Advertisement

G1 Phase: Components, Conundrums, Context

  • Stephanie J. Moeller
  • Robert J. SheaffEmail author
Chapter
  • 1.7k Downloads
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 42)

Abstract

A eukaryotic cell must coordinate DNA synthesis and chromosomal segregation to generate a faithful replica of itself. These events are confined to discrete periods designated synthesis (S) and mitosis (M), and are separated by two gap periods (G1 and G2). A complete proliferative cycle entails sequential and regulated progression through G1, S, G2, and M phases. During G1, cells receive information from the extracellular environment and determine whether to proliferate or to adopt an alternate fate. Work in yeast and cultured mammalian cells has implicated cyclin dependent kinases (Cdks) and their cyclin regulatory partners as key components controlling G1. Unique cyclin/Cdk complexes are temporally expressed in response to extracellular signaling, whereupon they phosphorylate specific targets to promote ordered G1 progression and S phase entry. Cyclins and Cdks are thought to be required and rate-limiting for cell proliferation because manipulating their activity in yeast and cultured mammalian cells alters G1 progression. However, recent evidence suggests that these same components are not necessarily required in developing mouse embryos or cells derived from them. The implications of these intriguing observations for understanding G1 progression and its regulation are discussed.

Keywords

Curr Opin Cell Biol Trophoblast Giant Cell Cell Cycle Machinery Type Cyclins Minimum Size Threshold 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Albanese C, Johnson J, Watanabe G, Eklund N, Vu D, Arnold A, Pestell RG (1995) Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J Biol Chem 270:23589–23597 PubMedCrossRefGoogle Scholar
  2. 2.
    Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson J (1994) Molecular biology of the cell. Garland Publishing, New York Google Scholar
  3. 3.
    Bartek J, Bartkova J, Lukas J (1996) The retinoblastoma protein pathway and the restriction point. Curr Opin Cell Biol 8:805–814 PubMedCrossRefGoogle Scholar
  4. 4.
    Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M (2004) Control of the SCFSkp2-Cks1 ubiquitin ligase by the APC/CCdh1 ubiquitin ligase. Nature 428:190–193 PubMedCrossRefGoogle Scholar
  5. 5.
    Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM (2004) p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev 18:862–876 PubMedCrossRefGoogle Scholar
  6. 6.
    Berthet C, Aleem E, Coppola V, Tessarollo L, Kaldis P (2003) Cdk2 knockout mice are viable. Curr Biol 13:1775–1785 PubMedCrossRefGoogle Scholar
  7. 7.
    Blagosklonny MV, Pardee AB (2002) The restriction point of the cell cycle. Cell Cycle 1:103–110 PubMedGoogle Scholar
  8. 8.
    Buchkovich K, Duffy LA, Harlow E (1989) The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58:1097–1105 PubMedCrossRefGoogle Scholar
  9. 9.
    Burdon T, Smith A, Savatier P (2002) Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 12:432–438 PubMedCrossRefGoogle Scholar
  10. 10.
    Campisi J, Medrano EE, Morreo G, Pardee AB (1982) Restriction point control of cell growth by a labile protein: evidence for increased stability in transformed cells. Proc Natl Acad Sci USA 79:436–440 PubMedCrossRefGoogle Scholar
  11. 11.
    Chen PL, Scully P, Shew JY, Wang JY, Lee WH (1989) Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 58:1193–1198 PubMedCrossRefGoogle Scholar
  12. 12.
    Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, Sicinski P (2002) Development of mice expressing a single D-typecyclin. Genes Dev 16:3277–3289 PubMedCrossRefGoogle Scholar
  13. 13.
    Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A, te Riele H (1992) Requirement for a functional Rb-1 gene in murine development. Nature 359:328–330 PubMedCrossRefGoogle Scholar
  14. 14.
    Clurman BE, Sheaff RJ, Thress K, Groudine M, Roberts JM (1996) Turnover of cyclin E by the ubiquitin–proteasome pathway is regulated by Cdk2 binding and cyclin phosphorylation. Genes Dev 10:1979–1990 PubMedGoogle Scholar
  15. 15.
    Coats S, Whyte P, Fero ML, Lacy S, Chung G, Randel E, Firpo E, Roberts JM (1999) A new pathway for mitogen-dependent Cdk2 regulation uncovered in p27Kip1-deficient cells. Curr Biol 9:163–173 PubMedCrossRefGoogle Scholar
  16. 16.
    Conlon I, Raff M (2003) Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J Biol 2:7 PubMedCrossRefGoogle Scholar
  17. 17.
    Contreras A, Hale TK, Stenoien DL, Rosen JM, Mancini MA, Herrera RE (2003) The dynamic mobility of histone H1 is regulated by cyclin/Cdk phosphorylation. Mol Cell Biol 23:8626–8636 PubMedCrossRefGoogle Scholar
  18. 18.
    Coverley D, Laman H, Laskey RA (2002) Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol 4:523–528 PubMedCrossRefGoogle Scholar
  19. 19.
    Datar SA, Jacobs HW, de la Cruz AF, Lehner CF, Edgar BA (2000) The Drosophila cyclin D-Cdk4 complex promotes cellular growth. Embo J 19:4543–4554 PubMedCrossRefGoogle Scholar
  20. 20.
    De Bondt HL, Rosenblatt J, Jancarik J, Jones HD, Morgan DO, Kim SH (1993) Crystal structure of cyclin-dependent kinase 2. Nature 363:595–602 PubMedCrossRefGoogle Scholar
  21. 21.
    DePamphilis ML (2003) The “ORC cycle”: a novel pathway for regulating eukaryotic DNA replication. Gene 310:1–15 PubMedCrossRefGoogle Scholar
  22. 22.
    Diehl JA, Zindy F, Sherr CJ (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 11:957–972 PubMedGoogle Scholar
  23. 23.
    Diffley JF, Labib K (2002) The chromosome replication cycle. J Cell Sci 115:869–872 PubMedGoogle Scholar
  24. 24.
    Dolznig H, Grebien F, Sauer T, Beug H, Mullner EW (2004) Evidence for a size-sensing mechanism in animal cells. Nat Cell Biol 6:899–905 PubMedCrossRefGoogle Scholar
  25. 25.
    Dynlacht BD, Flores O, Lees JA, Harlow E (1994) Differential regulation of E2F transactivation by cyclin/Cdk2 complexes. Genes Dev 8:1772–1786 PubMedGoogle Scholar
  26. 26.
    Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33:389–396 PubMedCrossRefGoogle Scholar
  27. 27.
    Fantl V, Stamp G, Andrews A, Rosewell I, Dickson C (1995) Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev 9:2364–2372 PubMedGoogle Scholar
  28. 28.
    Fay DS, Han M (2000) Mutations in cye-1, a Caenorhabditis elegans cyclin E homolog, reveal coordination between cell-cycle control and vulval development. Development 127:4049–4060 PubMedGoogle Scholar
  29. 29.
    Fero ML, Rivkin M, Tasch M, Porter P, Carow CE, Firpo E, Polyak K, Tsai LH, Broudy V, Perlmutter RM, Kaushansky K, Roberts JM (1996) A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27Kip1-deficient mice. Cell 85:733–744 PubMedCrossRefGoogle Scholar
  30. 30.
    Fero ML, Randel E, Gurley KE, Roberts JM, Kemp CJ (1998) The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 396:177–180 PubMedCrossRefGoogle Scholar
  31. 31.
    Flemming W (1965) Contributions to the knowledge of the cell and its vital processes. J Cell Biol 25:1–69 PubMedGoogle Scholar
  32. 32.
    Follette PJ, O'Farrell PH (1997) Connecting cell behavior to patterning: lessons from the cell cycle. Cell 88:309–314 PubMedCrossRefGoogle Scholar
  33. 33.
    Follette PJ, Duronio RJ, O'Farrell PH (1998) Fluctuations in cyclin E levels are required for multiple rounds of endocycle S phase in Drosophila. Curr Biol 8:235–238 PubMedCrossRefGoogle Scholar
  34. 34.
    Friend SH, Horowitz JM, Gerber MR, Wang XF, Bogenmann E, Li FP, Weinberg RA (1987) Deletions of a DNA sequence in retinoblastomas and mesenchymal tumors: organization of the sequence and its encoded protein. Proc Natl Acad Sci USA 84:9059–9063 PubMedCrossRefGoogle Scholar
  35. 35.
    Frolov MV, Dyson NJ (2004) Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 117:2173–2181 PubMedCrossRefGoogle Scholar
  36. 36.
    Frost JA, Alberts AS, Sontag E, Guan K, Mumby MC, Feramisco JR (1994) Simian virus 40 small t antigen cooperates with mitogen-activated kinases to stimulate AP-1 activity. Mol Cell Biol 14:6244-6252 PubMedGoogle Scholar
  37. 37.
    Geng Y, Whoriskey W, Park MY, Bronson RT, Medema RH, Li T, Weinberg RA, Sicinski P (1999) Rescue of cyclin D1 deficiency by knockin cyclin E. Cell 97:767–777 PubMedCrossRefGoogle Scholar
  38. 38.
    Geng Y, Yu Q, Whoriskey W, Dick F, Tsai KY, Ford HL, Biswas DK, Pardee AB, Amati B, Jacks T, Richardson A, Dyson N, Sicinski P (2001) Expression of cyclins E1 and E2 during mouse development and in neoplasia. Proc Natl Acad Sci USA 98:13138–13143 PubMedCrossRefGoogle Scholar
  39. 39.
    Geng Y, Yu Q, Sicinska E, Das M, Schneider JE, Bhattacharya S, Rideout WM, Bronson RT, Gardner H, Sicinski P (2003) Cyclin E ablation in the mouse. Cell 114:431–443 PubMedCrossRefGoogle Scholar
  40. 40.
    Harbour JW, Dean DC (2000) The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14:2393–2409 PubMedCrossRefGoogle Scholar
  41. 41.
    Hartwell LH, Mortimer RK, Culotti J, Culotti M (1973) Genetic control of the cell division cycle in yeast: genetic analysis of cdc mutants. Genetics 74:267–286 Google Scholar
  42. 42.
    Hartwell LH (1974) Saccharomyces cerevisiae cell cycle. Bacteriol Rev 38:164–198 PubMedGoogle Scholar
  43. 43.
    Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246:629–634 PubMedGoogle Scholar
  44. 44.
    Hatakeyama M, Herrera RA, Makela T, Dowdy SF, Jacks T, Weinberg RA (1994) The cancer cell and the cell cycle clock. Cold Spring Harb Symp Quant Biol 59:1–10 PubMedGoogle Scholar
  45. 45.
    Herrera RE, Sah VP, Williams BO, Makela TP, Weinberg RA, Jacks T (1996) Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol Cell Biol 16:2402–2407 PubMedGoogle Scholar
  46. 46.
    Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G (1999) Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283:851–854 PubMedCrossRefGoogle Scholar
  47. 47.
    Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA (1992) Effects of an Rb mutation in the mouse. Nature 359:295–300 PubMedCrossRefGoogle Scholar
  48. 48.
    Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432:316–323 PubMedCrossRefGoogle Scholar
  49. 49.
    Kiyokawa H, Kineman RD, Manova-Todorova KO, Soares VC, Hoffman ES, Ono M, Khanam D, Hayday AC, Frohman LA, Koff A (1996) Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27Kip1. Cell 85:721–732 PubMedCrossRefGoogle Scholar
  50. 50.
    Knoblich JA, Sauer K, Jones L, Richardson H, Saint R, Lehner CF (1994) Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77:107–120 PubMedCrossRefGoogle Scholar
  51. 51.
    Kohn MJ, Leung SW, Criniti V, Agromayor M, Yamasaki L (2004) Dp1 is largely dispensable for embryonic development. Mol Cell Biol 24:7197–7205 PubMedCrossRefGoogle Scholar
  52. 52.
    Kozar K, Ciemerych MA, Rebel VI, Shigematsu H, Zagozdzon A, Sicinska E, Geng Y, Yu Q, Bhattacharya S, Bronson RT, Akashi K, Sicinski P (2004) Mouse development and cell proliferation in the absence of D-cyclins. Cell 118:477–491 PubMedCrossRefGoogle Scholar
  53. 53.
    Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH, Bradley A (1992) Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288–294 PubMedCrossRefGoogle Scholar
  54. 54.
    Liu H, Dibling B, Spike B, Dirlam A, Macleod K (2004) New roles for the RB tumor suppressor protein. Curr Opin Genet Dev 14:55–64 PubMedCrossRefGoogle Scholar
  55. 55.
    Lohka MJ, Hayes MK, Maller JL (1988) Purification of maturation-promoting factor, an intracellular regulator of early mitotic events. Proc Natl Acad Sci USA 85:3009–3013 PubMedCrossRefGoogle Scholar
  56. 56.
    Lukas J, Bartkova J, Rohde M, Strauss M, Bartek J (1995) Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of Cdk4 activity. Mol Cell Biol 15:2600–2611 PubMedGoogle Scholar
  57. 57.
    Malek NP, Sundberg H, McGrew S, Nakayama K, Kyriakides TR, Roberts JM (2001) A mouse knock-in model exposes sequential proteolytic pathways that regulate p27Kip1 in G1 and S phase. Nature 413:323–327 PubMedCrossRefGoogle Scholar
  58. 58.
    Malumbres M, Sotillo R, Santamaria D, Galan J, Cerezo A, Ortega S, Dubus P, Barbacid M (2004) Mammalian cells cycle without the D-typecyclin-dependent kinases Cdk4 and Cdk6. Cell 118:493–504 PubMedCrossRefGoogle Scholar
  59. 59.
    Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129–145 PubMedCrossRefGoogle Scholar
  60. 60.
    Matsushime H, Ewen ME, Strom DK, Kato JY, Hanks SK, Roussel MF, Sherr CJ (1992) Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell 71:323–334 PubMedCrossRefGoogle Scholar
  61. 61.
    Matsuura I, Denissova NG, Wang G, He D, Long J, Liu F (2004) Cyclin-dependent kinases regulate the antiproliferative function of Smads. Nature 430:226–231 PubMedCrossRefGoogle Scholar
  62. 62.
    Mendez J, Stillman B (2000) Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol Cell Biol 20:8602–8612 PubMedCrossRefGoogle Scholar
  63. 63.
    Meyer CA, Jacobs HW, Lehner CF (2002) Cyclin D-Cdk4 is not a master regulator of cell multiplication in Drosophila embryos. Curr Biol 12:661–666 PubMedCrossRefGoogle Scholar
  64. 64.
    Meyerson M, Enders GH, Wu CL, Su LK, Gorka C, Nelson C, Harlow E, Tsai LH (1992) A family of human cdc2-related protein kinases. EMBO J 11:2909–2917 PubMedGoogle Scholar
  65. 65.
    Mitchison JM (1971) The biology of the cell cycle. Cambridge University Press, London Google Scholar
  66. 66.
    Moeller SJ, Head ED, Sheaff RJ (2003) p27Kip1 inhibition of GRB2-SOS formation can regulate Ras activation. Mol Cell Biol 23:3735–3752 PubMedCrossRefGoogle Scholar
  67. 67.
    Moons DS, Jirawatnotai S, Parlow AF, Gibori G, Kineman RD, Kiyokawa H (2002) Pituitary hypoplasia and lactotroph dysfunction in mice deficient for cyclin-dependent kinase-4. Endocrinology 143:3001–3008 PubMedCrossRefGoogle Scholar
  68. 68.
    Morgan DO (1995) Principles of Cdk regulation. Nature 374:131–134 PubMedCrossRefGoogle Scholar
  69. 69.
    Murrary A, Hunt T (1993) The cell cycle: an introduction. Freeman New York Google Scholar
  70. 70.
    Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116:221–234 PubMedCrossRefGoogle Scholar
  71. 71.
    Murray AW, Solomon MJ, Kirschner MW (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339:280–286 PubMedCrossRefGoogle Scholar
  72. 72.
    Nakayama K, Ishida N, Shirane M, Inomata A, Inoue T, Shishido N, Horii I, Loh DY (1996) Mice lacking p27Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85:707–720 PubMedCrossRefGoogle Scholar
  73. 73.
    Nasmyth K (2001) A prize for proliferation. Cell 107:689–701 PubMedCrossRefGoogle Scholar
  74. 74.
    Neufeld TP, Edgar BA (1998) Connections between growth and the cell cycle. Curr Opin Cell Biol 10:784–790 PubMedCrossRefGoogle Scholar
  75. 75.
    Nurse P (1975) Genetic control of cell size at cell division in yeast. Nature 256:547–551 PubMedCrossRefGoogle Scholar
  76. 76.
    Nurse P (1990) Universal control mechanism regulating onset of M-phase. Nature 344:503–508 PubMedCrossRefGoogle Scholar
  77. 77.
    Nurse P (2000a) The incredible life and times of biological cells. Science 289:1711–1716 PubMedCrossRefGoogle Scholar
  78. 78.
    Nurse P (2000b) A long twentieth century of the cell cycle and beyond. Cell 100:71–78 PubMedCrossRefGoogle Scholar
  79. 79.
    Nurse P, Thuriaux P, Nasmyth K (1976) Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 146:167–178 PubMedCrossRefGoogle Scholar
  80. 80.
    Ohtani K, DeGregori J, Nevins JR (1995) Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci USA 92:12146–12150 PubMedCrossRefGoogle Scholar
  81. 81.
    Ortega S, Prieto I, Odajima J, Martin A, Dubus P, Sotillo R, Barbero JL, Malumbres M, Barbacid M (2003) Cyclin-dependent kinase 2 is essential for meiosis but not for mitotic cell division in mice. Nat Genet 35:25–31 PubMedCrossRefGoogle Scholar
  82. 82.
    Pagano M, Jackson PK (2004) Wagging the dogma; tissue-specific cell cycle control in the mouse embryo. Cell 118:535–538 PubMedCrossRefGoogle Scholar
  83. 83.
    Pardee AB (1974) A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci USA 71:1286–1290 PubMedCrossRefGoogle Scholar
  84. 84.
    Pardee AB (1989) G1 events and regulation of cell proliferation. Science 246:603–608 PubMedGoogle Scholar
  85. 85.
    Parisi T, Beck AR, Rougier N, McNeil T, Lucian L, Werb Z, Amati B (2003) Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. Embo J 22:4794–4803 PubMedCrossRefGoogle Scholar
  86. 86.
    Reynisdottir I, Polyak K, Iavarone A, 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 PubMedGoogle Scholar
  87. 87.
    Richardson HE, Wittenberg C, Cross F, Reed SI (1989) An essential G1 function for cyclin-like proteins in yeast. Cell 59:1127–1133 PubMedCrossRefGoogle Scholar
  88. 88.
    Roberts JM, Koff A, Polyak K, Firpo E, Collins S, Ohtsubo M, Massague J (1994) Cyclins, Cdks, and cyclin kinase inhibitors. Cold Spring Harb Symp Quant Biol 59:31–38 PubMedGoogle Scholar
  89. 89.
    Roussel MF, Theodoras AM, Pagano M, Sherr CJ (1995) Rescue of defective mitogenic signaling by D-typecyclins. Proc Natl Acad Sci USA 92:6837–6841 PubMedCrossRefGoogle Scholar
  90. 90.
    Russo AA, Jeffrey PD, Patten AK, Massague J, Pavletich NP (1996) Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382:325-331 PubMedCrossRefGoogle Scholar
  91. 91.
    Rupes I (2002) Checking cell size in yeast. Trends Genet 18:479–485 PubMedCrossRefGoogle Scholar
  92. 92.
    Saucedo LJ, Edgar BA (2002) Why size matters: altering cell size. Curr Opin Genet Dev 12:565–571 PubMedCrossRefGoogle Scholar
  93. 93.
    Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE (1997) Cyclin E/Cdk2 is a regulator of p27Kip1. Genes Dev 11:1464–1478 PubMedGoogle Scholar
  94. 94.
    Sherr CJ (1994) G1 phase progression: cycling on cue. Cell 79:551–555 PubMedCrossRefGoogle Scholar
  95. 95.
    Sherr CJ, Roberts JM (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9:1149–1163 PubMedGoogle Scholar
  96. 96.
    Sherr CJ, Roberts JM (1999) Cdk inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501–1512 PubMedGoogle Scholar
  97. 97.
    Sherr CJ, Roberts JM (2004) Living with or without cyclins and cyclin-dependent kinases. Genes Dev 18:2699–2711 PubMedCrossRefGoogle Scholar
  98. 98.
    Sicinska E, Aifantis I, Le Cam L, Swat W, Borowski C, Yu Q, Ferrando AA, Levin SD, Geng Y, von Boehmer H, Sicinski P (2003) Requirement for cyclin D3 in lymphocyte development and T cell leukemias. Cancer Cell 4:451–461 PubMedCrossRefGoogle Scholar
  99. 99.
    Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, Robker RL, Richards JS, McGinnis LK, Biggers JD, Eppig JJ, Bronson RT, Elledge SJ, Weinberg RA (1996) Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 384:470–474 PubMedCrossRefGoogle Scholar
  100. 100.
    Solvason N, Wu WW, Parry D, Mahony D, Lam EW, Glassford J, Klaus GG, Sicinski P, Weinberg R, Liu YJ, Howard M, Lees E (2000) Cyclin D2 is essential for BCR-mediated proliferation and CD5 B cell development. Int Immunol 12:631–638 PubMedCrossRefGoogle Scholar
  101. 101.
    Stevaux O, Dyson NJ (2002) A revised picture of the E2F transcriptional network and RB function. Curr Opin Cell Biol 14:684–691 PubMedCrossRefGoogle Scholar
  102. 102.
    Su TT, O'Farrell PH (1998a) Chromosome association of minichromosome maintenance proteins in Drosophila endoreplication cycles. J Cell Biol 140:451–460 PubMedCrossRefGoogle Scholar
  103. 103.
    Su TT, O'Farrell PH (1998b) Size control: cell proliferation does not equal growth. Curr Biol 8:R687–R689 PubMedCrossRefGoogle Scholar
  104. 104.
    Takaki T, Fukasawa K, Suzuki-Takahashi I, Hirai H (2004) Cdk-mediated phosphorylation of pRB regulates HDAC binding in vitro. Biochem Biophys Res Commun 316:252–255 PubMedCrossRefGoogle Scholar
  105. 105.
    Tetsu O, McCormick F (2003) Proliferation of cancer cells despite Cdk2 inhibition. Cancer Cell 3:233–245 PubMedCrossRefGoogle Scholar
  106. 106.
    Trimarchi JM, Lees JA (2002) Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3:11–20 PubMedCrossRefGoogle Scholar
  107. 107.
    Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T (1998) Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell 2:293–304 PubMedCrossRefGoogle Scholar
  108. 108.
    Tsutsui T, Hesabi B, Moons DS, Pandolfi PP, Hansel KS, Koff A, Kiyokawa H (1999) Targeted disruption of CDK4 delays cell cycle entry with enhanced p27Kip1 activity. Mol Cell Biol 19:7011–7019 PubMedGoogle Scholar
  109. 109.
    Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H (1999) p27Kip1 ubiquitination and degradation is regulated by the SCFSkp2 complex through phosphorylated Thr187 in p27. Curr Biol 9:661–664 PubMedCrossRefGoogle Scholar
  110. 110.
    van den Heuvel S, Harlow E (1993) Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262:2050–2054 PubMedGoogle Scholar
  111. 111.
    Weinberg RA (1995) The retinoblastoma protein and cell cycle control. Cell 81:323–330 PubMedCrossRefGoogle Scholar
  112. 112.
    White RJ (2004) RNA polymerase III transcription and cancer. Oncogene 23:3208–3216 PubMedCrossRefGoogle Scholar
  113. 113.
    Winston JT, Pledger WJ (1993) Growth factor regulation of cyclin D1 mRNA expression through protein synthesis-dependent and -independent mechanisms. Mol Biol Cell 4:1133–1144 PubMedGoogle Scholar
  114. 114.
    Woo RA, Poon RY (2003) Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle 2:316–324 PubMedGoogle Scholar
  115. 115.
    Wu L, Timmers C, Maiti B, Saavedra HI, Sang L, Chong GT, Nuckolls F, Giangrande P, Wright FA, Field SJ, Greenberg ME, Orkin S, Nevins JR, Robinson ML, Leone G (2001) The E2F1-3 transcription factors are essential for cellular proliferation. Nature 414:457–462 PubMedCrossRefGoogle Scholar
  116. 116.
    Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G (2003) Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942–947 PubMedCrossRefGoogle Scholar
  117. 117.
    Ye X, Zhu C, Harper JW (2001) A premature-termination mutation in the Mus musculus cyclin-dependent kinase 3 gene. Proc Natl Acad Sci USA 98:1682–1686 PubMedCrossRefGoogle Scholar
  118. 118.
    Zetterberg A, Larsson O (1985) Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc Natl Acad Sci USA 82:5365–5369 PubMedCrossRefGoogle Scholar
  119. 119.
    Zetterberg A, Larsson O (1991) Coordination between cell growth and cell cycle transit in animal cells. Cold Spring Harb Symp Quant Biol 56:137–147 PubMedGoogle Scholar
  120. 120.
    Zetterberg A, Engstrom W, Larsson O (1982) Growth activation of resting cells: induction of balanced and imbalanced growth. Ann N Y Acad Sci 397:130–147 PubMedGoogle Scholar

Authors and Affiliations

  1. 1.Corporate Research Materials Laboratory3M CenterSt. PaulUSA
  2. 2.University of Minnesota Cancer Center, MMC 806MinneapolisUSA

Personalised recommendations