Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2001 Apr;157(4):1513–1522. doi: 10.1093/genetics/157.4.1513

Fission yeast Mog1p homologue, which interacts with the small GTPase Ran, is required for mitosis-to-interphase transition and poly(A)(+) RNA metabolism.

K Tatebayashi 1, T Tani 1, H Ikeda 1
PMCID: PMC1461609  PMID: 11290708

Abstract

We have cloned and characterized the Schizosaccharomyces pombe gene mog1(+), which encodes a protein with homology to the Saccharomyces cerevisiae Mog1p participating in the Ran-GTPase system. The S. pombe Mog1p is predominantly localized in the nucleus. In contrast to the S. cerevisiae MOG1 gene, the S. pombe mog1(+) gene is essential for cell viability. mog1(+) is required for the mitosis-to-interphase transition, as the mog1-1 mutant arrests at restrictive temperatures as septated, binucleated cells with highly condensed chromosomes and an aberrant nuclear envelope. FACS analysis showed that these cells do not undergo a subsequent round of DNA replication. Surprisingly, also unlike the Delta mog1 mutation in S. cerevisiae, the mog1-1 mutation causes nucleolar accumulation of poly(A)(+) RNA at the restrictive temperature in S. pombe, but the signals do not overlap with the fibrillarin-rich region of the nucleolus. Thus, we found that mog1(+) is required for the mitosis-to-interphase transition and a class of RNA metabolism. In our attempt to identify suppressors of mog1-1, we isolated the spi1(+) gene, which encodes the fission yeast homologue of Ran. We found that overexpression of Spi1p rescues the S. pombe Delta mog1 cells from death. On the basis of these results, we conclude that mog1(+) is involved in the Ran-GTPase system.

Full Text

The Full Text of this article is available as a PDF (431.0 KB).

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. Azad A. K., Tani T., Shiki N., Tsuneyoshi S., Urushiyama S., Ohshima Y. Isolation and molecular characterization of mRNA transport mutants in Schizosaccharomyces pombe. Mol Biol Cell. 1997 May;8(5):825–841. doi: 10.1091/mbc.8.5.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Basi G., Schmid E., Maundrell K. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene. 1993 Jan 15;123(1):131–136. doi: 10.1016/0378-1119(93)90552-e. [DOI] [PubMed] [Google Scholar]
  4. Becker J., Melchior F., Gerke V., Bischoff F. R., Ponstingl H., Wittinghofer A. RNA1 encodes a GTPase-activating protein specific for Gsp1p, the Ran/TC4 homologue of Saccharomyces cerevisiae. J Biol Chem. 1995 May 19;270(20):11860–11865. doi: 10.1074/jbc.270.20.11860. [DOI] [PubMed] [Google Scholar]
  5. Birkenbihl R. P., Subramani S. Cloning and characterization of rad21 an essential gene of Schizosaccharomyces pombe involved in DNA double-strand-break repair. Nucleic Acids Res. 1992 Dec 25;20(24):6605–6611. doi: 10.1093/nar/20.24.6605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Boguski M. S., McCormick F. Proteins regulating Ras and its relatives. Nature. 1993 Dec 16;366(6456):643–654. doi: 10.1038/366643a0. [DOI] [PubMed] [Google Scholar]
  8. Corbett A. H., Koepp D. M., Schlenstedt G., Lee M. S., Hopper A. K., Silver P. A. Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J Cell Biol. 1995 Sep;130(5):1017–1026. doi: 10.1083/jcb.130.5.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dasso M. The role of the Ran GTPase pathway in cell cycle control and interphase nuclear functions. Prog Cell Cycle Res. 1995;1:163–172. doi: 10.1007/978-1-4615-1809-9_13. [DOI] [PubMed] [Google Scholar]
  10. Demeter J., Morphew M., Sazer S. A mutation in the RCC1-related protein pim1 results in nuclear envelope fragmentation in fission yeast. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1436–1440. doi: 10.1073/pnas.92.5.1436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guacci V., Koshland D., Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell. 1997 Oct 3;91(1):47–57. doi: 10.1016/s0092-8674(01)80008-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Görlich D. Transport into and out of the cell nucleus. EMBO J. 1998 May 15;17(10):2721–2727. doi: 10.1093/emboj/17.10.2721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hartwell L. H. Macromolecule synthesis in temperature-sensitive mutants of yeast. J Bacteriol. 1967 May;93(5):1662–1670. doi: 10.1128/jb.93.5.1662-1670.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. He X., Hayashi N., Walcott N. G., Azuma Y., Patterson T. E., Bischoff F. R., Nishimoto T., Sazer S. The identification of cDNAs that affect the mitosis-to-interphase transition in Schizosaccharomyces pombe, including sbp1, which encodes a spi1p-GTP-binding protein. Genetics. 1998 Feb;148(2):645–656. doi: 10.1093/genetics/148.2.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Matynia A., Dimitrov K., Mueller U., He X., Sazer S. Perturbations in the spi1p GTPase cycle of Schizosaccharomyces pombe through its GTPase-activating protein and guanine nucleotide exchange factor components result in similar phenotypic consequences. Mol Cell Biol. 1996 Nov;16(11):6352–6362. doi: 10.1128/mcb.16.11.6352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997 Oct 3;91(1):35–45. doi: 10.1016/s0092-8674(01)80007-6. [DOI] [PubMed] [Google Scholar]
  20. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l. [DOI] [PubMed] [Google Scholar]
  21. Noguchi E., Hayashi N., Azuma Y., Seki T., Nakamura M., Nakashima N., Yanagida M., He X., Mueller U., Sazer S. Dis3, implicated in mitotic control, binds directly to Ran and enhances the GEF activity of RCC1. EMBO J. 1996 Oct 15;15(20):5595–5605. [PMC free article] [PubMed] [Google Scholar]
  22. Oki M., Nishimoto T. A protein required for nuclear-protein import, Mog1p, directly interacts with GTP-Gsp1p, the Saccharomyces cerevisiae ran homologue. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15388–15393. doi: 10.1073/pnas.95.26.15388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oki M., Noguchi E., Hayashi N., Nishimoto T. Nuclear protein import, but not mRNA export, is defective in all Saccharomyces cerevisiae mutants that produce temperature-sensitive forms of the Ran GTPase homologue Gsp1p. Mol Gen Genet. 1998 Apr;257(6):624–634. doi: 10.1007/s004380050690. [DOI] [PubMed] [Google Scholar]
  24. Ribbeck K., Lipowsky G., Kent H. M., Stewart M., Görlich D. NTF2 mediates nuclear import of Ran. EMBO J. 1998 Nov 16;17(22):6587–6598. doi: 10.1093/emboj/17.22.6587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  26. Sazer S., Nurse P. A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J. 1994 Feb 1;13(3):606–615. doi: 10.1002/j.1460-2075.1994.tb06298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sazer S. The search for the primary function of the Ran GTPase continues. Trends Cell Biol. 1996 Mar;6(3):81–85. doi: 10.1016/0962-8924(96)80992-5. [DOI] [PubMed] [Google Scholar]
  28. Shibuya T., Tsuneyoshi S., Azad A. K., Urushiyama S., Ohshima Y., Tani T. Characterization of the ptr6(+) gene in fission yeast: a possible involvement of a transcriptional coactivator TAF in nucleocytoplasmic transport of mRNA. Genetics. 1999 Jul;152(3):869–880. doi: 10.1093/genetics/152.3.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Steggerda S. M., Paschal B. M. The mammalian Mog1 protein is a guanine nucleotide release factor for Ran. J Biol Chem. 2000 Jul 28;275(30):23175–23180. doi: 10.1074/jbc.C000252200. [DOI] [PubMed] [Google Scholar]
  30. Stewart M., Baker R. P. 1.9 A resolution crystal structure of the Saccharomyces cerevisiae Ran-binding protein Mog1p. J Mol Biol. 2000 May 26;299(1):213–223. doi: 10.1006/jmbi.2000.3733. [DOI] [PubMed] [Google Scholar]
  31. Tani T., Derby R. J., Hiraoka Y., Spector D. L. Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol Biol Cell. 1996 Jan;7(1):173–192. doi: 10.1091/mbc.7.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tatebayashi K., Kato J., Ikeda H. Isolation of a Schizosaccharomyces pombe rad21ts mutant that is aberrant in chromosome segregation, microtubule function, DNA repair and sensitive to hydroxyurea: possible involvement of Rad21 in ubiquitin-mediated proteolysis. Genetics. 1998 Jan;148(1):49–57. doi: 10.1093/genetics/148.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Watanabe Y., Shinozaki-Yabana S., Chikashige Y., Hiraoka Y., Yamamoto M. Phosphorylation of RNA-binding protein controls cell cycle switch from mitotic to meiotic in fission yeast. Nature. 1997 Mar 13;386(6621):187–190. doi: 10.1038/386187a0. [DOI] [PubMed] [Google Scholar]
  34. van Hoof A., Lennertz P., Parker R. Yeast exosome mutants accumulate 3'-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol. 2000 Jan;20(2):441–452. doi: 10.1128/mcb.20.2.441-452.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES