Role of Septins in the Orientation of Forespore Membrane Extension during Sporulation in Fission Yeast

REFERENCES

• Abe, H., and C. Shimoda. 2000. Autoregulated expression of Schizosaccharomyces pombe meiosis-specific transcription factor Mei4 and a genome-wide search for its target genes. Genetics 154:1497–1508.
   PubMedGoogle Scholar
• Al-Awar, O. S. 1996. The role of septins in the morphogenesis of Schizosaccharomyces pombe and Drosophila melanogaster. Ph.D. thesis. University of North Carolina, Chapel Hill, NC.
   Google Scholar
• An, H., J. L. Morrell, J. L. Jennings, A. J. Link, and K. L. Gould. 2004. Requirements of fission yeast septins for complex formation, localization, and function. Mol. Biol. Cell 15:5551–5564.
   PubMed Web of Science ®Google Scholar
• Audhya, A., M. Foti, and S. D. Emr. 2000. Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell 11:2673–2689.
   PubMedGoogle Scholar
• Audhya, A., and S. D. Emr. 2002. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2:593–605.
   PubMed Web of Science ®Google Scholar
• Bähler, J., J. Q. Wu, M. S. Longtine, N. G. Shah, A. McKenzie III, A. B. Steever, A. Wach, P. Philippsen, and J. R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943–951.
   PubMed Web of Science ®Google Scholar
• Barral, Y., V. Mermall, M. S. Mooseker, and M. Snyder. 2000. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol. Cell 5:841–851.
   PubMed Web of Science ®Google Scholar
• Barral, Y. 2008. Yeast septins: a cortical organizer, p. 101 –123. In P. A. Hall, S. E. H. Russell, and J. R. Pringle (ed.), The septins. Wiley Blackwell, London, United Kingdom.
   Google Scholar
• Basi, G., E. Schmid, and K. Maundrell. 1993. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene 123:131–136.
   PubMed Web of Science ®Google Scholar
• Berlin, A., A. Paoletti, and F. Chang. 2003. Mid2p stabilizes septin rings during cytokinesis in fission yeast. J. Cell Biol. 160:1083–1092.
   PubMedGoogle Scholar
• Bertin, A., M. A. McMurray, P. Grob, S. Park, G. Garcia III, I. Patanwala, H. Ng, T. Alber, J. Thorner, and E. Nogales. 2008. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl. Acad. Sci. USA 105:8274–8279.
   PubMed Web of Science ®Google Scholar
• Byers, B., and L. Goetsch. 1976. A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol. 69:717–721.
   PubMed Web of Science ®Google Scholar
• Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99:7877–7882.
   PubMed Web of Science ®Google Scholar
• Casamayor, A., and M. Snyder. 2003. Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol. Cell. Biol. 23:2762–2777.
   PubMed Web of Science ®Google Scholar
• De Virgilio, C., D. J. DeMarini, and J. R. Pringle. 1996. SPR28, a sixth member of the septin gene family in Saccharomyces cerevisiae that is expressed specifically in sporulating cells. Microbiology 142:2897–2905.
   PubMedGoogle Scholar
• Egel, R., and M. Egel-Mitani. 1974. Premeiotic DNA synthesis in fission yeast. Exp. Cell Res. 88:127–134.
   PubMedGoogle Scholar
• Fares, H., L. Goetsch, and J. R. Pringle. 1996. Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J. Cell Biol. 132:399–411.
   PubMedGoogle Scholar
• Farkasovsky, M., P. Herter, B. Voss, and A. Wittinghofer. 2005. Nucleotide binding and filament assembly of recombinant yeast septin complexes. Biol. Chem. 386:643–656.
   PubMed Web of Science ®Google Scholar
• Field, C. M., O. Al-Awar, J. Rosenblatt, M. L. Wong, B. Alberts, and T. J. Mitchison. 1996. A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J. Cell Biol. 133:605–616.
   PubMedGoogle Scholar
• Frazier, J. A., M. L. Wong, M. S. Longtine, J. R. Pringle, M. Mann, T. J. Mitchison, and C. Field. 1998. Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J. Cell Biol. 143:737–749.
   PubMedGoogle Scholar
• Gale, C., M. Gerami-Nejad, M. McClellan, S. Vandoninck, M. S. Longtine, and J. Berman. 2001. Candida albicans Int1p interacts with the septin ring in yeast and hyphal cells. Mol. Biol. Cell 12:3538–3549.
   PubMedGoogle Scholar
• Gladfelter, A. S., J. R. Pringle, and D. J. Lew. 2001. The septin cortex at the yeast mother-bud neck. Curr. Opin. Microbiol. 4:681–689.
   PubMed Web of Science ®Google Scholar
• Gladfelter, A. S., and P. Sudbery. 2008. Septins in four model fungal systems: diversity in form and function, p. 125 –145. In P. A. Hall, S. E. H. Russell, and J. R. Pringle (ed.), The septins. Wiley Blackwell, London, United Kingdom.
   Google Scholar
• Gutz, H., H. Heslot, U. Leupold, and N. Loprieno. 1974. Schizosaccharomyces pombe. Handb. Genet. 1:395–446.
   Google Scholar
• Haarer, B. K., and J. R. Pringle. 1987. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol. Cell. Biol. 7:3678–3687.
   PubMed Web of Science ®Google Scholar
• Hagan, I., and M. Yanagida. 1995. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J. Cell Biol. 129:1033–1047.
   PubMed Web of Science ®Google Scholar
• Hall, P. A., S. E. H. Russell, and J. R. Pringle. 2008. The septins. Wiley Blackwell, London, United Kingdom.
   Google Scholar
• Hama, H., E. A. Schnieders, J. Thorner, J. Y. Takemoto, and D. B. DeWald. 1999. Direct involvement of phosphatidylinositol 4-phosphate in secretion in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 274:34294–34300.
   PubMedGoogle Scholar
• Hirata, A., and C. Shimoda. 1994. Structural modification of spindle pole bodies during meiosis II is essential for the normal formation of ascospores in Schizosaccharomyces pombe: ultrastructural analysis of spo mutants. Yeast 10:173–183.
   PubMedGoogle Scholar
• Ikemoto, S., T. Nakamura, M. Kubo, and C. Shimoda. 2000. S. pombe sporulation-specific coiled-coil protein Spo15p is localized to the spindle pole body and essential for its modification. J. Cell Sci. 113:545–554.
   PubMedGoogle Scholar
• John, C. M., R. K. Hite, C. S. Weirich, D. J. Fitzgerald, H. Jawhari, M. Faty, D. Schläpfer, R. Kroschewski, F. K. Winkler, T. Walz, Y. Barral, and M. O. Steinmetz. 2007. The Caenorhabditis elegans septin complex is nonpolar. EMBO J. 26:3296–3307.
   PubMed Web of Science ®Google Scholar
• Kaback, D. B., and L. R. Feldberg. 1985. Saccharomyces cerevisiae exhibits a sporulation-specific temporal pattern of transcript accumulation. Mol. Cell. Biol. 5:751–761.
   PubMed Web of Science ®Google Scholar
• Kaksonen, M., C. P. Toret, and D. G. Drubin. 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell. Biol. 7:404–414.
   PubMed Web of Science ®Google Scholar
• Kashiwazaki, J., T. Nakamura, T. Iwaki, K. Takegawa, and C. Shimoda. 2005. A role for fission yeast Rab GTPase Ypt7p in sporulation. Cell Struct. Funct. 30:43–49.
   PubMedGoogle Scholar
• Kimura, K., S. Miyake, M. Makuuchi, R. Morita, T. Usui, M. Yoshida, S. Horinouchi, and Y. Fukui. 1995. Phosphatidylinositol-3 kinase in fission yeast: a possible role in stress responses. Biosci. Biotechnol. Biochem. 59:678–682.
   PubMed Web of Science ®Google Scholar
• Kinoshita, M., C. M. Field, M. L. Coughlin, A. F. Straight, and T. J. Mitchison. 2002. Self- and actin-templated assembly of mammalian septins. Dev. Cell 3:791–802.
   PubMed Web of Science ®Google Scholar
• Knop, M., and K. Strasser. 2000. Role of the spindle pole body of yeast in mediating assembly of the prospore membrane during meiosis. EMBO J. 19:3657–3667.
   PubMed Web of Science ®Google Scholar
• Koga, T., M. Onishi, Y. Nakamura, A. Hirata, T. Nakamura, C. Shimoda, T. Iwaki, K. Takegawa, and Y. Fukui. 2004. Sorting nexin homologues are targets of phosphatidylinositol 3-phosphate in sporulation of Schizosaccharomyces pombe. Genes Cells 9:561–574.
   PubMedGoogle Scholar
• Kurahashi, H., Y. Imai, and M. Yamamoto. 2002. Tropomyosin is required for the cell fusion process during conjugation in fission yeast. Genes Cells 7:375–384.
   PubMedGoogle Scholar
• Leupold, U. 1970. Genetical methods for Schizosaccharomyces pombe. Methods Cell Physiol. 4:169–177.
   Google Scholar
• Longtine, M. S., D. J. DeMarini, M. L. Valencik, O. S. Al-Awar, H. Fares, C. De Virgilio, and J. R. Pringle. 1996. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8:106–119.
   PubMed Web of Science ®Google Scholar
• Lyne, R., G. Burns, J. Mata, C. J. Penkett, G. Rustici, D. Chen, C. Langford, D. Vetrie, and J. Bähler. 2003. Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4:27.
   PubMed Web of Science ®Google Scholar
• Maina, C. V., P. D. Riggs, A. G. Grandea III, B. E. Slatko, L. S. Moran, J. A. Tagliamonte, L. A. McReynolds, and C. D. Guan. 1988. An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein. Gene 74:365–373.
   PubMed Web of Science ®Google Scholar
• Martín-Cuadrado, A. B., J. L. Morrell, M. Konomi, H. An, C. Petit, M. Osumi, M. Balasubramanian, K. L. Gould, F. Del Rey, and C. R. Vázquez de Aldana. 2005. Role of septins and the exocyst complex in the function of hydrolytic enzymes responsible for fission yeast cell separation. Mol. Biol. Cell 16:4867–4881.
   PubMed Web of Science ®Google Scholar
• Mata, J., R. Lyne, G. Burns, and J. Bähler. 2002. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32:143–147.
   PubMed Web of Science ®Google Scholar
• McLeod, M., M. Stein, and D. Beach. 1987. The product of the mei3+ gene, expressed under control of the mating-type locus, induces meiosis and sporulation in fission yeast. EMBO J. 6:729–736.
   PubMed Web of Science ®Google Scholar
• McMurray, M. A., and J. Thorner. 2008. Biochemical properties and supramolecular architecture of septin hetero-oligomers and septin filaments, p. 49 –100. In P. A. Hall, S. E. H. Russell, and J. R. Pringle (ed.), The septins. Wiley Blackwell, London, United Kingdom.
   Google Scholar
• McMurray, M. A., and J. Thorner. 2008. Septin stability and recycling during dynamic structural transitions in cell division and development. Curr. Biol. 18:1203–1208.
   PubMedGoogle Scholar
• Mitra, P., Y. Zhang, L. E. Rameh, M. P. Ivshina, D. McCollum, J. J. Nunnari, G. M. Hendricks, M. L. Kerr, S. J. Field, L. C. Cantley, and A. H. Ross. 2004. A novel phosphatidylinositol(3,4,5)P3 pathway in fission yeast. J. Cell Biol. 166:205–211.
   PubMed Web of Science ®Google Scholar
• Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795–823.
   PubMed Web of Science ®Google Scholar
• Moreno-Borchart, A. C., K. Strasser, M. G. Finkbeiner, A. Shevchenko, A. Shevchenko, and M. Knop. 2001. Prospore membrane formation linked to the leading edge protein (LEP) coat assembly. EMBO J. 20:6946–6957.
   PubMedGoogle Scholar
• Nagaraj, S., A. Rajendran, C. E. Jackson, and M. S. Longtine. 2008. Role of nucleotide binding in septin-septin interactions and septin localization in Saccharomyces cerevisiae. Mol. Cell. Biol. 28:5120–5127.
   PubMedGoogle Scholar
• Nakamura, T., M. Nakamura-Kubo, A. Hirata, and C. Shimoda. 2001. The Schizosaccharomyces pombe spo3+ gene is required for assembly of the forespore membrane and genetically interacts with psy1+-encoding syntaxin-like protein. Mol. Biol. Cell 12:3955–3972.
   PubMedGoogle Scholar
• Nakamura, T., J. Kashiwazaki, and C. Shimoda. 2005. A fission yeast SNAP-25 homologue, SpSec9, is essential for cytokinesis and sporulation. Cell Struct. Funct. 30:15–24.
   PubMedGoogle Scholar
• Nakamura, T., H. Asakawa, Y. Nakase, J. Kashiwazaki, Y. Hiraoka, and C. Shimoda. 2008. Live observation of forespore membrane formation in fission yeast. Mol. Biol. Cell 19:3544–3553.
   PubMedGoogle Scholar
• Nakamura-Kubo, M., T. Nakamura, A. Hirata, and C. Shimoda. 2003. The fission yeast spo14+ gene encoding a functional homologue of budding yeast Sec12 is required for the development of forespore membranes. Mol. Biol. Cell 14:1109–1124.
   PubMedGoogle Scholar
• Nakase, Y., M. Nakamura-Kubo, Y. Ye, A. Hirata, C. Shimoda, and T. Nakamura. 2008. Meiotic spindle pole bodies acquire the ability to assemble the spore plasma membrane by sequential recruitment of sporulation-specific components in fission yeast. Mol. Biol. Cell 19:2476–2487.
   PubMedGoogle Scholar
• Neiman, A. M. 1998. Prospore membrane formation defines a developmentally regulated branch of the secretory pathway in yeast. J. Cell Biol. 140:29–37.
   PubMed Web of Science ®Google Scholar
• Neiman, A. M. 2005. Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69:565–584.
   PubMed Web of Science ®Google Scholar
• Okuzaki, D., W. Satake, A. Hirata, and H. Nojima. 2003. Fission yeast meu14+ is required for proper nuclear division and accurate forespore membrane formation during meiosis II. J. Cell Sci. 116:2721–2735.
   PubMedGoogle Scholar
• Onishi, M., T. Koga, R. Morita, Y. Nakamura, T. Nakamura, C. Shimoda, K. Takegawa, A. Hirata, and Y. Fukui. 2003. Role of phosphatidylinositol 3-phosphate in formation of forespore membrane in Schizosaccharomyces pombe. Yeast 20:193–206.
   PubMedGoogle Scholar
• Onishi, M., M. Iida, T. Koga, S. Yamada, A. Hirata, T. Iwaki, K. Takegawa, Y. Fukui, and H. Tachikawa. 2007. Schizosaccharomyces pombe Sst4p, a conserved Vps27/Hrs homolog, functions downstream of phosphatidylinositol 3-kinase Pik3p to mediate proper spore formation. Eukaryot. Cell 6:2343–2353.
   PubMedGoogle Scholar
• Pan, F., R. L. Malmberg, and M. Momany. 2007. Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol. Biol. 7:103.
   PubMed Web of Science ®Google Scholar
• Petersen, J., O. Nielsen, R. Egel, and I. M. Hagan. 1998. F-actin distribution and function during sexual differentiation in Schizosaccharomyces pombe. J. Cell Sci. 111:867–876.
   PubMedGoogle Scholar
• Petersen, J., O. Nielsen, R. Egel, and I. M. Hagan. 1998. FH3, a domain found in formins, targets the fission yeast formin Fus1 to the projection tip during conjugation. J. Cell Biol. 141:1217–1228.
   PubMedGoogle Scholar
• Roy, A., and T. P. Levine. 2004. Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J. Biol. Chem. 279:44683–44689.
   PubMedGoogle Scholar
• Sawano, A., and A. Miyawaki. 2000. Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res. 28:E78.
   PubMedGoogle Scholar
• Shimoda, C. 2004. Forespore membrane assembly in yeast: coordinating SPBs and membrane trafficking. J. Cell Sci. 117:389–396.
   PubMedGoogle Scholar
• Sirajuddin, M., M. Farkasovsky, F. Hauer, D. Kühlmann, I. G. Macara, M. Weyand, H. Stark, and A. Wittinghofer. 2007. Structural insight into filament formation by mammalian septins. Nature 449:311–315.
   PubMed Web of Science ®Google Scholar
• Spiliotis, E. T., and W. J. Nelson. 2006. Here come the septins: novel polymers that coordinate intracellular functions and organization. J. Cell Sci. 119:4–10.
   PubMedGoogle Scholar
• Tachikawa, H., A. Bloecher, K. Tatchell, and A. M. Neiman. 2001. A Gip1p-Glc7p phosphatase complex regulates septin organization and spore wall formation. J. Cell Biol. 155:797–808.
   PubMedGoogle Scholar
• Takegawa, K., D. B. DeWald, and S. D. Emr. 1995. Schizosaccharomyces pombe Vps34p, a phosphatidylinositol-specific PI 3-kinase essential for normal cell growth and vacuole morphology. J. Cell Sci. 108:3745–3756.
   PubMed Web of Science ®Google Scholar
• Takizawa, P. A., J. L. DeRisi, J. E. Wilhelm, and R. D. Vale. 2000. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290:341–344.
   PubMed Web of Science ®Google Scholar
• Tanaka, K., and A. Hirata. 1982. Ascospore development in the fission yeasts Schizosaccharomyces pombe and S. japonicus. J. Cell Sci. 56:263–279.
   PubMedGoogle Scholar
• Tanaka, K., T. Yonekawa, Y. Kawasaki, M. Kai, K. Furuya, M. Iwasaki, H. Murakami, M. Yanagida, and H. Okayama. 2000. Fission yeast Eso1p is required for establishing sister chromatid cohesion during S phase. Mol. Cell. Biol. 20:3459–3469.
   PubMedGoogle Scholar
• Tasto, J. J., J. L. Morrell, and K. L. Gould. 2003. An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J. Cell Biol. 160:1093–1103.
   PubMedGoogle Scholar
• Vrabioiu, A. M., and T. J. Mitchison. 2007. Symmetry of septin hourglass and ring structures. J. Mol. Biol. 372:37–49.
   PubMedGoogle Scholar
• Watanabe, T., K. Miyashita, T. T. Saito, T. Yoneki, Y. Kakihara, K. Nabeshima, Y. A. Kishi, C. Shimoda, and H. Nojima. 2001. Comprehensive isolation of meiosis-specific genes identifies novel proteins and unusual non-coding transcripts in Schizosaccharomyces pombe. Nucleic Acids Res. 29:2327–2337.
   PubMedGoogle Scholar
• Wu, J.-Q., J. R. Kuhn, D. R. Kovar, and T. D. Pollard. 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 5:723–734.
   PubMed Web of Science ®Google Scholar
• Xie, H., M. Surka, J. Howard, and W. S. Trimble. 1999. Characterization of the mammalian septin H5: distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motil. Cytoskel. 43:52–62.
   PubMedGoogle Scholar
• Yamamoto, M., and Y. Watanabe. 1997. Mating and sporulation in Schizosaccharomyces pombe, p. 1037–1106. In J. R. Pringle, J. R. Broach, and E. W. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces: cell cycle and cell biology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Yamashita, A., Y. Watanabe, N. Nukina, and M. Yamamoto. 1998. RNA-assisted nuclear transport of the meiotic regulator Mei2p in fission yeast. Cell 95:115–123.
   PubMedGoogle Scholar
• Zhang, J., C. Kong, H. Xie, P. S. McPherson, S. Grinstein, and W. S. Trimble. 1999. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr. Biol. 9:1458–1467.
   PubMed Web of Science ®Google Scholar