Home LiteratureArticle Details
PMID: 16380440 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Nuclear congression is driven by cytoplasmic microtubule plus end interactions in S. cerevisiae.

The Journal of cell biology ·Vol. 172 ·No. 1 ·2006-01-02 ·Pages 27-39

Molk JN, Salmon ED, Bloom K

Abstract

Nuclear movement before karyogamy in eukaryotes is known as pronuclear migration or as nuclear congression in Saccharomyces cerevisiae. In this study, S. cerevisiae is used as a model system to study microtubule (MT)-dependent nuclear movements during mating. We find that nuclear congression occurs through the interaction of MT plus ends rather than sliding and extensive MT overlap. Furthermore, the orientation and attachment of MTs to the shmoo tip before cell wall breakdown is not required for nuclear congression. The MT plus end-binding proteins Kar3p, a class 14 COOH-terminal kinesin, and Bik1p, the CLIP-170 orthologue, localize to plus ends in the shmoo tip and initiate MT interactions and depolymerization after cell wall breakdown. These data support a model in which nuclear congression in budding yeast occurs by plus end MT capture and depolymerization, generating forces sufficient to move nuclei through the cytoplasm. This is the first evidence that MT plus end interactions from oppositely oriented organizing centers can provide the force for organelle transport in vivo.

MeSH Terms
Cell Cycle Proteins/metabolism Cell Nucleus/metabolism Cells, Cultured Cytokinesis Cytoplasm/metabolism Genes, Mating Type, Fungal/physiology Microtubule-Associated Proteins/metabolism Microtubules/physiology Models, Biological Molecular Motor Proteins Saccharomyces cerevisiae/physiology Saccharomyces cerevisiae Proteins/metabolism
Chemicals
Bik1 protein, S cerevisiae Cell Cycle Proteins KAR3 protein, S cerevisiae KIP2 protein, S cerevisiae Microtubule-Associated Proteins Molecular Motor Proteins Saccharomyces cerevisiae Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Molk Jeffrey N
Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA.
Salmon E D
Bloom Kerry
References (35)
35 references, click to expand
  1. The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast.
    Mol Biol Cell. 1998 Aug;9(8):2051-68 PMID: 9693366
  2. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  3. The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization.
    J Cell Biol. 1999 Mar 8;144(5):963-75 PMID: 10085294
  4. Microtubule dynamics from mating through the first zygotic division in the budding yeast Saccharomyces cerevisiae.
    J Cell Biol. 1999 Mar 8;144(5):977-87 PMID: 10085295
  5. Yeast Bim1p promotes the G1-specific dynamics of microtubules.
    J Cell Biol. 1999 May 31;145(5):993-1007 PMID: 10352017
  6. High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae.
    Mol Biol Cell. 1999 Jun;10(6):2017-31 PMID: 10359612
  7. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo.
    J Cell Biol. 1999 Oct 4;147(1):135-50 PMID: 10508861
  8. The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae.
    Nat Cell Biol. 2000 Jan;2(1):36-41 PMID: 10620805
  9. The Kar3p kinesin-related protein forms a novel heterodimeric structure with its associated protein Cik1p.
    Mol Biol Cell. 2000 Jul;11(7):2373-85 PMID: 10888675
  10. Polyploids require Bik1 for kinetochore-microtubule attachment.
    J Cell Biol. 2001 Dec 24;155(7):1173-84 PMID: 11756471
  11. Yeast Cdk1 translocates to the plus end of cytoplasmic microtubules to regulate bud cortex interactions.
    EMBO J. 2003 Feb 3;22(3):438-49 PMID: 12554645
  12. The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast.
    J Cell Biol. 2003 Feb 3;160(3):355-64 PMID: 12566428
  13. Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning.
    Curr Biol. 2003 Mar 4;13(5):364-72 PMID: 12620184
  14. Spinning disk confocal microscope system for rapid high-resolution, multimode, fluorescence speckle microscopy and green fluorescent protein imaging in living cells.
    Methods Enzymol. 2003;360:597-617 PMID: 12622170
  15. Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables.
    J Cell Biol. 2003 May 12;161(3):483-8 PMID: 12743102
  16. The minus end-directed motor Kar3 is required for coupling dynamic microtubule plus ends to the cortical shmoo tip in budding yeast.
    Curr Biol. 2003 Aug 19;13(16):1423-8 PMID: 12932327
  17. Preferentially localized dynein and perinuclear dynactin associate with nuclear pore complex proteins to mediate genomic union during mammalian fertilization.
    J Cell Sci. 2003 Dec 1;116(Pt 23):4727-38 PMID: 14600259
  18. The differential roles of budding yeast Tem1p, Cdc15p, and Bub2p protein dynamics in mitotic exit.
    Mol Biol Cell. 2004 Apr;15(4):1519-32 PMID: 14718561
  19. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation.
    Dev Cell. 2004 Jun;6(6):815-29 PMID: 15177030
  20. Genes involved in the control of nuclear fusion during the sexual cycle of Saccharomyces cerevisiae.
    Mol Gen Genet. 1982;186(2):253-8 PMID: 7050632
  21. Theoretical problems related to the attachment of microtubules to kinetochores.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4404-8 PMID: 3859869
  22. Tubulin and actin topology during zygote formation of Saccharomyces cerevisiae.
    J Gen Microbiol. 1987 Dec;133(12):3355-63 PMID: 3332685
  23. KAR3, a kinesin-related gene required for yeast nuclear fusion.
    Cell. 1990 Mar 23;60(6):1029-41 PMID: 2138512
  24. Propagation and expression of cloned genes in yeast: 2-microns circle-based vectors.
    Methods Enzymol. 1990;185:234-79 PMID: 2199781
  25. BIK1, a protein required for microtubule function during mating and mitosis in Saccharomyces cerevisiae, colocalizes with tubulin.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2573-86 PMID: 2277073
  26. 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
  27. Nuclear congression and membrane fusion: two distinct events in the yeast karyogamy pathway.
    J Cell Biol. 1994 Aug;126(4):911-23 PMID: 8051211
  28. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  29. Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae.
    J Cell Biol. 1995 Sep;130(6):1373-85 PMID: 7559759
  30. ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Oct;16(10):5264-75 PMID: 8816439
  31. Nuclear fusion in the yeast Saccharomyces cerevisiae.
    Annu Rev Cell Dev Biol. 1996;12:663-95 PMID: 8970740
  32. Mitosis in living budding yeast: anaphase A but no metaphase plate.
    Science. 1997 Jul 25;277(5325):574-8 PMID: 9228009
  33. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast.
    J Cell Biol. 1998 Jan 26;140(2):377-90 PMID: 9442113
  34. Molecular mechanisms of kinetochore capture by spindle microtubules.
    Nature. 2005 Apr 21;434(7036):987-94 PMID: 15846338
  35. Cik1 targets the minus-end kinesin depolymerase kar3 to microtubule plus ends.
    Curr Biol. 2005 Aug 9;15(15):1420-7 PMID: 16085496
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.200510032
Published
2006-01-02
Epub
2005-00-27
Pages
27-39
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2063526
Subset
IM
Grants
NIGMS NIH HHS · GM-24364 · United States
NIGMS NIH HHS · R01 GM060678 · United States
NIGMS NIH HHS · R01 GM032238 · United States
NIGMS NIH HHS · GM-32238 · United States
NIGMS NIH HHS · R37 GM032238 · United States
NIGMS NIH HHS · R37 GM024364 · United States
NIGMS NIH HHS · R01 GM024364 · United States
NIGMS NIH HHS · GM-60678 · United States
External Links
PubMed source DOI: 10.1083/jcb.200510032 PMC Full Text View journal details
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: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2