Literature DB >> 11294895

The Schizosaccharomyces pombe spo20(+) gene encoding a homologue of Saccharomyces cerevisiae Sec14 plays an important role in forespore membrane formation.

Y Nakase1, T Nakamura, A Hirata, S M Routt, H B Skinner, V A Bankaitis, C Shimoda.   

Abstract

The Schizosaccharomyces pombe spo20-KC104 mutation was originally isolated in a screen for sporulation-deficient mutants, and the spo20-KC104 mutant exhibits temperature-sensitive growth. Herein, we report that S. pombe, spo20(+) is essential for fission yeast cell viability and is constitutively expressed throughout the life cycle. We also demonstrate that the spo20(+) gene product is structurally homologous to Saccharomyces cerevisiae Sec14, the major phosphatidylinositol transfer protein of budding yeast. This structural homology translates to a significant degree of functional relatedness because reciprocal complementation experiments demonstrate that each protein is able to fulfill the essential function of the other. Moreover, biochemical experiments show that, like Sec14, Spo20 is a phosphatidylinositol/phosphatidylcholine-transfer protein. That Spo20 is required for Golgi secretory function in vegetative cells is indicated by our demonstration that the spo20-KC104 mutant accumulates aberrant Golgi cisternae at restrictive temperatures. However, a second phenotype observed in Spo20-deficient fission yeast is arrest of cell division before completion of cell separation. Consistent with a direct role for Spo20 in controlling cell septation in vegetatively growing cells, localization experiments reveal that Spo20 preferentially localizes to the cell poles and to sites of septation of fission yeast cells. We also report that, when fission yeasts are challenged with nitrogen starvation, Spo20 translocates to the nucleus. This nuclear localization persists during conjugation and meiosis. On completion of meiosis, Spo20 translocates to forespore membranes, and it is the assembly of forespore membranes that is abnormal in spo20-KC104 cells. In such mutants, a considerable fraction of forming prespores fail to encapsulate the haploid nucleus. Our results indicate that Spo20 regulates the formation of specialized membrane structures in addition to its recognized role in regulating Golgi secretory function.

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Year:  2001        PMID: 11294895      PMCID: PMC32275          DOI: 10.1091/mbc.12.4.901

Source DB:  PubMed          Journal:  Mol Biol Cell        ISSN: 1059-1524            Impact factor:   4.138


  49 in total

Review 1.  Phosphatidylinositol transfer proteins: the long and winding road to physiological function.

Authors:  B G Kearns; J G Alb; V Bankaitis
Journal:  Trends Cell Biol       Date:  1998-07       Impact factor: 20.808

2.  Genes involved in meiosis and sporulation of a yeast.

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Journal:  Mol Gen Genet       Date:  1968

3.  Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.

Authors:  P S Thomas
Journal:  Proc Natl Acad Sci U S A       Date:  1980-09       Impact factor: 11.205

4.  General purpose tagging vectors for fission yeast.

Authors:  S L Forsburg; D A Sherman
Journal:  Gene       Date:  1997-06-03       Impact factor: 3.688

5.  Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe.

Authors:  C Kitayama; A Sugimoto; M Yamamoto
Journal:  J Cell Biol       Date:  1997-06-16       Impact factor: 10.539

6.  S. pombe sporulation-specific coiled-coil protein Spo15p is localized to the spindle pole body and essential for its modification.

Authors:  S Ikemoto; T Nakamura; M Kubo; C Shimoda
Journal:  J Cell Sci       Date:  2000-02       Impact factor: 5.285

7.  The Saccharomyces cerevisiae SEC14 gene encodes a cytosolic factor that is required for transport of secretory proteins from the yeast Golgi complex.

Authors:  V A Bankaitis; D E Malehorn; S D Emr; R Greene
Journal:  J Cell Biol       Date:  1989-04       Impact factor: 10.539

8.  Phospholipid transfer activity is relevant to but not sufficient for the essential function of the yeast SEC14 gene product.

Authors:  H B Skinner; J G Alb; E A Whitters; G M Helmkamp; V A Bankaitis
Journal:  EMBO J       Date:  1993-12       Impact factor: 11.598

9.  Ascospore development in the fission yeasts Schizosaccharomyces pombe and S. japonicus.

Authors:  K Tanaka; A Hirata
Journal:  J Cell Sci       Date:  1982-08       Impact factor: 5.285

10.  Mutations in the SAC1 gene suppress defects in yeast Golgi and yeast actin function.

Authors:  A E Cleves; P J Novick; V A Bankaitis
Journal:  J Cell Biol       Date:  1989-12       Impact factor: 10.539

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  36 in total

1.  Genetic ablation of phosphatidylinositol transfer protein function in murine embryonic stem cells.

Authors:  James G Alb; Scott E Phillips; Kathleen Rostand; Xiaoxia Cui; Jef Pinxteren; Laura Cotlin; Timothy Manning; Shuling Guo; John D York; Harald Sontheimer; James F Collawn; Vytas A Bankaitis
Journal:  Mol Biol Cell       Date:  2002-03       Impact factor: 4.138

2.  Role of the Rab GTP-binding protein Ypt3 in the fission yeast exocytic pathway and its connection to calcineurin function.

Authors:  Hong Cheng; Reiko Sugiura; Wenlian Wu; Masaaki Fujita; Yabin Lu; Susie O Sio; Rena Kawai; Kaoru Takegawa; Hisato Shuntoh; Takayoshi Kuno
Journal:  Mol Biol Cell       Date:  2002-08       Impact factor: 4.138

3.  Genetic evidence for phospholipid-mediated regulation of the Rab GDP-dissociation inhibitor in fission yeast.

Authors:  Yan Ma; Takayoshi Kuno; Ayako Kita; Toshiya Nabata; Satoshi Uno; Reiko Sugiura
Journal:  Genetics       Date:  2006-09-15       Impact factor: 4.562

4.  Reorganization of the growth pattern of Schizosaccharomyces pombe in invasive filament formation.

Authors:  James Dodgson; William Brown; Carlos A Rosa; John Armstrong
Journal:  Eukaryot Cell       Date:  2010-09-24

Review 5.  The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking.

Authors:  Carl J Mousley; Kimberly R Tyeryar; Patrick Vincent-Pope; Vytas A Bankaitis
Journal:  Biochim Biophys Acta       Date:  2007-04-12

6.  Specific and nonspecific membrane-binding determinants cooperate in targeting phosphatidylinositol transfer protein beta-isoform to the mammalian trans-Golgi network.

Authors:  Scott E Phillips; Kristina E Ile; Malika Boukhelifa; Richard P H Huijbregts; Vytas A Bankaitis
Journal:  Mol Biol Cell       Date:  2006-03-15       Impact factor: 4.138

7.  The fission yeast synaptobrevin ortholog Syb1 plays an important role in forespore membrane formation and spore maturation.

Authors:  Tomomi Yamaoka; Kazuki Imada; Kana Fukunishi; Yuriko Yamasaki; Chikashi Shimoda; Taro Nakamura
Journal:  Eukaryot Cell       Date:  2013-05-24

8.  Schizosaccharomyces pombe Sst4p, a conserved Vps27/Hrs homolog, functions downstream of phosphatidylinositol 3-kinase Pik3p to mediate proper spore formation.

Authors:  Masayuki Onishi; Michihiro Iida; Takako Koga; Sadayuki Yamada; Aiko Hirata; Tomoko Iwaki; Kaoru Takegawa; Yasuhisa Fukui; Hiroyuki Tachikawa
Journal:  Eukaryot Cell       Date:  2007-10-19

9.  Mug28, a meiosis-specific protein of Schizosaccharomyces pombe, regulates spore wall formation.

Authors:  Akira Shigehisa; Daisuke Okuzaki; Takashi Kasama; Hideki Tohda; Aiko Hirata; Hiroshi Nojima
Journal:  Mol Biol Cell       Date:  2010-04-21       Impact factor: 4.138

10.  A guaninine nucleotide exchange factor is a component of the meiotic spindle pole body in Schizosaccharomyces pombe.

Authors:  Hui-Ju Yang; Aaron M Neiman
Journal:  Mol Biol Cell       Date:  2010-02-03       Impact factor: 4.138

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