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PMID: 10444068 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila.

The Journal of cell biology ·Vol. 146 ·No. 3 ·1999-08-09 ·Pages 597-608

Robinson JT, Wojcik EJ, Sanders MA, McGrail M, Hays TS

Abstract

Cytoplasmic dynein is a multisubunit minus-end-directed microtubule motor that serves multiple cellular functions. Genetic studies in Drosophila and mouse have demonstrated that dynein function is essential in metazoan organisms. However, whether the essential function of dynein reflects a mitotic requirement, and what specific mitotic tasks require dynein remains controversial. Drosophila is an excellent genetic system in which to analyze dynein function in mitosis, providing excellent cytology in embryonic and somatic cells. We have used previously characterized recessive lethal mutations in the dynein heavy chain gene, Dhc64C, to reveal the contributions of the dynein motor to mitotic centrosome behavior in the syncytial embryo. Embryos lacking wild-type cytoplasmic dynein heavy chain were analyzed by in vivo analysis of rhodamine-labeled microtubules, as well as by immunofluorescence in situ methods. Comparisons between wild-type and Dhc64C mutant embryos reveal that dynein function is required for the attachment and migration of centrosomes along the nuclear envelope during interphase/prophase, and to maintain the attachment of centrosomes to mitotic spindle poles. The disruption of these centrosome attachments in mutant embryos reveals a critical role for dynein function and centrosome positioning in the spatial organization of the syncytial cytoplasm of the developing embryo.

MeSH Terms
Animals Brain/cytology,embryology,metabolism Cell Nucleus/genetics,metabolism Centrosome/metabolism Cytoplasm/metabolism Drosophila melanogaster/cytology,embryology,genetics Dyneins/genetics,metabolism Embryo, Nonmammalian/cytology,metabolism Female Giant Cells/cytology,metabolism Insect Proteins/genetics,metabolism Interphase Male Microtubules/metabolism Mitosis Movement Mutation Nuclear Envelope/metabolism Spindle Apparatus/metabolism
Chemicals
Insect Proteins Dyneins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Robinson J T
University of Minnesota, Department of Genetics, Cell Biology and Development, St. Paul, Minnesota 55108-1095, USA.
Wojcik E J
Sanders M A
McGrail M
Hays T S
References (54)
54 references, click to expand
  1. Drosophila cytoplasmic dynein, a microtubule motor that is asymmetrically localized in the oocyte.
    J Cell Biol. 1994 Sep;126(6):1475-94 PMID: 8089180
  2. Xklp2, a novel Xenopus centrosomal kinesin-like protein required for centrosome separation during mitosis.
    Cell. 1996 Jan 12;84(1):49-59 PMID: 8548825
  3. A cytoplasmic dynein motor in Drosophila: identification and localization during embryogenesis.
    J Cell Sci. 1994 Jun;107 ( Pt 6):1557-69 PMID: 7962198
  4. Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis.
    J Cell Biol. 1995 Jan;128(1-2):95-104 PMID: 7822426
  5. Saccharomyces cerevisiae kinesin- and dynein-related proteins required for anaphase chromosome segregation.
    J Cell Biol. 1995 Feb;128(4):617-24 PMID: 7860634
  6. Organelle movement. Dynactin: portrait of a dynein regulator.
    Curr Biol. 1994 Nov 1;4(11):1000-2 PMID: 7874478
  7. DYNEINS: molecular structure and cellular function.
    Annu Rev Cell Biol. 1994;10:339-72 PMID: 7888180
  8. Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex.
    J Cell Biol. 1995 Oct;131(2):411-25 PMID: 7593168
  9. Drosophila melanogaster syncytial nuclear divisions are patterned: time-lapse images, hypothesis and computational evidence.
    J Theor Biol. 1995 Aug 21;175(4):525-32 PMID: 7475088
  10. Dynein family of motor proteins: present status and future questions.
    Cell Motil Cytoskeleton. 1995;32(2):136-44 PMID: 8681396
  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. Direct cell lineage analysis in Drosophila melanogaster by time-lapse, three-dimensional optical microscopy of living embryos.
    J Cell Biol. 1989 Aug;109(2):505-16 PMID: 2503522
  13. Cytoplasmic dynein is localized to kinetochores during mitosis.
    Nature. 1990 May 17;345(6272):263-5 PMID: 2139717
  14. Localization of cytoplasmic dynein to mitotic spindles and kinetochores.
    Nature. 1990 May 17;345(6272):266-8 PMID: 2139718
  15. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein.
    J Cell Biol. 1991 Mar;112(6):1177-87 PMID: 1671864
  16. Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence.
    J Cell Sci Suppl. 1991;14:125-7 PMID: 1832165
  17. daughterless-abo-like, a Drosophila maternal-effect mutation that exhibits abnormal centrosome separation during the late blastoderm divisions.
    Development. 1990 Oct;110(2):311-23 PMID: 2133540
  18. Cytochalasin induces spindle fusion in the syncytial blastoderm of the early Drosophila embryo.
    Biol Cell. 1992;74(3):249-54 PMID: 1628108
  19. Maternal effect mutations of the sponge locus affect actin cytoskeletal rearrangements in Drosophila melanogaster embryos.
    J Cell Biol. 1992 Dec;119(5):1205-18 PMID: 1447298
  20. Mitotic spindle morphogenesis in animal cells.
    Semin Cell Biol. 1991 Aug;2(4):251-60 PMID: 1842343
  21. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation.
    J Cell Biol. 1993 Nov;123(4):849-58 PMID: 8227145
  22. 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
  23. 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
  24. Morphogenetic properties of microtubules and mitotic spindle assembly.
    Cell. 1996 Feb 9;84(3):401-10 PMID: 8608594
  25. Genetic interactions among cytoplasmic dynein, dynactin, and nuclear distribution mutants of Neurospora crassa.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4775-80 PMID: 8643479
  26. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts.
    Nature. 1996 Aug 1;382(6590):420-5 PMID: 8684481
  27. Targeting of cytoplasmic dynein to membranous organelles and kinetochores via dynactin.
    Cold Spring Harb Symp Quant Biol. 1995;60:803-11 PMID: 8824455
  28. Analysis of nuclear migration in Aspergillus nidulans.
    Cold Spring Harb Symp Quant Biol. 1995;60:813-9 PMID: 8824456
  29. Cytoplasmic dynein function is essential in Drosophila melanogaster.
    Genetics. 1996 Mar;142(3):865-78 PMID: 8849893
  30. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly.
    Cell. 1996 Nov 1;87(3):447-58 PMID: 8898198
  31. Microtubule release from the centrosome.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5078-83 PMID: 9144193
  32. The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila.
    Development. 1997 Jun;124(12):2409-19 PMID: 9199367
  33. The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila.
    Curr Biol. 1997 Jul 1;7(7):468-78 PMID: 9210377
  34. Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization.
    J Cell Biol. 1997 Aug 11;138(3):615-28 PMID: 9245790
  35. The bimC family of kinesins: essential bipolar mitotic motors driving centrosome separation.
    Biochim Biophys Acta. 1997 Jul 24;1357(3):257-71 PMID: 9268050
  36. Pathways of spindle pole formation: different mechanisms; conserved components.
    J Cell Biol. 1997 Sep 8;138(5):953-6 PMID: 9281574
  37. Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes.
    J Cell Biol. 1997 Sep 8;138(5):1055-66 PMID: 9281583
  38. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport.
    Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):12180-5 PMID: 9342383
  39. A method that allows the assembly of kinetochore components onto chromosomes condensed in clarified Xenopus egg extracts.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12378-83 PMID: 9356457
  40. Localization of motor-related proteins and associated complexes to active, but not inactive, centromeres.
    Hum Mol Genet. 1998 Apr;7(4):671-7 PMID: 9499420
  41. The role of the dynactin complex in intracellular motility.
    Int Rev Cytol. 1998;182:69-109 PMID: 9522459
  42. 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
  43. Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration.
    J Cell Sci. 1998 Jun;111 ( Pt 11):1555-66 PMID: 9580563
  44. Evidence for a role of CLIP-170 in the establishment of metaphase chromosome alignment.
    J Cell Biol. 1998 May 18;141(4):849-62 PMID: 9585405
  45. Mechanisms of nuclear positioning.
    J Cell Sci. 1998 Aug;111 ( Pt 16):2283-95 PMID: 9683624
  46. ZW10 helps recruit dynactin and dynein to the kinetochore.
    J Cell Biol. 1998 Aug 10;142(3):763-74 PMID: 9700164
  47. A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity.
    Curr Biol. 1998 Jul 30-Aug 13;8(16):903-13 PMID: 9707401
  48. Characterization of the p22 subunit of dynactin reveals the localization of cytoplasmic dynein and dynactin to the midbody of dividing cells.
    J Cell Biol. 1998 Aug 24;142(4):1023-34 PMID: 9722614
  49. Localization of the kinesin-like protein Xklp2 to spindle poles requires a leucine zipper, a microtubule-associated protein, and dynein.
    J Cell Biol. 1998 Nov 2;143(3):673-85 PMID: 9813089
  50. 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
  51. Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila.
    Mol Biol Cell. 1999 Mar;10(3):771-84 PMID: 10069817
  52. 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
  53. 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
  54. Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi.
    J Cell Biol. 1994 Oct;127(1):139-149 PMID: 7929559
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.146.3.597
Published
1999-08-09
Pages
597-608
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2150560
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.146.3.597 PMC Full Text View journal details
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