Advertisement
Journal Article
Novel roles for mammalian septins: from vesicle trafficking to oncogenesis
B. Kartmann, D. Roth
Journal of Cell Science 2001 114: 839-844;

Summary

In recent years a convergence of various aspects of cell biology has become apparent, and yet investigators are only beginning to grasp the underlying unifying mechanisms. Among the proteins that participate in diverse aspects of cell biology are the septins. These are a group of novel GTPase proteins that are broadly distributed in many eukaryotes except plants. Although septins were originally identified as a protein family involved in cytokinesis in yeast, recent advances in the field have now ascribed additional functions to these proteins. In particular, the number of known mammalian septin family members has increased dramatically as more data has become available through genome analyses. We suggest a classification for the mammalian septins based on the sequence homologies in their highly divergent N- and C-termini. Recent work suggests novel functions for septins in vesicle trafficking, oncogenesis and compartmentalization of the plasma membrane. Given the ability of the septins to bind GTP and phosphatidylinositol 4,5-bisphosphate in a mutually exclusive manner, these proteins might be crucial elements for the spatial and/or temporal control of diverse cellular functions. As the functions of the septins become unraveled, our understanding of seemingly different cellular processes may move a step further.

REFERENCES

    1. Barral, Y.,
    2. Parra, M.,
    3. Bidlingmaier, S. and
    4. Snyder, M.
    (1999). Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev 13, 176–187
    OpenUrlAbstract/FREE Full Text
    1. Barral, Y.,
    2. Mermall, V.,
    3. Mooseker, M. S. and
    4. Snyder, M.
    (2000). Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol. Cell 5, 841–851
    OpenUrlCrossRefPubMedWeb of Science
    1. Byers, B. and
    2. Goetsch, L.
    (1976). A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol 69, 717–721
    OpenUrlAbstract/FREE Full Text
    1. Caltagarone, J.,
    2. Rhodes, J.,
    3. Honer, W. G. and
    4. Bowser, R.
    (1998). Localization of a novel septin protein, hCDCrel-1, in neurons of human brain. NeuroReport 9, 2907–2912
    OpenUrlPubMedWeb of Science
    1. Corral, J.,
    2. Lavenir, I.,
    3. Impey, H.,
    4. Warren, A. J.,
    5. Forster, A.,
    6. Larson, T. A.,
    7. Bell, S.,
    8. McKenzie, A. N.,
    9. King, G. and
    10. Rabbitts, T. H.
    (1996). An MLL-AF9 fusion gene made by homologous recombination causes acute leukemia in chermic mice: a method to create fusion oncogenes. Cell 85, 853–861
    OpenUrlCrossRefPubMedWeb of Science
    1. Cooper, J. A. and
    2. Kiehart, D. P.
    (1996). Septins may form a ubiquitous family of cytoskeletal filaments. J. Cell Biol 134, 1345–1348
    OpenUrlFREE Full Text
    1. Czech, M. P.
    (2000). PtdIns(4,5)P2and PtdIns(4,5)P3: complex roles at the cell surface. Cell 100, 603–606
    OpenUrlCrossRefPubMedWeb of Science
    1. DeMarini, D. J.,
    2. Adams, A. E.,
    3. Fares, H.,
    4. De Virgilio, C.,
    5. Valle, G.,
    6. Chuang, J. S. and
    7. Pringle, J. R.
    (1997). A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol 139, 75–93
    OpenUrlAbstract/FREE Full Text
    1. DeVirgilio, C.,
    2. DeMarini, D. J. and
    3. 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, 2897–2905
    OpenUrlAbstract/FREE Full Text
    1. Fares, H.,
    2. Peifer, M. and
    3. Pringle, J. R.
    (1995). Localization and possible functions of Drosophila septins. Mol. Biol. Cell 6, 1843–1849
    OpenUrlAbstract/FREE Full Text
    1. Fares, H.,
    2. Goetsch, L. and
    3. Pringle, J. R.
    (1996). Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. J. Cell Biol 132, 399–401
    OpenUrlAbstract/FREE Full Text
    1. Felix, C. A.,
    2. Hosler, M. R.,
    3. Winick, N. J.,
    4. Masterson, M.,
    5. Wilson, A. E. and
    6. Lange, B. J.
    (1995). ALL-1 gene rearrangements in DNA topoisomerase II inhibitor-related leukemia in children. Blood 85, 3250–3256
    OpenUrlAbstract/FREE Full Text
    1. Field, C. M.,
    2. Al-Awar, O.,
    3. Rosenblatt, J.,
    4. Wong, M. L.,
    5. Alberts, B. and
    6. Mitchison, T. J.
    (1996). A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J. Cell Biol 133, 605–616
    OpenUrlAbstract/FREE Full Text
    1. Finger, F. P. and
    2. Novick, P.
    (1998). Spatial regulation of exocytosis: Lessons from yeast. J. Cell Biol 142, 609–612
    OpenUrlFREE Full Text
    1. Flescher, E. G.,
    2. Madden, K. and
    3. Snyder, M.
    (1993). Components required for cytokinesis are important for bud site selection in yeast. J. Cell Biol 122, 373–386
    OpenUrlAbstract/FREE Full Text
    1. Ford, S. K. and
    2. 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. Dev. Genet 12, 281–292
    OpenUrlCrossRefPubMedWeb of Science
    1. Frazier, J. A.,
    2. Wong, M. L.,
    3. Longtine, M. S.,
    4. Pringle, J. R.,
    5. Mann, M.,
    6. Mitchison, T. J. and
    7. Field, C.
    (1998). Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J. Cell Biol 143, 737–749
    OpenUrlAbstract/FREE Full Text
    1. Fung, E. T. and
    2. Scheller, R. H.
    (1999). Identification of a novel alternatively spliced septin. FEBS Lett 451, 203–208
    OpenUrlCrossRefPubMed
    1. Haarer, B. K. and
    2. Pringle, J. R.
    (1987). Immunofluorescence localization of the Saccharomyces cerevisiae cell cycle: localization of CDC3 gene product and the timing of events at the budding site. J. Cell Biol 7, 3678–3687
    OpenUrl
    1. Hartwell, L. H.
    (1971). Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res 69, 265–276
    OpenUrlCrossRefPubMedWeb of Science
    1. Hazuka, C. D.,
    2. Foletti, D. L.,
    3. Hsu, S. C.,
    4. Kee, Y.,
    5. Hopf, F. W. and
    6. Scheller, R. H.
    (1999). The sec6/8 complex is located at the neurite outgrowth and axonal synapse-assembly domains. J. Neurosci 19, 1324–1334
    OpenUrlAbstract/FREE Full Text
    1. Hsu, S. C.,
    2. Ting, A. E.,
    3. Hazuka, C. D.,
    4. Davanger, S.,
    5. Kenny, J. W.,
    6. Kee, Y. and
    7. Scheller, R. H.
    (1996). The mammalian brain rsec6/8 complex. Neuron 17, 1209–1219
    OpenUrlCrossRefPubMedWeb of Science
    1. Hsu, S. C.,
    2. Hazuka, C. D.,
    3. Roth, R.,
    4. Foletti, D. L.,
    5. Heuser, J. and
    6. Scheller, R. H.
    (1998). Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron 20, 1111–1122
    OpenUrlCrossRefPubMedWeb of Science
    1. Kalikin, L. M.,
    2. Sims, H. L. and
    3. Petty, E. M.
    (2000). Genomic and expression analyses of alternatively spliced transcripts of the MLL septin-like fusion gene (MSF) that map to a 17q25 region of loss in breast and ovarian tumors. Genomics 63, 165–172
    OpenUrlCrossRefPubMed
    1. Kim, H. B.,
    2. Haarer, B. K. and
    3. Pringle, J. R.
    (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, 535–544
    OpenUrlAbstract/FREE Full Text
    1. Kinoshita, M.,
    2. Kumar, S.,
    3. Mizoguchi, A.,
    4. Ide, C.,
    5. Kinoshita, A.,
    6. Haraguchi, T.,
    7. Hiraoka, Y. and
    8. Noda, M.
    (1997). Nedd 5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev 11, 1535–1547
    OpenUrlAbstract/FREE Full Text
    1. Longtine, M. S.,
    2. DeMarini, D. J.,
    3. Valencik, M. L.,
    4. Al-Awar, O. S.,
    5. Fares, H.,
    6. DeVirgilio, C. and
    7. Pringle, J. R.
    (1996). The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol 8, 106–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Megonigal, M. D.,
    2. Rappaport, E. F.,
    3. Jones, D. H.,
    4. Williams, T. M.,
    5. Lovett, B. D.,
    6. Kelly, K. M.,
    7. Lerou, P. H.,
    8. Moulton, T.,
    9. Budarf, M. L. and
    10. Felix, C. A.
    (1998). t(11;22)(q23;q11.2) in acute myeloid leukemia of infant twinsfuses MLL with hCDC rel, a cell division cycle gene in the genomic region of deletion in DiGeorge and velocardiofacial syndromes. Proc. Nat. Acad. Sci. USA 95, 6413–6418
    OpenUrlAbstract/FREE Full Text
    1. Neufeld, T. P. and
    2. 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, 371–379
    OpenUrlCrossRefPubMedWeb of Science
    1. Osaka, M.,
    2. Rowley, J. D. and
    3. Zeleznik-Le, N. J.
    (1999). MSF (MLL septin-like fusion), a fusion partner gene of MLL, in a therapy-related acute myeloid leukemia with a t(11;17)(q23;25). Proc. Nat. Acad. Sci. USA 96, 6428–6433
    OpenUrlAbstract/FREE Full Text
    1. Polakis, P. and
    2. McCormick, F.
    (1993). Structural requirements for the interaction of p21raswith GAP, exchange factors and its biological effector target. J. Biol. Chem 268, 9157–9160
    OpenUrlAbstract/FREE Full Text
    1. Singh, G.,
    2. Sinha, H. and
    3. Ashby, A. M.
    (2000). Cloning and expression studies during vegetative and sexual development of Pbs1, a septin homologue from Pyrenopeziza brassicae. Biochim. Biophys. Acta 1497, 168–174
    OpenUrlPubMed
    1. Sheu, Y. J.,
    2. Santos, B.,
    3. Fortin, N.,
    4. Costigan, C. and
    5. Snyder, M.
    (1998). Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol 18, 4053–4069
    OpenUrlAbstract/FREE Full Text
    1. Shulewitz, M. J.,
    2. Inouye, C. J. and
    3. Thorner, J.
    (1999). Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol 19, 7123–7137
    OpenUrlAbstract/FREE Full Text
    1. Söllner, T.,
    2. Whiteheart, S. W.,
    3. Brunner, M.,
    4. Erdjument-Bromage, H.,
    5. Geromanos, S.,
    6. Tempst, P. and
    7. Rothman, J. E.
    (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318–324
    OpenUrlCrossRefPubMedWeb of Science
    1. Taki, T.,
    2. Ohnishi, H.,
    3. Shinohara, K.,
    4. Sako, M.,
    5. Bessho, F.,
    6. Yanagisawa, M. and
    7. Hayashi, Y.
    (1999). AF17q25, a putative septin family gene, fuses the MLL gene in acute myeloid leukemia with t(11;17)(q23;q25). Cancer Res 59, 4261–4265
    OpenUrlAbstract/FREE Full Text
    1. Takizawa, P. A.,
    2. DeRisi, J. L.,
    3. Wilhelm, J. E. and
    4. Vale, R. D.
    (2000). Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 290, 341–344
    OpenUrlAbstract/FREE Full Text
    1. TerBush, D. R.,
    2. Maurice, T.,
    3. Roth, D. and
    4. Novick, P.
    (1998). The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15, 6483–6494
    OpenUrl
    1. Trimble, W. S.
    (1999). Septins: A highly conserved family of membrane-associated GTPases with functions in cell division and beyond. J. Membr. Biol 169, 75–81
    OpenUrlCrossRefPubMedWeb of Science
    1. Walikonis, R. S.,
    2. Jensen, O. N.,
    3. Mann, M.,
    4. Provance, D. W. Jr..,
    5. Mercer, J. A. and
    6. Kennedy, M. B.
    (2000). Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci 20, 4069–4080
    OpenUrlAbstract/FREE Full Text
    1. Xie, H.,
    2. Surka, M.,
    3. Howard, J. and
    4. Trimble, W. S.
    (1999). Characterization of the mammalian septin H5: distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motil. Cytoskeleton 43, 52–62
    OpenUrlCrossRefPubMedWeb of Science
    1. Xue, J.,
    2. Xin, W.,
    3. Malladi, C. S.,
    4. Kinoshita, M.,
    5. Milburn, P. J.,
    6. Lengyel, I.,
    7. Rostas, J. A. P. and
    8. Robinson, P. J.
    (2000). Phosphorylation of a new brain-specific septin, G-septin, by a cGMP-dependent protein kinase. J. Biol. Chem 275, 10047–10056
    OpenUrlAbstract/FREE Full Text
    1. Zhang, J.,
    2. Kong, C.,
    3. Xie, H.,
    4. McPherson, P. S.,
    5. Grinstein, S. and
    6. Trimble, W. S.
    (1999). Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr. Biol 9, 1458–1467
    OpenUrlCrossRefPubMedWeb of Science
    1. Ziemin-van der Poel, S.,
    2. McCabe, N. R.,
    3. Gill, H. J.,
    4. Espinosa, R. III.,
    5. Patel, Y.,
    6. Harden, A.,
    7. Rubinelli, P.,
    8. Smith, S. D.,
    9. LeBeau, M. M.,
    10. Rowley, J. D. and
    11. Diaz, M. O.
    (1991). Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc. Nat. Acad. Sci. USA 88, 19735–19739
    OpenUrl
Back to top

 Download PDF

Email
Journal Article
Novel roles for mammalian septins: from vesicle trafficking to oncogenesis
B. Kartmann, D. Roth
Journal of Cell Science 2001 114: 839-844;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

We are pleased to welcome Esperanza to the Journal of Cell Science team. The new Community Manager for FocalPlane, Esperanza is joining us from the Microscopy Core at Mount Sinai School of Medicine. Find out more about Esperanza in her introductory post over on FocalPlane.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

"Alongside pre-printing for early documentation of work, such mechanisms are particularly helpful for early-career researchers like me.”

Dr Chris MacDonald (University of York) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Cell scientist to watch: Romain Levayer

In an interview, Romain Levayer talks about starting his own lab, his love for preprints and his experience of balancing parenting with his research goals.

Live lactating mammary tissue

In a stunning video, Stewart et al. demonstrate warping of the alveolar unit due to basal cell-generated force as part of their recent work investigating roles for mechanically activated ion channels in lactation and involution.

Visit our YouTube channel to watch more videos from JCS, our sister journals and the Company.

JCS and COVID-19

For more information on measures Journal of Cell Science is taking to support the community during the COVID-19 pandemic, please see here.

If you have any questions or concerns, please do not hestiate to contact the Editorial Office.