Nuclear RanGTP is not required for targeting small nucleolar RNAs to the nucleolus

Journal of Cell Science

Volumn 116, Issue 1, 2003, Pages 177-186

  Narayanan, Aarthi ^a   Eifert, Julia ^a   Marfatia, Kavita A ^b   Macara, Ian G ^c   Corbett, Anita H ^b   Terns, Rebecca M ^a   Terns, Michael P ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Nucleolus; RanGTP; RNA transport; S. cerevisiae; Small nucleolar RNA; tsBN2; Xenopus oocytes

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MUTANT PROTEIN; NUCLEAR PROTEIN; NUCLEAR RNA; RAN PROTEIN; REGULATOR PROTEIN;

ANIMAL CELL; BUDDING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; INTRACELLULAR TRANSPORT; MICROINJECTION; MOLECULAR SIZE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; XENOPUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL COMPARTMENTATION; CELL CYCLE PROTEINS; CELL LINE; CELL NUCLEOLUS; CRICETINAE; CYTOPLASM; EUKARYOTIC CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MICROINJECTIONS; MUTATION; NUCLEAR PROTEINS; OOCYTES; RAN GTP-BINDING PROTEIN; RNA TRANSPORT; RNA, SMALL NUCLEOLAR; SACCHAROMYCES; XENOPUS; XENOPUS PROTEINS;

ANIMALIA; MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0037239731     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00176     Document Type: Review

References (77)

1. Adams, A., Gottschling, D. E., Kaiser, C. A. and Stearns, T. (1997). Methods in Yeast Genetics. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
2. Aebi, M., Clark, M. W., Vijayraghavan, U. and Abelson, J. (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.
3. Amberg, D. C., Goldstein, A. L. and Cole, C. N. (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., Fleischmann, M., Stagljar, I., Cole, C. N. and Aebi, M. (1993). Nuclear PRP20 protein is required for mRNA export. EMBO J. 12, 233-241.
5. Aris, J. P. and Blobel, G. (1988). Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein. J. Cell Biol. 107, 17-31.
6. Arts, G. J., Fornerod, M. and Mattaj, I. W. (1998). Identification of a nuclear export receptor for tRNA. Curr. Biol. 12, 305-314.
7. Azuma, Y. and Dasso, M. (2000). The role of Ran in nuclear function. Curr. Opin. Cell Biol. 12, 302-307.
8. Balakin, A., Smith, L. and Fournier, M. (1996). The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 86, 823-834.
9. Becker, J., Melchior, F., Gerke, V., Bischoff, F. R., Ponstigl, H. and Wittinghoffer, A. (1995). RNA1 encodes a GTPase-activating protein specific for Gsp1p, the Ran/TC4 homologue of Saccharomyces cerevisiae. J. Biol. Chem. 270, 11860-11865.
10. Bischoff, F. R. and Ponstingl, H. (1991). Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354, 80-82.
11. Bischoff, F. R., Klebe, C., Kretschmer, J., Wittinghofer, A. and Ponstingl, H. (1994). RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc. Natl. Acad. Sci. USA 91, 2587-2591.
12. Bringmann, P, Rinke, J., Appel, B., Reuter, R. and Luhrmann, R. (1983). Purification of snRNPs U1, U2, U4, U5 and U6 with 2,2,7-trimethylguanosine-specific antibody and definition of their constituent proteins reacting with anti-Sm and anti-(U1)RNP antisera. EMBO J. 2, 1129-1135.
13. Carey, K. L., Richards, S. A., Lounsbury, K. M. and Macara, I. G. (1996). Evidence using a green fluorescent protein-glucocorticoid receptor chimera that the RAN/TC4 GTPase mediates an essential function independent of nuclear protein import. J. Cell Biol. 133, 985-996.
14. Carmo-Fonseca, M., Custodio, N. and Calado, A. (1999). Intranuclear trafficking of messenger RNA. Crit. Rev. Eukaryot. Gene Expr. 9, 213-219.
15. Chavrier, P. and Goud, B. (1999). The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11, 466-475.
16. Cheng, Y., Dahlberg, J. E. and Lund, E. (1995). Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. Science 267, 1807-1810.
17. Clarke, P. R. and Zhang, C. (2001). Ran GTPase: a master regulator of nuclear structure and function during the eukaryotic cell division cycle? Trends Cell Biol. 11, 366-371.
18. Corbett, A. H., Koepp, D. M., Lee, M. S., Schlenstedt, G., Hopper, A. K. and Silver, P. A. (1995a). Rna1p, a Ran/TC4 GTPase activating protein is required for nuclear import. J. Cell Biol. 130, 1017-1026.
19. Corbett, A. H., Koepp, D. M., Schlenstedt, G., Lee, M. S., Hopper, A. K. and Silver, P. A. (1995b). Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J. Cell Biol. 130, 1017-1026.
20. Corbett, A. H. and Silver, P. A. (1997). Nucleocytoplasmic transport of macromolecules. Microbiol. Mol. Biol. Rev. 61, 193-211.
21. Dahlberg, J. E. and Lund, E. (1998). Functions of the GTPase Ran in RNA export from the nucleus. Curr. Opin. Cell Biol. 10, 400-408.
22. Damelin, M., Silver, P. A. and Corbett, A. H. (2002). Nuclear protein transport. Meth. Enzmol. 351, 587-607.
23. Dasso, M. (1993). RCC1 in the cell cycle: The regulator of chromosome condensation takes on new roles. Trends Biol. Sci. 13, 96-101.
24. Dasso, M. (2001). Running on Ran: nuclear transport and the mitotic spindle. Cell 104, 321-324.
25. Filipowicz, W., Pelczar, P., Pogacic, V. and Dragon, F. (1999). Structure and biogenesis of small nucleolar RNAs acting as guides for ribosomal RNA modification. Acta Biochim Pol 46, 377-389.
26. Fleig, U., Salus, S. S., Karig, I. and Sazer, S. (2000). The fission yeast ran GTPase is required for microtubule integrity. J. Cell Biol. 151, 1101-1112.
27. Ganot, P., Bortolin, M. L. and Kiss, T. (1997). Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89, 799-809.
28. Görlich, D. and Kutay, U. (1999). Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 15, 607-660.
29. Gruss, O. J., Carazo-Salus, R. E., Schatz, C. A., Guarguaglini, G., Kast, J., Wilm, M., le Bot, N., Vernos, I., Karsenti, E. and Mattaj, I. W. (2001). Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104, 83-93.
30. Henriquez, R., Blobel, G. and Aris, J. P. (1990). Isolation and sequencing of NOP1. A yeast gene encoding a nucleolar protein homologous to a human autoimmune antigen. J. Biol. Chem. 265, 2209-2215.
31. Hetzer, M., Bilbao-Cortes, D., Walther, T. C., Gruss, O. J. and Mattaj, I. W. (2000). GTP hydrolysis by Ran is required for nuclear envelope assembly. Mol. Cell 5, 1013-1024.
32. Hopper, A. K., Traglia, H. M. and Dunst, R. W. (1990). The yeast RNA1 gene product necessary for RNA processing is located in the cytosol and apparently excluded from the nucleus. J. Cell Biol. 111, 309-321.
33. Huang, S., Mayeda, A., Krainer, A. R. and Spector, D. L. (1997). RCC1 and nuclear organization. Mol. Biol. Cell 8, 1143-1157.
34. Hughes, M., Zhang, C., Avis, J. M., Hutchison, C. J. and Clarke, P. R. (1998). The role of the ran GTPase in nuclear assembly and DNA replication: characterisation of the effects of Ran mutants. J. Cell Sci. 111, 3017-3026.
35. Izaurralde, E. and Adam, S. (1998). Transport of macromolecules between the nucleus and the cytoplasm. RNA 4, 351-364.
36. Izaurralde, E., Lewis, J., Gamberi, C., Jarmalowski, A., McGuigan, C. and Mattaj, I. W. (1995). A cap-binding protein complex mediating U snRNA export. Nature 376, 709-712.
37. Izaurralde, E., Kutay, U., vonKobbe, C., Mattaj, I. W. and Görlich, D. (1997). The assymetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J. 16, 6535-6547.
38. Kadowaki, T., Hitomi, M., Chen, S. and Tartakoff, A. M. (1994). Nuclear mRNA accumulation causes nucleolar fragmentation in yeast mtr2 mutant. Mol. Biol. Cell 5, 1253-1263.
39. Kahana, J. A. and Cleveland, D. W. (1999). Beyond nuclear transport. Ran-GTP as a determinant of spindle assembly. J. Cell Biol. 146, 1205-1210.
40. Kahana, J. A. and Cleveland, D. W. (2001). Cell cycle. Some importin news about spindle assembly. Science 291, 1718-1719.
41. Kuersten, S., Ohno, M. and Mattaj, I. W. (2001). Nucleocytoplasmic transport: Ran, beta and beyond. Trends Cell Biol. 11, 497-503.
42. Kutay, U., Lipowsky, G., Izaurralde, E., Bischoff, F. R., Schwarzmaier, P., Hartmann, E. and Görlich, D. (1998). Identification of a tRNA-specific nuclear export receptor. Mol. Cell 1, 359-369.
43. Lange, T. S., Borovjagin, A., Maxwell, E. S. and Gerbi, S. A. (1998). Conserved boxes C and D are essential nucleolar localization elements of U14 and U8 snoRNAs. EMBO J. 17, 3176-3187.
44. Lange, T. S., Ezrokhi, M., Amaldi, F. and Gerbi, S. A. (1999). Box H and box ACA are nucleolar localization elements of U17 small nucleolar RNA. Mol. Biol. Cell 10, 3877-3890.
45. Lounsbury, K. M., Richards, S. A., Carey, K. L. and Macara, I. G. (1996). Mutations within the Ran/TC4 GTPase: effects on regulatory factor interactions and subcellular localization. J. Biol. Chem. 271, 32834-32841.
46. Matsumoto, T. and Beach, R. (1991). Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell 66, 347-360.
47. Mattaj, I. W. (1986). Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell 46, 905-911.
48. Mattaj, I. W. and Englmeier, L. (1998). Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67, 265-306.
49. Michienzi, A., Cagnon, L., Bahner, I. and Rossi, J. J. (2000). Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA. Proc. Natl. Acad. Sci. USA 97, 8955-8960.
50. Nachury, M. V., Maresca, T. J., Salmon, W. C., Waterman-Storer, C. M., Heald, R. and Weis, K. (2001). Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104, 95-106.
51. Nakielny, S., Fischer, U., Michael, W. M. and Dreyfuss, G. (1997). RNA transport. Annu. Rev. Neurosci. 20, 269-301.
52. Narayanan, A., Lukowiak, A., Jady, B. E., Dragon, F., Kiss, T., Terns, R. M. and Terns, M. P. (1999a). Nucleolar localization signals of box H/ACA small nucleolar RNAs. EMBO J. 18, 5120-5130.
53. Narayanan, A., Speckmann, W., Terns, R. and Terns, M. (1999b). Role of the box C/D motif in the localization of small nucleolar RNAs to nucleoli and coiled bodies. Mol. Biol. Cell 10, 2131-2147.
54. Nemergut, M. E., Mizzen, C. A., Stukenberg, T., Allis, C. D. and Macara, I. G. (2001). Chromatin docking and exchange activity enhancement of rcc1 by histones h2a and h2b. Science 292, 1540-1543.
55. Nishijima, H., Seki, T., Nishitani, H. and Nishimoto, T. (2000). Premature chromatin condensation caused by loss of RCC1. Prog. Cell Cycle Res. 4, 145-156.
56. - mutant od BHK cells. Cell 15, 475-483.
57. Nonet, M., Scale, C., Sexton, J. and Young, R. (1987). Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol. Cell Biol. 7, 1602-1611.
58. Ohtsubo, M., Kai, R., Furuno, N., Sekiguchi, T., Havashida, H., Kuma, K., Miyata, T., Fukushige, S., Murotu, T., Matsubara, K. et al. (1987). Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev. 1, 585-593.
59. Palacios, I., Weis, K., Klebe, C., Mattaj, I. W. and Dingwall, C. (1996). RAN/TC4 mutants identify a common requirement for snRNP and protein import into the nucleus. J. Cell Biol. 133, 485-494.
60. Quimby, B. B., Lamtina, T., L'Hernault, S. and Corbett, A. H. (2000a). The Mechanism of Ran import into the nucleus by NTF2. J. Biol. Chem. 275, 28575-28582.
61. Quimby, B. B., Wilson, C. A. and Corbett, A. H. (2000b). The interaction between Ran and NTF2 is required for cell cycle progression. Mol. Biol. Cell 11, 2617-2629.
62. Rexach, M. and Blobel, G. (1995). Protein import into the nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692.
63. Ruhl, D. D., Pusateri, M. E. and Eliceiri, G. L. (2000). Multiple conserved segments of E1 small nucleolar RNA are involved in the formation of a ribonucleoprotein particle in frog oocytes. Biochem. J. 348, 517-524.
64. Saavedra, C., Tung, K.-S., Amberg, D. C., Hopper, A. K. and Cole, C. N. (1996). Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev. 10, 1608-1620.
65. Samarsky, D. A., Fournier, M. J., Singer, R. H. and Bertrand, E. (1998). The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization. EMBO J. 17, 3747-3757.
66. Sazer, S. and Nurse, P. (1994). A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J. 13, 606-615.
67. Speckmann, W., Narayanan, A., Terns, R. and Terns, M. P. (1999). Nuclear retention elements of U3 small nucleolar RNA. Mol. Cell. Biol. 19, 8412-8421.
68. Takai, Y., Sasaki, T. and Matozaki, T. (2001). Small GTP-binding proteins. Physiol. Rev. 81, 153-208.
69. Terns, M. P. and Terns, R. M. (2002). Small nucleolar RNAs: versatile transacting molecules of ancient evolutionary origin. Gene Expr. 10, 17-39.
70. Terns, M. P., Grimm, C., Lund, E. and Dahlberg, J. E. (1995). A common maturation pathway for small nucleolar RNAs. EMBO J. 14, 4860-4871.
71. Tollervey, D. and Kiss, T. (1997). Function and synthesis of small nucleolar RNAs. Curr. Opin. Cell Biol. 9, 337-342.
72. Verheggen, C., Mouaikel, J., Thiry, M., Blanchard, J. M., Tollervey, D., Bordonne, R., Lafontaine, L. J. and Bertrand, E. (2001). Box C/D small nucleolar RNA trafficking involves small nucleolar RNP proteins, nucleolar factors, and a novel nuclear domain. EMBO J. 20, 5480-5490.
73. Weinstein, L. B. and Steitz, J. A. (1999). Guided tours: from precursor snoRNA to functional snoRNP. Curr. Opin. Cell Biol. 11, 378-384.
74. Will, C. L. and Luhrmann, R. (2001). Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13, 290-301.
75. Wong, D. H., Corbett, A. H., Kent, H. M., Stewart, M. and Silver, P. A. (1997). Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Molec. Cell. Biol. 17, 3755-3767.
76. Yang, H., Moss, M. L., Lund, E. and Dahlberg, J. E. (1992). Nuclear processing of the 3′-terminal nucleotides of pre-U1 RNA in Xenopus laevis oocytes. Mol. Cell. Biol. 12, 1553-1560.
77. Zhang, C. and Clarke, P. R. (2001). Roles of Ran-GTP and Ran-GDP in precursor vesicle recruitment and fusion during nuclear envelope assembly in a human cell-free system. Curr. Biol. 11, 208-212.