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PMID: 10637305 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Functional coordination of three mitotic motors in Drosophila embryos.

Molecular biology of the cell ·Vol. 11 ·No. 1 ·2000-01-00 ·Pages 241-53

Sharp DJ, Brown HM, Kwon M, Rogers GC, Holland G, Scholey JM

Abstract

It is well established that multiple microtubule-based motors contribute to the formation and function of the mitotic spindle, but how the activities of these motors interrelate remains unclear. Here we visualize spindle formation in living Drosophila embryos to show that spindle pole movements are directed by a temporally coordinated balance of forces generated by three mitotic motors, cytoplasmic dynein, KLP61F, and Ncd. Specifically, our findings suggest that dynein acts to move the poles apart throughout mitosis and that this activity is augmented by KLP61F after the fenestration of the nuclear envelope, a process analogous to nuclear envelope breakdown, which occurs at the onset of prometaphase. Conversely, we find that Ncd generates forces that pull the poles together between interphase and metaphase, antagonizing the activity of both dynein and KLP61F and serving as a brake for spindle assembly. During anaphase, however, Ncd appears to have no effect on spindle pole movements, suggesting that its activity is down-regulated at this time, allowing dynein and KLP61F to drive spindle elongation during anaphase B.

MeSH Terms
Anaphase/physiology Animals Blastoderm/ultrastructure Drosophila melanogaster/embryology Female Humans Interphase/physiology Male Metaphase/physiology Microtubules/ultrastructure Mitosis/physiology Molecular Motor Proteins Prophase/physiology Spindle Apparatus/physiology,ultrastructure
Chemicals
Molecular Motor Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Sharp D J
Section of Molecular and Cellular Biology, University of California-Davis, Davis, California 95616, USA.
Brown H M
Kwon M
Rogers G C
Holland G
Scholey J M
References (58)
58 references, click to expand
  1. The kinesin-like protein KLP61F is essential for mitosis in Drosophila.
    J Cell Biol. 1993 Nov;123(3):665-79 PMID: 8227131
  2. Loss of function of Saccharomyces cerevisiae kinesin-related CIN8 and KIP1 is suppressed by KAR3 motor domain mutations.
    Genetics. 1993 Sep;135(1):35-44 PMID: 8224825
  3. Disruption of mitotic spindle orientation in a yeast dynein mutant.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10096-100 PMID: 8234262
  4. Cytoplasmic dynein is required for normal nuclear segregation in yeast.
    Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11172-6 PMID: 8248224
  5. Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2100-4 PMID: 8134356
  6. Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends.
    EMBO J. 1994 Jun 1;13(11):2708-13 PMID: 7912193
  7. A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos.
    J Biol Chem. 1994 Sep 16;269(37):22913-6 PMID: 8083185
  8. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte.
    J Cell Biol. 1994 Sep;126(6):1475-94 PMID: 8089180
  9. A cytoplasmic dynein motor in Drosophila: identification and localization during embryogenesis.
    J Cell Sci. 1994 Jun;107 ( Pt 6):1557-69 PMID: 7962198
  10. Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation.
    J Cell Biol. 1995 Feb;128(4):617-24 PMID: 7860634
  11. Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae.
    J Cell Biol. 1995 Aug;130(3):687-700 PMID: 7622568
  12. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo.
    Cell. 1995 Dec 29;83(7):1159-69 PMID: 8548803
  13. A bipolar kinesin.
    Nature. 1996 Jan 18;379(6562):270-2 PMID: 8538794
  14. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis.
    J Cell Biol. 1996 Feb;132(4):617-33 PMID: 8647893
  15. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts.
    Nature. 1996 Aug 1;382(6590):420-5 PMID: 8684481
  16. Fission yeast pkl1 is a kinesin-related protein involved in mitotic spindle function.
    Mol Biol Cell. 1996 Oct;7(10):1639-55 PMID: 8898367
  17. An essential bipolar mitotic motor.
    Nature. 1996 Nov 21;384(6606):225 PMID: 8918872
  18. Centrosome and spindle function of the Drosophila Ncd microtubule motor visualized in live embryos using Ncd-GFP fusion proteins.
    J Cell Sci. 1996 Oct;109 ( Pt 10):2429-42 PMID: 8923204
  19. Genetic analysis of the mitotic spindle.
    Annu Rev Genet. 1996;30:7-33 PMID: 8982447
  20. Mitotic spindle function in Saccharomyces cerevisiae requires a balance between different types of kinesin-related motors.
    Mol Biol Cell. 1997 Jun;8(6):1025-33 PMID: 9201713
  21. The design plan of kinesin motors.
    Annu Rev Cell Dev Biol. 1997;13:745-77 PMID: 9442886
  22. Functions of motor proteins in echinoderm embryos: an argument in support of antibody inhibition experiments.
    Cell Motil Cytoskeleton. 1998;39(4):257-60 PMID: 9556327
  23. Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells.
    Curr Biol. 1998 Apr 23;8(9):541-4 PMID: 9560347
  24. Characterization of microtubule binding domains in the Arabidopsis kinesin-like calmodulin binding protein.
    Plant Cell. 1998 Jun;10(6):957-65 PMID: 9634584
  25. Time-lapse microscopy reveals unique roles for kinesins during anaphase in budding yeast.
    J Cell Biol. 1998 Nov 2;143(3):687-94 PMID: 9813090
  26. The bipolar kinesin, KLP61F, cross-links microtubules within interpolar microtubule bundles of Drosophila embryonic mitotic spindles.
    J Cell Biol. 1999 Jan 11;144(1):125-38 PMID: 9885249
  27. Using green fluorescent protein fusion proteins to quantitate microtubule and spindle dynamics in budding yeast.
    Methods Cell Biol. 1999;61:369-83 PMID: 9891324
  28. Two heteromeric kinesin complexes in chemosensory neurons and sensory cilia of Caenorhabditis elegans.
    Mol Biol Cell. 1999 Feb;10(2):345-60 PMID: 9950681
  29. Identification of microtubule binding sites in the Ncd tail domain.
    Biochemistry. 1999 Feb 9;38(6):1838-49 PMID: 10026264
  30. Cytoplasmic dynein and dynactin in cell division and intracellular transport.
    Curr Opin Cell Biol. 1999 Feb;11(1):45-53 PMID: 10047518
  31. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila.
    J Cell Biol. 1999 Aug 9;146(3):597-608 PMID: 10444068
  32. The kinesin-related protein Kip1p of Saccharomyces cerevisiae is bipolar.
    J Biol Chem. 1999 Oct 1;274(40):28779-86 PMID: 10497250
  33. Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos.
    Nat Cell Biol. 1999 May;1(1):51-4 PMID: 10559864
  34. On the mechanism of anaphase spindle elongation in Diatoma vulgare.
    J Cell Biol. 1977 Aug;74(2):377-88 PMID: 885908
  35. Polarity of spindle microtubules in Haemanthus endosperm.
    J Cell Biol. 1982 Sep;94(3):644-53 PMID: 7130276
  36. 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
  37. Distribution of F-actin during cleavage of the Drosophila syncytial blastoderm.
    J Cell Biol. 1984 Jan;98(1):156-62 PMID: 6423648
  38. Organization of the cytoskeleton in early Drosophila embryos.
    J Cell Biol. 1986 Apr;102(4):1494-509 PMID: 3514634
  39. KAR3, a kinesin-related gene required for yeast nuclear fusion.
    Cell. 1990 Mar 23;60(6):1029-41 PMID: 2138512
  40. Mediation of meiotic and early mitotic chromosome segregation in Drosophila by a protein related to kinesin.
    Nature. 1990 May 3;345(6270):81-3 PMID: 1691829
  41. Identification and characterization of a gene encoding a kinesin-like protein in Drosophila.
    Cell. 1990 Jun 15;61(6):991-1000 PMID: 2140958
  42. Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene.
    Nature. 1990 Oct 11;347(6293):563-6 PMID: 2145514
  43. The Drosophila claret segregation protein is a minus-end directed motor molecule.
    Nature. 1990 Oct 25;347(6295):780-2 PMID: 2146510
  44. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor.
    Cell. 1990 Dec 21;63(6):1159-65 PMID: 2261638
  45. Two activators of microtubule-based vesicle transport.
    J Cell Biol. 1991 Dec;115(5):1309-18 PMID: 1835460
  46. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein.
    J Cell Biol. 1991 Dec;115(6):1639-50 PMID: 1836789
  47. Photosensitized cleavage of dynein heavy chains. Cleavage at the "V1 site" by irradiation at 365 nm in the presence of ATP and vanadate.
    J Biol Chem. 1987 Feb 25;262(6):2780-6 PMID: 2950090
  48. Behaviour of microtubules and actin filaments in living Drosophila embryos.
    Development. 1988 Aug;103(4):675-86 PMID: 3248521
  49. The mitotic spindle.
    Sci Am. 1989 Oct;261(4):48-56 PMID: 2781260
  50. Directing cell division during development.
    Science. 1989 Nov 3;246(4930):635-40 PMID: 2683080
  51. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans.
    Cell. 1990 Mar 23;60(6):1019-27 PMID: 2138511
  52. Multiple kinesin-related proteins in yeast mitosis.
    Cold Spring Harb Symp Quant Biol. 1991;56:693-703 PMID: 1819517
  53. Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly.
    J Cell Biol. 1992 Jul;118(1):109-20 PMID: 1618897
  54. Kinesin-related proteins required for structural integrity of the mitotic spindle.
    Cell. 1992 Aug 7;70(3):451-8 PMID: 1643659
  55. Mitotic spindle organization by a plus-end-directed microtubule motor.
    Nature. 1992 Oct 8;359(6395):540-3 PMID: 1406972
  56. Suppression of the bimC4 mitotic spindle defect by deletion of klpA, a gene encoding a KAR3-related kinesin-like protein in Aspergillus nidulans.
    J Cell Biol. 1993 Jan;120(1):153-62 PMID: 8416986
  57. Structural and functional domains of the Drosophila ncd microtubule motor protein.
    J Biol Chem. 1993 Apr 25;268(12):9005-13 PMID: 8473343
  58. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation.
    J Cell Biol. 1993 Nov;123(4):849-58 PMID: 8227145
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.11.1.241
Published
2000-01-00
Pages
241-53
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC14771
Subset
IM
Grants
NIGMS NIH HHS · F32 GM019262 · United States
NIGMS NIH HHS · R01 GM055507 · United States
NIGMS NIH HHS · GM-19262 · United States
NIGMS NIH HHS · GM-55507 · United States
External Links
PubMed source DOI: 10.1091/mbc.11.1.241 PMC Full Text View journal details
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