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. 1981 Sep;78(9):5371–5375. doi: 10.1073/pnas.78.9.5371

Cell-surface heparan sulfate: an intercalated membrane proteoglycan.

L Kjellén, I Pettersson, M Höök
PMCID: PMC348747  PMID: 6458040

Abstract

Two pools of heparan sulfate proteoglycans have been selectively solubilized from rat liver plasma membranes by successive incubations with heparin and detergent. The two populations of proteoglycans have similar polyanionic properties as indicated by identical elution positions on ion-exchange chromatography on DEAE-Sephacel but differ in buoyant density in CsCl when analyzed by density gradient centrifugation in the presence of 4 M guanidine. The detergent-extracted proteoglycan has a lower buoyant density (less than or equal to 1.40 g/ml) and is, as determined by gel chromatography, slightly larger than the heparin-released proteoglycan (buoyant density, greater than or equal to 1.55 g/ml). Furthermore, in contrast to the heparin-released proteoglycan, the detergent-extracted proteoglycan is able to bind detergent micelles, shows affinity for the hydrophobic gel octyl-Sepharose, and can be inserted into liposomes. We conclude that the detergent-extracted heparan sulfate represents a proteoglycan species that has its core protein rooted in the lipid bilayer of the plasma membrane.

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Selected References

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  1. Brunner J., Hauser H., Semenza G. Single bilayer lipid-protein vesicles formed from phosphatidylcholine and small intestinal sucrase.isomaltase. J Biol Chem. 1978 Oct 25;253(20):7538–7546. [PubMed] [Google Scholar]
  2. Cássaro C. M., Dietrich C. P. Distribution of sulfated mucopolysaccharides in invertebrates. J Biol Chem. 1977 Apr 10;252(7):2254–2261. [PubMed] [Google Scholar]
  3. Dietrich C. P., Sampaio L. O., Toledo O. M. Characteristic distribution of sulfated mucopolysaccharides in different tissues and in their respective mitochondria. Biochem Biophys Res Commun. 1976 Jul 12;71(1):1–10. doi: 10.1016/0006-291x(76)90241-2. [DOI] [PubMed] [Google Scholar]
  4. Glimelius B., Busch C., Hök M. Binding of heparin on the surface of cultured human endothelial cells. Thromb Res. 1978 May;12(5):773–782. doi: 10.1016/0049-3848(78)90271-2. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Hedman K., Kurkinen M., Alitalo K., Vaheri A., Johansson S., Hök M. Isolation of the pericellular matrix of human fibroblast cultures. J Cell Biol. 1979 Apr;81(1):83–91. doi: 10.1083/jcb.81.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Helenius A., Simons K. Solubilization of membranes by detergents. Biochim Biophys Acta. 1975 Mar 25;415(1):29–79. doi: 10.1016/0304-4157(75)90016-7. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Kjellén L., Oldberg A., Hök M. Cell-surface heparan sulfate. Mechanisms of proteoglycan-cell association. J Biol Chem. 1980 Nov 10;255(21):10407–10413. [PubMed] [Google Scholar]
  10. Kjellén L., Oldberg A., Rubin K., Hök M. Binding of heparin and heparan sulphate to rat liver cells. Biochem Biophys Res Commun. 1977 Jan 10;74(1):126–133. doi: 10.1016/0006-291x(77)91384-5. [DOI] [PubMed] [Google Scholar]
  11. Kraemer P. M. Heparin releases heparan sulfate from the cell surface. Biochem Biophys Res Commun. 1977 Oct 24;78(4):1334–1340. doi: 10.1016/0006-291x(77)91438-3. [DOI] [PubMed] [Google Scholar]
  12. Kraemer P. M. Production of heparin related glycosaminoglycans by an extablished mammalian cell line. J Cell Physiol. 1968 Apr;71(2):109–120. doi: 10.1002/jcp.1040710202. [DOI] [PubMed] [Google Scholar]
  13. LINDAHL U., CIFONELLI J. A., LINDAHL B., RODEN L. THE ROLE OF SERINE IN THE LINKAGE OF HEPARIN TO PROTEIN. J Biol Chem. 1965 Jul;240:2817–2820. [PubMed] [Google Scholar]
  14. 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]
  15. Mutoh S., Funakoshi I., Ui N., Yamashina I. Structural characterization of proteoheparan sulfate isolated from plasma membranes of an ascites hepatoma, AH 66. Arch Biochem Biophys. 1980 Jun;202(1):137–143. doi: 10.1016/0003-9861(80)90415-4. [DOI] [PubMed] [Google Scholar]
  16. Ohnishi T., Ohshima E., Ohtsuka M. Effect of liver cell coat acid mucopolysaccharide on the appearance of density-dependent inhibition in hepatoma cell growth. Exp Cell Res. 1975 Jun;93(1):136–142. doi: 10.1016/0014-4827(75)90432-2. [DOI] [PubMed] [Google Scholar]
  17. Oldberg A., Hök M., Obrink B., Pertoft H., Rubin K. Structure and metabolism of rat liver heparan sulphate. Biochem J. 1977 Apr 15;164(1):75–81. doi: 10.1042/bj1640075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ray T. K. A modified method for the isolation of the plasma membrane from rat liver. Biochim Biophys Acta. 1970 Jan 6;196(1):1–9. doi: 10.1016/0005-2736(70)90159-8. [DOI] [PubMed] [Google Scholar]
  19. Rollins B. J., Culp L. A. Glycosaminoglycans in the substrate adhesion sites of normal and virus-transformed murine cells. Biochemistry. 1979 Jan 9;18(1):141–148. doi: 10.1021/bi00568a022. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Shively J. E., Conrad H. E. Formation of anhydrosugars in the chemical depolymerization of heparin. Biochemistry. 1976 Sep 7;15(18):3932–3942. doi: 10.1021/bi00663a005. [DOI] [PubMed] [Google Scholar]
  22. Toledo O. M., Dietrich C. P. Tissue specific distribution of sulfated mucopolysaccharides in mammals. Biochim Biophys Acta. 1977 Jun 23;498(1):114–122. doi: 10.1016/0304-4165(77)90092-7. [DOI] [PubMed] [Google Scholar]
  23. Underhill C. B., Keller J. M. Heparan sulfates of mouse cells. Analysis of parent and transformed 3T3 cell lines. J Cell Physiol. 1977 Jan;90(1):53–59. doi: 10.1002/jcp.1040900108. [DOI] [PubMed] [Google Scholar]
  24. Vogel K. G., Dolde J. Cell-surface glycosaminoglycans are not released from human diploid fibroblasts by non-enzymatic methods. Biochim Biophys Acta. 1979 Mar 23;552(1):194–200. doi: 10.1016/0005-2736(79)90259-1. [DOI] [PubMed] [Google Scholar]
  25. Winterbourne D. J., Mora P. T. Altered metabolism of heparan sulfate in simian virus 40 transformed cloned mouse cells. J Biol Chem. 1978 Jul 25;253(14):5109–5120. [PubMed] [Google Scholar]
  26. Wisher M. H., Evans W. H. Functional polarity of the rat hepatocyte surface membrane. Isolation and characterization of plasma-membrane subfractions from the blood-sinusoidal, bile-Canalicular and contiguous surfaces of the hepatocyte. Biochem J. 1975 Feb;146(2):375–388. doi: 10.1042/bj1460375. [DOI] [PMC free article] [PubMed] [Google Scholar]

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