Biochemical Properties and Supramolecular Architecture of Septin Hetero-Oligomers and Septin Filaments

The Septins

Volumn , Issue , 2008, Pages 47-100

  McMurray, Michael A ^a   Thorner, Jeremy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibodies; Complexes; Homology; Mutants; Organization; Purification; Stoichiometry; Structure

Indexed keywords

EID: 84889446035     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470779705.ch3     Document Type: Chapter

References (112)

1. An, H., Morrell, J.L., Jennings, J.L. et al. (2004) Requirements of fission yeast septins for complex formation, localization, and function. Molecular Biology of the Cell, 15, 5551-64.
2. Barral, Y. and Mansuy, I.M. (2007) Septins: cellular and functional barriers of neuronal activity. Current Biology, 17, R961-63.
3. Beausoleil, S.A., Villen, J., Gerber, S.A. et al. (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nature Biotechnology, 24, 1285-92.
4. Beranova-Giorgianni, S., Zhao, Y., Desiderio, D.M. and Giorgianni, F. (2006) Phos-phoproteomic analysis of the human pituitary. Pituitary, 9, 109-20.
5. Bertin, A., McMurray, M.A., Grob, P. et al. (2008) Assembly and supramolecular organization of the septin hetero-oligomers and filaments of the yeast, Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 105, 8274-9.
6. Byers, B. and Goetsch, L. (1976a) A highly ordered ring of membrane-associated filaments in budding yeast. Journal of Cell Biology, 69, 717-21.
7. Byers, B. and Goetsch, L. (1976b) Loss of the filamentous ring in cytokinesis-defective mutants of budding yeast. Journal of Cell Biology, 70, 35.
8. Carroll, C.W., Altman, R., Schieltz, D. et al. (1998) The septins are required for the mitosis-specific activation of the Gin4 kinase. Journal of Cell Biology, 143, 709-17.
9. Casamayor, A. and Snyder, M. (2003) Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Molecular and Cellular Biology, 23, 2762-77.
10. Caviston, J.P., Longtine, M., Pringle, J.R. and Bi, E. (2003) The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Molecular Biology of the Cell, 14, 4051-66.
11. Chi, A., Huttenhower, C., Geer, L.Y. et al. (2007) Analysis of phosphorylation sites on proteins from Saccharomyces cerevisiae by electron transfer dissociation (ETD) mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America, 104, 2193-98.
12. Chu, S., DeRisi, J., Eisen, M. et al. (1998) The transcriptional program of sporulation in budding yeast. Science, 282, 699-705.
13. Cid, V.J., Adamikova, L., Cenamor, R. et al. (1998) Cell integrity and morphogenesis in a budding yeast septin mutant. Microbiology, 144, 3463-74.
14. Cid, V.J., Adamikova, L., Sanchez, M. et al. (2001) Cell cycle control of septin ring dynamics in the budding yeast. Microbiology, 147, 1437-50.
15. Dai, J., Jin, W.H., Sheng, Q.H. et al. (2007) Protein phosphorylation and expression profiling by Yin-yang multidimensional liquid chromatography (Yin-yang MDLC) mass spectrometry. Journal of Proteome Research, 6, 250-62.
16. DeMarini, D.J., Adams, A.E., Fares, H. et al. (1997) A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. Journal of Cell Biology, 139, 75-93.
17. Deng, Y., Liu, J., Zheng, Q. et al. (2006) Antiparallel four-stranded coiled coil specified by a 3-3-1 hydrophobic heptad repeat. Structure, 14, 247-55.
18. De Virgilio, C., DeMarini, D.J. and Pringle, J.R. (1996) SPR28, a sixth member of the septin gene family in Saccharomyces cerevisiae that is expressed specifically in sporulating cells. Microbiology, 142 (Pt 10), 2897-905.
19. Dobbelaere, J. and Barral, Y. (2004) Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science, 305, 393-96.
20. Dobbelaere, J., Gentry, M.S., Hallberg, R.L. and Barral, Y. (2003) Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Developmental Cell, 4, 345-57.
21. Douglas, L.M., Alvarez, F.J., McCreary, C. and Konopka, J.B. (2005) Septin function in yeast model systems and pathogenic fungi. Eukaryotic Cell, 4, 1503-12.
22. Drees, B.L., Sundin, B., Brazeau, E. et al. (2001) A protein interaction map for cell polarity development. Journal of Cell Biology, 154, 549-71.
23. Egelhofer, T.A., Villen J., McCusker D., Gygi S.P. et al. (2008) The septins function in G1 pathways that influence the pattern of cell growth in budding yeast. PLoS ONE, 3, e2022.1-e2022.14.
24. Fares, H., Goetsch, L. and Pringle, J.R. (1996) Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. Journal of Cell Biology, 132, 399-411.
25. Farkasovsky, M., Herter, P., Voss, B. and Wittinghofer, A. (2005) Nucleotide binding and filament assembly of recombinant yeast septin complexes. Biological Chemistry, 386, 643-56.
26. Field, C.M., al-Awar, O., Rosenblatt, J. et al. (1996) A purified Drosophila septin complex forms filaments and exhibits GTPase activity. Journal of Cell Biology, 133, 605-16.
27. Field, S.J., Madson, N., Kerr, M.L. et al. (2005) Ptdlns(4,5)P2 functions at the cleavage furrow during cytokinesis. Current Biology, 15, 1407-12.
28. Fields, S. and Sternglanz, R. (1994) The two-hybrid system: an assay for protein-protein interactions. Trends in Genetics, 10, 286-92.
29. Finger, F.P., Kopish, K.R. and White, J.G. (2003) A role for septins in cellular and axonal migration in C. elegans. Developmental Biology, 261, 220-34.
30. Ford, S.K. and Pringle, J.R. (1991) Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site. Developmental Genetics, 12, 281-92.
31. Frazier, J.A., Wong, M.L., Longtine, M.S. et al. (1998) Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. Journal of Cell Biology, 143, 737-49.
32. Friedlander, G., Joseph-Strauss, D., Carmi, M. et al. (2006) Modulation of the transcription regulatory program in yeast cells committed to sporulation. Genome Biology, 7, R20.
33. Garcia, W., de Araujo, A.P., Lara, F. et al. (2007) An intermediate structure in the thermal unfolding of the GTPase domain of human septin 4 (SEPT4/Bradeion-beta) forms amyloid-like filaments in vitro. Biochemistry, 46, 11101-9.
34. Garrenton, L.S. (2007) Spatial and temporal regulation of the archetypal MAPK scaffold protein, Ste5, in the budding yeast Saccharomyces cerevisiae, Ph.D. Thesis, University of California,Berkeley.
35. Gevaert, K., Goethals, M., Martens, L. et al. (2003) Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N-terminal peptides. Nature Biotechnology, 21, 566-69.
36. Gladfelter, A.S. (2006) Control of filamentous fungal cell shape by septins and formins. Nature Reviews. Microbiology, 4, 223-29.
37. Gladfelter, A.S., Bose, I., Zyla, T.R. et al. (2002) Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. Journal of Cell Biology, 156, 315-26.
38. Gladfelter, A.S., Pringle, J.R. and Lew, D.J. (2001) The septin cortex at the yeast mother-bud neck. Current Opinion in Microbiology, 4, 681-89.
39. Gruhler, A., Olsen, J.V., Mohammed, S. et al. (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Molecular and Cellular Pro-teomics, 4, 310-27.
40. Haarer, B.K. and Pringle, J.R. (1987) Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Molecular and Cellular Biology, 7, 3678-87.
41. Hall, P.A. and Russell, S.E.H. (2004) The pathobiology of the septin gene family. The Journal of Pathology, 204, 489-505.
42. Hartwell, L.H. (1971) Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Experimental Cell Research, 69, 265-76.
43. Hartwell, L.H., Culotti, J., Pringle, J.R. and Reid, B.J. (1974) Genetic control of the cell division cycle in yeast. Science, 183, 46-51.
44. Hoffert, J.D., Pisitkun, T., Wang, G. et al. (2006) Quantitative phosphoproteomics of vasopressin-sensitive renal cells: regulation of aquaporin-2 phosphorylation at two sites. Proceedings of the National Academy of Sciences of the United States of America, 103, 7159-64.
45. Hsu, S.C., Hazuka, C.D., Roth, R. et al. (1998) Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron, 20, 1111-22.
46. Hu, H., Yu, W.B., Li, S.X. et al. (2006) Crystallization and preliminary crystallo-graphic studies of human septin 1 with site-directed mutations. Acta Crystallo-graphica Section F: Structural Biology and Crystallization Communications, 62, 128-32.
47. Huang, Y.W., Surka, M.C., Reynaud, D. et al. (2006) GTP binding and hydrolysis kinetics of human septin 2. FEBS Journal, 273, 3248-60.
48. Iwase, M., Luo, J., Bi, E. and Toh, E.A. (2007) Shs1 plays separable roles in septin organization and cytokinesis in Saccharomyces cerevisiae. Genetics, 177, 215-29.
49. Iwase, M., Luo, J., Nagaraj, S. et al. (2006) Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Molecular Biology of the Cell, 17, 1110-25.
50. Joberty, G., Perlungher, R.R., Sheffield, P.J. et al. (2001) Borg proteins control septin organization and are negatively regulated by Cdc42. Nature Cell Biology, 3, 861-66.
51. John, C.M., Hite, R.K., Weirich, C.S. et al. (2007) The Caenorhabditis elegans septin complex is nonpolar. EMBO Journal, 26, 3296-307.
52. Johnson, E.S. and Blobel, G. (1999) Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. Journal of Cell Biology, 147, 981-94.
53. Joo, E., Tsang, C.W. and Trimble, W.S. (2005) Septins: traffic control at the cytokinesis intersection. Traffic, 6, 626-34.
54. Kadota, J., Yamamoto, T., Yoshiuchi, S. et al. (2004) Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Molecular Biology of the Cell, 15, 5329-45.
55. Kim, H.B., Haarer, B.K. and Pringle, J.R. (1991) Cellular morphogenesis in the Sac-charomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. Journal of Cell Biology, 112, 535-44.
56. Kinoshita, M. (2003) Assembly of mammalian septins. Journal of Biochemistry, 134, 491-96.
57. Kinoshita, M. (2006) Diversity of septin scaffolds. Current Opinion in Cell Biology, 18, 54-60.
58. Kinoshita, M., Field, C.M., Coughlin, M.L. et al. (2002) Self-and actin-template figured assembly of mammalian septins. Developmental Cell, 3, 791-802.
59. Kinoshita, A., Kinoshita, M., Akiyama, H. et al. (1998) Identification of septins in neurofibrillary tangles in Alzheimer's disease. American Journal of Pathology, 153, 1551-60.
60. Kozubowski, L., Larson, J.R. and Tatchell, K. (2005) Role of the septin ring in the asymmetric localization of proteins at the mother-bud neck in Saccharomyces cere-visiae. Molecular Biology of the Cell, 16, 3455-66.
61. Kremer, B.E., Adang, L.A. and Macara, I.G. (2007) Septins regulate actin organization and cell-cycle arrest through nuclear accumulation of NCK mediated by SOCS7. Cell, 130, 837-50.
62. Kuhlenbaumer, G., Hannibal, M.C., Nelis, E. et al. (2005) Mutations in SEPT9 cause hereditary neuralgic amyotrophy. Nature Genetics, 37, 1044-46.
63. Lee, P.R., Song, S., Ro, H.S. et al. (2002) Bn15p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Molecular and Cellular Biology, 22, 6906-20.
64. Li, X., Gerber, S.A., Rudner, A.D. et al. (2007) Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae. Journal of Proteome Research, 6, 1190-97.
65. Longtine, M.S. and Bi, E. (2003) Regulation of septin organization and function in yeast. Trends in Cell Biology, 13, 403-9.
66. Longtine, M.S., Fares, H. and Pringle, J.R. (1998) Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. Journal of Cell Biology, 143, 719-36.
67. Longtine, M.S., Theesfeld, C.L., McMillan, J.N. et al. (2000) Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Molecular and Cellular Biology, 20, 4049-61.
68. Low, C. and Macara, I.G. (2006) Structural analysis of septin 2, 6, and 7 complexes. Journal of Biological Chemistry, 281, 30697-706.
69. Lukoyanova, N., Baldwin, S.A. and Trinick, J. (2008) 3D reconstruction of mammalian septin filaments. Journal of Molecular Biology, 376, 1-7.
70. Macara, I.G., Baldarelli, R., Field, C.M. et al. (2002) Mammalian septins nomenclature. Molecular Biology of the Cell, 13, 4111-13.
71. Matsuoka, S., Ballif, B.A., Smogorzewska, A. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-66.
72. McMurray, M.A. and Thorner, J. (2008) Septin stability and recycling during dynamic structural transitions in cell division and development. Current Biology, 18, 1205-1208.
73. McMurray, M.A., Votin, V., Moellmann, M.K. and Thorner, J. (2008) Requirement for septin Cdc10 in budding yeast cell division is masked by spontaneous epigenetic suppression and results in polyploidy. Genetics, manuscript in preparation.
74. Mendoza, M., Hyman, A.A. and Glotzer, M. (2002) GTP binding induces filament assembly of a recombinant septin. Current Biology, 12, 1858-63.
75. Mino, A., Tanaka, K., Kamei, T. et al. (1998) Shs1p: a novel member of septin that interacts with spa2p, involved in polarized growth in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications, 251, 732-36.
76. Mitchison, T.J. and Field, C.M. (2002) Cytoskeleton: what does GTP do for septins? Current Biology, 12, R788-90.
77. Molina, H., Horn, D.M., Tang, N. et al. (2007) Global proteomic profiling of phos-phopeptides using electron transfer dissociation tandem mass spectrometry. Proceedings of the National Academy of Sciences of the United States of America, 104, 2199-204.
78. Mortensen, E.M., McDonald, H., Yates, J.R. and Kellogg, D.R. (2002) Cell cycle-dependent assembly of a Gin4-septin complex. Molecular Biology of the Cell, 13, 2091-105.
79. Munton, R.P., Tweedie-Cullen, R., Livingstone-Zatchej, M. et al. (2007) Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Molecular and Cellular Proteomics, 6, 283-93.
80. Neufeld, T.P. and Rubin, G.M. (1994) The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell, 77, 371-79.
81. Nguyen, T.Q., Sawa, H., Okano, H. and White, J.G. (2000) The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. Journal of Cell Science, 113 (Pt 21), 3825-37.
82. Nousiainen, M., Sillje, H.H., Sauer, G. et al. (2006) Phosphoproteome analysis of the human mitotic spindle. Proceedings of the National Academy of Sciences of the United States ofAmerica, 103, 5391-96.
83. Olsen, J.V., Blagoev, B., Gnad, F. et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell, 127, 635-48.
84. O'Shea, E.K., Rutkowski, R., Stafford, W.F. III and Kim, P.S. (1989) Preferential heterodimer formation by isolated leucine zippers from fos and jun. Science, 245, 646-48.
85. Pan, F., Malmberg, R.L. and Momany, M. (2007) Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evolutionary Biology, 7, 103.
86. Rodriguez-Escudero, I., Roelants, F.M., Thorner, J. et al. (2005) Reconstitution of the mammalian P13K/PTEN/Akt pathway in yeast. Biochemical Journal, 390, 613-23.
87. Rush, J., Moritz, A., Lee, K.A. et al. (2005) Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nature Biotechnology, 23, 94-101.
88. Saul, D., Fabian, L., Forer, A. and Brill, J.A. (2004) Continuous phosphatidylinositol metabolism is required for cleavage of crane fly spermatocytes. Journal of Cell Science, 117, 3887-96.
89. Schirmer, E.C., Homann, O.R., Kowal, A.S. and Lindquist, S. (2004) Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Molecular Biology of the Cell, 15, 2061-72.
90. Schmidt, M., Varma, A., Drgon, T. et al. (2003) Septins, under Cla4p regulation, and the chitin ring are required for neck integrity in budding yeast. Molecular Biology of the Cell, 14, 2128-41.
91. Sheffield, P.J., Oliver, C.J., Kremer, B.E. et al. (2003) Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments. Journal of Biological Chemistry, 278, 3483-88.
92. Sirajuddin, M., Farkasovsky, M., Hauer, F. et al. (2007) Structural insight into filament formation by mammalian septins. Nature, 449, 311-15.
93. Smolka, M.B., Albuquerque, C.P., Chen, S.H. and Zhou, H. (2007) Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proceedings of the National Academy of Sciences of the United States of America, 104, 10364-69.
94. Smolka, M.B., Chen, S.H., Maddox, P.S. et al. (2006) An FHA domain-mediated protein interaction network of Rad53 reveals its role in polarized cell growth. Journal of Cell Biology, 175, 743-53.
95. Spiliotis, E.T. and Nelson, W.J. (2006) Here come the septins: novel polymers that coordinate intracellular functions and organization. Journal of Cell Science, 119, 4-10.
96. Stewart, M., Kent, H.M. and McCoy, A.J. (1998) The structure of the Q69L mutant of GDP-Ran shows a major conformational change in the switch II loop that accounts for its failure to bind nuclear transport factor 2 (NTF2). Journal of Molecular Biology, 284, 1517-27.
97. Sudo, K., Ito, H., Iwamoto, I. et al. (2007) SEPT9 sequence alternations causing hereditary neuralgic amyotrophy are associated with altered interactions with SEPT4/ SEPT11 and resistance to Rho/Rhotekin-signaling. Human Mutation, 28, 1005-13.
98. Sung, H., Chul Han, K., Chul Kim, J. et al. (2005) A set of epitope-tagging integration vectors for functional analysis in Saccharomyces cerevisiae. FEMS Yeast Research, 5, 943-50.
99. Takizawa, P.A., DeRisi, J.L., Wilhelm, J.E. and Vale, R.D. (2000) Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science, 290, 341-44.
100. Tang, C.S. and Reed, S.I. (2002) Phosphorylation of the septin cdc3 in g1 by the cdc28 kinase is essential for efficient septin ring disassembly. Cell Cycle, 1, 42-49.
101. Trinidad, J.C., Specht, C.G., Thalhammer, A. et al. (2006) Comprehensive identification of phosphorylation sites in postsynaptic density preparations. Molecular and Cellular Proteomics, 5, 914-22.
102. Uetz, P., Giot, L., Cagney, G. et al. (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature, 403, 623-27.
103. Versele, M., Gullbrand, B., Shulewitz, M.J. et al. (2004) Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae. Molecular Biology of the Cell, 15, 4568-83.
104. Versele, M. and Thorner, J. (2004) Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK Cla4. Journal of Cell Biology, 164, 701-15.
105. Versele, M. and Thorner, J. (2005) Some assembly required: yeast septins provide the instruction manual. Trends in Cell Biology, 15, 414-24.
106. Vetter, I.R. and Wittinghofer, A. (2001) The guanine nucleotide-binding switch in three dimensions. Science, 294, 1299-304.
107. Vrabioiu, A.M., Gerber, S.A., Gygi, S.P. et al. (2004) The majority of the Saccharomyces cerevisiae septin complexes do not exchange guanine nucleotides. Journal of Biological Chemistry, 279, 3111-18.
108. Vrabioiu, A. and Mitchison, T.J. (2006) Structural insights into yeast septin organization from polarized fluorescence microscopy. Nature, 443, 466-69.
109. Vrabioiu, A.M. and Mitchison, T.J. (2007) Symmetry of septin hourglass and ring structures. Journal of Molecular Biology, 372, 37-49.
110. Xie, H., Surka, M., Howard, J. and Trimble, W.S. (1999) Characterization of the mammalian septin H5: distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motility and the Cytoskeleton, 43, 52-62.
111. Xue, J., Milburn, P.J., Hanna, B.T. et al. (2004) Phosphorylation of septin 3 on Ser-91 by cGMP-dependent protein kinase-I in nerve terminals. Biochemical Journal, 381, 753-60.
112. Zhang, J., Kong, C., Xie, H. et al. (1999) Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Current Biology, 9, 1458-67.