Drosophila F-BAR protein Syndapin contributes to coupling the plasma membrane and contractile ring in cytokinesis

Open Biology

Volumn 3, Issue AUG, 2013, Pages

  Takeda, Tetsuya ^a,d   Robinson, Iain M ^b   Savoian, Matthew M ^a   Griffiths, John R ^c   Whetton, Anthony D ^c   McMahon, Harvey T ^d   Glover, David M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Actomyosin contractile ring; Cytokinesis; F BAR; Membrane; Phosphorylation; Tetsuya Takeda

Indexed keywords

ACTIN BINDING PROTEIN; ANILLIN; CARRIER PROTEIN; CONTRACTILE PROTEIN; DROSOPHILA PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SYNDAPIN PROTEIN, DROSOPHILA;

ACTIN FILAMENT; ACTOMYOSIN CONTRACTILE RING; ANIMAL; ARTICLE; CELL LINE; CELL MEMBRANE; CYTOKINESIS; DROSOPHILA MELANOGASTER; F-BAR; MEMBRANE; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

ACTOMYOSIN CONTRACTILE RING; CYTOKINESIS; F-BAR; MEMBRANE; PHOSPHORYLATION;

ACTIN CYTOSKELETON; ANIMALS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; CONTRACTILE PROTEINS; CYTOKINESIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MICROFILAMENT PROTEINS; MICROTUBULES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84885640041     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130081     Document Type: Article

References (52)

1. Green RA, Paluch E, Oegema K. 2012 Cytokinesis in animal cells. Annu. Rev. Cell Dev. Biol. 28, 29-58. (doi:10.1146/annurev-cellbio-101011-155718)
2. Lacroix B, Maddox AS. 2012 Cytokinesis, ploidy and aneuploidy. J. Pathol. 226, 338-351. (doi:10.1002/path.3013)
3. Li R. 2007 Cytokinesis in development and disease: variations on a common theme. Cell Mol. Life Sci. 64, 3044-3058. (doi:10.1007/s00018-007-7285-6) (Pubitemid 351152237)
4. D'Avino PP, Savoian MS, Glover DM. 2005 Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118, 1549-1558. (doi:10.1242/jcs.02335) (Pubitemid 40691883)
5. Capalbo L, Montembault E, Takeda T, Bassi ZI, Glover DM, D'Avino PP. 2012 The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis. Open Biol. 2, 120070. (doi:10.1098/rsob.120070)
6. Neto H, Collins LL, Gould GW. 2011 Vesicle trafficking and membrane remodelling in cytokinesis. Biochem. J. 437, 13-24. (doi:10.1042/BJ20110153)
7. D'Avino PP. 2009 How to scaffold the contractile ring for a safe cytokinesislessons from Anillinrelated proteins. J. Cell Sci. 122, 1071-1079. (doi:10.1242/jcs.034785)
8. Kechad A, Jananji S, Ruella Y, Hickson GR. 2012 Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr. Biol. 22, 197-203. (doi:10.1016/j.cub.2011.11.062)
9. Liu J, Fairn GD, Ceccarelli DF, Sicheri F, Wilde A. 2012 Cleavage furrow organization requires PIP(2)- mediated recruitment of anillin. Curr. Biol. 22, 64-69. (doi:10.1016/j.cub.2011.11.040)
10. Aspenstrom P, Fransson A, Richnau N. 2006 Pombe Cdc15 homology proteins: regulators of membrane dynamics and the actin cytoskeleton. Trends Biochem. Sci. 31, 670-679. (doi:10.1016/j.tibs.2006.10.001) (Pubitemid 44791944)
11. Itoh T, De Camilli P. 2006 BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912. (doi:10.1016/j.bbalip.2006.06.015) (Pubitemid 44332330)
12. Fankhauser C, Reymond A, Cerutti L, Utzig S, Hofmann K, Simanis V. 1995 The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis. Cell 82, 435-444. (doi:10.1016/0092-8674(95)90432-8)
13. Kamei T, Tanaka K, Hihara T, Umikawa M, Imamura H, Kikyo M, Ozaki K, Takai Y. 1998 Interaction of Bnr1p with a novel Src homology 3 domaincontaining Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273, 28 341-28 345. (doi:10.1074/jbc.273.43.28341) (Pubitemid 28496135)
14. Carnahan RH, Gould KL. 2003 The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J. Cell Biol. 162, 851-862. (doi:10.1083/jcb. 200305012) (Pubitemid 37087725)
15. Wachtler V, Huang Y, Karagiannis J, Balasubramanian MK. 2006 Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe. Mol. Biol. Cell 17, 3254-3266. (doi:10.1091/mbc.E05-11-1086) (Pubitemid 43993525)
16. Takeda T, Kawate T, Chang F. 2004 Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 6, 1142-1144. (doi:10.1038/ncb1189) (Pubitemid 39468017)
17. Lippincott J, Li R. 1998 Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143, 1947-1960. (doi:10.1083/jcb.143.7.1947) (Pubitemid 29022615)
18. Vallen EA, Caviston J, Bi E. 2000 Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell 11, 593-611. (doi:10.1091/mbc.11.2.593) (Pubitemid 30112168)
19. Spencer S, Dowbenko D, Cheng J, Li W, Brush J, Utzig S, Simanis V, Lasky LA. 1997 PSTPIP: a tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. J. Cell Biol. 138, 845-860. (doi:10.1083/jcb.138.4.845) (Pubitemid 27365047)
20. Smith CM, Chircop M. 2012 Clathrin-mediated endocytic proteins are involved in regulating mitotic progression and completion. Traffic 13, 1628-1641. (doi:10.1111/tra.12001)
21. Anggono V, Smillie KJ, Graham ME, Valova VA, Cousin MA, Robinson PJ. 2006 Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat. Neurosci. 9, 752-760. (doi:10.1038/nn1695)
22. Kessels MM, Qualmann B. 2002 Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 21, 6083-6094. (doi:10.1093/emboj/cdf604) (Pubitemid 35422657)
23. Edeling MA et al. 2009 Structural requirements for PACSIN/Syndapin operation during zebrafish embryonic notochord development. PLoS ONE 4, e8150. (doi:10.1371/journal.pone.0008150)
24. Dharmalingam E, Haeckel A, Pinyol R, Schwintzer L, Koch D, Kessels MM, Qualmann B. 2009 F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis. J. Neurosci. 29, 13 315-13 327. (doi:10.1523/JNEUROSCI.3973-09.2009)
25. Cousin H, Desimone DW, Alfandari D. 2008 PACSIN2 regulates cell adhesion during gastrulation in Xenopus laevis. Dev. Biol. 319, 86-99. (doi:10.1016/j.ydbio.2008.04.007)
26. Naslavsky N, Caplan S. 2011 EHD proteins: key conductors of endocytic transport. Trends Cell Biol. 21, 122-131. (doi:10.1016/j.tcb.2010.10.003)
27. Inoue YH, Savoian MS, Suzuki T, Mathe E, Yamamoto MT, Glover DM. 2004 Mutations in orbit/ mast reveal that the central spindle is comprised of two microtubule populations, those that initiate cleavage and those that propagate furrow ingression. J. Cell Biol. 166, 49-60. (doi:10.1083/jcb.200402052) (Pubitemid 38931916)
28. Wong R, Hadjiyanni I, Wei HC, Polevoy G, McBride R, Sem KP, Brill JA. 2005 PIP2 hydrolysis and calcium release are required for cytokinesis in Drosophila spermatocytes. Curr. Biol. 15, 1401-1406. (doi:10.1016/j.cub.2005.06. 060) (Pubitemid 41097545)
29. Brill JA, Wong R, Wilde A. 2011 Phosphoinositide function in cytokinesis. Curr. Biol. 21, R930-R934. (doi:10.1016/j.cub.2011.10.001)
30. Ben El Kadhi K, Roubinet C, Solinet S, Emery G, Carreno S. 2011 The inositol 5-phosphatase dOCRL controls PI(4,5)P2 homeostasis and is necessary for cytokinesis. Curr. Biol. 21, 1074-1079. (doi:10.1016/j.cub.2011.05.030)
31. Dambournet D et al. 2011 Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell Biol. 13, 981-988. (doi:10.1038/ncb2279)
32. D'Avino PP, Takeda T, Capalbo L, Zhang W, Lilley KS, Laue ED, Glover DM. 2008 Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J. Cell Sci. 121, 1151-1158. (doi:10.1242/jcs.026716) (Pubitemid 351753498)
33. Straight AF, Field CM, Mitchison TJ. 2005 Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol. Biol. Cell 16, 193-201. (doi:10.1091/mbc.E04-08-0758) (Pubitemid 40024302)
34. Zhai B, Villen J, Beausoleil SA, Mintseris J, Gygi SP. 2008 Phosphoproteome analysis of Drosophila melanogaster embryos. J. Proteome Res. 7, 1675-1682. (doi:10.1021/pr700696a)
35. Meitinger F, Boehm ME, Hofmann A, Hub B, Zentgraf H, Lehmann WD, Pereira G. 2011 Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev. 25, 875-888. (doi:10.1101/gad.622411)
36. Roberts-Galbraith RH, Ohi MD, Ballif BA, Chen JS, McLeod I, McDonald WH, Gygi SP, Yates 3rd JR, Gould KL. 2010 Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol. Cell 39, 86-99. (doi:10.1016/j.molcel.2010.06.012)
37. Cohen P, Holmes CF, Tsukitani Y. 1990 Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem. Sci. 15, 98-102. (doi:10.1016/0968-0004(90)90192-E)
38. Rao Y et al. 2010 Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc. Natl Acad. Sci. USA 107, 8213-8218. (doi:10.1073/pnas.1003478107)
39. Wang Q, Navarro MV, Peng G, Molinelli E, Lin Goh S, Judson BL, Rajashankar KR, Sondermann H. 2009 Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc. Natl Acad. Sci. USA 106, 12 700-12 705. (doi:10.1073/pnas.0902974106)
40. Lekomtsev S et al. 2012 Centralspindlin links the mitotic spindle to the plasma membrane during cytokinesis. Nature 492, 276-279. (doi:10.1038/ nature11773)
41. Sanchez-Diaz A, Marchesi V, Murray S, Jones R, Pereira G, Edmondson R, Allen T, Labib K. 2008 Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat. Cell Biol. 10, 395-406. (doi:10.1038/ncb1701)
42. Mohan K, Iglesias PA, Robinson DN. 2012 Separation anxiety: stress, tension and cytokinesis. Exp. Cell Res. 318, 1428-1434. (doi:10.1016/j.yexcr. 2012. 03.028)
43. Sedzinski J, Biro M, Oswald A, Tinevez JY, Salbreux G, Paluch E. 2011 Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476, 462-466. (doi:10.1038/nature10286)
44. Koch D et al. 2011 Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J. 30, 4955-4969. (doi:10.1038/emboj.2011.339)
45. Quan A, Xue J, Wielens J, Smillie KJ, Anggono V, Parker MW, Cousin MA, Graham ME, Robinson PJ. 2012 Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation. Proc. Natl Acad. Sci. USA 109, 3760-3765. (doi:10.1073/pnas.1108294109)
46. Zimmerberg J, Kozlov MM. 2006 How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19. (doi:10.1038/nrm1784) (Pubitemid 43361568)
47. D'Avino PP, Savoian MS, Capalbo L, Glover DM. 2006 RacGAP50C is sufficient to signal cleavage furrow formation during cytokinesis. J. Cell Sci. 119, 4402-4408. (doi:10.1242/jcs.03210) (Pubitemid 44830639)
48. Minestrini G, Mathe E, Glover DM. 2002 Domains of the Pavarotti kinesin-like protein that direct its subcellular distribution: effects of mislocalisation on the tubulin and actin cytoskeleton during Drosophila oogenesis. J. Cell Sci. 115, 725-736. (Pubitemid 34196332)
49. Bonaccorsi S, Giansanti MG, Gatti M. 2000 Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nat. Cell Biol. 2, 54-56. (doi:10.1038/71378)
50. D'Avino PP, Archambault V, Przewloka MR, Zhang W, Laue ED, Glover DM. 2009 Isolation of protein complexes involved in mitosis and cytokinesis from Drosophila cultured cells. Methods Mol. Biol. 545, 99-112. (doi:10.1007/978-1- 60327-993-2-6)
51. Unwin RD, Griffiths JR, Leverentz MK, Grallert A, Hagan IM, Whetton AD. 2005 Multiple reaction monitoring to identify sites of protein phosphorylation with high sensitivity. Mol. Cell Proteomics 4, 1134-1144. (doi:10.1074/mcp. M500113-MCP200) (Pubitemid 41223372)
52. Unwin RD, Griffiths JR, Whetton AD. 2009 A sensitive mass spectrometric method for hypothesisdriven detection of peptide post-translational modifications: multiple reaction monitoring-initiated detection and sequencing (MIDAS). Nat. Protoc. 4, 870-877. (doi:10.1038/nprot.2009.57)