The role of Cdc42 and Gic1 in the regulation of septin filament formation and dissociation

eLife

Volumn 2013, Issue 2, 2013, Pages

  Sadian, Yashar ^a   Gatsogiannis, Christos ^a   Patasi, Csilla ^b   Hofnagel, Oliver ^a   Goody, Roger S ^a   Farkašovský, Marian ^b   Raunser, Stefan ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES AND PROTEINS; PROTEIN CDC42; PROTEIN GIC1; SEPTIN; UNCLASSIFIED DRUG; GIC1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; GEL FILTRATION CHROMATOGRAPHY; NONHUMAN; POLYMERIZATION; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEPTIN FILAMENT FORMATION AND DISSOCIATION; BIOSYNTHESIS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; MICROSCOPY, ELECTRON; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEPTINS;

EID: 84888579944     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01085     Document Type: Article

References (37)

1. Bertin A, McMurray MA, Grob P, Park SS, Garcia G III, Patanwala I, et al. 2008. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci USA 105:8274-9. doi: 10.1073/pnas.0803330105.
2. Bertin A, McMurray MA, Thai L, Garcia G III, Votin V, Grob P, et al. 2010. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J Mol Biol 404:711-31. doi: 10.1016/j.jmb.2010.10.002.
3. Bröcker C, Kuhlee A, Gatsogiannis C, Kleine Balderhaar HJ, Honscher C, Engelbrecht-Vandre S, et al. 2012. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci USA 109:1991-6. doi: 10.1073/pnas.1117797109.
4. Brown JL, Jaquenoud M, Gulli MP, Chant J, Peter M. 1997. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev 11:2972-82. doi: 10.1101/gad.11.22.2972.
5. Butty A-C, Perrinjaquet N, Petit A, Jaquenoud M, Segall JE, Hofmann K, et al. 2002. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J 21:1565-76. doi: 10.1093/emboj/21.7.1565.
6. Byers B, Goetsch L. 1976. A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol 69:717-21. doi: 10.1083/jcb.69.3.717.
7. Caviston JP, Longtine M, Pringle JR, Bi E. 2003. The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol Biol Cell 14:4051-66. doi: 10.1091/mbc.E03-04-0247.
8. Chen GC, Kim YJ, Chan CS. 1997. The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev 11:2958-71. doi: 10.1101/gad.11.22.2958.
9. Farkasovsky M, Herter P, Voss B, Wittinghofer A. 2005. Nucleotide binding and filament assembly of recombinant yeast septin complexes. Biol Chem 386:643-56. doi: 10.1515/BC.2005.075.
10. Ford SK, Pringle JR. 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 12:281-92. doi: 10.1002/dvg.1020120405.
11. Gladfelter AS, Bose I, Zyla TR, Bardes ESG, Lew DJ. 2002. Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J Cell Biol 156:315-26. doi: 10.1083/jcb.200109062.
12. Goryachev AB, Pokhilko AV. 2008. Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett 582:1437-43. doi: 10.1016/j.febslet.2008.03.029.
13. Haarer BK, Pringle JR. 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 7:3678-87.
14. Hall PA, Russell SEH. 2004. The pathobiology of the septin gene family. J Pathol 204:489-505. doi: 10.1002/path.1654.
15. Hartwell LH. 1971. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69:265-76. doi: 10.1016/0014-4827(71)90223-0.
16. Hohn M, Tang G, Goodyear G, Baldwin PR, Huang Z, Penczek PA, et al. 2007. SPARX, a new environment for Cryo-EM image processing. J Struct Biol 157:47-55. doi: 10.1016/j.jsb.2006.07.003.
17. Ihara M, Kinoshita A, Yamada S, Tanaka H, Tanigaki A, Kitano A, et al. 2005. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell 8:343-52. doi: 10.1016/j.devcel.2004.12.005.
18. Iwase M, Luo J, Nagaraj S, Longtine M, Bai Kim H, Haarer BK, et al. 2006. Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol Biol Cell 17:1110-25. doi: 10.1091/mbc.E05-08-0793.
19. Joberty G, Perlungher RR, Sheffield PJ, Kinoshita M, Noda M, Haystead T, et al. 2001. Borg proteins control septin organization and are negatively regulated by Cdc42. Nat Cell Biol 3:861-6. doi: 10.1038/ncb1001-861.
20. Joberty G, Perlungher RR, Macara IG. 1999. The Borgs, a new family of Cdc42 and TC10 GTPase-interacting proteins. Mol Cell Biol 19:6585-97.
21. Kelley LA, Sternberg MJE. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-71. doi: 10.1038/nprot.2009.2.
22. Kim HB, Haarer BK, Pringle JR. 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 112:535-44. doi: 10.1083/jcb.112.4.535.
23. Kinoshita M. 2006. Diversity of septin scaffolds. Curr Opin Cell Biol 18:54-60. doi: 10.1016/j.ceb.2005.12.005.
24. Kozminski KG, Beven L, Angerman E, Hin Yan Tong A, Boone C, Park H-O. 2003. Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Mol Biol Cell 14:4958-70. doi: 10.1091/mbc.E03-06-0426.
25. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-6. doi: 10.1006/jsbi.1996.0013.
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-8. doi: 10.1093/bioinformatics/btm404.
27. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128:82-97. doi: 10.1006/jsbi.1999.4174.
28. McMurray MA, Thorner J. 2009. Reuse, replace, recycle. Specificity in subunit inheritance and assembly of higher-order septin structures during mitotic and meiotic division in budding yeast. Cell Cycle 8:195-203. doi: 10.4161/cc.8.2.7381.
29. Orlando K, Zhang J, Zhang X, Yue P, Chiang T, Bi E, et al. 2008. Regulation of Gic2 localization and function by phosphatidylinositol 4,5-bisphosphate during the establishment of cell polarity in budding yeast. J Biol Chem 283:14205-12. doi: 10.1074/jbc.M708178200.
30. Park H-O, Bi E. 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol Mol Biol Rev 71:48-96. doi: 10.1128/MMBR.00028-06.
31. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-12. doi: 10.1002/jcc.20084.
32. Rudolph MG, Bayer P, Abo A, Kuhlmann J, Vetter IR, Wittinghofer A. 1998. The Cdc42/Rac interactive binding region motif of the Wiskott Aldrich syndrome protein (WASP) is necessary but not sufficient for tight binding to Cdc42 and structure formation. J Biol Chem 273:18067-76.
33. Sheffield PJ, Oliver CJ, Kremer BE, Sheng S, Shao Z, Macara IG. 2003. Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments. J Biol Chem 278:3483-8. doi: 10.1074/jbc.M209701200.
34. Sirajuddin M, Farkasovsky M, Hauer F, Kühlmann D, Macara IG, Weyand M, et al. 2007. Structural insight into filament formation by mammalian septins. Nature 449:311-5. doi: 10.1038/nature06052.
35. Sirajuddin M, Farkasovsky M, Zent E, Wittinghofer A. 2009. GTP-induced conformational changes in septins and implications for function. Proc Natl Acad Sci USA 106:16592-7. doi: 10.1073/pnas.0902858106.
36. Stalling D, Westerhoff M, Hege HC. 2005. Amira: a highly interactive system for visual data analysis. The visualization handbook.
37. Tcheperegine SE, Gao X-D, Bi E. 2005. Regulation of cell polarity by interactions of Msb3 and Msb4 with Cdc42 and polarisome components. Mol Cell Biol 25:8567-80. doi: 10.1128/MCB.25.19.8567-8580.2005.