DOI QR코드

DOI QR Code

TGF-β-dependent Cell Growth Arrest and Apoptosis

  • Lee, Kwang-Youl (Department of Biochemistry, School of Medicine, and Medical Research Institute, Chungbuk National University) ;
  • Bae, Suk-Chul (Department of Biochemistry, School of Medicine, and Medical Research Institute, Chungbuk National University)
  • Published : 2002.01.31

Abstract

Keywords

References

  1. Alexandrow, M. G., Kawabata, M., Aakre, M. and Moses, H. L. (1995) Overexpression of the c-Myc oncoprotein blocks the growth inhibitory response but is required for the mitogenic effects of transforming growth factor $\beta$1. Proc. Natl. Acad. Sci.USA 92, 3239-3243. https://doi.org/10.1073/pnas.92.8.3239
  2. Atfi, A., Buisine, M., Mazars, A. and Gespach, C. (1997) Induction of apoptosis by DPC4, a transcription factor regulated by transforming growth factor-$\beta$through stress activated protein kinase/c-Jun N-terminal kinase (SAPKlJNK) signaling pathway. J. BioI. Chem. 272,24731-24734. https://doi.org/10.1074/jbc.272.40.24731
  3. Battegay, E. J., Raines, E. W., Seifert, R. A., Bowen-Pope, D. F. and Ross, R. (1990) TGF-beta induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 63, 515-524. https://doi.org/10.1016/0092-8674(90)90448-N
  4. Chan, F. K. M., Zhang, J., Chen, L., Shapiro, D. N. and Winoto, A. (1995) Identification of human/mouse p19, a novel CDK4/ CDK6 inhibitor with homology to $pI6^{ink4}$. Mol. Cell. BioI. 15,2682-2688. https://doi.org/10.1128/MCB.15.5.2682
  5. Chaouchi, N., Arvanitakis, L., Auffredou, M. T., Blanchard, D. A., Vazquez, A., and Sharma, S. (1995) Characterization of transforming growth factor $\beta$1 induced apoptosis in normal human B cells and lymphoma B cell lines. Oncogene 11, 1615-1622.
  6. Chen, R. H. and Chang, T. Y. (1997) Involvement of caspase family proteases in transforming growth factor $\beta$ induced apoptosis. Cell Growth Differ. 8,821-827.
  7. Chen, R. H., Chang, M. C., Su, Y. H., Tsai, Y. T. and Kuo, M. L. (1999) Interleukin-6 inhibits transforming growth factor $\beta$ induced apoptosis through the phosphatidylinositol 3-kinase/ Akt and signal transducers and activators of transcription 3 pathways. J. Biol. Chem. 274, 23013-23019. https://doi.org/10.1074/jbc.274.33.23013
  8. Chen, R. H., Su, Y. H., Chuang, R. L., and Chang, T. Y. (1998) Suppression of transforming growth factor-$\beta$ induced apoptosis through a phosphatidylinositol 3-kinase/ Akt dependent pathway. Oncogene 17, 1959-1968. https://doi.org/10.1038/sj.onc.1202111
  9. Chipuk, J. E., Bhat, M., Hsing, A. Y., Ma, J. and Danielpour D. (2001) BcI-XL blocks TGF-$\beta$1 induced apoptosis by inhibiting cytochrome C release and not by directly antagonizing Apaf-1 dependent caspase activation in prostate epithelial cells. J. Biol.Chem. 276, 26614-26621. https://doi.org/10.1074/jbc.M100913200
  10. Claassen, G. F. and Hann, S. R. (2000) A role for transcriptional repression of p21$^{cip1}$ by c-myc in overcoming transforming growth factor $\beta$ induced cell cycle arrest. Proc. Natl. Acad. Sci.USA 97, 9498-9503. https://doi.org/10.1073/pnas.150006697
  11. Coffey, R. J. Jr, Bascom, C. C., Sipes, N. J., Graves-Deal, R., Weissman, B. E. and Moses, H. L. (1988) Selective inhibition of growth-related gene expression in murine keratinocytes by transforming growth factor $\beta$. Mol. Cell. BioI. 8, 3088-3093. https://doi.org/10.1128/MCB.8.8.3088
  12. Dai, J. L., Bansal, R. K. and Kern, S. E. (1999) G1 cell cycle arrest and apoptosis induction by nuclear Smad4/Dpc4: Phenotypes reversed by a tumorigenic mutation. Proc. Natl.Acad. Sci. USA 96, 1427-1432. https://doi.org/10.1073/pnas.96.4.1427
  13. Datto, M. B., Li, Y., Panus, J. E, Howe, D. J., Xiong, Y. and Wang, X. F. (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. https://doi.org/10.1073/pnas.92.12.5545
  14. Dennler, S., Heut, S. and Gauthier, J. M. (1998) A short aminoacid sequence in MH1 domain is responsible for functional differences between Samd2 and Samd3. Oncogene 18, 1643-1648.
  15. Derynck, R., Akhurst, R. J. and Balmain, A. (2001) TFG-$\beta$ signaling in tumor suppression and cancer progression. Nature Genetic 29, 117-129. https://doi.org/10.1038/ng1001-117
  16. Derynck, R., Gelbart, W. M., Harland, R. M., Heldin, C. H., Kern, S. E., Massague, J., Melton, D. A., Mlodzik, M. B., Padgett, R. W., Roberts, A. B., Smith, J., Thomsen, G. H., Vogelstein, B., and Wang X.F. (1996) Nomenclature: vertebrate mediators of TGF-$\beta$ family signals. Cell 87, 173. https://doi.org/10.1016/S0092-8674(00)81335-5
  17. Derynck, R., Zhang, Y. and Feng, X.-H. (1998) Samds: transcriptional activators of TGF-$\beta$ responses. Cell 95, 737-740. https://doi.org/10.1016/S0092-8674(00)81696-7
  18. Dulie, V., Kaufmann, W. K., Wilson, S. J., Tlsty, T. D., Less, E., Harper, J. W., Elledge, S. J. and Reed, S. I. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76, 1013-1023. https://doi.org/10.1016/0092-8674(94)90379-4
  19. El-Deiry, W. S., Tokino, T., Velcillescu, V. E., Levy, D. B., Parsons, R., Lin, D., Mercer, E., Kinzler, K. W. and Vogelstein, B. (1993) WAF 1 , a potential mediator of p53 tumor suppression. Cell 75, 817-825. https://doi.org/10.1016/0092-8674(93)90500-P
  20. Ewen, M. E. (1994) The cell cycle and the retinoblastoma protein family. Cancer Metastasis Rev. 13, 45-66. https://doi.org/10.1007/BF00690418
  21. Ewen, M. E., Oliver, C. J., Sluss, H. K., Miller, S. J. and Peeper D. S. (1995) p53-dependent repression of cdk4 translation in TGF-$\beta$ induced G1 cell cycle arrest. Genes Dev. 9, 204-217. https://doi.org/10.1101/gad.9.2.204
  22. Ewen, M. E., Sluss, H. K., Sherr, C. J., Matsushime, H., Kato, J.Y. and Livingston, D. M. (1993) Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73, 487-497. https://doi.org/10.1016/0092-8674(93)90136-E
  23. Ewen, M. E., Sluss, H. K., Whitehouse, L. L. and Livingston, D. M. (1993) TGF-$\beta$inhibition of cdk4 synthesis is linked to cell cycle arrest. Cell 74, 1009-1020. https://doi.org/10.1016/0092-8674(93)90723-4
  24. Facchini, L. M. and Penn, L. Z. (1998) The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J. 12, 633-651. https://doi.org/10.1096/fasebj.12.9.633
  25. Fang, F. and Newport, J. W. (1991) Evidence that the G1-S and G2-M transitions are controlled by different cdc2 proteins in higher eukaryotes. Cell 66, 731-742. https://doi.org/10.1016/0092-8674(91)90117-H
  26. Feng, X. H., Lin, X. and Derynck, R. (2000) Samd2, Smad3 and Smad4 cooperate with Spl to induce $p15^{INK4B}$ transcription in response to TGF-$\beta$. EMBO J. 19,5178-5193. https://doi.org/10.1093/emboj/19.19.5178
  27. Galaktionov, K., Chen, X. and Beach, D. (1996) Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382, 511-517. https://doi.org/10.1038/382511a0
  28. Gu, Y., Turek, C. W. and Morgan, D. O. (1993) Inhibition of CDK2 activity in vivo by an associated 20K regulatory subunit. Nature 366, 707-710. https://doi.org/10.1038/366707a0
  29. Guan, K.-L., Jenkins, C. W., Li, Y., Michols, M. A., Wu, X., OKeefe, C. L., Matera, A. G. and Xiong, Y. (1994). Growth suppression by p18, a$ pI6^{INK4/MTS1}$_ and $ pI5^{INK4/MTS2}$_related CDK6 inhibitor, correlates with wild-type pRb function. Genes & Dev. 8, 2939-2952. https://doi.org/10.1101/gad.8.24.2939
  30. Hannon, G.J . and Beach, D. (1994) $p15^{INK4B}$is a potential effector of TGF-$\beta$ induced cell cycle arrest. Nature 371, 257-261. https://doi.org/10.1038/371257a0
  31. Harper, J. W., Adami, G. R, Wei, N., Keyomarsi, K. and Elledge, S. J. (1993) The p21 cdk-interacting protein Cipl is a potent inhibitor of G1 cycling-dependent kinases. Cell 75, 805-816. https://doi.org/10.1016/0092-8674(93)90499-G
  32. Hata, A., Langa, G., Massague, J. and Hemmati-Brivanlou, A (1998) Samd6 inhibits BMP/Samd1 signaling by specifically competing with the Smad4 tumor suppressor. Genes & Dev. 12, 186-197. https://doi.org/10.1101/gad.12.2.186
  33. Hayashi, H., Abdollah, S., Qiu, Y., Cai, J., Xu, Y. Y., Grinnell, B. W., Richardson, M. A, Topper, J. N., Gimbrone, Jr, M. A, Wrana, J. L. and Falb, D. (1997) The MAD-related protein Samd7 associates with the TGF-${\beta}$ receptor and functions as an antagonist of TGF-${\beta}$signaling. Cell 89, 1165-1173. https://doi.org/10.1016/S0092-8674(00)80303-7
  34. Heldin, C. H., Miyazano, K. and Tendijke, P. (1997) TGF- $\beta$ signaling from cell membrane to nucleus through smad proteins. Nature 390, 465-471. https://doi.org/10.1038/37284
  35. Hirai, H., Roussel, M. F., Kato, J., Ashumn, R. A. and Sherr, C. J. (1995) Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol. Cell BioI. 15, 2672-2681. https://doi.org/10.1128/MCB.15.5.2672
  36. Hoodless, P. A., Haerry, T., Abdollah, S., Stapleton, M., OConnor, M. B., Attisano, L. and Wrana, J. L. (1996) MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500. https://doi.org/10.1016/S0092-8674(00)81250-7
  37. Iavarone, A and Massague, J. (1997) Repression of the CDK activator cdc25A and cell cycle arrest by cytokine TGF-$\beta$ in cells lacking the CDK inhibitor p15. Nature 387, 417-422. https://doi.org/10.1038/387417a0
  38. Iavarone, A. and Massague, J. (1999) E2F and histone de acetylase mediate transforming growth factor $\beta$ repression of cdc25A during keratocyte cell cycle arrest. Mol. Cell BioI. 19,916-922. https://doi.org/10.1128/MCB.19.1.916
  39. Inamura, T., Takase, M., Nishihara, A., Oeda, E., Hanai, J.-I. Kawabata, M. and Miyazano, K. (1997) Samd6 inhibits signaling by the TGF-$\beta$ superfamily. Nature 389, 622-626. https://doi.org/10.1038/39355
  40. Ishisaki, A., Yamato, K., Nakao, A., Nonaka, K., Ohguchi, M., Tendijke, P. and 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. https://doi.org/10.1074/jbc.273.38.24293
  41. Itoh, S., Itoh, E., Goumans, M. J. and Tendijke, P. (2000) Signaling of transforming growth factor-$\beta$ family members through Smad proteins. Eur. J. Biochem. 267, 6954-6967. https://doi.org/10.1046/j.1432-1327.2000.01828.x
  42. Karin, M., Liu, Z.-G. and Zandi, E. (1997) AP-1 function and regulation. Curr Opin Cell BioI. 9, 240-246. https://doi.org/10.1016/S0955-0674(97)80068-3
  43. Kato, J.-Y., Matsushime, H., Hiebert, S. W., Ewen, M. E. and Sherr, C. J. (1993) 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. https://doi.org/10.1101/gad.7.3.331
  44. Kitagawa, M., Higashi, H., Jung, H.K., Suzuki-Takahashi, L., Ikeda, M., Tarnai, K., Kato, J., Segawa, K., Yoshida, E., Nishimura, S. and Taya, Y. (1996) The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15, 7060-7069.
  45. Laiho, M., DeCaprio, J. A., Ludlow, J. W., Livingston, D. M. and Massague, J. (1990) Growth inhibition by TGF-$\beta$ linked to suppression of retinoblastoma protein phosphorylation. Cell 62, l75-185. https://doi.org/10.1016/0092-8674(90)90251-9
  46. Laiho M. J., DeCaprio, J. A., Ludlow, J. W., Livingstone, D. M. and Massague, J. (1990) Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 62, 175-185. https://doi.org/10.1016/0092-8674(90)90251-9
  47. Lallemand, F, Mazars, A., Prunier, C., Bertrand, F., Komprost, M., Gallea, S., Roman, S., Cherqui, G. and Atfi, A. (2001) Samd7 inhibits the survival nuclear factor ${\kappa}B$ and potentiates apoptosis in epithelial cells. Oncogene 20, 879-884. https://doi.org/10.1038/sj.onc.1204167
  48. Landstorm, M., Heldin, N. E., Bu, S., Hermansson, A., ltoh, S., Tendijke, P. and Heldin, C. H. (2000) Samd7 mediates apoptosis induced by transforming growth factor b in prostatic carcinoma cells. Curr. BioI. 10, 535-538. https://doi.org/10.1016/S0960-9822(00)00470-X
  49. Langa, G., Hata, A., Hemmati-BrivanIou, A and Massague, J. (1996) Partnership between DPC4 and SMAD proteins in TGF-$\beta$ signaling pathways. Nature 383, 832-836. https://doi.org/10.1038/383832a0
  50. Lee, M. H., Reynisdottir, I. and Massague, J. (1995) Cloning of $p57^{KiP2}$, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes & Dev. 9, 639-649. https://doi.org/10.1101/gad.9.6.639
  51. Liberati, N. T., Datto, M. B., Frederick, J. P., Shen, X., Wong, C., Rougier-Chapman, E. M. and Wang, X. F. (1999) Smads bind directly to the Jun family of AP-1 transcription factors. Proc. Natl. Acad. Sci. USA 96, 4844-4849. https://doi.org/10.1073/pnas.96.9.4844
  52. Macias-Silva, M., Abdollah, S., Hoodless, P. A., Pirone, R., Attisano, L. and Wrana, J. L. (1996) MADR2 is a substrate of the TGF-$\beta$ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224. https://doi.org/10.1016/S0092-8674(00)81817-6
  53. Massague, J. (1992) Receptors for the TGF-beta family. Cell 69, 1067-1070. https://doi.org/10.1016/0092-8674(92)90627-O
  54. Massague, J. (1998) TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791. https://doi.org/10.1146/annurev.biochem.67.1.753
  55. Massague, J. (2000) How cells read TGF-$\beta$ signals. Nature Rev. Mol. Cell. Biol. 1, 169-178. https://doi.org/10.1038/35043051
  56. Massague, J. and Wotton, D. (2000) Transcriptional control by TGF-$\beta$/Samd signaling system. EMBO J. 19, 1745-1754. https://doi.org/10.1093/emboj/19.8.1745
  57. Massague, J., Blain, S. W. and Lo, R. S. (2000) TGF-$\beta$ signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309. https://doi.org/10.1016/S0092-8674(00)00121-5
  58. Matsuoka, S., Edwards, M., Bai, C., Parker, S., Zhang, P., Baldini, A., Harper, J. W. and Elledge, S. J. (1995) $p57^{KlP2}$, a structurally distinct member of the $p21^{ClP1}$ cdk inhibitor family, is a candidate tumor suppressor gene. Genes & Dev. 9, 650- 662. https://doi.org/10.1101/gad.9.6.650
  59. Matsushime, H., Ewen, M. E., Strom, D. K., Kato, J.-Y., Hanks, S. K., Roussel, M. E. and Sherr, C. J. (1992) Identification and properties of an atypical catalytic subunit (p34PSK13/CDK4) for mammalian D-type G1 cyclins. Cell 71, 323-334. https://doi.org/10.1016/0092-8674(92)90360-O
  60. McDonald, P. P., Fadok, V. A, Bratton, D. and Henson, P. M. (1999) Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J Irnrnunol. 163, 6164-6272.
  61. Meyerson, M. and Harlow, E. (1994) Identification of a G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. BioI. 14, 2077-2086 https://doi.org/10.1128/MCB.14.3.2077
  62. Miller, S. J., Suthiphongchai, T., Zambetti, G. P. and Ewen, M. E. (2000) p53 binds selectively to the 5' untranslated region of cdk4, an RNA element necessary and sufficient for transforming growth factor beta- and p53-mediated translational inhibition of cdk4. Mol. Cell. BioI. 20, 8420-8431 https://doi.org/10.1128/MCB.20.22.8420-8431.2000
  63. Miyazano, K., Tendijke, P. and Heldin, C. H. (2000) TGF-$\beta$signaling by Smad proteins. Adv. Immunol. 75, 115-157 https://doi.org/10.1016/S0065-2776(00)75003-6
  64. Moses, H. L., Yang, E. Y. and Pietenpol, J. A. (1990) TGF-$\beta$ stimulation and inhibition of cell proliferation: new mechanistic insights. Cell 63, 245-247. https://doi.org/10.1016/0092-8674(90)90155-8
  65. Nakao, A., Afrakhta, M., Moren, A., Najayama, T., Christian, J. L., Heuchel, R, Itoh, S., Kawabata, M., Heldin, N.-E., Heldin, C. H. and Tendijke, P. (1997) Identification of Smad7, a TGF-$\beta$ inducible antagonist of TGF-$\beta$signaling. Nature 289, 631- 635. https://doi.org/10.1038/289631a0
  66. Nakayama, K. (1998) Cip/Kip cyclin-dependent kinase inhibitors: brakes of the cell cycle engine during development. BioEssays 12, 1020-1029.
  67. Nakayama, K., Ishida, M., Shirame, M., Inomata, A., Inoue, T., Shishido, N., Horii, I., Loh, D. Y. and Nakayama, K (1996) Mice lacking $p27^{Kip1}$ display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85, 707-720. https://doi.org/10.1016/S0092-8674(00)81237-4
  68. Nevins, J. R. (1998) Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9, 585-593.
  69. Newman, M. J. (1993) Transforming growth factor beta and cell surface in tumor progression. Cancer Matastasis Rev. 12, 239- 254. https://doi.org/10.1007/BF00665956
  70. Oberhammer, E. A., Pavelka, M., Sharma, S., Tiefenbacher, R., Purchio, A. E., Bursch, W. and Schulte-Hermann, R. (1992) Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor $\beta1$. Proc. Natl. Acad. Sci. USA 89, 5408-5412. https://doi.org/10.1073/pnas.89.12.5408
  71. Padgett, R. W., Das, P. and Krishna, S. (1998) TGF-beta signaling, Smads, and tumor suppressors. Bioassays 20, 382-390. https://doi.org/10.1002/(SICI)1521-1878(199805)20:5<382::AID-BIES5>3.0.CO;2-Q
  72. Pardali, K., Kurisaki, A., Moren, A., Tendijke, P., Kardassis, D., and Moustakas, A. (2000) Role of Smad proteins and transcription factor Spl in $p21^{WAF1/Cip1}$regulation by transforming growth factor-$\beta$. J. Biol. Chem. 275, 29244-29256 https://doi.org/10.1074/jbc.M909467199
  73. Patil, S., Wildey, G. M., Brown, T. L., Choy, L., Derynck, R. and Howe, P. H. (2000) Samd7 is induced by CD40 and protects WEHI 231 B-Iymphocytes from transforming growth factor $\beta$ induced growth inhibition and apoptosis. J. Biol. Chem. 275, 38363-38370. https://doi.org/10.1074/jbc.M004861200
  74. Periman, P., Schiemann, W. P., Brooks, M. W., Lodish, H. E and Weinberg, R. A. (2001) TGF-$\beta$ induced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation. Nature Cell BioI. 3, 708-714. https://doi.org/10.1038/35087019
  75. Piek, E., Heldin, C. H. and Tendijke, P. (1999) Specificity, diversity, and regulation in TGF-$\beta$ superfamily signaling. FASEB J 13, 2105-2124. https://doi.org/10.1096/fasebj.13.15.2105
  76. Polyak, K., Kato, J.-Y., Solomon, M. J., Sherr, C. J., Massaue, J., Roberts, J. M. and Koff, A.(1994a) $p27^{Kip1}$, a cyclin-cdkinhibitor, links transforming growth factor-$\beta$ and contact inhibition to cell cycle arrest. Genes & Dev. 8, 9-22 https://doi.org/10.1101/gad.8.1.9
  77. Polyak, K., Lee, M.-H., Erdjument-Bromage, H., Koff, A, Roberts,J. M., Tepst, P. and Massague, J. (1994b ) Cloning of $p27^{Kip1}$, a eyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78, 59-66. https://doi.org/10.1016/0092-8674(94)90572-X
  78. Reynisdottir, I. and Massague, J. (1997) The subcellular location of $p15^{INK4B}\;and\;p27^{Kip1}$ coordinate their inhibitory interactions with cdk4 and cdk2. Genes & Dev. 11, 492-503. https://doi.org/10.1101/gad.11.4.492
  79. Reynisdottir, I., Polyak, K., Iavarone, A. and Massague, J. (1995) Kip/Cip and INK4 CDK inhibitors cooperate to induce cell cycle arrest in response to TGF-$\beta$. Genes & Dev. 9, 1831-1845. https://doi.org/10.1101/gad.9.15.1831
  80. Rotello, R. J., Lieberman, R. C., Purchio, A. F. and Gerschenson, L. E. (1991) Coordinated regulation of apoptosis and cell proliferation by transfonning growth factor ~$\beta$ in cultured uterine epithelial cells. Proc. Natl. Acad. Sci. USA 88, 3412- 3415. https://doi.org/10.1073/pnas.88.8.3412
  81. Saltzman, A., Munro, R., Searfoss, G., Franks, C., Jaye, M., and Ivaschenko, Y. (1998) Transfonning growth factor-$\beta$ mediated apoptosis in the Ramos B-lymphoma cell line is accompanied by caspase activation and BcI-$X_L$ down-regulation. Exp. Cell Res. 242, 244-254. https://doi.org/10.1006/excr.1998.4096
  82. Sanchez, A., Alvarez, A. M., Benito, M. and Fabregat, I. (1996) Apoptosis induced by transforming growth factor-beta in fetal hepatocyte primary cultures: involvement of reactive oxygen intermediates. J Biol Chem. 271, 7416-7422. https://doi.org/10.1074/jbc.271.13.7416
  83. Sanchez, A., Alvarez, A. M., Lopez Pedrosa, J. M., Roncero, C., Benito, M. and Fabregat, I. (1999) Apoptotic response to TGF-beta in fetal hepatocytes depends upon their state of differentiation. Exp. Cell Res. 252, 281-291. https://doi.org/10.1006/excr.1999.4624
  84. Sandhu, C., Garbe, J., Bhattacharya, N., Daksis, J., Pan, C.-H., Yaswen, P., Koh, J., Slingerland, J. M. and Stampfer, M. R (1997) Transforming growth factor $\beta$ stabilizes $p15^{INK4B}$ protein, increase $p15^{INKB}$_cdk4 complexes, and inhibits cyclin D1-cdk4 association in human mammary epithelial cells. Mol. Cell. Biol 17, 2458-2467. https://doi.org/10.1128/MCB.17.5.2458
  85. Selvakumaran, M., Lin, H. K., Sjin, R. T., Reed, J. C., Liebermann, D. A. and Hoffman, B. (1994) The novel primary response gene MyD118 and the proto-oncogenes myb, myc, and bcl-2 modulate transforming growth factor $\beta1$ induced apoptosis of myeloid leukemia cells. Mol Cell. BioI. 14, 2352- 2360. https://doi.org/10.1128/MCB.14.4.2352
  86. Seoane, J., Pouponnot, C., Staller, P., Schader, M., Eiiers, M. and Massague, J. (2001) TGF-$\beta$ influences Myc, Miz-1 and Smad to control the CDK inhibitor $p15^{INK4B}$. Nature Cell BioI. 3, 400- 408. https://doi.org/10.1038/35070086
  87. Serrano, M., Hannon, G. J. and Beach, D. (1993) A new regulatory motif in cell cycle control causing specific inhibition of cyclin D-CDK4. Nature 366, 704-707. https://doi.org/10.1038/366704a0
  88. Sherr, C. J. (1993) Mammalian G1 cyclins. Cell 73, 1059-1065.
  89. Sherr, C. J. (1996) Cancer cell cycles. Science 274, 1672-1677. https://doi.org/10.1126/science.274.5293.1672
  90. Sherr, C. J. and Roberts, J. M. (1995) Inhibitors of mammalian Gl cyclin-dependent kinases. Genes & Dev. 9, 1149-1163. https://doi.org/10.1101/gad.9.10.1149
  91. Sherr, C. J. and Roberts, J. M. (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512. https://doi.org/10.1101/gad.13.12.1501
  92. Shi, Y., Hata, A., Lo, R. S., Massague, J. and Pavletich, N. P. (1997) A structural basis for mutational inactivation of the tumor suppressor Smad4. Nature 388, 87-93. https://doi.org/10.1038/40431
  93. Shi, Y., Wang, Y. F., Jayararnan, L., Yang, H., Massague, J. and Pavletich, N. P. (1998) Crystal structure of a Smad MHI domain bound to DNA: insight on DNA binding in TGF-$\beta$ signaling. Cell 94, 585-594. https://doi.org/10.1016/S0092-8674(00)81600-1
  94. Shih, W. L., Kao, M. L., Chuang, S. E., Cheng, A. L. and Doong, S. L. (2000) Hepatitis B virus X protein inhibits transforming growth factor $\beta$ induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 275, 25858-25864. https://doi.org/10.1074/jbc.M003578200
  95. Shima, Y., Nakao, K., Nakashima, T., Kawakami, A., Nakata, K., Hamasaki, K., Kato, Y., Eguchi, K. and Ishii, N. (1999) Activation of caspase-8 in transfonning growth factor-$\beta$ induced apoptosis of human hepatoma cells. Hepatology 30, 1215-1222. https://doi.org/10.1002/hep.510300503
  96. Souchelnytskyi, S., Tendijke, P., Miyazano, K. and Heldin, C.H. (1996) Phosphorylation of Ser165 in TGF-$\beta$ type I receptor modulates TGF-${\beta}1$ induced cellular responses. EMBO J. 15, 6231-6240.
  97. Staller, P., Peukert, K., Kiermaier, A., Seoane, J., Lukas, J., Karunky, H., Moroy, T., Barte, K. J., Massague, J., Hanel, F. and Eilers, M. (2001) Repression of $p15^{INK4B}$ expression by Myc through association with Miz-1. Nature Cell Biol. 3, 392- 399. https://doi.org/10.1038/35070076
  98. Tanaka, S. and Wands, J. R (1996) Insulin receptor substrate 1 overexpression in human hepatocellular carcinoma cells prevents transfonning growth factor ${\beta}1$ induced apoptosis. Cancer Res. 56,3391-3394.
  99. Tendijke, P., Miyazano, K. and Heldin, C. (2000) Signaling inputs converge on nuclear effects in TGF-${\beta}$ signaling. Trends Biochem. Sci. 25, 64-70. https://doi.org/10.1016/S0968-0004(99)01519-4
  100. Toyoshima, H. and Hunter, T. (1994) p27, a novel inhibitors of G1 cyclin/lcdk protein kinase activity, is related p21. Cell 78, 67- 74. https://doi.org/10.1016/0092-8674(94)90573-8
  101. Wamer, B. J., Blain, S. W., Seoane, J. and Massague, J. (1999) Myc down-regulation by transfonning growth factor $\beta$ required for activation of the $p15^{INK4B}$ G1 arrest pathway. Mol. Cell. Biol. 19, 5913-5922. https://doi.org/10.1128/MCB.19.9.5913
  102. Weinberg, R. A. (1995) The retinoblastoma protein and cell cycle control. Cell 81, 323-330. https://doi.org/10.1016/0092-8674(95)90385-2
  103. Xiong, Y., Hannon, G. J., Zhang, H., Casso, D., Kobayashi, R., and Beach, D. (1993) p21 is a universal inhibitor of cyclin kinases. Nature 366, 701-704. https://doi.org/10.1038/366701a0
  104. Yamamura, Y., Hua, X., Bergelson, S. and Lodish, H. F. (2000) Critical role of Smads and AP-1 complex in transforming growth factor-beta -dependent apoptosis. J. Biol. Chem. 275, 36295-36302. https://doi.org/10.1074/jbc.M006023200
  105. Zhang, Y., Feng, X. H. and Derynck, R. (1996) Receptor-associated Mad homologues synergize as effectors of the TGF- $\beta$ response. Nature 383, 168-172. https://doi.org/10.1038/383168a0
  106. Zhang, Y., Feng, X. H. and Derynck, R. (1998) Smad3 and Srnad4 cooperate with c-Jun/lc-Fos to mediate TGF-beta-induced transcription. Nature 394, 909-913. https://doi.org/10.1038/29814

Cited by

  1. Transforming Growth Factor-β Regulates the Growth of Valve Interstitial Cells in Vitro vol.179, pp.4, 2011, https://doi.org/10.1016/j.ajpath.2011.06.007
  2. KLF10 affects pancreatic function via the SEI-1/p21Cip1 pathway vol.60, 2015, https://doi.org/10.1016/j.biocel.2014.12.021
  3. Cellular processes involved in human epidermal cells exposed to extremely low frequency electric fields vol.27, pp.5, 2015, https://doi.org/10.1016/j.cellsig.2015.02.007
  4. Emerging role of NF-κB signaling in the induction of senescence-associated secretory phenotype (SASP) vol.24, pp.4, 2012, https://doi.org/10.1016/j.cellsig.2011.12.006
  5. Porphyromonas gingivalis gingipains cause G1arrest in osteoblastic/stromal cells vol.23, pp.2, 2008, https://doi.org/10.1111/j.1399-302X.2007.00405.x
  6. Involvement of the c-Ski oncoprotein in cell cycle arrest and transformation during nurse cell formation after Trichinella spiralis infection vol.36, pp.10-11, 2006, https://doi.org/10.1016/j.ijpara.2006.05.012
  7. TGF-β induces connexin43 gene expression in normal murine mammary gland epithelial cells via activation of p38 and PI3K/AKT signaling pathways vol.217, pp.3, 2008, https://doi.org/10.1002/jcp.21551
  8. Mechanisms of prostate atrophy after LHRH antagonist cetrorelix injection: An experimental study in a rat model of benign prostatic hyperplasia vol.32, pp.3, 2012, https://doi.org/10.1007/s11596-012-0067-x
  9. Diversity of Fibroblasts – A Review on Implications for Skin Tissue Engineering vol.187, pp.3, 2008, https://doi.org/10.1159/000111805
  10. Regulation of Gastrointestinal Mucosal Growth vol.3, pp.2, 2011, https://doi.org/10.4199/C00028ED1V01Y201103ISP015
  11. Conditional overexpression of TGF-β1 disrupts mouse salivary gland development and function vol.90, pp.4, 2010, https://doi.org/10.1038/labinvest.2010.5
  12. Cell type-dependent gene transcription profile in a three-dimensional human skin tissue model exposed to low doses of ionizing radiation: Implications for medical exposures vol.53, pp.4, 2012, https://doi.org/10.1002/em.21682
  13. Occurrence and significance of epithelial-mesenchymal transition in breast cancer vol.66, pp.6, 2013, https://doi.org/10.1136/jclinpath-2012-201348
  14. The NR3C1 Glucocorticoid Receptor Gene Polymorphisms May Modulate the TGF-beta mRNA Expression in Asthma Patients vol.38, pp.4, 2015, https://doi.org/10.1007/s10753-015-0123-3
  15. An inhibitory role of NEK6 in TGFβ/Smad signaling pathway vol.48, pp.8, 2015, https://doi.org/10.5483/BMBRep.2015.48.8.225
  16. Imaging Bone Morphogenetic Protein 7 Induced Cell Cycle Arrest in Experimental Gliomas vol.13, pp.3, 2011, https://doi.org/10.1593/neo.101540
  17. Curcumin Suppresses Doxorubicin-Induced Epithelial–Mesenchymal Transition via the Inhibition of TGF-β and PI3K/AKT Signaling Pathways in Triple-Negative Breast Cancer Cells vol.61, pp.48, 2013, https://doi.org/10.1021/jf404092f
  18. Effects of 4-Nonylphenol and Bisphenol A on Stimulation of Cell Growth via Disruption of the Transforming Growth Factor-β Signaling Pathway in Ovarian Cancer Models vol.27, pp.1, 2014, https://doi.org/10.1021/tx400365z
  19. The transcription factor Lef1 switches partners from β-catenin to Smad3 during muscle stem cell quiescence vol.11, pp.540, 2018, https://doi.org/10.1126/scisignal.aan3000