Inactivation of a Cdk2 inhibitor during interleukin 2-induced proliferation of human T lymphocytes

Molecular and Cellular Biology

Volumn 14, Issue 7, 1994, Pages 4889-4901

  Firpo, Eduardo J ^a   Koff, Andrew ^b   Solomon, Mark J ^c   Roberts, James M ^a  

^a FRED HUTCHINSON CANCER RESEARCH CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLINE; ENZYME INHIBITOR; PROTEIN KINASE; RECOMBINANT INTERLEUKIN 2; T LYMPHOCYTE RECEPTOR;

AFFINITY CHROMATOGRAPHY; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; ENZYME INACTIVATION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MITOGENESIS; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 0028229732     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.14.7.4889     Document Type: Article

References (94)

1. Ajchenbaum, F., K. Ando, J. DeCaprio, and J. Griffin. 1993. Independent regulation of human D-type cyclin gene expression during G1 phase in primary human T-lymphocytes. J. Biol. Chem. 268:4113-4119.
2. Arion, D., L. Meijer, L. Brizuela, and D. Beach. 1988. Cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF. Cell 55:371-378.
3. Blow, J. J., and P. Nurse. 1990. A Cdc2-like protein is involved in the initiation of DNA replication in Xenopus egg extracts. Cell 62:855-862.
4. Boyum, A. 1968. Isolation of mononuclear cells and granulocytes from human blood. Scand. J. Clin. Lab. Invest. 21(Suppl. 97):77-89.
5. Chang, F., and I. Herskowitz. 1990. Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell 63:999-1011.
6. Crabtree, G. R. 1989. Contingent genetic regulatory events in lymphocyte activation. Science 243:355-361.
7. Dasso, M., and J. Newport. 1990. Completion of DNA replication is monitored by a feedback system that controls the initiation of mitosis in vitro: studies in Xenopus. Cell 61:811-823.
8. Desai, D., Y. Gu, and D. Morgan. 1992. Activation of human cyclin-dependent kinases in vitro. Mol. Biol. Cell 3:571-582.
9. Dulic, B., E. Lees, and S. Reed. 1992. Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257:1958-1961.
10. Dunphy, W. G., L. Brizuela, D. Beach, and J. Newport. 1988. The Xenopus Cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell 54:423-431.
11. D'Urso, G., R. L. Marraccino, D. R. Marshak, and J. M. Roberts. 1990. Cell cycle control of DNA replication by a homologue from human cells of the p34-Cdc2 protein kinase. Science 250:786-791.
12. El-Diery, W., T. Tokino, V. Velculescu, D. Levy, R. Parsons, J. Trent, D. Lin, E. Mercer, K. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
13. Elledge, S., R. Richman, F. Hall, R. Williams, N. Logsdon, and J. Harper. 1992. CDK2 encodes a 33 kd cyclin A-associated protein kinase and is expressed before CDC2 in the cell cycle. Proc. Natl. Acad. Sci. USA 89:2907-2911.
14. Enoch, T., and P. Nurse. 1990. Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell 60:665-673.
15. Ewen, M., H. K. Sluss, C. J. Sherr, H. Matsushime, J. Y. Kato, and D. M. Livingston. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73:487-497.
16. Ewen, M., H. K. Sluss, L. Whitehouse, and D. Livingston. 1993. cdk4 modulation by TGF-β leads to cell cycle arrest. Cell 74:1009-1020.
17. Fang, F., and J. Newport. 1991. Evidence that the G1-S and G2-M transitions are controlled by different Cdc2 proteins in higher eukaryotes. Cell 66:731-742.
18. Fesquet, D., J. C. Labbe, J. Derancourt, J. P. Capony, S. Galas, F. Girard, T. Lorca, J. Shuttleworth, M. Doree, and J. C. Cavadore. 1993. The MO15 gene encodes the catalytic subunit of a protein kinase that activates Cdc2 and other cyclin-dependent kinases (CDKs) through phosphorylation of Thr161 and its homologues. EMBO J. 12:3111-3121.
19. Firpo, E. J., and J. M. Roberts. Unpublished data.
20. Furakawa, Y., H. Piwnica-Worms, T. J. Ernst, Y. Kanakura, and J. D. Griffin. 1990. Cdc2 gene expression at the to S transition in human T lymphocytes. Science 250:805-808.
21. Gautier, J., C. Norbury, M. Lohka, P. Nurse, and J. L. Maller. 1988. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene Cdc2+. Cell 54:433-439.
22. Girard, F., U. Strausfeld, A. Fernandez, and N. Lamb. 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67:1169-1179.
23. Gould, K., S. Moreno, D. Owen, S. Sazer, and P. Nurse. 1991. Phosphorylation at Thr 167 is required for Schizosaccharomyces pombe p34CDC2 function. EMBO J. 10:3297-3309.
24. Gould, K. L., and P. Nurse. 1989. Tyrosine phosphorylation of the fission yeast Cdc2+ protein kinase regulates entry into mitosis. Nature (London) 342:39-45.
25. Greaves, M. F., G. Janossy, and P. Curtis. 1976. Purification of human T lymphocytes using nylon fiber columns, p. 217-229, In B. R. Bloom and J. R. David (ed.), In vitro methods in cell-mediated and tumor immunity. Academic Press, New York.
26. Gu, Y., J. Rosenblatt, and D. O. Morgan. 1992. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11:3995-4005.
27. Gu, Y., C. Turck, and D. O. Morgan. 1993. Inhibition of Cdk2 activity in vivo by an associated 20K regulatory subunit. Nature (London) 366:707-710.
28. Guadagno, T., M. Ohtsubo, J. Roberts, and R. Assoian. 1993. A link between cyclin A expression and adhesion-dependent cell cycle progression. Science 262:1572-1574.
29. Hagan, I., J. Hayles, and P. Nurse. 1988. Cloning and sequencing of the cyclin related cdc13 gene and a cytological study of its role in fission yeast mitosis. J. Cell Sci. 91:587-595.
30. Harper, J., G. Adami, N. Wei, K. Keyomarsi, and S. Elledge. 1993 The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
31. Hartwell, L. 1991. Twenty-five years of cell cycle genetics. Genetics 129:975-980.
32. Hartwell, L., J. Culotti, J. Pringle, and B. Reid. 1974. Genetic control of the cell division cycle in yeast. Science 183:46-51.
33. Hartwell, L., and T. Weinert. 1988. Checkpoints: controls that ensure the order of the cell cycle events. Science 246:629-634.
34. Hinds, P., S. Mittnacht, V. Dulic, A. Arnold, S. Reed, and R. Weinberg. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70:993-1006.
35. cdc2 phosphorylation and histone H1 kinase activity is associated with G1/S-phase growth arrest. Mol. Cell. Biol. 11:1185-1194.
36. Hoyt, M., L. Totis, and B. T. Roberts. 1991. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66:507-517.
37. Kato, J. Y., H. Matsushime, S. Hiebert, M. Ewen, and C. Sherr. 1993. Direct binding of cyclin D to the retinoblastoma gene product and pRb phosphorylation by the cyclin D-dependent kinase, cdk4. Genes Dev. 7:331-342.
38. Koff, A., F. Cross, A. Fisher, J. Schumacher, K. Leguellec, M. Philippe, and J. M. Roberts. 1991. Human cyclin E a new cyclin that interacts with two members of the Cdc2 gene family. Cell 66:1217-1228.
39. Koff, A., A. Giordano, D. Desai, K. Yamashita, W. Harper, S. Elledge, T. Nishimoto, D. Morgan, R. Franza, and J. Roberts. 1992. Formation and activation of a cyclin E/CDK2 complex during the G1 phase of the human cell cycle. Science 257:1689-1694.
40. Koff, A., M. Ohtsuki, K. Polyak, J. Roberts, and J. Massague. 1993. Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-β. Science 260:536-539.
41. Krek, W., and E. Nigg. 1991. Differential phosphorylation of vertebrate p34Cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J. 10:305-316.
42. Kumagai, A., and W. Dunphy. 1991. The Cdc25 protein controls tyrosine dephosphorylation of the Cdc2 protein in a cell free system. Cell 64:903-914.
43. Labbe, J. C., M. G. Lee, P. Nurse, A. Picard, and M. Doree. 1988. Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle gene Cdc2. Nature (London) 335:251-254.
44. Lew, D. J., V. Dulic, and S. I. Reed. 1991. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 66:1197-1206.
45. Li, R., and A. Murray. 1991. Feedback control of mitosis in budding yeast. Cell 66:519-531.
46. Lundgren, D., N. Walworth, R. Booher, M. Dembski, M. Kirschner, and D. Beach. 1991. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of Cdc2. Cell 64:1111-1122.
47. Marraccino, R., E. J. Firpo, and J. Roberts. 1992. Activation of the p34 Cdc2 protein kinase at the start of S phase in the human cell cycle. Mol. Biol. Cell 3:389-401.
48. Matsushime, H., M. Ewen, D. Strom, J.-Y. Kato, S. Hanks, M. Roussel, and C. Sherr. 1992. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D-type G1 cyclins. Cell 71:323-334.
49. Matsushime, H., D. Quelle, S. Shurtleff, M. Shibuya, C. Sherr, and J.-Y. Kato. 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol. 14:2066-2076.
50. Matsushime, H., M. Roussel, R. Ashmun, and C. J. Sherr. 1991. Colony stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65:701-713.
51. Mendenhall, M. 1993. An inhibitor of p34 CDC28 protein kinase activity from Saccharomyces cerevisiae. Science 259:216-219.
52. Meur, S. C., and K. H. M. zum Buschenfelde. 1986. T cell receptor triggering induces responsiveness to interleukin 1 and interleukin 2 but does not lead to T cell proliferation. J. Immunol. 136:11: 4106-4112.
53. Nurse, P. 1990. Universal control mechanism regulating onset of M-phase. Nature (London) 344:503-508.
54. Nurse, P., and Y. Bisset. 1981. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature (London) 292:558-560.
55. Ohtsubo, M., and J. Roberts. 1993. Cyclin dependent regulation of G1 in mammalian fibroblasts. Science 259:1908.
56. Pagano, M., R. Pepperkok, J. Lukas, B. Baldin, W. Ansorge, J. Bartek, and G. Draetta. 1993. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol. 121:101-111.
57. Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and G. Draetta. 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961-971.
58. Pardee, A. B. 1974. A restriction point for control of normal animal cell proliferation. Proc. Natl. Acad. Sci. USA 71:1286-1290.
59. Pardee, A. B. 1989. G1 events and regulation of cell proliferation. Science 246:603-608.
60. Peter, M., A. Gartner, J. Horecka, G. Ammerer, and I. Herskowitz. 1993. FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73:747-760.
61. Piggot, J. R., R. Rai, and B. L. A. Carter. 1982. A bifunctional gene product involved in two phases of the yeast cell cycle. Nature (London) 298:391-393.
62. Polacino, P. S., H. A. Liang, E. J. Firpo, and E. A. Clark. 1993. T-cell activation influences initial DNA synthesis of simian immunodeficiency virus in resting T lymphocytes from macaques. J. Virol. 67:7008-7016.
63. Polyak, K., J.-Y. Kato, M. J. Solomon, C. J. Sherr, J. Massague, J. M. Roberts, and A. Koff. 1994. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
64. Poon, R., K. Yamashita, J. Adamczewski, T. Hunt, and J. Shuttleworth. 1993. The Cdc2-related protein p40 MO15 is the catalytic subunit of a protein kinase that can activate p33 CDK2 and p34 CDC2. EMBO J. 12:3123-3132.
65. Reed, J. C., J. D. Alpers, and P. C. Nowell. 1986. Sequential expression of protooncogenes during lectin-stimulated mitogenesis of normal human lymphocytes. Proc. Natl. Acad. Sci. USA 83:3982-3986.
66. Reed, S. I., and C. Wittenberg. 1990. Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 87:5697-5701.
67. Reid, B., and L. Hartwell. 1977. Regulation of mating in the cell cycle of Saccharomyces cerevisiae. J. Cell Biol. 75:355-365.
68. Riabowol, K., G. Draetta, L. Brizuela, D. Vandre, and D. Beach. 1989. The Cdc2 kinase is a nuclear protein that is essential for mitosis in mammalian cells. Cell 57:393-401.
69. Roberts, J. Unpublished data.
70. Rosenblatt, J., Y. Gu, and D. Morgan. 1992. Human cyclin-dependent kinase 2 (CDK2) is activated during the S and G2 phase of the cell cycle and associates with cyclin A. Proc. Natl. Acad. Sci. USA 89:2824-2828.
71. Schwartz, R. H. 1990. A cell culture model for T lymphocyte clonal anergy. Science 248:1349-1356.
72. Sherr, C. 1993. Mammalian G1 cyclins. Cell 73:1059-1065.
73. Smith, K. A. 1988. Interleukin 2: inception, impact and implications. Science 240:1169-1176.
74. Smythe, C., and J. Newport. 1992. Coupling of mitosis to the completion of S phase in Xenopus occurs via modulation of the tyrosine kinase that phosphorylates p34 CDC2. Cell 68:787-797.
75. Solomon, M. J., M. Glotzer, T. H. Lee, M. Phillippe, and M. W. Kirschner. 1990. Cyclin activation of p34-Cdc2. Cell 63:1013-1024.
76. Solomon, M. J., J. W. Harper, and J. Shuttleworth. 1993. CAK, the p34 CDC2 activating kinase, contains a protein identical or closely related to p40 MO15. EMBO J. 12:3133-3142.
77. Solomon, M. J., T. Lee, and M. W. Kirschner. 1991. Role of phosphorylation in p34 CDC2 activation: identification of an activating kinase. Mol. Biol. Cell 3:13-27.
78. Th'ng, J. P. H., P. S. Wright, J. Hamaguchi, M. G. Lee, C. J. Norbury, P. Nurse, and E. M. Bradbury. 1990. The FT210 cell line is a mouse G2 phase mutant with a temperature-sensitive CDC2 gene product. Cell 63:313-324.
79. Traganos, R., Z. Darzynkiewicz, T. Sharpless, and M. R. Melamed. 1977. Simultaneous staining of ribonucleic and deoxyribonucleic acids in unfixed cells using acridine orange in a flow cytofluorometric system. J. Histochem. Cytochem. 25:46-56.
80. Truneh, A., F. Albert, P. Golstein, and A. Schmitt-Verhulst. 1985. Early steps of lymphocyte activation bypassed by synergy between calcium ionophores and phorbol ester. Nature (London) 313:318-320.
81. Tsai, L., E. Harlow, and M. Meyerson. 1991. Isolation of the human Cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase. Nature (London) 33:555-557.
82. Tsai, L., E. Lees, B. Haha, E. Harlow, and K. Riabowol. 1993. The cdk2 kinase is required for the G1-to-S phase transition in mammalian cells. Oncogene 8:1593-1602.
83. Tsoukas, C. D., B. Landgraf, J. Bentin, M. Valentine, M. Lotz, J. H. Vaughan, and D. A. Carson. 1985. Activation of resting T lymphocytes by anti-CD3 (T3) antibodies in the absence of monocytes. J. Immunol. 135:1719-1723.
84. Ullman, K. S., J. P. Northrop, C. L. Verweij, and G. R. Crabtree. 1990. Transmission of signals from the T lymphocyte antigen receptor to the genes responsible for cell proliferation and immune function: the missing link. Annu. Rev. Immunol. 8:421-452.
85. Weinert, T., and L. Hartwell. 1989. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241:317-322.
86. Weiss, A., and J. Imboden. 1987. Cell surface molecules and early events involved in human T lymphocyte activation. Adv. Immunol. 41:1-38.
87. Weiss, A., J. Imboden, D. Shoback, and J. Stobo. 1984. Role of T3 surface molecules in human T-cell activation: T3-dependent activation results in an increase in cytoplasmic free calcium. Proc. Natl. Acad. Sci. USA 81:4169-4173.
88. Winston, J. T., and W. J. Pledger. 1993. Growth factor regulation of cyclin D1 mRNA expression through protein synthesis-dependent and -independent mechanisms. Mol. Biol. Cell 4:1133-1144.
89. Won, K., Y. Xiong, D. Beach, and M. Gilman. 1992. Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. Proc. Natl. Acad. Sci. USA 89:9910-9914.
90. Xiong, Y., T. Connolly, B. Futcher, and D. Beach. 1991. Human D-type cyclin. Cell 65:691-699.
91. Xiong, Y., G. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature (London) 366:701-704.
92. Xiong, Y., H. Zhang, and D. Beach. 1992. D-type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71:505-514.
93. Xiong, Y., H. Zhang, and D. Beach. 1993. Subunit rearrangement of the cyclin-dependent kinases is associated with cellular transformation. Genes Dev. 7:1572-1583.
94. Zetterberg, A. 1990. Control of mammalian cell proliferation. Curr. Opin. Cell Biol. 2:296-300.