Attenuated type II TGF-B receptor signalling in human malignant oral keratinocytes induces a less differentiated and more aggressive phenotype that is associated with metastatic dissemination

International Journal of Cancer

Volumn 110, Issue 2, 2004, Pages 170-176

  Huntley, Suzy P ^a   Davies, Maria ^a   Matthews, John B ^b   Thomas, Gareth ^c   Marshall, John ^c   Robinson, C Max ^a   Eveson, John W ^a   Paterson, Ian C ^a   Prime, Stephen S ^a,d  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d BRISTOL DENTAL HOSPITAL   (United Kingdom)

Author keywords

Differentiation; Invasion; Metastases; Migration; TGF

Indexed keywords

COLLAGENASE; COMPLEMENTARY DNA; CYTOKERATIN 10; GELATINASE A; GELATINASE B; TRANSCRIPTION FACTOR FRA 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSFECTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; METASTASIS; MOLECULAR CLONING; MOUTH CARCINOMA; ONCOGENE C MYC; ONCOGENE RAS; ORTHOTOPIC TRANSPLANTATION; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; CELL DIVISION; CELL LINE, TUMOR; CELL MOVEMENT; HUMANS; KERATIN-10; KERATINOCYTES; KERATINS; LUNG NEOPLASMS; MOUTH NEOPLASMS; NEOPLASM METASTASIS; PHENOTYPE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 2342559112     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.20111     Document Type: Article

References (34)

1. Moore SR, Johnson NW. The epidemiology of mouth cancer: a review of global incidence. Oral Disease 2000;6:65-74.
2. Sturgis EM, Miller RH. Second primary malignancies in the head and neck cancer patient. Ann Otol Rhinol Laryngol 1995;104:946-54.
3. Dickens TA, Colletta AA. The pharmacological manipulation of members of the transforming growth factor beta family in the chemoprevention of breast cancer. Bioessays 1993;15:71-4.
4. Piek E, Roberts AB. Suppressor and oncogenic roles of transforming growth factor-β and its signaling pathways in tumorigenesis. Adv Cancer Res 2001;83:1-54.
5. Chen T, Yan W, Wells RG, Rimm DL, McNiff J, Leffell D, Reiss M. Novel inactivating mutations of transforming growth factor-β type I receptor gene in head-and-neck cancer metastases. Int J Cancer 2001;93:653-61.
6. Garrigue-Antar L, Munoz-Antonia T, Antonia SJ, Gesmonde J, Vellucci VF, Reiss M. Missense mutations of the transforming growth factor-beta type-II receptor in human head and neck squamous carcinoma cells. Cancer Res 1995;18:3982-7.
7. Wang D, Song H, Evans JA, Lang JC, Schuller DE, Weghorst CM. Mutation and downregulation of the transforming growth factor beta type II receptor gene in primary squamous cell carcinomas of the head and neck. Carcinogenesis 1997;18:2285-90.
8. Muro-Cacho CA, Rosario-Ortiz K, Livingstone S, Munoz-Antonia T. Defective transforming growth factor beta signaling pathway in head and neck squamous cell carcinoma as evidenced by the lack of expression of activated Smad2. Clin Cancer Res 2001;7:1618-26.
9. Kim SK, Fan Y, Papadimitrakopoulou V, Clayman G, Hittelman WN, Hong WK, Lotan R, Mao L. DPC4, a candidate tumour suppressor gene, is altered infrequently in head and neck squamous cell carcinoma. Cancer Res 1996;56:2519-21.
10. Paterson IC, Matthews JB, Huntley S, Robinson CM, Fahey M, Parkinson EK, Prime SS. Decreased expression of TGF-β cell surface receptors during progression of human oral squamous cell carcinoma. J Pathol 2001;193:458-67.
11. Bottinger EP, Jakubczak JL, Haines DC, Bagnall K, Wakefield LM. Transgenic mice overexpressing a dominant-negative mutant type II transforming growth factor β receptor show enhanced tumorigenesis in the mammary gland and lung in response to the carcinogen 7,12-dimethylbenz-[a]-anthracene. Cancer Res 1997;57:5564-70.
12. Amendt C, Schirmacher P, Weber H, Blessing M. 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 1998;17:25-34.
13. Kanzler S, Meyer E, Lohse AW, Schirmacher P, Henninger J, Galle PR, Blessing M. Hepatocellular expression of a dominant-negative mutant TGF-beta type II receptor accelerates chemically induced hepatocarcinogenesis. Oncogene 2001;20:5015-24.
14. Hahm KB, Lee KM, Kim YB, Hong WS, Lee WH, Han SU, Kim MW, Ahn BO, Oh TY, Lee MH, Green J, Kim SJ. Conditional loss of TGF-beta signalling leads to increased susceptibility to gastrointestinal carcinogenesis in mice. Aliment Pharmacol Ther 2002;16:115-27.
15. Prime SS, Nixon SVR, Crane IJ, Stone A, Matthews JB, Maitland NJ, Remnant L, Powell SK, Game SM, Scully C. The behaviour of human oral squamous cell carcinoma in culture. J Pathol 1990;160:259-69.
16. Prime SS, Matthews JB, Patel V, Game SM, Donnelly MJ, Stone A, Paterson IC, Sandy JR, Yeudall WA. TGF-β receptor regulation mediates the response to exogenous ligand but is independent of the degree of cellular differentiation in human oral keratinocytes. Int J Cancer 1994;56:406-12.
17. Yeudall WA, Torrance LK, Elsegood KA, Speight P, Scully C, Prime SS. Ras gene point mutation is a rare event in premalignant and malignant lesions of the oral cavity. Oral Oncol Eur J Cancer 1993;29B:63-8.
18. Thomas GJ, Lewis MP, Hart IR, Marshall JF, Speight PM. αVβ6 integrin promotes invasion of squamous carcinoma cells through up-regulation of matrix metalloproteinase-9. Int J Cancer 2001;92:641-50.
19. Mansell JP, Baily AJ. Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin Invest 1998;101:1596-603.
20. Davies M, Prime SS, Stone A, Heung Y-L, Huntley SP, Matthews JB, Eveson JW, Paterson IC. Overexpression of autocrine TGF-β1 suppresses the growth of spindle epithelial cells in vitro and in vivo in the rat 4NQO model of oral carcinogenesis. Int J Cancer 1997;73:68-74.
21. Derynck R, Akhurst RJ, Ballmain A. TGF-β signalling in tumour suppression and cancer progression. Nat Genet 2001;29:117-29.
22. Paterson IC, Eveson JW, Prime SS. Molecular changes in oral cancer reflect ethnic origin and aetiology. Oral Oncol Eur J Cancer 1996;32B:150-3.
23. Chen RH, Ebner R, Derynk R. Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science 1993;260:1335-8.
24. Amendt C, Mann A, Schirmacher P, Blessing M. Resistance of keratinocytes to TGF-β-mediated growth restriction and apoptosis induction accelerates re-epithelialisation in skin wounds. J Cell Science 2002;115:2189-98.
25. Yingling JM, Wang XF, Bassing CH. Signaling by the transforming growth factor-β receptors. Biochim Biophys Acta 1995;1242:115-136.
26. Dumont N, Bakin AV, Arteaga CL. Autocrine transforming growth factor-β signaling mediates Smad-independent motility in human cancer cells. J Biol Chem 2003;278:3275-85.
27. Bubb VJ, Curtis LJ, Cunningham C, Dunlop MG, Carothers AD, Morris RG, White S, Bird CC, Wyllie AH. Microsatellite instability and the role of hMSH2 in sporadic colorectal cancer. Oncogene 1996;12:2641-9.
28. Matsumoto K, Hashimoto K, Hashiro M, Yoshimasa H, Yoshikawa K. Modulation of growth and differentiation in normal human keratinocytes with transforming growth factor-beta. J Cell Physiol 1990;145:95-101.
29. Wang G, Higgins PJ, Gannon M, Staiano-Coico L. Transforming growth factor-beta 1 acts cooperatively with sodium butyrate to induce differentiation of normal human keratinocytes. Exp Cell Res 1992;198:27-30.
30. Tang B, Vu M, Booker T, Santner SJ, Miller FR, Anver MR, Wakefield LM. TGF-β switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. J Clin Invest 2003;112:1116-24.
31. Go C, He W, Zhong L, Li P, Huang J, Brinkley BR, Wang XJ. Aberrant cell cycle progression contributes to the early-stage accelerated carcinogenesis in transgenic epidermis expressing the dominant negative TGFbetaRII. Oncogene 2000;19:3623-31.
32. Im Y-H, Kim HT, Kim IY, Factor VM, Hahm K-B, Anzano M, Jang J-J, Flanders K, Haines DC, Thorgeirsson SS, Sizeland A, Kim S-J. Heterozygous mice for the transforming growth factor-β type II receptor gene have increased susceptibility to hepatocellular carcinogenesis. Cancer Res 2001;61:6665-8.
33. Siegel PM, Shu W, Cardiff RD, Muller WJ, Massague J. Transforming growth factor β signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc Natl Acad Sci USA 2003;100:8430-5.
34. Roberts AB, Wakefield LM. The two faces of transforming growth factor β in carcinogenesis. Proc Natl Acad Sci USA 2003;100:8621-3.