Endocytic traffic in animal cell cytokinesis

Current Opinion in Cell Biology

Volumn 20, Issue 4, 2008, Pages 454-461

  Montagnac, Guillaume ^a,b   Echard, Arnaud ^a,b   Chavrier, Philippe ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ARFOPHILIN 1; ARFOPHILIN 2; CLATHRIN; DYNAMIN; LIPID; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN; RAB11 FAMILY INTERACTING PROTEIN 3; RAB11 FAMILY INTERACTING PROTEIN 4; RAB11 PROTEIN; SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 2; TRANSFERRIN; VESICLE ASSOCIATED MEMBRANE PROTEIN 8;

ABSCISSION; ANAPHASE; CELL MEMBRANE; CELL ORGANELLE; CELL POLARITY; CYTOKINESIS; CYTOPLASM; DAUGHTER CELL; ENDOCYTOSIS; GENE MUTATION; GOLGI COMPLEX; HUMAN; MEMBRANE VESICLE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; SPINDLE POLE BODY; TELOPHASE;

ANIMALS; CELLULAR STRUCTURES; CYTOKINESIS; ENDOCYTOSIS; MITOSIS; MITOTIC SPINDLE APPARATUS; TRANSPORT VESICLES;

ANIMALIA;

EID: 47349133924     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2008.03.011     Document Type: Review

References (74)

1. Glotzer M. The molecular requirements for cytokinesis. Science 307 (2005) 1735-1739
2. Echard A., Hickson G.R., Foley E., and O'Farrell P.H. Terminal cytokinesis events uncovered after an RNAi screen. Curr Biol 14 (2004) 1685-1693
3. Schechtman A.M. Localized cortical growth as the immediate cause of cell division. Science 85 (1937) 222-223
4. Whaley W.G., and Mollenhauer H.H. The Golgi apparatus and cell plate formation - a postulate. J Cell Biol 17 (1963) 216-221
5. Bluemink J.G., and de Laat S.W. New membrane formation during cytokinesis in normal and cytochalasin B-treated eggs of Xenopus laevis. I. Electron microscope observations. J Cell Biol 59 (1973) 89-108
6. Jesuthasan S. Furrow-associated microtubule arrays are required for the cohesion of zebrafish blastomeres following cytokinesis. J Cell Sci 111 Pt 24 (1998) 3695-3703
7. Danilchik M.V., Bedrick S.D., Brown E.E., and Ray K. Furrow microtubules and localized exocytosis in cleaving Xenopus laevis embryos. J Cell Sci 116 (2003) 273-283
8. Shuster C.B., and Burgess D.R. Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis. Proc Natl Acad Sci U S A 99 (2002) 3633-3638
9. Eggert U.S., Mitchison T.J., and Field C.M. Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 75 (2006) 543-566
10. Skop A.R., Bergmann D., Mohler W.A., and White J.G. Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex. Curr Biol 11 (2001) 735-746
11. Xu H., Brill J.A., Hsien J., McBride R., Boulianne G.L., and Trimble W.S. Syntaxin 5 is required for cytokinesis and spermatid differentiation in Drosophila. Dev Biol 251 (2002) 294-306
12. Low S.H., Li X., Miura M., Kudo N., Quinones B., and Weimbs T. Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev Cell 4 (2003) 753-759
13. Schweitzer J.K., and D'Souza-Schorey C. A requirement for ARF6 during the completion of cytokinesis. Exp Cell Res 311 (2005) 74-83
14. Gromley A., Yeaman C., Rosa J., Redick S., Chen C.T., Mirabelle S., Guha M., Sillibourne J., and Doxsey S.J. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123 (2005) 75-87. The authors show that centriolin localizes to midbody ring, and associates with exocyst and SNARE proteins, which are involved in membrane docking/fusion events during cytokinesis. This has led to the proposal that centriolin acts as an anchor for protein complexes involved in membrane targeting and fusion during cytokinesis.
15. Chen X.W., Inoue M., Hsu S.C., and Saltiel A.R. RalA-exocyst-dependent recycling endosome trafficking is required for the completion of cytokinesis. J Biol Chem 281 (2006) 38609-38616
16. Kouranti I., Sachse M., Arouche N., Goud B., and Echard A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16 (2006) 1719-1725. Here, Rab35 is found to regulate fast endocytic recycling and is required for late steps of cytokinesis. The proposed function of Rab35 is to regulate PIP2 enrichment at the intracellular bridge and the proper SEPTIN2 localization during cytokinesis.
17. Boucrot E., and Kirchhausen T. Endosomal recycling controls plasma membrane area during mitosis. Proc Natl Acad Sci U S A 104 (2007) 7939-7944. Using live-cell imaging the authors show that the total surface area of diving cells diminishes during mitotic cell-rounding as a consequence of a block of endosomal recycling, while endocytic uptake remains normal contrasting with the classical view that endocytosis is shut down during mitosis. At the onset of anaphase, endosomal recycling resumes providing the excess membrane required for the two daughter cells to undergo cytokinesis in a mechanism that is Golgi-independent, and requires endosomal v-SNARE VAMP3- and VAMP7 function.
18. Dyer N., Rebollo E., Dominguez P., Elkhatib N., Chavrier P., Daviet L., Gonzalez C., and Gonzalez-Gaitan M. Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134 (2007) 4437-4447. This manuscript shows that otherwise normal arf6 null mutant flies are defective for spermatocyte cytokinesis resulting in multinucleated spermatids and male sterility. Live-cell imaging of mutant arf6 spermatids reveals a role for ARF6 in rapid addition of plasma membrane during cleavage furrow progression and localizes ARF6 to endosomal membranes associated with the central spindle.
19. Mullins J.M., and Biesele J.J. Terminal phase of cytokinesis in D-98s cells. J Cell Biol 73 (1977) 672-684
20. Gaietta G.M., Giepmans B.N., Deerinck T.J., Smith W.B., Ngan L., Llopis J., Adams S.R., Tsien R.Y., and Ellisman M.H. Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc Natl Acad Sci U S A 103 (2006) 17777-17782
21. Jurgens G. Cytokinesis in higher plants. Annu Rev Plant Biol 56 (2005) 281-299
22. Sisson J.C., Field C., Ventura R., Royou A., and Sullivan W. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 151 (2000) 905-918
23. Liu J., Tang X., Wang H., Oliferenko S., and Balasubramanian M.K. The localization of the integral membrane protein Cps1p to the cell division site is dependent on the actomyosin ring and the septation-inducing network in Schizosaccharomyces pombe. Mol Biol Cell 13 (2002) 989-1000
24. Tomas A., Futter C., and Moss S.E. Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis. J Cell Biol 165 (2004) 813-822
25. Altan-Bonnet N., Phair R.D., Polishchuk R.S., Weigert R., and Lippincott-Schwartz J. A role for Arf1 in mitotic Golgi disassembly, chromosome segregation, and cytokinesis. Proc Natl Acad Sci U S A 100 (2003) 13314-13319
26. Stoorvogel W., Oorschot V., and Geuze H.J. A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 132 (1996) 21-33
27. Dhonukshe P., Baluska F., Schlicht M., Hlavacka A., Samaj J., Friml J., and Gadella Jr. T.W. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10 (2006) 137-150
28. Reichardt I., Stierhof Y.D., Mayer U., Richter S., Schwarz H., Schumacher K., and Jurgens G. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr Biol 17 (2007) 2047-2053
29. Wienke D.C., Knetsch M.L., Neuhaus E.M., Reedy M.C., and Manstein D.J. Disruption of a dynamin homologue affects endocytosis, organelle morphology, and cytokinesis in Dictyostelium discoideum. Mol Biol Cell 10 (1999) 225-243
30. Gerald N.J., Damer C.K., O'Halloran T.J., and De Lozanne A. Cytokinesis failure in clathrin-minus cells is caused by cleavage furrow instability. Cell Motil Cytoskeleton 48 (2001) 213-223
31. Thompson H.M., Skop A.R., Euteneuer U., Meyer B.J., and McNiven M.A. The large GTPase dynamin associates with the spindle midzone and is required for cytokinesis. Curr Biol 12 (2002) 2111-2117
32. Schweitzer J.K., Burke E.E., Goodson H.V., and D'Souza-Schorey C. Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem 280 (2005) 41628-41635. The authors show that receptor-mediated endocytosis of transferrin, which shuts down during mitosis, resumes during cytokinesis and is required for abscission. Transferrin uptake occurs preferentially at the poles during early cytokinesis and close to the bridge at later steps. This report provides evidence that some vesicles are trafficked from distal endosomal clusters toward proximal ones near the intercellular bridge.
33. Eggert U.S., Kiger A.A., Richter C., Perlman Z.E., Perrimon N., Mitchison T.J., and Field C.M. Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets. PLoS Biol 2 (2004) e379
34. Skop A.R., Liu H., Yates III J., Meyer B.J., and Heald R. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 305 (2004) 61-66. A proteomic analysis of human cell midbody which identifies several proteins involved in cytokinesis, further combined with a comparative genomic analysis of candidate proteins by RNA interference in C. elegans. This study reveals the prominent role of proteins involved in membrane trafficking/secretion during cytokinesis.
35. Feng B., Schwarz H., and Jesuthasan S. Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres. Exp Cell Res 279 (2002) 14-20
36. Berlin R.D., Oliver J.M., and Walter R.J. Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell 15 (1978) 327-341
37. Sager P.R., Brown P.A., and Berlin R.D. Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell 39 (1984) 275-282
38. Warner A.K., Keen J.H., and Wang Y.L. Dynamics of membrane clathrin-coated structures during cytokinesis. Traffic 7 (2006) 205-215
39. Albertson R., Riggs B., and Sullivan W. Membrane traffic: a driving force in cytokinesis. Trends Cell Biol 15 (2005) 92-101
40. Baluska F., Menzel D., and Barlow P.W. Cytokinesis in plant and animal cells: endosomes 'shut the door'. Dev Biol 294 (2006) 1-10
41. Ullrich O., Reinsch S., Urbe S., Zerial M., and Parton R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135 (1996) 913-924
42. Wilcke M., Johannes L., Galli T., Mayau V., Goud B., and Salamero J. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 151 (2000) 1207-1220
43. Yu X., Prekeris R., and Gould G.W. Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 86 (2007) 25-35
44. Horgan C.P., Walsh M., Zurawski T.H., and McCaffrey M.W. Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis. Biochem Biophys Res Commun 319 (2004) 83-94
45. Wilson G.M., Fielding A.B., Simon G.C., Yu X., Andrews P.D., Hames R.S., Frey A.M., Peden A.A., Gould G.W., and Prekeris R. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 16 (2005) 849-860
46. Hales C.M., Griner R., Hobdy-Henderson K.C., Dorn M.C., Hardy D., Kumar R., Navarre J., Chan E.K.L., Lapierre L.A., and Goldenring J.R. Identification and characterization of a family of Rab11-interacting proteins. J Biol Chem 276 (2001) 39067-39075
47. Wallace D.M., Lindsay A.J., Hendrick A.G., and McCaffrey M.W. Rab11-FIP4 interacts with Rab11 in a GTP-dependent manner and its overexpression condenses the Rab11 positive compartment in HeLa cells. Biochem Biophys Res Commun 299 (2002) 770-779
48. Fielding A.B., Schonteich E., Matheson J., Wilson G., Yu X., Hickson G.R., Srivastava S., Baldwin S.A., Prekeris R., and Gould G.W. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 24 (2005) 3389-3399. An interaction of FIP3 and FIP4 with GTP-ARF6 is documented, and is involved for the recruitment of FIP3/4 into the intercellular bridge. The authors also report on a ternary complex between FIP3/4, ARF6 and the exocyst and further show that the exocyst component Exo70 is necessary for recruitment of FIP3/4 to the furrow. The authors propose a model whereby ARF6 interaction with FIP3/4 and exocyst facilitates docking of endocytic vesicles at the furrow.
49. Shin O.H., Couvillon A.D., and Exton J.H. Arfophilin is a common target of both class II and class III ADP-ribosylation factors. Biochemistry 40 (2001) 10846-10852
50. D'Souza-Schorey C., and Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7 (2006) 347-358
51. Schonteich E., Pilli M., Simon G.C., Matern H.T., Junutula J.R., Sentz D., Holmes R.K., and Prekeris R. Molecular characterization of Rab11-FIP3 binding to ARF GTPases. Eur J Cell Biol 86 (2007) 417-431
52. Schweitzer J.K., and D'Souza-Schorey C. Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis. J Biol Chem 277 (2002) 27210-27216
53. Hsu S.C., TerBush D., Abraham M., and Guo W. The exocyst complex in polarized exocytosis. Int Rev Cytol 233 (2004) 243-265
54. Zhang X.M., Ellis S., Sriratana A., Mitchell C.A., and Rowe T. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem 279 (2004) 43027-43034
55. Prigent M., Dubois T., Raposo G., Derrien V., Tenza D., Rosse C., Camonis J., and Chavrier P. ARF6 controls post-endocytic recycling through its downstream exocyst complex effector. J Cell Biol 163 (2003) 1111-1121
56. •].
57. Li W.M., Webb S.E., Lee K.W., and Miller A.L. Recruitment and SNARE-mediated fusion of vesicles in furrow membrane remodeling during cytokinesis in zebrafish embryos. Exp Cell Res 312 (2006) 3260-3275
58. Ang A.L., Taguchi T., Francis S., Folsch H., Murrells L.J., Pypaert M., Warren G., and Mellman I. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 167 (2004) 531-543
59. Carlton J.G., and Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316 (2007) 1908-1912
60. Dukes J.D., Richardson J.D., Simmons R., and Whitley P. A dominant negative ESCRT-III protein perturbs cytokinesis and trafficking to lysosomes. Biochem J (2007)
61. Morita E., Sandrin V., Chung H.Y., Morham S.G., Gygi S.P., Rodesch C.K., and Sundquist W.I. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26 (2007) 4215-4227. These three manuscripts independently provide evidence that components of the ESCRT complexes and accessory proteins involved in sorting and membrane invagination events during multi-vesicular body biogenesis, localize to the intercellular bridge and are essential for the terminal step of cytokinesis.
62. Hanson P.I., Roth R., Lin Y., and Heuser J.E. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J Cell Biol 180 (2008) 389-402
63. Kasahara K., Nakayama Y., Nakazato Y., Ikeda K., Kuga T., and Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem 282 (2007) 5327-5339
64. Emoto K., Inadome H., Kanaho Y., Narumiya S., and Umeda M. Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J Biol Chem 280 (2005) 37901-37907
65. Field S.J., Madson N., Kerr M.L., Galbraith K.A., Kennedy C.E., Tahiliani M., Wilkins A., and Cantley L.C. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr Biol 15 (2005) 1407-1412
66. Wong R., Hadjiyanni I., Wei H.C., Polevoy G., McBride R., Sem K.P., and Brill J.A. PIP2 hydrolysis and calcium release are required for cytokinesis in Drosophila spermatocytes. Curr Biol 15 (2005) 1401-1406
67. Brill J.A., Hime G.R., Scharer-Schuksz M., and Fuller M.T. A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis. Development 127 (2000) 3855-3864
68. Honda A., Nogami M., Yokozeki T., Yamazaki M., Nakamura H., Watanabe H., Kawamoto K., Nakayama K., Morris A.J., Frohman M.A., et al. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99 (1999) 521-532
69. Ng M.M., Chang F., and Burgess D.R. Movement of membrane domains and requirement of membrane signaling molecules for cytokinesis. Dev Cell 9 (2005) 781-790
70. Fan J., and Beck K.A. A role for the spectrin superfamily member Syne-1 and kinesin II in cytokinesis. J Cell Sci 117 (2004) 619-629
71. Delcros J.-G., Prigent C., and Giet R. Dynactin targets Pavarotti-KLP to the central spindle during anaphase and facilitates cytokinesis in Drosophila S2 cells. J Cell Sci 119 (2006) 4431-4441
72. Arden S.D., Puri C., Au J.S., Kendrick-Jones J., and Buss F. Myosin VI is required for targeted membrane transport during cytokinesis. Mol Biol Cell 18 (2007) 4750-4761. The Myosin VI motor is found to localize to the contractile actomyosin ring and subsequently to the midbody in late cytokinesis. In live-cell imaging of mammalian cells at cytokinesis, Myosin VI is observed on vesicles trafficking in both directions into the intercellular bridge some of which contain the transferrin-receptor. This observation together with the fact that alteration of Myosin VI activity leads to cytokinesis defects and multinucleated cells suggest that vesicular movements in and out of the midbody are required for successful cytokinesis.
73. Dunster K., Toh B.H., and Sentry J.W. Early endosomes, late endosomes, and lysosomes display distinct partitioning strategies of inheritance with similarities to Golgi-derived membranes. Eur J Cell Biol 81 (2002) 117-124
74. Shorter J., and Warren G. Golgi architecture and inheritance. Annu Rev Cell Dev Biol 18 (2002) 379-420