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. 1980 Jun 1;85(3):597–616. doi: 10.1083/jcb.85.3.597

Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney. an immunoferritin study of ultrathin frozen sections

PMCID: PMC2111464  PMID: 6993495

Abstract

Affinity-purified rabbit antibodies specific for collagen types I, III, AB2 and for a partially characterized type IV collagen derived from a murine tumor were used to study the distribution of collagens in the normal mouse kidney. Immunofluorescence staining of conventional frozen sections demonstrated that types I and III were present in bundles around large vessels and in fibers surrounding glomeruli and tubules, whereas types IV and AB2 were distributed in a linear fashion along basement membranes of tubules, glomeruli, and Bowman's capsule and in the mesangial stalk. The distribution of types IV nd AB2 was examined at the ultrastructural level by staining of 600- to 800-A thick frozen sections with a three-stage procedure employing specific collagen antibodies, biotinyl sheep antirabbit IgG, and avidin-ferritin conjugates. Labeling by this procedure demonstrated codistribution of types AB2 and the putative type IV in all three basement membranes. In addition, mesangial matrix was shown to contain both of these collagen types. These results support recent biochemical evidence of collagen heterogeneity in basement membranes, and also support the concept of a structural relationship between mesangial matrix and glomerular basement membranes.

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Selected References

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  1. Bailey A. J., Sims T. J., Duance V. C., Light N. D. Partial characterization of a second basement membrane collagen in human placenta. Evidence for the existence of two type IV collagen molecules. FEBS Lett. 1979 Mar 15;99(2):361–366. doi: 10.1016/0014-5793(79)80992-8. [DOI] [PubMed] [Google Scholar]
  2. Becker J. M., Wilchek M. Inactivation by avidin of biotin-modified bacteriophage. Biochim Biophys Acta. 1972 Mar 30;264(1):165–170. doi: 10.1016/0304-4165(72)90127-4. [DOI] [PubMed] [Google Scholar]
  3. Beil W., Furthmayr H., Timpl R. Chicken antibodies to soluble rat collagen. I. Characterization of the immune response by precipitation and agglutination methods. Immunochemistry. 1972 Aug;9(8):779–788. [PubMed] [Google Scholar]
  4. Benya P. D., Padilla S. R., Nimni M. E. The progeny of rabbit articular chondrocytes synthesize collagen types I and III and type I trimer, but not type II. Verifications by cyanogen bromide peptide analysis. Biochemistry. 1977 Mar 8;16(5):865–872. doi: 10.1021/bi00624a009. [DOI] [PubMed] [Google Scholar]
  5. Burgeson R. E., El Adli F. A., Kaitila I. I., Hollister D. W. Fetal membrane collagens: identification of two new collagen alpha chains. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2579–2583. doi: 10.1073/pnas.73.8.2579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chung E., Rhodes K., Miller E. J. Isolation of three collagenous components of probable basement membrane origin from several tissues. Biochem Biophys Res Commun. 1976 Aug 23;71(4):1167–1174. doi: 10.1016/0006-291x(76)90776-2. [DOI] [PubMed] [Google Scholar]
  7. Cohen M. P., Klein C. V. Evidence for heterogeneous origin of glomerular basement membrane. Biochem Biophys Res Commun. 1977 Aug 22;77(4):1326–1332. doi: 10.1016/s0006-291x(77)80124-1. [DOI] [PubMed] [Google Scholar]
  8. Cotmore S. F., Furthmayr H., Marchesi V. T. Immunochemical evidence for the transmembrane orientation of glycophorin A. Localization of ferritin-antibody conjugates in intact cells. J Mol Biol. 1977 Jul 5;113(3):539–553. doi: 10.1016/0022-2836(77)90237-6. [DOI] [PubMed] [Google Scholar]
  9. Crouch E., Bornstein P. Characterization of a type IV procollagen synthesized by human amniotic fluid cells in culture. J Biol Chem. 1979 May 25;254(10):4197–4204. [PubMed] [Google Scholar]
  10. Daniels J. R., Chu G. H. Basement membrane collagen of renal glomerulus. J Biol Chem. 1975 May 10;250(9):3531–3537. [PubMed] [Google Scholar]
  11. Glanville R. W., Rauter A., Fietzek P. P. Isolation and characterization of a native placental basement-membrane collagen and its component alpha chains. Eur J Biochem. 1979 Apr 2;95(2):383–389. doi: 10.1111/j.1432-1033.1979.tb12976.x. [DOI] [PubMed] [Google Scholar]
  12. Hauschka S. D., Konigsberg I. R. The influence of collagen on the development of muscle clones. Proc Natl Acad Sci U S A. 1966 Jan;55(1):119–126. doi: 10.1073/pnas.55.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hay E. D., Meier S. Stimulation of corneal differentiation by interaction between cell surface and extracellular matrix. II. Further studies on the nature and site of transfilter "induction". Dev Biol. 1976 Aug;52(1):141–157. doi: 10.1016/0012-1606(76)90014-2. [DOI] [PubMed] [Google Scholar]
  14. Heitzmann H., Richards F. M. Use of the avidin-biotin complex for specific staining of biological membranes in electron microscopy. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3537–3541. doi: 10.1073/pnas.71.9.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hong B. S., Davison P. F., Cannon D. J. Isolation and characterization of a distinct type of collagen from bovine fetal membranes and other tissues. Biochemistry. 1979 Oct 2;18(20):4278–4282. doi: 10.1021/bi00587a003. [DOI] [PubMed] [Google Scholar]
  16. Kefalides N. A. Chemical properties of basement membranes. Int Rev Exp Pathol. 1971;10:1–39. [PubMed] [Google Scholar]
  17. Kefalides N. A. Isolation and characterization of the collagen from glomerular basement membrane. Biochemistry. 1968 Sep;7(9):3103–3112. doi: 10.1021/bi00849a012. [DOI] [PubMed] [Google Scholar]
  18. Kefalides N. A. Structure and biosynthesis of basement membranes. Int Rev Connect Tissue Res. 1973;6:63–104. doi: 10.1016/b978-0-12-363706-2.50008-8. [DOI] [PubMed] [Google Scholar]
  19. Kraehenbuhl J. P., Jamieson J. D. Localization of intracellular antigens by immunoelectron microscopy. Int Rev Exp Pathol. 1974;13(0):1–53. [PubMed] [Google Scholar]
  20. Kresina T. F., Miller E. J. Isolation and characterization of basement membrane collagen from human placental tissue. Evidence for the presence of two genetically distinct collagen chains. Biochemistry. 1979 Jul 10;18(14):3089–3097. doi: 10.1021/bi00581a028. [DOI] [PubMed] [Google Scholar]
  21. Madri J. A., Furthmayr H. Isolation and tissue localization of type AB2 collagen from normal lung parenchyma. Am J Pathol. 1979 Feb;94(2):323–331. [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Orkin R. W., Gehron P., McGoodwin E. B., Martin G. R., Valentine T., Swarm R. A murine tumor producing a matrix of basement membrane. J Exp Med. 1977 Jan 1;145(1):204–220. doi: 10.1084/jem.145.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Painter R. G., Tokuyasu K. T., Singer S. J. Immunoferritin localization of intracellular antigens: the use of ultracryotomy to obtain ultrathin sections suitable for direct immunoferritin staining. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1649–1653. doi: 10.1073/pnas.70.6.1649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Peterkofsky B., Diegelmann R. Use of a mixture of proteinase-free collagenases for the specific assay of radioactive collagen in the presence of other proteins. Biochemistry. 1971 Mar 16;10(6):988–994. doi: 10.1021/bi00782a009. [DOI] [PubMed] [Google Scholar]
  26. Rhodes R. K., Miller E. J. Physicochemical characterization and molecular organization of the collagen A and B chains. Biochemistry. 1978 Aug 22;17(17):3442–3448. doi: 10.1021/bi00610a003. [DOI] [PubMed] [Google Scholar]
  27. Roll F. J., Madri J. A., Furthmayr H. A new method of iodinating collagens for use in radioimmunoassay. Anal Biochem. 1979 Jul 15;96(2):489–499. doi: 10.1016/0003-2697(79)90611-0. [DOI] [PubMed] [Google Scholar]
  28. Rowe D. W., McGoodwin E. B., Martin G. R., Sussman M. D., Grahn D., Faris B., Franzblau C. A sex-linked defect in the cross-linking of collagen and elastin associated with the mottled locus in mice. J Exp Med. 1974 Jan 1;139(1):180–192. doi: 10.1084/jem.139.1.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sage H., Woodbury R. G., Bornstein P. Structural studies on human type IV collagen. J Biol Chem. 1979 Oct 10;254(19):9893–9900. [PubMed] [Google Scholar]
  30. Shotton D. M., Burke B. E., Branton D. The molecular structure of human erythrocyte spectrin. Biophysical and electron microscopic studies. J Mol Biol. 1979 Jun 25;131(2):303–329. doi: 10.1016/0022-2836(79)90078-0. [DOI] [PubMed] [Google Scholar]
  31. Stenn K. S., Madri J. A., Roll F. J. Migrating epidermis produces AB2 collagen and requires continual collagen synthesis for movement. Nature. 1979 Jan 18;277(5693):229–232. doi: 10.1038/277229a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Timpl R., Glanville R. W., Wick G., Martin G. R. Immunochemical study on basement membrane (type IV) collagens. Immunology. 1979 Sep;38(1):109–116. [PMC free article] [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. Tokuyasu K. T. A study of positive staining of ultrathin frozen sections. J Ultrastruct Res. 1978 Jun;63(3):287–307. doi: 10.1016/s0022-5320(78)80053-7. [DOI] [PubMed] [Google Scholar]
  37. Tokuyasu K. T., Singer S. J. Improved procedures for immunoferritin labeling of ultrathin frozen sections. J Cell Biol. 1976 Dec;71(3):894–906. doi: 10.1083/jcb.71.3.894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Trelstad R. L., Lawley K. R. Isolation and initial characterization of human basement membrane collagens. Biochem Biophys Res Commun. 1976 May 23;76(2):376–384. doi: 10.1016/0006-291x(77)90735-5. [DOI] [PubMed] [Google Scholar]
  39. Tryggvason K., Kivirikko K. I. Heterogeneity of pepsin-solubilized human glomerular basement membrane collagen. Nephron. 1978;21(4):230–235. doi: 10.1159/000181397. [DOI] [PubMed] [Google Scholar]
  40. Wells A. F., Miller C. E., Nadel M. K. Rapid fluorescein and protein assay method for fluorescent-antibody conjugates. Appl Microbiol. 1966 Mar;14(2):271–275. doi: 10.1128/am.14.2.271-275.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wick G., Furthmayr H., Timpl R. Purified antibodies to collagen: an immunofluorescence study of their reaction with tissue collagen. Int Arch Allergy Appl Immunol. 1975;48(5):664–679. doi: 10.1159/000231354. [DOI] [PubMed] [Google Scholar]
  42. Wick G., Kraft D., Kokschka E. M., Timpl R. Defined immunofluorescence studies of anticollagen sera. Ann N Y Acad Sci. 1975 Jun 30;254:614–617. doi: 10.1111/j.1749-6632.1975.tb29208.x. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Ziparo E., Lemay A., Marchesi V. T. The distribution of spectrin along the membranes of normal and echinocytic human erythrocytes. J Cell Sci. 1978 Dec;34:91–101. doi: 10.1242/jcs.34.1.91. [DOI] [PubMed] [Google Scholar]

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