Myoblast fusion in Drosophila.

Somatic muscle formation is an unusual process as it requires the cells involved, the myoblasts, to relinquish their individual state and fuse with one another to form a syncitial muscle fiber. The potential use of myoblast fusion therapies to rebuild damaged muscles has generated continuing interest in elucidating the molecular basis of the fusion process. Yet, until recently, few of the molecular players involved in this process had been identified. Now, however, it has been possible to couple a detailed understanding of the cellular basis of the fusion process with powerful classical and molecular genetic strategies in the Drosophila embryo. We review the cellular studies, and the recent genetic and biochemical analyses that uncovered interacting extracellular molecules present on fusing myoblasts and the intracellular effectors that facilitate fusion. With the conservation of proteins and protein functions across species, it is likely that these findings in Drosophila will benefit understanding of the myoblast fusion process in higher organisms.

[1]  S. M. Abmayr,et al.  Drosophila myoblast city Encodes a Conserved Protein That Is Essential for Myoblast Fusion, Dorsal Closure, and Cytoskeletal Organization , 1997, The Journal of cell biology.

[2]  Y. Jan,et al.  Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. , 1994, Genes & development.

[3]  R. Artero,et al.  The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. , 2001, Development.

[4]  C. Machado,et al.  D-Titin , 2000, The Journal of cell biology.

[5]  E. Olson,et al.  Regulation of Microtubule Dynamics and Myogenic Differentiation by Murf, a Striated Muscle Ring-Finger Protein , 2000, The Journal of cell biology.

[6]  Hanh T. Nguyen,et al.  Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. , 2001, Development.

[7]  H. Sink,et al.  Characterization of Drosophila hibris, a gene related to human nephrin. , 2001, Development.

[8]  M. Bate,et al.  Specific muscle identities are regulated by Krüppel during Drosophila embryogenesis. , 1997, Development.

[9]  M. Bate,et al.  A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. , 2001, Development.

[10]  C. Sotelo,et al.  Development of the olivocerebellar projection. , 1997, Perspectives on developmental neurobiology.

[11]  J. Settleman Rac 'n Rho: the music that shapes a developing embryo. , 2001, Developmental cell.

[12]  M. Bate,et al.  twist: A Myogenic Switch in Drosophila , 1996, Science.

[13]  R. Klapper,et al.  A new approach reveals syncytia within the visceral musculature of Drosophila melanogaster. , 2001, Development.

[14]  K. Jagla,et al.  ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. , 1998, Development.

[15]  M. Duxson,et al.  Formation of primary and secondary myotubes in rat lumbrical muscles. , 1987, Development.

[16]  A. Paululat,et al.  The Mesodermal Expression of rolling stone (rost) Is Essential for Myoblast Fusion in Drosophila and Encodes a Potential Transmembrane Protein , 1997, The Journal of cell biology.

[17]  A. Nose,et al.  Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. , 1998, Development.

[18]  M. Frasch,et al.  A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. , 1990, Genes & development.

[19]  M. Frasch,et al.  Characterization and localization of the even‐skipped protein of Drosophila. , 1987, The EMBO journal.

[20]  G. Technau Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster , 1986, Roux's archives of developmental biology.

[21]  W. Chia,et al.  Drosophila rolling pebbles: a multidomain protein required for myoblast fusion that recruits D-Titin in response to the myoblast attractant Dumbfounded. , 2001, Developmental cell.

[22]  D. Featherstone,et al.  Drosophila D-titin is required for myoblast fusion and skeletal muscle striation. , 2000, Journal of cell science.

[23]  C. Keller,et al.  A role for nautilus in the differentiation of muscle precursors. , 1998, Developmental biology.

[24]  K. Fischbach,et al.  rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. , 2001, Development.

[25]  Jonathan B. Cohen,et al.  Role of Rapsyn Tetratricopeptide Repeat and Coiled-coil Domains in Self-association and Nicotinic Acetylcholine Receptor Clustering* , 2001, The Journal of Biological Chemistry.

[26]  L. Luo,et al.  Rac function and regulation during Drosophila development , 2002, Nature.

[27]  M. Ontell,et al.  The organogenesis of murine striated muscle: a cytoarchitectural study. , 1984, The American journal of anatomy.

[28]  C. Goodman,et al.  Genetic Analysis of Myoblast Fusion: blown fuse Is Required for Progression Beyond the Prefusion Complex , 1997, The Journal of cell biology.

[29]  John B. Thomas,et al.  apterous is a drosophila LIM domain gene required for the development of a subset of embryonic muscles , 1992, Neuron.

[30]  A. Michelson,et al.  rolling pebbles (rols) is required in Drosophila muscle precursors for recruitment of myoblasts for fusion. , 2001, Development.

[31]  A. Paululat,et al.  Essential genes for myoblast fusion in Drosophila embryogenesis , 1999, Mechanisms of Development.

[32]  M. Bate,et al.  The embryonic development of larval muscles in Drosophila. , 1990, Development.

[33]  A. Paululat,et al.  Fusion from myoblasts to myotubes is dependent on the rolling stone gene (rost) of Drosophila. , 1995, Development.

[34]  A. Mauro SATELLITE CELL OF SKELETAL MUSCLE FIBERS , 1961, The Journal of biophysical and biochemical cytology.

[35]  S. M. Abmayr,et al.  Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. , 2000, Genes & development.

[36]  M. Suster,et al.  myoblasts incompetent encodes a zinc finger transcription factor required to specify fusion-competent myoblasts in Drosophila. , 2002, Development.

[37]  D. W. Robinson,et al.  Biphasic development of muscle fibers in the fetal lamb. , 1972, Experimental neurology.

[38]  A. Kelly,et al.  THE HISTOGENESIS OF RAT INTERCOSTAL MUSCLE , 1969, The Journal of cell biology.

[39]  M. Bate,et al.  Drosophila Dumbfounded A Myoblast Attractant Essential for Fusion , 2000, Cell.

[40]  B. Carlson,et al.  The regeneration of skeletal muscle. A review. , 1973, The American journal of anatomy.

[41]  K. Fischbach,et al.  The irregular chiasm C-roughest locus of Drosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein. , 1993, Genes & development.

[42]  Zhiping Nie,et al.  Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons , 1995, Neuron.

[43]  A. Draeger,et al.  Primary, secondary and tertiary myotubes in developing skeletal muscle: A new approach to the analysis of human myogenesis , 1987, Journal of the Neurological Sciences.

[44]  K. Pelin,et al.  Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. , 2001, Journal of molecular biology.

[45]  M. Bate,et al.  Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. , 1995, Genes & development.

[46]  T. Hawke,et al.  Myogenic satellite cells: physiology to molecular biology. , 2001, Journal of applied physiology.

[47]  J. Settleman,et al.  Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. , 1998, Genes & development.

[48]  S. M. Abmayr,et al.  Identification of a Drosophila homologue to vertebrate Crk by interaction with MBC. , 1999, Gene.

[49]  Elizabeth H. Chen,et al.  Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. , 2001, Developmental cell.