-1H-IMIDAZOL-2-YL)BENZAMIDE; BENZAMIDE DERIVATIVE; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; TGF BETA TYPE I RECEPTOR; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DIFFERENTIATION; CONTROLLED STUDY; EPIDERMIS CELL; GENE INDUCTION; MOUSE; NONHUMAN; PAPILLOMA; PHENOTYPE; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SKIN INFLAMMATION; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; DISEASE COURSE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; ONCOGENE RAS; PHYSIOLOGY; SKIN TUMOR;

ANIMALS; BENZAMIDES; DIOXOLES; DISEASE PROGRESSION; GENES, RAS; MICE; PAPILLOMA; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; SMAD2 PROTEIN; TETRADECANOYLPHORBOL ACETATE; TRANSFORMING GROWTH FACTOR BETA1;

EID: 78649796293     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgq191     Document Type: Article

References (50)

1. Massague,J. (1998) TGF-beta signal transduction. Annu. Rev. Biochem., 67, 753-791.
2. Callahan,J.F. et al. (2002) Identification of novel inhibitors of the transforming growth factor beta1 (TGF-beta1) type 1 receptor (ALK5). J. Med. Chem., 45, 999-1001.
3. Inman,G.J. et al. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol., 62, 65-74.
4. Laping,N.J. et al. (2002) Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: sB-431542. Mol. Pharmacol., 62, 58-64.
5. Halder,S.K. et al. (2005) A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia, 7, 509-521.
6. Tojo,M. et al. (2005) The ALK-5 inhibitor A-83-01 inhibits Smad signaling and epithelial-to-mesenchymal transition by transforming growth factor-beta. Cancer Sci., 96, 791-800.
7. Uhl,M. et al. (2004) SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res., 64, 7954-7961.
8. Ge,R. et al. (2006) Inhibition of growth and metastasis of mouse mammary carcinoma by selective inhibitor of transforming growth factor-beta type I receptor kinase in vivo. Clin. Cancer Res., 12, 4315-4330.
9. Suzuki,E. et al. (2007) A novel small-molecule inhibitor of transforming growth factor beta type I receptor kinase (SM16) inhibits murine mesothelioma tumor growth in vivo and prevents tumor recurrence after surgical resection. Cancer Res., 67, 2351-2359.
10. Rausch,M.P. et al. (2009) An orally active small molecule TGF-beta receptor I antagonist inhibits the growth of metastatic murine breast cancer. Anticancer Res., 29, 2099-2109.
11. Hasegawa,T. et al. (2005) SB-431542 inhibits TGF-beta-induced contraction of collagen gel by normal and keloid fibroblasts. J. Dermatol. Sci., 39, 33-38.
12. Chen,Y. et al. (2006) Contribution of activin receptor-like kinase 5 (transforming growth factor beta receptor type I) signaling to the fibrotic phenotype of scleroderma fibroblasts. Arthritis Rheum., 54, 1309-1316.
13. Grygielko,E.T. et al. (2005) Inhibition of gene markers of fibrosis with a novel inhibitor of TGF{beta}-type I receptor kinase in puromycininduced nephritis. J. Pharmacol. Exp. Ther., 313, 943-951.
14. Petersen,M. et al. (2008) Oral administration of GW788388, an inhibitor of TGF-beta type I and II receptor kinases, decreases renal fibrosis. Kidney Int., 73, 705-715.
15. Bian,Y. et al. (2009) Progressive tumor formation in mice with conditional deletion of TGF-beta signaling in head and neck epithelia is associated with activation of the PI3K/Akt pathway. Cancer Res., 69, 5918-5926.
16. Mincione,G. et al. (2008) Loss of expression of TGF-beta1, TbetaRI, and TbetaRII correlates with differentiation in human oral squamous cell carcinomas. Int. J. Oncol., 32, 323-331.
17. Honjo,Y. et al. (2007) TGF-beta receptor I conditional knockout mice develop spontaneous squamous cell carcinoma. Cell Cycle, 6, 1360-1366.
18. Guasch,G. et al. (2007) Loss of TGFbeta signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia. Cancer Cell, 12, 313-327.
19. 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.
20. Yuspa,S.H. (1998) The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis. J. Dermatol. Sci., 17, 1-7.
21. Cui,W. et al. (1996) TGFβ1 inhibits the formation of benign skin tumors, but enhances progression to invasive spindle carcinomas in transgenic mice. Cell, 86, 531-542.
22. Blessing,M. et al. (1995) Chemical skin carcinogenesis is prevented in mice by the induced expression of a TGF-β related transgene. Teratog. Carcinog. Mutagen., 15, 11-21.
23. Pérez-Lorenzo,R. et al. (2010) Transforming growth factor {beta}1 enhances tumor promotion in mouse skin carcinogenesis. Carcinogenesis, 31, 1116-1123.
24. Li,A.G. et al. (2004) Smad3 knockout mice exhibit a resistance to skin chemical carcinogenesis. Cancer Res., 64, 7836-7845.
25. Glick,A.B. (2004) TGFbeta1, back to the future: revisiting its role as a transforming growth factor. Cancer Biol. Ther., 3, 276-283.
26. Jaubert,J. et al. (2004) Tetracycline-regulated transactivators driven by the involucrin promoter to achieve epidermal conditional gene expression. J. Invest. Dermatol., 123, 313-318.
27. Chin,L. et al. (1999) Essential role for oncogenic Ras in tumour maintenance. Nature, 400, 468-472.
28. Roop,D.R. et al. (1988) Transcriptional control of high molecular weight keratin gene expression in multistage mouse skin carcinogenesis. Cancer Res., 48, 3245-3252.
29. Cheng,C. et al. (1990) The v-ras oncogene inhibits the expression of differentiation markers and facilitates expression of cytokeratins 8 and 18 in mouse keratinocytes. Mol. Carcinog., 3, 363-373.
30. Pizza,F.X. et al. (2005) Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. J. Physiol., 562, 899-913.
31. Rozen,S. et al. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol., 132, 365-386.
32. Afrakhte,M. et al. (1998) Induction of inhibitory Smad6 and Smad7 mRNA by TGF-beta family members. Biochem. Biophys. Res. Commun., 249, 505-511.
33. Brodin,G. et al. (2000) Efficient TGF-beta induction of the Smad7 gene requires cooperation between AP-1, Sp1, and Smad proteins on the mouse Smad7 promoter. J. Biol. Chem., 275, 29023-29030.
34. Akhurst,R.J. et al. (1988) Localized production of TGF-beta mRNA in tumour promoter-stimulated mouse epidermis. Nature, 331, 363-365.
35. Glick,A. et al. (2007) The high-risk benign tumor: evidence from the twostage skin cancer model and relevance for human cancer. Mol. Carcinog., 46, 605-610.
36. Nischt,R. et al. (1988) Aberrant expression during two-stage mouse skin carcinogenesis of type I 47-kDa Keratin, K13, normally associated with terminal differentiation of internal stratified epithelia. Mol. Carcinog., 1, 96-108.
37. Larcher,F. et al. (1992) Aberrant expression of the simple epithelial type II keratin 8 by mouse skin carcinomas but not papillomas. Mol. Carcinog., 6, 112-121.
38. Fillies,T. et al. (2006) Cytokeratin 8/18 expression indicates a poor prognosis in squamous cell carcinomas of the oral cavity. BMC Cancer, 6, 10.
39. Laping,N.J. et al. (2007) Tumor-specific efficacy of transforming growth factor-beta RI inhibition in Eker rats. Clin. Cancer Res., 13, 3087-3099.
40. Go,C. et al. (1999) Blocking transforming growth factor b signaling in transgenic epidermis accelerates chemical carcinogenesis: a mechanism associated with increased angiogenesis. Cancer Res., 59, 2861-2868.
41. Lu,S.L. et al. (2006) Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev., 20, 1331-1342.
42. de Visser,K.E. et al. (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell, 7, 411-423.
43. Balkwill,F. et al. (2004) Cancer: an inflammatory link. Nature, 431, 405-406.
44. Reibman,J. et al. (1991) Transforming growth factor beta 1, a potent chemoattractant for human neutrophils, bypasses classic signal-transduction pathways. Proc. Natl Acad. Sci. USA, 88, 6805-6809.
45. Brandes,M.E. et al. (1991) Type I transforming growth factor-beta receptors on neutrophils mediate chemotaxis to transforming growth factor-beta. J. Immunol., 147, 1600-1606.
46. Amendt,C. et al. (1998) 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.
47. Go,C. et al. (2000) Aberrant cell cycle progression contributes to the earlystage accelerated carcinogenesis in transgenic epidermis expressing the dominant negative TGFbetaRII. Oncogene, 19, 3623-3631.
48. Darwiche,N. et al. (2007) Expression profile of skin papillomas with high cancer risk displays a unique genetic signature that clusters with squamous cell carcinomas and predicts risk for malignant conversion. Oncogene, 26, 6885-6895.
49. Casanova,M.L. et al. (1999) Exocrine pancreatic disorders in transsgenic mice expressing human keratin 8. J. Clin. Invest., 103, 1587-1595.
50. Shukla,A. et al. (2008) Cripto-1 alters keratinocyte differentiation via blockade of transforming growth factor-beta1 signaling: role in skin carcinogenesis. Mol. Cancer Res., 6, 509-516.