Skip to main content
PMC home page
Molecular Biology of the Cell logoLink to Molecular Biology of the Cell
. 1995 Nov;6(11):1515–1534. doi: 10.1091/mbc.6.11.1515

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

T Tani 1, R J Derby 1, Y Hiraoka 1, D L Spector 1
PMCID: PMC301308  PMID: 8589453

Abstract

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.

Full text

PDF
1517

Images in this article

1519Image
on p.1519
1520Image
on p.1520
1521Image
on p.1521
1522Image
on p.1522
1523Image
on p.1523
1524Image
on p.1524
1525Image
on p.1525
1526Image
on p.1526
1527Image
on p.1527
1529Image
on p.1529
1530Image
on p.1530

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aebi M., Clark M. W., Vijayraghavan U., Abelson J. A yeast mutant, PRP20, altered in mRNA metabolism and maintenance of the nuclear structure, is defective in a gene homologous to the human gene RCC1 which is involved in the control of chromosome condensation. Mol Gen Genet. 1990 Oct;224(1):72–80. doi: 10.1007/BF00259453. [DOI] [PubMed] [Google Scholar]
  2. Ainger K., Avossa D., Morgan F., Hill S. J., Barry C., Barbarese E., Carson J. H. Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J Cell Biol. 1993 Oct;123(2):431–441. doi: 10.1083/jcb.123.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amberg D. C., Fleischmann M., Stagljar I., Cole C. N., Aebi M. Nuclear PRP20 protein is required for mRNA export. EMBO J. 1993 Jan;12(1):233–241. doi: 10.1002/j.1460-2075.1993.tb05649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Amberg D. C., Goldstein A. L., Cole C. N. 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):1173–1189. doi: 10.1101/gad.6.7.1173. [DOI] [PubMed] [Google Scholar]
  5. Aris J. P., Blobel G. 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. doi: 10.1083/jcb.107.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berezney R. The nuclear matrix: a heuristic model for investigating genomic organization and function in the cell nucleus. J Cell Biochem. 1991 Oct;47(2):109–123. doi: 10.1002/jcb.240470204. [DOI] [PubMed] [Google Scholar]
  7. Bischoff F. R., Krebber H., Kempf T., Hermes I., Ponstingl H. Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rna1p involved in mRNA processing and transport. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1749–1753. doi: 10.1073/pnas.92.5.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bischoff F. R., Ponstingl H. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature. 1991 Nov 7;354(6348):80–82. doi: 10.1038/354080a0. [DOI] [PubMed] [Google Scholar]
  9. Bond U. 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. EMBO J. 1988 Nov;7(11):3509–3518. doi: 10.1002/j.1460-2075.1988.tb03227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bond V. C., Wold B. Nucleolar localization of myc transcripts. Mol Cell Biol. 1993 Jun;13(6):3221–3230. doi: 10.1128/mcb.13.6.3221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brockdorff N., Ashworth A., Kay G. F., McCabe V. M., Norris D. P., Cooper P. J., Swift S., Rastan S. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell. 1992 Oct 30;71(3):515–526. doi: 10.1016/0092-8674(92)90519-i. [DOI] [PubMed] [Google Scholar]
  12. Brown C. J., Hendrich B. D., Rupert J. L., Lafrenière R. G., Xing Y., Lawrence J., Willard H. F. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 1992 Oct 30;71(3):527–542. doi: 10.1016/0092-8674(92)90520-m. [DOI] [PubMed] [Google Scholar]
  13. Brown J. A., Bharathi A., Ghosh A., Whalen W., Fitzgerald E., Dhar R. A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J Biol Chem. 1995 Mar 31;270(13):7411–7419. doi: 10.1074/jbc.270.13.7411. [DOI] [PubMed] [Google Scholar]
  14. Carter K. C., Taneja K. L., Lawrence J. B. Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus. J Cell Biol. 1991 Dec;115(5):1191–1202. doi: 10.1083/jcb.115.5.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chang D. D., Sharp P. A. Messenger RNA transport and HIV rev regulation. Science. 1990 Aug 10;249(4969):614–615. doi: 10.1126/science.2143313. [DOI] [PubMed] [Google Scholar]
  16. Chang D. D., Sharp P. A. Regulation by HIV Rev depends upon recognition of splice sites. Cell. 1989 Dec 1;59(5):789–795. doi: 10.1016/0092-8674(89)90602-8. [DOI] [PubMed] [Google Scholar]
  17. Cheng Y., Dahlberg J. E., Lund E. Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. Science. 1995 Mar 24;267(5205):1807–1810. doi: 10.1126/science.7534442. [DOI] [PubMed] [Google Scholar]
  18. Chikashige Y., Ding D. Q., Funabiki H., Haraguchi T., Mashiko S., Yanagida M., Hiraoka Y. Telomere-led premeiotic chromosome movement in fission yeast. Science. 1994 Apr 8;264(5156):270–273. doi: 10.1126/science.8146661. [DOI] [PubMed] [Google Scholar]
  19. Ciejek E. M., Nordstrom J. L., Tsai M. J., O'Malley B. W. Ribonucleic acid precursors are associated with the chick oviduct nuclear matrix. Biochemistry. 1982 Sep 28;21(20):4945–4953. doi: 10.1021/bi00263a018. [DOI] [PubMed] [Google Scholar]
  20. Clark M. W., Yip M. L., Campbell J., Abelson J. 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. J Cell Biol. 1990 Nov;111(5 Pt 1):1741–1751. doi: 10.1083/jcb.111.5.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Cullen B. R., Hauber J., Campbell K., Sodroski J. G., Haseltine W. A., Rosen C. A. Subcellular localization of the human immunodeficiency virus trans-acting art gene product. J Virol. 1988 Jul;62(7):2498–2501. doi: 10.1128/jvi.62.7.2498-2501.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Denome R. M., Werner E. A., Patterson R. J. RNA metabolism in nuclei: adenovirus and heat shock alter intranuclear RNA compartmentalization. Nucleic Acids Res. 1989 Mar 11;17(5):2081–2098. doi: 10.1093/nar/17.5.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Deák I. I. Further experiments on the role of the nucleolus in the transfer of RNA from nucleus to cytoplasm. J Cell Sci. 1973 Sep;13(2):395–401. doi: 10.1242/jcs.13.2.395. [DOI] [PubMed] [Google Scholar]
  24. Ding D., Lipshitz H. D. Localized RNAs and their functions. Bioessays. 1993 Oct;15(10):651–658. doi: 10.1002/bies.950151004. [DOI] [PubMed] [Google Scholar]
  25. Dvorkin N., Clark M. W., Hamkalo B. A. Ultrastructural localization of nucleic acid sequences in Saccharomyces cerevisiae nucleoli. Chromosoma. 1991 Sep;100(8):519–523. doi: 10.1007/BF00352202. [DOI] [PubMed] [Google Scholar]
  26. Dworetzky S. I., Feldherr C. M. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J Cell Biol. 1988 Mar;106(3):575–584. doi: 10.1083/jcb.106.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Eckner R., Ellmeier W., Birnstiel M. L. Mature mRNA 3' end formation stimulates RNA export from the nucleus. EMBO J. 1991 Nov;10(11):3513–3522. doi: 10.1002/j.1460-2075.1991.tb04915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Felber B. K., Hadzopoulou-Cladaras M., Cladaras C., Copeland T., Pavlakis G. N. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1495–1499. doi: 10.1073/pnas.86.5.1495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Feldherr C. M., Akin D. EM visualization of nucleocytoplasmic transport processes. Electron Microsc Rev. 1990;3(1):73–86. doi: 10.1016/0892-0354(90)90014-j. [DOI] [PubMed] [Google Scholar]
  30. Fischer U., Lührmann R. An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus. Science. 1990 Aug 17;249(4970):786–790. doi: 10.1126/science.2143847. [DOI] [PubMed] [Google Scholar]
  31. Frendewey D., Barta I., Gillespie M., Potashkin J. Schizosaccharomyces U6 genes have a sequence within their introns that matches the B box consensus of tRNA internal promoters. Nucleic Acids Res. 1990 Apr 25;18(8):2025–2032. doi: 10.1093/nar/18.8.2025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Groner B., Phillips S. L. Polyadenylate metabolism in the nuclei and cytoplasm of Saccharomyces cerevisiae. J Biol Chem. 1975 Jul 25;250(14):5640–5646. [PubMed] [Google Scholar]
  33. Hamm J., Mattaj I. W. Monomethylated cap structures facilitate RNA export from the nucleus. Cell. 1990 Oct 5;63(1):109–118. doi: 10.1016/0092-8674(90)90292-m. [DOI] [PubMed] [Google Scholar]
  34. Harders J., Lukács N., Robert-Nicoud M., Jovin T. M., Riesner D. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO J. 1989 Dec 20;8(13):3941–3949. doi: 10.1002/j.1460-2075.1989.tb08577.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. He F., Peltz S. W., Donahue J. L., Rosbash M., Jacobson A. Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1- mutant. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7034–7038. doi: 10.1073/pnas.90.15.7034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Herrick D., Parker R., Jacobson A. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 1990 May;10(5):2269–2284. doi: 10.1128/mcb.10.5.2269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hirano T., Konoha G., Toda T., Yanagida M. Essential roles of the RNA polymerase I largest subunit and DNA topoisomerases in the formation of fission yeast nucleolus. J Cell Biol. 1989 Feb;108(2):243–253. doi: 10.1083/jcb.108.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hiraoka Y., Swedlow J. R., Paddy M. R., Agard D. A., Sedat J. W. Three-dimensional multiple-wavelength fluorescence microscopy for the structural analysis of biological phenomena. Semin Cell Biol. 1991 Jun;2(3):153–165. [PubMed] [Google Scholar]
  39. Hogan N. C., Traverse K. L., Sullivan D. E., Pardue M. L. The nucleus-limited Hsr-omega-n transcript is a polyadenylated RNA with a regulated intranuclear turnover. J Cell Biol. 1994 Apr;125(1):21–30. doi: 10.1083/jcb.125.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Hopper A. K., Banks F. A yeast mutant which accumulates precursor tRNAs. Cell. 1978 Jun;14(2):211–219. doi: 10.1016/0092-8674(78)90108-3. [DOI] [PubMed] [Google Scholar]
  41. Huang S., Deerinck T. J., Ellisman M. H., Spector D. L. In vivo analysis of the stability and transport of nuclear poly(A)+ RNA. J Cell Biol. 1994 Aug;126(4):877–899. doi: 10.1083/jcb.126.4.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Huang S., Spector D. L. Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. Genes Dev. 1991 Dec;5(12A):2288–2302. doi: 10.1101/gad.5.12a.2288. [DOI] [PubMed] [Google Scholar]
  43. Hynes N. E., Phillips S. L. Turnover of polyadenylate-containing ribonucleic acid in Saccharomyces cerevisiae. J Bacteriol. 1976 Feb;125(2):595–600. doi: 10.1128/jb.125.2.595-600.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Izaurralde E., Mattaj I. W. Transport of RNA between nucleus and cytoplasm. Semin Cell Biol. 1992 Aug;3(4):279–288. doi: 10.1016/1043-4682(92)90029-u. [DOI] [PubMed] [Google Scholar]
  45. Kadowaki T., Chen S., Hitomi M., Jacobs E., Kumagai C., Liang S., Schneiter R., Singleton D., Wisniewska J., Tartakoff A. M. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J Cell Biol. 1994 Aug;126(3):649–659. doi: 10.1083/jcb.126.3.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Kadowaki T., Goldfarb D., Spitz L. M., Tartakoff A. M., Ohno M. Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J. 1993 Jul;12(7):2929–2937. doi: 10.1002/j.1460-2075.1993.tb05955.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kadowaki T., Hitomi M., Chen S., Tartakoff A. M. Nuclear mRNA accumulation causes nucleolar fragmentation in yeast mtr2 mutant. Mol Biol Cell. 1994 Nov;5(11):1253–1263. doi: 10.1091/mbc.5.11.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kadowaki T., Zhao Y., Tartakoff A. M. A conditional yeast mutant deficient in mRNA transport from nucleus to cytoplasm. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2312–2316. doi: 10.1073/pnas.89.6.2312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kalland K. H., Langhoff E., Bos H. J., Göttlinger H., Haseltine W. A. Rex-dependent nucleolar accumulation of HTLV-I mRNAs. New Biol. 1991 Apr;3(4):389–397. [PubMed] [Google Scholar]
  50. Krainer A. R. Pre-mRNA splicing by complementation with purified human U1, U2, U4/U6 and U5 snRNPs. Nucleic Acids Res. 1988 Oct 25;16(20):9415–9429. doi: 10.1093/nar/16.20.9415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Lawrence J. B., Singer R. H., Marselle L. M. Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization. Cell. 1989 May 5;57(3):493–502. doi: 10.1016/0092-8674(89)90924-0. [DOI] [PubMed] [Google Scholar]
  52. Legrain P., Rosbash M. Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm. Cell. 1989 May 19;57(4):573–583. doi: 10.1016/0092-8674(89)90127-x. [DOI] [PubMed] [Google Scholar]
  53. Li O., Heath C. V., Amberg D. C., Dockendorff T. C., Copeland C. S., Snyder M., Cole C. N. 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. doi: 10.1091/mbc.6.4.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Lindquist S. Translational efficiency of heat-induced messages in Drosophila melanogaster cells. J Mol Biol. 1980 Feb 25;137(2):151–158. doi: 10.1016/0022-2836(80)90322-8. [DOI] [PubMed] [Google Scholar]
  55. Maquat L. E. Nuclear mRNA export. Curr Opin Cell Biol. 1991 Dec;3(6):1004–1012. doi: 10.1016/0955-0674(91)90121-e. [DOI] [PubMed] [Google Scholar]
  56. Mariman E. C., van Eekelen C. A., Reinders R. J., Berns A. J., van Venrooij W. J. Adenoviral heterogeneous nuclear RNA is associated with the host nuclear matrix during splicing. J Mol Biol. 1982 Jan 5;154(1):103–119. doi: 10.1016/0022-2836(82)90420-x. [DOI] [PubMed] [Google Scholar]
  57. Marshallsay C., Lührmann R. In vitro nuclear import of snRNPs: cytosolic factors mediate m3G-cap dependence of U1 and U2 snRNP transport. EMBO J. 1994 Jan 1;13(1):222–231. doi: 10.1002/j.1460-2075.1994.tb06252.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Matsumoto T., Beach D. Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell. 1991 Jul 26;66(2):347–360. doi: 10.1016/0092-8674(91)90624-8. [DOI] [PubMed] [Google Scholar]
  59. McCully E. K., Robinow C. F. Mitosis in the fission yeast Schizosaccharomyces pombe: a comparative study with light and electron microscopy. J Cell Sci. 1971 Sep;9(2):475–507. doi: 10.1242/jcs.9.2.475. [DOI] [PubMed] [Google Scholar]
  60. McKenzie S. L., Meselson M. Translation in vitro of Drosophila heat-shock messages. J Mol Biol. 1977 Nov 25;117(1):279–283. doi: 10.1016/0022-2836(77)90035-3. [DOI] [PubMed] [Google Scholar]
  61. Mehlin H., Daneholt B., Skoglund U. Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell. 1992 May 15;69(4):605–613. doi: 10.1016/0092-8674(92)90224-z. [DOI] [PubMed] [Google Scholar]
  62. Molenaar I., Sillevis Smitt W. W., Rozijn T. H., Tonino G. J. Biochemical and electron microscopic study of isolated yeast nuclei. Exp Cell Res. 1970 May;60(2):148–156. doi: 10.1016/0014-4827(70)90500-8. [DOI] [PubMed] [Google Scholar]
  63. Nigg E. A., Baeuerle P. A., Lührmann R. Nuclear import-export: in search of signals and mechanisms. Cell. 1991 Jul 12;66(1):15–22. doi: 10.1016/0092-8674(91)90135-l. [DOI] [PubMed] [Google Scholar]
  64. Nosaka T., Siomi H., Adachi Y., Ishibashi M., Kubota S., Maki M., Hatanaka M. Nucleolar targeting signal of human T-cell leukemia virus type I rex-encoded protein is essential for cytoplasmic accumulation of unspliced viral mRNA. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9798–9802. doi: 10.1073/pnas.86.24.9798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Ochs R. L., Lischwe M. A., Spohn W. H., Busch H. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell. 1985;54(2):123–133. doi: 10.1111/j.1768-322x.1985.tb00387.x. [DOI] [PubMed] [Google Scholar]
  66. Parsell D. A., Sanchez Y., Stitzel J. D., Lindquist S. Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature. 1991 Sep 19;353(6341):270–273. doi: 10.1038/353270a0. [DOI] [PubMed] [Google Scholar]
  67. Piper P. W., Aamand J. L. Yeast mutation thought to arrest mRNA transport markedly increases the length of the 3' poly(A) on polyadenylated RNA. J Mol Biol. 1989 Aug 20;208(4):697–700. doi: 10.1016/0022-2836(89)90159-9. [DOI] [PubMed] [Google Scholar]
  68. Potashkin J. A., Derby R. J., Spector D. L. Differential distribution of factors involved in pre-mRNA processing in the yeast cell nucleus. Mol Cell Biol. 1990 Jul;10(7):3524–3534. doi: 10.1128/mcb.10.7.3524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Russell P. R., Hall B. D. The primary structure of the alcohol dehydrogenase gene from the fission yeast Schizosaccharomyces pombe. J Biol Chem. 1983 Jan 10;258(1):143–149. [PubMed] [Google Scholar]
  71. Sadis S., Hickey E., Weber L. A. Effect of heat shock on RNA metabolism in HeLa cells. J Cell Physiol. 1988 Jun;135(3):377–386. doi: 10.1002/jcp.1041350304. [DOI] [PubMed] [Google Scholar]
  72. Santiago T. C., Purvis I. J., Bettany A. J., Brown A. J. The relationship between mRNA stability and length in Saccharomyces cerevisiae. Nucleic Acids Res. 1986 Nov 11;14(21):8347–8360. doi: 10.1093/nar/14.21.8347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Schimmang T., Tollervey D., Kern H., Frank R., Hurt E. C. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 1989 Dec 20;8(13):4015–4024. doi: 10.1002/j.1460-2075.1989.tb08584.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Schneiter R., Kadowaki T., Tartakoff A. M. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus. Mol Biol Cell. 1995 Apr;6(4):357–370. doi: 10.1091/mbc.6.4.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Schröder H. C., Bachmann M., Diehl-Seifert B., Müller W. E. Transport of mRNA from nucleus to cytoplasm. Prog Nucleic Acid Res Mol Biol. 1987;34:89–142. doi: 10.1016/s0079-6603(08)60494-8. [DOI] [PubMed] [Google Scholar]
  76. Shiokawa K., Pogo A. O. The role of cytoplasmic membranes in controlling the transport of nuclear messenger RNA and initiation of protein synthesis. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2658–2662. doi: 10.1073/pnas.71.7.2658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Singer R. H. The cytoskeleton and mRNA localization. Curr Opin Cell Biol. 1992 Feb;4(1):15–19. doi: 10.1016/0955-0674(92)90053-f. [DOI] [PubMed] [Google Scholar]
  78. Siomi H., Shida H., Nam S. H., Nosaka T., Maki M., Hatanaka M. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell. 1988 Oct 21;55(2):197–209. doi: 10.1016/0092-8674(88)90043-8. [DOI] [PubMed] [Google Scholar]
  79. Smith H. C., Harris S. G., Zillmann M., Berget S. M. Evidence that a nuclear matrix protein participates in premessenger RNA splicing. Exp Cell Res. 1989 Jun;182(2):521–533. doi: 10.1016/0014-4827(89)90255-3. [DOI] [PubMed] [Google Scholar]
  80. Smith H. C., Ochs R. L., Fernandez E. A., Spector D. L. Macromolecular domains containing nuclear protein p107 and U-snRNP protein p28: further evidence for an in situ nuclear matrix. Mol Cell Biochem. 1986 May;70(2):151–168. doi: 10.1007/BF00229430. [DOI] [PubMed] [Google Scholar]
  81. Smitt W. W., Vermeulen C. A., Vlak J. M., Rozijn T. H., Molenaar I. Electron microscopic autoradiographic study of RNA synthesis in yeast nucleus. Exp Cell Res. 1972 Jan;70(1):140–144. doi: 10.1016/0014-4827(72)90191-7. [DOI] [PubMed] [Google Scholar]
  82. Smitt W. W., Vlak J. M., Molenaar I., Rozijn T. H. Nucleolar function of the dense crescent in the yeast nucleus. A biochemical and ultrastructural study. Exp Cell Res. 1973 Aug;80(2):313–321. doi: 10.1016/0014-4827(73)90302-9. [DOI] [PubMed] [Google Scholar]
  83. Spector D. L. Macromolecular domains within the cell nucleus. Annu Rev Cell Biol. 1993;9:265–315. doi: 10.1146/annurev.cb.09.110193.001405. [DOI] [PubMed] [Google Scholar]
  84. Spector D. L., Schrier W. H., Busch H. Immunoelectron microscopic localization of snRNPs. Biol Cell. 1983;49(1):1–10. doi: 10.1111/j.1768-322x.1984.tb00215.x. [DOI] [PubMed] [Google Scholar]
  85. Spradling A., Pardue M. L., Penman S. Messenger RNA in heat-shocked Drosophila cells. J Mol Biol. 1977 Feb 5;109(4):559–587. doi: 10.1016/s0022-2836(77)80091-0. [DOI] [PubMed] [Google Scholar]
  86. Tanaka K., Kanbe T. Mitosis in the fission yeast Schizosaccharomyces pombe as revealed by freeze-substitution electron microscopy. J Cell Sci. 1986 Feb;80:253–268. doi: 10.1242/jcs.80.1.253. [DOI] [PubMed] [Google Scholar]
  87. Tani T., Ohshima Y. The gene for the U6 small nuclear RNA in fission yeast has an intron. Nature. 1989 Jan 5;337(6202):87–90. doi: 10.1038/337087a0. [DOI] [PubMed] [Google Scholar]
  88. Tani T., Ohshima Y. mRNA-type introns in U6 small nuclear RNA genes: implications for the catalysis in pre-mRNA splicing. Genes Dev. 1991 Jun;5(6):1022–1031. doi: 10.1101/gad.5.6.1022. [DOI] [PubMed] [Google Scholar]
  89. Uchida S., Sekiguchi T., Nishitani H., Miyauchi K., Ohtsubo M., Nishimoto T. Premature chromosome condensation is induced by a point mutation in the hamster RCC1 gene. Mol Cell Biol. 1990 Feb;10(2):577–584. doi: 10.1128/mcb.10.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Verheijen R., van Venrooij W., Ramaekers F. The nuclear matrix: structure and composition. J Cell Sci. 1988 May;90(Pt 1):11–36. doi: 10.1242/jcs.90.1.11. [DOI] [PubMed] [Google Scholar]
  91. Visa N., Puvion-Dutilleul F., Harper F., Bachellerie J. P., Puvion E. Intranuclear distribution of poly(A) RNA determined by electron microscope in situ hybridization. Exp Cell Res. 1993 Sep;208(1):19–34. doi: 10.1006/excr.1993.1218. [DOI] [PubMed] [Google Scholar]
  92. Vogelstein B., Hunt B. F. A subset of small nuclear ribonucleoprotein particle antigens is a component of the nuclear matrix. Biochem Biophys Res Commun. 1982 Apr 14;105(3):1224–1232. doi: 10.1016/0006-291x(82)91099-3. [DOI] [PubMed] [Google Scholar]
  93. Welch W. J., Suhan J. P. 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. J Cell Biol. 1985 Oct;101(4):1198–1211. doi: 10.1083/jcb.101.4.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Wilhelm J. E., Vale R. D. RNA on the move: the mRNA localization pathway. J Cell Biol. 1993 Oct;123(2):269–274. doi: 10.1083/jcb.123.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Xing Y. G., Lawrence J. B. Preservation of specific RNA distribution within the chromatin-depleted nuclear substructure demonstrated by in situ hybridization coupled with biochemical fractionation. J Cell Biol. 1991 Mar;112(6):1055–1063. doi: 10.1083/jcb.112.6.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Xing Y., Johnson C. V., Dobner P. R., Lawrence J. B. Higher level organization of individual gene transcription and RNA splicing. Science. 1993 Feb 26;259(5099):1326–1330. doi: 10.1126/science.8446901. [DOI] [PubMed] [Google Scholar]
  97. Yost H. J., Lindquist S. Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae. Mol Cell Biol. 1991 Feb;11(2):1062–1068. doi: 10.1128/mcb.11.2.1062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Yost H. J., Lindquist S. RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell. 1986 Apr 25;45(2):185–193. doi: 10.1016/0092-8674(86)90382-x. [DOI] [PubMed] [Google Scholar]
  99. Yost H. J., Lindquist S. Translation of unspliced transcripts after heat shock. Science. 1988 Dec 16;242(4885):1544–1548. doi: 10.1126/science.3201243. [DOI] [PubMed] [Google Scholar]
  100. Zachar Z., Kramer J., Mims I. P., Bingham P. M. Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans. J Cell Biol. 1993 May;121(4):729–742. doi: 10.1083/jcb.121.4.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Zeitlin S., Parent A., Silverstein S., Efstratiadis A. Pre-mRNA splicing and the nuclear matrix. Mol Cell Biol. 1987 Jan;7(1):111–120. doi: 10.1128/mcb.7.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Zeitlin S., Wilson R. C., Efstratiadis A. Autonomous splicing and complementation of in vivo-assembled spliceosomes. J Cell Biol. 1989 Mar;108(3):765–777. doi: 10.1083/jcb.108.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular Biology of the Cell are provided here courtesy of American Society for Cell Biology

RESOURCES