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The pathobiology of the septin gene family
Open accessAbstract
Septins are an evolutionarily conserved group of GTP‐binding and filament‐forming proteins that belong to the large superclass of P‐loop GTPases. While originally discovered in yeast as cell division cycle mutants with cytokinesis defects, they are now known to have diverse cellular roles which include polarity determination, cytoskeletal reorganization, membrane dynamics, vesicle trafficking, and exocytosis. Septin proteins form homo‐ and hetero‐oligomeric polymers which can assemble into higher‐order filaments. They are also known to interact with components of the cytoskeleton, ie actin and tubulin. The precise role of GTP binding is not clear but a current model suggests that it is associated with conformational changes which alter binding to other proteins. There are at least 12 human septin genes, and although information on expression patterns is limited, most undergo complex alternative splicing with some degree of tissue specificity. Nevertheless, an increasing body of data implicates the septin family in the pathogenesis of diverse disease states including neoplasia, neurodegenerative conditions, and infections. Here the known biochemical properties of mammalian septins are reviewed in the light of the data from yeast and other model organisms. The data implicating septins in human disease are considered and a model linking these data is proposed. It is posited that septins can act as regulatable scaffolds where the stoichiometry of septin associations, modifications, GTP status, and the interactions with other proteins allow the regulation of key cellular processes including polarity determination. Derangements of such septin scaffolds thus explain the role of septins in disease states. Copyright © 2004 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
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Holly, S. P., & BLUMER, K. J. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.4.845 · Cited by 110
Regulation of Cdc42‐mediated morphological effects: a novel function for p53
Gadéa, G., Lapasset, L., Gauthier‐Rouvière, C., & Roux, P. (2002) · The EMBO Journal · doi:10.1093/emboj/21.10.2373 · Cited by 109
Trimble, W. S. (1999) · The Journal of Membrane Biology · doi:10.1007/s002329900519 · Cited by 108
Polo, S., Pece, S., & Fiore, P. P. D. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.02.003 · Cited by 107
Biochemical and cell biological characterization of a mammalian septin, Sept11
Hanai, N., Nagata, K., Kawajiri, A., Shiromizu, T., Saitoh, N., Hasegawa, Y., Murakami, S., & Inagaki, M. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.05.030 · Cited by 107
Endocytosis proteins and cancer: a potential link?
Floyd, S., & Camilli, P. V. D. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(98)01316-6 · Cited by 102
Wightman, R., Bates, S., Amornrrattanapan, P., & Sudbery, P. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307176 · Cited by 100
Russell, S. E. H., McIlhatton, M. A., Burrows, J. F., Donaghy, P. G., Chanduloy, S., Petty, E. M., Kalikin, L. M., Church, S. W., McIlroy, S. P., Harkin, D. P., et al. (2000) · PubMed · Cited by 99
Self-citationCandida albicans Septin Mutants Are Defective for Invasive Growth and Virulence
Warenda, A. J., Kauffman, S., Sherrill, T. P., Becker, J. M., & Konopka, J. B. (2003) · Infection and Immunity · doi:10.1128/iai.71.7.4045-4051.2003 · Cited by 99
A role for septins in cellular and axonal migration in C. elegans
Finger, F. P., Kopish, K. R., & White, J. G. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00296-3 · Cited by 98
Septins Have a Dual Role in Controlling Mitotic Exit in Budding Yeast
Castillon, G. A., Adames, N. R., Rosello, C., Seidel, H. S., Longtine, M. S., Cooper, J. A., & Heil‐Chapdelaine, R. A. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00247-1 · Cited by 98
Xie, H., Surka, M. C., Howard, J., & Trimble, W. S. (1999) · Cell Motility and the Cytoskeleton · doi:10.1002/(sici)1097-0169(1999)43:1<52::aid-cm6>3.0.co;2-5 · Cited by 98
Vega, I. E., & Hsu, S. C. (2003) · Neuroreport · doi:10.1097/00001756-200301200-00006 · Cited by 94
Syntaxins 13 and 7 Function at Distinct Steps During Phagocytosis
Collins, R. F., Schreiber, A. D., Grinstein, S., et al. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.6.3250 · Cited by 93
Kalikin, L. M., Sims, H. L., & Petty, E. M. (2000) · Genomics · doi:10.1006/geno.1999.6077 · Cited by 90
Altered expression of the septin gene, SEPT9 , in ovarian neoplasia
Burrows, J. F., Chanduloy, S., McIlhatton, M. A., Nagar, H., Yeates, K., Donaghy, P. G., Price, J., Godwin, A. K., Johnston, P. G., & Russell, S. H. (2003) · The Journal of Pathology · doi:10.1002/path.1484 · Cited by 90
Self-citationThe Majority of the Saccharomyces cerevisiae Septin Complexes Do Not Exchange Guanine Nucleotides
Vrabioiu, A. M., Gerber, S. A., Gygi, S. P., Field, C. M., & Mitchison, T. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310941200 · Cited by 89
Distinct protein patterns associated with Listeria monocytogenes InlA- or InlB-phagosomes
Pizarro‐Cerdá, J., Jonquières, R., Gouin, E., Vandekerckhove, J. S., Garin, J., & Cossart, P. (2002) · Cellular Microbiology · doi:10.1046/j.1462-5822.2002.00169.x · Cited by 88
Kato, K., Martínez, C., Russell, S., Nurden, P., Nurden, A. T., Fiering, S., & Ware, J. L. (2004) · Blood · doi:10.1182/blood-2004-03-1127 · Cited by 85
Self-citationRole of the cytoskeleton in signaling networks
Forgács, G., Yook, S., Janmey, P. A., Jeong, H., & Burd, C. G. (2004) · Journal of Cell Science · doi:10.1242/jcs.01122 · Cited by 84
Septins may form a ubiquitous family of cytoskeletal filaments.
Cooper, J. A., & Kiehart, D. P. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.134.6.1345 · Cited by 84
Septin Scaffolds and Cleavage Planes in Saccharomyces
Chant, J. (1996) · Cell · doi:10.1016/s0092-8674(00)80972-1 · Cited by 83
Advances in Cytokinesis Research. Roles of Septins in the Mammalian Cytokinesis Machinery.
Kinoshita, M., & Noda, M. (2001) · Cell Structure and Function · doi:10.1247/csf.26.667 · Cited by 79
Lee, P. R., Song, S., Ro, H., Park, C. J., Lippincott, J., Li, R., Pringle, J. R., VIRGILIO, C. D., Longtine, M. S., & Lee, K. S. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.19.6906-6920.2002 · Cited by 78
Cytoskeletal remodeling in lymphocyte activation
Miletic, A. V., Swat, M., Fujikawa, K., & Swat, W. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(03)00054-2 · Cited by 73
Polarity establishment in yeast
Irazoqui, J. E., & Lew, D. J. (2004) · Journal of Cell Science · doi:10.1242/jcs.00953 · Cited by 70
Tang, C., & Reed, S. I. (2002) · Cell Cycle · doi:10.4161/cc.1.1.99 · Cited by 68
Mammalian septin Sept2 modulates the activity of GLAST, a glutamate transporter in astrocytes
Kinoshita, N., Kimura, K., Matsumoto, N., Watanabe, M., Fukaya, M., & Idé, C. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00696.x · Cited by 67
Phosphorylation of a New Brain-specific Septin, G-septin, by cGMP-dependent Protein Kinase
Xue, J., Wang, X., Malladi, C. S., Kinoshita, M., Milburn, P. J., Lengyel, I., Rostas, J. A. P., & Robinson, P. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.14.10047 · Cited by 66
Analysis of Mammalian Septin Expression in Human Malignant Brain Tumors
Kim, D.-S., Hubbard, S.-L., Peraud, A., Salhia, B., Sakai, K., & Rutka, J. T. (2004) · Neoplasia · doi:10.1593/neo.03310 · Cited by 65
Kadlec, L., & Pendergast, A. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12390 · Cited by 58
Aberrant protein expression in cerebral cortex of fetus with Down syndrome
Engidawork, E., Gulesserian, T., Fountoulakis, M., & Lübec, G. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00605-5 · Cited by 52
Localization of a novel septin protein, hCDCrel-1, in neurons of human brain
Caltagarone, J., Rhodes, J. L., Honer, W. G., & Bowser, R. P. (1998) · Neuroreport · doi:10.1097/00001756-199808240-00042 · Cited by 50
Cdk5 in Neuroskeletal Dynamics
Smith, D. S. (2003) · Neurosignals · doi:10.1159/000074626 · Cited by 45
Isolation and characterization of sixteen novel p53 response genes
Kostic, C., & Shaw, P. H. (2000) · Oncogene · doi:10.1038/sj.onc.1203747 · Cited by 43
Sørensen, A. B., Lund, A. H., Ethelberg, S., et al. (2000) · Journal of Virology · doi:10.1128/jvi.74.5.2161-2168.2000 · Cited by 41
The novel human platelet septin SEPT8 is an interaction partner of SEPT4
Bläser, S., Horn, J., Würmell, P., Bauer, H., Strümpell, S., Nurden, P., Pagenstecher, A., Busse, A., Wunderle, D., Hainmann, I., et al. (2004) · Thrombosis and Haemostasis · doi:10.1160/th03-09-0578 · Cited by 40
Expression of Nedd5, A Mammalian Septin, in Human Brain Tumors
Sakai, K., Kurimoto, M., Tsugu, A., Hubbard, S. L., Trimble, W. S., & Rutka, J. T. (2002) · Journal of Neuro-Oncology · doi:10.1023/a:1015721801075 · Cited by 34
Cytoskeleton: What Does GTP Do for Septins?
Mitchison, T. J., & Field, C. M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01295-2 · Cited by 32
Membrane Dynamics and the Regulation of Epithelial Cell Polarity
van der Wouden, J. M., Maier, O., van IJzendoorn, S. C. D., & Hoekstra, D. (2003) · International review of cytology · doi:10.1016/s0074-7696(03)01003-9 · Cited by 31
Cooper, J. A., & Titus, M. A. (2003) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2003.11.014 · Cited by 29
Bläser, S., Jersch, K., Hainmann, I., Zieger, W., Wunderle, D., Busse, A., & Zieger, B. (2003) · Gene · doi:10.1016/s0378-1119(03)00635-8 · Cited by 29
She, Y., Huang, Y., Zhang, L., & Trimble, W. S. (2004) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.1453 · Cited by 26
Fusion ofMLL andMSF in Adult De Novo Acute Myelomonocytic Leukemia (M4) with T(11;17)(Q23;Q25)
Yamamoto, K., Shibata, F., Yamaguchi, M., & Miura, O. (2002) · International Journal of Hematology · doi:10.1007/bf02982114 · Cited by 22
Finger, F. P. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00371-4 · Cited by 22
[23] Purification and assay of a septin complex from Drosophila embryos
Oegema, K., Desai, A. B., Wong, M. L., Mitchison, T. J., & Field, C. M. (1998) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(98)98025-9 · Cited by 21
Moffat, J., & Andrews, B. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00301-0 · Cited by 16
MDMA (Ecstasy) controls in concert a group of genes involved in GABA neurotransmission
Simantov, R., & Peng, W. (2004) · FEBS Letters · doi:10.1016/s0014-5793(04)00256-x · Cited by 16
Cited by
Structural insight into filament formation by mammalian septins
Sirajuddin, M., Farkasovsky, M., Hauer, F., Kühlmann, D., Macara, I. G., Weyand, M., Stark, H., & Wittinghofer, A. (2007) · Nature · doi:10.1038/nature06052 · Cited by 481
A Mitotic Septin Scaffold Required for Mammalian Chromosome Congression and Segregation
Spiliotis, E. T., Kinoshita, M., & Nelson, W. J. (2005) · Science · doi:10.1126/science.1106823 · Cited by 256
Distinct roles of septins in cytokinesis: SEPT9 mediates midbody abscission
Estey, M. P., Di Ciano-Oliveira, C., Froese, C. D., Bejide, M. T., & Trimble, W. S. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201006031 · Cited by 231
Tooley, A. J., Gilden, J., Jacobelli, J., Beemiller, P., Trimble, W. S., Kinoshita, M., & Krummel, M. F. (2009) · Nature Cell Biology · doi:10.1038/ncb1808 · Cited by 189
“Since septin expression is frequently altered in human and mouse tumors22,36,37 and Sept2 (Diff6) was first identified as an over-expressed gene in a tumor line selected for metastasis38, we speculate that destabilization of the cell cortex due to stoichiometric changes in septin complexes may…”
SEPT12 mutations cause male infertility with defective sperm annulus
Kuo, Y.-C., Lin, Y.-H., Chen, H.-I., Wang, Y.-Y., Chiou, Y.-W., Lin, H.-H., Pan, H.-A., Wu, C.-M., Su, S.-M., Hsu, C.-C., et al. (2012) · Human Mutation · doi:10.1002/humu.22028 · Cited by 128
Metadata
- Authors
- Hall, P. A., & Russell, S. H.
- Venue
- The Journal of Pathology
- Publisher
- Wiley
- Published
- 2004-10-19
- Volume
- 204
- Issue
- 4
- Pages
- 489-505
- ISSN
- 0022-3417 (ISSN-L)
- 1096-9896
- OpenAlex
- W2083555181
- Cited by
- 323
- References
- 159
- FWCI
- 6.01
- Type
- journal article
- Language
- en
- Open access
- bronze
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.