Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport.

Transport of mRNA from the nucleus to the cytoplasm plays an important role in gene expression in eukaryotic cells. In wild-type Schizosaccharomyces pombe cells poly(A)+ RNA is uniformly distributed throughout the nucleoplasm and cytoplasm. However, we found that a severe heat shock blocks mRNA transport in S. pombe, resulting in the accumulation of bulk poly(A)+ RNA, as well as a specific intron-less transcript, in the nucleoli. Pretreatment of cells with a mild heat shock, which induces heat shock proteins, before a severe heat shock protects the mRNA transport machinery and allows mRNA transport to proceed unimpeded. In heat-shocked S. pombe cells, the nucleolar region condensed into a few compact structures. Interestingly, poly(A)+ RNA accumulated predominantly in the condensed nucleolar regions of the heat-shocked cells. These data suggest that the yeast nucleolus may play a role in mRNA transport in addition to its roles in rRNA synthesis and preribosome assembly.

[1]  A. Ishihama,et al.  Isolation of thermolabile mutant RNA polymerase II from fission yeast Schizosaccharomyces pombe with mutations in the subunit 3 gene. , 1995, Journal of biochemistry.

[2]  R. Schneiter,et al.  mRNA transport in yeast: time to reinvestigate the functions of the nucleolus. , 1995, Molecular biology of the cell.

[3]  M. Snyder,et al.  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. , 1995, Molecular biology of the cell.

[4]  Julie A. Brown,et al.  A Mutation in the Schizosaccharomyces pombe rae1 Gene Causes Defects in Poly(A)+ RNA Export and in the Cytoskeleton (*) , 1995, The Journal of Biological Chemistry.

[5]  E. Lund,et al.  Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. , 1995, Science.

[6]  F. Bischoff,et al.  Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  S. Chen,et al.  Nuclear mRNA accumulation causes nucleolar fragmentation in yeast mtr2 mutant. , 1994, Molecular biology of the cell.

[8]  T. Deerinck,et al.  In vivo analysis of the stability and transport of nuclear poly(A)+ RNA , 1994, The Journal of cell biology.

[9]  R. Schneiter,et al.  Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants [published erratum appears in J Cell Biol 1994 Sep;126(6):1627] , 1994, The Journal of cell biology.

[10]  R. Schneiter,et al.  Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants , 1994 .

[11]  M. Yanagida,et al.  Telomere-led premeiotic chromosome movement in fission yeast. , 1994, Science.

[12]  M. Pardue,et al.  The nucleus-limited Hsr-omega-n transcript is a polyadenylated RNA with a regulated intranuclear turnover , 1994, The Journal of cell biology.

[13]  R. Lührmann,et al.  In vitro nuclear import of snRNPs: cytosolic factors mediate m3G‐cap dependence of U1 and U2 snRNP transport. , 1994, The EMBO journal.

[14]  R. Vale,et al.  RNA on the move: the mRNA localization pathway [published erratum appears in J Cell Biol 1993 Dec;123(6 Pt 1):1625] , 1993, The Journal of cell biology.

[15]  J. Carson,et al.  Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes , 1993, The Journal of cell biology.

[16]  H. Lipshitz,et al.  Localized RNAs and their functions , 1993, BioEssays : news and reviews in molecular, cellular and developmental biology.

[17]  J. Bachellerie,et al.  Intranuclear distribution of poly(A) RNA determined by electron microscope in situ hybridization. , 1993, Experimental cell research.

[18]  S. Peltz,et al.  Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1- mutant. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Goldfarb,et al.  Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. , 1993, The EMBO journal.

[20]  B. Wold,et al.  Nucleolar localization of myc transcripts , 1993, Molecular and cellular biology.

[21]  P. Bingham,et al.  Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans , 1993, The Journal of cell biology.

[22]  J. Lawrence,et al.  Higher level organization of individual gene transcription and RNA splicing. , 1993, Science.

[23]  M. Aebi,et al.  Nuclear PRP20 protein is required for mRNA export. , 1993, The EMBO journal.

[24]  D. Spector,et al.  Macromolecular domains within the cell nucleus. , 1993, Annual review of cell biology.

[25]  Carolyn J. Brown,et al.  The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus , 1992, Cell.

[26]  I. Mattaj,et al.  Transport of RNA between nucleus and cytoplasm. , 1992, Seminars in cell biology.

[27]  C. Cole,et al.  Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. , 1992, Genes & development.

[28]  B. Daneholt,et al.  Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography , 1992, Cell.

[29]  Y. Zhao,et al.  A conditional yeast mutant deficient in mRNA transport from nucleus to cytoplasm. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Robert H. Singer,et al.  The cytoskeleton and mRNA localization , 1992, Current Biology.

[31]  L. Maquat.  Nuclear mRNA export. , 1991, Current opinion in cell biology.

[32]  D. Spector,et al.  Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. , 1991, Genes & development.

[33]  J. Lawrence,et al.  Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus , 1991, The Journal of cell biology.

[34]  F. Bischoff,et al.  Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1 , 1991, Nature.

[35]  W. Ellmeier,et al.  Mature mRNA 3′ end formation stimulates RNA export from the nucleus. , 1991, The EMBO journal.

[36]  R Berezney,et al.  The nuclear matrix: A heuristic model for investigating genomic organization and function in the cell nucleus , 1991, Journal of cellular biochemistry.

[37]  S. Lindquist,et al.  Hspl04 is a highly conserved protein with two essential nucleotide-binding sites , 1991, Nature.

[38]  Tomohiro Matsumoto,et al.  Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase , 1991, Cell.

[39]  R. Lührmann,et al.  Nuclear import-export: In search of signals and mechanisms , 1991, Cell.

[40]  J. Swedlow,et al.  Three-dimensional multiple-wavelength fluorescence microscopy for the structural analysis of biological phenomena. , 1991, Seminars in cell biology.

[41]  Y. Ohshima,et al.  mRNA-type introns in U6 small nuclear RNA genes: implications for the catalysis in pre-mRNA splicing. , 1991, Genes & development.

[42]  K. Kalland,et al.  Rex-dependent nucleolar accumulation of HTLV-I mRNAs. , 1991, The New biologist.

[43]  J. Lawrence,et al.  Preservation of specific RNA distribution within the chromatin-depleted nuclear substructure demonstrated by in situ hybridization coupled with biochemical fractionation , 1991, The Journal of cell biology.

[44]  S. Lindquist,et al.  Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae , 1991, Molecular and cellular biology.

[45]  M. W. Clark,et al.  SSB-1 of the yeast Saccharomyces cerevisiae is a nucleolar-specific, silver-binding protein that is associated with the snR10 and snR11 small nuclear RNAs , 1990, The Journal of cell biology.

[46]  I. Mattaj,et al.  Monomethylated cap structures facilitate RNA export from the nucleus , 1990, Cell.

[47]  R. Lührmann,et al.  An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus. , 1990, Science.

[48]  D. Chang,et al.  Messenger RNA transport and HIV rev regulation. , 1990, Science.

[49]  J. Potashkin,et al.  Differential distribution of factors involved in pre-mRNA processing in the yeast cell nucleus , 1990, Molecular and cellular biology.

[50]  R Parker,et al.  Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae , 1990, Molecular and cellular biology.

[51]  M. Gillespie,et al.  Schizosaccharomyces U6 genes have a sequence within their introns that matches the B box consensus of tRNA internal promoters. , 1990, Nucleic acids research.

[52]  M. Ohtsubo,et al.  Premature chromosome condensation is induced by a point mutation in the hamster RCC1 gene , 1990, Molecular and cellular biology.

[53]  C. Feldherr,et al.  EM visualization of nucleocytoplasmic transport processes. , 1990, Electron microscopy reviews.

[54]  P. Sharp,et al.  Regulation by HIV Rev depends upon recognition of splice sites , 1989, Cell.

[55]  D. Tollervey,et al.  A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. , 1989, The EMBO journal.

[56]  M. Maki,et al.  Nucleolar targeting signal of human T-cell leukemia virus type I rex-encoded protein is essential for cytoplasmic accumulation of unspliced viral mRNA. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Riesner,et al.  Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. , 1989, The EMBO journal.

[58]  P. Piper,et al.  Yeast mutation thought to arrest mRNA transport markedly increases the length of the 3' poly(A) on polyadenylated RNA. , 1989, Journal of molecular biology.

[59]  S. Berget,et al.  Evidence that a nuclear matrix protein participates in premessenger RNA splicing. , 1989, Experimental cell research.

[60]  P. Legrain,et al.  Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm , 1989, Cell.

[61]  Robert H. Singer,et al.  Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization , 1989, Cell.

[62]  R. Patterson,et al.  RNA metabolism in nuclei: adenovirus and heat shock alter intranuclear RNA compartmentalization. , 1989, Nucleic acids research.

[63]  T. Copeland,et al.  rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[64]  S. Zeitlin,et al.  Autonomous splicing and complementation of in vivo-assembled spliceosomes , 1989, The Journal of cell biology.

[65]  T. Toda,et al.  Essential roles of the RNA polymerase I largest subunit and DNA topoisomerases in the formation of fission yeast nucleolus , 1989, The Journal of cell biology.

[66]  Y. Ohshima,et al.  The gene for the U6 small nuclear RNA in fission yeast has an intron , 1989, Nature.

[67]  J. Hyams,et al.  8 – General Cytology of Fission Yeasts , 1989 .

[68]  S. Lindquist,et al.  Translation of unspliced transcripts after heat shock. , 1988, Science.

[69]  U. Bond,et al.  Heat shock but not other stress inducers leads to the disruption of a sub‐set of snRNPs and inhibition of in vitro splicing in HeLa cells. , 1988, The EMBO journal.

[70]  A. Krainer.  Pre-mRNA splicing by complementation with purified human U1, U2, U4/U6 and U5 snRNPs. , 1988, Nucleic acids research.

[71]  M. Maki,et al.  Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing , 1988, Cell.

[72]  B. Cullen,et al.  Subcellular localization of the human immunodeficiency virus trans-acting art gene product , 1988, Journal of virology.

[73]  G. Blobel,et al.  Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein , 1988, The Journal of cell biology.

[74]  S. Sadis,et al.  Effect of heat shock on RNA metabolism in HeLa cells , 1988, Journal of cellular physiology.

[75]  W. V. van Venrooij,et al.  The nuclear matrix: structure and composition. , 1988, Journal of cell science.

[76]  C. Feldherr,et al.  Translocation of RNA-coated gold particles through the nuclear pores of oocytes , 1988, The Journal of cell biology.

[77]  S. Zeitlin,et al.  Pre-mRNA splicing and the nuclear matrix , 1987, Molecular and cellular biology.

[78]  H. Schröder,et al.  Transport of mRNA from nucleus to cytoplasm. , 1987, Progress in nucleic acid research and molecular biology.

[79]  I. Purvis,et al.  The relationship between mRNA stability and length in Saccharomyces cerevisiae. , 1986, Nucleic acids research.

[80]  S. Lindquist,et al.  RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis , 1986, Cell.

[81]  T. Kanbe,et al.  Mitosis in the fission yeast Schizosaccharomyces pombe as revealed by freeze-substitution electron microscopy. , 1986, Journal of cell science.

[82]  W. Welch,et al.  Morphological study of the mammalian stress response: characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment , 1985, The Journal of cell biology.

[83]  R. Ochs,et al.  Fibrillarin: a new protein of the nucleolus identified by autoimmune sera , 1985, Biology of the cell.

[84]  B. Hall,et al.  The primary structure of the alcohol dehydrogenase gene from the fission yeast Schizosaccharomyces pombe. , 1983, The Journal of biological chemistry.

[85]  D. Spector,et al.  Immunoelectron microscopic localization of snRNPs , 1983, Biology of the cell.

[86]  B. O’Malley,et al.  Ribonucleic acid precursors are associated with the chick oviduct nuclear matrix. , 1982, Biochemistry.

[87]  B. Vogelstein,et al.  A subset of small nuclear ribonucleoprotein particle antigens is a component of the nuclear matrix. , 1982, Biochemical and biophysical research communications.

[88]  E. Mariman,et al.  Adenoviral heterogeneous nuclear RNA is associated with the host nuclear matrix during splicing. , 1982, Journal of molecular biology.

[89]  S. Lindquist,et al.  Translational efficiency of heat-induced messages in Drosophila melanogaster cells. , 1980, Journal of molecular biology.

[90]  A. Hopper,et al.  A yeast mutant which accumulates precursor tRNAs , 1978, Cell.

[91]  M. Meselson,et al.  Translation in vitro of Drosophila heat-shock messages. , 1977, Journal of molecular biology.

[92]  A. Spradling,et al.  Messenger RNA in heat-shocked Drosophila cells. , 1977, Journal of molecular biology.

[93]  N. Hynes,et al.  Rate of Synthesis of Polyadenylate-Containing Ribonucleic Acid During the Yeast Cell Cycle , 1976, Journal of bacteriology.

[94]  N. Hynes,et al.  Turnover of polyadenylate-containing ribonucleic acid in Saccharomyces cerevisiae , 1976, Journal of bacteriology.

[95]  B. Groner,et al.  Polyadenylate metabolism in the nuclei and cytoplasm of Saccharomyces cerevisiae. , 1975, The Journal of biological chemistry.

[96]  K. Shiokawa,et al.  The role of cytoplasmic membranes in controlling the transport of nuclear messenger RNA and initiation of protein synthesis. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[97]  I. Deàk.  Further experiments on the role of the nucleolus in the transfer of RNA from nucleus to cytoplasm. , 1973, Journal of cell science.

[98]  J. Vlak,et al.  Nucleolar function of the dense crescent in the yeast nucleus. A biochemical and ultrastructural study. , 1973, Experimental cell research.

[99]  J. Vlak,et al.  Electron microscopic autoradiographic study of RNA synthesis in yeast nucleus. , 1972, Experimental cell research.

[100]  C. Robinow,et al.  Mitosis in the fission yeast Schizosaccharomyces pombe: a comparative study with light and electron microscopy. , 1971, Journal of cell science.

[101]  I. Molenaar,et al.  Biochemical and electron microscopic study of isolated yeast nuclei. , 1970, Experimental cell research.

[102]  H. Harris,et al.  The Role of the Nucleolus in the Transfer of RNA from Nucleus to Cytoplasm , 1969 .

[103]  E. Reynolds.  THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.