Integrins as mediators of morphogenesis in Drosophila

Developmental Biology

Volumn 223, Issue 1, 2000, Pages 1-16

  Brown, Nicholas H ^a,b   Gregory, Stephen L ^a,b   Martin Bermudo, Maria D ^b  

^a WELLCOME CRC INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; INTEGRIN;

CELL ADHESION; CELL MIGRATION; DEVELOPMENT; DROSOPHILA; MORPHOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0034235392     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2000.9711     Document Type: Review

References (95)

1. Adams J. A., Watt F. M. Regulation of development and differentiation by the extracellular matrix. Development. 117:1993;1183-1198.
2. Alatortsev V. E., Kramerova I. A., Frolov M. V., Lavrov S. A., Westphal E. D. Vinculin gene is non-essential in Drosophila melanogaster. FEBS Lett. 413:1997;197-210.
3. Baehrecke E. H. who encodes a KH RNA binding protein that functions in muscle development. Development. 124:1997;1323-1332.
4. Beumer K., Rohrbough J., Prokop A., Broadie K. A role for PS integrins in morphological growth and synaptic function at the postembryonic neuromuscular junction of Drosophila. Development. 126:1999;5833-5846.
5. PS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions. Genetics. 148:1998;1127-1142.
6. Borchiellini C., Coulon J., Le Parco Y. The function of type IV collagen during Drosophila muscle development. Mech. Dev. 58:1996;179-191.
7. Brabant M. C., Brower D. L. PS2 integrin requirements in Drosophila embryo and wing morphogenesis. Dev. Biol. 157:1993;49-59.
8. Brabant M. C., Fristrom D., Bunch T. A., Baker S. E., Brower D. L. The PS integrins are required for a regulatory event during Drosophila wing morphogenesis. Ann. N. Y. Acad. Sci. 857:1998;99-109.
9. Brabant M. C., Fristrom D., Bunch T. A., Brower D. L. Distinct spatial and temporal functions for PS integrins during Drosophila wing morphogenesis. Development. 122:1996;3307-3317.
10. Brakebush C., Hirsch E., Potocnik A., Fassler R. Genetic analysis of β1 integrin function: Confirmed, new and revised roles for a crucial family of cell adhesion molecules. J. Cell Sci. 110:1997;2895-2904.
11. Brancolini C., Benedetti M., Schneider C. Microfilament reorganization during apoptosis: The role of Gas2, a possible substrate for ICE-like proteases. EMBO J. 14:1995;5179-5190.
12. PS1 integrin subunit. Development. 121:1995;1311-1320.
13. Brower D. L., Wilcox M., Piovant M., Smith R. J., Reger L. A. Related cell-surface antigens expressed with positional specificity in Drosophila imaginal discs. Proc. Natl. Acad. Sci. USA. 81:1984;7485-7489.
14. Brown N. H. Integrins hold Drosophila together. BioEssays. 15:1993;383-390.
15. PS integrin subunit genes have distinct phenotypes. Development. 120:1994;1221-1231.
16. Bunch T. A., Graner M. W., Fessler L. I., Fessler J. H., Scheneider 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. 125:1998;1679-1689.
17. Science. 282:1998;2012-2018.
18. Cheresh D. A., Mecham R. P. Integrins: Molecular and Biological Responses to the Extracellular Matrix. 1994;Academic Press, London.
19. Chi H.-C., Hui C.-F. Primary structure of the Drosophila laminin B2 chain and comparison with human, mouse, and Drosophila laminin B1 and B2 chains. J. Biol. Chem. 264:1989;1543-1550.
20. Clark E. A., Brugge J. S. Integrins and signal transduction pathways: The road taken. Science. 268:1995;233-239.
21. Cubadda Y., Heitzler P., Ray R. P., Bourouis M., Ramain P., Gelbart W., Simpson P., Haenlin M. u-shaped encodes a zinc finger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila. Genes Dev. 11:1997;3083-3095.
22. Darribere T., Guida K., Lajarva H., Johnson K. E., Yamada K. M., Thiery J. P., Boucaut J. C. In vivo analyses of integrin β1 subunit function in fibronectin matrix assembly. J. Cell Biol. 110:1990;1813-1823.
23. 3 (platelet GPIIb-IIIa). Cell. 65:1991;409-416.
24. Dunin-Borkowski O. M., Brown N. H., Bate M. Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila. Development. 121:1995;4183-4193.
25. Nucleic Acids Res. 27:1999;85-88.
26. PS integrins. Development. 120:1994;1747-1758.
27. Fristrom D., Fristrom J. The metamorphic development of the adult epidermis. Bate M., Martinez-Arias A. The Development of Drosophila melanogaster. 1992;843-897 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
28. Fristrom D., Wilcox M., Fristrom J. The distribution of PS integrins, Laminin A and F-actin during key stages in Drosophila wing development. Development. 117:1993;509-523.
29. Fryberg C., Becker J., Barthmaier P., Mahaffey J., Fryberg E. A Drosophila muscle-specific gene related to the mouse quaking locus. Gene. 197:1997;315-323.
30. Giancotti F., Ruoslahti E. Integrin signaling. Science. 13:1999;1028-1032.
31. Golic K. G. Site-specific recombination between homologous chromosomes in Drosophila. Science. 252:1991;958-961.
32. Gotwals P. J., Fessler L. I., Wehril M., Hynes R. O. Drosophila PS1 integrin is a laminin receptor and differs in ligand specificity from PS2. Proc. Natl. Acad. Sci. USA. 91:1994a;11447-11451.
33. Gotwals P. J., Paine-Saunders S. E., Stark K., Hynes R. O. Drosophila integrins and their ligands. Curr. Opin. Cell. Biol. 6:1994b;734-739.
34. Graner M. W., Bunch T. A., Baumgartner S., Kerschen A., Brower D. L. Splice variants of the Drosophila PS2 integrins differentially interact with RGD-containing fragments of the extracellular proteins tiggrin, ten-m, and D-laminin 2. J. Biol. Chem. 273:1998;18235-18241.
35. Gregory S. L., Brown N. H. kakapo, a gene required for adhesion between and within cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J. Cell Biol. 143:1998;1271-1282.
36. Grotewiel M. S., Beck C. D. O., Wu K. H., Zhu X. R., Davis R. L. Integrin-mediated short-term memory in Drosophila. Nature. 391:1998;455-460.
37. Gumbiner B. M. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell. 84:1996;345-357.
38. Hoang B., Chiba A. Genetic analysis on the role of integrin during axon guidance in Drosophila. J. Neurosci. 18:1998;7847-7855.
39. Hynes R. O. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell. 69:1992;11-25.
40. Knust E. Drosophila morphogenesis: Movements behind the edge. Curr. Biol. 7:1997;558-561.
41. Leptin M., Bogaert T., Lehmann R., Wilcox M. The function of PS integrins during Drosophila embryogenesis. Cell. 56:1989;401-408.
42. Leung C. L., Sun D., Zheng M., Knowles D. R., Liem R. K. H. Microtubule actin cross-linking factor (MACF): A hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J. Cell Biol. 147:1999;1275-1285.
43. Lindsley D. L., Zimm G. The Genome of Drosophila melanogaster. 1992;Academic Press, London.
44. Longley R. L., Ready D. F. Integrins and the development of 3-dimensional structure in the Drosophila compound eye. Dev. Biol. 171:1995;415-433.
45. Lukashev M. E., Sheppard D., Pytela R. Disruption of integrin function and induction of tyrosine phosphorylation by the autonomously expressed β1 integrin cytoplasmic domain. J. Biol. Chem. 269:1994;18311-18314.
46. Martin D., Zusman S., Li X., Williams E., 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. 145:1999;191-201.
47. Martin-Bermudo M. D., Alvarez-Garcia I., Brown N. H. Migration of the Drosophila primordial midgut cells requires coordination of diverse PS integrin functions. Development. 126:1999;5161-5169.
48. Martin-Bermudo M. D., Brown N. H. Intracellular signals direct integrin localization to sites of function in embryonic muscles. J. Cell. Biol. 134:1996;217-226.
49. PS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo. Genes Dev. 13:1999;729-739.
50. Martin-Bermudo M. D., Dunin-Borkowski O. M., Brown N. H. Specificity of PS integrin function during embryogenesis resides in the α subunit extracellular domain. EMBO J. 16:1997;4184-4193.
51. Martin-Bermudo M. D., Dunin-Borkowski O. M., Brown N. H. Modulation of integrin activity is vital for morphogenesis. J. Cell Biol. 141:1998;1073-1081.
52. Miyamoto S., Akiyama S. K., Yamada K. M. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science. 267:1995a;883-885.
53. Miyamoto S., Teramoto H., Coso O. A., Gutkind J. S., Burbelo P. D., Akiyama S. K., Yamada K. M. Integrin function: Molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131:1995b;791-805.
54. Montagne J., Groppe J., Guillemin K., Krasnow M. A., Gehring W. J., Affolter M. The Drosophila serum response factor gene is required for the formation of the intervein tissue in the wing and is allelic to blistered. Development. 122:1996;2589-2597.
55. Montell D. J., Goodman C. S. Drosophila substrate adhesion molecule: Sequence of laminin B1 chain reveals domains of homology with mouse. Cell. 53:1988;463-473.
56. Montell D. J., Goodman C. S. Drosophila laminin: Sequence of B2 subunit and expression of all three subunits during embryogenesis. J. Cell Biol. 109:1989;2441-2453.
57. Newman S. M. Jr., Wright T. R. F. A histological and ultrastructural analysis of developmental defects produced by the mutation, lethal(1)myospheroid, in Drosophila melanogaster. Dev. Biol. 86:1981;393-402.
58. Nievers M., Schaapveld R., Sonnenberg A. Biology and function of hemidesmosomes. Matrix Biol. 18:1999;5-17.
59. Okuda T., Matsuda S., Nakatsugawa S., Ichigotani Y., Iwahashi N., Takahashi M., Ishigaki T., Hamaguchi M. Molecular cloning of macrophin, a human homologue of Drosophila kakapo with a close structural similarity to plectin and dystrophin. Biochem. Biophys. Res. Commun. 264:1999;568-574.
60. Panganiban G. E. F., Reuter R., Scott M., Hoffmann F. M. A Drosophila growth factor homolog, decapentaplegic, regulates homeotic gene expression within and across germ layers during midgut morphogenesis. Development. 110:1990;1041-1050.
61. Pankratz M. J., Hoch M. Control of epithelial morphogenesis by cell signaling and integrin molecules in the Drosophila foregut. Development. 121:1995;1885-1898.
62. Priddle H., Hemmings L., Monkley S., Woods A., Patel B., Sutton D., Dunn G., Zicha D., Critchley D. Disruption of the talin gene compromises focal adhesion assembly in undifferentiated but not differentiated embryonic stem cells. J. Cell Biol. 142:1998;1121-1133.
63. Prokop A., Martin-Bermudo M. D., Bate M., Brown N. H. In Drosophila embryos, the absence of the PS integrins or laminin A affects the extracellular adhesion of hemiadherens and neuromuscular junctions, but not their intracellular assembly. Dev. Biol. 196:1998a;58-76.
64. Prokop A., Uhler J., Roote J., Bate M. The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motorneurons. J. Cell Biol. 143:1998b;1283-1294.
65. Prout M., Damania Z., Soong J., Fristrom D., Fristrom J. W. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics. 146:1997;275-285.
66. Ramirez-Weber F. A., Kornberg T. B. Cytonemes: Cellular processes that project to the principal signalling centre in Drosophila imaginal discs. Cell. 97:1999;599-607.
67. Reuter R., Grunewald B., Leptin M. A role for mesoderm in endodermal migration and morphogenesis in Drosophila. Development. 119:1993;1135-1145.
68. Roote C. E., Zusman S. Functions for PS integrins in tissue adhesion, migration, and shape changes during early embryonic development in Drosophila. Dev. Biol. 169:1995;322-336.
69. Roote C. E., Zusman S. Alternatively spliced forms of the Drosophila αPS2 subunit of integrin are sufficient for viability and can replace the function of the αPS1 subunit of integrin in the retina. Development. 122:1996;1985-1994.
70. Sasaki T., Timpl R. Laminins. Kreis T., Vale R. Guidebook to the Extracellular Matrix, Anchor, and Adhesion Proteins. 1999;Oxford Univ. Press, Oxford.
71. Sastry S. K., Horwitz A. F. Adhesion-growth factor interactions during differentiation: An integrated biological response. Dev. Biol. 180:1996;455-467.
72. Schoenwaelder S., Burridge K. Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11:1999;274-286.
73. Skaer H. The alimentary canal. Bate M., Martinez Arias A. The Development of Drosophila melanogaster. 1993;941-1012 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
74. Stark K. A., Yee G. H., Roote C. E., Williams E. L., Zusman S., Hynes R. O. A novel α integrin subunit associates with βPS and functions in tissue morphogenesis and movement during Drosophila development. Development. 124:1997;4583-4594.
75. 2+-dependent protease, calpain. J. Cell Biol. 140:1998;699-707.
76. Strumpf D., Volk T. Kakapo, a novel cytoskeletal-associated protein is essential for the restricted localization of the neuregulin-like factor, vein, at the muscle-tendon junction site. J. Cell Biol. 143:1998;1259-1270.
77. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:1995;619-627.
78. Tepass U. Genetic analysis of cadherin function in animal morphogenesis. Curr. Opin. Cell Biol. 11:1999;540-548.
79. Velling T., Kusche-Gullberg M., Sejersen T., Gullberg D. cDNA cloning and chromosomal localization of human alpha(11) integrin: A collagen-binding, I domain-containing, beta(1)-associated integrin alpha-chain present in muscle tissues. J. Biol. Chem. 274:1999;25735-25742.
80. Vleminckx K., Kemler R. Cadherins and tissue formation: Integrating adhesion and signaling. BioEssays. 21:1999;211-220.
81. Volberg T., Geiger B., Kam Z., Pankov R., Simcha I., Sabanay H., Coll J., Adamson E., Ben-Ze'ev A. Focal adhesion formation by F9 embryonal carcinoma cells after vinculin gene disruption. J. Cell Sci. 108:1995;2253-2260.
82. Volk T. Singling out Drosophila tendon cells: A dialogue between two distinct cell types. Trends Genet. 15:1999;448-453.
83. Volk T., Fessler L. I., Fessler J. H. A role for integrin in the formation of sarcomeric cytoarchitecture. Cell. 63:1990;525-536.
84. Walsh E. P., Brown N. H. A screen to identify Drosophila genes required for integrin mediated adhesion. Genetics. 150:1998;791-805.
85. Wary K. K., Mainiero F., Isakoff S. J., Marcantonio E. E., Giancotti F. G. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell. 87:1996;1733-1743.
86. Wilcox M., Brown N., Piovant M., Smith R. J., White R. A. The Drosophila position-specific antigens are a family of cell surface glycoprotein complexes. EMBO J. 3:1984;2307-2313.
87. Wright T. R. F. The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster. J. Exp. Zool. 143:1960;77-99.
88. Xu T., Rubin G. M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1993;1223-1237.
89. Yarnitzki T., Volk T. Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev. Biol. 169:1995;609-618.
90. γ, expressed in the midgut of Drosophila melanogaster. Development. 118:1993;845-858.
91. Yip M. L., Lamka M. L., Lipshitz H. D. Control of germ-band retraction in Drosophila by the zinc-finger protein HINDSIGHT. Development. 124:1997;2129-2141.
92. Yurchenko P. D., Birk D. E., Mecham R. P. Extracellular Matrix Assembly and Structure. 1994;Academic Press, San Diego/London.
93. Yurochko A. D., Liu Y. D., Eierman D., Haskill S. Integrins as a primary signal transduction molecule regulating monocyte immediate-early gene induction. Proc. Natl. Acad. Sci. USA. 89:1992;9034-9038.
94. Zaffran S., Astier M., Gratecos D., Semeriva M. The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity. Development. 124:1997;2087-2098.
95. Zusman S., Patel K. R., ffrench C. C., Hynes R. O. Requirements for integrins during Drosophila development. Development. 108:1990;391-402.