Home LiteratureArticle Details
PMID: 9606208 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

ZYG-9, a Caenorhabditis elegans protein required for microtubule organization and function, is a component of meiotic and mitotic spindle poles.

The Journal of cell biology ·Vol. 141 ·No. 5 ·1998-06-01 ·Pages 1159-68

Matthews LR, Carter P, Thierry-Mieg D, Kemphues K

Abstract

We describe the molecular characterization of zyg-9, a maternally acting gene essential for microtubule organization and function in early Caenorhabditis elegans embryos. Defects in zyg-9 mutants suggest that the zyg-9 product functions in the organization of the meiotic spindle and the formation of long microtubules. One-cell zyg-9 embryos exhibit both meiotic and mitotic spindle defects. Meiotic spindles are disorganized, pronuclear migration fails, and the mitotic apparatus forms at the posterior, orients incorrectly, and contains unusually short microtubules. We find that zyg-9 encodes a component of the meiotic and mitotic spindle poles. In addition to the strong staining of spindle poles, we consistently detect staining in the region of the kinetochore microtubules at metaphase and early anaphase in mitotic spindles. The ZYG-9 signal at the mitotic centrosomes is not reduced by nocodazole treatment, indicating that ZYG-9 localization to the mitotic centrosomes is not dependent upon long astral microtubules. Interestingly, in embryos lacking an organized meiotic spindle, produced either by nocodazole treatment or mutations in the mei-1 gene, ZYG-9 forms a halo around the meiotic chromosomes. The protein sequence shows partial similarity to a small set of proteins that also localize to spindle poles, suggesting a common activity of the proteins.

MeSH Terms
Adenosine Triphosphatases/genetics Amino Acid Sequence Animals Caenorhabditis elegans/physiology Caenorhabditis elegans Proteins Cloning, Molecular Helminth Proteins/genetics,metabolism,physiology Humans Meiosis/physiology Microtubules/physiology Mitosis/physiology Molecular Sequence Data Mutation Sequence Homology, Amino Acid Spindle Apparatus/physiology
Chemicals
Caenorhabditis elegans Proteins Helminth Proteins ZYG-9 protein, C elegans Adenosine Triphosphatases MEI-1 protein, C elegans
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Matthews L R
Section of Genetics and Development, Cornell University, Ithaca, New York 14850, USA.
Carter P
Thierry-Mieg D
Kemphues K
References (43)
43 references, click to expand
  1. The Saccharomyces cerevisiae kinesin-related motor Kar3p acts at preanaphase spindle poles to limit the number and length of cytoplasmic microtubules.
    J Cell Biol. 1997 Apr 21;137(2):417-31 PMID: 9128252
  2. 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):1097-108 PMID: 1387400
  3. Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component.
    J Cell Biol. 1994 Jul;126(1):199-209 PMID: 8027178
  4. Maternal-effect lethal mutations on linkage group II of Caenorhabditis elegans.
    Genetics. 1988 Dec;120(4):977-86 PMID: 3224814
  5. Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts.
    Cell. 1991 Feb 22;64(4):827-39 PMID: 1671762
  6. Dominant maternal-effect mutations causing embryonic lethality in Caenorhabditis elegans.
    Genetics. 1990 Jun;125(2):351-69 PMID: 2379819
  7. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed.
    Cell. 1995 May 19;81(4):611-20 PMID: 7758115
  8. Cold-sensitive and caffeine-supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis.
    EMBO J. 1988 May;7(5):1465-73 PMID: 3409871
  9. The TOGp protein is a new human microtubule-associated protein homologous to the Xenopus XMAP215.
    J Cell Sci. 1998 May;111 ( Pt 10):1371-83 PMID: 9570755
  10. Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans.
    Dev Biol. 1986 Feb;113(2):449-60 PMID: 3949074
  11. XMAP310: a Xenopus rescue-promoting factor localized to the mitotic spindle.
    J Cell Biol. 1997 Nov 17;139(4):975-83 PMID: 9362515
  12. Characterization of the cDNA and pattern of expression of a new gene over-expressed in human hepatomas and colonic tumors.
    Eur J Biochem. 1995 Dec 1;234(2):406-13 PMID: 8536682
  13. Effect on microtubule dynamics of XMAP230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells.
    J Cell Biol. 1994 Dec;127(5):1289-99 PMID: 7962090
  14. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos.
    Cell. 1997 Aug 22;90(4):707-16 PMID: 9288750
  15. Gamma-tubulin is a highly conserved component of the centrosome.
    Cell. 1991 May 31;65(5):825-36 PMID: 1840506
  16. mei-1, a gene required for meiotic spindle formation in Caenorhabditis elegans, is a member of a family of ATPases.
    Genetics. 1994 Feb;136(2):533-46 PMID: 8150281
  17. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.
    EMBO J. 1991 Dec;10(12):3959-70 PMID: 1935914
  18. The Tc3 family of transposable genetic elements in Caenorhabditis elegans.
    Genetics. 1989 Jan;121(1):47-55 PMID: 2537252
  19. pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos.
    Cell. 1995 Nov 17;83(4):599-609 PMID: 7585963
  20. Katanin, the microtubule-severing ATPase, is concentrated at centrosomes.
    J Cell Sci. 1996 Mar;109 ( Pt 3):561-7 PMID: 8907702
  21. Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos.
    Cell. 1996 Oct 18;87(2):217-26 PMID: 8861906
  22. Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex.
    Nature. 1995 Dec 7;378(6557):578-83 PMID: 8524390
  23. Stu2p: A microtubule-binding protein that is an essential component of the yeast spindle pole body.
    J Cell Biol. 1997 Dec 1;139(5):1271-80 PMID: 9382872
  24. MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos.
    Cell. 1996 Oct 18;87(2):205-16 PMID: 8861905
  25. A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites.
    Genetics. 1992 Jul;131(3):609-24 PMID: 1321065
  26. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  27. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end.
    J Cell Biol. 1987 Nov;105(5):2203-15 PMID: 2890645
  28. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  29. gamma-tubulin is a minus end-specific microtubule binding protein.
    J Cell Biol. 1995 Oct;131(1):207-14 PMID: 7559777
  30. Confocal immunofluorescence microscopy of microtubules, microtubule-associated proteins, and microtubule-organizing centers during amphibian oogenesis and early development.
    Curr Top Dev Biol. 1995;31:383-431 PMID: 8746671
  31. The temporal and spatial relationships between cortical contraction, sperm trail formation, and pronuclear migration in fertilizedXenopus eggs.
    Wilehm Roux Arch Dev Biol. 1982 Jul;191(4):241-245 PMID: 28305054
  32. The Caenorhabditis elegans NK-2 class homeoprotein CEH-22 is involved in combinatorial activation of gene expression in pharyngeal muscle.
    Development. 1994 Aug;120(8):2175-86 PMID: 7925019
  33. Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo.
    Genetics. 1990 Nov;126(3):593-605 PMID: 2249759
  34. The genome of Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10836-40 PMID: 7479894
  35. Dissection of fission yeast microtubule associating protein p93Dis1: regions implicated in regulated localization and microtubule interaction.
    Genes Cells. 1996 Jul;1(7):633-44 PMID: 9078390
  36. XMAP from Xenopus eggs promotes rapid plus end assembly of microtubules and rapid microtubule polymer turnover.
    J Cell Biol. 1994 Nov;127(4):985-93 PMID: 7962080
  37. Pericentrin, a highly conserved centrosome protein involved in microtubule organization.
    Cell. 1994 Feb 25;76(4):639-50 PMID: 8124707
  38. The PIE-1 protein and germline specification in C. elegans embryos.
    Nature. 1996 Aug 22;382(6593):710-2 PMID: 8751440
  39. p93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites.
    Genes Dev. 1995 Jul 1;9(13):1572-85 PMID: 7628693
  40. Morphogenetic properties of microtubules and mitotic spindle assembly.
    Cell. 1996 Feb 9;84(3):401-10 PMID: 8608594
  41. Identification of katanin, an ATPase that severs and disassembles stable microtubules.
    Cell. 1993 Nov 5;75(3):419-29 PMID: 8221885
  42. Formation of the first cleavage spindle in nematode embryos.
    Dev Biol. 1984 Jan;101(1):61-72 PMID: 6692980
  43. Parental effects and phenotypic characterization of mutations that affect early development in Caenorhabditis elegans.
    Dev Biol. 1980 Feb;74(2):446-69 PMID: 7371984
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1998-06-01
Pages
1159-68
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2137183
Subset
IM
Grants
NICHD NIH HHS · HD27689 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]