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PMID: 9585508 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis.

Genes & development ·Vol. 12 ·No. 10 ·1998-05-15 ·Pages 1483-94

Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM

Abstract

Mutations in the Drosophila gene pavarotti result in the formation of abnormally large cells in the embryonic nervous system. In mitotic cycle 16, cells of pav mutant embryos undergo normal anaphase but then develop an abnormal telophase spindle and fail to undertake cytokinesis. We show that the septin Peanut, actin, and the actin-associated protein Anillin, do not become correctly localized in pav mutants. pav encodes a kinesin-like protein, PAV-KLP, related to the mammalian MKLP-1. In cellularized embryos, the protein is localized to centrosomes early in mitosis, and to the midbody region of the spindle in late anaphase and telophase. We show that Polo kinase associates with PAV-KLP with which it shows an overlapping pattern of subcellular localization during the mitotic cycle and this distribution is disrupted in pav mutants. We suggest that PAV-KLP is required both to establish the structure of the telophase spindle to provide a framework for the assembly of the contractile ring, and to mobilize mitotic regulator proteins.

MeSH Terms
Actins/metabolism Amino Acid Sequence Animals Cell Division/genetics Cell Size Centrosome/ultrastructure Cloning, Molecular Contractile Proteins/metabolism Drosophila Proteins Drosophila melanogaster/cytology,embryology,genetics Embryo, Nonmammalian/ultrastructure Genes, Insect Insect Proteins/genetics,metabolism,physiology Mammals/metabolism Microfilament Proteins Microtubule-Associated Proteins/chemistry,genetics,physiology Molecular Sequence Data Nervous System/cytology,embryology Protein Serine-Threonine Kinases/metabolism Sequence Alignment Sequence Homology, Amino Acid Species Specificity Spindle Apparatus/ultrastructure Subcellular Fractions/chemistry Telophase/genetics
Chemicals
Actins Contractile Proteins Drosophila Proteins Insect Proteins Microfilament Proteins Microtubule-Associated Proteins anillin pav protein, Drosophila pnut protein, Drosophila polo protein, Drosophila Protein Serine-Threonine Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Adams R R
Cancer Research Campaign (CRC) Laboratories, Cell Cycle Genetics Research Group, Department of Anatomy and Physiology, Medical Sciences Institute, University of Dundee, Dundee DD1 4HN, UK. d.m.glover@dundee.ac.uk
Tavares A A
Salzberg A
Bellen H J
Glover D M
References (48)
48 references, click to expand
  1. Nuclear antigens follow different pathways into daughter nuclei during mitosis in early Drosophila embryos.
    J Cell Sci. 1986 Jun;82:155-72 PMID: 3098744
  2. Plk is an M-phase-specific protein kinase and interacts with a kinesin-like protein, CHO1/MKLP-1.
    Mol Cell Biol. 1995 Dec;15(12):7143-51 PMID: 8524282
  3. Plk is a functional homolog of Saccharomyces cerevisiae Cdc5, and elevated Plk activity induces multiple septation structures.
    Mol Cell Biol. 1997 Jun;17(6):3408-17 PMID: 9154840
  4. Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation.
    J Cell Sci. 1991 Apr;98 ( Pt 4):443-61 PMID: 1860899
  5. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex.
    J Cell Biol. 1995 Oct;131(1):165-78 PMID: 7559773
  6. A kinesin-like protein required for distributive chromosome segregation in Drosophila.
    Cell. 1990 Sep 21;62(6):1053-62 PMID: 2144792
  7. Interpolar spindle microtubules in PTK cells.
    J Cell Biol. 1993 Dec;123(6 Pt 1):1475-89 PMID: 8253845
  8. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins.
    Cell. 1994 May 6;77(3):371-9 PMID: 8181057
  9. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor.
    Cell. 1990 Dec 21;63(6):1159-65 PMID: 2261638
  10. 'Anaphase' and cytokinesis in the absence of chromosomes.
    Nature. 1996 Aug 1;382(6590):466-8 PMID: 8684488
  11. Genetic Control of the Cell Division Cycle in Yeast: V. Genetic Analysis of cdc Mutants.
    Genetics. 1973 Jun;74(2):267-86 PMID: 17248617
  12. polo, a mitotic mutant of Drosophila displaying abnormal spindle poles.
    J Cell Sci. 1988 Jan;89 ( Pt 1):25-38 PMID: 3417791
  13. The conserved mitotic kinase polo is regulated by phosphorylation and has preferred microtubule-associated substrates in Drosophila embryo extracts.
    EMBO J. 1996 Sep 16;15(18):4873-83 PMID: 8890161
  14. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells.
    J Cell Biol. 1988 Feb;106(2):431-9 PMID: 2448315
  15. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes.
    J Cell Biol. 1996 Dec;135(6 Pt 2):1701-13 PMID: 8991084
  16. The kinesin-like protein KLP61F is essential for mitosis in Drosophila.
    J Cell Biol. 1993 Nov;123(3):665-79 PMID: 8227131
  17. Delay of HeLa cell cleavage into interphase using dihydrocytochalasin B: retention of a postmitotic spindle and telophase disc correlates with synchronous cleavage recovery.
    J Cell Biol. 1995 Oct;131(1):191-205 PMID: 7559776
  18. Experiments concerning the cleavage stimulus in sand dollar eggs.
    J Exp Zool. 1961 Oct;148:81-9 PMID: 14490383
  19. The white gene as a marker in a new P-element vector for gene transfer in Drosophila.
    Nucleic Acids Res. 1987 May 26;15(10):3947-59 PMID: 3108854
  20. Mutation of a gene for a Drosophila kinesin-like protein, Klp38B, leads to failure of cytokinesis.
    J Cell Sci. 1997 Apr;110 ( Pt 8):945-54 PMID: 9152020
  21. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles.
    Nature. 1992 Oct 8;359(6395):543-7 PMID: 1406973
  22. Functional cDNA libraries from Drosophila embryos.
    J Mol Biol. 1988 Sep 20;203(2):425-37 PMID: 3199441
  23. The conserved Schizosaccharomyces pombe kinase plo1, required to form a bipolar spindle, the actin ring, and septum, can drive septum formation in G1 and G2 cells.
    Genes Dev. 1995 May 1;9(9):1059-73 PMID: 7744248
  24. Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells.
    J Cell Biol. 1996 Nov;135(4):981-9 PMID: 8922381
  25. Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells.
    J Cell Biol. 1997 Mar 24;136(6):1169-83 PMID: 9087435
  26. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells.
    Mol Biol Cell. 1996 Feb;7(2):225-32 PMID: 8688554
  27. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: mutations affecting embryonic PNS development.
    Genetics. 1997 Dec;147(4):1723-41 PMID: 9409832
  28. Isolation and characterization of the gene encoding the heavy chain of Drosophila kinesin.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1864-8 PMID: 3126498
  29. Mitosis in vertebrate somatic cells with two spindles: implications for the metaphase/anaphase transition checkpoint and cleavage.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5107-12 PMID: 9144198
  30. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development.
    Neuron. 1994 Aug;13(2):269-87 PMID: 8060613
  31. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F.
    Genetics. 1997 Dec;147(4):1697-722 PMID: 9409831
  32. Cloning of a gene encoding an antigen associated with the centrosome in Drosophila.
    J Cell Sci. 1988 Apr;89 ( Pt 4):467-80 PMID: 3143740
  33. Telophase disc: a new mammalian mitotic organelle that bisects telophase cells with a possible function in cytokinesis.
    J Cell Sci. 1991 Jul;99 ( Pt 3):523-34 PMID: 1939370
  34. Microdissection studies on the dividing neuroblast of the grasshopper, with special reference to the mechanism of unequal cytokinesis.
    Exp Cell Res. 1977 Apr;106(1):127-37 PMID: 852508
  35. The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs.
    J Cell Biol. 1972 May;53(2):419-34 PMID: 5063470
  36. Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning.
    Cell. 1995 Apr 7;81(1):117-27 PMID: 7720067
  37. polo encodes a protein kinase homolog required for mitosis in Drosophila.
    Genes Dev. 1991 Dec;5(12A):2153-65 PMID: 1660828
  38. The septins: roles in cytokinesis and other processes.
    Curr Opin Cell Biol. 1996 Feb;8(1):106-19 PMID: 8791410
  39. The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila.
    Cell. 1991 Jun 28;65(7):1177-89 PMID: 1905980
  40. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis.
    J Cell Biol. 1995 Dec;131(5):1243-59 PMID: 8522587
  41. Traction forces of cytokinesis measured with optically modified elastic substrata.
    Nature. 1997 Jan 30;385(6615):450-4 PMID: 9009194
  42. The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis.
    J Cell Biol. 1995 May;129(3):709-23 PMID: 7730406
  43. Kinesin proteins: a phylum of motors for microtubule-based motility.
    Bioessays. 1996 Mar;18(3):207-19 PMID: 8867735
  44. A model for astral stimulation of cytokinesis in animal cells.
    J Cell Biol. 1989 Nov;109(5):2225-32 PMID: 2808526
  45. Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly.
    J Cell Biol. 1992 Jul;118(1):109-20 PMID: 1618897
  46. On the mechanisms of cytokinesis in animal cells.
    J Theor Biol. 1983 Mar 21;101(2):289-316 PMID: 6683772
  47. Predicting coiled coils from protein sequences.
    Science. 1991 May 24;252(5009):1162-4 PMID: 2031185
  48. A monoclonal antibody to a mitotic microtubule-associated protein blocks mitotic progression.
    J Cell Biol. 1990 Aug;111(2):511-22 PMID: 2199459
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
DOI
10.1101/gad.12.10.1483
Email
d.m.glover@dundee.ac.uk
Published
1998-05-15
Pages
1483-94
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC316841
Subset
IM
External Links
PubMed source DOI: 10.1101/gad.12.10.1483 PMC Full Text View journal details
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