Targeted in vivo expression of the cyclin-dependent kinase inhibitor p21 halts hepatocyte cell-cycle progression, postnatal liver development, and regeneration

Genes and Development

Volumn 10, Issue 3, 1996, Pages 245-260

  Wu, Hua ^a   Wade, Michael ^a,b   Krall, Leonard ^a   Grisham, Joe ^a   Xiong, Yue ^a   Van Dyke, Terry ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b CATO RESEARCH LTD   (United States)

Author keywords

CDK inhibitor; Cell cycle; cell specificity; growth arrest; liver development; liver regeneration; p21; trangenic mice

Indexed keywords

CYCLIN DEPENDENT KINASE; PROTEIN P21;

ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; GROWTH REGULATION; LIVER DEVELOPMENT; LIVER REGENERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; MUS MUSCULUS;

EID: 0030067581     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.3.245     Document Type: Article

References (77)

1. Albrecht, J.H., J.S. Hoffman, B.T. Kren, and C.J. Sherr.1993. Cyclin and cyclin-dependent kinase 1 mRNA expression in models of regenerating liver and human liver diseases. Am. J. Physiol. 265: G857-G864.
2. Aprelikova, O., Y. Xiong, and E.T. Liu. 1995. Both p16 and p21 families of CDK inhibitors block CDK phosphorylation by the CDK activating kinase (CAK). J. Biol. Chem. 270(31): 18195-18197.
3. Brugarolas, J., C. Chandrasekaran, J.I. Gordon, D. Beach, T. Jacks, and G.J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21-deficiency. Nature 377: 552-557.
4. Bucher, N.L.R. 1963. Regeneration of mammalian liver. Int. Rev. Cytol. 15: 245-300
5. Chen, J., P.K. Jackson, M.W. Kirschner, and A. Dutta. 1995. Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature 374: 386-388.
6. Costa, R.H., E. Lai, and J.E. Darnell. 1986. Transcriptional control of the mouse prealbumin (transthyretin) gene: Both promoter sequences and a distinct enhancer are cell specific. Mol. Cell. Biol. 6: 4697-4708.
7. Costa, R.H., D.R. Grayson, K.G. Xanthopoulos, and J.E. Darnell. 1988. A liver-specific DNA-binding protein recognizes multiple nucleotide sites in regulatory regions of transthyretin, alpha 1- antitrypsin, albumin, and simian virus 40 genes. Proc. Natl. Acad. Sci. 85: 3840-3844.
8. Datto, M.B., Y. Li, J.F. Panus, D.J. Howe, Y. Xiong, and X.-F. Wang. 1995. Transforming growth factor β induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. 92: 5545-5549.
9. CIP/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82: 675-684.
10. Dulic, V., W. Kaufman, S. Wilson, T. Tlsty, E. Lees, J. Harper, S. Elledge, and S. Reed. 1994. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76: 1013-1023.
11. Elbendary, A., A. Berchuck, P. Davis, L. Havrilesky, R.C. Bast, J.D. Inglehart, and J.R. Marks. 1994. Transforming growth factor beta 1 can induce CIP/WAF1 expression independent of the p53 pathway in ovarian cancer cells. Cell Growth Differ. 5(12): 1301-1307.
12. El-Deiry, W.S., T. Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D. Lin, W.E. Mercer, K.W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825.
13. El-Deiry, W.S., J.W. Harper, P.M. O'Connor, V.E. Velculescu, C.E. Canman, J. Jackman, and J.A. Pietenpol. 1994. WAF1/ CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54: 1169-1174.
14. Evarts, R.P, P. Nagy, E. Marsden, and S.S. Thorgeirsson. 1987. A precursor relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 8: 1737-1740.
15. Evarts, R.P., P. Nagy, H. Nakatsukasa, E.R. Marsden, and S.S. Thorgeirsson. 1989. In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res. 49: 1541-1547.
16. Fantl, V., G. Stamp, A. Andrews, I. Rosewell, and C. Dickson. 1995. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes & Dev. 9: 2364-2372.
17. Fausto, N. 1990. Hepatocyte differentiation and liver progenitor cells. Curr. Opin. Cell. Biol. 2: 1036-1042.
18. Flores-Rozas, H., Z. Kelman, F. Dean, Z. Pan, J. Harper, S. Elledge, M. O'Donnell, and J. Hurwitz. 1994. Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase delta holoenzyme. Proc. Natl. Acad. Sci. 91: 8655-8659.
19. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear fragmentation. J. Cell Biol. 119: 493-501.
20. Grisham, J.W. 1962. A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine-H3. Cancer Res. 22: 842-849.
21. INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes & Dev. 8: 2939-2952.
22. Guan, K.-L., C.W. Jenkins, Y. Li, C.L. O'Keefe, S. Noh, X. Wu, M. Zariwala, A.G. Matera, and Y. Xiong. 1996. Isolation of p19INK4d, a p16-related Inhibitor specific to CDK6 and CDK4. Mol. Biol Cell (in press).
23. Gumucio, J.J. 1989. Hepatocyte heterogeneity and liver function. Cell. Biol. Rev. 19: 1-161.
24. Guo, K., J. Wang, V. Andres, R.C. Smith, and K. Walsh. 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol. 15(7): 3823-3829.
25. Halevy, O., B.G. Novitch, D.B. Spicer, S.X. Skapek, J. Rhee, G.J. Hannon, D. Beach, and A.B. Lassar. 1995. Terminal cell cycle arrest of skeletal muscle correlates with induction of p21 by MyoD. Science 267: 1018-1021.
26. Hannon, G. and D. Beach. 1994. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 371: 257-261.
27. Harper, J.W., G.R. Adami, N. Wei, K. Keyomars, and S.J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816.
28. Harper, J.W., S.J. Elledge, K. Keyomarsi, B. Dynlacht, L.H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, E. Swindell, M.P. Fox, and N. Wei. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6: 387-400.
29. Higgins, G.M and R.M. Anderson. 1931. Experimental pathology of the liver. Arch. Pathol 12: 186-202.
30. Hirai, H., M.F. Roussel, J. Kato, R.A. Ashmun, and C.J. Sherr. 1995. Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol. Cell. Biol. 15: 2672-2681.
31. Hunter, T. and J. Pines. 1994. Cyclins and cancer II: Cyclin D and CDK inhibitors come of age. Cell 79: 573-582.
32. Huppi, K., D. Siwarski, J. Dosik, P. Michieli, M. Chedid, S. Reed, B. Mock, D. Givol, and J. Mushinski. 1994. Molecular Cloning, sequencing, chromosomal localization and expression of mouse p21 (Waf1). Oncogene 9: 3017-3020.
33. Jenkins, C.W. and Y. Xiong. 1995. Immunoprecipitation and immunoblotting in cell cycle studies. In Cell cycle: Materials and methods (ed. M. Pagano), pp. 250-263. Springer-Verlag, New York, NY.
34. Jiang, H., Z.-Z. Su, F. Collart, E. Huberman, and P. Fisher. 1994. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene 9: 3397-3406.
35. Jungermann, K. 1995. Zonation of metabolism and gene expression in liver. Histochemistry 103: 81-91.
36. Kamb, A., N.A. Gruis, J. Weaver-Feldhaus, Q. Liu, K. Harshman, S.V. Tavtigan, E. Stockert, R.S. Day, B.E. Johnson, and M.H. Skolnick. 1994. A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: 436-440.
37. Kip1) of cyclin-dependent kinase 4 activation. Cell 79: 487-496.
38. Koch, K.S., X.P. Lu, and H.L. Leffert. 1994. Primary rat hepatocytes express cyclin D1 messenger RNA during their growth cycle and during mitogenic transitions induced by transforming growth factor-alpha. Biochem. Biophys. Res. Commun. 204(1): 91-97.
39. Kudryavtsev, B.N., M.V. Kudryavtsev, G.A. Sakuta, and G.I. Stein. 1993. Human hepatocyte polyploidization kinetics in the course of life cycle. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 64(6): 387-393.
40. KIP2, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes & Dev. 9: 639-649.
41. Li, C.Y., L. Suardet, and J.B. Little. 1995. Potential role of Waf1/ Cip1/p21 as a mediator of TGF-β cytoinhibitory effect. J. Biol. Chem. 270(10): 4971-4974.
42. Li, R., S. Waga, G. Hannon, D. Beach, and B. Stillman. 1994. Differential effects by the p21 inhibitor on PCNA-dependent DNA replication and repair. Nature 371: 534-537.
43. Loyer, P., D. Glaise, S. Cariou, G. Baffet, L. Meijers, and C. Guguen-Guillouzo. 1994. Expression and activation of cdks (1 and 2) and cyclins in the cell cycle progression during liver regeneration. J. Biol. Chem. 269(4): 2491-2500.
44. Lu, X.P., K.S. Koch, D.J. Lew, V. Dulic, J. Pines, S.I. Reed, T. Hunter, and H.L. Leffert. 1992. Induction of cyclin mRNA and cyclin-associated histone H1 kinase during liver regeneration. J. Biol Chem. 267(5): 2841-2844.
45. CIP1. Nature 375: 159-161.
46. Kip2, a structurally distinct member of the p21CIP1 CDK inhibitor family, is a candidate tumor suppressor gene. Genes & Dev. 9: 650-662.
47. Michaeli, P., M. Chedid, D. Lin, J.H. Pierce, W.E. Mercer, and D. Givol. 1994. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res. 54: 3391-3395.
48. ink4. Mol. Cell. Biol. 15: 2682-2688.
49. Missero, C., E. Calautti, R. Eckner, J. Chin, L.H. Tsai, D.M. Livingston, and G.P. Dotto. 1995. Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. 92: 5451-5455.
50. Morgan, D.O. 1995. Principles of CDK regulation. Nature 374: 131-134.
51. Nishida, N., Y. Fukuda, T. Komeda, R. Kita, T. Sando, M. Furukawa, M. Amenomori, I. Shibagaki, K. Nakao, M. Ikenaga, and K. Ishizaki. 1994. Amplification and overexpression of the cyclin D1 gene in aggressive human hepatocellular carcinoma. Cancer Res. 54: 3107-3110.
52. Nobori, T., K. Miura, D. Wu, A. Lois, K. Takabayshi, and D. Carson. 1994. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature 368: 753-756.
53. Noda, A., Y. Ning, S.F. Venable, O.M. Pereira-Smith, and J.R. Smith. 1994. Cloning of senescent cell-derived inhibitor of DNA synthesis using an expression screen. Exp. Cell. Res. 211: 90-98.
54. Noguchi, S., Y. Ohba, and T. Oka. 1991. Influence of epidermal growth factor on liver regeneration after partial hepatectomy in mice. J. Endocrinol. 128: 425-431.
55. Cip1 in muscle and other terminally differentiating cells. Science 267: 1024-1027.
56. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78: 59-66.
57. Sandgren, E.P., R.D. Palmiter, J.L. Heckel, C.C. Daugherty, R.L. Brinster, and J.L. Degen. 1991. Complete hepatic regeneration after somatic deletion of an albumin-plasminogen activator transgene. Cell 66: 245-256.
58. Segal, S., B. Shiomo, A. Fiorino, and L. Reid. 1992. The liver as a stem cell lineage system. Am. J. Physiol. 263: 139-148.
59. Serrano, M., G. Hannon, and D. Beach. 1993. A new regulatory motif in cell cycle control causing specific inhibition of cyclin D/CDK4. Nature 366: 704-707.
60. Shaw, P., R. Bovey, S. Tardy, R. Sahli, B. Sordat, and J. Costa. 1992. Induction of apoptosis by wild-type p53 in a human colon tumor-derived cell line. Proc. Natl. Acad. Sci. 89: 4495-4499.
61. Sherr, C.J. 1994. G1 phase progression: Cycling on cue. Cell 79: 551-555.
62. 1 cyclin-dependent kinases. Genes & Dev. 9: 1149-1163.
63. Shiohara, M., W.S. El-Deiry, M. Wada, T. Nakamaki, S. Takeuchi, R. Yang, D.L. Chen, B. Vogelstein, and H.P. Koeffler. 1994. Absence of WAF1 mutations in a variety of human malignancies. Blood 84: 3781-3784.
64. Sicinski, P., J.L. Donaher, S.B. Parker, T. Li, A. Fazeli, H. Gardner, S.Z. Haslam, R.T. Bronson, S.J. Elledge, and R.A. Weinberg. 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82: 621-630.
65. Solomon, M.J. 1994. The function(s) of CAK, the p34cdc2-activating kinase. Trends Biochem. Sci. 19(11): 496-500.
66. Steinman, R.A., B. Hoffman, A. Iro, C. Guillouf, D.A. Liebermann, and M.E. El-houseini. 1994. Induction of p21 (WAF1/ CIP1) during differentiation. Oncogene 9: 3389-3396.
67. Symonds, H.S., S.A. McCarthy, J. Chen, J.M. Pipas, and T. Van Dyke. 1993. Use of transgenic mice reveals cell-specific transformation by a simian virus 40 T-antigen amino-terminal mutant. Mol Cell. Biol. 13: 3255-3265.
68. Symonds, H., L. Krall, L. Remington, M. Saenz-Robles, S. Lowe, T. Jacks, and T. Van Dyke. 1994. p53-Dependent apoptosis supresses tumor growth and progression in vivo. Cell 78: 703-711.
69. Toyoshima, H. and T. Hunter. 1994. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity is related to p21. Cell 78: 1-20.
70. Vassy, J. and M. Kraemer. 1993. Fetal and postnatal growth. In Molecular and cell biology of the liver (ed. A.V. LeBouton), pp. 265-306. CRC Press Inc., Boca Raton, FL.
71. Waga, S., G.J. Hannon, D. Beach, and B. Stillman.1994. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369: 574-578.
72. Xiong, Y., G.J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993a. p21 is a universal inhibitor of cyclin kinases. Nature 366: 701-704.
73. Xiong, Y., H. Zhang, and D. Beach. 1993b. Subunit rearrangement of cyclin-dependent kinases is associated with cellular transformation. Genes & Dev. 7: 1572-1583.
74. Yan, C., R.H. Costa, J.E. Darnell, J.D. Chen, and T.A. Van Dyke. 1990. Distinct positive and negative elements control the limited hepatocyte and choroid plexus expression of transthyretin in transgenic mice. EMBO J. 9: 869-878.
75. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. 1991. Wild-type p53 induces apoptosis of myeloid leukaemic cells that is inhibited by interleukin-6. Nature 352: 345-340.
76. Zhang, H., Y. Xiong, and D. Beach. 1993. Proliferating cell nuclear antigen and p21 are components of multiple cell cycle kinase complexes. Mol. Biol. Cell 4: 897-906.
77. Zhang, H., G. Hannon, and D. Beach. 1994. p21-containing cyclin kinases exist in both active and inactive states. Genes & Dev. 8: 1750-1758.