The carboxy-terminal tails of septins Cdc11 and Shs1 recruit myosin-II binding factor Bni5 to the bud neck in Saccharomyces cerevisiae

Genetics

Volumn 200, Issue 3, 2015, Pages 821-840

  Finnigan, Gregory C ^a   Booth, Elizabeth A ^a   Duvalyan, Angela ^a   Liao, Elizabeth N ^a   Thorner, Jeremy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Complexes; Cytokinesis; Filaments; Mutants; Yeast

Indexed keywords

CHIMERIC PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN I; MYOSIN II BINDING FACTOR BNI5; NANOBODY; SACCHAROMYCES CEREVISIAE PROTEIN; SEPTIN; SEPTIN CDC11; SEPTIN SHS1; UNCLASSIFIED DRUG; BNI5 PROTEIN, S CEREVISIAE; CDC11 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; PROTEIN BINDING; SHS1 PROTEIN, S CEREVISIAE;

ALTERNATIVE RNA SPLICING; ARTICLE; BUD NECK; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FUNGAL CELL; FUNGAL GENETICS; FUNGAL STRUCTURES; GENE DOSAGE; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; CYTOKINESIS; CYTOSKELETON; METABOLISM; PHYSIOLOGY; PROTEIN MOTIF;

SACCHAROMYCES CEREVISIAE;

AMINO ACID MOTIFS; CELL CYCLE PROTEINS; CYTOKINESIS; CYTOSKELETAL PROTEINS; CYTOSKELETON; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84937061343     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.176503     Document Type: Article

References (105)

1. Alonso, A., S. D'Silva, M. Rahman, P. B. Meluh, J. Keeling et al., 2012 The yeast homologue of the microtubule-associated protein Lis1 interacts with the SUMOylation machinery and a SUMOtargeted ubiquitin ligase. Mol. Biol. Cell 23: 4552-4566.
2. Asano, S., J. E. Park, L. R. Yu, M. Zhou, K. Sakchaisri et al., 2006 Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J. Biol. Chem. 281: 27090-27098.
3. 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.
4. Bertin, A., M. A. McMurray, P. Grob, S. S. Park, G. Garcia, 3rd et al., 2008 Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl. Acad. Sci. USA 105: 8274-8279.
5. Bertin, A., M. A. McMurray, L. Thai, G. Garcia, 3rd, V. Votin et al., 2010 Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J. Mol. Biol. 404: 711-731.
6. Bertin, A., M. A. McMurray, J. Pierson, L. Thai, K. L. McDonald et al., 2012 Three-dimensional ultrastructure of the septin filament network in Saccharomyces cerevisiae. Mol. Biol. Cell 23: 423-432.
7. Bessa, D., F. Pereira, R. Moreira, B. Johansson, and O. Queirós, 2012 Improved gap repair cloning in yeast: treatment of the gapped vector with Taq DNA polymerase avoids vector selfligation. Yeast 29: 419-423.
8. Bouquin, N., Y. Barral, R. Courbeyrette, M. Blondel, M. Snyder et al., 2000 Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae. J. Cell Sci. 113: 1435-1445.
9. Buttery, S. M., S. Yoshida, and D. Pellman, 2007 Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell 18: 1826-1838.
10. Buttery, S. M., K. Kono, E. Stokasimov, and D. Pellman, 2012 Regulation of the formin Bnr1 by septins anda MARK/ Par1-family septin-associated kinase. Mol. Biol. Cell 23: 4041-4053.
11. Chao, J. T., A. K. Wong, S. Tavassoli, B. P. Young, A. Chruscicki et al., 2014 Polarization of the endoplasmic reticulum by ERseptin tethering. Cell 158: 620-632.
12. Chen, H., C. C. Kuo, H. Kang, A. S. Howell, T. R. Zyla et al., 2012 Cdc42p regulation of the yeast formin Bni1p mediated by the effector Gic2p. Mol. Biol. Cell 23: 3814-3826.
13. Claret, S., X. Gatti, F. Doignon, D. Thoraval, and M. Crouzet, 2005 The Rgd1p Rho GTPase-activating protein and the Mid2p cell wall sensor are required at low pH for protein kinase C pathway activation and cell survival in Saccharomyces cerevisiae. Eukaryot. Cell 4: 1375-1386.
14. Crutchley, J., K. M. King, M. A. Keaton, L. Szkotnicki, D. A. Orlando et al., 2009 Molecular dissection of the checkpoint kinase Hsl1p. Mol. Biol. Cell 20: 1926-1936.
15. Dolat, L., Q. Hu, and E. T. Spiliotis, 2014 Septin functions in organ system physiology and pathology. Biol. Chem. 395: 123-141.
16. Edelstein, A., N. Amodaj, K. Hoover, R. Vale, and N. Stuurman, 2010 Computer control of microscopes using microManager. Curr Protoc Mol Biol Chapter 14: Unit14.20.
17. Estey, M. P., C. Di Ciano-Oliveira, C. D. Froese, M. T. Bejide, and W. S. Trimble, 2010 Distinct roles of septins in cytokinesis: SEPT9 mediates midbody abscission. J. Cell Biol. 191: 741-749.
18. Ewers, H., T. Tada, J. D. Petersen, B. Racz, M. Sheng et al., 2014 A septin-dependent diffusion barrier at dendritic spine necks. PLoS One 9: e113916.1-e113916.19.
19. Fang, X., J. Luo, R. Nishihama, C. Wloka, C. Dravis et al., 2010 Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin II. J. Cell Biol. 191: 1333-1350.
20. Finnigan, G. C., J. Tagaki, C. Cho and J. Thorner, 2015 Comprehensive genetic analysis of paralogous terminal septin subunits Shs1 and Cdc11 in Saccharomyces cerevisiae. Genetics 200: 841-861.
21. Füchtbauer, A., L. B. Lassen, A. B. Jensen, J. Howard, S. Quiroga Ade et al., 2011 Septin9 is involved in septin filament formation and cellular stability. Biol. Chem. 392: 769-777.
22. Gao, L., W. Liu, and A. Bretscher, 2010 The yeast formin Bnr1p has two localization regions that show spatially and temporally distinct association with septin structures. Mol. Biol. Cell 21: 1253-1262.
23. Gao, X. D., L. M. Sperber, S. A. Kane, Z. Tong, A. H. Tong et al., 2007 Sequential and distinct roles of the cadherin domaincontaining protein Axl2p in cell polarization in yeast cell cycle. Mol. Biol. Cell 18: 2542-2560.
24. Garcia, 3rd, G., A. Bertin, Z. Li, Y. Song, M. A. McMurray et al., 2011 Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J. Cell Biol. 195: 993-1004.
25. Ghossoub, R., Q. Hu, and M. Failler, M. C. Rouyez, B. Spitzbarth et al., 2013 Septins 2, 7 and 9 and MAP4 colocalize along the axoneme in the primary cilium and control ciliary length. J. Cell Sci. 126: 2583-2594.
26. Gilden, J. K., S. Peck, Y. C. Chen, and M. F. Krummel, 2012 The septin cytoskeleton facilitates membrane retraction during motility and blebbing. J. Cell Biol. 196: 103-114.
27. 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.
28. Goldstein, A. L., and J. H. McCusker, 1999 Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
29. Gong, T., Y. Liao, F. He, Y. Yang, D. D. Yang et al., 2013 Control of polarized growth by the Rho family GTPase Rho4 in budding yeast: requirement of the N-terminal extension of Rho4 and regulation by the Rho GTPase-activating protein Bem2. Eukaryot. Cell 12: 368-377.
30. Graziano, B. R., and E. M. Jonasson, J. G. Pullen, C. J. Gould, and B. L. Goode, 2013 Ligand-induced activation of a formin-NPF pair leads to collaborative actin nucleation. J. Cell Biol. 201: 595-611.
31. Hall, P. A., and S. E. Russell, 2012 Mammalian septins: dynamic heteromers with roles in cellular morphogenesis and compartmentalization. J. Pathol. 226: 287-299.
32. Hoang, M. L., R. P. Leon, L. Pessoa-Brandao, S. Hunt, M. K. Raghuraman et al., 2007 Structural changes in Mcm5 protein bypass Cdc7-Dbf4 function and reduce replication origin efficiency in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 7594-7602.
33. Hu, Q., L. Milenkovic, H. Jin, M. P. Scott, M. V. Nachury et al., 2010 A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329: 436-439.
34. Huh, W. K., J. V. Falvo, L. C. Gerke, A. S. Carroll, R. W. Howson et al., 2003 Global analysis of protein localization in budding yeast. Nature 425: 686-691.
35. Iwase, M., and A. Toh-e, 2001 Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet. Syst. 76: 335-343.
36. Iwase, M., J. Luo, E. Bi, and A. Toh-e, 2007 Shs1 plays separable roles in septin organization and cytokinesis in Saccharomyces cerevisiae. Genetics 177: 215-229.
37. Johnson, C. R., A. D. Weems, J. M. Brewer, J. Thorner, and M. A. McMurray, 2015 Cytosolic chaperones mediate quality control of higher-order septin assembly in budding yeast. Mol. Biol. Cell 26: 1323-1344.
38. Kang, P. J., M. E. Lee, and H. O. Park, 2014 Bud3 activates Cdc42 to establish a proper growth site in budding yeast. J. Cell Biol. 206: 19-28.
39. Kelley, L. A., and M. J. E. Sternberg, 2009 Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4: 363-371.
40. Kikyo, M., K. Tanaka, T. Kamei, K. Ozaki, T. Fujiwara et al., 1999 An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18: 7046-7054.
41. Kim, M. S., C. D. Froese, M. P. Estey, and W. S. Trimble, 2011 occupies the terminal positions in septin octamers and mediates polymerization-dependent functions in abscission. J. Cell Biol. 195: 815-826.
42. Kitada, K., A. L. Johnson, L. H. Johnston, and A. Sugino, 1993 A multicopy suppressor gene of the Saccharomyces cerevisiae G1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol. Cell. Biol. 13: 4445-4457.
43. Kitazono, A. A., 2009 Improved gap-repair cloning method that uses oligonucleotides to target cognate sequences. Yeast 26: 497-505.
44. Knaus, M., M. P. Pelli-Gulli, F. van Drogen, S. Springer, M. Jaquenoud et al., 2007 Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J. 26: 4501-4513.
45. Kota, J., and P. O. Ljungdahl, 2005 Specialized membranelocalized chaperones prevent aggregation of polytopic proteins in the ER. J. Cell Biol. 168: 79-88.
46. Kozubowski, L., H. Panek, A. Rosenthal, A. Bloecher, D. J. DeMarini et al., 2003 A Bni4-Glc7 phosphatase complex that recruits chitin synthase to the site of bud emergence. Mol. Biol. Cell 14: 26-39.
47. Kubala, M. H., O. Kovtun, K. Alexandrov, and B. M. Collins, 2010 Structural and thermodynamic analysis of the GFP: GFP-nanobody complex. Protein Sci. 19: 2389-2401.
48. Kumar, A., S. Agarwal, J. A. Heyman, S. Matson, M. Heidtman et al., 2002 Subcellular localization of the yeast proteome. Genes Dev. 16: 707-719.
49. Lee, P. R., S. Song, H. S. Ro, C. J. Park, J. Lippincott et al., 2002 Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 6906-6920.
50. Makanae, K., R. Kintaka, T. Makino, H. Kitano, and H. Moriya, 2013 Identification of dosage-sensitive genes in Saccharomyces cerevisiae using the genetic tug-of-war method. Genome Res. 23: 300-311.
51. McMurray, M. A., and J. Thorner, 2008 Biochemical properties and supramolecular architecture of septin hetero-oligomers and septin filaments, pp. 49-100 in The Septins, edited by P. A. Hall, S. E. G. Russell, and J. R. Pringle. John Wiley & Sons, Chichester, West Sussex.
52. McMurray, M. A., A. Bertin, G. Garcia, 3rd, L. Lam, E. Nogales et al., 2011 Septin filament formation is essential in budding yeast. Dev. Cell 20: 540-549.
53. Meitinger, F., M. E. Boehm, A. Hofmann, B. Hub, H. Zentgraf et al., 2011 Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev. 25: 875-888.
54. Meitinger, F., S. Palani, B. Hub, and G. Pereira, 2013 Dual function of the NDR-kinase Dbf2 in the regulation of the F-BAR protein Hof1 during cytokinesis. Mol. Biol. Cell 24: 1290-1304.
55. Meitinger, F., A. Khmelinskii, S. Morlot, S. Kurtulmus, S. Palani et al., 2014 A memory system of negative polarity cues prevents replicative aging. Cell 159: 1056-1069.
56. Meseroll, R. A., P. Occhipinti, and A. S. Gladfelter, 2013 Septin phosphorylation and coiled-coil domains function in cell and septin ring morphology in the filamentous fungus Ashbya gossypii. Eukaryot. Cell 12: 182-193.
57. Mino, A., K. Tanaka, T. Kamei, M. Umikawa, T. Fujiwara et al., 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.
58. Moriya, H., and K. Isono, 1999 Analysis of genetic interactions between DHH1, SSD1 and ELM1 indicates their involvement in cellular morphology determination in Saccharomyces cerevisiae. Yeast 15: 481-496.
59. Mortensen, E. M., H. McDonald, J. Yates, 3rd, and D. R. Kellogg, 2002 Cell cycle-dependent assembly of a Gin4-septin complex. Mol. Biol. Cell 13: 2091-2105.
60. Mostowy, S., M. Bonazzi, M. A. Hamon, T. N. Tham, A. Mallet et al., 2010 Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8: 433-444.
61. Muhlrad, D., R. Hunter, and R. Parker, 1992 A rapid method for localized mutagenesis of yeast genes. Yeast 8: 79-82.
62. Mumberg, D., R. Müller, and M. Funk, 1994 Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22: 5767-5768.
63. Nam, S. C., H. Sung, Y. B. Chung, C. K. Lee, D. H. Lee et al., 2007a Requirement of Bni5 phosphorylation for bud morphogenesis in Saccharomyces cerevisiae. J. Microbiol. 45: 34-40.
64. Nam, S. C., H. Sung, S. H. Kang, J. Y. Joo, S. J. Lee et al., 2007b Phosphorylation-dependent septin interaction of Bni5 is important for cytokinesis. J. Microbiol. 45: 227-233.
65. Nishihama, R., J. H. Schreiter, M. Onishi, E. A. Vallen, J. Hanna et al., 2009 Role of Inn1 and its interactions with Hof1 and Cyk3 in promoting cleavage furrow and septum formation in S. cerevisiae. J. Cell Biol. 185: 995-1012.
66. Okuzaki, D., S. Tanaka, H. Kanazawa, and H. Nojima, 1997 Gin4 of S. cerevisiae is a bud neck protein that interacts with the Cdc28 complex. Genes Cells 2: 753-770.
67. Okuzaki, D., T. Watanabe, S. Tanaka, and H. Nojima, 2003 The Saccharomyces cerevisiae bud-neck proteins Kcc4 and Gin4 have distinct but partially-overlapping cellular functions. Genes Genet. Syst. 78: 113-126.
68. Ong, K., C. Wloka, S. Okada, T. Svitkina, and E. Bi, 2014 Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle. Nat. Commun. 5: 5698.1-5698.10.
69. Ono, N., T. Yabe, M. Sudoh, T. Nakajima, T. Yamada-Okabe et al., 2000 The yeast Chs4 protein stimulates the trypsin-sensitive activity of chitin synthase 3 through an apparent protein-protein interaction. Microbiology 146: 385-391.
70. Renz, C., N. Johnsson, and T. Gronemeyer, 2013 An efficient protocol for the purification and labeling of entire yeast septin rods from E. coli for quantitative in vitro experimentation. BMC Biotechnol. 13: 60.
71. Roelants, F. M., B. M. Su, J. von Wulffen, S. Ramachandran, E. Sartorel et al., 2015 Protein kinase Gin4 negatively regulates flippase function and controls plasma membrane asymmetry. J. Cell Biol. 208: 299-311.
72. Roeseler, S., K. Sandrock, I. Bartsch, and B. Zieger, 2009 Septins, a novel group of GTP-binding proteins: relevance in hemostasis, neuropathology and oncogenesis. Klin. Padiatr. 221: 150-155.
73. Roncero, C., and Y. Sánchez, 2010 Cell separation and the maintenance of cell integrity during cytokinesis in yeast: the assembly of a septum. Yeast 27: 521-530.
74. Rothbauer, U., K. Zolghadr, S. Tillib, D. Nowak, L. Schermelleh et al., 2006 Targeting and tracing antigens in live cells with fluorescent nanobodies. Nat. Methods 3: 887-889.
75. Saarikangas, J., and Y. Barral, 2011 The emerging functions of septins in metazoans. EMBO Rep. 12: 1118-1126.
76. Sakchaisri, K., S. Asano, L. R. Yu, M. J. Shulewitz, C. J. Park et al., 2004 Coupling morphogenesis to mitotic entry. Proc. Natl. Acad. Sci. USA 101: 4124-4129.
77. Sambrook, J., and D. W. Russell, 2001 Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
78. Schneider, C., J. Grois, C. Renz, T. Gronemeyer, and N. Johnsson, 2013 Septin rings act as a template for myosin higher-order structures and inhibit redundant polarity establishment. J. Cell Sci. 126: 3390-3400.
79. Sellin, M. E., L. Sandblad, S. Stenmark, and M. Gullberg, 2011 Deciphering the rules governing assembly order of mammalian septin complexes. Mol. Biol. Cell 22: 3152-3164.
80. Sellin, M. E., S. Stenmark, and M. Gullberg, 2014 Cell typespecific expression of SEPT3-homology subgroup members controls the subunit number of heteromeric septin complexes. Mol. Biol. Cell 25: 1594-1607.
81. 2+ entry. Nature 499: 238-242.
82. Shulewitz, M. J., C. J. Inouye, and J. Thorner, 1999 Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 7123-7137.
83. 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.
84. Smith,G.R., S. A. Givan, P.Cullen, and G. F. J. Sprague, 2002 GTPaseactivating proteins for Cdc42. Eukaryot. Cell 1: 469-480.
85. Sopko, R., D. Huang, N. Preston, G. Chua, B. Papp et al., 2006 Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21: 319-330.
86. Stevenson, L. F., B. K. Kennedy, and E. Harlow, 2001 A large-scale overexpression screen in Saccharomyces cerevisiae identifies previously uncharacterized cell cycle genes. Proc. Natl. Acad. Sci. USA 98: 3946-3951.
87. Sugino, Y., K. Ichioka, T. Soda, M. Ihara, M. Kinoshita et al., 2008 Septins as diagnostic markers for a subset of human asthenozoospermia. J. Urol. 180: 2706-2709.
88. Tada, T., A. Simonetta, M. Batterton, M. Kinoshita, D. Edbauer et al., 2007 Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr. Biol. 17: 1752-1758.
89. Tian, C., Y. Wu, and N. Johnsson, 2014 Stepwise and cooperative assembly of a cytokinetic core complex in Saccharomyces cerevisiae. J. Cell Sci. 127: 3614-3624.
90. Tooley, A. J., J. Gilden, J. Jacobelli, P. Beemiller, W. S. Trimble et al., 2009 Amoeboid T lymphocytes require the septin cytoskeleton for cortical integrity and persistent motility. Nat. Cell Biol. 11: 17-26.
91. Toure, A., B. Rode, G. R. Hunnicutt, D. Escalier, and G. Gacon, 2011 Septins at the annulus of mammalian sperm. Biol. Chem. 392: 799-803.
92. Trimble, W. S., and S. Grinstein, 2015 Barriers to the free diffusion of proteins and lipids in the plasma membrane. J. Cell Biol. 208: 259-271.
93. Tu, D., B. R. Graziano, E. Park, W. Zheng, Y. Li et al., 2012 Structure of the formin-interaction domain of the actin nucleation-promoting factor Bud6. Proc. Natl. Acad. Sci. USA 109: E3424-E3433.
94. Tully, G. H., R. Nishihama, J. R. Pringle, and D. O. Morgan, 2009 The anaphase-promoting complex promotes actomyosinring disassembly during cytokinesis in yeast. Mol. Biol. Cell 20: 1201-1212.
95. Versele, M., and J. Thorner, 2004 Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J. Cell Biol. 164: 701-715.
96. Versele, M., B. Gullbrand, M. J. Shulewitz, V. J. Cid, S. Bahmanyar et al., 2004 Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 4568-4583.
97. Volceanov, L., K. Herbst, M. Biniossek, O. Schilling, D. Haller et al., 2014 Septins arrange F-actin-containing fibers on the Chlamydia trachomatis inclusion and are required for normal release of the inclusion by extrusion. MBio 5: e01802-14.1- e01802-14.12.
98. Vrabioiu, A. M., and T. J. Mitchison, 2006 Structural insights into yeast septin organization from polarized fluorescence microscopy. Nature 443: 466-469.
99. Wloka, C., and E. Bi, 2012 Mechanisms of cytokinesis in budding yeast. Cytoskeleton (Hoboken) 69: 710-726.
100. Wloka, C., R. Nishihama, M. Onishi, Y. Oh, J. Hanna et al., 2011 Evidence that a septin diffusion barrier is dispensable for cytokinesis in budding yeast. Biol. Chem. 392: 813-829.
101. Wloka, C., and E. A. Vallen, L. Thé, X. Fang, Y. Oh et al., 2013 Immobile myosin-II plays a scaffolding role during cytokinesis in budding yeast. J. Cell Biol. 200: 271-286.
102. Wu, H., J. Guo, Y. T. Zhou, and X. D. Gao, 2015 The anillinrelated region of Bud4 is the major functional determinant for Bud4's function in septin organization during bud growth and axial bud-site selection in budding yeast. Eukaryot. Cell 14: 241-251.
103. Yoshikawa, K., T. Tanaka, Y. Ida, C. Furusawa, T. Hirasawa et al., 2011 Comprehensive phenotypic analysis of single-gene deletion and overexpression strains of Saccharomyces cerevisiae. Yeast 28: 349-361.
104. Zheng, B., J. N. Wu, W. Schober, D. E. Lewis, and T. Vida, 1998 Isolation of yeast mutants defective for localization of vacuolar vital dyes. Proc. Natl. Acad. Sci. USA 95: 11721-11726.
105. Zheng, L., U. Baumann and J. L. Reymond, 2004 An efficient onestep site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32: e115.111-e115.115.