The septins

Hartwell LH: Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res. 1971, 69: 265-276. The original report describing the isolation of the septin mutants. Longtine MS, Demarini DJ, Valencik ML, Al-Awar OS, Fares H, De Virgilio C, Pringle JR: The septins, roles in cytokinesis and other processes. Curr Opin Cell Biol. 1996, 8: 106-119. 10.1016/S0955-0674(96)80054-8. The first comprehensive review on the septin family, including important previously unpublished observations and insights based on original data. Cooper JA, Kiehart DP: Septins may form a ubiquitous family of cytoskeletal filaments. J Cell Biol. 1996, 134: 1345-1348. This article and [4] are reviews of the septin family that focus on their role as components of a novel cytoskeletal system. Field CM, Kellogg D: Septins, cytoskeletal polymers or signalling GTPases?. Trends Cell Biol. 1999, 9: 387-394. 10.1016/S0962-8924(99)01632-3. See [3]. Byers B, Goetsch L: A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol. 1976, 69: 717-721. The historical discovery of the electron-dense striations at the mother-bud neck. Bourne HR, Sanders DA, McCormick F: The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991, 349: 117-127. 10.1038/349117a0. A classic review on biochemical and structural aspects of the GTP-binding protein families. Field CM, Al-Awar O, Rosenblatt J, Wong ML, Alberts BM, Mitchison TJ: A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J Cell Biol. 1996, 133: 605-616. A pioneering study of the biochemistry, ultrastructure, and self-assembly of the fly septin complex. Kinoshita M, Kumar S, Mizoguchi A, Ide C, Kinoshita A, Haraguchi T, Hiraoka Y, Noda M: Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev. 1997, 11: 1535-1547. Identification of the mouse and human Sept2 proteins and cell biological studies for their roles in cytokinesis and interphase. Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS: Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol. 1999, 9: 1458-1467. 10.1016/S0960-9822(00)80115-3. The discovery of a septin-phospholipid interaction in vitro. Sheffield PJ, Oliver CJ, Kremer BE, Sheng S, Shao Z, Macara IG: Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments. J Biol Chem. 2003, 278: 3483-3488. 10.1074/jbc.M209701200. The first reconstitution of partial and complete septin complexes using a bacterial expression system. Casamayor A, Snyder M: Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol Cell Biol. 2003, 23: 2762-2777. 10.1128/MCB.23.8.2762-2777.2003. A series of mutant studies to map septins' functional domains. Frazier JA, Wong ML, Longtine MS, Pringle JR, Mann M, Mitchison TJ, Field CM: Polymerization of purified yeast septins, evidence that organized filament arrays may not be required for septin function. J Cell Biol. 1998, 143: 737-749. 10.1083/jcb.143.3.737. An excellent combination of genetic, biochemical and ultrastructural analyses on the budding yeast septin complexes. Joberty G, Perlungher RR, Sheffield PJ, Kinoshita M, Noda M, Haystead T, Macara IG: Borg proteins control septin organisation and are negatively regulated by Cdc42. Nat Cell Biol. 2001, 3: 861-866. 10.1038/ncb1001-861. The discovery of a family of adapter proteins that link Cdc42 and the mammalian Sept2-Sept6-Sept7 complex. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ: Self- and actin-templated assembly of mammalian septins. Dev Cell. 2002, 3: 791-802. The first reconstitution of the filamentous septin complex and the higher-order structures, also demonstrating a septin-actin interaction mediated by anillin. De Virgilio C, DeMarini DJ, Pringle JR: SPR28, a sixth member of the septin gene family in Saccharomyces cerevisiae that is expressed specifically in sporulating cells. Microbiology. 1996, 142: 2897-2905. This report and [31,32] describe the identification and characterization of the sporulation-specific septins. Johnson ES, Blobel G: Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol. 1999, 147: 981-994. 10.1083/jcb.147.5.981. An original study connecting the two distinct fields of 'septinology' and 'sumology'. Kinoshita A, Noda M, Kinoshita M: Differential localization of septins in the mouse brain. J Comp Neurol. 2000, 428: 223-239. 10.1002/1096-9861(20001211)428:2<223::AID-CNE3>3.0.CO;2-M. The first ultrastructural mapping of septins in postmitotic neurons and glial cells by immuno-electron microscopy. Gladfelter AS, Pringle JR, Lew DJ: The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol. 2001, 4: 681-689. 10.1016/S1369-5274(01)00269-7. A comprehensive review of the septins and other molecules localized at the cell cortex. Mino A, Tanaka K, Kamei T, Umikawa M, Fujiwara T, Takai Y: Shs1p: a novel member of septin that interacts with Spa2p, involved in polarized growth in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 1998, 251: 732-736. 10.1006/bbrc.1998.9541. The discovery and characterization of a budding yeast septin that had not been identified in [1]. Chant J, Mischke M, Mitchell E, Herskowitz I, Pringle JR: Role of Bud3p in producing the axial budding pattern of yeast. J Cell Biol. 1995, 129: 767-778. This paper and [21] are the initial studies on the relationship between cell polarity-related proteins and the septin ring. Sanders SL, Herskowitz I: 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. 1996, 134: 413-427. See [20]. Barral Y, Mermall V, Mooseker MS, Snyder M: Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol Cell. 2000, 5: 841-851. 10.1016/S1097-2765(00)80324-X. This paper and [23] are two independent studies that established a concept of the septin ring as a diffusion barrier for bud-specific cortical proteins. Takizawa PA, DeRisi JL, Wilhelm JE, Vale RD: Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science. 2000, 290: 341-344. 10.1126/science.290.5490.341. See [22]. DeMarini DJ, Adams AE, Fares H, De Virgilio C, Valle G, Chuang JS, Pringle JR: A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J Cell Biol. 1997, 139: 75-93. 10.1083/jcb.139.1.75. An elaborate study that established the concept of the septin ring as a scaffold for the cell-wall synthesis machinery. Kusch J, Meyer A, Snyder MP, Barral Y: Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast. Genes Dev. 2002, 16: 1627-1639. 10.1101/gad.222602. A study proposing that the mitotic spindle may physically contact the septin ring for proper positioning against the cell cortex. Carroll CW, Altman R, Schieltz D, Yates JR, Kellogg D: The septins are required for the mitosis-specific activation of the Gin4 kinase. J Cell Biol. 1998, 143: 709-717. 10.1083/jcb.143.3.709. This article and [27,28] report the discoveries that the three similar kinases, Gin4p, Hsl1p and Kcc4p and the septin ring are inter-dependent and cooperatively control mitosis. Longtine MS, Fares H, Pringle JR: Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J Cell Biol. 1998, 143: 719-736. 10.1083/jcb.143.3.719. See [26]. Barral Y, Parra M, Bidlingmaier S, Snyder M: Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 1999, 13: 176-187. See [26]. Jimenez J, Cid VJ, Cenamor R, Yuste M, Molero G, Nombela C, Sanchez M: Morphogenesis beyond cytokinetic arrest in Saccharomyces cerevisiae. J Cell Biol. 1998, 143: 1617-1634. 10.1083/jcb.143.6.1617. This paper and [30] report initial studies indicating septin's functional interaction with components of the mitotic exit network. Lippincott J, Shannon KB, Shou W, Deshaies RJ, Li R: The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J Cell Sci. 2001, 114: 1379-1386. See [29]. Ozsarac N, Bhattacharyya M, Dawes IW, Clancy MJ: The SPR3 gene encodes a sporulation-specific homologue of the yeast CDC3/10/11/12 family of bud neck microfilaments and is regulated by ABFI. Gene. 1995, 164: 157-162. 10.1016/0378-1119(95)00438-C. See [15]. Fares H, Goetsch L, Pringle JR: Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J Cell Biol. 1996, 132: 399-411. See [15]. Berlin A, Paoletti A, Chang F: Mid2p stabilizes septin rings during cytokinesis in fission yeast. J Cell Biol. 2003, 160: 1083-1092. 10.1083/jcb.200212016. This paper and [34] report characterization of the septin ring and its dependence on one of the two anillin-related proteins in fission yeast. Tasto JJ, Morrell JL, Gould KL: An anillin homologue, Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J Cell Biol. 2003, 160: 1093-1103. 10.1083/jcb.200211126. See [33]. White JG, Horvitz HR, Sulston JE: Neurone differentiation in cell lineage mutants of Caenorhabditis elegans. Nature. 1982, 297: 584-587. This paper and [36] are the original reports describing genetic screening and morphology of the nematode septin mutants. Nguyen TQ, Sawa H, Okano H, White JG: 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. J Cell Sci. 2000, 113: 3825-3837. See [35]. Neufeld TP, Rubin GM: The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell. 1994, 77: 371-379. A citation classic describing identification and phenotype of the first metazoan septin mutant lacking Pnut. Fares H, Peifer M, Pringle JR: Localization and possible functions of Drosophila septins. Mol Biol Cell. 1995, 6: 1843-1859. A report on subcellular co-localization and co-immunoprecipitation of Pnut and Sep1, indicating their complex formation in cytokinesis and embryonic development. Adam JC, Pringle JR, Peifer M: Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell. 2000, 11: 3123-3135. A genetic and morphological dataset indicating functional diversity and redundancy of the fly septin system. Hime GR, Brill JA, Fuller MT: Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci. 1996, 109: 2779-2788. A report on similarities and differences in the ring canals between male and female germ cells in Drosophila. Robinson DN, Cooley L: Genetic analysis of the actin cytoskeleton in the Drosophila ovary. Annu Rev Cell Dev Biol. 1997, 13: 147-170. 10.1146/annurev.cellbio.13.1.147. An insightful review on the ring canals of Drosophila. Hsu SC, Hazuka CD, Roth R, Foletti DL, Heuser J, Scheller RH: Subunit composition, protein interactions, and structures of the mammalian brain Sec6/8 complex and septin filaments. Neuron. 1998, 20: 1111-1122. A report on copurification of the mammalian septin complexes with the Sec6/8 complex from the rat brain. Their direct interaction has not been demonstrated. Xie H, Surka M, Howard J, Trimble WS: Characterization of the mammalian septin H5: distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motil Cytoskeleton. 1999, 43: 52-62. 10.1002/(SICI)1097-0169(1999)43:1<52::AID-CM6>3.3.CO;2-X. A careful study showing the differential subcellular localization of Sept2 and Sept4. Beites CL, Xie H, Bowser R, Trimble WS: The septin CDCrel-1 binds syntaxin and inhibits exocytosis. Nat Neurosci. 1999, 2: 434-439. 10.1038/8100. The discovery of a physical and functional interaction between the general secretory machinery and Sept5. Surka MC, Tsang CW, Trimble WS: The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol Biol Cell. 2002, 13: 3532-3545. 10.1091/mbc.E02-01-0042. This paper and [46] are two careful studies demonstrating a Sept9-microtubule interaction and examining its significance in mitosis. Nagata KI, Kawajiri A, Matsui S, Takagishi M, Shiromizu T, Saitoh N, Izawa I, Kiyono T, Itoh TJ, Hotani H, Inagaki M: Filament formation of MSF-A, a mammalian septin, in mammary epithelial cells depends on interactions with microtubules. J Biol Chem. 2003, 278: 18538-18543. 10.1074/jbc.M205246200. See [45]. Peng XR, Jia Z, Zhang Y, Ware J, Trimble WS: The septin CDCrel-1 is dispensable for normal development and neurotransmitter release. Mol Cell Biol. 2002, 22: 378-387. 10.1128/MCB.22.1.378-387.2002. This paper and [48] are the first attempts to genetically disrupt a mammalian septin that is mainly expressed in the brain and blood platelets. The absence of Sept5 affected platelet functions but was tolerated in the brain. Dent J, Kato K, Peng XR, Martinez C, Cattaneo M, Poujol C, Nurden P, Nurden A, Trimble WS, Ware J: A prototypic platelet septin and its participation in secretion. Proc Natl Acad Sci USA. 2002, 99: 3064-3069. 10.1073/pnas.052715199. See [47]. Dobbelaere J, Gentry MS, Hallberg RL, Barral Y: Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell. 2003, 4: 345-357. A breakthrough demonstrating the two kinases and a phosphatase subunit that control the turnover of the septin ring. Larisch S, Yi Y, Lotan R, Kerner H, Eimerl S, Tony Parks W, Gottfried Y, Birkey Reffey S, de Caestecker MP, Danielpour D, et al: A novel mitochondrial septin-like protein, ARTS, mediates apoptosis dependent on its P-loop motif. Nat Cell Biol. 2000, 2: 915-921. 10.1038/35046566. The discovery of a splice variant of Sept4 with an incomplete set of GTPase motifs. Osaka M, Rowley JD, Zeleznik-Le NJ: MSF (MLL septin-like fusion), a fusion partner gene of MLL, in a therapy-related acute myeloid leukemia with a t(11;17)(q23;q25). Proc Natl Acad Sci USA. 1999, 96: 6428-6433. 10.1073/pnas.96.11.6428. One of the earliest reports on the Sept9-MLL gene fusion in human malignancies. Montagna C, Lyu MS, Hunter K, Lukes L, Lowther W, Reppert T, Hissong B, Weaver Z, Ried T: The Septin 9 (MSF) gene is amplified and overexpressed in mouse mammary gland adenocarcinomas and human breast cancer cell lines. Cancer Res. 2003, 63: 2179-2187. A demonstration of cancer-associated amplification and overexpression of the Sept9 gene in two species. Kinoshita A, Kinoshita M, Akiyama H, Tomimoto H, Kumar S, Noda M, Kimura J: Identification of septins in the neurofibrillary tangles in Alzheimer's disease. Am J Pathol. 1998, 153: 1551-1560. A serendipitous discovery of a subset of septins in the human pathology. Ihara M, Tomimoto H, Kitayama H, Morioka Y, Akiguchi I, Shibasaki H, Noda M, Kinoshita M: Association of the cytoskeletal GTP-binding protein Sept4/H5 with cytoplasmic inclusions found in Parkinson's disease and other synucleinopathies. J Biol Chem. 2003, 278: 24095-24102. 10.1074/jbc.M301352200. Histopathological and biochemical analyses of the interaction between Sept4 and α-synuclein. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM: Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci USA. 2000, 97: 13354-13359. 10.1073/pnas.240347797. Identification of Sept5 as a substrate of an E3 ligase, parkin. Lupas A, Van Dyke M, Stock J: Predicting coiled coils from protein sequences. Science. 1991, 252: 1162-1164. A program for predicting coiled-coil-forming regions (available at [57]). COILS - prediction of coiled coil regions in proteins. See [56]., [http://www.ch.embnet.org/software/COILS_form.html] Macara IG, Baldarelli R, Field CM, Glotzer M, Hayashi Y, Hsu SC, Kennedy MB, Kinoshita M, Longtine M, Low C, et al: Mammalian septins nomenclature. Mol Biol Cell. 2002, 13: 4111-4113. 10.1091/mbc.E02-07-0438. The nightmarish confusion of the mammalian septins nomenclature becomes history. Phylip. A free package of programs for inferring phylogenies., [http://evolution.genetics.washington.edu/phylip.html]