COPI-mediated membrane trafficking is required for cytokinesis in drosophila male meiotic divisions

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3649-3660

  Kitazawa, Daishi ^a   Yamaguchi, Masamitsu ^a   Mori, Hajime ^a   Inoue, Yoshihiro H ^a  

^a KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Cell division; COPI; Cytokinesis; Drosophila melanogaster; Meiosis

Indexed keywords

COATOMER PROTEIN COMPLEX; DYNEIN ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; CYTOKINESIS; CYTOPLASM; DROSOPHILA; GENE SILENCING; GOLGI COMPLEX; INHERITANCE; MICROTUBULE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SPERMATOCYTE;

ANIMALS; CHROMOSOME SEGREGATION; COAT PROTEIN COMPLEX I; CYTOKINESIS; DROSOPHILA MELANOGASTER; MALE; MEIOSIS; MICROTUBULES; SPERMATOCYTES;

DROSOPHILA MELANOGASTER;

EID: 84869099034     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.103317     Document Type: Article

References (70)

1. Albertson, R., Riggs, B. and Sullivan, W. (2005). Membrane traffic: a driving force in cytokinesis. Trends Cell Biol. 15, 92-101.
2. Albertson, R., Cao, J., Hsieh, T.-S. and Sullivan, W. (2008). Vesicles and actin are targeted to the cleavage furrow via furrow microtubules and the central spindle. J. Cell Biol. 181, 777-790.
3. Altan-Bonnet, N., Phair, R. D., Polishchuk, R. S., Weigert, R. and Lippincott- Schwartz, J. (2003). A role for Arf1 in mitotic golgi disassembly, chromosome segregation, and cytokinesis. Proc. Natl. Acad. Sci. U S A. 100, 13314-13319.
4. Arai, S., Noda, Y., Kainuma, S., Wada, I. and Yoda, K. (2008). Ypt11 functions in bud-directed transport of the Golgi by linking Myo2 to the coatomer subunit Ret2. Curr. Biol. 18, 987-991.
5. Barbosa, V., Yamamoto, R. R., Henderson, D. S. and Glover, D. M. (2000). Mutation of a Drosophila gamma tubulin ring complex subunit encoded by discs degenerate-4 differentially disrupts centrosomal protein localization. Genes Dev. 14, 3126-3139.
6. Beller, M., Sztalryd, C., Southall, N., Bell, M., Jäckle, H., Auld, D. S. and Oliver, B. (2008). COPI complex is a regulator of lipid homeostasis. PLoS Biol. 6, e292.
7. Bobinnec, Y., Marcaillou, C., Morin, X. and Debec, A. (2003). Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell Motil. Cytoskeleton 54, 217-225.
8. Bonaccorsi, S., Giansanti, M. G. and Gatti, M. (1998). Spindle self-organization and cytokinesis during male meiosis in asterless mutants of Drosophila melanogaster. J. Cell Biol. 142, 751-761.
9. Bonaccorsi, S., Giansanti, M. G., Cenci, G. and Gatti, M. (2000). Cytological analysis of spermatocytes growth and male meiosis in Drosophila melanogaster.In Drosophila Protocol (ed. W. Sullivan, M. Ashburner and R. S. Hawley), pp. 87- 109. New York: Cold Spring Harbor Laboratory Press Ltd.
10. Boucrot, E. and Kirchhausen, T. (2007). Endosomal recycling controls plasma membrane area during mitosis. Proc. Natl. Acad. Sci. USA 104, 7939-7944.
11. Cao, J., Albertson, R., Riggs, B., Field, C. M. and Sullivan, W. (2008). Nuf, a Rab11 effector, maintains cytokinetic furrow integrity by promoting local actin polymerization. J. Cell Biol. 182, 301-313.
12. Cao, L. G. and Wang, Y. L. (1996). Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol. Biol. Cell 7, 225-232
13. Castrillon, D. H., Gönczy, P., Alexander, S., Rawson, R., Eberhart, C. G., Viswanathan, S., DiNardo, S. and Wasserman, S. A. (1993). Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135, 489- 505.
14. Cermelli, S., Guo, Y., Gross, S. P. and Welte, M. A. (2006). The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr. Biol. 16, 1783-1795
15. Civelekoglu-Scholey, G., Tao, L., Brust-Mascher, I., Wollman, R. and Scholey, J. M. (2010). Prometaphase spindle maintenance by an antagonistic motor-dependent force balance made robust by a disassembling lamin-B envelope. J. Cell Biol. 188, 49- 68.
16. D'Avino, P. P., Savoian, M. S. and Glover, D. M. (2005). Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118, 1549-1558.
17. Dorogova, N. V., Nerusheva, O. O. and Omelyanchuk, L. V. (2009). Structural organization and dynamics of the endoplasmic reticulum during spermatogenesis of Drosophila melanogaster: Studies using PDI-GFP chimera protein. Biochemistry (Moscow). Supplement. Series A, Membrane and Cell Biology 3, 55-61.
18. Duden, R., Kajikawa, L., Wuestehube, L. and Schekman, R. (1998). epsilon-COP is a structural component of coatomer that functions to stabilize alpha-COP. EMBO J. 17, 985-995.
19. Dyer, N., Rebollo, E., Domínguez, P., Elkhatib, N., Chavrier, P., Daviet, L., González, C. and González-Gaitán, M. (2007). Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134, 4437-4447.
20. Echard, A., Hickson, G. R., Foley, E. and O'Farrell, P. H. (2004). Terminal cytokinesis events uncovered after an RNAi screen. Curr. Biol. 14, 1685-1693.
21. Eggert, U. S., Kiger, A. A., Richter, C., Perlman, Z. E., Perrimon, N., Mitchison, T. J. and Field, C. M. (2004). Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets. PLoS Biol. 2, e379.
22. Farkas, R. M., Giansanti, M. G., Gatti, M. and Fuller, M. T. (2003). The Drosophila Cog5 homologue is required for cytokinesis, cell elongation, and assembly of specialized Golgi architecture during spermatogenesis. Mol. Biol. Cell 14, 190-200
23. Fuller, M. T. (1993). Spermatogenesis. In The development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 71-147. New York: Cold Spring Harbor Press Ltd.
24. Giansanti, M. G., Bonaccorsi, S., Williams, B., Williams, E. V., Santolamazza, C., Goldberg, M. L. and Gatti, M. (1998). Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev. 12, 396- 410.
25. Giansanti, M. G., Bonaccorsi, S., Kurek, R., Farkas, R. M., Dimitri, P., Fuller, M. T. and Gatti, M. (2006). The class I PITP giotto is required for Drosophila cytokinesis. Curr. Biol. 16, 195-201.
26. Giansanti, M. G., Belloni, G. and 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.
27. Glotzer, M. (2001). Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351-386
28. Goldberg, M. L., Gunsalus, K. C., Karess, R. E. and Chang, F. (1998). Cytokinesis in Dynamics of Cell Division (ed. S. A. Endow and D. M. Glover), pp. 270-316. London: Oxford University Press Ltd.
29. Grieder, N. C., Kloter, U. and Gehring, W. J. (2005). Expression of COPI components during development of Drosophila melanogaster. Gene Expr. Patterns 6, 11-21.
30. Grieder, N. C., Caussinus, E., Parker, D. S., Cadigan, K., Affolter, M. and Luschnig, S. (2008). gammaCOP is required for apical protein secretion and epithelial morphogenesis in Drosophila melanogaster. PLoS ONE 3, e3241.
31. Griffiths, G., Pepperkok, R., Locker, J. K. and Kreis, T. E. (1995). Immunocytochemical localization of b-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108,2839- 2856.
32. Hernandez-Verdun, D. (2011). Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2, 189-194.
33. Hernandez-Verdun, D., Roussel, P. and Gébrane-Younès, J. (2002). Emerging concepts of nucleolar assembly. J. Cell Sci. 115, 2265-2270.
34. Hosobuchi, M., Kreis, T. and Schekman, R. (1992). SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer. Nature 360, 603-605.
35. Ichihara, K., Shimizu, H., Taguchi, O., Yamaguchi, M. and Inoue, Y. H. (2007). A Drosophila orthologue of larp protein family is required for multiple processes in male meiosis. Cell Struct. Funct. 32, 89-100.
36. Inoue, Y. H., Savoian, M., Suzuki, T., Máthé, E., Yamamoto, M. T. and Glover, D. M. (2004). Mutation 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.
37. Inoue, Y. H., Miyauchi, C., Ogata, T. and Kitazawa, D. (2011). Dynamic alteration of cellular component of male meiosis in Drosophila. In Meiosis (ed. A. Swan). Croatia, China: InTech Open Access Publisher.
38. Jayaram, S. A., Senti, K-A., Tiklová, K., Tsarouhas, V., Hemphälä, J. and Samakovlis, C. (2008). COPI vesicle transport is a common requirement for tube expansion in Drosophila. PLoS ONE 3, e1964.
39. Kamena, F., Diefenbacher, M., Kilchert, C., Schwarz, H. and Spang, A. (2008). Ypt1p is essential for retrograde Golgi-ER transport and for Golgi maintenance in S. cerevisiae. J. Cell Sci. 121, 1293-1302.
40. Kemphues, K. J., Raff, E. C., Raff, R. A. and Kaufman, T. C. (1980). Mutation in a testis-specific beta-tubulin in Drosophila: analysis of its effects on meiosis and map location of the gene. Cell 21, 445-451.
41. Kirchner, J., Vissi, E., Gross, S., Szoor, B., Rudenko, A., Alphey, L. and White- Cooper, H. (2008). Drosophila Uri, a PP1a binding protein, is essential for viability, maintenance of DNA integrity and normal transcriptional activity. BMC Mol. Biol. 9, 36.
42. Kondylis, V. and Rabouille, C. (2009). The Golgi apparatus: lessons from Drosophila. FEBS Lett. 583, 3827-3838.
43. Lippincott-Schwartz, J., Cole, N. B. and Donaldson, J. G. (1998). Building a secretory apparatus: role of ARF1/COPI in Golgi biogenesis and maintenance. Histochem. Cell Biol. 109, 449-462.
44. Liu, Z. and Zheng, Y. (2009). A requirement for epsin in mitotic membrane and spindle organization. J. Cell Biol. 186, 473-480.
45. Maines, J. and Wasserman, S. (1997). Regulation and execution of meiosis in Drosophila males. Curr. Top. Dev. Biol. 37, 301-332.
46. Mishima, M. and Glotzer, M. (2003). Cytokinesis: a logical GAP. Curr. Biol. 13, R589-R591.
47. Montagnac, G., Echard, A. and Chavrier, P. (2008). Endocytic traffic in animal cell cytokinesis. Curr. Opin. Cell Biol. 20, 454-461.
48. Moreno, R. D., Ramalho-Santos, J., Sutovsky, P., Chan, E. K. and Schatten, G. (2000). Vesicular traffic and golgi apparatus dynamics during mammalian spermatogenesis: implications for acrosome architecture. Biol. Reprod. 63, 89-98.
49. Oprins, A., Duden, R., Kreis, T. E., Geuze, H. J. and Slot, J. W. (1993). Beta-COP localizes mainly to the cis-Golgi side in exocrine pancreas. J. Cell Biol. 121, 49-59
50. Papoulas, O., Hays, T. S. and Sisson, J. C. (2005). The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat. Cell Biol. 7, 612-618.
51. Polevoy, G., Wei, H.-C., Wong, R., Szentpetery, Z., Kim, Y. J., Goldbach, P., Steinbach, S. K., Balla, T. and Brill, J. A. (2009). Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J. Cell Biol. 187, 847-858.
52. Prekeris, R. and Gould, G. W. (2008). Breaking up is hard to do - membrane traffic in cytokinesis. J. Cell Sci. 121, 1569-1576.
53. Rabouille, C. and Jokitalo, E. (2003). Golgi apparatus partitioning during cell division. Mol. Membr. Biol. 20, 117-127.
54. Rebollo, E. and González, C. (2000). Visualizing the spindle checkpoint in Drosophila spermatocytes. EMBO Rep. 1, 65-70.
55. Rebollo, E., Llamazares, S., Reina, J. and Gonzalez, C. (2004). Contribution of noncentrosomal microtubules to spindle assembly in Drosophila spermatocytes. PLoS Biol. 2, e8.
56. Ripoche, J., Link, B., Yucel, J. K., Tokuyasu, K. and Malhotra, V. (1994). Location of Golgi membranes with reference to dividing nuclei in syncytial Drosophila embryos. Proc. Natl. Acad. Sci. USA 91, 1878-1882.
57. Robinett, C. C., Giansanti, M. G., Gatti, M. and Fuller, M. T. (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.
58. Rogers, G. C., Rusan, N. M., Peifer, M. and Rogers, S. L. (2008). A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells. Mol. Biol. Cell 19, 3163-3178.
59. Satterwhite, L. L. and Pollard, T. D. (1992). Cytokinesis. Curr. Opin. Cell Biol. 4, 43- 52.
60. Shima, D. T., Cabrera-Poch, N., Pepperkok, R. and Warren, G. (1998). An ordered inheritance strategy for the Golgi apparatus: visualization of mitotic disassembly reveals a role for the mitotic spindle. J. Cell Biol. 141, 955-966.
61. Simon, G. C., Schonteich, E., Wu, C. C., Piekny, A., Ekiert, D., Yu, X., Gould, G. W., Glotzer, M. and Prekeris, R. (2008). Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J. 27, 1791-1803.
62. Sisson, J. C., Field, C., Ventura, R., Royou, A. and Sullivan, W. (2000). Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J. Cell Biol. 151, 905-918.
63. Skop, A. R., Liu, H., Yates, J., 3rd, Meyer, B. J. and Heald, R. (2004). Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 305, 61-66.
64. Stafstrom, J. P. and Staehelin, L. A. (1984). Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the Drosophila embryo. Eur. J. Cell Biol. 34, 179-189.
65. Tates, A. D. (1971). Cytodifferentiation during spermatogenesis in Drosophila melanogaster: An electron microscope study. Ph.D. thesis. Rijksuniversiteit, Leiden, Netherlands.
66. Uehara, R., Nozawa, R. S., Tomioka, A., Petry, S., Vale, R. D., Obuse, C. and Goshima, G. (2009). The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 106, 6998-7003.
67. Wei, J. H. and Seemann, J. (2009). The mitotic spindle mediates inheritance of the Golgi ribbon structure. J. Cell Biol. 184, 391-397.
68. Xu, H., Brill, J. A., Hsien, J., McBride, R., Boulianne, G. L. and Trimble, W. S. (2002). Syntaxin 5 is required for cytokinesis and spermatid differentiation in Drosophila. Dev. Biol. 251, 294-306.
69. Zhao, W. M., Seki, A. and Fang, G. (2006). Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis. Mol. Biol. Cell 17, 3881-3896.
70. Zheng, Y. (2010). A membranous spindle matrix orchestrates cell division. Nat. Rev. Mol. Cell Biol. 11, 529-535.