Home LiteratureArticle Details
PMID: 9001245 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

C-terminal truncations of the yeast nucleoporin Nup145p produce a rapid temperature-conditional mRNA export defect and alterations to nuclear structure.

Molecular and cellular biology ·Vol. 17 ·No. 2 ·1997-02-00 ·Pages 906-20

Dockendorff TC, Heath CV, Goldstein AL, Snay CA, Cole CN

Abstract

A screen for temperature-sensitive mutants of Saccharomyces cerevisiae defective in nucleocytoplasmic trafficking of poly(A)+ RNA has identified an allele of the NUP145 gene, which encodes an essential nucleoporin. NUP145 was previously identified by using a genetic synthetic lethal screen (E. Fabre, W. C. Boelens, C. Wimmer, I. W. Mattaj, and E. C. Hurt, Cell 78:275-289, 1994) and by using a monoclonal antibody which recognizes the GLFG family of vertebrate and yeast nucleoporins (S. R. Wente and G. Blobel, J. Cell Biol. 125:955-969, 1994). Cells carrying the new allele, nup145-10, grew at 23 and 30 degrees C but were unable to grow at 37 degrees C. Many cells displayed a modest accumulation of poly(A)+ RNA under permissive growth conditions, and all cells showed dramatic and rapid nuclear accumulation of poly(A)+ RNA following a shift to 37 degrees C. The mutant allele contains a nonsense codon which truncates the 1,317-amino-acid protein to 698 amino acids. This prompted us to examine the role of the carboxyl half of Nup145p. Several additional alleles that encode C-terminally truncated proteins or proteins containing internal deletions of portions of the carboxyl half of Nup145p were constructed. Analysis of these mutants indicates that some sequences between amino acids 698 and 1095 are essential for RNA export and for growth at 37 degrees C. In these strains, nuclear accumulation of poly(A)+ RNA and fragmentation of the nucleolus occurred rapidly following a shift to 37 degrees C. Constitutive defects in nuclear pore complex distribution and nuclear structure were also seen in these strains. Although cells lacking Nup145p grew extremely slowly at 23 degrees C and did not grow at 30 degrees C, efficient growth at 23 or 30 degrees C occurred as long as cells produced either the amino 58% or the carboxyl 53% of Nup145p. Strains carrying alleles of NUP145 lacking up to 200 amino acids from the carboxy terminus were viable at 37 degrees C but displayed nucleolar fragmentation and some nuclear accumulation of poly(A)+ RNA following a shift to 37 degrees C. Surprisingly, these strains grew efficiently at 37 degrees C in spite of a reduction in the level of synthesis of rRNAs to approximately 25% of the wild-type level.

MeSH Terms
Biological Transport Cell Nucleus/metabolism,ultrastructure Fungal Proteins/genetics,metabolism Nuclear Pore Complex Proteins RNA, Messenger/metabolism RNA, Ribosomal/biosynthesis RNA-Binding Proteins/genetics,metabolism Saccharomyces cerevisiae/growth & development,metabolism Saccharomyces cerevisiae Proteins Sequence Deletion Temperature
Chemicals
Fungal Proteins NUP145 protein, S cerevisiae Nuclear Pore Complex Proteins RNA, Messenger RNA, Ribosomal RNA-Binding Proteins Saccharomyces cerevisiae Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dockendorff T C
Department of Biochemistry, Dartmouth Medical School, Hanover, New Hampshire 03755, USA.
Heath C V
Goldstein A L
Snay C A
Cole C N
References (49)
49 references, click to expand
  1. The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast.
    J Biol Chem. 1973 Feb 25;248(4):1412-6 PMID: 4568815
  2. Genetic approaches to nuclear pore structure and function.
    Trends Genet. 1995 Jun;11(6):235-41 PMID: 7638906
  3. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C.
    Yeast. 1995 Jan;11(1):53-5 PMID: 7762301
  4. Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif.
    Cell. 1994 Jul 29;78(2):275-89 PMID: 8044840
  5. Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1187-91 PMID: 7862658
  6. Pores for thought: nuclear pore complex proteins.
    Trends Cell Biol. 1994 Oct;4(10):357-65 PMID: 14731624
  7. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
  8. A temperature-sensitive NUP116 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic.
    J Cell Biol. 1993 Oct;123(2):275-84 PMID: 7691829
  9. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector.
    Gene. 1987;60(2-3):237-43 PMID: 3327750
  10. Labeling of RNA and phosphoproteins in Saccharomyces cerevisiae.
    Methods Enzymol. 1991;194:423-8 PMID: 2005801
  11. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast.
    Methods Enzymol. 1991;194:281-301 PMID: 2005793
  12. RNA export.
    Cell. 1995 Apr 21;81(2):153-9 PMID: 7537634
  13. A low-viscosity epoxy resin embedding medium for electron microscopy.
    J Ultrastruct Res. 1969 Jan;26(1):31-43 PMID: 4887011
  14. NUP2, a novel yeast nucleoporin, has functional overlap with other proteins of the nuclear pore complex.
    Mol Biol Cell. 1993 Feb;4(2):209-22 PMID: 8443417
  15. A new family of yeast nuclear pore complex proteins.
    J Cell Biol. 1992 Nov;119(4):705-23 PMID: 1385442
  16. Monoclonal antibodies identify a group of nuclear pore complex glycoproteins.
    J Cell Biol. 1987 May;104(5):1143-56 PMID: 2437126
  17. Yeast Srp1p has homology to armadillo/plakoglobin/beta-catenin and participates in apparently multiple nuclear functions including the maintenance of the nucleolar structure.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6880-4 PMID: 8041713
  18. High resolution scanning electron microscopy of the nuclear envelope: demonstration of a new, regular, fibrous lattice attached to the baskets of the nucleoplasmic face of the nuclear pores.
    J Cell Biol. 1992 Dec;119(6):1429-40 PMID: 1469043
  19. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers.
    Yeast. 1990 Sep-Oct;6(5):363-6 PMID: 2220072
  20. A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1.
    EMBO J. 1992 Dec;11(13):5051-61 PMID: 1464327
  21. Nuclear export of different classes of RNA is mediated by specific factors.
    J Cell Biol. 1994 Mar;124(5):627-35 PMID: 7509815
  22. Mutations in nucleolar proteins lead to nucleolar accumulation of polyA+ RNA in Saccharomyces cerevisiae.
    Mol Biol Cell. 1995 Sep;6(9):1103-10 PMID: 8534909
  23. nup1 mutants exhibit pleiotropic defects in nuclear pore complex function.
    J Cell Biol. 1994 Oct;127(2):319-32 PMID: 7929578
  24. Nuclear pore complex clustering and nuclear accumulation of poly(A)+ RNA associated with mutation of the Saccharomyces cerevisiae RAT2/NUP120 gene.
    J Cell Biol. 1995 Dec;131(6 Pt 2):1677-97 PMID: 8557737
  25. Pleiotropic nuclear defects associated with a conditional allele of the novel nucleoporin Rat9p/Nup85p.
    Mol Biol Cell. 1996 Jun;7(6):917-34 PMID: 8816998
  26. mRNA nuclear export.
    Curr Opin Genet Dev. 1994 Apr;4(2):305-9 PMID: 8032209
  27. NUP82 is an essential yeast nucleoporin required for poly(A)+ RNA export.
    J Cell Biol. 1995 Sep;130(6):1275-81 PMID: 7559751
  28. Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae.
    J Bacteriol. 1975 Oct;124(1):511-23 PMID: 1100612
  29. Nuclear transport.
    Curr Opin Cell Biol. 1994 Jun;6(3):335-42 PMID: 7917322
  30. Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes.
    Mol Biol Cell. 1995 Apr;6(4):401-417 PMID: 7626806
  31. Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA.
    Genes Dev. 1992 Jul;6(7):1173-89 PMID: 1628825
  32. Nuclear pore complex antigens delineate nuclear envelope dynamics in vegetative and conjugating Saccharomyces cerevisiae.
    Yeast. 1993 Mar;9(3):235-49 PMID: 8488725
  33. The nuclear pore complex.
    Annu Rev Biochem. 1995;64:865-96 PMID: 7574503
  34. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution.
    EMBO J. 1994 Dec 15;13(24):6062-75 PMID: 7813444
  35. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy.
    J Cell Biol. 1993 Jul;122(1):1-19 PMID: 8314837
  36. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
    Nucleic Acids Res. 1993 Jul 11;21(14):3329-30 PMID: 8341614
  37. Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport.
    J Cell Biol. 1995 Dec;131(6 Pt 2):1659-75 PMID: 8557736
  38. A conditional allele of the novel repeat-containing yeast nucleoporin RAT7/NUP159 causes both rapid cessation of mRNA export and reversible clustering of nuclear pore complexes.
    J Cell Biol. 1995 May;129(4):939-55 PMID: 7744966
  39. Transmission electron microscopy and immunocytochemical studies of yeast: analysis of HMG-CoA reductase overproduction by electron microscopy.
    Methods Cell Biol. 1989;31:473-512 PMID: 2674630
  40. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus.
    Mol Biol Cell. 1995 Apr;6(4):357-70 PMID: 7626803
  41. A novel receptor-mediated nuclear protein import pathway.
    Cell. 1996 Sep 20;86(6):985-94 PMID: 8808633
  42. NSP1: a yeast nuclear envelope protein localized at the nuclear pores exerts its essential function by its carboxy-terminal domain.
    Cell. 1990 Jun 15;61(6):979-89 PMID: 2112428
  43. NUP145 encodes a novel yeast glycine-leucine-phenylalanine-glycine (GLFG) nucleoporin required for nuclear envelope structure.
    J Cell Biol. 1994 Jun;125(5):955-69 PMID: 8195299
  44. Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein.
    J Cell Biol. 1988 Jul;107(1):17-31 PMID: 3292539
  45. Toward a more complete 3-D structure of the nuclear pore complex.
    J Struct Biol. 1991 Dec;107(3):291-308 PMID: 1725493
  46. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  47. A novel nuclear pore protein Nup82p which specifically binds to a fraction of Nsp1p.
    J Cell Biol. 1995 Sep;130(6):1263-73 PMID: 7559750
  48. Isolation of the yeast nuclear pore complex.
    J Cell Biol. 1993 Nov;123(4):771-83 PMID: 8227139
  49. Architecture and design of the nuclear pore complex.
    Cell. 1992 Jun 26;69(7):1133-41 PMID: 1617726
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-02-00
Pages
906-20
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC231817
Subset
IM
Grants
NIGMS NIH HHS · R01 GM033998 · United States
NCI NIH HHS · CA09658 · United States
NCI NIH HHS · CA16038 · United States
NIGMS NIH HHS · GM33998 · United States
Corrections
ErratumIn
-
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: [email protected]