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A multicopy suppressor ofnin1-1 of the yeastSaccharomyces cerevisiae is a counterpart of theDrosophila melanogaster diphenol oxidase A2 gene,Dox-A2

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Abstract

NIN1 is an essential gene for growth of the yeastSaccharomyces cerevisiae and was recently found to encode a component of the regulatory subunit of the 26S proteasome. Thenin1-1 mutant is temperature sensitive and its main defect is in G1/S progression and G2/M progression at non-permissive temperatures. One of the two multicopy suppressors ofnin1-1, SUN2 (SUppressor of Nin1-1), was found to encode a protein of 523 amino acids whose sequence is similar to those ofDrosophila melanogaster diphenol oxidase A2 and the mouse mast-cell Tum transplantation antigen, P91A. The C-terminal half of Sun2p was found to be functional as Sun2p at 25° C, 30° C, and 34° C but not at 37° C. The open reading frame (ORF) of theDrosophila diphenol oxidase A2 gene (Dox-A2) was obtained from a lambda phage cDNA library using the polymerase chain reaction technique. TheDox-A2 ORF driven by theTDH3 promoter complemented the phenotype of a strain deleted forsun2. ThisDox-A2-dependent strain was temperature sensitive and accumulated dumb-bell-shaped cells, with an undivided nucleus at the isthmus, after temperature upshift. This morphology is similar to that ofnin1-1 cells kept at a restrictive temperature. These results suggest thatSUN2 is a functional counterpart ofDox-A2 and that these genes play a pivotal role in the cell cycle in each organism.

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References

  • Fujimura K, Tanaka K, Nakano A, Toh-e A (1994) TheSaccharomyces cerevisiae MS14 gene encodes the yeast counterpart of component A of Rab geranylgeranyltransferase. J Biol Chem 269:9205–9212

    PubMed  Google Scholar 

  • Ghislain M, Udvardy A, Mann C (1993)S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase. Nature 366:358–362

    PubMed  Google Scholar 

  • Glotzer M, Murray A, Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349:132–138

    PubMed  Google Scholar 

  • Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359

    PubMed  Google Scholar 

  • Holland JP, Holland MJ (1980) Structural comparison of two non-tandemly repeated yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 255:2596–2605

    PubMed  Google Scholar 

  • Irie K, Araki H, Oshima Y (1991) A new protein kinase,SSP31, modulating theSMP3 gene product involved in plasmid maintenance inSaccharomyces cerevisiae. Gene 108:139–144

    PubMed  Google Scholar 

  • Irniger S, Piatti S, Michaelis C, Nasmyth K (1995) Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81:269–277

    PubMed  Google Scholar 

  • Jones JS, Prakash L (1990) YeastSaccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast 6:363–366

    PubMed  Google Scholar 

  • Kilmartin JV, Adams AEM (1984) Structural rearrangement of tubulin and actin during the cell cycle of the yeastSaccharomyces. J Cell Biol 98:922–933

    PubMed  Google Scholar 

  • King RW, Peters J-M, Tugendreich ST, Rolfe M, Hieter P, Kirschner MW (1995) A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279–288

    PubMed  Google Scholar 

  • Kominami K, Toh-e A (1994) Characterization of the function of theNINI gene product ofSaccharomyces cerevisiae. Exp Cell Res 211:203–211

    PubMed  Google Scholar 

  • Kominami K, DeMartino GN, Moomaw CR, Slaughter CA, Shimbara N, Fujimuro M, Yokosawa H, Hisamatsu H, Tanahashi N, Shimizu Y, Tanaka K, Toh-e A (1995) Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase ofSaccharomyces cerevisiae. EMBO J 14:3105–3115

    PubMed  Google Scholar 

  • Lamb JR, Michaud WA, Sikorski RS, Hieter P (1994) Cdc16p, Cdc23p, and Cdc27p form a complex essential for mitosis. EMBO J 13:4321–4328

    PubMed  Google Scholar 

  • Lurquin C, Van Pel A, Mariame B, De Plean E, Szikora JP, Janssens C, Reddehase MJ, Lejeune J, Thierry B (1989) Structure of the gene of Tum transplantation antigen P91A: the mutated exon encodes a peptide recognized with Ld by cytolytic T cells. Cell 58:293–303

    PubMed  Google Scholar 

  • McKinney JD, Chang F, Heitz N, Cross FR (1993) Negative regulation ofFAR1 at the start of the yeast cell cycle. Genes Dev 7:833–843

    PubMed  Google Scholar 

  • Mitchell HK, Weber UM (1965)Drosophila phenol oxidases. Science 148:964–965

    PubMed  Google Scholar 

  • Murray AW (1995) Cyclin ubiquitination: the destructive end of mitosis. Cell 81:149–152

    PubMed  Google Scholar 

  • Nisogi H, Kominami K, Tanaka K, Toh-e A (1992) A new essential gene ofSaccharomyces cerevisiae, a defect in it may result in instability of nucleus. Exp Cell Res 200:48–57

    PubMed  Google Scholar 

  • Ohnishi E, Dohke K, Ashida M (1970) Activation of prephenoloxidase. II. Activation by alpha-chymotrypsin. Arch Biochem Biophys 139:143–148

    PubMed  Google Scholar 

  • Pagano M, Tam SW, Theodoras AM, Beer-Romero P, Del Sal G, Chan V, Yew PR, Draetta GF, Rolfe M (1995) Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin dependent kinase inhibitor p27. Science 269:682–685

    PubMed  Google Scholar 

  • Pentz ES, Wright TRF (1986) A diphenol oxidase gene is part of a cluster of genes involved in catecholamine metabolism and sclerotization inDrosophila. II. Molecular localization of the Dox-A2 coding region. Genetics 112:843–859

    PubMed  Google Scholar 

  • Pentz ES, Wright TRF (1991)Drosophila melanogaster diphenol oxidase A2: gene structure and homology with the mouse mast-cell tum transplantation antigen, P91A, Gene 103:239–242

    PubMed  Google Scholar 

  • Pentz ES, Black BC, Wright TRF (1986) A diphenol oxidase gene is part of a cluster of genes involved in catecholamine metabolism and sclerotization inDrosophila. I. Identification in the biochemical defect inDox-A2 [I(2)37Bf] mutants. Genetics 112:823–841

    PubMed  Google Scholar 

  • Peters J-M (1994) Proteasomes: protein degradation machines of the cell. Trends Biochem Sci 19:377–382

    PubMed  Google Scholar 

  • Rose MD, Winston F, Hieter P (1990) Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with thermostable DNA polymerase. Science 239:487–491

    PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    PubMed  Google Scholar 

  • Schwob E, Boehm T, Mendenhall MD, Nasmyth K (1994) The B-type cyclin kinase inhibitor p40SICI controls the G1 to S transition inS. cerevisiae. Cell 79:233–244

    PubMed  Google Scholar 

  • Sherwood SW, Kung AL, Roitelman J, Simoni RD, Schimke RT (1993) In vivo inhibition of cyclin B degradation and induction of cell-cycle arrest in mammalian cells by the neutral cysteine protease inhibitorN-acetylleucylleucylnorleucinal. Proc Natl Acad Sci USA 90:3353–3357

    PubMed  Google Scholar 

  • Verlant V, Amar-Costesec A, Gdelaine D, Turu C, Van Pel A, De Plaen E, Dautry-Varsat A, Beaufay H (1993) The Tum antigens P91A and P198 derive from proteins located in the cytosolic compartment of cells. Eur J Immunol 23:1727–1730

    PubMed  Google Scholar 

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Communicated by C. P. Hollenberg

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Kawamura, M., Kominami, K., Takeuchi, J. et al. A multicopy suppressor ofnin1-1 of the yeastSaccharomyces cerevisiae is a counterpart of theDrosophila melanogaster diphenol oxidase A2 gene,Dox-A2 . Molec. Gen. Genet. 251, 146–152 (1996). https://doi.org/10.1007/BF02172912

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  • DOI: https://doi.org/10.1007/BF02172912

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