DOI: 10.1083/jcb.143.7.1789. <i>Saccharomyces cerevisiae</i> Ndc1p Is a Shared Component of Nuclear Pore Complexes and Spindle Pole Bodies

Saccharomyces cerevisiae Ndc1p Is a Shared Component of Nuclear Pore Complexes and Spindle Pole Bodies

10.1083/jcb.143.7.1789

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

We report a novel connection between nuclear pore complexes (NPCs) and spindle pole bodies (SPBs) revealed by our studies of the Saccharomyces cerevisiae NDC1 gene. Although both NPCs and SPBs are embedded in the nuclear envelope (NE) in yeast, their known functions are quite distinct. Previous work demonstrated that NDC1 function is required for proper SPB duplication (Winey, M., M.A. Hoyt, C. Chan, L. Goetsch, D. Botstein, and B. Byers. 1993. J. Cell Biol. 122:743–751). Here, we show that Ndc1p is a membrane protein of the NE that localizes to both NPCs and SPBs. Indirect immunofluorescence microscopy shows that Ndc1p displays punctate, nuclear peripheral localization that colocalizes with a known NPC component, Nup49p. Additionally, distinct spots of Ndc1p localization colocalize with a known SPB component, Spc42p. Immunoelectron microscopy shows that Ndc1p localizes to the regions of NPCs and SPBs that interact with the NE. The NPCs in ndc1-1 mutant cells appear to function normally at the nonpermissive temperature. Finally, we have found that a deletion of POM152, which encodes an abundant but nonessential nucleoporin, suppresses the SPB duplication defect associated with a mutation in the NDC1 gene. We show that Ndc1p is a shared component of NPCs and SPBs and propose a shared function in the assembly of these organelles into the NE.

Bibliography

Chial, H. J., Rout, M. P., Giddings, T. H., & Winey, M. (1998). Saccharomyces cerevisiae Ndc1p Is a Shared Component of Nuclear Pore Complexes and Spindle Pole Bodies. The Journal of Cell Biology, 143(7), 1789â1800.

Authors 4

Heidi J. Chial (first)
Michael P. Rout (additional)
Thomas H. Giddings (additional)
Mark Winey (additional)

References 55 Referenced 116

10.1083/jcb.131.6.1659 / J Cell Biol / Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport by Aitchison (1995)
10.1083/jcb.131.5.1133 / J Cell Biol / Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p by Aitchison (1995)
{'key': '2023072900330229300_B3'}
10.1093/nar/21.14.3329 / Nucleic Acids Res / A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. by Baudin (1993)
10.1083/jcb.136.6.1185 / J Cell Biol / In vivo dynamics of nuclear pore complexes in yeast by Bucci (1997)
10.1091/mbc.9.9.2439 / Mol Biol Cell / A novel fluorescence-based genetic strategy identifies mutants of Saccharomyces cerevisiaedefective for nuclear pore complex assembly by Bucci (1998)
10.1016/S0092-8674(00)80295-0 / Cell / The yeast spindle pole body is assembled around a central crystal of Spc42p by Bullitt (1997)
10.1099/00221287-143-2-303 / Microbiology / Yeast-enhanced green fluorescent protein (yEGFP) a reporter of gene expression in Candida albicans. by Cormack (1997)
10.1016/0092-8674(86)90784-1 / Cell / Identification and characterization of a nuclear pore complex protein by Davis (1986)
10.1073/pnas.84.21.7552 / Proc Natl Acad Sci USA / Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway by Davis (1987)
10.1016/0092-8674(90)90062-J / Cell / The NUP1gene encodes an essential component of the yeast nuclear pore complex by Davis (1990)
10.1091/mbc.8.8.1461 / Mol Biol Cell / The spindle pole body of Schizosaccharomyces pombeenters and leaves the nuclear envelope as the cell cycle proceeds by Ding (1997)
10.1083/jcb.132.5.887 / J Cell Biol / Spc42p: a phosphorylated component of the S. cerevisiaespindle pole body (SPB) with an essential function during SPB duplication by Donaldson (1996)
10.1016/S0955-0674(97)80014-2 / Curr Opin Cell Biol / From nucleoporins to nuclear pore complexes by Doye (1997)
10.1002/j.1460-2075.1994.tb06953.x / EMBO (Eur Mol Biol Organ) J / A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution by Doye (1994)
10.1016/0378-1119(88)90202-8 / Gene / A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae. by Elledge (1988)
10.1006/abio.1994.1148 / Anal Biochem / An improved procedure for enzymatic digestion of polyvinyldiene difluoride-bound proteins for internal sequence analysis by Fernandez (1994)
10.1002/j.1460-2075.1993.tb05975.x / EMBO (Eur Mol Biol Organ) J / Purification of NSP1 reveals complex formation with “GLFG” nucleoporins and a novel nuclear pore protein NIC96 by Grandi (1993)
10.1002/j.1460-2075.1995.tb06977.x / EMBO (Eur Mol Biol Organ) J / Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p and a novel protein Nup57p by Grandi (1995)
10.1091/mbc.8.10.2017 / Mol Biol Cell / Nup93, a vertebrate homologue of yeast Nic96p, forms a complex with a novel 205-kD protein and is required for correct nuclear pore assembly by Grandi (1997)
10.1083/jcb.131.6.1677 / J Cell Biol / Nuclear pore complex clustering and nuclear accumulation of poly(A)+ RNA associated with mutation of the Saccharomyces cerevisiae RAT2/NUP120gene by Heath (1995)
10.1091/mbc.9.2.355 / Mol Biol Cell / The integral membrane protein Snl1p is genetically linked to yeast nuclear pore complex function by Ho (1998)
10.1083/jcb.106.6.1997 / J Cell Biol / Diverse effects of beta-tubulin mutations on microtubule formation and function by Huffaker (1988)
10.1099/00221287-113-2-369 / J Gen Microbiol / Microbial determinations by flow cytometry by Hutter (1979)
{'key': '2023072900330229300_B25', 'first-page': '1440', 'article-title': 'Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae.', 'volume': '4', 'author': 'Johnston', 'year': '1984', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. by Johnston (1984)
10.1083/jcb.123.5.1175 / J Cell Biol / A spacer protein in the Saccharomyces cerevisiaespindle pole body whose transcript is cell cycle-regulated by Kilmartin (1993)
10.1083/jcb.133.6.1153 / J Cell Biol / The yeast nucleoporin Nup188p interacts genetically and physically with the core structures of the nuclear pore complex by Nehrbass (1996)
10.1073/pnas.92.4.1187 / Proc Natl Acad Sci USA / Disruption of the nucleoporin gene NUP133results in clustering of nuclear pore complexes by Pemberton (1995)
10.1016/0076-6879(91)94022-5 / Methods Enzymol / Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast by Rothstein (1991)
10.1083/jcb.111.5.1913 / J Cell Biol / Components of the yeast spindle and spindle pole body by Rout (1990)
10.1101/SQB.1991.056.01.077 / Cold Spring Harb Symp Quant Biol / Yeast spindle pole body components by Rout (1991)
10.1083/jcb.123.4.771 / J Cell Biol / Isolation of the yeast nuclear pore complex by Rout (1993)
10.1016/0962-8924(94)90085-X / Trends Cell Biol / Pores for thought: nuclear pore complex proteins by Rout (1994)
{'key': '2023072900330229300_B34'}
10.1091/mbc.8.1.33 / Mol Biol Cell / In vitroreconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p, and Nup57p by Schlaich (1997)
10.1073/pnas.92.1.225 / Proc Natl Acad Sci USA / The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A)+ RNA in the cytoplasm by Schlenstedt (1995)
10.1091/mbc.9.4.759 / Mol Biol Cell / New alleles of the yeast MPS1gene reveal multiple requirements in spindle pole body duplication by Schutz (1998)
{'key': '2023072900330229300_B38'}
10.1093/genetics/122.1.19 / Genetics / A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. by Sikorski (1989)
10.1007/BF00362281 / Chromosoma / The spindle pole body of yeast by Snyder (1994)
10.1083/jcb.131.1.19 / J Cell Biol / Isolation and characterization of nuclear envelopes from the yeast Saccharomyces. by Strambio-de-Castillia (1995)
10.1016/0092-8674(86)90485-X / Cell / A gene required for the separation of chromosomes on the spindle apparatus in yeast by Thomas (1986)
10.1002/j.1460-2075.1990.tb08084.x / EMBO (Eur Mol Biol Organ) J / Characterization of nuclear localizing sequences derived from yeast ribosomal protein L29 by Underwood (1990)
10.1002/yea.320101310 / Yeast / New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. by Wach (1994)
10.1083/jcb.119.4.705 / J Cell Biol / A new family of yeast nuclear pore complex proteins by Wente (1992)
{'key': '2023072900330229300_B46'}
10.1091/mbc.9.10.2839 / Mol Biol Cell / cut11+: a gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. by West (1998)
10.1016/0168-9525(93)90247-F / Trends Genet / Assembly and functions of the spindle pole body in budding yeast by Winey (1993)
10.1083/jcb.122.4.743 / J Cell Biol / NDC1: a nuclear periphery component required for yeast spindle pole body duplication by Winey (1993)
10.1083/jcb.129.6.1601 / J Cell Biol / Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiaemitotic spindle by Winey (1995)
10.1091/mbc.8.11.2119 / Mol Biol Cell / Nuclear pore complex number and distribution throughout the Saccharomyces cerevisiaecell cycle by three-dimensional reconstruction from electron micrographs of nuclear envelopes by Winey (1997)
10.1002/(SICI)1097-0061(199704)13:5<399::AID-YEA126>3.0.CO;2-9 / Yeast / Review: an overview of the Saccharomyces cerevisiaemicrotubule and microfilament cytoskeleton by Winsor (1997)
10.1083/jcb.125.1.31 / J Cell Biol / POM152is an integral protein of the pore membrane domain of the yeast nuclear envelope by Wozniak (1994)
10.1016/S1097-2765(00)80023-4 / Mol Cell / Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications by Yang (1998)
10.1083/jcb.133.6.1141 / J Cell Biol / Nic96p is required for nuclear pore formation and functionally interacts with a novel nucleoporin, Nup188p by Zabel (1996)

Dates

Type	When
Created	23 years ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 8:33 p.m.)
Indexed	10 months, 4 weeks ago (Sept. 22, 2024, 11:39 p.m.)
Issued	26 years, 7 months ago (Dec. 28, 1998)
Published	26 years, 7 months ago (Dec. 28, 1998)
Published Online	26 years, 7 months ago (Dec. 28, 1998)
Published Print	26 years, 7 months ago (Dec. 28, 1998)

Funders 0

None

BibTeX

@article{Chial_1998, title={Saccharomyces cerevisiae Ndc1p Is a Shared Component of Nuclear Pore Complexes and Spindle Pole Bodies}, volume={143}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.143.7.1789}, DOI={10.1083/jcb.143.7.1789}, number={7}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Chial, Heidi J. and Rout, Michael P. and Giddings, Thomas H. and Winey, Mark}, year={1998}, month=dec, pages={1789–1800} }

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      "author": "Aitchison",
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      "article-title": "A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.",
      "volume": "21",
      "author": "Baudin",
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      "journal-title": "Nucleic Acids Res"
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      "author": "Bucci",
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      "journal-title": "J Cell Biol"
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      "first-page": "2439",
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      "article-title": "A novel fluorescence-based genetic strategy identifies mutants of Saccharomyces cerevisiaedefective for nuclear pore complex assembly",
      "volume": "9",
      "author": "Bucci",
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      "journal-title": "Mol Biol Cell"
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      "article-title": "Diverse effects of beta-tubulin mutations on microtubule formation and function",
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