Microtubules support a disk-like septin arrangement at the plasma membrane of mammalian cells

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4588-4601

  Sellin, Mikael E ^a   Holmfeldt, Per ^a   Stenmark, Sonja ^a   Gullberg, Martin ^b  

^a UMEÅ UNIVERSITY   (Sweden)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEPTIN;

ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL MEMBRANE; CELL TYPE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERPHASE; LYMPHOID CELL; MAMMAL CELL; MICROTUBULE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FAMILY;

CELL ADHESION; CELL CYCLE PROTEINS; CELL LINE; CELL MEMBRANE; GREEN FLUORESCENT PROTEINS; HUMANS; JURKAT CELLS; K562 CELLS; LEUKEMIA, ERYTHROBLASTIC, ACUTE; MICROTUBULES; PERMEABILITY; RECOMBINANT PROTEINS; SEPTINS; T-LYMPHOCYTES;

EID: 82655181327     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-09-0754     Document Type: Article

References (62)

1. Arencibia I, Suarez NC, Wolf-Watz H, Sundqvist KG (1997). Yersinia invasin, a bacterial beta1-integrin ligand, is a potent inducer of lymphocyte motility and migration to collagen type IV and fibronectin. J Immunol 159, 1853-1859. (Pubitemid 127484173)
2. Bertin A, McMurray MA, Grob P, Park SS, Garcia G, III, Patanwala I, Ng HL, Alber T, Thorner J, Nogales E (2008). Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc Natl Acad Sci USA 105, 8274-8279. (Pubitemid 351904746)
3. Bertin A, McMurray MA, Thai L, Garcia G, III, Votin V, Grob P, Allyn T, Thorner J, Nogales E (2010). Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J Mol Biol 404, 711-731.
4. Bhamidipati A, Lewis SA, Cowan NJ (2000). ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. J Cell Biol 149, 1087-1096. (Pubitemid 30354258)
5. Bowen JR, Hwang D, Bai X, Roy D, Spiliotis ET (2011). Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J Cell Biol 194, 187-197.
6. Cao L, Ding X, Yu W, Yang X, Shen S, Yu L (2007). Phylogenetic and evolutionary analysis of the septin protein family in metazoan. FEBS Lett 581, 5526-5532. (Pubitemid 350101514)
7. Casamayor A, Snyder M (2003). Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol Cell Biol 23, 2762-2777. (Pubitemid 36403076)
8. Caudron F, Barral Y (2009). Septins and the lateral compartmentalization of eukaryotic membranes. Dev Cell 16, 493-506.
9. DeMay BS, Bai X, Howard L, Occhipinti P, Meseroll RA, Spiliotis ET, Oldenbourg R, Gladfelter AS (2011). Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals. J Cell Biol 193, 1065-1081.
10. DeMay BS, Meseroll RA, Occhipinti P, Gladfelter AS (2009). Regulation of distinct septin rings in a single cell by Elm1p and Gin4p kinases. Mol Biol Cell 20, 2311-2326.
11. Gladfelter AS (2010). Guides to the final frontier of the cytoskeleton: septins in filamentous fungi. Curr Opin Microbiol 13, 720-726.
12. Holmfeldt P, Brannstrom K, Stenmark S, Gullberg M (2003a). Deciphering the cellular functions of the Op18/Stathmin family of microtubule-regulators by plasma membrane-targeted localization. Mol Biol Cell 14, 3716-3729. (Pubitemid 37151621)
13. Holmfeldt P, Brattsand G, Gullberg M (2002). MAP4 counteracts microtubule catastrophe promotion but not tubulin-sequestering activity in intact cells. Curr Biol 12, 1034-1039. (Pubitemid 34703336)
14. Holmfeldt P, Brattsand G, Gullberg M (2003b). Interphase and monoastralmitotic phenotypes of overexpressed MAP4 are modulated by free tubulin concentrations. J Cell Sci 116, 3701-3711. (Pubitemid 37185299)
15. Holmfeldt P, Sellin ME, Gullberg M (2009). Predominant regulators of tubulin monomer-polymer partitioning and their implication for cell polarization. Cell Mol Life Sci 66, 3263-3276.
16. Holmfeldt P, Stenmark S, Gullberg M (2004). Differential functional interplay of TOGp/XMAP215 and the KinI kinesin MCAK during interphase and mitosis. EMBO J 23, 627-637. (Pubitemid 38282394)
17. Holmfeldt P, Stenmark S, Gullberg M (2007). Interphase-specific phosphorylation-mediated regulation of tubulin dimer partitioning in human cells. Mol Biol Cell 18, 1909-1917. (Pubitemid 46717570)
18. Hu Q, Milenkovic L, Jin H, Scott MP, Nachury MV, Spiliotis ET, Nelson WJ (2010). A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436-439.
19. Huang YW, Yan M, Collins RF, Diciccio JE, Grinstein S, Trimble WS (2008). Mammalian septins are required for phagosome formation. Mol Biol Cell 19, 1717-1726. (Pubitemid 351805123)
20. Ihara M, et al. (2005). Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell 8, 343-352. (Pubitemid 40309805)
21. Kinoshita M (2003a). Assembly of mammalian septins. J Biochem 134, 491-496.
22. Kinoshita M (2003b). The septins. Genome Biol 4, 236.
23. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ (2002). Self- and actin-templated assembly of mammalian septins. Dev Cell 3, 791-802. (Pubitemid 35460780)
24. Kissel H, Georgescu MM, Larisch S, Manova K, Hunnicutt GR, Steller H (2005). The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell 8, 353-364. (Pubitemid 40309806)
25. Kremer BE, Adang LA, Macara IG (2007). Septins regulate actin organization and cell-cycle arrest through nuclear accumulation of NCK mediated by SOCS7. Cell 130, 837-850. (Pubitemid 47332569)
26. Kremer BE, Haystead T, Macara IG (2005). Mammalian septins regulate microtubule stability through interaction with the microtubule-binding protein MAP4. Mol Biol Cell 16, 4648-4659. (Pubitemid 41416448)
27. Lindsey R, Momany M (2006). Septin localization across kingdoms: three themes with variations. Curr Opin Microbiol 9, 559-565. (Pubitemid 44791990)
28. Lingwood D, Simons K (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
29. Martinez C, Corral J, Dent JA, Sesma L, Vicente V, Ware J (2006). Platelet septin complexes form rings and associate with the microtubular network. J Thromb Haemost 4, 1388-1395.
30. McMurray MA, Bertin A, Garcia G, III, Lam L, Nogales E, Thorner J (2011). Septin filament formation is essential in budding yeast. Dev Cell 20, 540-549.
31. McMurray MA, Thorner J (2008). Septin stability and recycling during dynamic structural transitions in cell division and development. Curr Biol 18, 1203-1208.
32. McMurray MA, Thorner J (2009). Reuse, replace, recycle. Specificity in subunit inheritance and assembly of higher-order septin structures during mitotic and meiotic division in budding yeast. Cell Cycle 8, 195-203.
33. 2+/calmodulin-dependent kinase IV/Gr-dependent phosphorylation of oncoprotein 18. Mol Cell Biol 17, 3459-3467.
34. Mostowy S et al. (2010). Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microbe 8, 433-444.
35. Muller U, Bossy B, Venstrom K, Reichardt LF (1995). Integrin alpha 8 beta 1 promotes attachment, cell spreading, and neurite outgrowth on fibronectin. Mol Biol Cell 6, 433-448.
36. Nagata K et al. (2003). Filament formation of MSF-A, a mammalian septin, in human mammary epithelial cells depends on interactions with microtubules. J Biol Chem 278, 18538-18543. (Pubitemid 36799479)
37. Oegema K, Savoian MS, Mitchison TJ, Field CM (2000). Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J Cell Biol 150, 539-552.
38. Oh Y, Bi E (2011). Septin structure and function in yeast and beyond. Trends Cell Biol 21, 141-148.
39. Pablo-Hernando ME, Arnaiz-Pita Y, Tachikawa H, del Rey F, Neiman AM, Vazquez de Aldana CR (2008). Septins localize to microtubules during nutritional limitation in Saccharomyces cerevisiae. BMC Cell Biol 9, 55.
40. Pan F, Malmberg RL, Momany M (2007). Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol Biol 7, 103.
41. Peterson EA, Petty EM (2010). Conquering the complex world of human septins: implications for health and disease. Clin Genet 77, 511-524.
42. Riedl J et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat Methods 5, 605-607. (Pubitemid 351911864)
43. Schmidt K, Nichols BJ (2004). Functional interdependence between septin and actin cytoskeleton. BMC Cell Biol 5, 43.
44. Sellin ME, Holmfeldt P, Stenmark S, Gullberg M (2008a). Global regulation of the interphase microtubule system by abundantly expressed Op18/Stathmin. Mol Biol Cell 19, 2897-2906.
45. Sellin ME, Holmfeldt P, Stenmark S, Gullberg M (2008b). Op18/Stathmin counteracts the activity of overexpressed tubulin-disrupting proteins in a human leukemia cell line. Exp Cell Res 314, 1367-1377.
46. Sellin ME, Sandblad L, Stenmark S, Gullberg M (2011). Deciphering the rules governing assembly order of mammalian septin complexes. Mol Biol Cell 22, 3152-3164.
47. Sheffield PJ, Oliver CJ, Kremer BE, Sheng S, Shao Z, Macara IG (2003). Borg/septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments. J Biol Chem 278, 3483-3488. (Pubitemid 36801265)
48. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, Weyand M, Stark H, Wittinghofer A (2007). Structural insight into filament formation by mammalian septins. Nature 449, 311-315. (Pubitemid 47443471)
49. Sirajuddin M, Farkasovsky M, Zent E, Wittinghofer A (2009). GTP-induced conformational changes in septins and implications for function. Proc Natl Acad Sci USA 106, 16592-16597.
50. Spiliotis ET (2010). Regulation of microtubule organization and functions by septin GTPases. Cytoskeleton (Hoboken) 67, 339-345.
51. Spiliotis ET, Kinoshita M, Nelson WJ (2005). A mitotic septin scaffold required for mammalian chromosome congression and segregation. Science 307, 1781-1785. (Pubitemid 40388620)
52. Surka MC, Tsang CW, Trimble WS (2002). The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol Biol Cell 13, 3532-3545. (Pubitemid 35191373)
53. Tada T, Simonetta A, Batterton M, Kinoshita M, Edbauer D, Sheng M (2007). Role of septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr Biol 17, 1752-1758. (Pubitemid 47576672)
54. Tanaka-Takiguchi Y, Kinoshita M, Takiguchi K (2009). Septin-mediated uniform bracing of phospholipid membranes. Curr Biol 19, 140-145.
55. Tooley AJ, Gilden J, Jacobelli J, Beemiller P, Trimble WS, Kinoshita M, Krummel MF (2009). Amoeboid T lymphocytes require the septin cytoskeleton for cortical integrity and persistent motility. Nat Cell Biol 11, 17-26.
56. Varnai P, Balla T (2007). Visualization and manipulation of phosphoinositide dynamics in live cells using engineered protein domains. Pflugers Arch 455, 69-82. (Pubitemid 47403977)
57. Vega IE, Hsu SC (2003). The septin protein Nedd5 associates with both the exocyst complex and microtubules and disruption of its GTPase activity promotes aberrant neurite sprouting in PC12 cells. Neuroreport 14, 31-37. (Pubitemid 36160737)
58. Weirich CS, Erzberger JP, Barral Y (2008). The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 9, 478-489. (Pubitemid 351733401)
59. Vrabioiu AM, Mitchison TJ (2006). Structural insights into yeast septin organization from polarized fluorescence microscopy. Nature 443, 466-469. (Pubitemid 44477284)
60. Xie Y, Vessey JP, Konecna A, Dahm R, Macchi P, Kiebler MA (2007). The GTP-binding protein septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr Biol 17, 1746-1751. (Pubitemid 47576665)
61. Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS (1999). Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol 9, 1458-1467. (Pubitemid 30023480)
62. Zhu M et al. (2008). Septin 7 interacts with centromere-associated protein E and is required for its kinetochore localization. J Biol Chem 283, 18916-18925.