Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Oct 1;103(4):1569–1575. doi: 10.1083/jcb.103.4.1569

Attachment of cells to basement membrane collagen type IV

PMCID: PMC2114329  PMID: 3771647

Abstract

Of ten different cell lines examined, three showed distinct attachment and spreading on collagen IV substrates, and neither attachment nor spreading was enhanced by adding soluble laminin or fibronectin. This reaction was not inhibited by cycloheximide or antibodies to laminin, indicating a direct attachment to collagen IV without the need of mediator proteins. Cell-binding sites were localized to the major triple-helical domain of collagen IV and required an intact triple helical conformation for activity. Fibronectin showed preferential binding to denatured collagen IV necessary to mediate cell binding to the substrate. Fibronectin binding sites of collagen IV were mapped to unfolded structures of the major triple-helical domain and show a similar specificity to fibronectin-binding sites of collagen I. The data extend previous observations on biologically potential binding sites located in the triple helix of basement membrane collagen IV.

Full Text

The Full Text of this article is available as a PDF (820.1 KB).

Selected References

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

  1. Adelmann-Grill B. C. Independence of reciprocal attachment sites on denatured collagen and fibronectin from antigenic sites, and binding of gelatin-based plasma substitutes to plasma fibronectin. Coll Relat Res. 1981 Jul;1(4):367–75. doi: 10.1016/s0174-173x(81)80013-1. [DOI] [PubMed] [Google Scholar]
  2. Alitalo K., Bornstein P., Vaheri A., Sage H. Biosynthesis of an unusual collagen type by human astrocytoma cells in vitro. J Biol Chem. 1983 Feb 25;258(4):2653–2661. [PubMed] [Google Scholar]
  3. Alitalo K., Kurkinen M., Vaheri A., Virtanen I., Rohde H., Timpl R. Basal lamina glycoproteins are produced by neuroblastoma cells. Nature. 1980 Oct 2;287(5781):465–466. doi: 10.1038/287465a0. [DOI] [PubMed] [Google Scholar]
  4. Alitalo K., Myllyla R., Sage H., Pritzl P., Vaheri A., Bornstein P. Biosynthesis of type V procollagen by A204, a human rhabdomyosarcoma cell line. J Biol Chem. 1982 Aug 10;257(15):9016–9024. [PubMed] [Google Scholar]
  5. Alitalo K., Vaheri A., Krieg T., Timpl R. Biosynthesis of two subunits of type IV procollagen and of other basement membrane proteins by a human tumor cell line. Eur J Biochem. 1980 Aug;109(1):247–255. doi: 10.1111/j.1432-1033.1980.tb04790.x. [DOI] [PubMed] [Google Scholar]
  6. Aumailley M., Krieg T., Razaka G., Müller P. K., Bricaud H. Influence of cell density on collagen biosynthesis in fibroblast cultures. Biochem J. 1982 Sep 15;206(3):505–510. doi: 10.1042/bj2060505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Babel W., Glanville R. W. Structure of human-basement-membrane (type IV) collagen. Complete amino-acid sequence of a 914-residue-long pepsin fragment from the alpha 1(IV) chain. Eur J Biochem. 1984 Sep 17;143(3):545–556. doi: 10.1111/j.1432-1033.1984.tb08404.x. [DOI] [PubMed] [Google Scholar]
  8. Borg T. K., Rubin K., Lundgren E., Borg K., Obrink B. Recognition of extracellular matrix components by neonatal and adult cardiac myocytes. Dev Biol. 1984 Jul;104(1):86–96. doi: 10.1016/0012-1606(84)90038-1. [DOI] [PubMed] [Google Scholar]
  9. Butler W. T., Piez K. A., Bornstein P. Isolation and characterization of the cyanogen bromide peptides from the alpha-1 chain of rat skin collagen. Biochemistry. 1967 Dec;6(12):3771–3780. doi: 10.1021/bi00864a022. [DOI] [PubMed] [Google Scholar]
  10. Charonis A. S., Tsilibary E. C., Yurchenco P. D., Furthmayr H. Binding of laminin to type IV collagen: a morphological study. J Cell Biol. 1985 Jun;100(6):1848–1853. doi: 10.1083/jcb.100.6.1848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chiang T. M., Kang A. H. Isolation and purification of collagen alpha 1(I) receptor from human platelet membrane. J Biol Chem. 1982 Jul 10;257(13):7581–7586. [PubMed] [Google Scholar]
  12. Dennis J., Waller C., Timpl R., Schirrmacher V. Surface sialic acid reduces attachment of metastatic tumour cells to collagen type IV and fibronectin. Nature. 1982 Nov 18;300(5889):274–276. doi: 10.1038/300274a0. [DOI] [PubMed] [Google Scholar]
  13. Dziadek M., Paulsson M., Timpl R. Identification and interaction repertoire of large forms of the basement membrane protein nidogen. EMBO J. 1985 Oct;4(10):2513–2518. doi: 10.1002/j.1460-2075.1985.tb03964.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edgar D., Timpl R., Thoenen H. The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J. 1984 Jul;3(7):1463–1468. doi: 10.1002/j.1460-2075.1984.tb01997.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Engel J., Odermatt E., Engel A., Madri J. A., Furthmayr H., Rohde H., Timpl R. Shapes, domain organizations and flexibility of laminin and fibronectin, two multifunctional proteins of the extracellular matrix. J Mol Biol. 1981 Jul 25;150(1):97–120. doi: 10.1016/0022-2836(81)90326-0. [DOI] [PubMed] [Google Scholar]
  16. Engvall E., Bell M. L., Carlsson R. N., Miller E. J., Ruoslahti E. Nonhelical, fibronectin-binding basement-membrane collagen from endodermal cell culture. Cell. 1982 Jun;29(2):475–482. doi: 10.1016/0092-8674(82)90164-7. [DOI] [PubMed] [Google Scholar]
  17. Engvall E., Ruoslahti E., Miller E. J. Affinity of fibronectin to collagens of different genetic types and to fibrinogen. J Exp Med. 1978 Jun 1;147(6):1584–1595. doi: 10.1084/jem.147.6.1584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fujiwara S., Wiedemann H., Timpl R., Lustig A., Engel J. Structure and interactions of heparan sulfate proteoglycans from a mouse tumor basement membrane. Eur J Biochem. 1984 Aug 15;143(1):145–157. doi: 10.1111/j.1432-1033.1984.tb08353.x. [DOI] [PubMed] [Google Scholar]
  19. Goldberg B. Binding of soluble type I collagen molecules to the fibroblast plasma membrane. Cell. 1979 Feb;16(2):265–275. doi: 10.1016/0092-8674(79)90004-7. [DOI] [PubMed] [Google Scholar]
  20. Kleinman H. K., Cannon F. B., Laurie G. W., Hassell J. R., Aumailley M., Terranova V. P., Martin G. R., DuBois-Dalcq M. Biological activities of laminin. J Cell Biochem. 1985;27(4):317–325. doi: 10.1002/jcb.240270402. [DOI] [PubMed] [Google Scholar]
  21. Kleinman H. K., McGoodwin E. B., Martin G. R., Klebe R. J., Fietzek P. P., Woolley D. E. Localization of the binding site for cell attachment in the alpha1(I) chain of collagen. J Biol Chem. 1978 Aug 25;253(16):5642–5646. [PubMed] [Google Scholar]
  22. Kurkinen M., Taylor A., Garrels J. I., Hogan B. L. Cell surface-associated proteins which bind native type IV collagen or gelatin. J Biol Chem. 1984 May 10;259(9):5915–5922. [PubMed] [Google Scholar]
  23. Labarca C., Paigen K. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980 Mar 1;102(2):344–352. doi: 10.1016/0003-2697(80)90165-7. [DOI] [PubMed] [Google Scholar]
  24. Laurie G. W., Bing J. T., Kleinman H. K., Hassell J. R., Aumailley M., Martin G. R., Feldmann R. J. Localization of binding sites for laminin, heparan sulfate proteoglycan and fibronectin on basement membrane (type IV) collagen. J Mol Biol. 1986 May 5;189(1):205–216. doi: 10.1016/0022-2836(86)90391-8. [DOI] [PubMed] [Google Scholar]
  25. Lesot H., Kühl U., Mark K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J. 1983;2(6):861–865. doi: 10.1002/j.1460-2075.1983.tb01514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Malinoff H. L., Wicha M. S. Isolation of a cell surface receptor protein for laminin from murine fibrosarcoma cells. J Cell Biol. 1983 May;96(5):1475–1479. doi: 10.1083/jcb.96.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mollenhauer J., Bee J. A., Lizarbe M. A., von der Mark K. Role of anchorin CII, a 31,000-mol-wt membrane protein, in the interaction of chondrocytes with type II collagen. J Cell Biol. 1984 Apr;98(4):1572–1579. doi: 10.1083/jcb.98.4.1572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mollenhauer J., von der Mark K. Isolation and characterization of a collagen-binding glycoprotein from chondrocyte membranes. EMBO J. 1983;2(1):45–50. doi: 10.1002/j.1460-2075.1983.tb01378.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Murray J. C., Stingl G., Kleinman H. K., Martin G. R., Katz S. I. Epidermal cells adhere preferentially to type IV (basement membrane) collagen. J Cell Biol. 1979 Jan;80(1):197–202. doi: 10.1083/jcb.80.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Oberbäumer I., Wiedemann H., Timpl R., Kühn K. Shape and assembly of type IV procollagen obtained from cell culture. EMBO J. 1982;1(7):805–810. doi: 10.1002/j.1460-2075.1982.tb01251.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ott U., Odermatt E., Engel J., Furthmayr H., Timpl R. Protease resistance and conformation of laminin. Eur J Biochem. 1982 Mar;123(1):63–72. doi: 10.1111/j.1432-1033.1982.tb06499.x. [DOI] [PubMed] [Google Scholar]
  32. Palotie A., Peltonen L., Risteli L., Risteli J. Effect of the structural components of basement membranes on the attachment of teratocarcinoma-derived endodermal cells. Exp Cell Res. 1983 Mar;144(1):31–37. doi: 10.1016/0014-4827(83)90438-x. [DOI] [PubMed] [Google Scholar]
  33. Palotie A., Tryggvason K., Peltonen L., Seppä H. Components of subendothelial aorta basement membrane. Immunohistochemical localization and role in cell attachment. Lab Invest. 1983 Sep;49(3):362–370. [PubMed] [Google Scholar]
  34. Paulsson M., Deutzmann R., Timpl R., Dalzoppo D., Odermatt E., Engel J. Evidence for coiled-coil alpha-helical regions in the long arm of laminin. EMBO J. 1985 Feb;4(2):309–316. doi: 10.1002/j.1460-2075.1985.tb03630.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rao C. N., Margulies I. M., Tralka T. S., Terranova V. P., Madri J. A., Liotta L. A. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed] [Google Scholar]
  36. Rao N. C., Barsky S. H., Terranova V. P., Liotta L. A. Isolation of a tumor cell laminin receptor. Biochem Biophys Res Commun. 1983 Mar 29;111(3):804–808. doi: 10.1016/0006-291x(83)91370-0. [DOI] [PubMed] [Google Scholar]
  37. Risteli J., Wick G., Timpl R. Immunological characterization of the 7-S domain of type IV collagens. Coll Relat Res. 1981 Sep;1(5):419–432. doi: 10.1016/s0174-173x(81)80026-x. [DOI] [PubMed] [Google Scholar]
  38. Rubin K., Hök M., Obrink B., Timpl R. Substrate adhesion of rat hepatocytes: mechanism of attachment to collagen substrates. Cell. 1981 May;24(2):463–470. doi: 10.1016/0092-8674(81)90337-8. [DOI] [PubMed] [Google Scholar]
  39. Terranova V. P., Rao C. N., Kalebic T., Margulies I. M., Liotta L. A. Laminin receptor on human breast carcinoma cells. Proc Natl Acad Sci U S A. 1983 Jan;80(2):444–448. doi: 10.1073/pnas.80.2.444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Terranova V. P., Rohrbach D. H., Martin G. R. Role of laminin in the attachment of PAM 212 (epithelial) cells to basement membrane collagen. Cell. 1980 Dec;22(3):719–726. doi: 10.1016/0092-8674(80)90548-6. [DOI] [PubMed] [Google Scholar]
  41. Timpl R., Bruckner P., Fietzek P. Characterization of pepsin fragments of basement membrane collagen obtained from a mouse tumor. Eur J Biochem. 1979 Apr 2;95(2):255–263. doi: 10.1111/j.1432-1033.1979.tb12961.x. [DOI] [PubMed] [Google Scholar]
  42. Timpl R., Johansson S., van Delden V., Oberbäumer I., Hök M. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes. J Biol Chem. 1983 Jul 25;258(14):8922–8927. [PubMed] [Google Scholar]
  43. Timpl R., Martin G. R., Bruckner P., Wick G., Wiedemann H. Nature of the collagenous protein in a tumor basement membrane. Eur J Biochem. 1978 Mar;84(1):43–52. doi: 10.1111/j.1432-1033.1978.tb12139.x. [DOI] [PubMed] [Google Scholar]
  44. Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
  45. Timpl R., Wiedemann H., van Delden V., Furthmayr H., Kühn K. A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem. 1981 Nov;120(2):203–211. doi: 10.1111/j.1432-1033.1981.tb05690.x. [DOI] [PubMed] [Google Scholar]
  46. Vlodavsky I., Levi A., Lax I., Fuks Z., Schlessinger J. Induction of cell attachment and morphological differentiation in a pheochromocytoma cell line and embryonal sensory cells by the extracellular matrix. Dev Biol. 1982 Oct;93(2):285–300. doi: 10.1016/0012-1606(82)90118-x. [DOI] [PubMed] [Google Scholar]
  47. Woodley D. T., Rao C. N., Hassell J. R., Liotta L. A., Martin G. R., Kleinman H. K. Interactions of basement membrane components. Biochim Biophys Acta. 1983 Dec 27;761(3):278–283. doi: 10.1016/0304-4165(83)90077-6. [DOI] [PubMed] [Google Scholar]
  48. Yamada K. M. Cell surface interactions with extracellular materials. Annu Rev Biochem. 1983;52:761–799. doi: 10.1146/annurev.bi.52.070183.003553. [DOI] [PubMed] [Google Scholar]
  49. Yurchenco P. D., Furthmayr H. Self-assembly of basement membrane collagen. Biochemistry. 1984 Apr 10;23(8):1839–1850. doi: 10.1021/bi00303a040. [DOI] [PubMed] [Google Scholar]
  50. von der Mark H., Oberbäumer I., Timpl R., Kemler R., Wick G. Immunochemical and autoantigenic properties of the globular domain of basement membrane collagen (type IV). Eur J Biochem. 1985 Feb 1;146(3):555–562. doi: 10.1111/j.1432-1033.1985.tb08687.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES