Sensitivity to transforming growth factor β1-induced growth arrest is common in human squamous cell carcinoma cell lines: c-MYC down-regulation and p21(waf1) induction are important early events

Cell Growth and Differentiation

Volumn 7, Issue 10, 1996, Pages 1291-1304

  Malliri, Angeliki ^a   Andrew Yeudall, W ^b   Nikolic, Margareta ^a   Crouch, Dorothy H ^c   Kenneth Parkinson, E ^a   Ozanne, Bradford ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN P21; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INDUCTION; SQUAMOUS CELL CARCINOMA;

CARCINOMA, SQUAMOUS CELL; CELL DIVISION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; HUMANS; ORGAN SPECIFICITY; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED;

EID: 10244232854     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Kingsley, D. M. The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev., 8: 133-146, 1994.
2. Wright, J. A., Turley, E. A., and Greenberg, A. H. Transforming growth factor β and fibroblast growth factor as promoters of tumour progression to malignancy. Crit. Rev. Oncog., 4: 473-492, 1993.
3. Alexandrow, M. G., and Moses, H. L. Transforming growth factor β and cell cycle regulation. Cancer Res., 55: 1452-1457, 1995.
4. Fynan, T. M., and Reiss, M. Resistance to inhibition of cell growth by transforming growth factor-β and its role in oncogenesis. Crit. Rev. Oncog., 4: 493-540, 1993.
5. Manning, A. M., Williams, A. C., Game, S. M., and Paraskeva, S. Differential sensitivity of human colonic adenoma and carcinoma cells to transforming growth factor β (TGF-β): conversion of an adenoma cell line to a tumorigenic phenotype is accompanied by a reduced response to the inhibitory effects of TGF-β. Oncogene, 6: 1471-1476, 1991.
6. Haddow, S., Fowlis, D. J., Parkinson, K., Akhurst, R. J., and Balmain, A. Loss of growth control by TGF-β occurs at the late stage of mouse skin carcinogenesis and is independent of ras gene activation. Oncogene, 6: 1465-1470, 1991.
7. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F., and Massagué, J. Mechanism of activation of the TGF β receptor. Nature (Lond.), 370: 341-347, 1994.
8. Weis-Garcia, F., and Massagué, J. Complementation between kinase-defective and activation-defective TGF-β receptors reveals a novel form of receptor cooperativity essential for signalling. EMBO J., 15: 276-289, 1996.
9. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Far, R. S., Zborowska, E., Kinzler, K. W., Vogelstein, B., Brattain, M., and Willson, J. K. V. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science (Washington DC), 268: 1336-1338, 1995.
10. Garrigue-Antar, L., Munoz-Antonia, T., Antonia, S. J., Gesmonde, J., Vellucci, V. F., and Reiss, M. Missense mutations of the transforming growth factor β type II receptor in human head and neck squamous carcinoma cells. Cancer Res., 55: 3982-3987, 1995.
11. Pietenpol, J. A., Stein, R. W., Moran, E., Yaciuk, P., Schlegel, R., Lyons, R. M., Pittelkow, M. R., Munger, K., Howley, P. M., and Moses, H. L. TGF-β1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell, 61: 777-785, 1990.
12. Missero, C., Filvaroff, E., and Dotto, G. P. Induction of transforming growth factor β1 resistance by the E1A oncogens requires binding to a specific set of cellular proteins. Proc. Natl. Acad. Sci. USA, 88: 3489-3493, 1991.
13. Kip1 by the viral E1A oncoprotein in TGF-β-treated cells. Nature (Lond.), 380: 262-265, 1996.
14. Reiss, M., Vellucci, V. F., and Zhou, Z. Mutant p53 tumor suppressor gene causes resistance to transforming growth factor β1 in murine keratinocytes. Cancer Res., 53: 899-904, 1993.
15. Chen, R-H., Ebner, R., and Derynck, R. Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science (Washington DC), 260: 1335-1338, 1993.
16. Okamoto, A., Jiang, W., Kim, S-J, Spillare, E. A., Stoner, G. D., Weinstein, I. B., and Harris, C. C. Overexpression of human cyclin D1 reduces the transforming growth factor β (TGF-β) type II receptor and growth inhibition by TGF-β1 in an immortalized human esophageal epithelial cell line. Proc. Natl. Acad. Sci. USA, 91: 11576-11580, 1994.
17. Ewen, M. E., Sluss, H. K., Whitehouse, L. L., and Livingston, D. M. TGFβ inhibition of CDK4 synthesis is linked to cell cycle arrest. Cell, 74: 1009-1020, 1993.
18. Schwarz, J. K., Bassing, C. H., Kovesdi, I., Datto, M. B., Blazing, M., George, S., Wang, X-F., and Nevins, J. R. Expression of the E2F1 transcription factor overcomes type β transforming growth factor-mediated growth suppression. Proc. Natl. Acad. Sci. USA, 92: 483-487, 1995.
19. Alexandrow, M. G., Kawabata, M., Aakre, M., and Moses, H. L. Overexpression of the c-myc oncoprotein blocks the growth inhibitory response but is required for the mitogenic effects of transforming growth factor β1. Proc. Natl. Acad. Sci. USA, 92: 3239-3243, 1995.
20. Reiss, M., Munoz-Antonia, T., Cowan, J. M., Wilkins, P. C., Zhou, Z., and Vellucci, V. F. Resistance of human squamous carcinoma cells to transforming growth factor β1 is a recessive trait. Proc. Natl. Acad. Sci. USA, 90: 6280-6284, 1993.
21. Coffey, R. J., Bascom, C. C., Sipes, N. J., Graves-Deal, R., Weissman, B. E., and Moses, H. L. Selective inhibition of growth-related gene expression in murine keratinocytes by transforming growth factor β. Mol. Cell. Biol., 8: 3088-3093, 1988.
22. Pietenpol, J. A., Holt, J. T., Stein, R. W., and Moses, H. L. Transforming growth factor β1 suppression of c-myc gene transcription: role in inhibition of keratinocyte proliferation. Proc. Natl. Acad. Sci. USA, 87: 3758-3762, 1990.
23. Landesman, Y., Pagano, M., Draetta, G., Rotter, V., Fusenig, N. E., and Kimchi, A. Modifications of cell cycle controlling nuclear proteins by transforming growth factor β in the HaCaT keratinocyte cell line. Oncogene, 7: 1661-1665, 1992.
24. Elbendary, A., Berchuck, A., Davis, P., Havrilesky, L., Bast, R. C., Iglehart, J. J. D., and Marks, J. R. Transforming growth factor β1 can induce CIP1/WAF1 expression independent of the p53 pathway in ovarian cancer cells. Cell Growth & Differ., 5: 1301-1307, 1994.
25. Datto, M. B., Li, Y., Panus, J. F., Howe, D. J., Xiong, Y., and Wang, X-F. Transforming growth factor β induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. USA, 92: 5545-5549, 1995.
26. Li, C-Y, Suardet, L., and Little, J. B. Potential role of WAF1/Cip1/p21 as a mediator of TGF-β cytoinhibitory effect. J. Biol. Chem., 270: 4971-4974, 1995.
27. Reynisdottir, I., Polyak, K., Iavarone, A., and Massagué, J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev., 9: 1831-1845, 1995.
28. INK4B is a potential effector of TGF-β-induced cell cycle arrest. Nature (Lond.), 371: 257-261, 1994.
29. Ko, T. C., Sheng, H. M., Reisman, D., Thompson, E. A., and Beauchamp, R. D. Transforming growth factor-β1 inhibits cyclin D1 expression in intestinal epithelial cells. Oncogene, 10: 177-184, 1995.
30. Laiho, M., DeCaprio, J. A., Ludlow, J. W., Livingston, D. M., and Massagué, J. Growth inhibition by TGF-β linked to suppression of retinoblastoma protein phosphorylation. Cell, 62: 175-185, 1990.
31. Eilers, M., Schirm, S., and Bishop, J. M. The MYC protein activates transcription of the α-prothymosin gene. EMBO J., 10: 133-141, 1991.
32. Shibuya, H., Yoneyama, M., Ninomiya-Tsuji, J., Mastumoto, K., and Taniguchi, T. IL-2 and EGF receptors stimulate the hematopoietic cell cycle via different signalling pathways: demonstration of a novel role for c-myc. Cell, 70: 57-67, 1992.
33. Meichle, A., Phillip, A., and Eilers, M. The functions of Myc proteins. Biochim. Biophys. Acta, 1114: 129-146, 1992.
34. Field, J. K., and Spandidos, D. A. The role of ras and myc oncogenes in human solid tumours and their relevance in diagnosis and prognosis. Anticancer Res., 10: 1-22, 1990.
35. Spencer, C. A., and Groudine, M. Control of c-myc regulation in normal and neoplastic cells. Adv. Cancer Res., 56: 1-48, 1991.
36. Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M., Waters, C. M., Penn, L. Z., and Hancock, D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell, 69: 119-128, 1992.
37. Hermeking, H., and Eick, D. Mediation of c-myc-induced apoptosis by p53. Science (Washington DC), 265: 2091-2093, 1994.
38. Kip1, a cyclin-CDK inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev., 8: 9-22, 1994.
39. Stanton, P., Richards, S., Reeves, J., Nikolic, M., Edington, K., Clark, L, Robertson, G., Souter, D., Mitchell, R., Hendler, F. J., Cooke, T., Parkinson, E. K., and Ozanne, B. W. Epidermal growth factor receptor expression by human squamous cell carcinomas of the head and neck, cell lines and xenografts. Br. J. Cancer, 70: 427-433, 1994.
40. Burns, J. E., Baird, M. C., Clark, L. J., Burns, P. A., Edington, K., Chapman, C., Mitchell, R., Robertson, G., Soutar, D., and Parkinson, E. K. Gene mutations and increased levels of p53 protein in human squamous cell carcinomas and their cell lines. Br. J. Cancer, 67: 1274-1284, 1993.
41. INK4A with human head and neck keratinocyte replicative senescence: relationship of dysfunction to immortality and neoplasia. Oncogene, 13: 561-568, 1996.
42. Edington, K. G., Loughran, O., Berry, I. J., and Parkinson, E. K. Cellular immortality: a late event in the progression of human squamous cell carcinoma of the head and neck associated with p53 alteration and a high frequency of allele loss. Mol. Carcinog., 13: 254-265, 1995.
43. Hawley-Nelson, P., Vousden, K. H., Hubbert, N. L., Lowy, D. R., and Schiller, J. T. HPV16 E6 and E7 cooperate to immortalize human foreskin keratinocytes. EMBO J., 8: 3905-3910, 1989.
44. Sherr, C. J., and Roberts, J. M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev., 9: 1149-1163, 1995.
45. Harper, J. W., and Elledge, S. J. Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev., 6: 56-64, 1996.
46. Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature (Lond.), 372: 570-573, 1994.
47. Kip1 accumulation during the cell cycle. Science (Washington DC), 271: 1861-1864, 1996.
48. PSK-J3/CDK4) for mammalian D type G1 cyclins. Cell, 71: 323-334, 1992.
49. Kato, J-Y., Matsushime, H., Hiebert, S. W., Ewen, M. E., and Sherr, C. J. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev., 7: 331-342, 1993.
50. Hunter, T., and Pines, J. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell, 79: 573-582, 1994.
51. 1S-phase growth arrest. Mol. Cell. Biol., 11: 1185-1194, 1991.
52. 1 independent of effects on gene transcription. Cancer Res., 55: 3928-3932, 1995.
53. Lukas, J., Pagano, M., Staskova, Z., Draetta, G., and Bartek, J. Cyclin D1 protein oscillates and is essential for cell cycle progression in human tumour cell lines. Oncogene, 9: 707-718, 1994.
54. 1. Genes & Dev., 7: 812-821, 1993.
55. Motokura, T., Keyomarsi, K., Kronenberg, H. M., and Arnold, A. Cloning and characterization of human cyclin D3, a cDNA closely related in sequence to the PRAD/Cyclin D1 proto-oncogene. J. Biol. Chem., 267: 20412-20415, 1992.
56. Ruissen, F., Erp, P. E. J., Jongh, G. J., Boezeman, J. B. M., Kerkhof, P. C. M., and Schalkwijk, J. Cell kinetic characterization of growth arrest in cultured human keratinocytes. J. Cell Sci., 107: 2219-2228, 1994.
57. Prime, S. S., Matthews, J. B., Patel, V., Game, S. M., Donnelly, M., Stone, A., Paterson, I. C., Sandy, J. R., and Yeudall, W. A. 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, 56: 406-412, 1994.
58. 1 checkpoint control. Cell, 82: 675-684, 1995.
59. waf1. Cancer Res., 55: 4536-4539, 1995.
60. Dimri, G. P., Nakanishi, M., Desprez, P-Y., Smith, J. R., and Campisi, J. Inhibition of E2F activity by the cyclin-dependent protein kinase inhibitor p21 in cells expressing or lacking a functional retinoblastoma protein. Mol. Cell. Biol., 16: 2987-2997, 1996.
61. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
62. cdc2 regulation in ras-transfected epithelial cells. Oncogene, 7: 1549-1556, 1992.
63. Rollins, B. J., O'Connell, T. M., Bennett, G., Burton, L. E., Stiles, C. D., and Rheinwald, J. G. Environment-dependent growth inhibition of human epidermal keratinocytes by recombinant human transforming growth factor-β. J. Cell. Physiol., 139: 455-462, 1989.
64. Kumar, V., Green, S., Staub, A., and Chambon, P. Localisation of the oestradiol-binding and putative DNA-binding domains of the human oestrogen receptor. EMBO J., 5: 2231-2236, 1986.
65. Morgenstern, J. P., and Land, H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18: 3587-3596, 1990.
66. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory, 1989.
67. Hu, Q., Bautista, C., Edwards, G. M., Defeo-Jones, D., Jones, R. E., and Harlow, E. Antibodies specific for the human retinoblastoma protein identify a family of related polypeptides. Mol. Cell. Biol., 11: 5792-5799, 1991.