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. 1994 Feb 1;13(3):595–605. doi: 10.1002/j.1460-2075.1994.tb06297.x

Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins.

P Gallant 1, E A Nigg 1
PMCID: PMC394849  PMID: 8313904

Abstract

Cyclins play a key role in controlling progression through the cell cycle. They act as regulatory subunits of p34cdc2/CDC28 and related cyclin-dependent protein kinases (cdks). In vertebrates, cyclins B1 and B2 function during M phase, whereas cyclin A is required for S phase as well as the G2 to M phase transition. Here, we describe the identification and characterization of a novel vertebrate cyclin, termed cyclin B3. The assignment of this cyclin to the B-type subfamily is based on its cDNA-derived sequence and its pattern of expression in synchronized cells, both suggesting a distant relationship to other B-type cyclins. Interestingly, however, cyclin B3 also displays properties that resemble those of A- rather than B-type cyclins. Specifically, cyclin B3 localizes to the cell nucleus throughout the cell cycle, and is able to associate in vivo with at least two kinase subunits, p34cdc2 and p33cdk2. Furthermore, deletion of 26 amino acids from the C-terminus of cyclin B3 impairs both its interaction with kinase catalytic subunits and its nuclear localization, reminiscent of recent results obtained with cyclin A. Based on these observations, we conclude that cyclin B3 may share functional properties with both A- and B-type cyclins.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bailly E., Pines J., Hunter T., Bornens M. Cytoplasmic accumulation of cyclin B1 in human cells: association with a detergent-resistant compartment and with the centrosome. J Cell Sci. 1992 Mar;101(Pt 3):529–545. doi: 10.1242/jcs.101.3.529. [DOI] [PubMed] [Google Scholar]
  2. Bandara L. R., Adamczewski J. P., Hunt T., La Thangue N. B. Cyclin A and the retinoblastoma gene product complex with a common transcription factor. Nature. 1991 Jul 18;352(6332):249–251. doi: 10.1038/352249a0. [DOI] [PubMed] [Google Scholar]
  3. Bandara L. R., Adamczewski J. P., Zamanian M., Poon R. Y., Hunt T., Thangue N. B. Cyclin A recruits p33cdk2 to the cellular transcription factor DRTF1. J Cell Sci Suppl. 1992;16:77–85. doi: 10.1242/jcs.1992.supplement_16.10. [DOI] [PubMed] [Google Scholar]
  4. Behra R., Christen P., Sonderegger P. Independent quantitation of the mitochondrial and the cytosolic isoenzyme of aspartate aminotransferase in chicken tissues by radioimmunoassays. J Biol Chem. 1981 Apr 10;256(7):3381–3384. [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  6. Breitbart R. E., Andreadis A., Nadal-Ginard B. Alternative splicing: a ubiquitous mechanism for the generation of multiple protein isoforms from single genes. Annu Rev Biochem. 1987;56:467–495. doi: 10.1146/annurev.bi.56.070187.002343. [DOI] [PubMed] [Google Scholar]
  7. Bréchot C. Oncogenic activation of cyclin A. Curr Opin Genet Dev. 1993 Feb;3(1):11–18. doi: 10.1016/s0959-437x(05)80335-1. [DOI] [PubMed] [Google Scholar]
  8. Buendia B., Clarke P. R., Félix M. A., Karsenti E., Leiss D., Verde F. Regulation of protein kinases associated with cyclin A and cyclin B and their effect on microtubule dynamics and nucleation in Xenopus egg extracts. Cold Spring Harb Symp Quant Biol. 1991;56:523–532. doi: 10.1101/sqb.1991.056.01.059. [DOI] [PubMed] [Google Scholar]
  9. Buendia B., Draetta G., Karsenti E. Regulation of the microtubule nucleating activity of centrosomes in Xenopus egg extracts: role of cyclin A-associated protein kinase. J Cell Biol. 1992 Mar;116(6):1431–1442. doi: 10.1083/jcb.116.6.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cao L., Faha B., Dembski M., Tsai L. H., Harlow E., Dyson N. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature. 1992 Jan 9;355(6356):176–179. doi: 10.1038/355176a0. [DOI] [PubMed] [Google Scholar]
  11. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clarke P. R., Leiss D., Pagano M., Karsenti E. Cyclin A- and cyclin B-dependent protein kinases are regulated by different mechanisms in Xenopus egg extracts. EMBO J. 1992 May;11(5):1751–1761. doi: 10.1002/j.1460-2075.1992.tb05227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Devoto S. H., Mudryj M., Pines J., Hunter T., Nevins J. R. A cyclin A-protein kinase complex possesses sequence-specific DNA binding activity: p33cdk2 is a component of the E2F-cyclin A complex. Cell. 1992 Jan 10;68(1):167–176. doi: 10.1016/0092-8674(92)90215-x. [DOI] [PubMed] [Google Scholar]
  14. Dingwall C., Laskey R. A. Nuclear targeting sequences--a consensus? Trends Biochem Sci. 1991 Dec;16(12):478–481. doi: 10.1016/0968-0004(91)90184-w. [DOI] [PubMed] [Google Scholar]
  15. Draetta G. Cdc2 activation: the interplay of cyclin binding and Thr161 phosphorylation. Trends Cell Biol. 1993 Sep;3(9):287–289. doi: 10.1016/0962-8924(93)90001-h. [DOI] [PubMed] [Google Scholar]
  16. Dulić V., Lees E., Reed S. I. Association of human cyclin E with a periodic G1-S phase protein kinase. Science. 1992 Sep 25;257(5078):1958–1961. doi: 10.1126/science.1329201. [DOI] [PubMed] [Google Scholar]
  17. Epstein C. B., Cross F. R. CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev. 1992 Sep;6(9):1695–1706. doi: 10.1101/gad.6.9.1695. [DOI] [PubMed] [Google Scholar]
  18. Evan G. I., Lewis G. K., Ramsay G., Bishop J. M. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985 Dec;5(12):3610–3616. doi: 10.1128/mcb.5.12.3610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Evans T., Rosenthal E. T., Youngblom J., Distel D., Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell. 1983 Jun;33(2):389–396. doi: 10.1016/0092-8674(83)90420-8. [DOI] [PubMed] [Google Scholar]
  20. Ewen M. E., Faha B., Harlow E., Livingston D. M. Interaction of p107 with cyclin A independent of complex formation with viral oncoproteins. Science. 1992 Jan 3;255(5040):85–87. doi: 10.1126/science.1532457. [DOI] [PubMed] [Google Scholar]
  21. Faha B., Ewen M. E., Tsai L. H., Livingston D. M., Harlow E. Interaction between human cyclin A and adenovirus E1A-associated p107 protein. Science. 1992 Jan 3;255(5040):87–90. doi: 10.1126/science.1532458. [DOI] [PubMed] [Google Scholar]
  22. Fang F., Newport J. W. Evidence that the G1-S and G2-M transitions are controlled by different cdc2 proteins in higher eukaryotes. Cell. 1991 Aug 23;66(4):731–742. doi: 10.1016/0092-8674(91)90117-h. [DOI] [PubMed] [Google Scholar]
  23. Fitch I., Dahmann C., Surana U., Amon A., Nasmyth K., Goetsch L., Byers B., Futcher B. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol Biol Cell. 1992 Jul;3(7):805–818. doi: 10.1091/mbc.3.7.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Forsburg S. L., Nurse P. Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu Rev Cell Biol. 1991;7:227–256. doi: 10.1146/annurev.cb.07.110191.001303. [DOI] [PubMed] [Google Scholar]
  25. Gabrielli B. G., Roy L. M., Maller J. L. Requirement for Cdk2 in cytostatic factor-mediated metaphase II arrest. Science. 1993 Mar 19;259(5102):1766–1769. doi: 10.1126/science.8456304. [DOI] [PubMed] [Google Scholar]
  26. Galaktionov K., Beach D. Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: evidence for multiple roles of mitotic cyclins. Cell. 1991 Dec 20;67(6):1181–1194. doi: 10.1016/0092-8674(91)90294-9. [DOI] [PubMed] [Google Scholar]
  27. Gallant P., Nigg E. A. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells. J Cell Biol. 1992 Apr;117(1):213–224. doi: 10.1083/jcb.117.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gautier J., Maller J. L. Cyclin B in Xenopus oocytes: implications for the mechanism of pre-MPF activation. EMBO J. 1991 Jan;10(1):177–182. doi: 10.1002/j.1460-2075.1991.tb07934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ghiara J. B., Richardson H. E., Sugimoto K., Henze M., Lew D. J., Wittenberg C., Reed S. I. A cyclin B homolog in S. cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell. 1991 Apr 5;65(1):163–174. doi: 10.1016/0092-8674(91)90417-w. [DOI] [PubMed] [Google Scholar]
  30. Giordano A., Whyte P., Harlow E., Franza B. R., Jr, Beach D., Draetta G. A 60 kd cdc2-associated polypeptide complexes with the E1A proteins in adenovirus-infected cells. Cell. 1989 Sep 8;58(5):981–990. doi: 10.1016/0092-8674(89)90949-5. [DOI] [PubMed] [Google Scholar]
  31. Girard F., Strausfeld U., Fernandez A., Lamb N. J. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell. 1991 Dec 20;67(6):1169–1179. doi: 10.1016/0092-8674(91)90293-8. [DOI] [PubMed] [Google Scholar]
  32. Glotzer M., Murray A. W., Kirschner M. W. Cyclin is degraded by the ubiquitin pathway. Nature. 1991 Jan 10;349(6305):132–138. doi: 10.1038/349132a0. [DOI] [PubMed] [Google Scholar]
  33. Grandin N., Reed S. I. Differential function and expression of Saccharomyces cerevisiae B-type cyclins in mitosis and meiosis. Mol Cell Biol. 1993 Apr;13(4):2113–2125. doi: 10.1128/mcb.13.4.2113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hamaguchi J. R., Tobey R. A., Pines J., Crissman H. A., Hunter T., Bradbury E. M. Requirement for p34cdc2 kinase is restricted to mitosis in the mammalian cdc2 mutant FT210. J Cell Biol. 1992 Jun;117(5):1041–1053. doi: 10.1083/jcb.117.5.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Harris N. L., Senapathy P. Distribution and consensus of branch point signals in eukaryotic genes: a computerized statistical analysis. Nucleic Acids Res. 1990 May 25;18(10):3015–3019. doi: 10.1093/nar/18.10.3015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Hunt T. Cyclins and their partners: from a simple idea to complicated reality. Semin Cell Biol. 1991 Aug;2(4):213–222. [PubMed] [Google Scholar]
  37. Hunt T., Luca F. C., Ruderman J. V. The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J Cell Biol. 1992 Feb;116(3):707–724. doi: 10.1083/jcb.116.3.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hunter T., Pines J. Cyclins and cancer. Cell. 1991 Sep 20;66(6):1071–1074. doi: 10.1016/0092-8674(91)90028-w. [DOI] [PubMed] [Google Scholar]
  39. Knoblich J. A., Lehner C. F. Synergistic action of Drosophila cyclins A and B during the G2-M transition. EMBO J. 1993 Jan;12(1):65–74. doi: 10.1002/j.1460-2075.1993.tb05632.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kobayashi H., Golsteyn R., Poon R., Stewart E., Gannon J., Minshull J., Smith R., Hunt T. Cyclins and their partners during Xenopus oocyte maturation. Cold Spring Harb Symp Quant Biol. 1991;56:437–447. doi: 10.1101/sqb.1991.056.01.051. [DOI] [PubMed] [Google Scholar]
  41. Kobayashi H., Minshull J., Ford C., Golsteyn R., Poon R., Hunt T. On the synthesis and destruction of A- and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis. J Cell Biol. 1991 Aug;114(4):755–765. doi: 10.1083/jcb.114.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Koff A., Cross F., Fisher A., Schumacher J., Leguellec K., Philippe M., Roberts J. M. Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell. 1991 Sep 20;66(6):1217–1228. doi: 10.1016/0092-8674(91)90044-y. [DOI] [PubMed] [Google Scholar]
  43. Krek W., Maridor G., Nigg E. A. Casein kinase II is a predominantly nuclear enzyme. J Cell Biol. 1992 Jan;116(1):43–55. doi: 10.1083/jcb.116.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Krek W., Nigg E. A. 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. 1991 Feb;10(2):305–316. doi: 10.1002/j.1460-2075.1991.tb07951.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Krek W., Nigg E. A. Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: evidence for a double block to p34cdc2 kinase activation in vertebrates. EMBO J. 1991 Nov;10(11):3331–3341. doi: 10.1002/j.1460-2075.1991.tb04897.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Kühne C., Linder P. A new pair of B-type cyclins from Saccharomyces cerevisiae that function early in the cell cycle. EMBO J. 1993 Sep;12(9):3437–3447. doi: 10.1002/j.1460-2075.1993.tb06018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lees E., Faha B., Dulic V., Reed S. I., Harlow E. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev. 1992 Oct;6(10):1874–1885. doi: 10.1101/gad.6.10.1874. [DOI] [PubMed] [Google Scholar]
  48. Lehner C. F., Kurer V., Eppenberger H. M., Nigg E. A. The nuclear lamin protein family in higher vertebrates. Identification of quantitatively minor lamin proteins by monoclonal antibodies. J Biol Chem. 1986 Oct 5;261(28):13293–13301. [PubMed] [Google Scholar]
  49. Lehner C. F., O'Farrell P. H. Expression and function of Drosophila cyclin A during embryonic cell cycle progression. Cell. 1989 Mar 24;56(6):957–968. doi: 10.1016/0092-8674(89)90629-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Lehner C. F., O'Farrell P. H. The roles of Drosophila cyclins A and B in mitotic control. Cell. 1990 May 4;61(3):535–547. doi: 10.1016/0092-8674(90)90535-m. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Lew D. J., Dulić V., Reed S. I. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell. 1991 Sep 20;66(6):1197–1206. doi: 10.1016/0092-8674(91)90042-w. [DOI] [PubMed] [Google Scholar]
  52. Lew D. J., I Reed S. A proliferation of cyclins. Trends Cell Biol. 1992 Mar;2(3):77–81. doi: 10.1016/0962-8924(92)90076-y. [DOI] [PubMed] [Google Scholar]
  53. Lorca T., Labbé J. C., Devault A., Fesquet D., Strausfeld U., Nilsson J., Nygren P. A., Uhlen M., Cavadore J. C., Dorée M. Cyclin A-cdc2 kinase does not trigger but delays cyclin degradation in interphase extracts of amphibian eggs. J Cell Sci. 1992 May;102(Pt 1):55–62. doi: 10.1242/jcs.102.1.55. [DOI] [PubMed] [Google Scholar]
  54. Luca F. C., Shibuya E. K., Dohrmann C. E., Ruderman J. V. Both cyclin A delta 60 and B delta 97 are stable and arrest cells in M-phase, but only cyclin B delta 97 turns on cyclin destruction. EMBO J. 1991 Dec;10(13):4311–4320. doi: 10.1002/j.1460-2075.1991.tb05009.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Maridor G., Gallant P., Golsteyn R., Nigg E. A. Nuclear localization of vertebrate cyclin A correlates with its ability to form complexes with cdk catalytic subunits. J Cell Sci. 1993 Oct;106(Pt 2):535–544. doi: 10.1242/jcs.106.2.535. [DOI] [PubMed] [Google Scholar]
  56. Meijer L., Arion D., Golsteyn R., Pines J., Brizuela L., Hunt T., Beach D. Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J. 1989 Aug;8(8):2275–2282. doi: 10.1002/j.1460-2075.1989.tb08353.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Minshull J., Blow J. J., Hunt T. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis. Cell. 1989 Mar 24;56(6):947–956. doi: 10.1016/0092-8674(89)90628-4. [DOI] [PubMed] [Google Scholar]
  58. Minshull J., Golsteyn R., Hill C. S., Hunt T. The A- and B-type cyclin associated cdc2 kinases in Xenopus turn on and off at different times in the cell cycle. EMBO J. 1990 Sep;9(9):2865–2875. doi: 10.1002/j.1460-2075.1990.tb07476.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Motokura T., Arnold A. Cyclin D and oncogenesis. Curr Opin Genet Dev. 1993 Feb;3(1):5–10. doi: 10.1016/s0959-437x(05)80334-x. [DOI] [PubMed] [Google Scholar]
  60. Motokura T., Keyomarsi K., Kronenberg H. M., Arnold A. Cloning and characterization of human cyclin D3, a cDNA closely related in sequence to the PRAD1/cyclin D1 proto-oncogene. J Biol Chem. 1992 Oct 5;267(28):20412–20415. [PubMed] [Google Scholar]
  61. Mudryj M., Devoto S. H., Hiebert S. W., Hunter T., Pines J., Nevins J. R. Cell cycle regulation of the E2F transcription factor involves an interaction with cyclin A. Cell. 1991 Jun 28;65(7):1243–1253. doi: 10.1016/0092-8674(91)90019-u. [DOI] [PubMed] [Google Scholar]
  62. Murray A. W. Creative blocks: cell-cycle checkpoints and feedback controls. Nature. 1992 Oct 15;359(6396):599–604. doi: 10.1038/359599a0. [DOI] [PubMed] [Google Scholar]
  63. Nasmyth K. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol. 1993 Apr;5(2):166–179. doi: 10.1016/0955-0674(93)90099-c. [DOI] [PubMed] [Google Scholar]
  64. Nigg E. A., Gallant P., Krek W. Regulation of p34cdc2 protein kinase activity by phosphorylation and cyclin binding. Ciba Found Symp. 1992;170:72–96. doi: 10.1002/9780470514320.ch6. [DOI] [PubMed] [Google Scholar]
  65. Norbury C., Blow J., Nurse P. Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates. EMBO J. 1991 Nov;10(11):3321–3329. doi: 10.1002/j.1460-2075.1991.tb04896.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Norbury C., Nurse P. Animal cell cycles and their control. Annu Rev Biochem. 1992;61:441–470. doi: 10.1146/annurev.bi.61.070192.002301. [DOI] [PubMed] [Google Scholar]
  67. Ookata K., Hisanaga S., Okano T., Tachibana K., Kishimoto T. Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J. 1992 May;11(5):1763–1772. doi: 10.1002/j.1460-2075.1992.tb05228.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Padgett R. A., Grabowski P. J., Konarska M. M., Seiler S., Sharp P. A. Splicing of messenger RNA precursors. Annu Rev Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  69. Pagano M., Draetta G., Jansen-Dürr P. Association of cdk2 kinase with the transcription factor E2F during S phase. Science. 1992 Feb 28;255(5048):1144–1147. doi: 10.1126/science.1312258. [DOI] [PubMed] [Google Scholar]
  70. Pagano M., Pepperkok R., Lukas J., Baldin V., Ansorge W., Bartek J., Draetta G. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J Cell Biol. 1993 Apr;121(1):101–111. doi: 10.1083/jcb.121.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Pagano M., Pepperkok R., Verde F., Ansorge W., Draetta G. Cyclin A is required at two points in the human cell cycle. EMBO J. 1992 Mar;11(3):961–971. doi: 10.1002/j.1460-2075.1992.tb05135.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Palmero I., Holder A., Sinclair A. J., Dickson C., Peters G. Cyclins D1 and D2 are differentially expressed in human B-lymphoid cell lines. Oncogene. 1993 Apr;8(4):1049–1054. [PubMed] [Google Scholar]
  73. Peeper D. S., Parker L. L., Ewen M. E., Toebes M., Hall F. L., Xu M., Zantema A., van der Eb A. J., Piwnica-Worms H. A- and B-type cyclins differentially modulate substrate specificity of cyclin-cdk complexes. EMBO J. 1993 May;12(5):1947–1954. doi: 10.1002/j.1460-2075.1993.tb05844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Pines J. Cell proliferation and control. Curr Opin Cell Biol. 1992 Apr;4(2):144–148. doi: 10.1016/0955-0674(92)90024-7. [DOI] [PubMed] [Google Scholar]
  75. Pines J. Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem Sci. 1993 Jun;18(6):195–197. doi: 10.1016/0968-0004(93)90185-p. [DOI] [PubMed] [Google Scholar]
  76. Pines J. Cyclins: wheels within wheels. Cell Growth Differ. 1991 Jun;2(6):305–310. [PubMed] [Google Scholar]
  77. Pines J., Hunter T. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature. 1990 Aug 23;346(6286):760–763. doi: 10.1038/346760a0. [DOI] [PubMed] [Google Scholar]
  78. Pines J., Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J Cell Biol. 1991 Oct;115(1):1–17. doi: 10.1083/jcb.115.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Pines J., Hunter T. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell. 1989 Sep 8;58(5):833–846. doi: 10.1016/0092-8674(89)90936-7. [DOI] [PubMed] [Google Scholar]
  80. Reed S. I. G1-specific cyclins: in search of an S-phase-promoting factor. Trends Genet. 1991 Mar;7(3):95–99. doi: 10.1016/0168-9525(91)90279-Y. [DOI] [PubMed] [Google Scholar]
  81. Riabowol K., Draetta G., Brizuela L., Vandre D., Beach D. The cdc2 kinase is a nuclear protein that is essential for mitosis in mammalian cells. Cell. 1989 May 5;57(3):393–401. doi: 10.1016/0092-8674(89)90914-8. [DOI] [PubMed] [Google Scholar]
  82. Richardson H., Lew D. J., Henze M., Sugimoto K., Reed S. I. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 1992 Nov;6(11):2021–2034. doi: 10.1101/gad.6.11.2021. [DOI] [PubMed] [Google Scholar]
  83. Rosenblatt J., Gu Y., Morgan D. O. Human cyclin-dependent kinase 2 is activated during the S and G2 phases of the cell cycle and associates with cyclin A. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2824–2828. doi: 10.1073/pnas.89.7.2824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Sap J., Muñoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986 Dec 18;324(6098):635–640. doi: 10.1038/324635a0. [DOI] [PubMed] [Google Scholar]
  85. Schwob E., Nasmyth K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 1993 Jul;7(7A):1160–1175. doi: 10.1101/gad.7.7a.1160. [DOI] [PubMed] [Google Scholar]
  86. Sherr C. J. Mammalian G1 cyclins. Cell. 1993 Jun 18;73(6):1059–1065. doi: 10.1016/0092-8674(93)90636-5. [DOI] [PubMed] [Google Scholar]
  87. Shirodkar S., Ewen M., DeCaprio J. A., Morgan J., Livingston D. M., Chittenden T. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in a cell cycle-regulated manner. Cell. 1992 Jan 10;68(1):157–166. doi: 10.1016/0092-8674(92)90214-w. [DOI] [PubMed] [Google Scholar]
  88. Solomon M. J. Activation of the various cyclin/cdc2 protein kinases. Curr Opin Cell Biol. 1993 Apr;5(2):180–186. doi: 10.1016/0955-0674(93)90100-5. [DOI] [PubMed] [Google Scholar]
  89. Standart N., Minshull J., Pines J., Hunt T. Cyclin synthesis, modification and destruction during meiotic maturation of the starfish oocyte. Dev Biol. 1987 Nov;124(1):248–258. doi: 10.1016/0012-1606(87)90476-3. [DOI] [PubMed] [Google Scholar]
  90. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  91. Surana U., Robitsch H., Price C., Schuster T., Fitch I., Futcher A. B., Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 1991 Apr 5;65(1):145–161. doi: 10.1016/0092-8674(91)90416-v. [DOI] [PubMed] [Google Scholar]
  92. Swenson K. I., Farrell K. M., Ruderman J. V. The clam embryo protein cyclin A induces entry into M phase and the resumption of meiosis in Xenopus oocytes. Cell. 1986 Dec 26;47(6):861–870. doi: 10.1016/0092-8674(86)90801-9. [DOI] [PubMed] [Google Scholar]
  93. Th'ng J. P., Wright P. S., Hamaguchi J., Lee M. G., Norbury C. J., Nurse P., Bradbury E. M. The FT210 cell line is a mouse G2 phase mutant with a temperature-sensitive CDC2 gene product. Cell. 1990 Oct 19;63(2):313–324. doi: 10.1016/0092-8674(90)90164-a. [DOI] [PubMed] [Google Scholar]
  94. Thomas L., Clarke P. R., Pagano M., Gruenberg J. Inhibition of membrane fusion in vitro via cyclin B but not cyclin A. J Biol Chem. 1992 Mar 25;267(9):6183–6187. [PubMed] [Google Scholar]
  95. Verde F., Dogterom M., Stelzer E., Karsenti E., Leibler S. Control of microtubule dynamics and length by cyclin A- and cyclin B-dependent kinases in Xenopus egg extracts. J Cell Biol. 1992 Sep;118(5):1097–1108. doi: 10.1083/jcb.118.5.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Walker D. H., Maller J. L. Role for cyclin A in the dependence of mitosis on completion of DNA replication. Nature. 1991 Nov 28;354(6351):314–317. doi: 10.1038/354314a0. [DOI] [PubMed] [Google Scholar]
  97. Wang J., Chenivesse X., Henglein B., Bréchot C. Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature. 1990 Feb 8;343(6258):555–557. doi: 10.1038/343555a0. [DOI] [PubMed] [Google Scholar]
  98. Westendorf J. M., Swenson K. I., Ruderman J. V. The role of cyclin B in meiosis I. J Cell Biol. 1989 Apr;108(4):1431–1444. doi: 10.1083/jcb.108.4.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Whitfield W. G., Gonzalez C., Maldonado-Codina G., Glover D. M. The A- and B-type cyclins of Drosophila are accumulated and destroyed in temporally distinct events that define separable phases of the G2-M transition. EMBO J. 1990 Aug;9(8):2563–2572. doi: 10.1002/j.1460-2075.1990.tb07437.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Xiong Y., Beach D. Population explosion in the cyclin family. Curr Biol. 1991 Dec;1(6):362–364. doi: 10.1016/0960-9822(91)90193-z. [DOI] [PubMed] [Google Scholar]
  101. Xiong Y., Connolly T., Futcher B., Beach D. Human D-type cyclin. Cell. 1991 May 17;65(4):691–699. doi: 10.1016/0092-8674(91)90100-d. [DOI] [PubMed] [Google Scholar]
  102. Zindy F., Lamas E., Chenivesse X., Sobczak J., Wang J., Fesquet D., Henglein B., Bréchot C. Cyclin A is required in S phase in normal epithelial cells. Biochem Biophys Res Commun. 1992 Feb 14;182(3):1144–1154. doi: 10.1016/0006-291x(92)91851-g. [DOI] [PubMed] [Google Scholar]
  103. van Loon A. E., Colas P., Goedemans H. J., Néant I., Dalbon P., Guerrier P. The role of cyclins in the maturation of Patella vulgata oocytes. EMBO J. 1991 Nov;10(11):3343–3349. doi: 10.1002/j.1460-2075.1991.tb04898.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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