Absence of PS integrins or laminin a affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos

Developmental Biology

Volumn 196, Issue 1, 1998, Pages 58-76

  Prokop, Andreas ^a,d   Martín Bermudo, Maria D ^b,c   Bate, Michael ^a   Brown, Nicholas H ^b,c  

^a Department of Zoology ^*  (United Kingdom)

^b WELLCOME CRC INSTITUTE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Adhesion; Drosophila; Extracellular matrix; Integrin; Laminin; Neuromuscular junction

Indexed keywords

INTEGRIN; LAMININ;

ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; EPIDERMIS; EXTRACELLULAR MATRIX; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; HEXAPODA;

EID: 0345055334     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1997.8830     Document Type: Article

References (62)

1. Ashhurst, D.E. (1982). The structure and development of insect connective tissues. In "Insect Ultrastructure" (R. C. King and H. Akai, Eds.), pp. 313-350. Plenum Press, New York.
2. Barclay, A. N., Beyers, A. D., Birkeland, M. L., Brown, M. H., Davis, S. J., Somoza, C., and Williams, A. F. (1993). "The Leucocyte Antigen Facts Book." Academic Press, London.
3. Bate, M. (1993). The mesoderm and its derivatives. In "The Development of Drosophila melanogaster" (M. Bate and A. Martínez Arias, Eds.), pp. 1013-1090. CSH Laboratory Press, Cold Spring Harbor, NY.
4. 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.
5. Bogaert, T., Brown, N., and Wilcox, M. (1987). The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments. Cell 51, 929-940.
6. Borchiellini, C., Coulon, J., and LeParco, Y. (1996). The function of type IV collagen during Drosophila muscle development. Mech. Dev. 58, 179-191.
7. Brabant, M. C., and Brower, D. L. (1993). PS integrin requirements in Drosophila embryo and wing morphogenesis. Dev. Biol. 157, 49-59.
8. Brower, D. L., Bunch, T. A., Mukai, L., Adamson, T. E., Wehrli, M., Lam, S., Friedlander, E., Roote, C. E., and Zusman, S. (1995). Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the αPS1 integrin subunit. Development 121, 1311-1320.
9. Brown, N. H. (1993). Integrins hold Drosophila together. BioEssays 15, 383-390.
10. Brown, N. H. (1994). Null mutations in the αPS2 and βPS integrin subunit genes have distinct phenotypes. Development 120, 1221-1231.
11. Bunch, T. A., Salatino, R., Engelsgjerd, M. C., Mukai, L., West, R. F., and Brower, D. L. (1992). Characterisation of mutant alleles of myospheroid, the gene encoding the β subunit of the Drosophila PS integrins. Genetics 132, 519-528.
12. Butcher, E. C. (1991). Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67, 1033-1036.
13. 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.
14. Campos-Ortega, J. A., and Hartenstein, V. (1985). The embryonic development of Drosophila melanogaster. Springer Verlag, Berlin.
15. Carrell, N. A., Fitzgerald, L. A., Steiner, B., Erikson, H. P., and Phillips, D. R. (1985). Structure of human platelet membrane glycoprotein IIb and glycoprotein Ilia as determined by electron microscopy. J. Biol. Chem. 260, 1743-1749.
16. DiPersio, C. M., Hodivala Dilke, K.M., Jaenisch, R., Kreidberg, J. A., and Hynes, R. O. (1997). α3β1 integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137, 729-742.
17. Bowling, J., Yu, Q.-C., and Fuchs, E. (1996). β4 Integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol. 134, 559-572.
18. Dustin, M. L., and Springer, T. A. (1991). Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu. Rev. Immunol. 9, 2-66.
19. Elder, H. Y. (1975). Muscle structure. In "Insect Muscle" (P. N. R. Usherwood, Ed.), pp. 1-74. Academic Press, New York.
20. Ervasti, J. M., and Campbell, K. P. (1993). A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823.
21. Fernandes, J. J., Celniker, S. E., and VijayRaghavan, K. (1996). Development of the indirect flight muscle attachment sites in Drosophila: Role of the PS Integrins and the stripe gene. Dev. Biol. 176, 166-184.
22. Fogerty, F. J., Fessler, L. I., Bunch, T. A., Taron, Y., Parker, C. G., Nelson, R. E., Brower, D. L., Gullberg, D., and Fessler, J. H. (1994). Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila αPS2βPS integrins. Development 120, 1747-1758.
23. Galey, F. R., and Nilsson, S. E. G. (1966). A new method for transferring sections from the liquid surface of the trough through staining solutions to the supporting film of a grid. J. Ultrastruct. Res. 14, 405-410.
24. Garrod, D. R. (1993). Desmosomes and hemidesmosomes. Curr. Opin. Cell Biol. 5, 30-40.
25. Georges-Labouesse, E., Messaddeq, N., Yehia, G., Cadalber, L., Dierich, A., and Le Meur, M. (1996). Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nat. Gen. 13, 370-373.
26. Gotwals, P. J., Fessler, L. I., Wehril, M., and Hynes, R. O. (1994a). Drosophila PS1 integrin is a laminin receptor and differs in ligand specificity from PS2. Proc. Natl. Acad. Sci. USA 91, 11447-11451.
27. Gotwals, P. J., Paine-Saunders, S. E., Stark, K., and Hynes, R. O. (1994b). Drosophila integrins and their ligands. Curr. Opin. Cell. Biol. 6, 734-739.
28. Hall, Z. W., and Sanes, J. R. (1993). Synaptic structure and development: The neuromuscular junction. Cell/Neuron (Suppl.)72/10, 99-121.
29. Halpern, M. E., Chiba, A., Johansen, J., and Keshishian, H. (1991). Growth cone behaviour underlying the development of Stereotypie synaptic connections in Drosophila embryos. J. Neurosci. 11, 3227-3238.
30. Henchcliffe, C., García-Alonso, L. A., Tang, J., and Goodman, C. S. (1993). Genetic analysis of laminin A reveals diverse functions during morphogenesis in Drosophila. Development 118, 325-337.
31. Hynes, R. O. (1992). Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
32. Ibraghimov-Beskrovnaya, O., Ervasti, J. M., Leveille, C. J., Slaughter, C. A., Sernett, S.W., and Campbell, K.P. (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 396-702.
33. Keshishian, H., Broadie, K., Chiba, A., and Bate, M. (1996). The Drosophila neuromuscular junction: A model system for studying synaptic development and function. Annu. Rev. Neurosci. 19, 545-75.
34. Kiehart, D. P., and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
35. Koch, P. J., Mahoney, M. G., Ishikawa, H., Pulkkinen, L., Uitto, J., Shultz, L., Murphy, G. F., Whitaker-Menezes, D., and Stanley, J. R. (1997). Targeted disruption of the pemphigus vulgaris antigen (Desmoglein3) gene in mice causes loss of keratinocyte cell adhesion with a phenotype similar to pemphigus vulgaris. J. Cell Biol. 137, 1091-1102.
36. Leptin, M., Bogaert, T., Lehmann, R., and Wilcox, M. (1989). The function of PS Integrins during Drosophila embryogenesis. Cell 56, 401-408.
37. Littleton, J. T., Bellen, H. J., and Perin, M. S. (1993). Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles in the synapse. Development 118, 1077-1088.
38. Martín-Bermudo, M. D., and Brown, N. H. (1996). Intracellular signals direct integrin localization to sites of function in embryonic muscles. J. Cell Biol. 134, 217-226.
39. Martín-Bermudo, M. D., Dunin-Borkowski, O. M., and Brown, N. H. (1997). Specificity of PS integrin function during embryogenesis resides in the a subunit extracellular domain. EMBO J., in press.
40. Mayhew, T. M. (1991). The new stereological methods for interpreting functional morphology from slices of cells and organs. Exp. Physiol. 76, 639-665.
41. McGrath, J. A., Gatalica, B., Christiano, A. M., Li, K., Owaribe, K., McMillan, J. R., Eady, R. A. J., and Uitto, J. (1995). Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. Nat. Genet. 11, 83-86.
42. Meadows, L. A., Gell, D., Broadie, K., Gould, A. P., and White, R. A. H. (1994). The cell adhesion molecule, Connectin, and the development of the Drosophila neuromuscular system. J. Cell Sci. 107, 321-328.
43. Murugasu-Oei, B., Rodrigues, V., Yang, X., and Chia, W. (1995). Masquerade: A novel secreted serine protease-like molecule is required for somatic muscle attachment in the Drosophila embryo. Genes Dev. 9, 139-154.
44. Nermut, M. V., Green, N.M., Eason, P., Yamada, S. S., and Yamada, K. M. (1988). Electron microscopy and structural model of human fibronectin receptor. EMBO J. 7, 4093-4099.
45. Newman, S. M., and Wright, T. R. F. (1981). A histological and ultrastructural analysis of developmental defects produced by the mutation lethal(1)myospheroid in Drosophila melanogaster. Dev. Biol. 86, 393-402.
46. Nose, A., Mahajan, V. B., and Goodman, C. S. (1992). Connectin: A homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70, 553-567.
47. Prokop, A., Broadie, K. S., Zhu, X.-R., and Davis, R. (1998). αVolado, an integrin involved in learning and memory, as well as PS-integrins regulate synaptic plasticity in Drosophila (Abstract 6th European Symposium on Drosophila Neurobiology). J. Neurogenet., in press.
48. Prokop, A., Landgraf, M., Rushton, E., Broadie, K., and Bate, M. (1996). Presynaptic development at the Drosophila neuromuscular junction: The assembly and localisation of presynaptic active zones. Neuron 17, 617-626.
49. Prokop, A., and Technau, G. M. (1993). Cell transplantation. In "Cellular Interactions in Development: A Practical Approach" (D. Hartley, Ed.), pp. 33-57. Oxford Univ. Press, London.
50. Roberts, R. C., McCarthy, K. E., Du, F., Ottersen, O. P., Okuno, E., and Schwarcz, R. (1995). 3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum. J. Neurosci. 15, 1150-1161.
51. Roote, C. E., and Zusman, S. (1995). Functions for PS Integrins in tissue adhesion, migration, and shape changes during early embryonic development in Drosophila. Dev. Biol. 169, 322-336.
52. Schuster, C. M., Davis, W. D., Fetter, R. D., and Goodman, C. S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilisation and growth. Neuron 17, 641-654.
53. Seecof, R. L., Teplitz, R. L., Gerson, I., Ikeda, K., and Donady, J. J. (1972). Differentiation of neuromuscular junctions in cultures of embryonic Drosophila cells. Proc. Natl. Acad. Sci. USA 69, 566-570.
54. Tepass, U., and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
55. Timpl, R. (1989). Structure and biological activity of basement membrane proteins. Eur. J. Biochem. 180, 487-502.
56. Umemiya, T., Takeichi, M., and Nose, A. (1997). M-Spondin, a novel ECM protein highly homologous to vertebrate F-Spondin, is localized at the muscle attachment sites in the Drosophila embryo. Dev. Biol. 186, 165-176.
57. van der Neut, R., Krimpenfort, P., Calafat, J., Niessen, C. M., and Sonnenberg, A. (1996). Epithelial detachment due to absence of hemidesmosomes in integrin beta4 null mice. Nat. Genet. 13, 366-369.
58. Volk, T., Fessler, L. I., and Fessler, J. H. (1990). A role for integrin in the formation of sarcomeric cytoarchitecture. Cell 63, 525-536.
59. Wieschaus, E., Nusslein-Volhard, C., and Jürgens, G. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. III. Zygotic loci on the X-chromosome and fourth chromosome. Roux Arch. Dev. Biol. 193, 296-307.
60. Wright, T. R. F. (1960). The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster. J. Exp. Zool. 143, 77-99.
61. Yarnitzki, T., and Volk, T. (1995). Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev. Biol. 169, 609-618.
62. Yurchenco, P. D., Cheng, Y.-S., and Colognato, H. (1992). Laminin forms an independent network in basement membranes. J. Cell Biol. 117, 1119-1133.