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

Abstract

NIN1 is an essential gene for growth of the yeast_Saccharomyces cerevisiae_ and was recently found to encode a component of the regulatory subunit of the 26S proteasome. The_nin1-1_ 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 of_nin1-1, SUN2_ (SUppressor of Nin1-1), was found to encode a protein of 523 amino acids whose sequence is similar to those of_Drosophila 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 the_Drosophila_ diphenol oxidase A2 gene (Dox-A2) was obtained from a lambda phage cDNA library using the polymerase chain reaction technique. The_Dox-A2_ ORF driven by the_TDH3_ promoter complemented the phenotype of a strain deleted for_sun2_. This_Dox-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 of_nin1-1_ cells kept at a restrictive temperature. These results suggest that_SUN2_ is a functional counterpart of_Dox-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) The_Saccharomyces 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 the_SMP3_ gene product involved in plasmid maintenance in_Saccharomyces 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) Yeast_Saccharomyces 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 yeast_Saccharomyces_. 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 the_NINI_ gene product of_Saccharomyces 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 of_Saccharomyces 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 of_FAR1_ 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 of_Saccharomyces 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 in_Drosophila_. 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 in_Drosophila_. I. Identification in the biochemical defect in_Dox-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 in_S. 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 inhibitor_N_-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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Author notes

1. M. Kawamura
   Present address: First Department of Internal Medicine, Faculty of Medicine, University of Tokyo, Hongo, 113, Tokyo
2. K. Kominami
   Present address: ICRF, Laboratory of Cell Regulation, WC2A 3PX, London, UK

Authors and Affiliations

1. Laboratory of Genetics, Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, 113, Tokyo, Japan
   M. Kawamura, K. Kominami, J. Takeuchi & A. Toh-e

Authors

1. M. Kawamura
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2. K. Kominami
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3. J. Takeuchi
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4. A. Toh-e
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Communicated by C. P. Hollenberg

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Kawamura, M., Kominami, K., Takeuchi, J. et al. A multicopy suppressor of_nin1-1_ of the yeast_Saccharomyces cerevisiae_ is a counterpart of the_Drosophila melanogaster_ diphenol oxidase A2 gene,Dox-A2.Molec. Gen. Genet. 251, 146–152 (1996). https://doi.org/10.1007/BF02172912

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• Received: 04 October 1995
• Accepted: 29 November 1995
• Issue Date: May 1996
• DOI: https://doi.org/10.1007/BF02172912

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