Born to run: Creating the muscle fiber

Current Opinion in Cell Biology

Volumn 22, Issue 5, 2010, Pages 566-574

  Schejter, Eyal D ^a   Baylies, Mary K ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

CELL ELONGATION; CELL FUSION; CELL INTERACTION; CELL JUNCTION; DROSOPHILA; EPIDERMIS; EXTRACELLULAR MATRIX; MOLECULAR MODEL; MORPHOGENESIS; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

ANIMALS; DROSOPHILA; HUMANS; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL;

EID: 77957237835     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.08.009     Document Type: Review

References (88)

1. Bate M. The embryonic development of larval muscles in Drosophila. Development 1990, 110:791-804.
2. Ciglar L., Furlong E.E. Conservation and divergence in developmental networks: a view from Drosophila myogenesis. Curr Opin Cell Biol 2009, 21:754-760.
3. Daczewska M., Picchio L., Jagla T., Figeac N., Jagla K. Muscle development and regeneration in normal and pathological conditions: learning from Drosophila. Curr Pharm Des 2010, 16:929-941.
4. Figeac N., Daczewska M., Marcelle C., Jagla K. Muscle stem cells and model systems for their investigation. Dev Dyn 2007, 236:3332-3342.
5. Frasch M. Controls in patterning and diversification of somatic muscles during Drosophila embryogenesis. Curr Opin Genet Dev 1999, 9:522-529.
6. Nguyen H.T., Frasch M. MicroRNAs in muscle differentiation: lessons from Drosophila and beyond. Curr Opin Genet Dev 2006, 16:533-539.
7. Schnorrer F., Dickson B.J. Muscle building; mechanisms of myotube guidance and attachment site selection. Dev Cell 2004, 7:9-20.
8. Bate M., Rushton E., Currie D.A. Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 1991, 113:79-89.
9. Baylies M.K., Michelson A.M. Invertebrate myogenesis: looking back to the future of muscle development. Curr Opin Genet Dev 2001, 11:431-439.
10. Beckett K., Baylies M.K. The development of the Drosophila larval body wall muscles. Int Rev Neurobiol 2006, 75:55-70.
11. Gildor B., Massarwa R., Shilo B.Z., Schejter E.D. Making muscles: Arp, two, three. Fly (Austin) 2010, 4:145-148.
12. Haralalka S., Abmayr S.M. Myoblast fusion in Drosophila. Exp Cell Res 2010, 10.1016/j.yexcr.2010.05.018.
13. Onel S.F., Renkawitz-Pohl R. FuRMAS: triggering myoblast fusion in Drosophila. Dev Dyn 2009, 238:1513-1525.
14. Rochlin K., Yu S., Roy S., Baylies M.K. Myoblast fusion: when it takes more to make one. Dev Biol 2009, 341:66-83.
15. Beckett K., Baylies M.K. 3D analysis of founder cell and fusion competent myoblast arrangements outlines a new model of myoblast fusion. Dev Biol 2007, 309:113-125.
16. Shelton C., Kocherlakota K.S., Zhuang S., Abmayr S.M. The immunoglobulin superfamily member Hbs functions redundantly with Sns in interactions between founder and fusion-competent myoblasts. Development 2009, 136:1159-1168.
17. Sohn R.L., Huang P., Kawahara G., Mitchell M., Guyon J., Kalluri R., Kunkel L.M., Gussoni E. A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion. Proc Natl Acad Sci USA 2009, 106:9274-9279.
18. Srinivas B.P., Woo J., Leong W.Y., Roy S. A conserved molecular pathway mediates myoblast fusion in insects and vertebrates. Nat Genet 2007, 39:781-786.
19. Kesper D.A., Stute C., Buttgereit D., Kreiskother N., Vishnu S., Fischbach K.F., Renkawitz-Pohl R. Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev Dyn 2007, 236:404-415.
20. Balagopalan L., Chen M.H., Geisbrecht E.R., Abmayr S.M. The CDM superfamily protein MBC directs myoblast fusion through a mechanism that requires phosphatidylinositol 3,4,5-triphosphate binding but is independent of direct interaction with DCrk. Mol Cell Biol 2006, 26:9442-9455.
21. Berger S., Schafer G., Kesper D.A., Holz A., Eriksson T., Palmer R.H., Beck L., Klambt C., Renkawitz-Pohl R., Onel S.F. WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J Cell Sci 2008, 121:1303-1313.
22. Chen E.H., Olson E.N. Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. Dev Cell 2001, 1:705-715.
23. Chen E.H., Pryce B.A., Tzeng J.A., Gonzalez G.A., Olson E.N. Control of myoblast fusion by a guanine nucleotide exchange factor, loner, and its effector ARF6. Cell 2003, 114:751-762.
24. Gildor B., Massarwa R., Shilo B.Z., Schejter E.D. The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep 2009, 10:1043-1050.
25. Kim S., Shilagardi K., Zhang S., Hong S.N., Sens K.L., Bo J., Gonzalez G.A., Chen E.H. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev Cell 2007, 12:571-586.
26. Massarwa R., Carmon S., Shilo B.Z., Schejter E.D. WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 2007, 12:557-569.
27. Menon S.D., Chia W. Drosophila rolling pebbles: a multidomain protein required for myoblast fusion that recruits D-Titin in response to the myoblast attractant Dumbfounded. Dev Cell 2001, 1:691-703.
28. Rau A., Buttgereit D., Holz A., Fetter R., Doberstein S.K., Paululat A., Staudt N., Skeath J., Michelson A.M., Renkawitz-Pohl R. rolling pebbles (rols) is required in Drosophila muscle precursors for recruitment of myoblasts for fusion. Development 2001, 128:5061-5073.
29. Richardson B.E., Beckett K., Nowak S.J., Baylies M.K. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 2007, 134:4357-4367.
30. Schroter R.H., Lier S., Holz A., Bogdan S., Klambt C., Beck L., Renkawitz-Pohl R. kette and blown fuse interact genetically during the second fusion step of myogenesis in Drosophila. Development 2004, 131:4501-4509.
31. Campellone K.G., Welch M.D. A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 2010, 11:237-251.
32. Richardson B.E., Nowak S.J., Baylies M.K. Myoblast fusion in fly and vertebrates: new genes, new processes and new perspectives. Traffic 2008, 9:1050-1059.
33. Volk T. Singling out Drosophila tendon cells: a dialogue between two distinct cell types. Trends Genet 1999, 15:448-453.
34. Kramer S.G., Kidd T., Simpson J.H., Goodman C.S. Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 2001, 292:737-740.
35. Kidd T., Bland K.S., Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 1999, 96:785-794.
36. Estrada B., Gisselbrecht S.S., Michelson A.M. The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo. Development 2007, 134:4469-4478.
37. Guerin C.M., Kramer S.G. RacGAP50C directs perinuclear gamma-tubulin localization to organize the uniform microtubule array required for Drosophila myotube extension. Development 2009, 136:1411-1421.
38. Schnorrer F., Kalchhauser I., Dickson B.J. The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev Cell 2007, 12:751-766.
39. Swan L.E., Wichmann C., Prange U., Schmid A., Schmidt M., Schwarz T., Ponimaskin E., Madeo F., Vorbruggen G., Sigrist S.J. A glutamate receptor-interacting protein homolog organizes muscle guidance in Drosophila. Genes Dev 2004, 18:223-237.
40. Ataman B., Ashley J., Gorczyca D., Gorczyca M., Mathew D., Wichmann C., Sigrist S.J., Budnik V. Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc Natl Acad Sci USA 2006, 103:7841-7846.
41. Dong H., O'Brien R.J., Fung E.T., Lanahan A.A., Worley P.F., Huganir R.L. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 1997, 386:279-284.
42. Hoogenraad C.C., Milstein A.D., Ethell I.M., Henkemeyer M., Sheng M. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 2005, 8:906-915.
43. Wayburn B., Volk T. LRT, a tendon-specific leucine-rich repeat protein, promotes muscle-tendon targeting through its interaction with Robo. Development 2009, 136:3607-3615.
44. Gilsohn E., Volk T. Fine tuning cellular recognition: the function of the leucine rich repeat (LRR) trans-membrane protein. LRT, in muscle targeting to tendon cells. Cell Adhes Migr 2010, 4:368-371.
45. Swan L.E., Schmidt M., Schwarz T., Ponimaskin E., Prange U., Boeckers T., Thomas U., Sigrist S.J. Complex interaction of Drosophila GRIP PDZ domains and Echinoid during muscle morphogenesis. EMBO J 2006, 25:3640-3651.
46. Fetting J.L., Spencer S.A., Wolff T. The cell adhesion molecules Echinoid and Friend of Echinoid coordinate cell adhesion and cell signaling to regulate the fidelity of ommatidial rotation in the Drosophila eye. Development 2009, 136:3323-3333.
47. Rawlins E.L., Lovegrove B., Jarman A.P. Echinoid facilitates Notch pathway signalling during Drosophila neurogenesis through functional interaction with Delta. Development 2003, 130:6475-6484.
48. Wei S.Y., Escudero L.M., Yu F., Chang L.H., Chen L.Y., Ho Y.H., Lin C.M., Chou C.S., Chia W., Modolell J., et al. Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev Cell 2005, 8:493-504.
49. Laplante C., Nilson L.A. Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 2006, 133:3255-3264.
50. Lin H.P., Chen H.M., Wei S.Y., Chen L.Y., Chang L.H., Sun Y.J., Huang S.Y., Hsu J.C. Cell adhesion molecule Echinoid associates with unconventional myosin VI/Jaguar motor to regulate cell morphology during dorsal closure in Drosophila. Dev Biol 2007, 311:423-433.
51. Stegmuller J., Werner H., Nave K.A., Trotter J. The proteoglycan NG2 is complexed with alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by the PDZ glutamate receptor interaction protein (GRIP) in glial progenitor cells. Implications for glial-neuronal signaling. J Biol Chem 2003, 278:3590-3598.
52. Karram K., Chatterjee N., Trotter J. NG2-expressing cells in the nervous system: role of the proteoglycan in migration and glial-neuron interaction. J Anat 2005, 207:735-744.
53. Nishiyama A., Komitova M., Suzuki R., Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 2009, 10:9-22.
54. Mishima M., Kaitna S., Glotzer M. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2002, 2:41-54.
55. D'Avino P.P. How to scaffold the contractile ring for a safe cytokinesis-lessons from Anillin-related proteins. J Cell Sci 2009, 122:1071-1079.
56. Zavortink M., Contreras N., Addy T., Bejsovec A., Saint R. Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J Cell Sci 2005, 118:5381-5392.
57. Musa H., Orton C., Morrison E.E., Peckham M. Microtubule assembly in cultured myoblasts and myotubes following nocodazole induced microtubule depolymerisation. J Muscle Res Cell Motil 2003, 24:301-308.
58. Brown N.H., Gregory S.L., Martin-Bermudo M.D. Integrins as mediators of morphogenesis in Drosophila. Dev Biol 2000, 223:1-16.
59. Bokel C., Brown N.H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev Cell 2002, 3:311-321.
60. Newman S.M., Wright T.R. A histological and ultrastructural analysis of developmental defects produced by the mutation, lethal(1)myospheroid, in Drosophila melanogaster. Dev Biol 1981, 86:393-402.
61. Leptin M., Bogaert T., Lehmann R., Wilcox M. The function of PS integrins during Drosophila embryogenesis. Cell 1989, 56:401-408.
62. Brown N.H. Null mutations in the alpha PS2 and beta PS integrin subunit genes have distinct phenotypes. Development 1994, 120:1221-1231.
63. Brabant M.C., Brower D.L. PS2 integrin requirements in Drosophila embryo and wing morphogenesis. Dev Biol 1993, 157:49-59.
64. Martin D., Zusman S., Li X., Williams E.L., Khare N., DaRocha S., Chiquet-Ehrismann R., Baumgartner S. wing blister, a new Drosophila laminin alpha chain required for cell adhesion and migration during embryonic and imaginal development. J Cell Biol 1999, 145:191-201.
65. Bunch T.A., Graner M.W., Fessler L.I., Fessler J.H., Schneider K.D., Kerschen A., Choy L.P., Burgess B.W., Brower D.L. The PS2 integrin ligand tiggrin is required for proper muscle function in Drosophila. Development 1998, 125:1679-1689.
66. Fogerty F.J., Fessler L.I., Bunch T.A., Yaron Y., Parker C.G., Nelson R.E., Brower D.L., Gullberg D., Fessler J.H. Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila alpha PS2 beta PS integrins. Development 1994, 120:1747-1758.
67. Subramanian A., Wayburn B., Bunch T., Volk T. Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 2007, 134:1269-1278.
68. Chanana B., Graf R., Koledachkina T., Pflanz R., Vorbruggen G. AlphaPS2 integrin-mediated muscle attachment in Drosophila requires the ECM protein Thrombospondin. Mech Dev 2007, 124:463-475.
69. Adams J.C., Lawler J. The thrombospondins. Int J Biochem Cell Biol 2004, 36:961-968.
70. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
71. Bentley A.A., Adams J.C. The evolution of thrombospondins and their ligand-binding activities. Mol Biol Evol 2010, 27:2187-2197.
72. Yarnitzky T., Min L., Volk T. The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev 1997, 11:2691-2700.
73. Gilsohn E., Volk T. Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 2010, 137:785-794.
74. Bicker F., Schmidt M.H. EGFL7: a new player in homeostasis of the nervous system. Cell Cycle 2010, 9.
75. Schmidt M.H., Bicker F., Nikolic I., Meister J., Babuke T., Picuric S., Muller-Esterl W., Plate K.H., Dikic I. Epidermal growth factor-like domain 7 (EGFL7) modulates Notch signalling and affects neural stem cell renewal. Nat Cell Biol 2009, 11:873-880.
76. Faulkner G., Pallavicini A., Formentin E., Comelli A., Ievolella C., Trevisan S., Bortoletto G., Scannapieco P., Salamon M., Mouly V., et al. ZASP: a new Z-band alternatively spliced PDZ-motif protein. J Cell Biol 1999, 146:465-475.
77. Krcmery J., Camarata T., Kulisz A., Simon H.G. Nucleocytoplasmic functions of the PDZ-LIM protein family: new insights into organ development. Bioessays 2010, 32:100-108.
78. Jani K., Schock F. Zasp is required for the assembly of functional integrin adhesion sites. J Cell Biol 2007, 179:1583-1597.
79. Loer B., Bauer R., Bornheim R., Grell J., Kremmer E., Kolanus W., Hoch M. The NHL-domain protein Wech is crucial for the integrin-cytoskeleton link. Nat Cell Biol 2008, 10:422-428.
80. Lin Y.C., Hsieh L.C., Kuo M.W., Yu J., Kuo H.H., Lo W.L., Lin R.J., Yu A.L., Li W.H. Human TRIM71 and its nematode homologue are targets of let-7 microRNA and its zebrafish orthologue is essential for development. Mol Biol Evol 2007, 24:2525-2534.
81. Maller Schulman B.R., Liang X., Stahlhut C., DelConte C., Stefani G., Slack F.J. The let-7 microRNA target gene, Mlin41/Trim71 is required for mouse embryonic survival and neural tube closure. Cell Cycle 2008, 7:3935-3942.
82. Munir M. TRIM proteins: another class of viral victims. Sci Signal 2010, 3:jc2.
83. Zervas C.G., Gregory S.L., Brown N.H. Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J Cell Biol 2001, 152:1007-1018.
84. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
85. Schnorrer F., Schonbauer C., Langer C.C., Dietzl G., Novatchkova M., Schernhuber K., Fellner M., Azaryan A., Radolf M., Stark A., et al. Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 2010, 464:287-291.
86. Estrada B., Choe S.E., Gisselbrecht S.S., Michaud S., Raj L., Busser B.W., Halfon M.S., Church G.M., Michelson A.M. An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet 2006, 2:e16.
87. Sandmann T., Jensen L.J., Jakobsen J.S., Karzynski M.M., Eichenlaub M.P., Bork P., Furlong E.E. A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev Cell 2006, 10:797-807.
88. Zinzen R.P., Girardot C., Gagneur J., Braun M., Furlong E.E. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009, 462:65-70.