Tenectin is a novel αPS2βPS integrin ligand required for wing morphogenesis and male genital looping in Drosophila

Developmental Biology

Volumn 340, Issue 2, 2010, Pages 504-517

  Fraichard, Stéphane ^b   Bougé, Anne Laure ^b,c   Kendall, Timmy ^a   Chauvel, Isabelle ^b   Bouhin, Hervé ^b   Bunch, Thomas A ^a  

^a University of Arizona   (United States)

^b CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

^c CNRS   (France)

Author keywords

Adhesion; Ecdysone; Integrin; Left right asymmetry; Looping morphogenesis; Metamorphosis; Tenectin

Indexed keywords

ALPHAPS2 INTEGRIN; BETAPS INTEGRIN; ECDYSONE; SCLEROPROTEIN; TENECTIN; UNCLASSIFIED DRUG; ALPHA INTEGRIN; DROSOPHILA PROTEIN; IF PROTEIN, DROSOPHILA; LIGAND; TNC PROTEIN, DROSOPHILA;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE INTERACTION; GENE STRUCTURE; GONAD DEVELOPMENT; IMAGINAL DISC; LIMB DEVELOPMENT; MALE; METAMORPHOSIS; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ANIMAL; DROSOPHILA; FORELIMB; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LARVA; MALE GENITAL SYSTEM; METABOLISM; MUTATION; PHYSIOLOGY; TRANSGENE;

HEXAPODA;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EXTRACELLULAR MATRIX PROTEINS; GENITALIA, MALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTEGRIN ALPHA CHAINS; LARVA; LIGANDS; MALE; MORPHOGENESIS; MUTATION; TRANSGENES; WING;

EID: 77951209268     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.02.008     Document Type: Article

References (111)

1. Abbott M.K., Lengyel J.A. Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics 1991, 129:783-789.
2. Ádám G., Perrimon N., Noselli S. The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 2003, 130:2397-2406.
3. Andres A.J., Fletcher J.C., Karim F.D., Thummel C.S. Molecular analysis of the initiation of insect metamorphosis: a comparative study of Drosophila ecdysteroid-regulated transcription. Dev. Biol. 1993, 160:388-404.
4. Bellen H.J., Levis R.W., Liao G., He Y., Carlson J.W., Tsang G., Evans-Holm M., Hiesinger P.R., Schulze K.L., Rubin G.M., Hoskins R.A., Spradling A.C. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 2004, 167:761-781.
5. Bloor J.W., Brown N.H. Genetic analysis of the Drosophila alphaPS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions. Genetics 1998, 148:1127-1142.
6. Bökel C., Brown N.H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell 2002, 3:311-321.
7. Borchiellini C., Coulon J., Le Parco Y. The function of type IV collagen during Drosophila muscle development. Mech. Dev. 1996, 58:179-191.
8. Brabant M.C., Brower D.L. PS2 integrin requirements in Drosophila embryo and wing morphogenesis. Dev. Biol. 1993, 157:49-59.
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 1996, 122:3307-3317.
10. Brower D.L. Platelets with wings: the maturation of Drosophila integrin biology. Curr. Opin. Cell Biol. 2003, 15:607-613.
11. Brower D.L., Bunch T.A., Mukai L., Adamson T.E., Wehrli M., Lam S., Friedlander E., Roote C.E., Zusman S. Nonequivalent requirements for PS1 and PS2 integrin at cell attachments in Drosophila: genetic analysis of the alpha PS1 integrin subunit. Development 1995, 121:1311-1320.
12. Brower D.L., Jaffe S.M. Requirement for integrins during Drosophila wing development. Nature 1989, 342:285-287.
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. U. S. A. 1984, 81:7485-7489.
14. Brown N.H. Null mutations in the alpha PS2 and beta PS integrin subunit genes have distinct phenotypes. Development 1994, 120:1221-1231.
15. Brown N.H., Gregory S.L., Martin-Bermudo M.D. Integrins as mediators of morphogenesis in Drosophila. Dev. Biol. 2000, 223:1-16.
16. Bunch T.A., Brower D.L. Drosophila PS2 integrin mediates RGD-dependent cell-matrix interactions. Development 1992, 116:239-247.
17. 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.
18. Cardamone M., Puri N.K., Brandon M.R. Comparing the refolding and reoxidation of recombinant porcine growth hormone from a urea denatured state and from Escherichia coli inclusion bodies. Biochemistry 1995, 34:5773-5794.
19. Casanova J., Sánchez-Herrero E., Morata G. Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell 1986, 47:627-636.
20. Casares F., Sánchez L., Guerrero I., Sánchez-Herrero E. The geneital disc of Drosophila melanogaster. I. Segmental and compartmental organization. Dev. Genes Evol. 1997, 207:216-228.
21. Chaturvedi P., Singh A.P., Batra S.K. Structure, evolution, and biology of the MUC4 mucin. FASEB J. 2008, 22:966-981.
22. Chaturvedi P., Singh A.P., Moniaux N., Senapati S., Chakraborty S., Meza J.L., Batra S.K. MUC4 mucin potentiates pancreatic tumor cell proliferation, survival, and invasive properties and interferes with its interaction to extracellular matrix proteins. Mol. Cancer Res. 2007, 5:309-320.
23. Costello W.J., Thomas J.B. Development of thoracic muscles in muscle-specific mutant and normal Drosophila melanogaster. Neuroscience 1981, 7:543. Abstr.
24. Coutelis J.B., Petzoldt A.G., Spéder P., Suzanne M., Noselli S. Left-right asymmetry in Drosophila. Semin. Cell Dev. Biol. 2008, 19:252-262.
25. D'Avino P.P., Crispi S., Polito L.C., Furia M. The role of the BR-C locus on the expression of genes located at the ecdysone-regulated 3C puff of Drosophila melanogaster. Mech. Dev. 1995, 49:161-171.
26. D'Avino P.P., Thummel C.S. The ecdysone regulatory pathway controls wing morphogenesis and integrin expression during Drosophila metamorphosis. Dev. Biol. 2000, 220:211-224.
27. Danen E.H., Sonnenberg A. Integrins in regulation of tissue development and function. J. Pathol. 2003, 201:632-641.
28. Deak I.I., Bellamy P.R., Bienz M., Dubuis Y., Fenner E., Gollin M., Rähmi A., Ramp T., Reinhardt C.A., Cotton B. Mutations affecting the indirect flight muscles of Drosophila melanogaster. J. Embryol. Exp. Morphol. 1982, 69:61-81.
29. Enerly E., Larsson J., Lambertsson A. Reverse genetics in Drosophila: from sequence to phenotype using UAS-RNAi transgenic flies. Genesis 2002, 34:152-155.
30. 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.
31. Fortier E., Belote J.M. Temperature-dependent gene silencing by an expressed inverted repeat in Drosophila. Genesis 2000, 26:240-244.
32. Fraichard S., Bouge A.L., Chauvel I., Bouhin H. Tenectin, a novel extracellular matrix protein expressed during Drosophila melanogaster embryonic development. Gene Expr. Patterns 2006, 6:772-776.
33. Fristrom D.R., Fristrom J.W. The metamorphic development of the adult epidermis. The Development of Drosophila melanogaster, Vol. 2 1993, 843-897. Cold Spring Harbor Laboratory Press, New York. M. Bate, A. Martinez Arias (Eds.).
34. Fristrom D., Wilcox M., Fristrom J. The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development 1993, 117:509-523.
35. Gleichauf R. Anatomie und variabilität des geschlechtapparates von Drosophila melanogaster (Meigen). Z. Wiss. Zool. 1936, 148:1-66.
36. 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. 1998, 273:18235-18241.
37. Grether M.E., Abrams J.M., Agapite J., White K., Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
38. Grotewiel M.S., Beck C.D., Wu K.H., Zhu X.R., Davis R.L. Integrin-mediated short-term memory in Drosophila. Nature 1998, 391:455-460.
39. Hamidpour M., Behrendt M., Griffiths B., Partridge L., Lindsey N. The isolation and characterisation of antiplatelet antibodies. Eur. J. Haematol. 2006, 76:331-338.
40. Handler A.M. Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev. Biol. 1982, 93:73-82.
41. Henchcliffe C., García-Alonso L., Tang J., Goodman C.S. Genetic analysis of laminin A reveals diverse functions during morphogenesis in Drosophila. Development 1993, 118:325-337.
42. Henrich V.C., Rybczynski R., Gilbert L.I. Peptide hormones, steroid hormones, and puffs: mechanisms and models in insect development. Vitam. Horm. 1999, 55:73-125.
43. Hirano Y., Kando Y., Hayashi T., Goto K., Nakajima A. Synthesis and cell attachment activity of bioactive oligopeptides: RGD, RGDS, RGDV, and RGDT. J. Biomed. Mater. Res. 1991, 25:1523-1534.
44. Hollingsworth M.A., Swanson B.J. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 2004, 4:45-60.
45. Hozumi S., Maeda R., Taniguchi K., Kanai M., Shirakabe S., Sasamura T., Spéder P., Noselli S., Aigaki T., Murakami R., Matsuno K. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 2006, 440:798-802.
46. Hunt L.T., Barker W.C. von Willebrand factor shares a distinctive cysteine-rich domain with thrombospondin and procollagen. Biochem. Biophys. Res. Commun. 1987, 144:876-882.
47. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
48. James B.P., Bunch T.A., Krishnamoorthy S., Perkins L.A., Brower D.L. Nuclear localization of the ERK MAP kinase mediated by Drosophila alphaPS2betaPS integrin and importin-7. Mol. Biol. Cell 2007, 18:4190-4199.
49. Jannuzi A.L., Bunch T.A., Brabant M.C., Miller S.W., Mukai L., Zavortink M., Brower D.L. Disruption of C-terminal cytoplasmic domain of betaPS integrin subunit has dominant negative properties in developing Drosophila. Mol. Biol. Cell 2002, 13:1352-1365.
50. Jannuzi A.L., Bunch T.A., West R.F., Brower D.L. Identification of integrin beta subunit mutations that alter heterodimer function in situ. Mol. Biol. Cell 2004, 15:3829-3840.
51. Johnson S.A., Milner M.J. The final stages of wing development in Drosophila melanogaster. Tissue Cell 1987, 19:505-513.
52. Juárez P., Comas I., González-Candelas F., Calvete J.J. Evolution of snake venom disintegrins by positive Darwinian selection. Mol. Biol. Evol. 2008, 25:2391-2407.
53. Karim F.D., Thummel C.S. Ecdysone coordinates the timing and amounts of E74A and E74B transcription in Drosophila. Genes Dev. 1991, 5:1067-1079.
54. Karim F.D., Thummel C.S. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J. 1992, 11:4083-4093.
55. Kennerdell J.R., Carthew R.W. Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 2000, 18:896-898.
56. Kiger J.A., Natzle J.E., Kimbrell D.A., Paddy M.R., Kleinhesselink K., Green M.M. Tissue remodeling during maturation of the Drosophila wing. Dev. Biol. 2007, 301:178-191.
57. Lam G., Thummel C.S. Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila. Curr. Biol. 2000, 10:957-963.
58. Lee S.B., Cho K.S., Kim E., Chung J. blistery encodes Drosophila tensin protein and interacts with integrin and the JNK signaling pathway during wing development. Development 2003, 130:4001-4010.
59. Leptin M., Aebersold R., Wilcox M. Drosophila position-specific antigens resemble the vertebrate fibronectin-receptor family. EMBO J. 1987, 6:1037-1043.
60. Lindsley D.L., Grell E.H. Genetic Variations of Drosophila melanogaster 1968, Carnegie Inst., Wash., Publ. No. 627.
61. Macías A., Romero N.M., Martín F., Suárez L., Rosa A.L., Morata G. PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia. Int. J. Dev. Biol. 2004, 48:1087-1094.
62. 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.
63. Martin-Bermudo M.D., Brown N.H. Uncoupling integrin adhesion and signaling: the betaPS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo. Genes Dev. 1999, 13:729-739.
64. Martin-Bermudo M.D., Dunin-Borkowski O.M., Brown N.H. Specificity of PS integrin function during embryogenesis resides in the alpha subunit extracellular domain. EMBO J. 1997, 16:4184-4193.
65. Meloty-Kapella C.V., Degen M., Chiquet-Ehrismann R., Tucker R.P. Effects of tenascin-W on osteoblasts in vitro. Cell Tissue Res. 2008, 334:445-455.
66. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
67. O'Connell P.O., Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984, 12:5495-5513.
68. Oberlander H. The imaginal discs. Comprehensive Insect Physiology, Biochemistry and Pharmacology 1985, vol. 2:151-182. Cold Spring Harbor Laboratory Press, Oxford.
69. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
70. Prasad K.S., Andre P., He M., Bao M., Manganello J., Phillips D.R. Soluble CD40 ligand induces beta3 integrin tyrosine phosphorylation and triggers platelet activation by outside-in signaling. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12367-12371.
71. Prout M., Damania Z., Soong J., Fristrom D., Fristrom J.W. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics 1997, 146:275-285.
72. Richards G. The radioimmune assay of ecdysteroid titres in Drosophila melanogaster. Mol. Cell. Endocrinol. 1981, 21:181-197.
73. Richards G. Switching partners?. Curr. Biol. 1992, 2:657-659.
74. Royer V., Hourdry A., Fraichard S., Bouhin H. Characterization of a putative extracellular matrix protein from the beetle Tenebrio molitor: hormonal regulation during metamorphosis. Dev. Genes Evol. 2004, 214:115-121.
75. Ruoslahti E., Pierschbacher M.D. New perspectives in cell adhesion: RGD and integrins. Science 1987, 238:491-497.
76. Russell S.R., Heimbeck G., Goddard C.M., Carpenter A.T., Ashburner M. The Drosophila Eip78C gene is not vital but has a role in regulating chromosome puffs. Genetics 1996, 144:159-170.
77. Sanchez-Herrero E., Crosby M.A. The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions. EMBO J. 1988, 7:2163-2173.
78. Sangiorgi F.O., Benson-Chanda V., de Wet W.J., Sobel M.E., Ramirez F. Analysis of cDNA and genomic clones coding for the pro alpha 1 chain of calf type II collagen. Nucleic Acids Res. 1985, 13:2815-2826.
79. Sasai Y., Lu B., Steinbeisser H., Geissert D., Gont L.K., De Robertis E.M. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994, 79:779-790.
80. Schöck F., Perrimon N. Retraction of the Drosophila germ band requires cell-matrix interaction. Genes Dev. 2003, 17:597-602.
81. Segraves W.A. Steroid receptors and orphan receptors in Drosophila development. Semin. Cell Biol. 1994, 5:105-113.
82. Spéder P., Ádám G., Noselli S. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 2006, 440:803-807.
83. Spéder P., Petzoldt A., Suzanne M., Noselli S. Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr. Opin. Genet. Dev. 2007, 17:351-358.
84. Springer T.A., Zhu J., Xiao T. Structural basis for distinctive recognition of fibrinogen gammaC peptide by the platelet integrin alphaIIbbeta3. J. Cell Biol. 2008, 182:791-800.
85. Stark K.A., Yee G.H., Roote C.E., Williams E.L., Zusman S., Hynes R.O. A novel alpha integrin subunit associates with betaPS and functions in tissue morphogenesis and movement during Drosophila development. Development 1997, 124:4583-4594.
86. Stone B.L., Thummel C.S. The Drosophila 78C early late puff contains E78, an ecdysone-inducible gene that encodes a novel member of the nuclear hormone receptor superfamily. Cell 1993, 75:307-320.
87. 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.
88. Syed Z.A., Härd T., Uv A., van Dijk-Härd I.F. A potential role for Drosophila mucins in development and physiology. PLoS ONE 2008, 3:e3041.
89. Takada Y., Ye X., Simon S. The integrins. Genome Biol. 2007, 8:215.
90. Taub R., Gould R.J., Garsky V.M., Ciccarone T.M., Hoxie J., Friedman P.A., Shattil S.J. A monoclonal antibody against the platelet fibrinogen receptor contains a sequence that mimics a receptor recognition domain in fibrinogen. J. Biol. Chem. 1989, 264:259-265.
91. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 1989, 98:81-85.
92. Thummel C.S. Files on steroids-Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet. 1996, 12:306-310.
93. Thummel C.S. Dueling orphans-interacting nuclear receptors coordinate Drosophila metamorphosis. Bioessays 1997, 19:669-672.
94. Tomiyama Y., Brojer E., Ruggeri Z.M., Shattil S.J., Smiltneck J., Gorski J., Kumar A., Kieber-Emmons T., Kunicki T.J. A molecular model of RGD ligands. Antibody D gene segments that direct specificity for the integrin alpha IIb beta 3. J. Biol. Chem. 1992, 267:18085-18092.
95. Van de Walle G.R., Peters S.T., VanderVen B.C., O'Callaghan D.J., Osterrieder N. Equine herpesvirus 1 entry via endocytosis is facilitated by alphaV integrins and an RSD motif in glycoprotein D. J. Virol. 2008, 82:11859-11868.
96. Verweij C.L., Diergaarde P.J., Hart M., Pannekoek H. Full-length von Willebrand factor (vWF) cDNA encodes a highly repetitive protein considerably larger than the mature vWF subunit. EMBO J. 1986, 5:1839-1847.
97. von Heijne G. How signal sequences maintain cleavage specificity. J. Mol. Biol. 1984, 173:243-251.
98. Waddington C.H. The genetic control of wing development in Drosophila. J. Genet. 1940, 41:75-139.
99. Walsh E.P., Brown N.H. A screen to identify Drosophila genes required for integrin-mediated adhesion. Genetics 1998, 150:791-805.
100. Wang P., Granados R.R. Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J. Biol. Chem. 1997, 272:16663-16669.
101. Warren J.T., Yerushalmi Y., Shimell M.J., O'Connor M.B., Restifo L.L., Gilbert L.I. Discrete pulses of molting hormone, 20-hydroxyecdysone, during late larval development of Drosophila melanogaster: correlations with changes in gene activity. Dev. Dyn. 2006, 235:315-326.
102. Wassarman D.A., Aoyagi N., Pile L.A., Schlag E.M. TAF250 is required for multiple developmental events in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1154-1159.
103. Wehrli M., DiAntonio A., Fearnley I.M., Smith R.J., Wilcox M. Cloning and characterization of alpha PS1, a novel Drosophila melanogaster integrin. Mech. Dev. 1993, 43:21-36.
104. Wilcox M., Brower D.L., Smith R.J. A position-specific cell surface antigen in the Drosophila wing imaginal disc. Cell 1981, 25:159-164.
105. Wilcox M., DiAntonio A., Leptin M. The function of PS integrins in Drosophila wing morphogenesis. Development 1989, 107:891-897.
106. Wilson T.G., Yerushalmi Y., Donnell D.M., Restifo L.L. Interaction between hormonal signaling pathways in Drosophila melanogaster as revealed by genetic interaction between Methoprene-tolerant and Broad-Complex. Genetics 2006, 172:253-264.
107. Yamada K.M. Adhesive recognition sequences. J. Biol. Chem. 1991, 266:12809-12812.
108. Zavortink M., Bunch T.A., Brower D.L. Functional properties of alternatively spliced forms of the Drosophila PS2 integrin alpha subunit. Cell Adhes. Commun. 1993, 1:251-264.
109. Zhang L., Zhang Y., Ten Hagen K.G. A mucin-type O-glycosyltransferase modulates cell adhesion during Drosophila development. J. Biol. Chem. 2008, 283:34076-34086.
110. Zusman S., Grinblat Y., Yee G., Kafatos F.C., Hynes R.O. Analyses of PS integrin functions during Drosophila development. Development 1993, 118:737-750.
111. Zusman S., Patel-King R.S., Ffrench-Constant C., Hynes R.O. Requirements for integrins during Drosophila development. Development 1990, 108:391-402.