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. 1996 Mar 2;132(6):1161–1176. doi: 10.1083/jcb.132.6.1161

Cloning of mouse integrin alphaV cDNA and role of the alphaV-related matrix receptors in metanephric development

PMCID: PMC2120751  PMID: 8601592

Abstract

Metanephrogenesis has been a long-standing model to study cell-matrix interactions. A number of adhesion molecules, including matrix receptors (i.e., integrins), are believed to be involved in such interactions. The integrins contain alpha and beta s ubunits and are present in various tissues in different heterodimeric forms. In this study, one of the members of the integrin superfamily, alphaV, was characterized, and its relevance in murine nephrogenesis was investigated. Mouse embryonic renal cDNA libraries were prepared and screened for alphaV, and multiple clones were isolated and sequenced. The deduced amino acid sequence of the alpha-v cDNA clones and hydropathic analysis revealed that it has a typical signal sequence and extracellular, transmembrane, and cytoplasmic domains, with multiple Ca2+ binding sites. No A(U)nA mRNA instability motifs were present. Conformational analysis revealed no rigid long-range-ordered structure in murine alphaV. The alphaV was expressed in the embryonic kidney at day 13 of the gestation, with a transcript size of approximately 7 kb. Its expression increased progressively during the later gestational stages and in the neonatal period. It was distributed in the epithelial elements of developing nephrons and was absent in the uninduced mesenchyme. In mature metanephroi, the expression was relatively high in the glomeruli and blood vessels, as compared to the tubules. Various heterodimeric associations of alphaV, i.e., with beta1, beta3, beta5, and beta6, were observed in metanephric tissues. Inclusion of alphaV- antisense-oligodeoxynucleotide or -antibody in metanephric culture induced dysmorphogenesis of the kidney with reduced population of the nephrons, disorganization of the ureteric bud branches, and reduction of mRNA and protein expressions of alphaV. The expressions of integrin beta3, beta5, and beta6 were unaltered. These findings suggest that the integrin alphaV is developmentally regulated, has a distinct spatio- temporal expression, and is relevant in the mammalian organogenesis.

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Selected References

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  1. Argraves W. S., Suzuki S., Arai H., Thompson K., Pierschbacher M. D., Ruoslahti E. Amino acid sequence of the human fibronectin receptor. J Cell Biol. 1987 Sep;105(3):1183–1190. doi: 10.1083/jcb.105.3.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Biesecker G. The complement SC5b-9 complex mediates cell adhesion through a vitronectin receptor. J Immunol. 1990 Jul 1;145(1):209–214. [PubMed] [Google Scholar]
  3. Blystone S. D., Graham I. L., Lindberg F. P., Brown E. J. Integrin alpha v beta 3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor alpha 5 beta 1. J Cell Biol. 1994 Nov;127(4):1129–1137. doi: 10.1083/jcb.127.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bodary S. C., McLean J. W. The integrin beta 1 subunit associates with the vitronectin receptor alpha v subunit to form a novel vitronectin receptor in a human embryonic kidney cell line. J Biol Chem. 1990 Apr 15;265(11):5938–5941. [PubMed] [Google Scholar]
  5. Bossy B., Reichardt L. F. Chick integrin alpha V subunit molecular analysis reveals high conservation of structural domains and association with multiple beta subunits in embryo fibroblasts. Biochemistry. 1990 Nov 6;29(44):10191–10198. doi: 10.1021/bi00496a006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boucaut J. C., Darribère T., Poole T. J., Aoyama H., Yamada K. M., Thiery J. P. Biologically active synthetic peptides as probes of embryonic development: a competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J Cell Biol. 1984 Nov;99(5):1822–1830. doi: 10.1083/jcb.99.5.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bronner-Fraser M. Neural crest cell formation and migration in the developing embryo. FASEB J. 1994 Jul;8(10):699–706. doi: 10.1096/fasebj.8.10.8050668. [DOI] [PubMed] [Google Scholar]
  8. Brooks P. C., Clark R. A., Cheresh D. A. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science. 1994 Apr 22;264(5158):569–571. doi: 10.1126/science.7512751. [DOI] [PubMed] [Google Scholar]
  9. Burridge K., Fath K., Kelly T., Nuckolls G., Turner C. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol. 1988;4:487–525. doi: 10.1146/annurev.cb.04.110188.002415. [DOI] [PubMed] [Google Scholar]
  10. Busk M., Pytela R., Sheppard D. Characterization of the integrin alpha v beta 6 as a fibronectin-binding protein. J Biol Chem. 1992 Mar 25;267(9):5790–5796. [PubMed] [Google Scholar]
  11. Cazenave C., Stein C. A., Loreau N., Thuong N. T., Neckers L. M., Subasinghe C., Hélène C., Cohen J. S., Toulmé J. J. Comparative inhibition of rabbit globin mRNA translation by modified antisense oligodeoxynucleotides. Nucleic Acids Res. 1989 Jun 12;17(11):4255–4273. doi: 10.1093/nar/17.11.4255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheresh D. A. Human endothelial cells synthesize and express an Arg-Gly-Asp-directed adhesion receptor involved in attachment to fibrinogen and von Willebrand factor. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6471–6475. doi: 10.1073/pnas.84.18.6471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheresh D. A., Smith J. W., Cooper H. M., Quaranta V. A novel vitronectin receptor integrin (alpha v beta x) is responsible for distinct adhesive properties of carcinoma cells. Cell. 1989 Apr 7;57(1):59–69. doi: 10.1016/0092-8674(89)90172-4. [DOI] [PubMed] [Google Scholar]
  14. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  15. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  16. Chou P. Y., Fasman G. D. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. doi: 10.1002/9780470122921.ch2. [DOI] [PubMed] [Google Scholar]
  17. Cosio F. G., Sedmak D. D., Nahman N. S., Jr Cellular receptors for matrix proteins in normal human kidney and human mesangial cells. Kidney Int. 1990 Nov;38(5):886–895. doi: 10.1038/ki.1990.287. [DOI] [PubMed] [Google Scholar]
  18. Davies J., Warwick J., Totty N., Philp R., Helfrich M., Horton M. The osteoclast functional antigen, implicated in the regulation of bone resorption, is biochemically related to the vitronectin receptor. J Cell Biol. 1989 Oct;109(4 Pt 1):1817–1826. doi: 10.1083/jcb.109.4.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dedhar S., Robertson K., Gray V. Induction of expression of the alpha v beta 1 and alpha v beta 3 integrin heterodimers during retinoic acid-induced neuronal differentiation of murine embryonal carcinoma cells. J Biol Chem. 1991 Nov 15;266(32):21846–21852. [PubMed] [Google Scholar]
  20. Delannet M., Martin F., Bossy B., Cheresh D. A., Reichardt L. F., Duband J. L. Specific roles of the alpha V beta 1, alpha V beta 3 and alpha V beta 5 integrins in avian neural crest cell adhesion and migration on vitronectin. Development. 1994 Sep;120(9):2687–2702. doi: 10.1242/dev.120.9.2687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Erle D. J., Rüegg C., Sheppard D., Pytela R. Complete amino acid sequence of an integrin beta subunit (beta 7) identified in leukocytes. J Biol Chem. 1991 Jun 15;266(17):11009–11016. [PubMed] [Google Scholar]
  22. Felding-Habermann B., Mueller B. M., Romerdahl C. A., Cheresh D. A. Involvement of integrin alpha V gene expression in human melanoma tumorigenicity. J Clin Invest. 1992 Jun;89(6):2018–2022. doi: 10.1172/JCI115811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Filardo E. J., Cheresh D. A. A beta turn in the cytoplasmic tail of the integrin alpha v subunit influences conformation and ligand binding of alpha v beta 3. J Biol Chem. 1994 Feb 11;269(6):4641–4647. [PubMed] [Google Scholar]
  24. Fitzgerald L. A., Poncz M., Steiner B., Rall S. C., Jr, Bennett J. S., Phillips D. R. Comparison of cDNA-derived protein sequences of the human fibronectin and vitronectin receptor alpha-subunits and platelet glycoprotein IIb. Biochemistry. 1987 Dec 15;26(25):8158–8165. doi: 10.1021/bi00399a021. [DOI] [PubMed] [Google Scholar]
  25. Freed E., Gailit J., van der Geer P., Ruoslahti E., Hunter T. A novel integrin beta subunit is associated with the vitronectin receptor alpha subunit (alpha v) in a human osteosarcoma cell line and is a substrate for protein kinase C. EMBO J. 1989 Oct;8(10):2955–2965. doi: 10.1002/j.1460-2075.1989.tb08445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Galileo D. S., Majors J., Horwitz A. F., Sanes J. R. Retrovirally introduced antisense integrin RNA inhibits neuroblast migration in vivo. Neuron. 1992 Dec;9(6):1117–1131. doi: 10.1016/0896-6273(92)90070-t. [DOI] [PubMed] [Google Scholar]
  27. Gehlsen K. R., Davis G. E., Sriramarao P. Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin Exp Metastasis. 1992 Mar;10(2):111–120. doi: 10.1007/BF00114587. [DOI] [PubMed] [Google Scholar]
  28. Giancotti F. G., Ruoslahti E. Elevated levels of the alpha 5 beta 1 fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell. 1990 Mar 9;60(5):849–859. doi: 10.1016/0092-8674(90)90098-y. [DOI] [PubMed] [Google Scholar]
  29. Gilliland G., Perrin S., Blanchard K., Bunn H. F. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2725–2729. doi: 10.1073/pnas.87.7.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hall D. E., Neugebauer K. M., Reichardt L. F. Embryonic neural retinal cell response to extracellular matrix proteins: developmental changes and effects of the cell substratum attachment antibody (CSAT). J Cell Biol. 1987 Mar;104(3):623–634. doi: 10.1083/jcb.104.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hayman E. G., Pierschbacher M. D., Ohgren Y., Ruoslahti E. Serum spreading factor (vitronectin) is present at the cell surface and in tissues. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4003–4007. doi: 10.1073/pnas.80.13.4003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ho S. N., Hunt H. D., Horton R. M., Pullen J. K., Pease L. R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989 Apr 15;77(1):51–59. doi: 10.1016/0378-1119(89)90358-2. [DOI] [PubMed] [Google Scholar]
  33. Hogervorst F., Kuikman I., von dem Borne A. E., Sonnenberg A. Cloning and sequence analysis of beta-4 cDNA: an integrin subunit that contains a unique 118 kd cytoplasmic domain. EMBO J. 1990 Mar;9(3):765–770. doi: 10.1002/j.1460-2075.1990.tb08171.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Holzmann B., Weissman I. L. Peyer's patch-specific lymphocyte homing receptors consist of a VLA-4-like alpha chain associated with either of two integrin beta chains, one of which is novel. EMBO J. 1989 Jun;8(6):1735–1741. doi: 10.1002/j.1460-2075.1989.tb03566.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  36. Juliano R. L., Haskill S. Signal transduction from the extracellular matrix. J Cell Biol. 1993 Feb;120(3):577–585. doi: 10.1083/jcb.120.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kerjaschki D., Ojha P. P., Susani M., Horvat R., Binder S., Hovorka A., Hillemanns P., Pytela R. A beta 1-integrin receptor for fibronectin in human kidney glomeruli. Am J Pathol. 1989 Feb;134(2):481–489. [PMC free article] [PubMed] [Google Scholar]
  38. Klein G., Langegger M., Timpl R., Ekblom P. Role of laminin A chain in the development of epithelial cell polarity. Cell. 1988 Oct 21;55(2):331–341. doi: 10.1016/0092-8674(88)90056-6. [DOI] [PubMed] [Google Scholar]
  39. Korhonen M., Laitinen L., Ylänne J., Gould V. E., Virtanen I. Integrins in developing, normal and malignant human kidney. Kidney Int. 1992 Mar;41(3):641–644. doi: 10.1038/ki.1992.98. [DOI] [PubMed] [Google Scholar]
  40. Korhonen M., Ylänne J., Laitinen L., Virtanen I. Distribution of beta 1 and beta 3 integrins in human fetal and adult kidney. Lab Invest. 1990 May;62(5):616–625. [PubMed] [Google Scholar]
  41. Korhonen M., Ylänne J., Laitinen L., Virtanen I. The alpha 1-alpha 6 subunits of integrins are characteristically expressed in distinct segments of developing and adult human nephron. J Cell Biol. 1990 Sep;111(3):1245–1254. doi: 10.1083/jcb.111.3.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kornberg L. J., Earp H. S., Turner C. E., Prockop C., Juliano R. L. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8392–8396. doi: 10.1073/pnas.88.19.8392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  44. Lehmann M., Rabenandrasana C., Tamura R., Lissitzky J. C., Quaranta V., Pichon J., Marvaldi J. A monoclonal antibody inhibits adhesion to fibronectin and vitronectin of a colon carcinoma cell line and recognizes the integrins alpha v beta 3, alpha v beta 5, and alpha v beta 6. Cancer Res. 1994 Apr 15;54(8):2102–2107. [PubMed] [Google Scholar]
  45. Lelongt B., Makino H., Dalecki T. M., Kanwar Y. S. Role of proteoglycans in renal development. Dev Biol. 1988 Aug;128(2):256–276. doi: 10.1016/0012-1606(88)90289-8. [DOI] [PubMed] [Google Scholar]
  46. Liu Z. Z., Dalecki T. M., Kashihara N., Wallner E. I., Kanwar Y. S. Effect of puromycin on metanephric differentiation: morphological, autoradiographic and biochemical studies. Kidney Int. 1991 Jun;39(6):1140–1155. doi: 10.1038/ki.1991.145. [DOI] [PubMed] [Google Scholar]
  47. Liu Z. Z., Kumar A., Wallner E. I., Wada J., Carone F. A., Kanwar Y. S. Trophic effect of insulin-like growth factor-I on metanephric development: relationship to proteoglycans. Eur J Cell Biol. 1994 Dec;65(2):378–391. [PubMed] [Google Scholar]
  48. MacKrell A. J., Blumberg B., Haynes S. R., Fessler J. H. The lethal myospheroid gene of Drosophila encodes a membrane protein homologous to vertebrate integrin beta subunits. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2633–2637. doi: 10.1073/pnas.85.8.2633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. McLean J. W., Vestal D. J., Cheresh D. A., Bodary S. C. cDNA sequence of the human integrin beta 5 subunit. J Biol Chem. 1990 Oct 5;265(28):17126–17131. [PubMed] [Google Scholar]
  50. Milner R., Ffrench-Constant C. A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development. 1994 Dec;120(12):3497–3506. doi: 10.1242/dev.120.12.3497. [DOI] [PubMed] [Google Scholar]
  51. Moyle M., Napier M. A., McLean J. W. Cloning and expression of a divergent integrin subunit beta 8. J Biol Chem. 1991 Oct 15;266(29):19650–19658. [PubMed] [Google Scholar]
  52. Neugebauer K. M., Emmett C. J., Venstrom K. A., Reichardt L. F. Vitronectin and thrombospondin promote retinal neurite outgrowth: developmental regulation and role of integrins. Neuron. 1991 Mar;6(3):345–358. doi: 10.1016/0896-6273(91)90244-t. [DOI] [PubMed] [Google Scholar]
  53. Okayama H., Berg P. High-efficiency cloning of full-length cDNA. Mol Cell Biol. 1982 Feb;2(2):161–170. doi: 10.1128/mcb.2.2.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rabinowich H., Lin W. C., Amoscato A., Herberman R. B., Whiteside T. L. Expression of vitronectin receptor on human NK cells and its role in protein phosphorylation, cytokine production, and cell proliferation. J Immunol. 1995 Feb 1;154(3):1124–1135. [PubMed] [Google Scholar]
  55. Rahilly M. A., Fleming S. Differential expression of integrin alpha chains by renal epithelial cells. J Pathol. 1992 Jul;167(3):327–334. doi: 10.1002/path.1711670311. [DOI] [PubMed] [Google Scholar]
  56. Ramaswamy H., Hemler M. E. Cloning, primary structure and properties of a novel human integrin beta subunit. EMBO J. 1990 May;9(5):1561–1568. doi: 10.1002/j.1460-2075.1990.tb08275.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Savill J., Dransfield I., Hogg N., Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature. 1990 Jan 11;343(6254):170–173. doi: 10.1038/343170a0. [DOI] [PubMed] [Google Scholar]
  59. Seftor R. E., Seftor E. A., Gehlsen K. R., Stetler-Stevenson W. G., Brown P. D., Ruoslahti E., Hendrix M. J. Role of the alpha v beta 3 integrin in human melanoma cell invasion. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1557–1561. doi: 10.1073/pnas.89.5.1557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Seiffert D., Keeton M., Eguchi Y., Sawdey M., Loskutoff D. J. Detection of vitronectin mRNA in tissues and cells of the mouse. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9402–9406. doi: 10.1073/pnas.88.21.9402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sheppard D., Rozzo C., Starr L., Quaranta V., Erle D. J., Pytela R. Complete amino acid sequence of a novel integrin beta subunit (beta 6) identified in epithelial cells using the polymerase chain reaction. J Biol Chem. 1990 Jul 15;265(20):11502–11507. [PubMed] [Google Scholar]
  62. Smith J. W., Vestal D. J., Irwin S. V., Burke T. A., Cheresh D. A. Purification and functional characterization of integrin alpha v beta 5. An adhesion receptor for vitronectin. J Biol Chem. 1990 Jul 5;265(19):11008–11013. [PubMed] [Google Scholar]
  63. Sorokin L., Sonnenberg A., Aumailley M., Timpl R., Ekblom P. Recognition of the laminin E8 cell-binding site by an integrin possessing the alpha 6 subunit is essential for epithelial polarization in developing kidney tubules. J Cell Biol. 1990 Sep;111(3):1265–1273. doi: 10.1083/jcb.111.3.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Stöckbauer P., Gahmberg C. G., Andersson L. C. Changes in cell surface glycoproteins and antigens during differentiation of the human myeloid leukemia cell lines ML-1, ML-2, and HL-60. Cancer Res. 1985 Jun;45(6):2821–2826. [PubMed] [Google Scholar]
  65. Suzuki S., Argraves W. S., Arai H., Languino L. R., Pierschbacher M. D., Ruoslahti E. Amino acid sequence of the vitronectin receptor alpha subunit and comparative expression of adhesion receptor mRNAs. J Biol Chem. 1987 Oct 15;262(29):14080–14085. [PubMed] [Google Scholar]
  66. Suzuki S., Huang Z. S., Tanihara H. Cloning of an integrin beta subunit exhibiting high homology with integrin beta 3 subunit. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5354–5358. doi: 10.1073/pnas.87.14.5354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Suzuki S., Naitoh Y. Amino acid sequence of a novel integrin beta 4 subunit and primary expression of the mRNA in epithelial cells. EMBO J. 1990 Mar;9(3):757–763. doi: 10.1002/j.1460-2075.1990.tb08170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Takada Y., Elices M. J., Crouse C., Hemler M. E. The primary structure of the alpha 4 subunit of VLA-4: homology to other integrins and a possible cell-cell adhesion function. EMBO J. 1989 May;8(5):1361–1368. doi: 10.1002/j.1460-2075.1989.tb03516.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tokunaga K., Taniguchi H., Yoda K., Shimizu M., Sakiyama S. Nucleotide sequence of a full-length cDNA for mouse cytoskeletal beta-actin mRNA. Nucleic Acids Res. 1986 Mar 25;14(6):2829–2829. doi: 10.1093/nar/14.6.2829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Venstrom K., Reichardt L. Beta 8 integrins mediate interactions of chick sensory neurons with laminin-1, collagen IV, and fibronectin. Mol Biol Cell. 1995 Apr;6(4):419–431. doi: 10.1091/mbc.6.4.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Vogel B. E., Tarone G., Giancotti F. G., Gailit J., Ruoslahti E. A novel fibronectin receptor with an unexpected subunit composition (alpha v beta 1). J Biol Chem. 1990 Apr 15;265(11):5934–5937. [PubMed] [Google Scholar]
  72. Vuori K., Ruoslahti E. Association of insulin receptor substrate-1 with integrins. Science. 1994 Dec 2;266(5190):1576–1578. doi: 10.1126/science.7527156. [DOI] [PubMed] [Google Scholar]
  73. Wada J., Liu Z. Z., Alvares K., Kumar A., Wallner E., Makino H., Kanwar Y. S. Cloning of cDNA for the alpha subunit of mouse insulin-like growth factor I receptor and the role of the receptor in metanephric development. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10360–10364. doi: 10.1073/pnas.90.21.10360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yamada K. M. Adhesive recognition sequences. J Biol Chem. 1991 Jul 15;266(20):12809–12812. [PubMed] [Google Scholar]
  75. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

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