Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Oct 1;95(1):340–344. doi: 10.1083/jcb.95.1.340

Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes

PMCID: PMC2112347  PMID: 6216257

Abstract

Electron microscopic immunostaining of rat duodenum and incisor tooth was used to examine the location of four known components of the basement-membrane region: type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin. Antibodies or antisera against these substances were localized by direct or indirect peroxidase methods on 60-microns thick slices of formaldehyde-fixed tissues. In the basement- membrane region of the duodenal epithelium, enamel-organ epithelium, and blood-vessel endothelium, immunostaining for all four components was observed in the basal lamina (also called lamina densa). The bulk of the lamina lucida (rara) was unstained, but it was traversed by narrow projections of the basal lamina that were immunostained for all four components. In the subbasement-membrane fibrous elements or reticular lamina, immunostaining was confined to occasional "bridges" extending from the epithelial basal-lamina to that of adjacent capillaries. The joint presence of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin in the basal lamina indicates that these substances do not occur in separate layers but are integrated into a common structure.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. Adamson E. D., Ayers S. E. The localization and synthesis of some collagen types in developing mouse embryos. Cell. 1979 Apr;16(4):953–965. doi: 10.1016/0092-8674(79)90110-7. [DOI] [PubMed] [Google Scholar]
  2. Avrameas S., Ternynck T. Peroxidase labelled antibody and Fab conjugates with enhanced intracellular penetration. Immunochemistry. 1971 Dec;8(12):1175–1179. doi: 10.1016/0019-2791(71)90395-8. [DOI] [PubMed] [Google Scholar]
  3. Boselli J. M., Macarak E. J., Clark C. C., Brownell A. G., Martinez-Hernandez A. Fibronectin: its relationship to basement membranes. I. Light microscopic studies. Coll Relat Res. 1981 Sep;1(5):391–404. doi: 10.1016/s0174-173x(81)80024-6. [DOI] [PubMed] [Google Scholar]
  4. Cohn R. H., Banerjee S. D., Bernfield M. R. Basal lamina of embryonic salivary epithelia. Nature of glycosaminoglycan and organization of extracellular materials. J Cell Biol. 1977 May;73(2):464–478. doi: 10.1083/jcb.73.2.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Courtoy P. J., Kanwar Y. S., Hynes R. O., Farquhar M. G. Fibronectin localization in the rat glomerulus. J Cell Biol. 1980 Dec;87(3 Pt 1):691–696. doi: 10.1083/jcb.87.3.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Foidart J. M., Bere E. W., Jr, Yaar M., Rennard S. I., Gullino M., Martin G. R., Katz S. I. Distribution and immunoelectron microscopic localization of laminin, a noncollagenous basement membrane glycoprotein. Lab Invest. 1980 Mar;42(3):336–342. [PubMed] [Google Scholar]
  7. Gordon J. R., Bernfield M. R. The basal lamina of the postnatal mammary epithelium contains glycosaminoglycans in a precise ultrastructural organization. Dev Biol. 1980 Jan;74(1):118–135. doi: 10.1016/0012-1606(80)90056-1. [DOI] [PubMed] [Google Scholar]
  8. Hassell J. R., Robey P. G., Barrach H. J., Wilczek J., Rennard S. I., Martin G. R. Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494–4498. doi: 10.1073/pnas.77.8.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hay E. D., Meier S. Glycosaminoglycan synthesis by embryonic inductors: neural tube, notochord, and lens. J Cell Biol. 1974 Sep;62(3):889–898. doi: 10.1083/jcb.62.3.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hogan B. L., Cooper A. R., Kurkinen M. Incorporation into Reichert's membrane of laminin-like extracellular proteins synthesized by parietal endoderm cells of the mouse embryo. Dev Biol. 1980 Dec;80(2):289–300. doi: 10.1016/0012-1606(80)90405-4. [DOI] [PubMed] [Google Scholar]
  11. Howe C. C., Solter D. Identification of noncollagenous basement membrane glycopolypeptides synthesized by mouse parietal entoderm and an entodermal cell line. Dev Biol. 1980 Jun 15;77(2):480–487. doi: 10.1016/0012-1606(80)90489-3. [DOI] [PubMed] [Google Scholar]
  12. Kanwar Y. S., Farquhar M. G. Anionic sites in the glomerular basement membrane. In vivo and in vitro localization to the laminae rarae by cationic probes. J Cell Biol. 1979 Apr;81(1):137–153. doi: 10.1083/jcb.81.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kanwar Y. S., Farquhar M. G. Presence of heparan sulfate in the glomerular basement membrane. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1303–1307. doi: 10.1073/pnas.76.3.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Karim A., Cournil I., Leblond C. P. Immunohistochemical localization of procollagens. II. Electron microscopic distribution of procollagen I antigenicity in the odontoblasts and predentin of rat incisor teeth by a direct method using peroxidase linked antibodies. J Histochem Cytochem. 1979 Jul;27(7):1070–1083. doi: 10.1177/27.7.89154. [DOI] [PubMed] [Google Scholar]
  15. Kefalides N. A., Alper R., Clark C. C. Biochemistry and metabolism of basement membranes. Int Rev Cytol. 1979;61:167–228. doi: 10.1016/s0074-7696(08)61998-1. [DOI] [PubMed] [Google Scholar]
  16. Laurie G. W., Leblond C. P., Cournil I., Martin G. R. Immunohistochemical evidence for the intracellular formation of basement membrane collagen (type IV) in developing tissues. J Histochem Cytochem. 1980 Dec;28(12):1267–1274. doi: 10.1177/28.12.6164715. [DOI] [PubMed] [Google Scholar]
  17. Laurie G. W., Leblond C. P., Martin G. R. Intracellular localization of basement membrane precursors in the endodermal cells of the rat parietal yolk sac. II. Immunostaining for type IV collagen and its precursors. J Histochem Cytochem. 1982 Oct;30(10):983–990. doi: 10.1177/30.10.6752264. [DOI] [PubMed] [Google Scholar]
  18. Laurie G. W., Leblond C. P., Martin G. R., Silver M. H. Intracellular localization of basement membrane precursors in the endodermal cells of the rat parietal yolk sac. III. Immunostaining for laminin and its precursors. J Histochem Cytochem. 1982 Oct;30(10):991–998. doi: 10.1177/30.10.6752265. [DOI] [PubMed] [Google Scholar]
  19. Madri J. A., Roll F. J., Furthmayr H., Foidart J. M. Ultrastructural localization of fibronectin and laminin in the basement membranes of the murine kidney. J Cell Biol. 1980 Aug;86(2):682–687. doi: 10.1083/jcb.86.2.682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Martinez-Hernandez A., Marsh C. A., Clark C. C., Macarak E. J., Brownell A. G. Fibronectin: its relationship to basement membranes. II. Ultrastructural studies in rat kidney. Coll Relat Res. 1981 Sep;1(5):405–418. doi: 10.1016/s0174-173x(81)80025-8. [DOI] [PubMed] [Google Scholar]
  21. Mayer B. W., Jr, Hay E. D., Hynes R. O. Immunocytochemical localization of fibronectin in embryonic chick trunk and area vasculosa. Dev Biol. 1981 Mar;82(2):267–286. doi: 10.1016/0012-1606(81)90451-6. [DOI] [PubMed] [Google Scholar]
  22. Moriarty G. C. Adenohypophysis: ultrastructural cytochemistry. A review. J Histochem Cytochem. 1973 Oct;21(10):855–894. doi: 10.1177/21.10.855. [DOI] [PubMed] [Google Scholar]
  23. Moriarty G. C., Moriarty C. M., Sternberger L. A. Ultrastructural immunocytochemistry with unlabeled antibodies and the peroxidase-antiperoxidase complex. A technique more sensitive than radioimmunoassay. J Histochem Cytochem. 1973 Sep;21(9):825–833. doi: 10.1177/21.9.825. [DOI] [PubMed] [Google Scholar]
  24. Paiement J., Leblond C. P. Localization of thyroiglobulin antigenicity in rat thyroid sections using antibodies labeled with peroxidase or 125I-radioiodine. J Cell Biol. 1977 Sep;74(3):992–1015. doi: 10.1083/jcb.74.3.992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rennard S. I., Berg R., Martin G. R., Foidart J. M., Robey P. G. Enzyme-linked immunoassay (ELISA) for connective tissue components. Anal Biochem. 1980 May 1;104(1):205–214. doi: 10.1016/0003-2697(80)90300-0. [DOI] [PubMed] [Google Scholar]
  26. Rennard S. I., Church R. L., Rohrbach D. H., Shupp D. E., Abe S., Hewitt A. T., Murray J. C., Martin G. R. Localization of the human fibronectin (FN) gene on chromosome 8 by a specific enzyme immunoassay. Biochem Genet. 1981 Jun;19(5-6):551–566. doi: 10.1007/BF00484626. [DOI] [PubMed] [Google Scholar]
  27. Roll F. J., Madri J. A., Albert J., Furthmayr H. Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney. an immunoferritin study of ultrathin frozen sections. J Cell Biol. 1980 Jun;85(3):597–616. doi: 10.1083/jcb.85.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ruoslahti E., Engvall E., Hayman E. G. Fibronectin: current concepts of its structure and functions. Coll Relat Res. 1981;1(1):95–128. doi: 10.1016/s0174-173x(80)80011-2. [DOI] [PubMed] [Google Scholar]
  29. Sakashita S., Engvall E., Ruoslahti E. Basement membrane glycoprotein laminin binds to heparin. FEBS Lett. 1980 Jul 28;116(2):243–246. doi: 10.1016/0014-5793(80)80654-5. [DOI] [PubMed] [Google Scholar]
  30. Sanes J. R. Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol. 1982 May;93(2):442–451. doi: 10.1083/jcb.93.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Seligman A. M., Karnovsky M. J., Wasserkrug H. L., Hanker J. S. Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB). J Cell Biol. 1968 Jul;38(1):1–14. doi: 10.1083/jcb.38.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith K. K., Strickland S. Structural components and characteristics of Reichert's membrane, an extra-embryonic basement membrane. J Biol Chem. 1981 May 10;256(9):4654–4661. [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. 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]
  36. Trelstad R. L., Hayashi K., Toole B. P. Epithelial collagens and glycosaminoglycans in the embryonic cornea. Macromolecular order and morphogenesis in the basement membrane. J Cell Biol. 1974 Sep;62(3):815–830. doi: 10.1083/jcb.62.3.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tryggvason K., Robey P. G., Martin G. R. Biosynthesis of type IV procollagens. Biochemistry. 1980 Apr 1;19(7):1284–1289. doi: 10.1021/bi00548a003. [DOI] [PubMed] [Google Scholar]
  38. Weiss M. A., Ooi B. S., Ooi Y. M., Engvall E., Ruoslahti E. Immunofluorescent localization of fibronectin in the human kidney. Lab Invest. 1979 Oct;41(4):340–347. [PubMed] [Google Scholar]
  39. Yaoita H., Foidart J. M., Katz S. I. Localization of the collagenous component in skin basement membrane. J Invest Dermatol. 1978 Apr;70(4):191–193. doi: 10.1111/1523-1747.ep12541313. [DOI] [PubMed] [Google Scholar]

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

RESOURCES