Id-1 modulates senescence and TGF-β1 sensitivity in prostate epithelial cells

Biology of the Cell

Volumn 98, Issue 9, 2006, Pages 523-533

  Di, Kaijun ^a   Ling, Ming Tat ^a   Tsao, Sai Wah ^a   Wong, Yong Chuan ^a   Wang, Xianghong ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cell proliferation; Downstream effector; G2 M cell cycle arrest; Growth arrest; Human epithelial cell

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; INHIBITOR OF DIFFERENTIATION 1; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MALE; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; UPREGULATION; WESTERN BLOTTING;

CELL AGING; CELL DIVISION; CELL LINE, TRANSFORMED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; EPITHELIAL CELLS; G2 PHASE; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MALE; PROSTATE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 33748647207     PISSN: 02484900     EISSN: None     Source Type: Journal    
DOI: 10.1042/BC20060026     Document Type: Article

References (52)

1. Benezra, R., Davis, R.L., Lockshon, D., Turner, D.L. and Weintraub, H. (1990) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59
2. Braun, L., Durst, M., Mikumo, R. and Gruppuso, P. (1990) Differential response of nontumorigenic and tumorigenic human papillomavirus type 16-positive epithelial cells to transforming growth factor β1. Cancer Res. 50, 7324-7332
3. Bright, R.K., Vocke, C.D., Emmert-Buck, M.R., Duray, P.H., Solomon, D., Fetsch, P., Rhim, J.S., Linehan, W.M. and Topalian, S.L. (1997) Generation and genetic characterization of immortal human prostate epithelial cell lines derived from primary cancer specimens. Cancer Res. 57, 995-1002
4. Coppe, J.P., Smith, A.P. and Desprez, P.Y. (2003) Id proteins in epithelial cells. Exp. Cell Res. 285, 131-145
5. 3 in NRP-152 rat prostatic epithelial cells. J. Cell Physiol. 166, 231-239
6. Datto, M.B., Li, Y., Panus, J.F., Howe, D.J., Xiong, Y. and Wang, X.F. (1995) Transforming growth factor β induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. U.S.A. 92, 5545-5549
7. Desprez, P.Y., Hara, E., Bissell, M.J. and Campisi, J. (1995) Suppression of mammary epithelial cell differentiation by the helix-loop-helix protein Id-1. Mol. Cell. Biol. 15, 3398-3404
8. Dimri, G.P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I. and Pereira-Smith, O. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U.S.A. 92, 9363-9367
9. Dyson, N., Howley, P.M., Munger, K. and Harlow, E. (1989) The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243, 934-937
10. Elliott, R.L. and Blobe, G.C. (2005) Role of transforming growth factor β in human cancer. J. Clin. Oncol. 23, 2078-2093
11. Everly, Jr, D.N., Mainou, B.A. and Raab-Traub, N. (2004) Induction of Id1 and Id3 by latent membrane protein 1 of Epstein-Barr virus and regulation of p27/Kip and cyclin-dependent kinase 2 in rodent fibroblast transformation. J. Virol. 78, 13470-13478
12. Ewan, K.B., Henshall-Powell, R.L., Ravani, S.A., Pajares, M.J., Arteaga, C., Warters, R., Akhurst, R.J. and Barcellos-Hoff, M.H. (2002) Transforming growth factor-β1 mediates cellular response to DNA damage in situ. Cancer Res. 62, 5627-5631
13. Flanders, K.C., Sullivan, C.D., Fujii, M., Sowers, A., Anzano, M.A., Arabshahi, A., Major, C., Deng, C., Russo, A., Mitchell, J.B. and Roberts, A.B. (2002) Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am. J. Pathol. 160, 1057-1068
14. Grady, W.M., Myeroff, L.L., Swinler, S.E., Rajput, A., Thiagalingam, S., Lutterbaugh, J.D., Neumann, A., Brattain, M.G., Chang, J., Kim, S.J. et al. (1999) Mutational inactivation of transforming growth factor β receptor type II in microsatellite stable colon cancers. Cancer Res. 59, 320-324
15. Hanahan, D. and Weinberg, R.A. (2000) The hallmarks of cancer. Cell 100, 57-70
16. Hara, E., Yamaguchi, T., Nojima, H., Ide, T., Campisi, J., Okayama, H. and Oda, K. (1994) Id-related genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269, 2139-2145
17. Hasskarl, J., Duensing, S., Manuel, E. and Munger, K. (2004) The helix-loop-helix protein ID1 localizes to centrosomes and rapidly induces abnormal centrosome numbers. Oncogene 23, 1930-1938
18. Hayflick, L. (1965) The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636
19. Hocevar, B.A. and Howe, P.H. (1998) Mechanisms of TGF-β-induced cell cycle arrest. Miner. Electrolyte Metab. 24, 131-135
20. Kang, Y., Chen, C.R. and Massague, J. (2003) A self-enabling TGFβ response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11, 915-926
21. Kondo, M., Cubillo, E., Tobiume, K., Shirakihara, T., Fukuda, N., Suzuki, H., Shimizu, K., Takehara, K., Cano, A., Saitoh, M. and Miyazono, K. (2004) A role for Id in the regulation of TGF-β-induced epithelial-mesenchymal transdifferentiation. Cell Death Differ. 11, 1092-1101
22. Ling, M.T., Wang, X., Ouyang, X.S., Lee, T.K., Fan, T.Y., Xu, K., Tsao, S.W. and Wong, Y.C. (2002a) Activation of MAPK signaling pathway is essential for Id-1 induced serum independent prostate cancer cell growth. Oncogene 21, 8498-8505
23. Ling, M.T., Wang, X., Tsao, S.W. and Wong, Y.C. (2002b) Down-regulation of Id-1 expression is associated with TGF-β1-induced growth arrest in prostate epithelial cells. Biochim. Biophys. Acta 1570, 145-152
24. Ling, M.T., Wang, X., Ouyang, X.S., Xu, K., Tsao, S.W. and Wong, Y.C. (2003) Id-1 expression promotes cell survival through activation of NF-κB signalling pathway in prostate cancer cells. Oncogene 22, 4498-4508
25. Lucia, M.S., Anzano, M.A., Slayter, M.V., Anver, M.R., Green, D.M., Shrader, M.W., Logsdon, D.L., Driver, C.L., Brown, C.C. and Peer, C.W. (1995) Chemopreventive activity of tamoxifen, N-(4-hydroxyphenyl)retinamide, and the vitamin D analogue Ro24-5531 for androgen-promoted carcinomas of the rat seminal vesicle and prostate. Cancer Res. 55, 5621-5627
26. Miyazono, K., Ten, D.P., Ichijo, H. and Heldin, C.H. (1994) Receptors for transforming growth factor-β. Adv. Immunol. 55, 181-220
27. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
28. Nickoloff, B.J., Chaturvedi, V., Bacon, P., Qin, J.Z., Denning, M.F. and Diaz, M.O. (2000) Id-1 delays senescence but does not immortalize keratinocytes. J. Biol. Chem. 275, 27501-27504
29. Nigg, E.A. (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32
30. Norton, J.D., Deed, R.W., Craggs, G. and Sablitzky, F. (1998) Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8, 58-65
31. Ouyang, X.S., Wang, X., Lee, D.T., Tsao, S.W. and Wong, Y.C. (2001) Up-regulation of TRPM-2, MMP-7 and ID-1 during sex hormone-induced prostate carcinogenesis in the Noble rat. Carcinogenesis 22, 965-973
32. Ouyang, X.S., Wang, X., Lee, D.T., Tsao, S.W. and Wong, Y.C. (2002a) Overexpression of Id-1 in prostate cancer. J. Urol. 167, 2598-2602
33. Ouyang, X.S., Wang, X., Ling, M.T., Wong, H.L., Tsao, S.W. and Wong, Y.C. (2002b) Id-1 stimulates serum independent prostate cancer cell proliferation through inactivation of p16(INK4a)/pRB pathway. Carcinogenesis 23, 721-725
34. Perk, J., Iavarone, A. and Benezra, R. (2005) Id family of helix-loop-helix proteins in cancer. Nat. Rev. Cancer 5, 603-614
35. Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 8, 9-22
36. Prabhu, S., Ignatova, A., Park, S.T. and Sun, X.H. (1997) Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol. Cell. Biol. 17, 5888-5896
37. Rorke, E.A., Zhang, D., Choo, C.K., Eckert, R.L. and Jacobberger, J.W. (2000) TGF-β-mediated cell cycle arrest of HPV16-immortalized human ectocervical cells correlates with decreased E6/E7 mRNA and increased p53 and p21(WAF-1) expression. Exp. Cell Res. 259, 149-157
38. Scheffner, M., Werness, B.A., Huibregtse, J.M., Levine, A.J. and Howley, P.M. (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129-1136
39. Schwarze, S.R., DePrimo, S.E., Grabert, L.M., Fu, V.X., Brooks, J.D. and Jarrard, D.F. (2002) Novel pathways associated with bypassing cellular senescence in human prostate epithelial cells. J. Biol. Chem. 277, 14877-14883
40. Swarbrick, A., Akerfeldt, M.C., Lee, C.S., Sergio, C.M., Caldon, C.E., Hunter, L.J., Sutherland, R.L. and Musgrove, E.A. (2005) Regulation of cyclin expression and cell cycle progression in breast epithelial cells by the helix-loop-helix protein Id1. Oncogene 24, 381-389
41. Tang, J., Gordon, G.M., Nickoloff, B.J. and Foreman, K.E. (2002) The helix-loop-helix protein Id-1 delays onset of replicative senescence in human endothelial cells. Lab. Invest. 82, 1073-1079
42. Timme, T.L., Truong, L.D., Merz, V.W., Krebs, T., Kadmon, D., Flanders, K.C., Park, S.H. and Thompson, T.C. (1994) Mesenchymal-epithelial interactions and transforming growth factor-β expression during mouse prostate morphogenesis. Endocrinology 134, 1039-1045
43. Tournay, O. and Benezra, R. (1996) Transcription of the dominant-negative helix-loop-helix protein Id1 is regulated by a protein complex containing the immediate-early response gene Egr-1. Mol. Cell. Biol. 16, 2418-2430
44. Untergasser, G., Koch, H.B., Menssen, A. and Hermeking, H. (2002) Characterization of epithelial senescence by serial analysis of gene expression: identification of genes potentially involved in prostate cancer. Cancer Res. 62, 6255-6262
45. Untergasser, G., Gander, R., Rumpold, H., Heinrich, E., Plas, E. and Berger, P. (2003) TGF-β cytokines increase senescence-associated β-galactosidase activity in human prostate basal cells by supporting differentiation processes, but not cellular senescence. Exp. Gerontol. 38, 1179-1188
46. van de Loosdrecht, A.A., Nennie, E., Ossenkoppele, G.J., Beelen, R.H. and Langenhuijsen, M.M. (1991) Cell mediated cytotoxicity against U 937 cells by human monocytes and macrophages in a modified colorimetric MTT assay. A methodological study. J. Immunol. Methods 141, 15-22
47. Villanueva, A., Garcia, C., Paules, A.B., Vicente, M., Megias, M., Reyes, G., de, V.P., Agell, N., Lluis, F., Bachs, O. and Capella, G. (1998) Disruption of the antiproliferative TGF-β signaling pathways in human pancreatic cancer cells. Oncogene 17, 1969-1978
48. Wang, X., Jin, D.Y., Ng, R.W., Feng, H., Wong, Y.C., Cheung, A.L. and Tsao, S.W. (2002) Significance of MAD2 expression to mitotic checkpoint control in ovarian cancer cells. Cancer Res. 62, 1662-1668
49. Wong, Y.C., Wang, X. and Ling, M.T. (2004) Id-1 expression and cell survival. Apoptosis 9, 279-289
50. Woodworth, C.D., Notario, V. and DiPaolo, J.A. (1990) Transforming growth factors β1 and 2 transcriptionally regulate human papillomavirus (HPV) type 16 early gene expression in HPV-immortalized human genital epithelial cells. J. Virol. 64, 4767-4775
51. Yokota, Y. and Mori, S. (2002) Role of Id family proteins in growth control. J. Cell Physiol. 190, 21-28
52. WAF1/CIP1. Proc. Natl. Acad. Sci. U.S.A. 97, 6427-6432