Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis

doi:10.1083/jcb.131.5.1243

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Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis

KC Gunsalus, S Bonaccorsi, E Williams, F Verni, M Gatti and ML Goldberg
Section of Genetics and Development, Cornell University, Ithaca, New York 14853, USA.

We describe the phenotypic and molecular characterization of twinstar (tsr), an essential gene in Drosophila melanogaster. Two P-element induced alleles of tsr (tsr1 and tsr2) result in late larval or pupal lethality. Cytological examination of actively dividing tissues in these mutants reveals defects in cytokinesis in both mitotic (larval neuroblast) and meiotic (larval testis) cells. In addition, mutant spermatocytes show defects in aster migration and separation during prophase/prometaphase of both meiotic divisions. We have cloned the gene affected by these mutations and shown that it codes for a 17-kD protein in the cofilin/ADF family of small actin severing proteins. A cDNA for this gene has previously been described by Edwards et al. (1994). Northern analysis shows that the tsr gene is expressed throughout development, and that the tsr1 and tsr2 alleles are hypomorphs that accumulate decreased levels of tsr mRNA. These findings prompted us to examine actin behavior during male meiosis to visualize the effects of decreased twinstar protein activity on actin dynamics in vivo. Strikingly, both mutants exhibit abnormal accumulations of F- actin. Large actin aggregates are seen in association with centrosomes in mature primary spermatocytes. Later, during ana/telophase of both meiotic divisions, aberrantly large and misshaped structures appear at the site of contractile ring formation and fail to disassemble at the end of telophase, in contrast with wild-type. We discuss these results in terms of possible roles of the actin-based cytoskeleton in centrosome movement and in cytokinesis.
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Palmgren, S., Vartiainen, M., Lappalainen, P. (2002). Twinfilin, a molecular mailman for actin monomers. J. Cell Sci. 115: 881-886 [Abstract] [Full Text]
Dong, C.-H., Xia, G.-X., Hong, Y., Ramachandran, S., Kost, B., Chua, N.-H. (2001). ADF Proteins Are Involved in the Control of Flowering and Regulate F-Actin Organization, Cell Expansion, and Organ Growth in Arabidopsis. Plant Cell 13: 1333-1346 [Abstract] [Full Text]
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Toshima, J., Toshima, J. Y., Amano, T., Yang, N., Narumiya, S., Mizuno, K. (2001). Cofilin Phosphorylation by Protein Kinase Testicular Protein Kinase 1 and Its Role in Integrin-mediated Actin Reorganization and Focal Adhesion Formation. Mol. Biol. Cell 12: 1131-1145 [Abstract] [Full Text]
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Noguchi, T, Mabuchi, I (2001). Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. J. Cell Sci. 114: 401-412 [Abstract]
Ouellet, F., Carpentier, E., Cope, M. J. T.V., Monroy, A. F., Sarhan, F. (2001). Regulation of a Wheat Actin-Depolymerizing Factor during Cold Acclimation. Plant Physiol. 125: 360-368 [Abstract] [Full Text]
Meberg, P. J., Bamburg, J. R. (2000). Increase in Neurite Outgrowth Mediated by Overexpression of Actin Depolymerizing Factor. J. Neurosci. 20: 2459-2469 [Abstract] [Full Text]
Brill, J., Hime, G., Scharer-Schuksz, M, Fuller, M. (2000). A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis. Development 127: 3855-3864 [Abstract]
Carlier, M.-F., Ressad, F., Pantaloni, D. (1999). Control of Actin Dynamics in Cell Motility. ROLE OF ADF/COFILIN. J. Biol. Chem. 274: 33827-33830 [Full Text]
Prokopenko, S. N., Brumby, A., O'Keefe, L., Prior, L., He, Y., Saint, R., Bellen, H. J. (1999). A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev. 13: 2301-2314 [Abstract] [Full Text]
Ressad, F., Didry, D., Egile, C., Pantaloni, D., Carlier, M.-F. (1999). Control of Actin Filament Length and Turnover by Actin Depolymerizing Factor (ADF/Cofilin) in the Presence of Capping Proteins and ARP2/3 Complex. J. Biol. Chem. 274: 20970-20976 [Abstract] [Full Text]
Ono, S., Baillie, D. L., Benian, G. M. (1999). UNC-60B, an ADF/Cofilin Family Protein, Is Required for Proper Assembly of Actin into Myofibrils in Caenorhabditis elegans Body Wall Muscle. JCB 145: 491-502 [Abstract] [Full Text]
Edwards, D. C., Gill, G. N. (1999). Structural Features of LIM Kinase That Control Effects on the Actin Cytoskeleton. J. Biol. Chem. 274: 11352-11361 [Abstract] [Full Text]
Mathur, J, Spielhofer, P, Kost, B, Chua, N (1999). The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559-5568 [Abstract]
Okada, K, Obinata, T, Abe, H (1999). XAIP1: a Xenopus homologue of yeast actin interacting protein 1 (AIP1), which induces disassembly of actin filaments cooperatively with ADF/cofilin family proteins. J. Cell Sci. 112: 1553-1565 [Abstract]
Lappalainen, P., Kessels, M. M., Cope, M. J. T.V., Drubin, D. G. (1998). The ADF Homology (ADF-H) Domain: A Highly Exploited Actin-binding Module. Mol. Biol. Cell 9: 1951-1959 [Full Text]
Adams, R. R., Tavares, A. A.M., Salzberg, A., Bellen, H. J., Glover, D. M. (1998). pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for�cytokinesis. Genes Dev. 12: 1483-1494 [Abstract] [Full Text]
Ono, S., Benian, G. M. (1998). Two Caenorhabditis elegans Actin Depolymerizing Factor/Cofilin Proteins, Encoded by the unc-60 Gene, Differentially Regulate Actin Filament Dynamics. J. Biol. Chem. 273: 3778-3783 [Abstract] [Full Text]
Van Troys, M., Dewitte, D., Verschelde, J.-L., Goethals, M., Vandekerckhove, J., Ampe, C. (1997). Analogous F-actin Binding by Cofilin and Gelsolin Segment 2�Substantiates Their Structural Relationship. J. Biol. Chem. 272: 32750-32758 [Abstract] [Full Text]
McGough, A., Pope, B., Chiu, W., Weeds, A. (1997). Cofilin Changes the Twist of F-Actin: Implications for Actin Filament Dynamics and Cellular Function. JCB 138: 771-781 [Abstract] [Full Text]
Rosenblatt, J., Agnew, B. J., Abe, H., Bamburg, J. R., Mitchison, T. J. (1997). Xenopus Actin Depolymerizing Factor/Cofilin (XAC) Is Responsible for the Turnover of Actin Filaments in Listeria monocytogenes Tails. JCB 136: 1323-1332 [Abstract] [Full Text]
Theriot, J. A. (1997). Accelerating on a Treadmill: ADF/Cofilin Promotes Rapid Actin Filament Turnover in the Dynamic Cytoskeleton. JCB 136: 1165-1168 [Full Text]
Ohkura, H, Torok, T, Tick, G, Hoheisel, J, Kiss, I, Glover, D. (1997). Mutation of a gene for a Drosophila kinesin-like protein, Klp38B, leads to failure of cytokinesis. J. Cell Sci. 110: 945-954 [Abstract]
Pfannstiel, J., Cyrklaff, M., Habermann, A., Stoeva, S., Griffiths, G., Shoeman, R., Faulstich, H. (2001). Human Cofilin Forms Oligomers Exhibiting Actin Bundling Activity. J. Biol. Chem. 276: 49476-49484 [Abstract] [Full Text]
Mandato, C. A., Bement, W. M. (2001). Contraction and polymerization cooperate to assemble and close actomyosin rings around Xenopus oocyte wounds. JCB 154: 785-798 [Abstract] [Full Text]
Wahlstrom, G., Vartiainen, M., Yamamoto, L., Mattila, P. K., Lappalainen, P., Heino, T. I. (2001). Twinfilin is required for actin-dependent developmental processes in Drosophila. JCB 155: 787-796 [Abstract] [Full Text]
Vartiainen, M. K., Mustonen, T., Mattila, P. K., Ojala, P. J., Thesleff, I., Partanen, J., Lappalainen, P. (2002). The Three Mouse Actin-depolymerizing Factor/Cofilins Evolved to Fulfill Cell-Type-specific Requirements for Actin Dynamics. Mol. Biol. Cell 13: 183-194 [Abstract] [Full Text]