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. 1997 Sep 1;25(17):3433–3439. doi: 10.1093/nar/25.17.3433

Sce3, a suppressor of the Schizosaccharomyces pombe septation mutant cdc11, encodes a putative RNA-binding protein.

S Schmidt 1, K Hofmann 1, V Simanis 1
PMCID: PMC146901  PMID: 9254700

Abstract

In the fission yeast Schizosaccharomyces pombe, the cdc11 gene is required for the initiation of septum formation at the end of mitosis. The sce3 gene was cloned as a multi-copy suppressor of the heat-sensitive mutant cdc11-136. When over-expressed, it rescues all mutants of cdc11 and also a heat-sensitive allele of cdc14, but not the cdc14 null mutant. Deletion shows that sce3 is not essential for cell proliferation. It encodes a putative RNA-binding protein which shows homology to human eIF4B. Immunolocalisation indicates that Sce3p is located predominantly in the cytoplasm. Elevated expression of sce3 increases the steady-state level of cdc14 mRNA. Possible mechanisms of its action are discussed.

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Selected References

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

  1. Altmann M., Müller P. P., Wittmer B., Ruchti F., Lanker S., Trachsel H. A Saccharomyces cerevisiae homologue of mammalian translation initiation factor 4B contributes to RNA helicase activity. EMBO J. 1993 Oct;12(10):3997–4003. doi: 10.1002/j.1460-2075.1993.tb06077.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balasubramanian M. K., Feoktistova A., McCollum D., Gould K. L. Fission yeast Sop2p: a novel and evolutionarily conserved protein that interacts with Arp3p and modulates profilin function. EMBO J. 1996 Dec 2;15(23):6426–6437. [PMC free article] [PubMed] [Google Scholar]
  3. Balasubramanian M. K., Helfman D. M., Hemmingsen S. M. A new tropomyosin essential for cytokinesis in the fission yeast S. pombe. Nature. 1992 Nov 5;360(6399):84–87. doi: 10.1038/360084a0. [DOI] [PubMed] [Google Scholar]
  4. Balasubramanian M. K., Hirani B. R., Burke J. D., Gould K. L. The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis. J Cell Biol. 1994 Jun;125(6):1289–1301. doi: 10.1083/jcb.125.6.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barbet N., Muriel W. J., Carr A. M. Versatile shuttle vectors and genomic libraries for use with Schizosaccharomyces pombe. Gene. 1992 May 1;114(1):59–66. doi: 10.1016/0378-1119(92)90707-v. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Blau H. M. Differentiation requires continuous active control. Annu Rev Biochem. 1992;61:1213–1230. doi: 10.1146/annurev.bi.61.070192.010025. [DOI] [PubMed] [Google Scholar]
  8. Burd C. G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994 Jul 29;265(5172):615–621. doi: 10.1126/science.8036511. [DOI] [PubMed] [Google Scholar]
  9. Chang F., Drubin D., Nurse P. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J Cell Biol. 1997 Apr 7;137(1):169–182. doi: 10.1083/jcb.137.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chang F., Woollard A., Nurse P. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J Cell Sci. 1996 Jan;109(Pt 1):131–142. doi: 10.1242/jcs.109.1.131. [DOI] [PubMed] [Google Scholar]
  11. Chuang R. Y., Weaver P. L., Liu Z., Chang T. H. Requirement of the DEAD-Box protein ded1p for messenger RNA translation. Science. 1997 Mar 7;275(5305):1468–1471. doi: 10.1126/science.275.5305.1468. [DOI] [PubMed] [Google Scholar]
  12. Fankhauser C., Marks J., Reymond A., Simanis V. The S. pombe cdc16 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis? EMBO J. 1993 Jul;12(7):2697–2704. doi: 10.1002/j.1460-2075.1993.tb05931.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fankhauser C., Reymond A., Cerutti L., Utzig S., Hofmann K., Simanis V. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell. 1995 Aug 11;82(3):435–444. doi: 10.1016/0092-8674(95)90432-8. [DOI] [PubMed] [Google Scholar]
  14. Fankhauser C., Simanis V. The Schizosaccharomyces pombe cdc14 gene is required for septum formation and can also inhibit nuclear division. Mol Biol Cell. 1993 May;4(5):531–539. doi: 10.1091/mbc.4.5.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fankhauser C., Simanis V. The cdc7 protein kinase is a dosage dependent regulator of septum formation in fission yeast. EMBO J. 1994 Jul 1;13(13):3011–3019. doi: 10.1002/j.1460-2075.1994.tb06600.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hagan I. M., Hyams J. S. The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1988 Mar;89(Pt 3):343–357. doi: 10.1242/jcs.89.3.343. [DOI] [PubMed] [Google Scholar]
  17. Hoheisel J. D., Maier E., Mott R., McCarthy L., Grigoriev A. V., Schalkwyk L. C., Nizetic D., Francis F., Lehrach H. High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast S. pombe. Cell. 1993 Apr 9;73(1):109–120. doi: 10.1016/0092-8674(93)90164-l. [DOI] [PubMed] [Google Scholar]
  18. Jacobson A., Peltz S. W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu Rev Biochem. 1996;65:693–739. doi: 10.1146/annurev.bi.65.070196.003401. [DOI] [PubMed] [Google Scholar]
  19. Jamieson D. J., Rahe B., Pringle J., Beggs J. D. A suppressor of a yeast splicing mutation (prp8-1) encodes a putative ATP-dependent RNA helicase. Nature. 1991 Feb 21;349(6311):715–717. doi: 10.1038/349715a0. [DOI] [PubMed] [Google Scholar]
  20. Jessen T. H., Oubridge C., Teo C. H., Pritchard C., Nagai K. Identification of molecular contacts between the U1 A small nuclear ribonucleoprotein and U1 RNA. EMBO J. 1991 Nov;10(11):3447–3456. doi: 10.1002/j.1460-2075.1991.tb04909.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kanaoka Y., Nojima H. SCR: novel human suppressors of cdc2/cdc13 mutants of Schizosaccharomyces pombe harbour motifs for RNA binding proteins. Nucleic Acids Res. 1994 Jul 11;22(13):2687–2693. doi: 10.1093/nar/22.13.2687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kelly T. J., Martin G. S., Forsburg S. L., Stephen R. J., Russo A., Nurse P. The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell. 1993 Jul 30;74(2):371–382. doi: 10.1016/0092-8674(93)90427-r. [DOI] [PubMed] [Google Scholar]
  23. Marks J., Fankhauser C., Simanis V. Genetic interactions in the control of septation in Schizosaccharomyces pombe. J Cell Sci. 1992 Apr;101(Pt 4):801–808. doi: 10.1242/jcs.101.4.801. [DOI] [PubMed] [Google Scholar]
  24. Maundrell K. nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J Biol Chem. 1990 Jul 5;265(19):10857–10864. [PubMed] [Google Scholar]
  25. McCollum D., Balasubramanian M. K., Pelcher L. E., Hemmingsen S. M., Gould K. L. Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis. J Cell Biol. 1995 Aug;130(3):651–660. doi: 10.1083/jcb.130.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McCollum D., Feoktistova A., Morphew M., Balasubramanian M., Gould K. L. The Schizosaccharomyces pombe actin-related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. EMBO J. 1996 Dec 2;15(23):6438–6446. [PMC free article] [PubMed] [Google Scholar]
  27. Minet M., Nurse P., Thuriaux P., Mitchison J. M. Uncontrolled septation in a cell division cycle mutant of the fission yeast Schizosaccharomyces pombe. J Bacteriol. 1979 Jan;137(1):440–446. doi: 10.1128/jb.137.1.440-446.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Moore A. L., Wang T. S. Down-regulation of genes encoding DNA replication proteins during cell cycle exit. Cell Growth Differ. 1994 May;5(5):485–494. [PubMed] [Google Scholar]
  29. 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]
  30. Méthot N., Pause A., Hershey J. W., Sonenberg N. The translation initiation factor eIF-4B contains an RNA-binding region that is distinct and independent from its ribonucleoprotein consensus sequence. Mol Cell Biol. 1994 Apr;14(4):2307–2316. doi: 10.1128/mcb.14.4.2307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nagai K., Oubridge C., Ito N., Avis J., Evans P. The RNP domain: a sequence-specific RNA-binding domain involved in processing and transport of RNA. Trends Biochem Sci. 1995 Jun;20(6):235–240. doi: 10.1016/s0968-0004(00)89024-6. [DOI] [PubMed] [Google Scholar]
  32. Nagai K. RNA-protein complexes. Curr Opin Struct Biol. 1996 Feb;6(1):53–61. doi: 10.1016/s0959-440x(96)80095-9. [DOI] [PubMed] [Google Scholar]
  33. Naranda T., Strong W. B., Menaya J., Fabbri B. J., Hershey J. W. Two structural domains of initiation factor eIF-4B are involved in binding to RNA. J Biol Chem. 1994 May 20;269(20):14465–14472. [PubMed] [Google Scholar]
  34. Nurse P., Thuriaux P., Nasmyth K. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet. 1976 Jul 23;146(2):167–178. doi: 10.1007/BF00268085. [DOI] [PubMed] [Google Scholar]
  35. Ohkura H., Hagan I. M., Glover D. M. The conserved Schizosaccharomyces pombe kinase plo1, required to form a bipolar spindle, the actin ring, and septum, can drive septum formation in G1 and G2 cells. Genes Dev. 1995 May 1;9(9):1059–1073. doi: 10.1101/gad.9.9.1059. [DOI] [PubMed] [Google Scholar]
  36. Okazaki K., Okazaki N., Kume K., Jinno S., Tanaka K., Okayama H. High-frequency transformation method and library transducing vectors for cloning mammalian cDNAs by trans-complementation of Schizosaccharomyces pombe. Nucleic Acids Res. 1990 Nov 25;18(22):6485–6489. doi: 10.1093/nar/18.22.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Oubridge C., Ito N., Evans P. R., Teo C. H., Nagai K. Crystal structure at 1.92 A resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature. 1994 Dec 1;372(6505):432–438. doi: 10.1038/372432a0. [DOI] [PubMed] [Google Scholar]
  38. Ptushkina M., Fierro-Monti I., van den Heuvel J., Vasilescu S., Birkenhäger R., Mita K., McCarthy J. E. Schizosaccharomyces pombe has a novel eukaryotic initiation factor 4F complex containing a cap-binding protein with the human eIF4E C-terminal motif KSGST. J Biol Chem. 1996 Dec 20;271(51):32818–32824. doi: 10.1074/jbc.271.51.32818. [DOI] [PubMed] [Google Scholar]
  39. Query C. C., Bentley R. C., Keene J. D. A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell. 1989 Apr 7;57(1):89–101. doi: 10.1016/0092-8674(89)90175-x. [DOI] [PubMed] [Google Scholar]
  40. Ross J. Control of messenger RNA stability in higher eukaryotes. Trends Genet. 1996 May;12(5):171–175. doi: 10.1016/0168-9525(96)10016-0. [DOI] [PubMed] [Google Scholar]
  41. Schmidt S., Sohrmann M., Hofmann K., Woollard A., Simanis V. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe. Genes Dev. 1997 Jun 15;11(12):1519–1534. doi: 10.1101/gad.11.12.1519. [DOI] [PubMed] [Google Scholar]
  42. Simanis V. The control of septum formation and cytokinesis in fission yeast. Semin Cell Biol. 1995 Apr;6(2):79–87. doi: 10.1016/1043-4682(95)90004-7. [DOI] [PubMed] [Google Scholar]
  43. Sohrmann M., Fankhauser C., Brodbeck C., Simanis V. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev. 1996 Nov 1;10(21):2707–2719. doi: 10.1101/gad.10.21.2707. [DOI] [PubMed] [Google Scholar]
  44. Song K., Mach K. E., Chen C. Y., Reynolds T., Albright C. F. A novel suppressor of ras1 in fission yeast, byr4, is a dosage-dependent inhibitor of cytokinesis. J Cell Biol. 1996 Jun;133(6):1307–1319. doi: 10.1083/jcb.133.6.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tay D. L., Bhathal P. S., Fox R. M. Quantitation of G0 and G1 phase cells in primary carcinomas. Antibody to M1 subunit of ribonucleotide reductase shows G1 phase restriction point block. J Clin Invest. 1991 Feb;87(2):519–527. doi: 10.1172/JCI115026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Thuillier V., Stettler S., Sentenac A., Thuriaux P., Werner M. A mutation in the C31 subunit of Saccharomyces cerevisiae RNA polymerase III affects transcription initiation. EMBO J. 1995 Jan 16;14(2):351–359. doi: 10.1002/j.1460-2075.1995.tb07009.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Woods A., Sherwin T., Sasse R., MacRae T. H., Baines A. J., Gull K. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J Cell Sci. 1989 Jul;93(Pt 3):491–500. doi: 10.1242/jcs.93.3.491. [DOI] [PubMed] [Google Scholar]

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