Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1979 Jun 1;149(6):1450–1459. doi: 10.1084/jem.149.6.1450

Basal lamina heterogeneity in the glomerular capillary tufts of human kidneys

TW Huang
PMCID: PMC2184889  PMID: 376776

Abstract

Two classes of glomerular basal laminas are identified with a newly developed guanidine technique. The electron-opaque epithelial basal lamina is the most prominent element of the glomerular basal lamina scaffold. It is a continuous layer within each glomerulus, folding into capillary tufts and loops, but never completely encircling the entire circumference of each capillary, similar to the serosa covering the intestinal loop and mesentery. The vascular space so defined is further partitioned into individual capillary lumen by an electron-lucent mesangial basal lamina, that forms a meshwork continuous with the vascular pole of the glomerulus and extends peripherally to surround capillary lumens. The latter, designated endothelial basal lamina, is extremely attenuated and appears as a vestigial structure in glomerular capillary loops. Changes in juxtamesangial epithelial basal lamina indicate that it may be the site of the bulk removal and renewal of the epithelial basal lamina. The unique epithelial origin of glomerular capillary basal lamina and its organization provide a structural basis for understanding the glomerular physiology gained by various tracer studies. The results also suggest that the guanidine technique may be a useful new approach to the analysis of basal lamina alterations in various glomerular diseases.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

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

  1. CRUICKSHANK B., HILL A. G. The histochemical identification of a connective-tissue antigen in the rat. J Pathol Bacteriol. 1953 Jul;66(1):283–289. doi: 10.1002/path.1700660132. [DOI] [PubMed] [Google Scholar]
  2. Cattell V., Bradfield J. W. Focal mesangial proliferative glomerulonephritis in the rat caused by habu snake venom. A morphologic study. Am J Pathol. 1977 Jun;87(3):511–524. [PMC free article] [PubMed] [Google Scholar]
  3. Caulfield J. P., Farquhar M. G. The permeability of glomerular capillaries to graded dextrans. Identification of the basement membrane as the primary filtration barrier. J Cell Biol. 1974 Dec;63(3):883–903. doi: 10.1083/jcb.63.3.883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Elema J. D., Hoyer J. R., Vernier R. L. The glomerular mesangium: uptake and transport of intravenously injected colloidal carbon in rats. Kidney Int. 1976 May;9(5):395–406. doi: 10.1038/ki.1976.49. [DOI] [PubMed] [Google Scholar]
  6. FARQUHAR M. G., WISSIG S. L., PALADE G. E. Glomerular permeability. I. Ferritin transfer across the normal glomerular capillary wall. J Exp Med. 1961 Jan 1;113:47–66. doi: 10.1084/jem.113.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Grant M. E., Harwood R., Williams I. F. The biosynthesis of basement-membrane collagen by isolated rat glomeruli. Eur J Biochem. 1975 Jun;54(2):531–540. doi: 10.1111/j.1432-1033.1975.tb04166.x. [DOI] [PubMed] [Google Scholar]
  8. Grant M. E., Kefalides N. A., Prockop D. J. The biosynthesis of basement membrane collagen in embryonic chick lens. I. Delay between the synthesis of polypeptide chains and the secretion of collagen by matrix-free cells. J Biol Chem. 1972 Jun 10;247(11):3539–3544. [PubMed] [Google Scholar]
  9. Howard B. V., Macarak E. J., Gunson D., Kefalides N. A. Characterization of the collagen synthesized by endothelial cells in culture. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2361–2364. doi: 10.1073/pnas.73.7.2361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huang T. W. Composite epithelial and endothelial basal laminas in human lungs. A structural basis for their separation and apposition in reaction to injury. Am J Pathol. 1978 Dec;93(3):681–692. [PMC free article] [PubMed] [Google Scholar]
  11. Huang T. W., Wiegenstein L. M. Mesangiolytic glomerulonephritis in an infant with immune deficiency and echovirus infection. Arch Pathol Lab Med. 1977 Mar;101(3):125–128. [PubMed] [Google Scholar]
  12. Kefalides N. A., Cameron J. D., Tomichek E. A., Yanoff M. Biosynthesis of basement membrane collagen by rabbit corneal endothelium in vitro. J Biol Chem. 1976 Feb 10;251(3):730–733. [PubMed] [Google Scholar]
  13. 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]
  14. Leiper J. M., Thomson D., MacDonald M. K. Uptake and transport of Imposil by the glomerular mesangium in the mouse. Lab Invest. 1977 Nov;37(5):526–533. [PubMed] [Google Scholar]
  15. Mauer S. M., Fish A. J., Blau E. B., Michael A. F. The glomerular mesangium. I. Kinetic studies of macromolecular uptake in normal and nephrotic rats. J Clin Invest. 1972 May;51(5):1092–1101. doi: 10.1172/JCI106901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Michael A. F., Fish A. J., Good R. A. Glomerular localization and transport of aggregated proteins in mice. Lab Invest. 1967 Jul;17(1):14–29. [PubMed] [Google Scholar]
  17. PAK POY R. K. Electron microscopy of the mammalian renal glomerulus; the problems of intercapillary tissue and the capillary loop basement membrane. Am J Pathol. 1958 Sep-Oct;34(5):885–895. [PMC free article] [PubMed] [Google Scholar]
  18. PIERCE G. B., Jr, BEALS T. F., RAM J. S., MIDGLEY A. R., Jr BASEMENT MEMBRANES. IV. EPITHELIAL ORGIN AND IMMUNOLOGIC CROSS REACTIONS. Am J Pathol. 1964 Dec;45:929–961. [PMC free article] [PubMed] [Google Scholar]
  19. Price R. G., Spiro R. G. Studies on the metabolism of the renal glomerular basement membrane. Turnover measurements in the rat with the use of radiolabeled amino acids. J Biol Chem. 1977 Dec 10;252(23):8597–8602. [PubMed] [Google Scholar]
  20. Scheinman J. I., Fish A. J., Brown D. M., Michael A. J. Human glomerular smooth muscle (mesangial) cells in culture. Lab Invest. 1976 Feb;34(2):150–158. [PubMed] [Google Scholar]
  21. Simionescu N., Simionescu M., Palade G. E. Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J Cell Biol. 1972 May;53(2):365–392. doi: 10.1083/jcb.53.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Spiro R. G. Studies on the renal glomerular basement membrane. Preparation and chemical composition. J Biol Chem. 1967 Apr 25;242(8):1915–1922. [PubMed] [Google Scholar]
  23. Striker G. E., Smuckler E. A. An ultrastructural study of glomerular basement membrane synthesis. Am J Pathol. 1970 Mar;58(3):531–555. [PMC free article] [PubMed] [Google Scholar]
  24. Sulitzeanu D. Antigenic components of rat connective tissue. Br J Exp Pathol. 1965 Oct;46(5):481–488. [PMC free article] [PubMed] [Google Scholar]
  25. Suzuki Y., Churg J., Grishman E., Mautner W., Dachs S. The Mesangium of the Renal Glomerulus: Electron Microscopic Studies of Pathologic Alterations. Am J Pathol. 1963 Oct;43(4):555–578. [PMC free article] [PubMed] [Google Scholar]
  26. Tanzer M. L., Kefalides N. A. Collagen crosslinks: occurrence in basement membrane collagens. Biochem Biophys Res Commun. 1973 Apr 2;51(3):775–780. doi: 10.1016/0006-291x(73)91382-x. [DOI] [PubMed] [Google Scholar]
  27. Thorning D., Vracko R. Renal glomerular basal lamina scaffold: embryologic development, anatomy, and role in cellular reconstruction of rat glomeruli injured by freezing and thawing. Lab Invest. 1977 Jul;37(1):105–119. [PubMed] [Google Scholar]
  28. 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]
  29. VERNIER R. L., BIRCH-ANDERSEN A. Studies of the human fetal kidney. I. Development of the glomerulus. J Pediatr. 1962 May;60:754–768. doi: 10.1016/s0022-3476(62)80103-6. [DOI] [PubMed] [Google Scholar]
  30. Vogt A., Bockhorn H., Kozima K., Sasaki M. Electron microscopic localization of the nephrotoxic antibody in the glomeruli of the rat after intravenous application of purified nephritogenic antibody-ferritin conjugates. J Exp Med. 1968 May 1;127(5):867–878. doi: 10.1084/jem.127.5.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES