Analysis of septins across kingdoms reveals orthology and new motifs

Springer Science and Business Media LLC - Tập 7 - Trang 1-17 - 2007
Fangfang Pan1, Russell L Malmberg1, Michelle Momany1
1Plant Biology Department, University of Georgia, Athens, USA

Tóm tắt

Septins are cytoskeletal GTPase proteins first discovered in the fungus Saccharomyces cerevisiae where they organize the septum and link nuclear division with cell division. More recently septins have been found in animals where they are important in processes ranging from actin and microtubule organization to embryonic patterning and where defects in septins have been implicated in human disease. Previous studies suggested that many animal septins fell into independent evolutionary groups, confounding cross-kingdom comparison. In the current work, we identified 162 septins from fungi, microsporidia and animals and analyzed their phylogenetic relationships. There was support for five groups of septins with orthology between kingdoms. Group 1 (which includes S. cerevisiae Cdc10p and human Sept9) and Group 2 (which includes S. cerevisiae Cdc3p and human Sept7) contain sequences from fungi and animals. Group 3 (which includes S. cerevisiae Cdc11p) and Group 4 (which includes S. cerevisiae Cdc12p) contain sequences from fungi and microsporidia. Group 5 (which includes Aspergillus nidulans AspE) contains sequences from filamentous fungi. We suggest a modified nomenclature based on these phylogenetic relationships. Comparative sequence alignments revealed septin derivatives of already known G1, G3 and G4 GTPase motifs, four new motifs from two to twelve amino acids long and six conserved single amino acid positions. One of these new motifs is septin-specific and several are group specific. Our studies provide an evolutionary history for this important family of proteins and a framework and consistent nomenclature for comparison of septin orthologs across kingdoms.

Tài liệu tham khảo

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 (3): 399-411. 10.1083/jcb.132.3.399.

Longtine MS, Bi E: Regulation of septin organization and function in yeast. Trends Cell Biol. 2003, 13 (8): 403-409. 10.1016/S0962-8924(03)00151-X.

Douglas LM, Alvarez FJ, McCreary C, Konopka JB: Septin Function in Yeast Model Systems and Pathogenic Fungi. Eukaryotic Cell. 2005, 4 (9): 1503-1512. 10.1128/EC.4.9.1503-1512.2005.

Hall PA, Russell SE: The pathobiology of the septin gene family. J Pathol. 2004, 204 (4): 489-505. 10.1002/path.1654.

Spiliotis ET, Kinoshita M, Nelson WJ: A mitotic septin scaffold required for Mammalian chromosome congression and segregation. Science. 2005, 307 (5716): 1781-1785. 10.1126/science.1106823.

Kinoshita M: Diversity of septin scaffolds. Curr Opin Cell Biol. 2006, 18 (1): 54-60. 10.1016/j.ceb.2005.12.005.

Bourne HR, Sanders DA, McCormick F: The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991, 349 (6305): 117-127. 10.1038/349117a0.

Saraste M, Sibbald PR, Wittinghofer A: The P-loop--a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 1990, 15 (11): 430-434. 10.1016/0968-0004(90)90281-F.

Vetter IR, Wittinghofer A: Nucleoside triphosphate-binding proteins: different scaffolds to achieve phosphoryl transfer. Q Rev Biophys. 1999, 32 (1): 1-56. 10.1017/S0033583599003480.

Dever TE, Glynias MJ, Merrick WC: GTP-binding domain: three consensus sequence elements with distinct spacing. Proceedings of the National Academy of Sciences of the United States of America. 1987, 84 (7): 1814-1818. 10.1073/pnas.84.7.1814.

Field CM, Kellogg D: Septins: cytoskeletal polymers or signalling GTPases?. Trends Cell Biol. 1999, 9 (10): 387-394. 10.1016/S0962-8924(99)01632-3.

Field CM, al-Awar O, Rosenblatt J, Wong ML, Alberts B, Mitchison TJ: A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J Cell Biol. 1996, 133 (3): 605-616. 10.1083/jcb.133.3.605.

Mendoza M, Hyman AA, Glotzer M: GTP binding induces filament assembly of a recombinant septin. Curr Biol. 2002, 12 (21): 1858-1863. 10.1016/S0960-9822(02)01258-7.

Vrabioiu AM, Gerber SA, Gygi SP, Field CM, Mitchison TJ: The majority of the Saccharomyces cerevisiae septin complexes do not exchange guanine nucleotides. J Biol Chem. 2004, 279 (4): 3111-3118. 10.1074/jbc.M310941200.

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 (8): 2762-2777. 10.1128/MCB.23.8.2762-2777.2003.

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 (24): 1458-1467. 10.1016/S0960-9822(00)80115-3.

Versele M, Gullbrand B, Shulewitz MJ, Cid VJ, Bahmanyar S, Chen RE, Barth P, Alber T, Thorner J: Protein-protein interactions governing septin heteropentamer assembly and septin filament organization in Saccharomyces cerevisiae. Mol Biol Cell. 2004, 15 (10): 4568-4583. 10.1091/mbc.E04-04-0330.

An H, Morrell JL, Jennings JL, Link AJ, Gould KL: Requirements of fission yeast septins for complex formation, localization, and function. Mol Biol Cell. 2004, 15 (12): 5551-5564. 10.1091/mbc.E04-07-0640.

Versele M, Thorner J: Some assembly required: yeast septins provide the instruction manual. Trends in Cell Biology. 2005, 15 (8): 414-424. 10.1016/j.tcb.2005.06.007.

Momany M, Zhao J, Lindsey R, Westfall PJ: Characterization of the Aspergillus nidulans septin (asp) gene family. Genetics. 2001, 157 (3): 969-977.

Schultz J, Milpetz F, Bork P, Ponting CP: SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences of the United States of America. 1998, 95 (11): 5857-5864. 10.1073/pnas.95.11.5857.

Boyce KJ, Chang H, D'Souza CA, Kronstad JW: An Ustilago maydis septin is required for filamentous growth in culture and for full symptom development on maize. Eukaryot Cell. 2005, 4 (12): 2044-2056. 10.1128/EC.4.12.2044-2056.2005.

Hall PA, Jung K, Hillan KJ, Russell SE: Expression profiling the human septin gene family. J Pathol. 2005, 206 (3): 269-278. 10.1002/path.1789.

Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19 (12): 1572-1574. 10.1093/bioinformatics/btg180.

Sanderson MJ, Wojciechowski MF: Improved bootstrap confidence limits in large-scale phylogenies, with an example from Neo-Astragalus (Leguminosae). Syst Biol. 2000, 49 (4): 671-685. 10.1080/106351500750049761.

Soltis PS, Soltis DE: Applying the Bootstrap in Phylogeny Reconstruction. Statistical Science. 2003, Institute of Mathematical Statistics, 18 (2): 256-267. 10.1214/ss/1063994980.

Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. Genome Res. 2004, 14 (6): 1188-1190. 10.1101/gr.849004.

Schneider TD, Stephens RM: Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990, 18 (20): 6097-6100. 10.1093/nar/18.20.6097.

Mason JM, Arndt KM: Coiled coil domains: stability, specificity, and biological implications. Chembiochem. 2004, 5 (2): 170-176. 10.1002/cbic.200300781.

Newman JR, Wolf E, Kim PS: A computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America. 2000, 97 (24): 13203-13208. 10.1073/pnas.97.24.13203.

Lupas A, Van Dyke M, Stock J: Predicting coiled coils from protein sequences. Science. 1991, 252 (5010): 1162-1164. 10.1126/science.252.5009.1162.

McIlhatton MA, Burrows JF, Donaghy PG, Chanduloy S, Johnston PG, Russell SE: Genomic organization, complex splicing pattern and expression of a human septin gene on chromosome 17q25.3. Oncogene. 2001, 20 (41): 5930-5939. 10.1038/sj.onc.1204752.

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25 (17): 3389-3402. 10.1093/nar/25.17.3389.

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25 (24): 4876-4882. 10.1093/nar/25.24.4876.

BioEdit Sequence Alignment Editor for Windows 95/98/NT/XP. [http://www.mbio.ncsu.edu/BioEdit/bioedit.html]

Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003, 52 (5): 696-704. 10.1080/10635150390235520.

Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P: SMART 4.0: towards genomic data integration. Nucleic Acids Res. 2004, 32 (Database issue): D142-4. 10.1093/nar/gkh088.

Marchler-Bauer A, Bryant SH: CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004, 32 (Web Server issue): W327-31. 10.1093/nar/gkh454.

McGuffin LJ, Bryson K, Jones DT: The PSIPRED protein structure prediction server. Bioinformatics. 2000, 16 (4): 404-405. 10.1093/bioinformatics/16.4.404.

Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B, de Rosa R: The new animal phylogeny: reliability and implications. Proceedings of the National Academy of Sciences of the United States of America. 2000, 97 (9): 4453-4456. 10.1073/pnas.97.9.4453.