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PMID: 2351692 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Protein synthesis and the cell cycle: centrosome reproduction in sea urchin eggs is not under translational control.

The Journal of cell biology ·Vol. 110 ·No. 6 ·1990-06-00 ·Pages 2025-32

Sluder G, Miller FJ, Cole R, Rieder CL

Abstract

The reproduction, or duplication, of the centrosome is an important event in a cell's preparation for mitosis. We sought to determine if centrosome reproduction is regulated by the synthesis and accumulation of cyclin proteins and/or the synthesis of centrosome-specific proteins at each cell cycle. We continuously treat sea urchin eggs, starting before fertilization, with a combination of emetine and anisomycin, drugs that have separate targets in the protein synthetic pathway. These drugs inhibit the postfertilization incorporation of [35S]methionine into precipitable material by 97.3-100%. Autoradiography of SDS-PAGE gels of drug-treated zygotes reveals that [35S]methionine incorporates exclusively into material that does not enter the gel and material that runs at the dye front; no other labeled bands are detected. Fertilization events and syngamy are normal in drug-treated zygotes, but the cell cycle arrests before first mitosis. The sperm aster doubles once in all zygotes to yield two asters. In a variable but significant percentage of zygotes, the asters continue to double. This continued doubling is slower than normal, asynchronous between zygotes, and sometimes asynchronous within individual zygotes. High voltage electron microscopy of serial semithick sections from drug-treated zygotes reveals that 90% of the daughter centrosomes contain two centrioles of normal appearance. From these results, we conclude that centrosome reproduction in sea urchin zygotes is not controlled by the accumulation of cyclin proteins or the synthesis of centrosome-specific proteins at each cell cycle. New centrosomes are assembled from preexisting pools of ready-to-use subunits. Furthermore, our results indicate that centrosomal and nuclear events are regulated by separate pathways.

MeSH Terms
Animals Anisomycin/pharmacology Cell Cycle/physiology Centrioles/physiology,ultrastructure Egg Proteins/biosynthesis,genetics Emetine/pharmacology Microscopy, Electron Ovum/cytology,metabolism,ultrastructure Protein Biosynthesis/drug effects,physiology Ribosomes/drug effects,physiology,ultrastructure Sea Urchins Spindle Apparatus/physiology,ultrastructure
Chemicals
Egg Proteins Anisomycin Emetine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sluder G
Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 01545.
Miller F J
Cole R
Rieder C L
References (30)
30 references, click to expand
  1. Purification and characterization of Chlamydomonas flagellar dyneins.
    Methods Enzymol. 1986;134:291-306 PMID: 3029544
  2. The reproduction of centrosomes: nuclear versus cytoplasmic controls.
    J Cell Biol. 1986 Nov;103(5):1873-81 PMID: 3782286
  3. Fine structural studies of the bipolarization of the mitotic apparatus in the fertilized sea urchin egg. I. The structure and behavior of centrosomes before fusion of the pronuclei.
    Eur J Cell Biol. 1987 Oct;44(2):195-204 PMID: 3691547
  4. Relationship between nuclear DNA synthesis and centrosome reproduction in sea urchin eggs.
    J Exp Zool. 1987 Oct;244(1):89-100 PMID: 3694143
  5. 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
  6. Reproductive capacity of sea urchin centrosomes without centrioles.
    Cell Motil Cytoskeleton. 1989;13(4):264-73 PMID: 2776224
  7. Basal body/centriolar DNA: molecular genetic studies in Chlamydomonas.
    Cell. 1989 Oct 6;59(1):121-32 PMID: 2571418
  8. 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
  9. Simple and complex cell cycles.
    Annu Rev Cell Biol. 1989;5:341-96 PMID: 2574592
  10. Cyclin is a component of maturation-promoting factor from Xenopus.
    Cell. 1990 Feb 9;60(3):487-94 PMID: 1967981
  11. Some structural and functional aspects of the mitotic apparatus in sea urchin embryos.
    J Cell Biol. 1962 Sep;14:475-87 PMID: 13952946
  12. THE DNA SYNTHETIC PERIOD DURING EARLY DEVELOPMENT OF THE SEA URCHIN EGG.
    Exp Cell Res. 1964 Oct;36:53-61 PMID: 14222747
  13. Protein synthesis in sea urchin eggs: a "late" response to fertilization.
    Proc Natl Acad Sci U S A. 1967 Apr;57(4):899-906 PMID: 5232369
  14. The centriole cycle in synchronized HeLa cells.
    J Cell Biol. 1968 Feb;36(2):329-39 PMID: 5638885
  15. Activation of an Na + -dependent amino acid transport system upon fertilization of sea urchin eggs.
    Exp Cell Res. 1972 May;72(1):74-89 PMID: 4337147
  16. Mitosis.
    Adv Cell Biol. 1971;2:225-97 PMID: 5005502
  17. Repetitive procurement of mature gametes from individual sea stars and sea urchins.
    J Cell Biol. 1973 Jun;57(3):879-81 PMID: 4698908
  18. Dependence of centriole formation on protein synthesis.
    J Cell Biol. 1976 Jul;70(1):9-19 PMID: 932104
  19. The pericentriolar material in Chinese hamster ovary cells nucleates microtubule formation.
    J Cell Biol. 1977 Jun;73(3):601-15 PMID: 559676
  20. Dual ionic controls for the activation of protein synthesis at fertilization.
    Nature. 1980 Oct 9;287(5782):558-60 PMID: 7422008
  21. Structural polarity of kinetochore microtubules in PtK1 cells.
    J Cell Biol. 1981 May;89(2):338-45 PMID: 7251657
  22. Thick and thin serial sectioning for the three-dimensional reconstruction of biological ultrastructure.
    Methods Cell Biol. 1981;22:215-49 PMID: 6167835
  23. The timing of synthesis of proteins required for mitosis in the cell cycle of the sea urchin embryo.
    Exp Cell Res. 1983 Apr 1;144(2):393-403 PMID: 6840219
  24. Activity and stability of centrosomes in Chinese hamster ovary cells in nucleation of microtubules in vitro.
    J Cell Sci. 1984 Mar;66:277-95 PMID: 6540269
  25. Centriole number and the reproductive capacity of spindle poles.
    J Cell Biol. 1985 Mar;100(3):887-96 PMID: 3972899
  26. Experimental separation of pronuclei in fertilized sea urchin eggs: chromosomes do not organize a spindle in the absence of centrosomes.
    J Cell Biol. 1985 Mar;100(3):897-903 PMID: 3972900
  27. The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs.
    J Cell Biol. 1985 Jun;100(6):1968-76 PMID: 2987274
  28. Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs.
    Proc Natl Acad Sci U S A. 1986 Jan;83(1):105-9 PMID: 2417231
  29. Transient synthesis of a specific set of proteins during the rapid cleavage phase of sea urchin development.
    Dev Biol. 1986 Apr;114(2):403-15 PMID: 3956873
  30. The centrosome and its role in the organization of microtubules.
    Int Rev Cytol. 1987;106:227-93 PMID: 3294718
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1990-06-00
Pages
2025-32
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2116128
Subset
IM
Grants
NIGMS NIH HHS · GM-30758 · United States
NIGMS NIH HHS · GM-40198 · United States
PHS HHS · P0 30-12708 · United States
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