Epidermal tendon cells require Broad Complex function for correct attachment of the indirect flight muscles in Drosophila melanogaster

Journal of Cell Science

Volumn 112, Issue 22, 1999, Pages 4051-4065

  Sandstrom, David J ^a,b   Restifo, Linda L ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

Author keywords

Ecdysone cascade; Genetic mosaic; Metamorphosis; Myotendinous junction

Indexed keywords

ECDYSONE; ISOPROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; DEVELOPMENT; DROSOPHILA MELANOGASTER; EMBRYO; EPIDERMIS CELL; FLIGHT MUSCLE; GENE; GENE MUTATION; GENOTYPE; INSECT; METAMORPHOSIS; MICROTUBULE; MOSAICISM; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STRESS; TENDON; ULTRASTRUCTURE;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPIDERMIS; FLIGHT, ANIMAL; MICROSCOPY, ELECTRON; MOSAICISM; MUSCLE DEVELOPMENT; MUSCLE FIBERS; MUSCLES; MUTATION; NEUROMUSCULAR JUNCTION; PHENOTYPE; TENDONS; TRANSCRIPTION FACTORS;

ANIMALIA; DROSOPHILA MELANOGASTER; INSECTA; MELANOGASTER;

EID: 0033490052     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (97)

1. Anand, A., Fernandes, J., Arunan, M. C., Bhosekar, S., Chopra, A., Dedhia, N., Sequiera, K., Hasan, G., Palazzolo, M. J., VijayRaghavan, K. and Rodrigues, V. (1990). Drosophila 'enhancer trap' transposants: gene expression in chemosensory and motor pathways and identification of mutants affected in smell and taste ability. J. Genet. 69, 151-168.
2. Armand, P., Knapp, A. C., Hirsch, A. J., Wieschaus, E. F. and Cole, M. D. (1994). A novel basic helix-loop-helix protein is expressed in muscle attachment sites of the Drosophila epidermis. Mol. Cell. Biol. 14, 4145-4154.
3. Ashburner, M. (1989). Drosophila: A Laboratory Handbook. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
4. Auber, J. (1963). Ultrastructure de la jonction myo-épidermique chez les diptères. J. Microscopie 2, 325-336.
5. Bainbridge, S. P. and Bownes, M. (1981). Staging of the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66, 57-80.
6. Baker, B. S. (1975). paternal loss (pal): a meiotic mutant in Drosophila melanogaster causing loss of paternal chromosomes. Genetics 80, 267-296.
7. Baker, R. and Schubiger, G. (1995). Ectoderm induces muscle-specific gene expression in Drosophila embryos. Development 121, 1387-1398.
8. Bate, M. (1993). The mesoderm and its derivatives. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 1013-1090. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
9. Bate, M., Landgraf, M. and Gomez-Bate, M. R. (1999). Development of larval body wall muscles. In Neuromuscular Junctions in Drosophila (ed. V. Budnik and L. S. Gramates), pp. 25-44. San Diego, CA: Academic Press. [alt: Int. Rev. Neurobiol.] 43, 25-44.
10. Bayer, C. A., Holley, B. and Fristrom, J. W. (1996a). A switch in Broad-Complex zinc-finger isoform expression is regulated post-transcriptionally during the metamorphosis of Drosophila imaginal discs. Dev. Biol. 176, 166-184.
11. Bayer, C. A., von Kalm, L. and Fristrom, J. W. (1996b). Gene regulation in imaginal disc and salivary gland development during Drosophila metamorphosis. In Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells (ed. L. I. Gilbert, J. R. Tata and B. G. Atkinson), pp. 322-361. Academic Press, San Diego.
12. Bayer, C. A., von Kalm, L. and Fristrom, J. W. (1997). Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev. Biol. 187, 267-282.
13. Becker, S., Pasca, G., Strumpf, D., Min, L. and Volk, T. (1997). Reciprocal signaling between Drosophila epidermal muscle attachment cells and their corresponding muscles. Development 124, 2615-2622
14. Bernstein, S. I., O'Donnell, P. T. and Cripps, R. M. (1993). Molecular genetic analysis of muscle development, structure, and function in Drosophila. Int. Rev. Cytol. 143, 63-152.
15. Bogaert, T., Brown, N. and Wilcox, M. (1987). The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localised to muscle attachments. Cell 51, 929-940.
16. Buttgereit, D., Leiss, D., Michiels, F. and Renkawitz-Pohl, R. (1991) During Drosophila embryogenesis the beta 1 tubulin gene is specifically expressed in the nervous system and the apodemes. Mech. Dev. 33, 107-118
17. Buttgereit, D. (1996). Transcription of the β1 tubulin (βTub56D) gene in apodemes is strictly dependent on muscle insertion during embryogenesis in Drosophila melanogaster. Eur. J. Cell Biol. 71, 183-191.
18. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila. Development 122, 2761-2767.
19. Campos, A. R., Grossman, D. and White, K. (1985). Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J. Neurogenet. 2, 197-218.
20. Cantera, R. and Technau, G. M. (1996). Glial cells phagocytose neuronal debris during the metamorphosis of the central nervous system in Drosophila melanogaster. Dev. Genes Evol. 206, 277-280.
21. Caveney, S. (1969). Muscle attachment related to cuticle architecture in Apterygota. J. Cell Sci. 4, 541-559.
22. Chao, A. T. and Guild, G. M. (1986). Molecular analysis of the ecdysterone-inducible 2B5 'early' puff in Drosophila melanogaster. EMBO J. 5, 143-150.
23. Coggshall, J. C. (1978). Neurons associated with the dorsal longitudinal flight muscles of Drosophila melanogaster. J. Comp. Neurol. 177, 707-720.
24. Costello, W. J. and Wyman, R. J. (1986). Development of an indirect flight muscle in a muscle-specific mutant of Drosophila melanogaster. Dev. Biol. 118, 247-258.
25. Crossgrove, K., Bayer, C. A., Fristrom, J. W. and Guild, G. M. (1996). The Drosophila Broad-Complex early gene directly regulates late gene transcription during the ecdysone-induced puffing cascade. Dev. Biol. 180, 745-758.
26. de la Pompa, J. L., Garcia, J. R. and Ferrus, A. (1989). Genetic analysis of muscle development in Drosophila melanogaster. Dev. Biol. 131, 439-454.
27. Deng, W.-M. and Bownes, M. (1997). Two signaling pathways specify localised expression of the Broad-Complex in Drosophila eggshell. Development 124, 4639-4647.
28. DiBello, P. R., Withers, D. A., Bayer, C. A., Fristrom, J. W. and Guild, G. M. (1991). The Drosophila Broad-Complex encodes a family of related proteins containing zinc-fingers. Genetics 129, 385-397.
29. Dickinson, M. H. and Tu, M. S. (1997). The function of dipteran flight muscle. Comp. Biochem. Physiol. 116A, 223-238.
30. Dressel, U., Thormeyer, D., Altincicek, B., Paululat, A., Eggert, M., Schneider, S., Tenbaum, S. P., Renkawitz, R. and Baniahmad, A. (1999). Alien, a highly conserved protein with characteristics of a corepressor for members of the nuclear hormone receptor superfamily. Mol. Cell. Biol. 19, 3383-3394.
31. Drysdale, R., Rushton, E. and Bate, M. (1993). Genes required for embryonic muscle development in Drosophila melanogaster. Roux's Arch. Dev. Biol. 202, 276-295.
32. Eccles, J. C. (1944). Investigations on muscle atrophies arising from disuse and tenotomy. J. Physiol 103, 253-266.
33. Elgin, S. R. and Miller, D. W. (1978). Mass rearing of flies and mass production and harvesting of eggs. In The Genetics and Biology of Drosophila (ed. M. Ashburner and T. R. F. Wright). pp. 112-121. New York: Academic Press.
34. Emery, I. F., Bedian, V. and Guild, G. M. (1994). Differential expression of Broad-Complex transcription factors may forecast distinct developmental tissue fates during Drosophila metamorphosis. Development 120, 3275-3287.
35. Ewer, J., Frisch, B., Hamblen-Coyle, M. J., Rosbash, M. and Hall, J. C. (1992). Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on behavioral rhythms. J. Neurosci. 12, 3321-3349.
36. Fernandes, J. J. and Keshishian, H. (1998). Nerve-muscle interaction during flight muscle development in Drosophila. Development 125, 1769-1779.
37. Fernandes, J. and VijayRaghavan, K. (1993). The development of indirect flight muscle innervation in Drosophila melanogaster. Development 118, 215-227.
38. Fernandes, J., Bate, M. and VijayRaghavan, K. (1991). Development of the indirect flight muscles of Drosophila. Development 113, 67-77.
39. Fernandes, J. J., Celniker, S. E. and VijayRaghavan, K. (1996). Development of the indirect flight muscle attachment sites in Drosophila. The role of the PS integrins and the stripe gene. Dev. Biol. 176, 166-184.
40. Fristrom, D. and Fristrom, J. (1993). The metamorphic development of the adult epidermis. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 843-897. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Fristrom, D., Wilcox, M. and Fristrom, J. (1993). The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development 117, 509-523.
42. Frommer, G., Vobrüggen, G., Pasca, G., Jäckle, H. and Volk, T. (1996). Epidermal egr-like zinc-finger protein of Drosophila participates in myotube guidance. EMBO J. 15, 1642-1649.
43. Gollvik, L., Kellerth, J. O. and Ulfhake, B. (1988). The effects of tenotomy and overload on the postnatal development of muscle fibre histochemislry in the cat triceps surae. Acta Physiol. Scand. 132, 353-362.
44. Goriely, A., Dumont, N., Dambly-Chaudiere, C. and Ghysen, A. (1991). The determination of sense organs in Drosophila: effect of the neurogenic mutations in the embryo. Development 113, 1395-1404.
45. Goubeaud, A., Knirr, S., Renkawitz-Pohl, R. and Paululat, A. (1996). The Drosophila gene alien is expressed in the muscle attachment sites during embryogenesis and encodes a protein highly conserved between plants, Drosophila and vertebrates. Mech. Dev. 57, 59-68.
46. Halfon, M. S. and Keshishian, H. (1998). The Toll pathway is required in the epidermis for muscle development in the Drosophila embryo. Dev. Biol. 199, 164-174.
47. Hartenstein, V. and Posakony, J. W. (1989). Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 389-405.
48. Hartenstein, V., Technau, G. M. and Campos-Ortega, J. (1985). Fate mapping in wild-type Drosophila melanogaster. III. A fate map of the blastoderm. Roux's Arch. Dev. Biol. 194, 213-216.
49. Hess, N., Kronert, W. A. and Bernstein, S. I. (1989). Transcriptional and post-transcriptional regulation of Drosophila myosin heavy chain gene expression. In Cellular and Molecular Biology of Muscle Development (ed. L. Kedes and F Stockdale), pp. 621-631. New York: Alan R. Liss.
50. Huang, R.-Y. and Orr, W. C. (1992). Broad-Complex function during oogenesis in Drosophila melanogaster. Dev Genet. 13, 277-288.
51. Huet, F., Ruiz, C. and Richards, G. (1993). Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development 118, 613-627.
52. Hummon, M. R. and Costello, W. J. (1993). Flight muscle formation in Drosophila mosaics: requirement for normal shibire function of endocytosis. Roux's Arch. Dev. Biol. 202, 95-102.
53. Ikeda, K. and Koenig, J. H. (1988). Morphological identification of the motor neurons innervating the dorsal longitudinal muscle of Drosophila melanogaster. J. Comp. Neurol. 273, 436-444.
54. Kardon, G. (1998). Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019-4032.
55. Karim, F. D., Guild, G. M. and Thummel, C. S. (1993). The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118, 977-988.
56. Karpati, G., Carpenter, S. and Eisen, A. A. (1972). Experimental core-like lesions and nemaline rods. A correlative morphological and physiological study. Arch. Neurol. 27, 237-251.
57. Kiss, I., Beaton, A. H., Tardiff, J., Fristrom, D. and Fristrom, J. W. (1988). Interactions and developmental effects of mutations in the Broad Complex of Drosophila melanogaster. Genetics 118, 247-259.
58. Kok, L. P. and Boon, M. E. (1992). Microwave Cookbook for Microscopists. Leiden: Coulomb Press Leyden.
59. Kurata, S., Saito, H. and Natori, S. (1992). The 29-kDa hemocyte proteinase dissociates fat body at metamorphosis of Sarcophaga. Dev. Biol. 153, 115-121.
60. Lai-Fook, J. (1963). The structure of developing muscle insertions in insects. J. Morphol. 123, 503-528.
61. Lawrence, P. A. (1982). Cell lineage of the thoracic muscles of Drosophila. Cell 29, 493-503.
62. Lawrence, P. A. and Johnston, P. (1986). Observations on cell lineage of internal organs of Drosophila. J. Embryol. Exp. Morphol. 91, 251-266.
63. Lee, J. C., VijayRaghavan, K., Celniker, S. E. and Tanouye, M. A. (1995). Identilication of a Drosophila muscle development gene with structural homology to mammalian early growth response transcription factors. Proc. Nat. Acad. Sci. USA 92, 10344-10348.
64. Lindsley, D. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.
65. Liu, E. and Restifo, L. L. (1998). Identification of a Broad Complex-regulated enhancer in the developing visual system of Drosophila. J. Neurobiol. 34, 253-270.
66. Login, G. R. and Dvorak, A. M. (1994). The Microwave Tool Book. Boston, MA: Beth Israel Corp.
67. Longhurst, C. M. and Jennings, L. K. (1998). Integrin-mediated signal transduction. Cell. Mol. Life Sci. 54, 514-526.
68. Margolis, R. N. and Baker, J. H. (1983). Ultrastructure and biochemical changes in rat soleus muscle following tenotomy. Anat Rec. 206, 239-245.
69. Modolell, J. (1997). Patterning of the adult peripheral nervous system of Drosophila. Perspect. Dev. Neurobiol. 4, 285-296.
70. Newman, S. M. Jr and Wright T. R. (1981). A histological and ultrastructural analysis of developmental defects produced by the mutation. letha(l)myospheroid, in Drosophila melanogaster. Dev. Biol. 86, 393-402
71. Pauli, D., Arrigo, A.-P. and Tissières, A. (1992). Heat shock response in Drosophila. Experientia 48, 623-629.
72. Poodry, C. A. (1980). Epidermis: morphology and development. In Genetics and Biology of Drosophila vol. 2d (ed. M. Ashburner and T. R. F. Wright), pp. 443-497. Academic Press, New York.
73. Poulson, D. F. (1945). Chromosomal control of embryogenesis in Drosophila. Am. Nat. 79, 340-363
74. Prokop, A., Martin-Bermudo, M. D., Bate, M. and Brown, N. H. (1998). Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embyros. Dev. Biol. 196, 58-76.
75. Prout, M., Damania, Z., Soong, J., Fristrom, D. and Fristrom, J. W. (1997). Autosomal mutations affecting adhesions between wing surfaces in Drosophila melanogaster. Genetics 146, 275-285.
76. Reedy, M. C. and Beall, C. (1993a). Ultrastructure of developing flight muscles in Drosophila. I. Assembly of myotibrits. Dev. Biol. 160, 443-465.
77. Reedy, M. C. and Beall, C. (1993b). Ultrastructure of developing flight muscles in Drosophila. II. Formation of the myotendon junction. Dev. Biol. 160, 466-479.
78. Reedy, M. C. and Reedy, M. K. (1985). Rigor crossbridge structure in tilted single filament layers and flared-X formations from insect flight muscle. J. Mol. Biol. 185, 145-176.
79. Restifo, L. L. and Hauglum, W. (1998). Parallel molecular genetic pathways operate during CNS metamorphosis in Drosophila. Mol. Cell. Neurosci. 11, 134-148.
80. Restifo, L. L. and White, K. (1991) Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev. Biol. 148, 174-194.
81. Restifo, L. L., and White, K. (1992). Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle and gut. Roux's. Dev. Biol. 201, 221-234.
82. Reynolds, E. S. (1963). Use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-213.
83. Rheuben, M. B. (1992). Degenerative changes in the muscle fibers of Manduca sexta during metamorphosis. J. Exp. Biol. 167, 91-117.
84. Sandstrom, D. J., Bayer, C. A., Fristrom, J. W. and Restifo, L. L. (1997). Broad-Complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev. Biol. 181, 168-185.
85. Shatoury, H. H. (1956). Developmental interactions in the development of the imaginal muscles of Drosophila. J. Embryo. Exp. Morph. 4, 228-239.
86. Shilo, B.-Z. and Raz, E. (1991). Developmental control of the Drosophila EGF receptor homolog DER. Trends Genet. 7, 388-392.
87. Smith, D. S. (1982). The structure of insect muscles. In Insect Ultrastructure, vol. 2 (ed. R. C. King and H. Akai), pp. 111-150. Plenum Press, New York.
88. Sokal, R. R. and Rohlf, J. F. (1993). Biometry. W. H. Freeman and Company, New York.
89. Strumpf, D. and Volk, T. (1998). Kakapo, a novel cytoskeletal-associated protein is essential for the restricted localisation of the neuregulin-like factor, Vein, at the muscle-tendon junction site. J. Cell Biol. 143, 1259-1270.
90. Tepass, U. and Hartenstein, V. (1994). The development of intercellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
91. VijayRaghavan, K., Gendre, N. and Stocker, R. F. (1996). Transplanted wing and leg imaginal dises in Drosophila melanogaster demonstrate interactions between epidermis and myoblasts in muscle formation. Dev. Genes Evol. 206, 46-53.
92. Volk, T. and VijayRaghavan, K. (1994). A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 120, 59-70.
93. von Kalm, L., Crossgrove, K., Von Seggern, D., Guild, G. M. and Beckendorf, S. K. (1994). The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J. 13, 3505-3516.
94. Vorbrüggen, G. and Jäckle, H. (1997). Epidermal muscle attachment site-specific target gene expression and interference with myotube guidance in response to ectopic stripe expression in the developing Drosophila epidermis. Proc. Nat. Acad. Sci. USA 94, 8606-8611.
95. Williams, C. M. and Williams, M. V. (1943). The flight muscles of Drosophila repleta. J. Morphol. 72, 589-599.
96. Williams, G. J. and Caveney, S. (1980). A gradient of morphogenetic information involved in muscle patterning. J. Embryol. Exp. Morphol. 58, 35-61.
97. Yarnitzky, T., Min, L. and Volk, T. (1997). The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev. 11, 2691-2700.