A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall

Journal of Cell Biology

Volumn 139, Issue 1, 1997, Pages 75-93

  DeMarini, Douglas J ^a,e   Adams, Alison E M ^b   Fares, Hanna ^a,f   De Virgilio, Claudio ^a,g   Valle, Giorgio ^c   Chuang, John S ^d   Pringle, John R ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b University of Arizona   (United States)

^c UNIVERSITY OF PADOVA   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e GLAXOSMITHKLINE   (United Kingdom)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; CHITIN SYNTHASE; MEMBRANE PROTEIN; PROTEIN;

ARTICLE; CELL WALL; CYTOKINESIS; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TEMPERATURE SENSITIVE MUTANT;

AMINO ACID SEQUENCE; BASE SEQUENCE; CELL CYCLE PROTEINS; CELL WALL; CHITIN; CHITIN SYNTHASE; CHROMOSOME MAPPING; CLONING, MOLECULAR; CYTOSKELETAL PROTEINS; FUNGAL PROTEINS; GENES, LETHAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 0030763146     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.1.75     Document Type: Article

References (77)

1. Adams, A.E.M. 1984. Cellular morphogenesis in the yeast Saccharomyces cerevisiae. Ph.D. thesis. The University of Michigan, Ann Arbor, MI. 179 pp.
2. Adams, A.E.M., and J.R. Pringle. 1984. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J. Cell Biol. 98:934-945.
3. Andrews, B.J., and S.W. Mason. 1993. Gene expression and the cell cycle: a family affair. Science (Wash. DC). 261:1543-1544.
4. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1995. Current Protocols in Molecular Biology. John Wiley and Sons Ltd., New York.
5. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
6. Beltzer, J.P., L.-F.L. Chang, A.E. Hinkkanen, and G.B. Kohlhaw. 1986. Structure of yeast LEU4. J. Biol. Chem. 261:5160-5167.
7. Bi, E., and J.R. Pringle. 1996. ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:5264-5275.
8. Breeden, L. 1996. Start-specific transcription in yeast. Curr. Top. Microbiol. Immunol. 208:95-125.
9. Briza, P., M. Breitenbach, A. Ellinger, and J. Segall. 1990. Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 4:1775-1789.
10. Briza, P., M. Eckerstorfer, and M. Breitenbach. 1994. The sporulation-specific enzymes encoded by the DIT1 and DIT2 genes catalyze a two-step reaction leading to a soluble LL-dityrosine-containing precursor of the yeast spore wall. Proc. Natl. Acad. Sci. USA. 91:4524-4528.
11. Bulawa, C.E. 1992. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol. Cell. Biol. 12:1764-1776.
12. Bulawa, C.E. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47:505-534.
13. Byers, B. 1981. Cytology of the yeast life cycle. In The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance. J.N. Strathern, E.W. Jones, and J.R. Broach, editors. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 59-96.
14. Byers, B., and L. Goetsch. 1976. A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol. 69:717-721.
15. Cabib, E. 1994. Nomenclature of genes related to chitin synthesis. In Yeast: A Newsletter for Persons Interested in Yeast, Volume 43. M.-A. LaChance, editor. 58.
16. Cabib, E., A. Sburlati, B. Bowers, and S.J. Silverman. 1989. Chitin synthase 1, an auxiliary enzyme for chitin synthesis in Saccharomyces cerevisiae. J. Cell Biol. 108:1665-1672.
17. Cabib, E., S.J. Silverman, and J.A. Shaw. 1992. Chitinase and chitin synthase 1: counterbalancing activities in cell separation of Saccharomvces cerevisiae. J. Gen. Microbiol. 138:97-102.
18. Chalfie, M., Y. Tu, G. Euskirchen, W.W. Ward, and D.C. Prasher. 1994. Green fluorescent protein as a marker for gene expression. Science (Wash. DC). 263:802-804.
19. Chant, J., M. Mischke, E. Mitchell, I. Herskowitz, and J.R. Pringle. 1995. Role of Bud3p in producing the axial budding pattern of yeast. J. Cell Biol. 129: 767-778.
20. Christianson, T.W., R.S. Sikorski, M. Dante, J.H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene (Amst.). 110: 119-122.
21. Chuang, J.S., and R.W. Schekman. 1996. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.J. Cell Biol. 135: 597-610.
22. Cooper, J.A., and D.P. Kiehart. 1996. Septins may form a ubiquitous family of cytoskeletal filaments. J. Cell Biol. 134:1345-1348.
23. Davis, R.W., D. Botstein, and J.R. Roth. 1980. Advanced Bacterial Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 251 pp.
24. 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 (Reading). 142:2897-2905.
25. Douglas, C.M., F. Foor, J.A. Marrinan, N. Morin, J.B. Nielsen, A.M. Dahl, P. Mazur, W. Baginsky, W. Li, M. El-Sherbeini et al. 1994. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-β-D-glucan synthase. Proc. Natl. Acad. Sci. USA. 91: 12907-12911.
26. Drubin, D.G., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
27. Fares, H., M. Peifer, and J.R. Pringle. 1995. Localization and possible functions of Drosophila septins. Mol. Biol. Cell. 6:1843-1859.
28. 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.
29. 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.
30. Fields, S., and R. Sternglanz. 1994. The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 10:286-292.
31. 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.
32. 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.
33. Gietz, R.D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene (Amst.). 74:527-534.
34. Guthrie, C., and G.R. Fink, editors. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1-933.
35. Gyuris, J., E. Golemis, H. Chertkov, and R. Brent. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell. 75:791-803.
36. 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.
37. rat to the plasma membrane. Cell. 63:133-139.
38. Hartwell, L.H. 1971a. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69:265-276.
39. Hartwell, L.H. 1971b. Genetic control of the cell division cycle in yeast. II. Genes controlling DNA replication and its initiation. J. Mol. Biol. 59:183-194.
40. Hayashibe, M., and S. Katohda. 1973. Initiation of budding and chitin-ring. J. Gen. Appl. Microbiol. 19:23-39.
41. Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene (Amst.). 28:351-359.
42. Hill, J.E., A.M. Myers, T.J. Koerner, and A. Tzagoloff. 1986. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 2:163-167.
43. Igual, J.C., A.L. Johnson, and L.H. Johnston. 1996. Coordinated regulation of gene expression by the cell cycle transcription factor SWI4 and the protein kinase C MAP kinase pathway for yeast cell integrity. EMBO J. 15:5001-5013.
44. Kawamoto, S., M. Nomura, and T. Ohno. 1992. Cloning and characterization of SKT5, a Saccharomyces cerevisiae gene that affects protoplast regeneration and resistance to killer toxin of Kluyveromyces lactis. J. Ferment. Bioeng. 4: 199-208.
45. 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.
46. Koch, C., and K. Nasmyth. 1994. Cell cycle regulated transcription in yeast. Curr. Opin. Cell Biol. 6:451-459.
47. Konopka, J.B., C. DeMattei, and C. Davis. 1995. AFR1 promotes polarized apical morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:723-730.
48. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 227:680-685.
49. Lillie, S.H., and J.R. Pringle. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143: 1384-1394.
50. 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.
51. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science (Wash. DC). 252:1162-1164.
52. Maina, C.V., P.D. Riggs, A.G. Grandea III, B.E. Slatko, L.S. Moran, J.A. Tagliamonte, L.A. McReynolds, and C. di Guan. 1988. An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein. Gene (Amst.). 74:365-373.
53. Mortimer, R.K., and D. Schild. 1980. Genetic map of Saccharomyces cerevisiae. Microbiol. Rev. 44:519-571.
54. 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.
55. Orlean, P. 1996. Biogenesis of yeast wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomvces. Cell Cycle and Cell Biology. J.R. Pringle, J.R. Broach, and E.W. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 229-362.
56. Pammer, M., P. Briza, A. Ellinger, T. Schuster, R. Stucka, H. Feldmann, and M. Breitenbach. 1992. DIT101 (CSD2, CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls. Yeast. 8:1089-1099.
57. Pandolfo, D., A. De Antoni, G. Lanfranchi, and G. Valle. 1996. The DNA sequence of cosmid 14-5 from chromosome XIV reveals 21 open reading frames including a novel gene encoding a globin-like domain. Yeast. 12: 1071-1076.
58. Pringle, J.R., R.A. Preston, A.E.M. Adams, T. Stearns, D.G. Drubin, B.K. Haarer, and E.W. Jones. 1989. Fluorescence microscopy methods for yeast. Methods Cell Biol. 31:357-435.
59. Pringle, J.R., E. Bi, H.A. Harkins, J.E. Zahner, C. De Virgilio, J. Chant, K. Corrado, and H. Fares. 1995. Establishment of cell polarity in yeast. Cold Spring Harbor Symp. Quant. Biol. 60:729-744.
60. Qadota, H., C.P. Python, S.B. Inoue, M. Arisawa, Y. Anraku, Y. Zheng, T. Watanabe, D.E. Levin, and Y. Ohya. 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science (Wash. DC). 272:279-281.
61. Riles, L., J.E. Dutchik, A. Baktha, B.K. McCauley, E.C. Thayer, M.P. Leckie, V.V. Braden, J.E. Depke, and M.V. Olson. 1993. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs. Genetics. 134:81-150.
62. Roberts, R.L., B. Bowers, M.L. Slater, and E. Cabib. 1983. Chitin synthesis and localization in cell division cycle mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 3:922-930.
63. Roncero, C., M.H. Valdivieso, J.C. Ribas, and A. Durán. 1988. Isolation and characterization of Saccharomvces cerevisiae mutants resistant to Calcofluor White. J. Bacteriol. 170:1950-1954.
64. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
65. Sanders, S.L., and C.M. Field. 1994. Septins in common? Curr. Biol. 4:907-910.
66. Sanders, S.L., and I. Herskowitz. 1996. The Bud4 protein of yeast, required for axial budding, is localized to the mother/bud neck in a cell cycle-dependent manner. J. Cell Biol. 134:413-427.
67. Santos, B., and M. Snyder. 1997. Targeting of chitin synthase 3 to polarized growth sites in yeast requires Chs5p and Myo2p. J. Cell Biol. 136:95-110.
68. Scherens, B., M. El Bakkoury, F. Vierendeels, E. Dubois, and F. Messenguy. 1993. Sequencing and functional analysis of a 32,560 bp segment on the left arm of yeast chromosome II. Identification of 26 open reading frames, including the KIP1 and SEC17 genes. Yeast. 9:1355-1371.
69. Shapira, S.K., J. Chow, F.V. Richaud, and M.J. Casadaban. 1983. New versatile plasmid vectors for expression of hybrid proteins coded by a cloned gene fused to lacZ gene sequences encoding an enzymatically active carboxy-terminal portion of β-galactosidase. Gene (Amst.). 25:71-82.
70. Shaw, J.A., P.C. Mol, B. Bowers, S.J. Silverman, M.H. Valdivieso, A. Durán, and E. Cabib. 1991. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 114:111-123.
71. Sikorski, R.S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
72. Slater, M.L., B. Bowers, and E. Cabib. 1985. Formation of septum-like structures at locations remote from the budding sites in cytokinesis-defective mutants of Saccharomyces cerevisiae. J. Bacteriol. 162:763-767.
73. Sloat, B.F., A. Adams, and J.R. Pringle. 1981. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 89:395-405.
74. 8-barrel proteins of tryptophan biosynthesis in the hyperthermophile Thermotoga maritima. EMBO J. 14:4395-4402.
75. Trilla, J.A., T. Cos. A. Durán, and C. Roncero. 1997. Characterisation of CHS4 (CAL2), a gene of Saccharomvces cerevisiae involved in chitin biosynthesis and allelic to SKT5 and CSD4. Yeast. 13:795-807.
76. Valdivieso, M.H., P.C. Mol, J.A. Shaw, E. Cabib, and A. Durán. 1991. CAL1, a gene required for activity of chitin synthase 3 in Saccharomyces cerevisiae. J. Cell Biol. 114:101-109.
77. Zervos, A.S., J. Gyuris, and R. Brent. 1993. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell. 72:223-232.