Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis

Genes and Development

Volumn 12, Issue 3, 1998, Pages 396-410

  Giansanti, Maria Grazia ^a   Bonaccorsi, Silvia ^a   Williams, Byron ^b   Williams, Erika V ^b   Santolamazza, Carlo ^a   Goldberg, Michael L ^b   Gatti, Maurizio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Cornell University ^*  (United States)

Author keywords

Central spindle; Chickadee mutations; Contractile ring; Cytokinesis; Drosophila; Profilin

Indexed keywords

CYTOCHALASIN; F ACTIN;

ACTIN FILAMENT; ALLELE; ANIMAL CELL; ARTICLE; CELL ULTRASTRUCTURE; CENTROSOME; CYTOKINESIS; DROSOPHILA MELANOGASTER; GENE LOCATION; GENETIC RECOMBINATION; MEIOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN POLYMERIZATION;

ANIMALIA; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0032006529     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.3.396     Document Type: Article

References (79)

1. Andreassen, P.R., D.K. Palmer, M.H. Weiner, and R.L. Margolis. 1991. Telophase disk: A new mammalian mitotic organelle that bisects telophase cells with a possible function in cytokinesis. J. Cell Sci. 99: 523-534.
2. Aubin, J.E., M. Osborn, and K. Weber. 1981. Inhibition of cytokinesis and altered contractile ring morphology induced by cytochalasins in synchronized PtK2 cells. Exp. Cell Res. 136: 63-79.
3. + gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125: 1289-1301.
4. Bier, B.S., H. Vaessin, S. Sheperd, K. Lee, K. McCall, S. Barbel, L. Ackerman, R. Carretto, T. Uemura, E. Grell et al. 1989. Searching for pattern and mutation in Drosophila genome with P-lacZ vector. Genes & Dev. 3: 1273-1287.
5. Byers, T.J., R. Dubreuil, D. Branton, D.P. Kiehart, and L.S.B. Goldstein. 1987. Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J. Cell Biol. 105: 2103-2110.
6. Cao, L.-G. and Y.-L. Wang. 1996. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol. Biol. Cell. 7: 225-232.
7. Carlsson, M., L.-E. Nystrom, I. Sundkvist, F. Markey, and U. Lindberg. 1977. Actin polymerizability is influenced by profilin, a low molecular weight protein in nonmuscle cells. J. Mol. Biol. 115: 465-483.
8. Castrillon, D.H. and S.A. Wasserman. 1994. diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120: 3367-3377.
9. Cenci, G., S. Bonaccorsi, C. Pisano, F. Verni, and M. Gatti. 1994. Chromatin and microtubule organization during premeiotic, meiotic, and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J. Cell Sci. 107: 3521-3534.
10. Chang, F., A. Woollard, and P. Nurse. 1996. Identification and characterization of fission yeast mutants defective in actin ring assembly and placement. J. Cell Sci. 109: 131-142.
11. _. 1997. cdc12, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol 137: 169-182.
12. Cooke, C.A., M.M.S. Heck, and W.C. Earnshaw. 1987. The INCENP antigens: Movement from the inner centromere to the midbody during mitosis. J. Cell Biol. 105: 1053-2067.
13. Cooley, L., E. Verheyen, and K. Ayers. 1992. chickadee encodes a profilin required for intercellular transport during Drosophila oogenesis. Cell 69: 173-184.
14. Cooper, J.A. 1987. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105: 1473-1478.
15. Earnshaw, W.C. and R.L. Bernat. 1990. Chromosomal passengers: Towards an integrated view of mitosis. Chromosoma 100: 139-146.
16. Earnshaw, W.C. and C.A. Cooke. 1991. Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of three distinct substages of metaphase and early events in cleavage furrow formation. J. Cell Sci. 98: 443-461.
17. Eckley, D.M., A.M. Ainsztein, A.M. MacKay, I.G. Goldberg, and W.C. Earnshaw. 1997. Chromosomal proteins and cytokinesis: Patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and midanaphase cells. J. Cell Biol. 136: 1169-1183.
18. Edamatsu, M., M. Hirono, and Y. Watanabe. 1992. Tetrahymena profilin is localized in the division furrow. J. Biochem. 112: 637-642.
19. Field, C. and B.M. Alberts. 1995. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131: 165-178.
20. Fishkind, D.J. and Y.-L. Wang. 1995. New horizons for cytokinesis. Curr. Opin. Cell Biol. 7: 23-31.
21. Fishkind, D.J., J.D. Silverman, and Y.-L. Wang. 1996. Function of spindle microtubules in directing cortical movements and actin filaments organization in dividing cultured cells. J. Cell Sci. 109: 2041-2051.
22. Fuller, M.T. 1993. Spermatogenesis. In The development of Drosophila melanogaster. Vol. I. (ed. M. Bate and A.M. Arias), pp. 71-147. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Gatti, M. and M.L. Goldberg. 1991. Mutations affecting cell divisions in Drosophila. Methods Cell Biol. 35: 543-586.
24. Giansanti, M.G., S. Bonaccorsi, B.C. Williams, K. Gunsalus, E.V. Williams, M.L. Goldberg, and M. Gatti. 1996. Genes controlling cytokinesis in Drosophila melanogaster male meiosis. In Proceedings on chromosome segregation and aneuploidy (ed. A. Abbondandolo, B.K. Vig, and R. Roy), pp. 304-316. Istituto Nazionale per la Ricerca sul Cancro (IST), Genoa, Italy.
25. Goldberg, M.L., K. Gunsalus, R.E. Karess, and F. Chang. 1997. Cytokinesis, or breaking up is hard to do. In Mechanics of cell division, (ed. S. Endow and D. Glover). Oxford University Press, London. (In press).
26. Goldschmidt-Clermont, P.J., J.W. Kim, L.M. Machesky, S.G. Rhee, and T.D. Pollard. 1991. Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. Science 251: 1231-1233.
27. Goldschmidt-Clermont, P.J., M.I. Furman, D. Wachsstock, D. Safer, V.T. Nachmias, and T.D. Pollard. 1992. The control of actin nucleotide exchange by thimosin β4 and profilin: A potential regulatory mechanism for actin polymerization in cells. Mol. Biol. Cell 3: 1015-1024.
28. Gonzalez, C., J. Casal, and P. Ripoll. 1989. Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. Genet. Res. 54: 205-212.
29. Griffith, L. and T.D. Pollard. 1978. Evidence for actin filament-microtubule interaction mediated by microtubule-associated proteins. J. Cell Biol. 78: 958-965.
30. Gunsalus, K.C., S. Bonaccorsi, E. Williams, F. Verni, M. Gatti, and M.L. Goldberg. 1995. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homolog, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131: 1-17.
31. Haarer, B.K., S.H. Lillie, A.E.M. Adams, V. Magdolen, W. Bandlow, and S.S. Brown. 1990. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110: 105-114.
32. Hamaguchi, Y. 1975. Microinjection of colchicine into sea urchin eggs. Dev. Growth Differ. 17: 1-117.
33. Haugwitz, M., A.A. Noegel, J. Karakesisoglou, and M. Schleicher. 1994. Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 79: 303-314.
34. Hime, G.R., J.A. Brill, and M.T. Fuller. 1996. Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci. 109: 2779-2788.
35. Hiramoto, Y. 1956. Cell division without mitotic apparatus in sea urchin eggs. Exp. Cell Res. 11: 630-636.
36. _. 1971. Analysis of cleavage stimulus by means of micromanipulation of sea urchin eggs. Exp. Cell Res. 8: 291-298.
37. Hyman, A.A. 1989. Centrosome movement in the early divisions of Caenorhabditis elegans: A cortical site determining centrosome position. J. Cell Biol. 109: 1185-1193.
38. Hyman, A.A. and J.G. White. 1987. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J. Cell Biol 105: 2123-2135.
39. Inoue, S. 1990. Dynamics of mitosis and cleavage. Ann. N.Y. Acad. Sci. 582: 1-14.
40. Kawamura, K. 1977. Microdissection studies on the dividing neuroblast of the grasshopper, with special reference to the mechanism of unequal cytokinesis. Exp. Cell Res. 106: 127-137.
41. Lappalainen, P. and D.G. Drubin. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature 388: 78-82.
42. Lassing, I. and U. Lindberg. 1985. Specific interaction between phosphatidylinositol 4,5-biphoshate and profilactin. Nature 314: 472-474.
43. Lin, H., L. Yue, and A.C. Spradling. 1994. The Drosophila fusome, a germline specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956.
44. Lindsley, D.L. and G.G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, San Diego, CA.
45. Machesky, L.M. and T.D. Pollard. 1993. Profilin as a potential mediator of membrane cytoskeleton communication. Trends Cell Biol. 3: 381-385.
46. Margolis, R.L. and P.R. Andreassen. 1993. The telophase disc: Its possible role in mammalian cell cleavage. BioEssays 15: 201-207.
47. Miller, A.L., R.A. Fluck, J.A. McLaughlin, and L.F. Jaffe. 1993. Calcium buffer injections inhibit cytokinesis in Xenopus eggs. J. Cell Sci. 106: 523-534.
48. Nislow, C., C. Sellitto, R. Kuriyama, and J.R. McIntosh. 1990. A monoclonal antibody to a mitotic microtubule-associated protein blocks mitotic progression. J. Cell Biol. 111: 511-522.
49. _. 1992. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature 359: 543-547.
50. Palmer, R.E., D.S. Sullivan, T. Huffaker, and D. Koshland. 1992. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 119: 583-593.
51. Pantaloni, D. and M.-F, Carlier. 1993. How profilin promotes actin filament assembly in the presence of thymosin β4. Cell 75: 1007-1014.
52. Pedrotti, B., R. Colombo, and K. Islam. 1994. Microtubule associated protein MAP1A is an actin-binding and crosslinking protein. Cell Motil. Cytoskeleton 29: 110-116.
53. Pirrotta, V. 1986. Cloning Drosophila genes. In Drosophila: A practical approach, (ed. D. B. Roberts), pp. 83-100. IRL Press, Oxford, UK.
54. Pollard, T.D. and J.A. Cooper. 1984. Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry 23: 6631-6641.
55. Rappaport, R. 1961. Experiments concerning the cleavage stimulus in sand dollar eggs. J. Exp. Zool. 148: 81-89.
56. _. 1985. Repeated furrow formation from a single mitotic apparatus in cylindrical sand dollar eggs. J. Exp. Zool. 234: 167-171.
57. _. 1986. Establishment of the mechanism of cytokinesis in animal cells. Int. Rev. Cytol. 105: 245-281.
58. _. 1991. Cytokinesis. In Oogenesis, spermatogenesis and reproduction, comparative physiology, (ed. K.H. Kinn), vol. 10. pp. 1-36. Karger, Basel, Switzerland.
59. Rappaport, R. and B.N. Rappaport. 1974. Establisment of cleavage furrows by the mitotic spindle. J. Exp. Zool. 189: 189-196.
60. _. 1983. Cytokinesis: Effects of blocks between the mitotic apparatus and the surface on the furrow establishment in flattened echinoderm eggs. J. Exp. Zool. 227: 213-227.
61. Robinson, D.N. and L. Cooley. 1996. Stable intercellular bridges in development: The cytoskeleton lining the tunnel. Trends Cell Biol. 6: 474-479.
62. Sanger, F., S. Niecklen, and I.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. 74: 5463-5467.
63. Satterwhite, L.L. and T.D. Pollard. 1992. Cytokinesis. Curr. Opin. Cell Biol. 4: 43-52.
64. Sattilaro, R.F., W.L. Dentier, and E.L. LeCluyse. 1981. Microtubule-associated proteins (MAPs) and organization of actin filaments in vitro. J. Cell Biol. 90: 467-473.
65. Sellitto, C. and R. Kuriyama. 1988. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells. J. Cell Biol. 106: 431-439.
66. Schroer, T.A. 1994. New insights into the interaction of cytoplasmic dynein with actin related protein, Arp1. J. Cell Biol. 127: 1-4.
67. Sohn, R.H. and P.J. Goldschmidt-Clermont. 1994. Profilin: At the crossroads of signal transduction and the actin cytoskeleton. BioEssays 16: 465-470.
68. Tates, A.D. 1971. Cytodifferentiation during spermatogenesis in Drosophila melanogaster: An electron microscope study. Ph.D. Thesis. Rijksuniversiteit, Leiden, The Netherlands.
69. Theriot, J.A. 1997. Accelerating on a treadmill: ADF/cofilin promotes rapid actin filament turnover in the dynamic cytoskeleton. J. Cell Biol. 136: 1165-1168.
70. Theriot, J.A. and T. Michison 1993. The three faces of profilin. Cell 75: 835-838.
71. Verheyen, E.M. and L. Cooley. 1994. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120: 717-728.
72. Vernos, I., J. Raats, T. Hirano, J. Heasman, E. Karsenti, and C. Wylie. 1995. Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning. Cell 81: 117-127.
73. Waddle, J.A., J.A. Cooper, and R.H. Waterson. 1994. Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions. Development 120: 2317-2328.
74. Wang, S.-Z. and R. Adler. 1995. Chromokinesin: A DNA-binding, kinesin-like nuclear protein. J. Cell Biol. 128: 761-768.
75. Wheatley, S.P. and Y.-L. Wang. 1996. Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells. J. Cell Biol. 135: 981-989.
76. White, J.G. and G.G. Borisy. 1983. On the mechanism of cytokinesis in animal cells. J. Theor. Biol. 101: 289-316.
77. Williams, B.C., M.F. Riedy, E.V. Williams, M. Gatti, and M.L. Goldberg. 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.
78. Yen, T.J., D.A. Compton, D. Wise, R.P. Zinkowski, B.R. Brinkley, W.C. Earnshaw, and D.W. Cleveland. 1991. CENP-E, a novel human centromere-associated protein required for progression from metaphase to anaphase. EMBO J. 10: 1245-1254.
79. Yen, T.J., G. Li, B.T. Schaar, I. Szilak, and D.W. Cleveland. 1992. CENP-E is a putative kinetochore motor that accumulates just before mitosis. Nature 359: 336-339.