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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Aug;77(8):4494–4498. doi: 10.1073/pnas.77.8.4494

Isolation of a heparan sulfate-containing proteoglycan from basement membrane.

J R Hassell, P G Robey, H J Barrach, J Wilczek, S I Rennard, G R Martin
PMCID: PMC349870  PMID: 6449008

Abstract

We have isolated a unique, basement membrane proteoglycan from the Engelbreth-Holm-Swarm (EHS) sarcoma. This proteoglycan, estimated to be 0.75 X 10(6) daltons, was found to contain about equal amounts of protein and covalently linked heparan sulfate. Antibody prepared against this proteoglycan reacts with the basement membrane matrix in the tumor and with the basement membranes in skin, kidney, and cornea. These studies indicate that the heparan sulfate proteoglycan is a normal constituent of basement membranes that presumably plays an important role in the organization of basement membrane components and that also may determine the permeability of basement membranes to acidic molecules.

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Selected References

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  1. BITTER T., MUIR H. M. A modified uronic acid carbazole reaction. Anal Biochem. 1962 Oct;4:330–334. doi: 10.1016/0003-2697(62)90095-7. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Bernfield M. R., Wessells N. K. Intra- and extracellular control of epithelial morphogenesis. Symp Soc Dev Biol. 1970;29:195–249. doi: 10.1016/b978-0-12-395534-0.50014-5. [DOI] [PubMed] [Google Scholar]
  4. Caulfield J. P., Farquhar M. G. Distribution of annionic sites in glomerular basement membranes: their possible role in filtration and attachment. Proc Natl Acad Sci U S A. 1976 May;73(5):1646–1650. doi: 10.1073/pnas.73.5.1646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caulfield J. P., Farquhar M. G. Loss of anionic sites from the glomerular basement membrane in aminonucleoside nephrosis. Lab Invest. 1978 Nov;39(5):505–512. [PubMed] [Google Scholar]
  6. DAVIDSON E. A., MEYER K. Chondroitin, a new mucopolysaccharide. J Biol Chem. 1954 Dec;211(2):605–611. [PubMed] [Google Scholar]
  7. 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]
  8. GOODMAN M., GREENSPON S. A., KRAKOWER C. A. The antigenic composition of the various anatomic structures of the canine kidney. J Immunol. 1955 Aug;75(2):96–104. [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Hascall V. C., Sajdera S. W. Physical properties and polydispersity of proteoglycan from bovine nasal cartilage. J Biol Chem. 1970 Oct 10;245(19):4920–4930. [PubMed] [Google Scholar]
  12. Hassell J. R., Newsome D. A., Hascall V. C. Characterization and biosynthesis of proteoglycans of corneal stroma from rhesus monkey. J Biol Chem. 1979 Dec 25;254(24):12346–12354. [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Kanwar Y. S., Farquhar M. G. Isolation of glycosaminoglycans (heparan sulfate) from glomerular basement membranes. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4493–4497. doi: 10.1073/pnas.76.9.4493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. LEBLOND C. P., GLEGG R. E., EIDINGER D. Presence of carbohydrates with free 1,2-glycol groups in sites stained by the periodic acid-Schiff technique. J Histochem Cytochem. 1957 Sep;5(5):445–458. doi: 10.1177/5.5.445. [DOI] [PubMed] [Google Scholar]
  19. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Linder E., Vaheri A., Ruoslahti E., Wartiovaara J. Distribution of fibroblast surface antigen in the developing chick embryo. J Exp Med. 1975 Jul 1;142(1):41–49. doi: 10.1084/jem.142.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MEYER K., LINKER A., DAVIDSON E. A., WEISSMANN B. The mucopolysaccharides of bovine cornea. J Biol Chem. 1953 Dec;205(2):611–616. [PubMed] [Google Scholar]
  23. McMANUS J. F. A. The periodic acid routing applied to the kidney. Am J Pathol. 1948 May;24(3):643–653. [PMC free article] [PubMed] [Google Scholar]
  24. Oegema T. R., Jr, Hascall V. C., Dziewiatkowski D. D. Isolation and characterization of proteoglycans from the swarm rat chondrosarcoma. J Biol Chem. 1975 Aug 10;250(15):6151–6159. [PubMed] [Google Scholar]
  25. Oldberg A., Kjellén L., Hök M. Cell-surface heparan sulfate. Isolation and characterization of a proteoglycan from rat liver membranes. J Biol Chem. 1979 Sep 10;254(17):8505–8510. [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Saito H., Yamagata T., Suzuki S. Enzymatic methods for the determination of small quantities of isomeric chondroitin sulfates. J Biol Chem. 1968 Apr 10;243(7):1536–1542. [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. 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]
  32. Wasteson A. A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulphate. J Chromatogr. 1971 Jul 8;59(1):87–97. doi: 10.1016/s0021-9673(01)80009-1. [DOI] [PubMed] [Google Scholar]
  33. 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]

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