Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Sep 1;111(3):1245–1254. doi: 10.1083/jcb.111.3.1245

The alpha 1-alpha 6 subunits of integrins are characteristically expressed in distinct segments of developing and adult human nephron

PMCID: PMC2116295  PMID: 2144000

Abstract

We studied the distribution of the alpha 1-alpha 6 subunits of beta 1 integrins in developing and adult human kidney using a panel of mAbs in indirect immunofluorescence microscopy. Uninduced mesenchyme displayed a diffuse immunoreactivity for only the alpha 1 integrin subunit. At the S-shaped body stage of nephron development, several of the alpha subunits were characteristically expressed in distinct fetal nephron segments, and the pattern was retained also in the adult nephron. Thus, the alpha 1 subunit was characteristically expressed in mesangial and endothelial cells, the alpha 2 in glomerular endothelium and distal tubules, the alpha 3 in podocytes, Bowman's capsule, and distal tubules, and the alpha 6 subunit basally in all tubules, and only transiently in podocytes during development. Unlike the alpha 3 and alpha 6 subunits, the alpha 2 subunit displayed an overall cell surface distribution in distal tubules. It was also distinctly expressed in glomerular endothelia during glomerulogenesis. The beta 4 subunit was expressed only in fetal collecting ducts, and hence the alpha 6 subunit seems to be complexed with the beta 1 rather than beta 4 subunit in human kidney. Of the two fibronectin receptor alpha subunits, alpha 4 and alpha 5, only the latter was expressed, confined to endothelia of developing and adult blood vessels, suggesting that these receptor complexes play a minor role during nephrogenesis. The present results suggest that distinct integrins play a role during differentiation of specific nephron segments. They also indicate that alpha 3 beta 1 and alpha 6 beta 1 integrin complexes may function as basement membrane receptors in podocytes and tubular epithelial cells.

Full Text

The Full Text of this article is available as a PDF (4.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahamson D. R., Irwin M. H., St John P. L., Perry E. W., Accavitti M. A., Heck L. W., Couchman J. R. Selective immunoreactivities of kidney basement membranes to monoclonal antibodies against laminin: localization of the end of the long arm and the short arms to discrete microdomains. J Cell Biol. 1989 Dec;109(6 Pt 2):3477–3491. doi: 10.1083/jcb.109.6.3477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams J. C., Watt F. M. Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature. 1989 Jul 27;340(6231):307–309. doi: 10.1038/340307a0. [DOI] [PubMed] [Google Scholar]
  3. Aufderheide E., Chiquet-Ehrismann R., Ekblom P. Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol. 1987 Jul;105(1):599–608. doi: 10.1083/jcb.105.1.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aumailley M., Timpl R., Sonnenberg A. Antibody to integrin alpha 6 subunit specifically inhibits cell-binding to laminin fragment 8. Exp Cell Res. 1990 May;188(1):55–60. doi: 10.1016/0014-4827(90)90277-h. [DOI] [PubMed] [Google Scholar]
  5. Bacallao R., Fine L. G. Molecular events in the organization of renal tubular epithelium: from nephrogenesis to regeneration. Am J Physiol. 1989 Dec;257(6 Pt 2):F913–F924. doi: 10.1152/ajprenal.1989.257.6.F913. [DOI] [PubMed] [Google Scholar]
  6. Beck K., Hunter I., Engel J. Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 1990 Feb 1;4(2):148–160. doi: 10.1096/fasebj.4.2.2404817. [DOI] [PubMed] [Google Scholar]
  7. Boucaut J. C., Darribère T., Boulekbache H., Thiery J. P. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. 1984 Jan 26-Feb 1Nature. 307(5949):364–367. doi: 10.1038/307364a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Bronner-Fraser M. Alterations in neural crest migration by a monoclonal antibody that affects cell adhesion. J Cell Biol. 1985 Aug;101(2):610–617. doi: 10.1083/jcb.101.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bronner-Fraser M. An antibody to a receptor for fibronectin and laminin perturbs cranial neural crest development in vivo. Dev Biol. 1986 Oct;117(2):528–536. doi: 10.1016/0012-1606(86)90320-9. [DOI] [PubMed] [Google Scholar]
  11. Chen W. T., Chen J. M., Mueller S. C. Coupled expression and colocalization of 140K cell adhesion molecules, fibronectin, and laminin during morphogenesis and cytodifferentiation of chick lung cells. J Cell Biol. 1986 Sep;103(3):1073–1090. doi: 10.1083/jcb.103.3.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. De Strooper B., Van der Schueren B., Jaspers M., Saison M., Spaepen M., Van Leuven F., Van den Berghe H., Cassiman J. J. Distribution of the beta 1 subgroup of the integrins in human cells and tissues. J Histochem Cytochem. 1989 Mar;37(3):299–307. doi: 10.1177/37.3.2645360. [DOI] [PubMed] [Google Scholar]
  13. Desjardins M., Bendayan M. Heterogenous distribution of type IV collagen, entactin, heparan sulfate proteoglycan, and laminin among renal basement membranes as demonstrated by quantitative immunocytochemistry. J Histochem Cytochem. 1989 Jun;37(6):885–897. doi: 10.1177/37.6.2723404. [DOI] [PubMed] [Google Scholar]
  14. Duband J. L., Rocher S., Chen W. T., Yamada K. M., Thiery J. P. Cell adhesion and migration in the early vertebrate embryo: location and possible role of the putative fibronectin receptor complex. J Cell Biol. 1986 Jan;102(1):160–178. doi: 10.1083/jcb.102.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ekblom M., Klein G., Mugrauer G., Fecker L., Deutzmann R., Timpl R., Ekblom P. Transient and locally restricted expression of laminin A chain mRNA by developing epithelial cells during kidney organogenesis. Cell. 1990 Jan 26;60(2):337–346. doi: 10.1016/0092-8674(90)90748-4. [DOI] [PubMed] [Google Scholar]
  16. Ekblom P., Alitalo K., Vaheri A., Timpl R., Saxén L. Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci U S A. 1980 Jan;77(1):485–489. doi: 10.1073/pnas.77.1.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ekblom P. Developmentally regulated conversion of mesenchyme to epithelium. FASEB J. 1989 Aug;3(10):2141–2150. doi: 10.1096/fasebj.3.10.2666230. [DOI] [PubMed] [Google Scholar]
  18. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. doi: 10.1083/jcb.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ekblom P., Lehtonen E., Saxén L., Timpl R. Shift in collagen type as an early response to induction of the metanephric mesenchyme. J Cell Biol. 1981 May;89(2):276–283. doi: 10.1083/jcb.89.2.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ekblom P., Miettinen A., Virtanen I., Wahlström T., Dawnay A., Saxén L. In vitro segregation of the metanephric nephron. Dev Biol. 1981 May;84(1):88–95. doi: 10.1016/0012-1606(81)90373-0. [DOI] [PubMed] [Google Scholar]
  21. Ekblom P., Vestweber D., Kemler R. Cell-matrix interactions and cell adhesion during development. Annu Rev Cell Biol. 1986;2:27–47. doi: 10.1146/annurev.cb.02.110186.000331. [DOI] [PubMed] [Google Scholar]
  22. Fradet Y., Cordon-Cardo C., Thomson T., Daly M. E., Whitmore W. F., Jr, Lloyd K. O., Melamed M. R., Old L. J. Cell surface antigens of human bladder cancer defined by mouse monoclonal antibodies. Proc Natl Acad Sci U S A. 1984 Jan;81(1):224–228. doi: 10.1073/pnas.81.1.224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fujimoto T., Singer S. J. Immunocytochemical studies of endothelial cells in vivo. II. Chicken aortic and capillary endothelial cells exhibit different cell surface distributions of the integrin complex. J Histochem Cytochem. 1988 Oct;36(10):1309–1317. doi: 10.1177/36.10.2458407. [DOI] [PubMed] [Google Scholar]
  24. Gehlsen K. R., Dickerson K., Argraves W. S., Engvall E., Ruoslahti E. Subunit structure of a laminin-binding integrin and localization of its binding site on laminin. J Biol Chem. 1989 Nov 15;264(32):19034–19038. [PubMed] [Google Scholar]
  25. 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]
  26. Giltay J. C., Brinkman H. J., Modderman P. W., von dem Borne A. E., van Mourik J. A. Human vascular endothelial cells express a membrane protein complex immunochemically indistinguishable from the platelet VLA-2 (glycoprotein Ia-IIa) complex. Blood. 1989 Apr;73(5):1235–1241. [PubMed] [Google Scholar]
  27. Grant D. S., Tashiro K., Segui-Real B., Yamada Y., Martin G. R., Kleinman H. K. Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell. 1989 Sep 8;58(5):933–943. doi: 10.1016/0092-8674(89)90945-8. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Hedin U., Bottger B. A., Luthman J., Johansson S., Thyberg J. A substrate of the cell-attachment sequence of fibronectin (Arg-Gly-Asp-Ser) is sufficient to promote transition of arterial smooth muscle cells from a contractile to a synthetic phenotype. Dev Biol. 1989 Jun;133(2):489–501. doi: 10.1016/0012-1606(89)90052-3. [DOI] [PubMed] [Google Scholar]
  30. Heino J., Ignotz R. A., Hemler M. E., Crouse C., Massagué J. Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit. J Biol Chem. 1989 Jan 5;264(1):380–388. [PubMed] [Google Scholar]
  31. Hemler M. E., Crouse C., Sonnenberg A. Association of the VLA alpha 6 subunit with a novel protein. A possible alternative to the common VLA beta 1 subunit on certain cell lines. J Biol Chem. 1989 Apr 15;264(11):6529–6535. [PubMed] [Google Scholar]
  32. Hemler M. E., Huang C., Schwarz L. The VLA protein family. Characterization of five distinct cell surface heterodimers each with a common 130,000 molecular weight beta subunit. J Biol Chem. 1987 Mar 5;262(7):3300–3309. [PubMed] [Google Scholar]
  33. Hemler M. E., Huang C., Takada Y., Schwarz L., Strominger J. L., Clabby M. L. Characterization of the cell surface heterodimer VLA-4 and related peptides. J Biol Chem. 1987 Aug 25;262(24):11478–11485. [PubMed] [Google Scholar]
  34. Hemler M. E., Sanchez-Madrid F., Flotte T. J., Krensky A. M., Burakoff S. J., Bhan A. K., Springer T. A., Strominger J. L. Glycoproteins of 210,000 and 130,000 m.w. on activated T cells: cell distribution and antigenic relation to components on resting cells and T cell lines. J Immunol. 1984 Jun;132(6):3011–3018. [PubMed] [Google Scholar]
  35. Holzmann B., McIntyre B. W., Weissman I. L. Identification of a murine Peyer's patch--specific lymphocyte homing receptor as an integrin molecule with an alpha chain homologous to human VLA-4 alpha. Cell. 1989 Jan 13;56(1):37–46. doi: 10.1016/0092-8674(89)90981-1. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Horikoshi S., Koide H., Shirai T. Monoclonal antibodies against laminin A chain and B chain in the human and mouse kidneys. Lab Invest. 1988 May;58(5):532–538. [PubMed] [Google Scholar]
  38. Hunter D. D., Shah V., Merlie J. P., Sanes J. R. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature. 1989 Mar 16;338(6212):229–234. doi: 10.1038/338229a0. [DOI] [PubMed] [Google Scholar]
  39. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  40. Hynes R. O., Marcantonio E. E., Stepp M. A., Urry L. A., Yee G. H. Integrin heterodimer and receptor complexity in avian and mammalian cells. J Cell Biol. 1989 Jul;109(1):409–420. doi: 10.1083/jcb.109.1.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kajiji S. M., Davceva B., Quaranta V. Six monoclonal antibodies to human pancreatic cancer antigens. Cancer Res. 1987 Mar 1;47(5):1367–1376. [PubMed] [Google Scholar]
  42. Kajiji S., Tamura R. N., Quaranta V. A novel integrin (alpha E beta 4) from human epithelial cells suggests a fourth family of integrin adhesion receptors. EMBO J. 1989 Mar;8(3):673–680. doi: 10.1002/j.1460-2075.1989.tb03425.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kashgarian M., Biemesderfer D., Caplan M., Forbush B., 3rd Monoclonal antibody to Na,K-ATPase: immunocytochemical localization along nephron segments. Kidney Int. 1985 Dec;28(6):899–913. doi: 10.1038/ki.1985.216. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. 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]
  47. Kramer R. H., Marks N. Identification of integrin collagen receptors on human melanoma cells. J Biol Chem. 1989 Mar 15;264(8):4684–4688. [PubMed] [Google Scholar]
  48. Kramer R. H., McDonald K. A., Vu M. P. Human melanoma cells express a novel integrin receptor for laminin. J Biol Chem. 1989 Sep 15;264(26):15642–15649. [PubMed] [Google Scholar]
  49. Krotoski D. M., Domingo C., Bronner-Fraser M. Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo. J Cell Biol. 1986 Sep;103(3):1061–1071. doi: 10.1083/jcb.103.3.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Laitinen L., Hormia M., Virtanen I. Psophocarpus tetragonolobus agglutinin reveals N-acetyl galactosaminyl residues confined to endothelial cells and some epithelial cells in human tissues. J Histochem Cytochem. 1990 Jun;38(6):875–884. doi: 10.1177/38.6.2110587. [DOI] [PubMed] [Google Scholar]
  51. Languino L. R., Gehlsen K. R., Wayner E., Carter W. G., Engvall E., Ruoslahti E. Endothelial cells use alpha 2 beta 1 integrin as a laminin receptor. J Cell Biol. 1989 Nov;109(5):2455–2462. doi: 10.1083/jcb.109.5.2455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Larjava H., Peltonen J., Akiyama S. K., Yamada S. S., Gralnick H. R., Uitto J., Yamada K. M. Novel function for beta 1 integrins in keratinocyte cell-cell interactions. J Cell Biol. 1990 Mar;110(3):803–815. doi: 10.1083/jcb.110.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Laurie G. W., Horikoshi S., Killen P. D., Segui-Real B., Yamada Y. In situ hybridization reveals temporal and spatial changes in cellular expression of mRNA for a laminin receptor, laminin, and basement membrane (type IV) collagen in the developing kidney. J Cell Biol. 1989 Sep;109(3):1351–1362. doi: 10.1083/jcb.109.3.1351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Liesi P., Dahl D., Vaheri A. Laminin is produced by early rat astrocytes in primary culture. J Cell Biol. 1983 Mar;96(3):920–924. doi: 10.1083/jcb.96.3.920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Menko A. S., Boettiger D. Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation. Cell. 1987 Oct 9;51(1):51–57. doi: 10.1016/0092-8674(87)90009-2. [DOI] [PubMed] [Google Scholar]
  56. Morrow J. S., Cianci C. D., Ardito T., Mann A. S., Kashgarian M. Ankyrin links fodrin to the alpha subunit of Na,K-ATPase in Madin-Darby canine kidney cells and in intact renal tubule cells. J Cell Biol. 1989 Feb;108(2):455–465. doi: 10.1083/jcb.108.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pytela R., Pierschbacher M. D., Ruoslahti E. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell. 1985 Jan;40(1):191–198. doi: 10.1016/0092-8674(85)90322-8. [DOI] [PubMed] [Google Scholar]
  58. Rogers S. L., Letourneau P. C., Pech I. V. The role of fibronectin in neural development. Dev Neurosci. 1989;11(4-5):248–265. doi: 10.1159/000111904. [DOI] [PubMed] [Google Scholar]
  59. Rosa J. P., McEver R. P. Processing and assembly of the integrin, glycoprotein IIb-IIIa, in HEL cells. J Biol Chem. 1989 Jul 25;264(21):12596–12603. [PubMed] [Google Scholar]
  60. Ruoslahti E. Fibronectin and its receptors. Annu Rev Biochem. 1988;57:375–413. doi: 10.1146/annurev.bi.57.070188.002111. [DOI] [PubMed] [Google Scholar]
  61. Ruoslahti E., Giancotti F. G. Integrins and tumor cell dissemination. Cancer Cells. 1989 Dec;1(4):119–126. [PubMed] [Google Scholar]
  62. Sanes J. R. Extracellular matrix molecules that influence neural development. Annu Rev Neurosci. 1989;12:491–516. doi: 10.1146/annurev.ne.12.030189.002423. [DOI] [PubMed] [Google Scholar]
  63. Sariola H., Aufderheide E., Bernhard H., Henke-Fahle S., Dippold W., Ekblom P. Antibodies to cell surface ganglioside GD3 perturb inductive epithelial-mesenchymal interactions. Cell. 1988 Jul 15;54(2):235–245. doi: 10.1016/0092-8674(88)90556-9. [DOI] [PubMed] [Google Scholar]
  64. Schittny J. C., Timpl R., Engel J. High resolution immunoelectron microscopic localization of functional domains of laminin, nidogen, and heparan sulfate proteoglycan in epithelial basement membrane of mouse cornea reveals different topological orientations. J Cell Biol. 1988 Oct;107(4):1599–1610. doi: 10.1083/jcb.107.4.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sonnenberg A., Janssen H., Hogervorst F., Calafat J., Hilgers J. A complex of platelet glycoproteins Ic and IIa identified by a rat monoclonal antibody. J Biol Chem. 1987 Jul 25;262(21):10376–10383. [PubMed] [Google Scholar]
  66. Sonnenberg A., Modderman P. W., Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 1988 Dec 1;336(6198):487–489. doi: 10.1038/336487a0. [DOI] [PubMed] [Google Scholar]
  67. Springer T. A., Dustin M. L., Kishimoto T. K., Marlin S. D. The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: cell adhesion receptors of the immune system. Annu Rev Immunol. 1987;5:223–252. doi: 10.1146/annurev.iy.05.040187.001255. [DOI] [PubMed] [Google Scholar]
  68. Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development. 1988 Apr;102(4):639–655. doi: 10.1242/dev.102.4.639. [DOI] [PubMed] [Google Scholar]
  69. Vainio S., Lehtonen E., Jalkanen M., Bernfield M., Saxén L. Epithelial-mesenchymal interactions regulate the stage-specific expression of a cell surface proteoglycan, syndecan, in the developing kidney. Dev Biol. 1989 Aug;134(2):382–391. doi: 10.1016/0012-1606(89)90110-3. [DOI] [PubMed] [Google Scholar]
  70. Vartio T., Laitinen L., Närvänen O., Cutolo M., Thornell L. E., Zardi L., Virtanen I. Differential expression of the ED sequence-containing form of cellular fibronectin in embryonic and adult human tissues. J Cell Sci. 1987 Nov;88(Pt 4):419–430. doi: 10.1242/jcs.88.4.419. [DOI] [PubMed] [Google Scholar]
  71. Vestweber D., Kemler R., Ekblom P. Cell-adhesion molecule uvomorulin during kidney development. Dev Biol. 1985 Nov;112(1):213–221. doi: 10.1016/0012-1606(85)90135-6. [DOI] [PubMed] [Google Scholar]
  72. Wayner E. A., Carter W. G. Identification of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J Cell Biol. 1987 Oct;105(4):1873–1884. doi: 10.1083/jcb.105.4.1873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wayner E. A., Garcia-Pardo A., Humphries M. J., McDonald J. A., Carter W. G. Identification and characterization of the T lymphocyte adhesion receptor for an alternative cell attachment domain (CS-1) in plasma fibronectin. J Cell Biol. 1989 Sep;109(3):1321–1330. doi: 10.1083/jcb.109.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Werb Z., Tremble P. M., Behrendtsen O., Crowley E., Damsky C. H. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J Cell Biol. 1989 Aug;109(2):877–889. doi: 10.1083/jcb.109.2.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Ylänne J., Virtanen I. The Mr 140,000 fibronectin receptor complex in normal and virus-transformed human fibroblasts and in fibrosarcoma cells: identical localization and function. Int J Cancer. 1989 Jun 15;43(6):1126–1136. doi: 10.1002/ijc.2910430628. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES