Molecular dissection of a yeast septin: Distinct domains are required for septin interaction, localization, and function

Molecular and Cellular Biology

Volumn 23, Issue 8, 2003, Pages 2762-2777

  Casamayor, Antonio ^a   Snyder, Michael ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 11; CYCLIN DEPENDENT KINASE 3; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; LIPID; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL 5 PHOSPHATE; PROTEIN BEM4; SEPTIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BUDDING; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; FUNGAL CELL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL CYCLE PROTEINS; CYTOSKELETAL PROTEINS; FUNGAL PROTEINS; GENES, FUNGAL; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MUTATION; PHOSPHATIDYLINOSITOLS; PLASMIDS; PROFILINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037383708     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.8.2762-2777.2003     Document Type: Article

References (69)

1. 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.
2. 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.
3. 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.
4. Barral, Y., M. Parra, S. Bidlingmaier, and M. Snyder. 1999. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 13:176-187.
5. Byers, B., and L. Goetsch. 1976. A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol. 69:717-721.
6. Casamayor, A., and M. Snyder. 2002. Bud-site selection and cell polarity in budding yeast. Curr. Opin. Microbiol. 5:179-186.
7. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119-122.
8. Deak, M., A. Casamayor, R. A. Currie, C. P. Downes, and D. R. Alessi. 1999. Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett. 451:220-226.
9. DeMarini, D. J., A. E. M. Adams, H. Fares, C. D. Virgilio, G. Valle, J. S. Chuang, and J. R. Pringle. 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 139:75-93.
10. Dove, S. K., F. T. Cooke, M. R. Douglas, L. G. Sayers, P. J. Parker, and R. H. Michell. 1996. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187-192.
11. Dowler, S., G. Kular, and D. R. Alessi. 2002. Protein lipid overlay assay. Sci. STKE http://stke.sciencemag.org/cgi/content/full/sigtrans;2002/129/p16.
12. Drees, B. L., B. Sundin, E. Brazeau, J. P. Caviston, G. C. Chen, W. Guo, K. G. Kozminski, M. W. Lau, J. J. Moskow, A. Tong, L. R. Schenkman, A. McKenzie III, P. Brennwald, M. Longtine, E. Bi, C. Chan, P. Novick, C. Boone, J. R. Pringle, T. N. Davis, S. Fields, and D. G. Drubin. 2001. A protein interaction map for cell polarity development. J. Cell Biol. 154:549-571.
13. 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.
14. Fares, H., M. Peifer, and J. R. Pringle. 1995. Localization and possible functions of Drosophila septins. Mol. Biol. Cell 6:1843-1859.
15. Faty, M., M. Fink, and Y. Barral. 2002. Septins: a ring to part mother and daughter. Curr. Genet. 41:123-131.
16. 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.
17. Field, C. M., and D. Kellogg. 1999. Septins: cytoskeletal polymers or signalling GTPases? Trends Cell Biol. 9:387-394.
18. Flescher, E. G., K. Madden, and M. Snyder. 1993. Components required for cytokinesis are important for bud site selection in yeast. J. Cell Biol. 122:373-386.
19. Ford, S. K., and J. R. Pringle. 1991. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site. Dev. Genet. 12:281-292.
20. 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.
21. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Cruciat, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
22. Gelperin, D., L. Horton, J. Beckman, J. Hensold, and S. K. Lemmon. 2001. Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 7:1268-1283.
23. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
24. 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.
25. Hartwell, L. H. 1971. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69:265-276.
26. Hartwell, L. H., R. K. Mortimer, J. Culotti, and M. Culotti. 1974. Genetic control of the cell division cycle in yeast. V. Genetic analysis of cdc mutants. Genetics 74:267-286.
27. Hartwig, J. H., S. Kung, T. Kovacsovics, P. A. Janmey, L. C. Cantley, T. P. Stossel, and A. Toker. 1996. D3 phosphoinositides and outside-in integrin signaling by glycoprotein IIb-IIIa mediate platelet actin assembly and filopodial extension induced by phorbol 12-myristate 13-acetate. J. Biol. Chem. 271:32986-32993.
28. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Yang, C. Wolting, I. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sorensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
29. James, P., J. Halladay, and E. A. Craig. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425-1436.
30. Janmey, P., J. Lamb, P. Allen, and P. Matsudaira. 1992. Phosphoinositide-binding peptides derived from the sequences of gelsolin and villin. J. Biol. Chem. 267:11818-11823.
31. Kartmann, B., and D. Roth. 2001. Novel roles for mammalian septins: from vesicle trafficking to oncogenesis. J. Cell Sci. 114:839-844.
32. Kim, H. B., B. K. Haarer, and J. R. Pringle. 1991. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. J. Cell Biol. 112:535-544.
33. 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.
34. Kinoshita, M., S. Kumar, A. Mizoguchi, C. Ide, A. Kinoshita, T. Haraguchi, Y. Hiraoka, and M. Noda. 1997. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev. 11:1535-1547.
35. Kinoshita, M., and M. Noda. 2001. Roles of septins in the mammalian cytokinesis machinery. Cell Struct. Funct. 26:667-670.
36. Komatsu, K., W. J. Driscoll, Y. C. Koh, and C. A. Strott. 1994. A P-loop related motif (GxxGxxK) highly conserved in sulfotransferases is required for binding the activated sulfate donor. Biochem. Biophys. Res. Commun. 204:1178-1185.
37. a. Kusch, J., A. Meyer, M. P. Snyder, and Y. Barral. 2002. Microbubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev. 16:1627-1639.
38. Lee, P. R., S. Song, H.-S. Ro, C. J. Park, J. Lippincott, R. Li, J. R. Pringle, C. De Virgilio, M. S. Longtine, and K. S. Lee. 2002. Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22:6906-6920.
39. 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.
40. Longtine, M. S., A. R. McKenzie, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyes cerevisiae. Yeast 14:953-961.
41. Longtine, M. S., C. L. Theesfeld, J. N. McMillan, E. Weaver, J. R. Pringle, and D. J. Lew. 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:4049-4061.
42. Lorenz, M. C., R. S. Muir, E. Lim, J. McElver, S. C. Weber, and J. Heitman. 1995. Gene disruption with PCR products in Saccharomyces cerevisiae. Gene 158:113-117.
43. Lu, P.-J., W.-R. Shieh, S. G. Rhee, H. L. Yin, and C.-S. Chen. 1996. Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity. Biochemistry 35:14027-14034.
44. Ma, X. J., Q. Lu, and M. Grunstein. 1996. A search for proteins that interact genetically with histone H3 and H4 amino termini uncovers novel regulators of the Swe1 kinase in Saccharomyces cerevisiae. Genes Dev. 10:1327-1340.
45. Martin, T. F. 1998. Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell Dev. Biol. 14:231-264.
46. McKean, P. G., S. Vaughan, and K. Gull. 2001. The extended tubulin superfamily. J. Cell Sci. 114:2723-2733.
47. Mino, A., K. Tanaka, T. Kamei, M. Umikawa, T. Fujiwara, and Y. Takai. 1998. Shs1p: a novel member of septin that interacts with Spa2p, involved in polarized growth in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 251:732-736.
48. Mitchell, D. A., T. K. Marshall, and R. J. Deschenes. 1993. Vector for the inducible overexpression of gluthatione S-transferase fusion protein in yeast. Yeast 9:715-723.
49. Neufeld, T. P., and G. M. Rubin. 1994. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell 77:371-379.
50. Robinson, J. S., D. J. Klionsky, L. M. Banta, and S. D. Emr. 1988. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and sorting of multiple vacuolar hydrolases. Mol. Cell. Biol. 8:4936-4948.
51. Roh, D.-H., B. Bowers, M. Schmidt, and E. Cabib. 2002. The septation apparatus, an autonomous system in budding yeast. Mol. Biol. Cell 13:2747-2759.
52. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
54. Santos, B., and M. Snyder. 2000. Sbe2p and Sbe22p, two homologous Golgi proteins involved in yeast cell wall formation. Mol. Biol. Cell 11:435-452.
55. Saraste, M., P. R. Sibbald, and A. Wittinghofer. 1990. The P-loop. A common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15:430-434.
56. Scheffers, D.-J., and A. J. M. Driessen. 2001. The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett. 506:6-10.
57. Schenkman, L. R., C. Caruso, N. Page, and J. R. Pringle. 2002. The role of cell cycle-regulated expression in the localization of spatial landmark proteins in yeast. J. Cell Biol. 156:829-841.
58. Schorr, M., A. Then, S. Tahirovic, N. Hug, and P. Mayinger. 2001. The phosphoinositide phosphatase Sac1p controls trafficking of the yeast Chs3p chitin synthase. Curr. Biol. 11:1421-1426.
59. Self, A. J., and A. Hall. 1995. Measurement of intrinsic nucleotide exchange and GTP hydrolysis rates. Methods Enzymol. 256:67-76.
60. P2. Cell Biol. Int. 25:1201-1206.
61. Sohn, R. H., J. Chen, K. S. Koblan, P. F. Bray, and P. J. Goldschmidt-Clermont. 1995. Localization of a binding site for phosphatidylinositol 4,5-bisphosphate on human profilin. J. Biol. Chem. 270:21114-21120.
62. Tachikawa, H., A. Bloecher, K. Tatchell, and A. M. Neiman. 2001. A Gip1p-G1c7p phosphatase complex regulates septin organization and spore wall formation. J. Cell Biol. 155:797-808.
63. Walch-Solimena, C., and P. Novick. 1991. The yeast phosphatidylinositol-4-OH kinase Pik1 regulates secretion at the Golgi. Nat. Cell Biol. 1:523-525.
64. 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. Cytoskeleton 43:52-62.
65. Yoneya, T., M. Tagaya, F. Kishi, A. Nakazawa, and T. Fukui. 1989. Site-directed mutagenesis of Gly-15 and Gly-20 in the glycine-rich region of adenylate kinase. J. Biochem. (Tokyo) 105:158-160.
66. Yonezawa, N., Y. Homma, I. Yahara, H. Sakai, and E. Nishida. 1991. A short sequence responsible for both phosphoinositide binding and actin binding activities of cofilin. J. Biol. Chem. 266:17218-17221.
67. 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.
68. Zheng, Y., M. J. Hart, and R. A. Cerione. 1995. Guanine nucleotide exchange catalyzed by db1 oncogene product. Methods Enzymol. 256:77-84.
69. Zhu, H., M. Bilgin, R. Bangham, D. Hall, A. Casamayor, P. Bertone, N. Lan, R. Jansen, S. Bidlingmaier, T. Houfek, T. Mitchell, P. Miller, R. A. Dean, M. Gerstein, and M. Snyder. 2001. Global analysis of protein activities using proteome chips. Science 293:2101-2105.