What Drosophila spermatocytes tell us about the mechanisms underlying cytokinesis

Cytoskeleton

Volumn 69, Issue 11, 2012, Pages 869-881

  Giansanti, Maria Grazia ^a   Fuller, Margaret T ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell cycle; Cytokinesis; Cytoskeleton; Drosophila; Membrane trafficking

Indexed keywords

AURORA B KINASE; F ACTIN; MYOSIN II; PEROXIN; POLO LIKE KINASE 1; RHO FACTOR; VERY LONG CHAIN FATTY ACID;

ACTIN POLYMERIZATION; ANAPHASE; CELL CYCLE CHECKPOINT; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIVISION; CELL MIGRATION; CELL MUTANT; CELL SIZE; CENTROSOME; CHROMOSOME SEGREGATION; CYTOKINESIS; CYTOSKELETON; DROSOPHILA; GENE SILENCING; GENETIC SCREENING; INSECT CHROMOSOME; MEIOSIS; MITOSIS; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM;

ANIMALS; CELL CYCLE CHECKPOINTS; CYTOKINESIS; DROSOPHILA MELANOGASTER; MALE; MEIOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; SPERMATOCYTES;

EID: 84869499939     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21063     Document Type: Review

References (135)

1. Adam JC, Pringle JR, Peifer M. 2000. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol Biol Cell 11: 3123-3135.
2. Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM. 1998. Pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev 12: 1483-1494.
3. Adams RR, Wheatley SP, Gouldsworthy AM, Kandels-Lewis SE, Carmena M, Smythe C, Gerloff DL, Earnshaw WC. 2000. INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow. Curr Biol 10: 1075-1078.
4. Adams RR, Maiato H, Earnshaw WC, Carmena M. 2001. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J Cell Biol 153: 865-880.
5. Aoki T, Ichimura S, Itoh A, Kuramoto M, Shinkawa T, Isobe T, Tagaya M. 2009. Identification of the neuroblastoma-amplified gene product as a component of the syntaxin 18 complex implicated in Golgi-to-endoplasmic reticulum retrograde transport. Mol Biol Cell 20: 2639-2649.
6. Arasaki K, Taniguchi M, Tani K, Tagaya M. 2006. RINT-1 regulates the localization and entry of ZW10 to the syntaxin 18 complex. Mol Biol Cell 17: 2780-2788.
7. Barr FA, Gruneberg E. 2007. Cytokinesis: placing the final cut. Cell 131: 847-860.
8. Barr FA, Sillje HH, Nigg EA. 2004. Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5: 429-440.
9. Bathe M, Chang F. 2010. Cytokinesis and the contractile ring in fission yeast: towards a systems-level understanding. Trends Microbiol 18: 38-45.
10. Belloni G, Sechi S, Riparbelli MG, Fuller MT, Callaini G, Giansanti MG. 2012. Mutations in Cog7 affect Golgi structure, meiotic cytokinesis and sperm development during Drososphila spermatogenesis. J Cell Sci; doi: 10.1242/jcs.108878.
11. Bertin A, McMurray MA, Thai L, Garcia G 3rd, 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( 4): 711-731.
12. Bobinnec Y, Marcaillou C, Morin X, Debec A. 2003. Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell Motil Cytoskeleton 54( 3): 217-225.
13. Bonaccorsi S, Giansanti MG, Gatti M. 1998. Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J Cell Biol 142: 51-61.
14. Brennan IM, Peters U, Kapoor TM, Straight AF. 2007. Polo-like kinase controls vertebrate spindle elongation and cytokinesis. PLoS One 2: e409.
15. Brill JA, Hime GR, Scharer-Schuksz M, Fuller MT. 2000. A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis. Development 127: 3855-3864.
16. Brill JA, Wong R, Wilde A. 2011. Phosphoinositide function in cytokinesis. Curr Biol 21: R930-R934.
17. Bringmann H, Hyman AA. 2005. Cytokinesis furrow is positioned by two consecutive signals. Nature 436: 731-734.
18. Bucciarelli E, Giansanti MG, Bonaccorsi S, Gatti M. 2003. Spindle assembly and cytokinesis in the absence of chromosomes during Drosophila male meiosis. J Cell Biol 160: 993-999.
19. Burkard ME, Maciejowski J, Rodriguez-Bravo V, Repka M, Lowery DM, Clauser KR, Zhang C, Shokat KM, Carr SA, Yaffe MB, Jallepalli PV. 2009. Plk1 self-organization and priming phosphorylation of HsCYK-4 at the spindle midzone regulate the onset of division in human cells. PLoS Biol 7: e1000111.
20. Cabernard C, Prehoda KE, Doe CQ. 2010. A spindle-independent cleavage furrow positioning pathway. Nature 467: 91-95.
21. Carmena M. 2008. Cytokinesis: the final stop for the chromosomal passengers. Biochem Soc Trans 36: 367-370.
22. Carmena M, Riparbelli MG, Minestrini G, Tavares AM, Adams R, Callaini G, Glover DM. 1998. Drosophila polo kinase is required for cytokinesis. J Cell Biol 143: 659-671.
23. Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP. 2003. Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116: 2987-2998.
24. Carvalho A, Desai A, Oegema K. 2009. Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 137: 926-937.
25. Chen H, Liu Z, Huang X. 2010. Drosophila models of peroxisomal biogenesis disorder: peroxins are required for spermatogenesis and very-long-chain fatty acid metabolism. Hum Mol Genet 19: 494-505.
26. Church K, Lin HP. 1982. Meiosis in Drosophila melanogaster. II. The prometaphase-I kinetochore microtubule bundle and kinetochore orientation in males. J Cell Biol 93: 365-373.
27. D'Avino PP. 2009. How to scaffold the contractile ring for a safe cytokinesis-lessons from anillin-related proteins. J Cell Sci 122: 1071-1079.
28. 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.
29. D'Avino PP, Archambault V, Przewloka MR, Zhang W, Lilley KS, Laue E, Glover DM. 2007. Recruitment of Polo kinase to the spindle midzone during cytokinesis requires the Feo/Klp3A complex. PLoS One 2: e572.
30. D'Avino PP, Takeda T, Capalbo L, Zhang W, Lilley KS, Laue E, 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.
31. Dechant R, Glotzer M. 2003. Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev Cell 4: 333-344.
32. Douglas ME, Davies T, Joseph N, Mishima M. 2010. Aurora B and 14-3-3 coordinately regulate clustering of centralspindlin during cytokinesis. Curr Biol 20: 927-933.
33. Dyer N, Rebollo E, Domínguez P, Elkhatib N, Chavrier P, Daviet L, González C, González-Gaitán M. 2007. Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134: 4437-4447.
34. Eggert US, Mitchison TJ, Field CM. 2006. Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 75: 543-566.
35. Farkas RM, Giansanti MG, Gatti M, Fuller MT. 2003. Drosophila Cog5/COG4 is required for cytokinesis, polarized cell growth and normal Golgi architecture during spermatogenesis. Mol Biol Cell 14: 190-200.
36. Field CM, al-Awar O, Rosenblatt J, Wong ML, Alberts B, Mitchison TJ. 1996. A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J Cell Biol 133: 605-616.
37. Fuller MT. 1993. Spermatogenesis. In: Bate M, Martinez-Arias A, editors. The Development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Press. pp 71-147.
38. Fuller MT, Spradling AC. 2007. Male and female Drosophila germline stem cells: two versions of immortality. Science 316( 5823): 402-404.
39. Gao S, Giansanti MG, Buttrick GJ, Ramasubramanyan S, Auton A, Gatti M, Wakefield JG. 2008. Australin: a chromosomal passenger protein required specifically for Drosophila melanogaster male meiosis. J Cell Biol 180: 521-535.
40. Gassmann R, Carvalho A, Henzing AJ, Ruchaud S, Hudson DF, Honda R, Nigg EA, Gerloff DL, Earnshaw WC. 2004. Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J Cell Biol 166: 179-191.
41. Gatt MK, Glover DM. 2006. The Drosophila phosphatidylinositol transfer protein encoded by vibrator is essential to maintain cleavage-furrow ingression in cytokinesis. J Cell Sci 119: 2225-2235.
42. Giansanti MG, Bonaccorsi S, Williams B, Williams EV, Santolamazza C, Goldberg ML, Gatti M. 1998. Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev 12: 396-410.
43. Giansanti MG, Bonaccorsi S, Gatti M. 1999. The role of anillin in meiotic cytokinesis of Drosophila males. J Cell Sci 112: 2323-2334.
44. Giansanti MG, Bonaccorsi S, Bucciarelli E, Gatti M. 2001. Drosophila male meiosis as a model system for the study of cytokinesis in animal cells. Cell Struct Funct 26: 609-617.
45. Giansanti MG, Farkas RM, Bonaccorsi S, Lindsley DL, Wakimoto BT, Fuller MT, Gatti M. 2004. Genetic dissection of meiotic cytokinesis in Drosophila. Mol Biol Cell 15: 2509-2522.
46. Giansanti MG, Bonaccorsi S, Kurek R, Farkas RM, Dimitri P, Fuller MT, Gatti M. 2006. The class I PITP giotto is required for Drosophila cytokinesis. Curr Biol 16: 195-201.
47. Giansanti MG, Belloni G, Gatti M. 2007. Rab11 is required for membrane trafficking and actomyosin ring constriction in meiotic cytokinesis of Drosophila males. Mol Biol Cell 18: 5034-5047.
48. Giansanti MG, Bucciarelli E, Bonaccorsi S, Gatti M. 2008. Drosophila SPD-2 is an essential centriole component required for PCM recruitment and astral-microtubule nucleation. Curr Biol 18: 303-309.
49. Giet R, Glover DM. 2001. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152: 669-682.
50. Glotzer M. 2005. The molecular requirements for cytokinesis. Science 307: 1735-1739.
51. Glotzer M. 2009. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 10( 1): 9-20.
52. Goldbach P, Wong R, Beise N, Sarpal R, Trimble WS, Brill JA. 2010. Stabilization of the actomyosin ring enables spermatocyte cytokinesis in Drosophila. Mol Biol Cell 21: 1482-1493.
53. Goode BL, Ect MJ. 2007. Mechanisms and function of formins in the control of actin assembly. Annu Rev Biochem 76: 593-627.
54. Green RA, Paluch E, Oegema K. 2012. Cytokinesis in Animal Cells. Annu Rev Cell Dev Biol; DOI: 10.1146/annurev-cellbio-101011-155718.
55. Gregory SL, Ebrahimi S, Milverton J, Jones WM, Bejsovec A, Saint R. 2008. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol 18( 1): 25-9.
56. Gunsalus KC, Bonaccorsi S, Williams E, Verni F, Gatti M, Goldberg ML. 1995. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J Cell Biol 131: 1243-1259.
57. Guse A, Mishima M, Glotzer M. 2005. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis. Curr Biol 15: 778-786.
58. Herrmann S, Amorim I, Sunkel CE. 1998. The POLO kinase is required at multiple stages during spermatogenesis in Drosophila melanogaster. Chromosoma 107: 440-451.
59. Hime GR, Brill JA, Fuller MT. 1996. Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci 109: 2779-2788.
60. Hirose H, Arasaki K, Dohmae N, Takio K, Hatsuzawa K, Nagahama M, Tani K, Yamamoto A, Tohyama M, Tagaya M. 2004. Implication of ZW10 in membrane trafficking between the endoplasmic reticulum and Golgi. EMBO J 23: 1267-1278.
61. Honda R, Körner R, Nigg EA. 2003. Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol Biol Cell 14: 3325-3341.
62. Inoue YH, Savoian MS, Suzuki T, Máthé 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.
63. Jordan P, Karess R. 1997. Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J Cell Biol 139: 1805-1819.
64. Kamijo K, Ohara N, Abe M, Uchimura T, Hosoya H, Lee JS, Miki T. 2006. Dissecting the role of Rho-mediated signaling in contractile ring formation. Mol Biol Cell 17: 43-55.
65. Karess R. 2005. Rod-Zw10-Zwilch: a key player in the spindle checkpoint. Trends Cell Biol 15: 386-932.
66. Kee YS, Ren Y, Dorfman D, Iijima M, Firtel R, Iglesias PA, Robinson DN. 2012. A mechanosensory system governs myosin II accumulation in dividing cells. Mol Biol Cell 23( 8): 1510-1523.
67. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ. 2002. Self- and actin-templated assembly of mammalian septins. Dev Cell 3: 791-802.
68. Kitazawa D, Yamaguchi M, Mori H, Inoue YH. 2012. COPI-mediated membrane trafficking is required for cytokinesis in Drosophila male meiotic divisions. J Cell Sci; doi: 10.1242/jcs.103317.
69. Kondylis V, Rabouille C. 2009. The Golgi apparatus: lessons from Drosophila. FEBS Lett 583: 3827-3838.
70. Kramerova IA, Kramerov AA. 1999. Mucinoprotein is a universal constituent of stable intercellular bridges in Drosophila melanogaster germ line and somatic cells. Dev Dyn 216: 349-360.
71. Lacroix B, Maddox AS. 2012. Cytokinesis, ploidy and aneuploidy. J Pathol 226: 338-351.
72. Lens SM, Rodriguez JA, Vader G, Span SW, Giaccone G, Medema RH. 2006. Uncoupling the central spindle-associated function of the chromosomal passenger complex from its role at centromeres. Mol Biol Cell 17: 1897-1909.
73. Lewellyn L, Dumont J, Desai A, Oegema K. 2010. Analyzing the effects of delaying aster separation on furrow formation during cytokinesis in the Caenorhabditis elegans embryo. Mol Biol Cell 21( 1): 50-62.
74. Lewellyn L, Carvalho A, Desai A, Maddox AS, Oegema K. 2011. The chromosomal passenger complex and centralspindlin independently contribute to contractile ring assembly. J Cell Biol 193: 155-169.
75. Lind GE, Raiborg C, Danielsen SA, Rognum TO, Thiis-Evensen E, Hoff G, Nesbakken A, Stenmark H, Lothe RA. 2011. SPG20, a novel biomarker for early detection of colorectal cancer, encodes a regulator of cytokinesis. Oncogene 30: 3967-3978.
76. Lindsley DL, Tokuyasu KT. 1980. Spermatogenesis. In: Ashburner M, Wright TRF, editors. Genetics and Biology of Drosophila. New York: Academic Press. pp 225-294.
77. Liu J, Fairn GD, Ceccarelli DF, Sicheri F, Wilde A. 2012. Cleavage furrow organization requires PIP(2)-mediated recruitment of anillin. Curr Biol 22( 1): 64-69.
78. Llamazares S, Moreira A, Tavares A, Girdham C, Spruce BA, Gonzalez C, Karess RE, Glover DM, Sunkel CE. 1991. Polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev 5: 2153-2165.
79. Ma X, Kovács M, Conti MA, Wang A, Zhang Y, Sellers JR, Adelstein RS. 2012. Nonmuscle myosin II exerts tension but does not translocate actin in vertebrate cytokinesis. Proc Natl Acad Sci USA 109( 12): 4509-4514.
80. Matsumara F, Yamakita Y, Yamashiro S. 2011. Myosin light chain kinases and phosphatase in mitosis and cytokinesis. Arch Biochem Byophys 510: 76-82.
81. McKay HF, Burgess DR. 2011. 'Life is a highway': membrane trafficking during cytokinesis. Traffic 12: 247-251.
82. Miller AL. 2011. The contractile ring. Curr Biol 21( 24): R976-R978.
83. Miller KG, Field CM, Alberts BM. 1989. Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatography. J Cell Biol 109: 2963-2975.
84. Montembault E, Zhang W, Przewloka MR, Archambault V, Sevin EW, Laue ED, Glover DM, D'Avino PP. 2010. Nessun Dorma, a novel centralspindlin partner, is required for cytokinesis in Drosophila spermatocytes. J Cell Biol 191: 1351-1365.
85. Musacchio A, Salmon ED. 2007. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393.
86. Neef R, Klein UR, Kopajtich R, Barr FA. 2006. Cooperation between mitotic kinesins controls the late stages of cytokinesis. Curr Biol 16: 301-307.
87. Neto H, Collins LL, Gould GW. 2011. Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 437: 13-24.
88. Nishimura Y, Yonemura S. 2006. Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 119: 104-114.
89. Normand G, King RW. 2010. Understanding cytokinesis failure. Adv Exp Med Biol 676: 27-55.
90. Ono S. 2007. Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int Rev Cytol. 258: 1-82.
91. Piekny A, Werner M, Glotzer M. 2005. Cytokinesis: welcome to the Rho zone. Trends Cell Biol 15: 651-658.
92. Polevoy G, Wei HC, Wong R, Szentpetery Z, Kim YJ, Goldbach P, Steinbach SK, Balla T, Brill JA. 2009. Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J Cell Biol 187: 847-858.
93. Pollard TD. 2010. Mechanics of cytokinesis in eukaryotes. Curr Opin Cell Biol. 22( 1): 50-56.
94. Pollard TD, Wu JQ. 2010. Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 11: 149-155.
95. Prekeris R, Gould GW. 2008. Breaking up is hard to do-membrane traffic in cytokinesis. J Cell Sci 121: 1569-1576.
96. Rappaport R. 1961. Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 148: 81-89.
97. Rebollo E, Gonzalez C. 2000. Visualizing the spindle checkpoint in Drosophila spermatocytes. EMBO Rep 1: 65-70.
98. Reichl EM, Ren Y, Morphew MK, Delannoy M, Effler JC, Girard KD, Divi S, Iglesias PA, Kuo SC, Robinson DN. 2008. Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr Biol 18( 7): 471-480.
99. Resnick TD, Satinover DL, MacIsaac F, Stukenberg PT, Earnshaw WC, Orr-Weaver TL, Carmena M. 2006. INCENP and Aurora B promote meiotic sister chromatid cohesion through localization of the Shugoshin MEI-S332 in Drosophila. Dev Cell 11: 57-68.
100. Riparbelli MG, Callaini G, Glover DM, Avides Mdo C. 2002. A requirement for the Abnormal Spindle protein to organise microtubules of the central spindle for cytokinesis in Drosophila. J Cell Sci 115: 913-922.
101. Robinett CC, Giansanti MG, Gatti M, Fuller MT. 2009. TRAPPII is required for cleavage furrow ingression and localization of Rab11 in dividing male meiotic cells of Drosophila. J Cell Sci 122: 4526-4534.
102. Roversi G, Pfundt R, Moroni RF, Magnani I, van Reijmersdal S, Pollo B, Straatman H, Larizza L, Schoenmakers EF. 2006. Identification of novel genomic markers related to progression to glioblastoma through genomic profiling of 25 primary glioma cell lines. Oncogene 25: 1571-1583.
103. Ruchaud S, Carmena M, Earnshaw WC. 2007a Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
104. Ruchaud S, Carmena M, Earnshaw WC. 2007b The chromosomal passenger complex: one for all and all for one. Cell 131: 230-231.
105. Santamaria A, Neef R, Eberspächer U, Eis K, Husemann M, Mumberg D, Prechtl S, Schulze V, Siemeister G, Wortmann L, Barr FA, Nigg EA. 2007. Use of the novel Plk1 inhibitor ZK-thiazolidinone to elucidate functions of Plk1 in early and late stages of mitosis. Mol Biol Cell 18: 4024-4036.
106. Satterwhite LL, Pollard TD. 1992. Cytokinesis. Curr Opin Cell Biol 4: 43-52.
107. Saunders RD, Avides MC, Howard T, Gonzalez C, Glover DM. 1997. The Drosophila gene abnormal spindle encodes a novel microtubule-associated protein that associates with the polar regions of the mitotic spindle. J Cell Biol 137( 4): 881-890.
108. Scaerou F, Starr DA, Piano F, Papoulas O, Karess RE, Goldberg ML. 2001. The ZW10 and rough deal checkpoint proteins function together in a large, evolutionarily conserved complex targeted to the kinetochore. J Cell Sci 114: 3103-3114.
109. Schmitt HD. 2010. Dsl1p/Zw10: common mechanisms behind tethering vesicles and microtubules. Trends Cell Biol 20: 257-268.
110. Schneiter R, Brügger B, Amann CM, Prestwich GD, Epand RF, Zellnig G, Wieland FT, Epand RM. 2004. Identification and biophysical characterization of a very-long-chain-fatty-acid-substituted phosphatidylinositol in yeast subcellular membranes. Biochem J 381( 3): 941-949.
111. Schroeder TE. 1990. The contractile ring and furrowing in dividing cells. Ann N Y Acad Sci 582: 78-87.
112. Sinha S, Mondal G, Hwang EJ, Han da W, Dutta SK, Iyer S, Karumanchi SA, Kim KI, Couch FJ, Mukhopadhyay D. 2011. Von Hippel-Lindau gene product directs cytokinesis: a new tumor suppressor function. J Cell Sci 124: 2132-2142.
113. Sisson JC, Field C, Ventura R, Royou A, Sullivan W. 2000. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol 151: 905-918.
114. Somers WG, Saint R. 2003. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell 4: 29-39.
115. Starr DA, Williams BC, Hays TS, Goldberg ML. 1998. ZW10 helps recruit dynactin and dynein to the kinetochore. J Cell Biol 142: 763-774.
116. Straight AF, Field CM, Mitchison TJ. 2005. Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol Biol Cell 16: 193-201.
117. Sun Y, Shestakova A, Hunt L, Sehgal S, Lupashin V, Storrie B. 2007. Rab6 regulates both ZW10/RINT-1 and conserved oligomeric Golgi complex-dependent Golgi trafficking and homeostasis. Mol Biol Cell 18: 4129-4142.
118. Szafer-Glusman E, Giansanti MG, Nishihama R, Bolival B, Pringle J, Gatti M, Fuller MT. 2008. A role for very-long-chain fatty acids in furrow ingression during cytokinesis in Drosophila spermatocytes. Curr Biol 18: 1426-1431.
119. Szafer-Glusman E, Fuller MT, Giansanti MG. 2011. Role of Survivin in cytokinesis revealed by a separation-of-function allele. Mol Biol Cell 22: 3779-3790.
120. Tates AD. 1971. Cytodifferentiation during spermatogenesis in Drosophila melanogaster: an electron microscope study. PhD Thesis. Leiden, Netherlands: Rijksuniversiteit de leiden.
121. Vader G, Medema RH, Lens SM. 2006. The chromosomal passenger complex: guiding Aurora-B through mitosis. J Cell Biol 19: 833-837.
122. Vagnarelli P, Earnshaw WC. 2004. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 113: 211-222.
123. van der Waal MS, Hengeveld RC, van der Horst A, Lens SM. 2012. Cell division control by the chromosomal passenger complex. Exp Cell Res 318( 12): 1407-2140.
124. Varma D, Dujardin DL, Stehman SA, Vallee RB. 2006. Role of the kinetochore/cell cycle checkpoint protein ZW10 in interphase cytoplasmic dynein function. J Cell Biol 172: 655-662.
125. Vernì F, Somma MP, Gunsalus KC, Bonaccorsi S, Belloni G, Goldberg ML, Gatti M. 2004. Feo, the Drosophila homolog of PRC1, is required for central-spindle formation and cytokinesis. Curr Biol 14: 1569-1575.
126. Wainman A, Giansanti MG, Goldberg ML, Gatti M. 2012. The Drosophila RZZ complex: roles in membrane traffic and cytokinesis. J Cell Sci; doi: 10.1242/jcs.099820.
127. Wakefield JG, Bonaccorsi S, Gatti M. 2001. The Drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J Cell Biol 153: 637-648.
128. Williams BC, Riedy MF, Williams EV, Gatti M, Goldberg ML. 1995. The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis. J Cell Biol 129: 709-723.
129. Williams BC, Li Z, Liu S, Williams EV, Leung G, Yen TJ, Goldberg ML. 2003. Zwilch, a new component of the ZW10/ROD complex required for kinetochore functions. Mol Biol Cell 14: 1379-1391.
130. Wolfe BA, Takaki T, Petronczki M, Glotzer M. 2009. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol 7: e1000110.
131. 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.
132. Xu H, Brill JA, Hsien J, McBride R, Boulianne GL, Trimble WS. 2002. Syntaxin 5 is required for cytokinesis and spermatid differentiation in Drosophila. Dev Biol 251: 294-296.
133. Yin HL, Janmey PA. 2003. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65: 761-789.
134. Yuce O Piekny A Glotzer M. 2005. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 170: 571-582.
135. Zao WM, Fang G. 2005. MgcRacGAP controls the assembly of the contractile ring and the initiation of cytokinesis. Proc Natl Acad Sci USA 102: 13158-13163.