© The Rockefeller University Press,
0021-9525/1997//589 $5.00
The Journal of Cell Biology, Volume 138, Number 3,
, 1997 589-603
Drosophila myoblast city Encodes a Conserved Protein That Is Essential for Myoblast Fusion, Dorsal Closure, and Cytoskeletal Organization
Mary Ruth S. Erickson,
Brian J. Galletta, and
Susan M. Abmayr
Department of Biochemistry and Molecular Biology and Center for Gene Regulation, The Pennsylvania State University, University Park, Pennsylvania 16802
The Drosophila myoblast city (mbc) locus was previously identified on the basis of a defect in myoblast fusion (Rushton et al., 1995. Development [Camb.]. 121:1979–1988). We describe herein the isolation and characterization of the mbc gene. The mbc transcript and its encoded protein are expressed in a broad range of tissues, including somatic myoblasts, cardial cells, and visceral mesoderm. It is also expressed in the pole cells and in ectodermally derived tissues, including the epidermis. Consistent with this latter expression, mbc mutant embryos exhibit defects in dorsal closure and cytoskeletal organization in the migrating epidermis. Both the mesodermal and ectodermal defects are reminiscent of those induced by altered forms of Drac1 and suggest that mbc may function in the same pathway. MBC bears striking homology to human DOCK180, which interacts with the SH2-SH3 adapter protein Crk and may play a role in signal transduction from focal adhesions. Taken together, these results suggest the possibility that MBC is an intermediate in a signal transduction pathway from the rho/rac family of GTPases to events in the cytoskeleton and that this pathway may be used during myoblast fusion and dorsal closure.
Abbreviations used in this paper: mbc, myoblast city; MHC, myosin heavy chain; nau, nautilus; nts, nucleotides; ORF, open reading frame.
Various portions of this work have been supported by National Science Foundation grant IBN 9204891, National Institutes of Health grant RO1 AR44274, The Muscular Dystrophy Association, and a Junior Faculty Award from the American Cancer Society to S.M. Abmayr.
Please address all correspondence to Susan M. Abmayr, Department of Biochemistry and Molecular Biology and Center for Gene Regulation, The Pennsylvania State University, University Park, PA 16802. Tel.: (814) 863-8254. Fax: (814) 863-7024. E-mail: sma1{at}psu.edu

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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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277: 23747-23754
[Abstract]
[Full Text]
-
Van Aelst, L., Symons, M.
(2002). Role of Rho family GTPases in epithelial morphogenesis. Genes Dev.
16: 1032-1054
[Full Text]
-
Lamorte, L., Royal, I., Naujokas, M., Park, M.
(2002). Crk Adapter Proteins Promote an Epithelial-Mesenchymal-like Transition and Are Required for HGF-mediated Cell Spreading and Breakdown of Epithelial Adherens Junctions. Mol. Biol. Cell
13: 1449-1461
[Abstract]
[Full Text]
-
Qiu, J.-L., Jilk, R., Marks, M. D., Szymanski, D. B.
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14: 101-118
[Abstract]
[Full Text]
-
Rau, A., Buttgereit, D., Holz, A., Fetter, R., Doberstein, S. K., Paululat, A., Staudt, N., Skeath, J., Michelson, A. M., Renkawitz-Pohl, R.
(2001). rolling pebbles (rols) is required in Drosophila muscle precursors for recruitment of myoblasts for fusion. Development
128: 5061-5073
[Abstract]
[Full Text]
-
Lundquist, E. A., Reddien, P. W., Hartwieg, E., Horvitz, H. R., Bargmann, C. I.
(2001). Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development
128: 4475-4488
[Abstract]
[Full Text]
-
Giles, K. M., Ross, K., Rossi, A. G., Hotchin, N. A., Haslett, C., Dransfield, I.
(2001). Glucocorticoid Augmentation of Macrophage Capacity for Phagocytosis of Apoptotic Cells Is Associated with Reduced p130Cas Expression, Loss of Paxillin/pyk2 Phosphorylation, and High Levels of Active Rac. J. Immunol.
167: 976-986
[Abstract]
[Full Text]
-
Takai, Y., Sasaki, T., Matozaki, T.
(2001). Small GTP-Binding Proteins. Physiol. Rev.
81: 153-208
[Abstract]
[Full Text]
-
Machado, C., Andrew, D. J.
(2000). D-Titin: A Giant Protein with Dual Roles in Chromosomes and Muscles. JCB
151: 639-652
[Abstract]
[Full Text]
-
Bour, B. A., Chakravarti, M., West, J. M., Abmayr, S. M.
(2000). Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev.
14: 1498-1511
[Abstract]
[Full Text]
-
Fernandez, R., Takahashi, F., Liu, Z., Steward, R., Stein, D., Stanley, E. R.
(2000). The Drosophila Shark tyrosine kinase is required for embryonic dorsal closure. Genes Dev.
14: 604-614
[Abstract]
[Full Text]
-
Cheresh, D. A., Leng, J., Klemke, R. L.
(1999). Regulation of Cell Contraction and Membrane Ruffling by Distinct Signals in Migratory Cells. JCB
146: 1107-1116
[Abstract]
[Full Text]
-
Lu, Y., Settleman, J.
(1999). The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev.
13: 1168-1180
[Abstract]
[Full Text]
-
Nakashima, N., Rose, D. W., Xiao, S., Egawa, K., Martin, S. S., Haruta, T., Saltiel, A. R., Olefsky, J. M.
(1999). The Functional Role of CrkII in Actin Cytoskeleton Organization and Mitogenesis. J. Biol. Chem.
274: 3001-3008
[Abstract]
[Full Text]
-
Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T., Matsuda, M.
(1998). Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev.
12: 3331-3336
[Abstract]
[Full Text]
-
Nolan, K. M., Barrett, K., Lu, Y., Hu, K.-Q., Vincent, S., Settleman, J.
(1998). Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev.
12: 3337-3342
[Abstract]
[Full Text]
-
Philips, J., Herskowitz, I.
(1998). Identification of Kel1p, a Kelch Domain-containing Protein Involved in Cell Fusion and Morphology in Saccharomyces cerevisiae. JCB
143: 375-389
[Abstract]
[Full Text]
-
Elia, L., Marsh, L.
(1998). A Role for a Protease in Morphogenic Responses during Yeast Cell Fusion. JCB
142: 1473-1485
[Abstract]
[Full Text]
-
Kiyokawa, E., Hashimoto, Y., Kurata, T., Sugimura, H., Matsuda, M.
(1998). Evidence That DOCK180 Up-regulates Signals from the CrkII-p130Cas Complex. J. Biol. Chem.
273: 24479-24484
[Abstract]
[Full Text]
-
Goh, E. L. K., Zhu, T., Yakar, S., LeRoith, D., Lobie, P. E.
(2000). CrkII Participation in the Cellular Effects of Growth Hormone and Insulin-like Growth Factor-1. PHOSPHATIDYLINOSITOL-3 KINASE DEPENDENT AND INDEPENDENT EFFECTS. J. Biol. Chem.
275: 17683-17692
[Abstract]
[Full Text]