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PMID: 2142452 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

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.

The EMBO journal ·Vol. 9 ·No. 8 ·1990-08-00 ·Pages 2563-72

Whitfield WG, Gonzalez C, Maldonado-Codina G, Glover DM

Abstract

We show that the sequence of Drosophila cyclin B has greater identity with B-type cyclins from other animal phyla than with Drosophila cyclin A, suggesting that the two cyclins have distinct roles that have been maintained in evolution. Cyclin A is not detectable in unfertilized eggs and is present at low levels prior to cellularization of the syncytial embryo. In contrast, the levels of cyclin B remain uniformly high throughout these developmental stages. In cells within cellularized embryos and the larval brain, cyclin A accumulates to peak levels in prophase and is degraded throughout the period in which chromosomes are becoming aligned on the metaphase plate. The degradation of cyclin B, on the other hand, does not occur until the metaphase-anaphase transition. In cells arrested at c-metaphase by treating with microtubule destabilizing drugs to prevent spindle formation, cyclin A has been degraded in the arrested cells, whereas cyclin B is maintained at high levels. These observations suggest that cyclin A has a role in the G2-M transition that is independent of spindle formation, and that entry into anaphase is a key requirement for the degradation of cyclin B.

MeSH Terms
Amino Acid Sequence Animals Antibodies/isolation & purification Base Sequence Bivalvia/genetics Blotting, Western Cell Cycle Cell Division Cloning, Molecular Cyclins Drosophila/embryology,genetics Electrophoresis, Polyacrylamide Gel Embryo, Nonmammalian/cytology,physiology Gene Library Invertebrate Hormones/genetics,isolation & purification,metabolism Mitosis Molecular Sequence Data Sequence Homology, Nucleic Acid
Chemicals
Antibodies Cyclins Invertebrate Hormones
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Whitfield W G
Department of Biochemistry, The University, Dundee, Scotland.
Gonzalez C
Maldonado-Codina G
Glover D M
References (46)
46 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase.
    Cell. 1989 Jul 14;58(1):181-91 PMID: 2473838
  3. Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone.
    Dev Biol. 1974 Jun;38(2):394-400 PMID: 4545456
  4. Molecular features of colchicine associated with antimitotic activity and inhibition of tubulin polymerization.
    Biochem Pharmacol. 1976 Jun 15;25(12):1383-7 PMID: 938560
  5. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  6. A cytoplasmic clock with the same period as the division cycle in Xenopus eggs.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):462-6 PMID: 6928638
  7. Optimal spatial requirements for the location of basic residues in peptide substrates for the cyclic AMP-dependent protein kinase.
    J Biol Chem. 1980 May 10;255(9):4240-5 PMID: 6246116
  8. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences.
    Nucleic Acids Res. 1982 May 11;10(9):2951-61 PMID: 7099970
  9. Functionally homologous cell cycle control genes in budding and fission yeast.
    Nature. 1982 Dec 23;300(5894):706-9 PMID: 6757758
  10. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division.
    Cell. 1983 Jun;33(2):389-96 PMID: 6134587
  11. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis.
    J Cell Sci. 1983 May;61:31-70 PMID: 6411748
  12. Localization of antigenic determinants in whole Drosophila embryos.
    Dev Biol. 1983 Sep;99(1):261-4 PMID: 6194030
  13. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs.
    J Cell Biol. 1984 Apr;98(4):1247-55 PMID: 6425302
  14. Proteins shifting from the cytoplasm into the nuclei during early embryogenesis of Drosophila melanogaster.
    Dev Biol. 1984 Jul;104(1):37-48 PMID: 6428951
  15. The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila.
    Cell. 1986 Aug 1;46(3):457-68 PMID: 3089628
  16. 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):861-70 PMID: 2946420
  17. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes.
    J Mol Biol. 1986 May 5;189(1):113-30 PMID: 3537305
  18. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates.
    Nucleic Acids Res. 1987 Feb 25;15(4):1353-61 PMID: 3822832
  19. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2.
    Nature. 1987 May 7-13;327(6117):31-5 PMID: 3553962
  20. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster.
    Dev Biol. 1988 Jan;125(1):145-57 PMID: 3119399
  21. Molecular cloning and characterization of the mRNA for cyclin from sea urchin eggs.
    EMBO J. 1987 Oct;6(10):2987-95 PMID: 2826125
  22. Interaction between cdc13+ and cdc2+ in the control of mitosis in fission yeast; dissociation of the G1 and G2 roles of the cdc2+ protein kinase.
    EMBO J. 1987 Nov;6(11):3441-7 PMID: 3428262
  23. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+.
    Cell. 1988 Jul 29;54(3):433-9 PMID: 3293803
  24. Cyclin in fission yeast.
    Cell. 1988 Sep 9;54(6):738-40 PMID: 2900688
  25. Activation at M-phase of a protein kinase encoded by a starfish homologue of the cell cycle control gene cdc2+.
    Nature. 1988 Sep 15;335(6187):251-4 PMID: 3412486
  26. cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF.
    Cell. 1988 Oct 21;55(2):371-8 PMID: 2844417
  27. Involvement of cdc13+ in mitotic control in Schizosaccharomyces pombe: possible interaction of the gene product with microtubules.
    EMBO J. 1988 Aug;7(8):2321-7 PMID: 2847913
  28. Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis.
    Cell. 1989 Jul 14;58(1):193-203 PMID: 2473839
  29. Cloning and sequencing of the cyclin-related cdc13+ gene and a cytological study of its role in fission yeast mitosis.
    J Cell Sci. 1988 Dec;91 ( Pt 4):587-95 PMID: 2908246
  30. 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):833-46 PMID: 2570636
  31. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis.
    Nature. 1989 Nov 2;342(6245):39-45 PMID: 2682257
  32. Directing cell division during development.
    Science. 1989 Nov 3;246(4930):635-40 PMID: 2683080
  33. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B.
    EMBO J. 1989 Oct;8(10):3053-8 PMID: 2531073
  34. Mitotic domains reveal early commitment of cells in Drosophila embryos.
    Development. 1989 Sep;107(1):1-22 PMID: 2516798
  35. The role of cyclin synthesis, modification and destruction in the control of cell division.
    J Cell Sci Suppl. 1989;12:77-97 PMID: 2534558
  36. Cyclin synthesis, modification and destruction during meiotic maturation of the starfish oocyte.
    Dev Biol. 1987 Nov;124(1):248-58 PMID: 15669148
  37. Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2009-19 PMID: 3143733
  38. Transcripts of one of two Drosophila cyclin genes become localized in pole cells during embryogenesis.
    Nature. 1989 Mar 23;338(6213):337-40 PMID: 2564167
  39. Cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF.
    Cell. 1989 Mar 10;56(5):829-38 PMID: 2538242
  40. Expression and function of Drosophila cyclin A during embryonic cell cycle progression.
    Cell. 1989 Mar 24;56(6):957-68 PMID: 2564316
  41. The role of cyclin B in meiosis I.
    J Cell Biol. 1989 Apr;108(4):1431-44 PMID: 2522454
  42. Genetic control of cell division patterns in the Drosophila embryo.
    Cell. 1989 Apr 7;57(1):177-87 PMID: 2702688
  43. Purification of MPF from starfish: identification as the H1 histone kinase p34cdc2 and a possible mechanism for its periodic activation.
    Cell. 1989 Apr 21;57(2):253-63 PMID: 2649251
  44. Cyclin synthesis drives the early embryonic cell cycle.
    Nature. 1989 May 25;339(6222):275-80 PMID: 2566917
  45. Dephosphorylation and activation of Xenopus p34cdc2 protein kinase during the cell cycle.
    Nature. 1989 Jun 22;339(6226):626-9 PMID: 2543932
  46. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes.
    J Exp Zool. 1971 Jun;177(2):129-45 PMID: 5106340
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1990-08-00
Pages
2563-72
Language
English
Region
England
NLM ID
8208664
PMCID
PMC552287
Subset
IM
Databases
GENBANK
X55542
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