Abstract
Saccharomyces cerevisiae cells are exquisitely sensitive to altered dosage of the spindle pole body duplication gene, NDC1. We show that the NDC1 locus is haploinsufficient because diploid yeast cells cannot survive with a single chromosomal copy of the NDC1 gene. Diploid cells with a single copy of NDC1 can survive by gaining an extra copy of the NDC1-containing chromosome. NDC1 haploinsufficiency is a dominant loss-of-function phenotype that leads to aneuploidy. Furthermore, we report that overexpression of NDC1 leads to spindle pole body duplication defects indistinguishable from those observed in ndc1-1 mutant cells. Cells overexpressing NDC1 arrest with monopolar spindles and exhibit increase-in-ploidy phenotypes. Thus, both increased and decreased NDC1 dosage can lead to aneuploidy. The striking sensitivity of yeast cells to changes in NDC1 gene dosage suggests a model for the behavior of some tumor suppressor genes and oncogenes in which loss-of-function mutations and overexpression, respectively, lead to increased genetic instability.
MeSH Terms
Aneuploidy
Fungal Proteins/genetics,metabolism
Gene Dosage
Genotype
Nuclear Pore Complex Proteins
Nuclear Proteins/genetics,metabolism
Phenotype
Polyploidy
Saccharomyces cerevisiae/genetics,growth & development,ultrastructure
Saccharomyces cerevisiae Proteins
Spindle Apparatus/genetics
Chemicals
Fungal Proteins
NDC1 protein, S cerevisiae
Nuclear Pore Complex Proteins
Nuclear Proteins
Saccharomyces cerevisiae Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Chial H J
Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, CO 80309-0347, USA.
Giddings T H
Siewert E A
Hoyt M A
Winey M
References (30)
30 references, click to expand
-
Mutation and cancer: statistical study of retinoblastoma.
Proc Natl Acad Sci U S A. 1971 Apr;68(4):820-3
PMID: 5279523
-
Mechanisms of genetic instability revealed by analysis of yeast spindle pole body duplication.
Biol Cell. 1999 Jul;91(6):439-50
PMID: 10519004
-
Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae.
Mol Cell Biol. 1984 Aug;4(8):1440-8
PMID: 6092912
-
A gene required for the separation of chromosomes on the spindle apparatus in yeast.
Cell. 1986 Jan 17;44(1):65-76
PMID: 3510081
-
Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins.
Mol Cell Biol. 1986 Nov;6(11):3722-33
PMID: 3540600
-
KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast.
Cell. 1987 Mar 27;48(6):1047-60
PMID: 3030557
-
Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates.
J Gen Virol. 1987 Nov;68 ( Pt 11):2769-80
PMID: 2445904
-
5-Fluoroorotic acid as a selective agent in yeast molecular genetics.
Methods Enzymol. 1987;154:164-75
PMID: 3323810
-
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
Genetics. 1989 May;122(1):19-27
PMID: 2659436
-
Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae.
Mol Cell Biol. 1991 Mar;11(3):1295-305
PMID: 1996092
-
Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast.
Methods Enzymol. 1991;194:281-301
PMID: 2005793
-
Tumor suppressor genes.
Science. 1991 Nov 22;254(5035):1138-46
PMID: 1659741
-
Multifunctional yeast high-copy-number shuttle vectors.
Gene. 1992 Jan 2;110(1):119-22
PMID: 1544568
-
A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
Nucleic Acids Res. 1993 Jul 11;21(14):3329-30
PMID: 8341614
-
NDC1: a nuclear periphery component required for yeast spindle pole body duplication.
J Cell Biol. 1993 Aug;122(4):743-51
PMID: 8349727
-
New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
Yeast. 1994 Dec;10(13):1793-808
PMID: 7747518
-
Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption.
Science. 1996 Aug 16;273(5277):953-6
PMID: 8688079
-
Oncoprotein networks.
Cell. 1997 Feb 7;88(3):333-46
PMID: 9039260
-
Genetic instability in colorectal cancers.
Nature. 1997 Apr 10;386(6625):623-7
PMID: 9121588
-
Aneuploidy correlated 100% with chemical transformation of Chinese hamster cells.
Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14506-11
PMID: 9405643
-
Centrosome hypertrophy in human breast tumors: implications for genomic stability and cell polarity.
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2950-5
PMID: 9501196
-
Mutations of mitotic checkpoint genes in human cancers.
Nature. 1998 Mar 19;392(6673):300-3
PMID: 9521327
-
New alleles of the yeast MPS1 gene reveal multiple requirements in spindle pole body duplication.
Mol Biol Cell. 1998 Apr;9(4):759-74
PMID: 9529376
-
A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers.
EMBO J. 1998 Jun 1;17(11):3052-65
PMID: 9606188
-
Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae.
J Cell Biol. 1998 Aug 10;142(3):711-22
PMID: 9700160
-
Retention of wild-type p53 in tumors from p53 heterozygous mice: reduction of p53 dosage can promote cancer formation.
EMBO J. 1998 Aug 17;17(16):4657-67
PMID: 9707425
-
Trisomy 7-harbouring non-random duplication of the mutant MET allele in hereditary papillary renal carcinomas.
Nat Genet. 1998 Sep;20(1):66-9
PMID: 9731534
-
Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation.
Nat Genet. 1998 Oct;20(2):189-93
PMID: 9771714
-
Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies.
J Cell Biol. 1998 Dec 28;143(7):1789-800
PMID: 9864355
-
Microbial determinations by flow cytometry.
J Gen Microbiol. 1979 Aug;113(2):369-75
PMID: 390094