Regulation of mRNA export in response to stress in Saccharomyces cerevisiae

Genes and Development

Volumn 10, Issue 13, 1996, Pages 1608-1620

  Saavedra, Claudio ^a   Tuug, Kuei Shu ^b,c   Amberg, David C ^a,d   Hopper, Anita K ^b   Cole, Charles N ^a,d  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^c YALE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

heat shock; in situ hybridization; Nucleocytoplamic transport; protein import; Ran TC4; yeast

Indexed keywords

ALCOHOL; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; NUCLEAR PROTEIN; NUCLEOPORIN; POLYADENYLATED RNA;

ARTICLE; CELLULAR DISTRIBUTION; CONSENSUS SEQUENCE; HEAT SHOCK; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN TRANSPORT; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; STRESS; TATA BOX;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0029737693     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.13.1608     Document Type: Article

References (73)

1. Aebi, M., M.W. Clark, U. Vijayraghavan, and J. Abelson. 1990. 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. 224: 72-80.
2. Amberg, D.C. 1992. "Isolation and characterization of essential genes of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA." Ph.D. thesis. Dartmouth College, Hanover, NH.
3. Amberg, D.C., A.L. Goldstein, and C.N. Cole. 1992. Isolation and characterization of RAT1, an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes & Dev. 6: 1173-1189.
4. Amberg, D.C., M. Fleischmann, I. Stagliar, C.N. Cole, and M. Aebi. 1993. Nuclear PRP20 protein is required for mRNA export. EMBO J. 12: 233-241.
5. Ashburner, M. and J.J. Bonner. 1979. The induction of gene activity in Drosophila by heat shock. Cell 17: 241-254.
6. Atkinson, N.S., R.W. Dunst, and A.K. Hopper. 1985. Characterization of an essential Saccharomyces cerevisiae gene related to RNA processing: Cloning of RNA1 and generation of a new allele with a novel phenotype. Mol. Cell. Biol. 5: 907-915.
7. Becker, J., F. Melchior, V. Cerke, F.R. Bischoff, H. Ponstingl, and A. Wittinghofer. 1995. RNA1 encodes a GTPase-activating protein specific for Gsplp, the Ran/TC4 homologue of Saccharomyces cerevisiae. J. Biol. Chem. 270: 11860-11865.
8. Belhumeur, P., A. Lee, R. Tam, T. DiPaolo, N. Fortin, and M.W. Clark. 1993. GSP1 and GSP2, genetic suppressors of the prp20-1 mutant in Saccharomyces cerevisiae: GTP-binding proteins involved in the maintenance of nuclear organization. Mol. Cell Biol. 13: 2152-2161.
9. Bischoff, F.R., H. Krebber, T. Kempf, I. Hermes, and H. Ponstingl. 1995. Human RanGTPase-activating protein RanGAP1 is a homologue of yeast Rnalp involved in mRNA processing and transport. Proc. Natl. Acad. Sci. 92: 1749-1753.
10. Bond, U. 1988. Heat shock but not other stress inducers leads to disruption of a sub-set of snRNPs and inhibition of in vitro splicing in HeLa cells. EMBO J. 7: 3509-3518.
11. Boorstein, W.R. and E.A. Craig. 1990. Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J. Biol. Chem. 265: 18912-18921.
12. Bossie, M., C. Dehoratius, G. Barcelo, and P. Silver. 1992. A mutant nuclear protein with similarity to RNA binding proteins interferes with nuclear protein import in yeast. Mol. Biol. Cell 3: 875-893.
13. Clark, K.L. and G.F. Sprague. 1989. Yeast pheromone response pathway: Characterization of a suppressor that restores mating to receptorless mutants. Mol. Cell. Biol. 9: 2682-2694.
14. Corbett, A.H., D.M. Koepp, G. Schlenstedt, M.S. Lee, A.K. Hopper, and P.A. Silver. 1995. Rnalp, a Ran/TC4 GTPase activating protein, is required for nuclear import. J. Cell Biol. 130: 1017-1026.
15. Craig, E.A. 1992. The heat shock response of Saccharomyces cerevisiae. In The molecular and cellular biology of the yeast Saccharomyces cerevisiae: Gene expression (ed. E.W. Jones, J.R. Pringle, and J.R. Broach), pp. 501-538. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
16. Dasso, M. 1993. RCC1 and the cell cycle: The regulator of chromosome condensation takes on new roles. Trends Biochem. Sci. 18: 96-101.
17. Dreyfuss, G. 1986. Structure and function of nuclear and cytoplasmic ribonucleoprotein particles. Annu. Rev. Cell Biol. 2: 459-498.
18. Dreyfuss, G., J.J. Mantunis, S. Pinol-Roma, and C.G. Burd. 1993. HnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62: 289-321.
19. Fischer, U., J. Huber, W.C. Boelens, I.W. Mattaj, and R. Lührmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular mRNAs. Cell 82: 475-483.
20. Flach, J., J. Vogel, M. Bossie, A. Corbett, T. Jinks, D. Willins, and P.A. Silver. 1994. A yeast RNA binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell. Biol. 12: 8399-8407.
21. Forrester, W., F. Stutz, M. Rosbash, and M. Wickens. 1992. Defects in mRNA 3′-end formation, transcription initiation, and mRNA transport associated with the yeast mutation prp20: Possible coupling of mRNA processing and chromatin structure. Genes & Dev. 6: 1914-1926.
22. Giardina, C. and J.T. Lis. 1995a. Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol. Cell. Biol. 15: 2737-2744.
23. _, 1995b. Sodium salicylate and yeast heat shock gene transcription. J. Biol. Chem. 270: 10269-10272.
24. Gorsch, L.C., T.C. Dockendorff, and C.N. Cole. 1995. 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. 129: 939-955.
25. Gross, D.S., K.E. English, K.W. Collins, and S. Lee. 1990. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements. J. Mol. Biol. 216: 611-631.
26. Gross, D.S., G.G. Adams, S. Lee, and B. Stentz. 1993. A critical role for the heat shock transcription factor in establishing a nucleosome-free region over the TATA-initiation site of the yeast HSP82 heat shock gene. EMBO J. 12: 3931-3945.
27. Guthrie, C. and G.R. Fink. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194: 423-424.
28. Hamm, J. and I.W. Mattaj. 1990. Monomethylated cap structures facilitate RNA export from the nucleus. Cell 63: 109-118.
29. Hartwell, L.H. 1967. Macromolecular synthesis in temperature-sensitive mutants in yeast. J. Bacterial. 93: 1662-1670.
30. Herruer, M.H., W.H. Mager, H.A. Raue, P. Vreken, E. Wilms, and R.J. Planta. 1988. Mild temperature shock affects transcription of yeast ribosomal protein genes as well as the stability of their mRNAs. Nucleic Acids Res. 16: 7917-7929.
31. Hopper, A.K., F. Banks, and V. Evangelidis. 1978. A yeast mutant which accumulates precursor tRNAs. Cell 14: 211-219.
32. Hopper, A.K., M.H. Traglia, and R.W. Dunst. 1990. The yeast RNA1 gene product necessary for RNA processing is located in the cytoplasm and apparently excluded from the nucleus. J. Cell Biol. 111: 309-321.
33. Jarmolowski, A., W.C. Boelens, E. Izaurralde, and I.W. Mattaj. 1994. Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol. 124: 627-635.
34. Kadowaki, T., Y. Zhao, and A.M. Tartakoff. 1992. A conditional yeast mutant deficient in mRNA transport from nucleus to cytoplasm. Proc. Natl. Acad. Sci. 89: 2312-2316.
35. Kadowaki, T., D. Goldfarb, L.M. Spitz, A.M. Tartakoff, and M. Ohno. 1993. Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J. 12: 2929-2937.
36. Lee, M.S., M. Henry, and P.A. Silver. 1996. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of mRNA export. Genes &. Dev. 10: 1233-1246.
37. Lindquist, S. 1986. The heat shock response. Annu. Rev. Biochem, 55: 1151-1191.
38. Lindquist, S. and E.A. Craig. 1988. The heat shock proteins. Annu. Rev. Genet. 22: 631-677.
39. McAlister, L. and D.B. Finkelstein. 1980. Alteration in translatable ribonucleic acid after heat shock of Saccharomyces cerevisiae. J. Bacteriol. 143: 603-612.
40. Melchior, F., and L. Gerace. 1995. Mechanisms of nuclear protein import. Curr. Opin. Cell Biol. 7: 310-318.
41. Melchior, F., B. Paschal, J. Evans, and L. Gerace. 1993. Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 123: 1649-1659.
42. Melchior, F., T. Guan, N. Yokoyama, T. Nishimoto, and L. Gerace. 1995. GTP hydrolysis by Ran occurs at the nuclear pore complex in an early step of protein import. J. Cell Biol. 131: 571-581.
43. Meyer, B.W. and M.H. Malim. 1994. The HIV-1 Rev trans-activator shuttles between the nucleus and cytoplasm. Genes &. Dev. 8: 1538-1547.
44. Michael, W.M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: A signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83: 415-422.
45. Miller, M.J., N.-H. Xuong, and E.P. Geiduschek. 1982. Quantitative analysis of the heat shock responses of Saccharomyces cerevisiae. J. Bacteriol. 151: 311-327.
46. Moore, M.S. and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365: 661-663.
47. Morimoto, R., A. Tissières, and C. Georgopoulos. 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Najarian, D., M.E. Dihanich, N.C. Martin, and A.K. Hopper. 1987. DNA sequence and transcript mapping of MODS: Features of the 5′ region which suggest two translational starts. Mol. Cell. Biol. 7: 185-191.
49. Nicolet, C.N. and E.A. Craig. 1991. Inducing and assaying heat-shock response in Saccharomyces cerevisiae. Methods Enzymol. 194: 710-717.
50. O'Brien, T. and J.T. Lis. 1991. RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene. Mol. Cell. Biol. 11: 5285-5290.
51. _. 1993. Rapid changes in Drosophila transcription after an instantaneous heat shock. Mol. Cell. Biol. 13: 3456-3463.
52. Osteryoung, K.W., H. Sundberg, and E. Vierling. 1993. Poly(A) tail length of a heat shock protein RNA is increased by severe heat stress, but intron splicing is unaffected. Mol. & Gen. Genet. 239: 323-333.
53. Peterson, G.L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83: 346-356.
54. Pinol-Roma, S. and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355: 730-732.
55. Rasmussen, E.B. and J.T. Lis. 1993. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl. Acad. Sci. 90: 7923-7927.
56. Rose, M.D., F. Winston, and P. Hieter. 1989. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Russell, I.D. and D. Tollervey. 1992. NOP3 is an essential yeast protein which is required for pre-rRNA processing. J. Cell Biol. 119: 737-747.
58. Sadis, S., E. Hickey, and L.A. Weber. 1988. Effect of heat shock on RNA metabolism in HeLa cells. J. Cell. Physiol. 135:377-386.
59. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. Sazer, S. 1996. The search for the primary function of the Ran GTPase continues. Trends Cell Biol. 6: 81-85.
61. Schlenstedt, G., C. Saavedra, J.D.J. Loeb, C.N. Cole, and P.A. Silver. 1995. The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A)+ RNA in the cytoplasm. Proc. Natl. Acad. Sci. 92: 225-229.
62. Schultz, L.D., K.J. Hofmann, L.M. Mylin, D.L. Montgomery, R.W. Ellis, and J.E. Hopper. 1987. Regulated overproduction of the GAL4 gene product greatly increases expression from galactose-inducible promoters on multicopy expression vectors in yeast. Gene 61: 123-133.
63. Shiokawa, K. and K.O. Pogo. 1974. The role of cytoplasmic membranes in controlling the transport of nuclear messenger RNA and initiation of protein synthesis. Proc. Natl. Acad. Sci. 71: 2658-2662.
64. Shukla, R.R., Z. Dominiski, T. Zwierzynski, and R. Kole. 1990. Inactivation of splicing factors in HeLa cells subjected to heat shock. J. Biol. Chem. 265: 20377-20383.
65. Tani, T., R.J. Derby, Y. Hiraoka, and D.L. Spector. 1995. Nucleolar accumulation of poly(A) + RNA in heat-shocked yeast cells: Implication of nucleolar involvement in mRNA transport. Mol. Biol. Cell 6: 1515-1534.
66. Traglia, H.M., N.S. Atkinson, and A.K. Hopper. 1989. Structural and functional analysis of Saccharomyces cerevisiae wild-type and mutant RNA1 genes. Mol. Cell. Biol. 9: 2989-2999.
67. Vijayraghavan, U., M. Company, and J. Abelson. 1989. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes & Dev. 3: 1206-1216.
68. Wilson, S.M., K.V. Datar, M.R. Paddy, J.R. Swedlow, and M.S. Swanson. 1994. Characterization of nuclear polyadenylated RNA binding proteins in Saccharomyces cerevisiae. J. Cell Biol. 127: 1173-1184.
69. Wu, C. 1980. The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 286: 854-860.
70. Yost, H.J. and S. Lindquist. 1986. RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45: 185-193.
71. _. 1991. Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae. Mol. Cell Biol. 11: 1062-1068.
72. Yost, H.J., R.B. Peterson, and S. Lindquist. 1990. RNA metabolism: strategies for regulation in heat shock response. Trends Genet. 6: 223-227.
73. Young, M.R. and E.A. Craig. 1993. Saccharomyces cerevisiae HSP70 heat shock elements are functionally distinct. Mol. Cell. Biol. 9: 5637-5646.