Essential genes for myoblast fusion in Drosophila embryogenesis

Mechanisms of Development

Volumn 83, Issue 1-2, 1999, Pages 17-26

  Paululat, Achim ^a   Holz, Anne ^a   Renkawitz Pohl, Renate ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Drosophila; Membrane fusion; Molecular analysis; Myogenesis; Ultrastructure

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL TISSUE; CELL ADHESION; CELL FUSION; CELL INTERACTION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE ISOLATION; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; BODY PATTERNING; CELL ADHESION; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GTP-BINDING PROTEINS; INSECT PROTEINS; INTRACELLULAR MEMBRANES; MALE; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUSCLES; MUTAGENESIS; MYOGENIC REGULATORY FACTORS; RAC GTP-BINDING PROTEINS; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

ANIMALIA; HEXAPODA; MAMMALIA; VERTEBRATA;

EID: 0032968355     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(99)00029-5     Document Type: Review

References (75)

1. Abmayr S.M., Erickson M.R., Bour B.A., Kulp M. Genetic analysis of muscle formation in Drosophila. J. Cell. Biochem. (Suppl.). 18D:1994;474.
2. Abmayr S.M., Erickson M.R.S., Bour B. Embryonic development of the larval body wall musculature of Drosophila melanogaster. Trends Genet. 11:1995;153-159.
3. Abmayr S.M., Keller C.A. Drosophila myogenesis and insights into the role of nautilus. Curr. Top. Dev. Biol. 38:1998;35-80.
4. Arnold H.H., Braun T. Targeted inactivation of myogenic factor genes reveals their role during mouse myogenesis: a review. J. Dev. Biol. 40:1996;345-355.
5. Artalejo C.R., Elhamdani A., Palfrey H.C. Secretion: dense-core vesicles can kiss-and-run too. Curr. Biol. 8:1998;62-65.
6. Bate, M., 1993. The mesoderm and its derivatives. In: Bate, M., Martinez Arias, A. (Eds.), The Development of Drosophila melanogaster, Vol. 2, Cold Spring Harbor Laboratory Press, New York, pp. 1013-1090.
7. Baylies M.K., Bate M., Ruiz Gómez M. Myogenesis: a view from Drosophila. Cell. 93:1998;921-927.
8. Beer J., Technau G.M., Campos-Ortega J.A. Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster. IV. Commitment and proliferative capabilities of mesodermal cells. Roux's Arch. Dev. Biol. 196:1987;222-230.
9. Blobel C.P., Wolfsberg T.G., Turck C.W., Myles D.G., Promakoff P., White J.M. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature. 356:1992;248-252.
10. Bour B.A., O'Brien M.A., Lockwood W.L., Goldstein E.S., Bodmer R., Taghert P.H., Abmayr S.M., Nguyen H.T. Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev. 9:1995;730-741.
11. Carmena A., Bate M., Jimenez F. Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev. 9:1995;2373-2383.
12. Carmena A., Murugasu-Oei B., Menom D., Jiménez F., Chia W. Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 12:1998;217-231.
13. Charlton C.A., Mohler W.A., Radice G.L., Hynes R.O., Blau H.M. Fusion competence of myoblast rendered genetically null for N-cadherin in culture. J. Cell Biol. 138:1997;331-336.
14. Cifuentes-Diaz C., Nicolet M., Alameddine H., Goudou D., Dehaupas M., Rieger F., Mége R.M. M-cadherin localization in developing adult and regenerating mouse skeletal muscle: possible involvement in secondary myogenesis. Mech. Dev. 50:1995;85-97.
15. Damm C., Wolk A., Buttgereit D., Löher K., Wagner E., Lilly B., Olson E.N., Hasenpusch-Theil K., Renkawitz-Pohl R. Independent regulatory elements in the upstream region of the Drosophila β3 tubulin gene (βTub60D) guide expression in the dorsal vessel and the somatic muscles. Dev. Biol. 199:1998;138-149.
16. Dohrmann C., Azpiazu N., Frasch M. A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev. 4:1990;2098-2111.
17. Donalies M., Cramer M., Ringwald M., Starzinski-Powitz A. Expression of M-cadherin, a member of the cadherin multigene family, correlates differentiation of skeletal muscle cells. Proc. Natl. Acad. Sci. USA. 88:1991;8024-8028.
18. Doberstein S.K., Fetter R.D., Mehta A.Y., Goodman C.S. Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 136:1997;1249-1261.
19. Drysdale R., Rushton E., Bate M. Genes required for embryonic muscle development in Drosophila melanogaster. Roux's Arch. Dev. Biol. 202:1993;276-295.
20. Elion E.A., Trueheart J., Fink G.R. Fus2 localizes near the site of cell fusion and is required for both cell fusion and nuclear alignment during zygote formation. J. Cell Biol. 130:1995;1283-1296.
21. Erickson M.R.S., Galletta B.J., Abmayr S.M. Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J. Cell Biol. 138:1997;589-603.
22. Firulli A.B., Olson E.N. Modular regulation of muscle gene transcription: a mechanism for muscle cell diversity. Trends Genet. 13:1997;364-369.
23. Fuller, M.T., 1993. Spermatogenesis. In: Bate, M., Martinez Arias, A. (Eds.), The Development of Drosophila melanogaster, Vol. I, Cold Spring Harbor Laboratory Press, New York, pp. 71-147.
24. Galletta, B.J., Niu, X.P., Erickson, M.R.S., Abmayr, S.M., 1999. Identification of a Drosophila homologue to vertebrate Crk by interaction with MBC. Gene (in press).
25. Gasch, A., Hinz, U., Renkawitz-Pohl, R., 1989. Intron and upstream sequences regulate expression of the Drosophila β3-tubulin gene in the visceral and somatic musculature, respectively. Proc. Natl. Acad. Sci. USA 86, 3215-3218.
26. Hasegawa H., Kiyokawa E., Tanaka S., Nagashima K., Gotoh N., Shibuya M., Kurata T., Matsuda M. DOCK 180, a major Crk binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16:1996;1770-1776.
27. Hales K.G., Fuller M.T. Developmental regulated mitochondrial fusion mediated by a conserved, novel predicted GTPase. Cell. 90:1997;121-129.
28. Hay J.C., Scheller R.H. SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9:1997;505-512.
29. Hernandez L.D., Hofman L.R., Wolfsberg T.G., White J.M. Virus-cell and cell-cell fusion. Ann. Rev. Dev. Biol. 12:1996;627-661.
30. Holz A., Meise M., Janning W. Adepithelial cells in Drosophila melanogaster: origin and cell lineage. Mech. Dev. 62:1997;93-101.
31. Hughson F.M. Structural characterization of viral fusion proteins. Curr. Biol. 5:1995;265-274.
32. Hughson F.M. Enveloped viruses: a common mode of membrane fusion? Curr. Biol. 7:1997;565-569.
33. Kalderon N., Gilula N.B. Membrane events involved in myoblast fusion. J. Cell Biol. 81:1979;411-425.
34. Kiehart D.P., Feghali R. Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103:1986;1517-1525.
35. Kirkwood S.P., Munn E.A., Brooks G.A. Mitochondrial reticulum in limb skeleton muscle. Am. J. Physiol. 251:1986;C395-C402.
36. Klapper R., Holz A., Janning W. Fate map and cell lineage relationships of thoracic and abdominal mesodermal anlagen in Drosophila melanogaster. Mech. Dev. 71:1998;77-87.
37. Knirr S., Breuer S., Paululat A., Renkawitz-Pohl R. Somatic mesoderm differentiation and the development of a subset of pericardial cells depend on the not enough muscles (nem) locus, which contains the inscuteable gene and the intron located gene, skittles. Mech. Dev. 67:1997;69-81.
38. 2+-dependent adhesion molecule, N-cadherin, in myoblast interaction during myogenesis. Exp. Cell Res. 188:1990;175-184.
39. Lawrence P.A. Cell lineage of the thoracic muscles of Drosophila. Cell. 29:1982;493-503.
40. Leiss D., Hinz U., Gasch A., Mertz R., Renkawitz-Pohl R. ß3 tubulin expression characterises the differentiating mesodermal germ layer during Drosophila embryogenesis. Development. 104:1988;525-531.
41. Lilly, B., Galewsky, S., Firulli, A.B., Schulz, R.A., Olson, E.N., 1994. D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle lineages during Drosophila embryogenesis. Proc. Natl. Acad. Sci. USA 91, 5662-5666.
42. Lilly B., Zhao B., Ranganayakulu G., Paterson B.M., Schulz R.A., Olson E.N. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science. 267:1995;688-693.
43. Lin M.H., Nguyen H.T., Dybala C., Storti R.V. Myocyte-specific enhancer factor 2 acts cooperatively with a muscle activator region to regulate Drosophila tropomyosin gene muscle expression. Proc. Natl. Acad. Sci. USA. 93:1996;4623-4628.
44. Luo L., Liao Y.J., Jan L.Y., Jan Y.N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8:1994;1787-1802.
45. Maeland K., Bloor J.M., Brown N.H. Characterization of singles bar, a new mutant in Drosophila melanogaster required for muscle development. Mol. Cell. Biol. 7:1996;39A.
46. Mege R.M., Goudou D., Diaz C., Nicolet M., Garcia L., Geraud G., Rieger F. N-cadherin and N-CAM in myoblast fusion: compared localisation and effect of blockade by peptides and antibodies. J. Cell Sci. 103:1992;897-906.
47. Moore R., Walsh F.S. The adhesion molecule M-cadherin is specifically expressed in developing and regenerating, but not denervated skeletal muscle. Development. 117:1993;1409-1420.
48. Nguyen H.T., Bodmer R., Abmayr S.M., McDermott J.C., Spoerel N.A. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. USA. 191:1994;7520-7524.
49. Nolan K.M., Barrett K., Lu Y., Hu K.Q., Vincent S., Settleman J. Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev. 12:1998;3337-3342.
50. Olson E.N., Klein W.H. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8:1994;1-18.
51. Olson E.N., Perry M., Schulz R.A. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172:1995;2-14.
52. Olson E.N., Spizz G., Tainsky M.A. The oncogenic version forms of N-ras or H-ras prevent skeletal myoblast differentiation. Mol. Cell. Biol. 7:1987;2104-2111.
53. Olson E.N., Arnold H.H., Rigly R.W.J., Wold B. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell. 85:1996;1-4.
54. Paululat A., Burchard S., Renkawitz-Pohl R. Fusion from myoblasts to myotubes is dependent on the rolling stone gene (rost) of Drosophila. Development. 121:1995;2611-2620.
55. Paululat A., Goubeaud A., Damm C., Knirr S., Burchard S., Renkawitz-Pohl R. The mesodermal expression of rolling stone (rost) is essential for myoblast fusion in Drosophila and encodes a potential transmembrane protein. J. Cell Biol. 138:1997;337-348.
56. Paululat, A., Breuer, S., Renkawitz-Pohl, R., 1999. Determination and development of the larval muscle pattern in Drosophila melanogaster. Cell Tissue Res. (in press).
57. Pfeffer S.R. Transport vesicle docking: SNAREs and associates. Ann. Rev. Cell. Dev. Biol. 12:1996;441-461.
58. Radice G.L., Rayburn H., Matsunami H., Knudsen K.A., Takeichi M., Hynes R.O. Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181:1997;64-78.
59. Ranganayakulu G., Zhao B., Dokidis A., Molkentin J.D., Olson E.N., Schulz R.A. A series of mutations in the D-MEF2 transcription factor reveal multiple functions in the larval and adult myogenesis in Drosophila. Dev. Biol. 171:1995;169-181.
60. Rash J.E., Fambourgh D. Ultrastructural and elektrophysiological correlates of cell coupling and cytoplasmic fusion during myogenesis in vitro. Dev. Biol. 30:1973;166-186.
61. Ridley A.J. Rho: theme and variations. Curr. Biol. 6:1996;1256-1264.
62. Rothman J.E., Söllner T.H. Throttles and dampers: controlling the engine of membrane fusion. Science. 276:1997;1212-1213.
63. Roy S., VijayRaghavan K. Homeotic genes and the regulation of myoblast migration, fusion, and fibre-specific gene expression during adult myogenesis in Drosophila. Development. 124:1997;3333-3341.
64. Roy S., VijayRaghavan K. Patterning muscles using organizers: larval muscle templates and adult myoblasts actively interact to pattern the dorsal longitudinal flight muscles of Drosophila. J. Cell Biol. 141:1998;1135-1145.
65. Ruiz Gómez M., Bate M. Segregation of myogenic lineages in Drosophila requires numb. Development. 124:1997;3407-3414.
66. Rushton E., Drysdale R., Abmayr S.M., Michelson A.M., Bate M. Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development. 121:1995;1979-1988.
67. Südhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 375:1995;645-653.
68. Taylor, M.V., 1996. A myogenic switch. Muscle development. Curr. Biol. 6, 924-926.
69. Taylor M.V., Beatty K.E., Hunter H.K., Baylies M.K. Drosophila MEF2 is regulated by twist and is expressed in both the primordia and differentiated cells of the embryonic somatic, visceral and heart musculature. Mech. Dev. 50:1995;29-41.
70. Wassarman P.M. Towards molecular mechanisms for gamete adhesion and fusion during mammalian fertilization. Curr. Opin. Cell Biol. 7:1995;658-664.
71. Weber T., Zemelman B.V., McNew J.A., Westerman B., Gmachl M., Parlati F., Söllner T.H., Rothman J.E. SNAREpins: minimal machinery for membrane fusion. Cell. 92:1998;759-772.
72. Wilson N.F., Snell W.J. Microvilli and cell-cell fusion during fertilization. Trends Cell Biol. 8:1998;93-96.
73. Yaffe M.P. Mitochondrial morphogenesis: fusion factor for fly fertility. Curr. Biol. 7:1997;782-783.
74. Yagami-Hiromasa T., Sato T., Kurisaki T., Kamijo K., Nabeshima Y., Fujisawa-Sehara A. A metalloprotease-desintegrin participating in myoblast fusion. Nature. 377:1995;652-656.
75. Zeschnigk M., Kozian D., Kuch C., Schmoll M., Starzinski-Powitz A. Involvement of M-cadherin in terminal differentation of skeletal muscle cells. J. Cell Sci. 108:1995;2973-2981.