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. 1995 Feb;146(2):520–529.

Source of peritoneal proteoglycans. Human peritoneal mesothelial cells synthesize and secrete mainly small dermatan sulfate proteoglycans.

S Yung 1, G J Thomas 1, E Stylianou 1, J D Williams 1, G A Coles 1, M Davies 1
PMCID: PMC1869848  PMID: 7856761

Abstract

This study describes experiments that compare the proteoglycans (PGs) extracted from the dialysate from patients receiving continuous peritoneal ambulatory dialysis (CAPD) with those secreted by metabolically labeled human peritoneal mesothelial cells in vitro. The PGs isolated from both sources were predominantly small chondroitin sulfate/dermatan sulfate PGs. Western blot of the core proteins obtained after chondroitin ABC lyase treatment with specific antibodies identified decorin and biglycan. With [35S]sulfate and [35S]methionine as labeling precursors it was shown that dermatan sulfate rather than chondroitin sulfate were the major glycosaminoglycan chains and that decorin was the predominant species. These data provide the first evidence that human peritoneal mesothelial cells may be the principal source of PGs in the peritoneum. Given the proposed functions of decorin and biglycan, the results suggest that these PGs may be involved in the control of transforming growth factor-beta activity and collagen fibril formation in the peritoneum.

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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. Border W. A., Noble N. A., Yamamoto T., Tomooka S., Kagami S. Antagonists of transforming growth factor-beta: a novel approach to treatment of glomerulonephritis and prevention of glomerulosclerosis. Kidney Int. 1992 Mar;41(3):566–570. doi: 10.1038/ki.1992.83. [DOI] [PubMed] [Google Scholar]
  3. Choi H. U., Johnson T. L., Pal S., Tang L. H., Rosenberg L., Neame P. J. Characterization of the dermatan sulfate proteoglycans, DS-PGI and DS-PGII, from bovine articular cartilage and skin isolated by octyl-sepharose chromatography. J Biol Chem. 1989 Feb 15;264(5):2876–2884. [PubMed] [Google Scholar]
  4. Coene M. C., Van Hove C., Claeys M., Herman A. G. Arachidonic acid metabolism by cultured mesothelial cells. Different transformations of exogenously added and endogenously. Biochim Biophys Acta. 1982 Mar 12;710(3):437–445. doi: 10.1016/0005-2760(82)90127-8. [DOI] [PubMed] [Google Scholar]
  5. Danielson K. G., Fazzio A., Cohen I., Cannizzaro L. A., Eichstetter I., Iozzo R. V. The human decorin gene: intron-exon organization, discovery of two alternatively spliced exons in the 5' untranslated region, and mapping of the gene to chromosome 12q23. Genomics. 1993 Jan;15(1):146–160. doi: 10.1006/geno.1993.1022. [DOI] [PubMed] [Google Scholar]
  6. Davies M., Stylianou E., Yung S., Thomas G. J., Coles G. A., Williams J. D. Proteoglycans of CAPD-dialysate fluid and mesothelium. Contrib Nephrol. 1990;85:134–141. doi: 10.1159/000419073. [DOI] [PubMed] [Google Scholar]
  7. Day A. A., McQuillan C. I., Termine J. D., Young M. R. Molecular cloning and sequence analysis of the cDNA for small proteoglycan II of bovine bone. Biochem J. 1987 Dec 15;248(3):801–805. doi: 10.1042/bj2480801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Farndale R. W., Sayers C. A., Barrett A. J. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res. 1982;9(4):247–248. doi: 10.3109/03008208209160269. [DOI] [PubMed] [Google Scholar]
  9. Fisher L. W., Hawkins G. R., Tuross N., Termine J. D. Purification and partial characterization of small proteoglycans I and II, bone sialoproteins I and II, and osteonectin from the mineral compartment of developing human bone. J Biol Chem. 1987 Jul 15;262(20):9702–9708. [PubMed] [Google Scholar]
  10. Fisher L. W., Lindner W., Young M. F., Termine J. D. Synthetic peptide antisera: their production and use in the cloning of matrix proteins. Connect Tissue Res. 1989;21(1-4):43–50. doi: 10.3109/03008208909049994. [DOI] [PubMed] [Google Scholar]
  11. Fisher L. W., Termine J. D., Young M. F. Deduced protein sequence of bone small proteoglycan I (biglycan) shows homology with proteoglycan II (decorin) and several nonconnective tissue proteins in a variety of species. J Biol Chem. 1989 Mar 15;264(8):4571–4576. [PubMed] [Google Scholar]
  12. Fleischmajer R., Fisher L. W., MacDonald E. D., Jacobs L., Jr, Perlish J. S., Termine J. D. Decorin interacts with fibrillar collagen of embryonic and adult human skin. J Struct Biol. 1991 Feb;106(1):82–90. doi: 10.1016/1047-8477(91)90065-5. [DOI] [PubMed] [Google Scholar]
  13. Iozzo R. V. Proteoglycans: structure, function, and role in neoplasia. Lab Invest. 1985 Oct;53(4):373–396. [PubMed] [Google Scholar]
  14. Järveläinen H. T., Kinsella M. G., Wight T. N., Sandell L. J. Differential expression of small chondroitin/dermatan sulfate proteoglycans, PG-I/biglycan and PG-II/decorin, by vascular smooth muscle and endothelial cells in culture. J Biol Chem. 1991 Dec 5;266(34):23274–23281. [PubMed] [Google Scholar]
  15. Krusius T., Ruoslahti E. Primary structure of an extracellular matrix proteoglycan core protein deduced from cloned cDNA. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7683–7687. doi: 10.1073/pnas.83.20.7683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Ledbetter S. R., Tyree B., Hassell J. R., Horigan E. A. Identification of the precursor protein to basement membrane heparan sulfate proteoglycans. J Biol Chem. 1985 Jul 5;260(13):8106–8113. [PubMed] [Google Scholar]
  18. Lyon M., Gallagher J. T. Purification and partial characterization of the major cell-associated heparan sulphate proteoglycan of rat liver. Biochem J. 1991 Jan 15;273(Pt 2):415–422. doi: 10.1042/bj2730415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meyer D. H., Krull N., Dreher K. L., Gressner A. M. Biglycan and decorin gene expression in normal and fibrotic rat liver: cellular localization and regulatory factors. Hepatology. 1992 Jul;16(1):204–216. doi: 10.1002/hep.1840160131. [DOI] [PubMed] [Google Scholar]
  20. Neame P. J., Choi H. U., Rosenberg L. C. The primary structure of the core protein of the small, leucine-rich proteoglycan (PG I) from bovine articular cartilage. J Biol Chem. 1989 May 25;264(15):8653–8661. [PubMed] [Google Scholar]
  21. Nicholson L. J., Clarke J. M., Pittilo R. M., Machin S. J., Woolf N. The mesothelial cell as a non-thrombogenic surface. Thromb Haemost. 1984 Oct 31;52(2):102–104. [PubMed] [Google Scholar]
  22. Okuda S., Languino L. R., Ruoslahti E., Border W. A. Elevated expression of transforming growth factor-beta and proteoglycan production in experimental glomerulonephritis. Possible role in expansion of the mesangial extracellular matrix. J Clin Invest. 1990 Aug;86(2):453–462. doi: 10.1172/JCI114731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rauch U., Glössl J., Kresse H. Comparison of small proteoglycans from skin fibroblasts and vascular smooth-muscle cells. Biochem J. 1986 Sep 1;238(2):465–474. doi: 10.1042/bj2380465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rubin J., Herrera G. A., Collins D. An autopsy study of the peritoneal cavity from patients on continuous ambulatory peritoneal dialysis. Am J Kidney Dis. 1991 Jul;18(1):97–102. doi: 10.1016/s0272-6386(12)80297-6. [DOI] [PubMed] [Google Scholar]
  25. Schmidt G., Hausser H., Kresse H. Interaction of the small proteoglycan decorin with fibronectin. Involvement of the sequence NKISK of the core protein. Biochem J. 1991 Dec 1;280(Pt 2):411–414. doi: 10.1042/bj2800411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schmidt G., Robenek H., Harrach B., Glössl J., Nolte V., Hörmann H., Richter H., Kresse H. Interaction of small dermatan sulfate proteoglycan from fibroblasts with fibronectin. J Cell Biol. 1987 Jun;104(6):1683–1691. doi: 10.1083/jcb.104.6.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schwarz K., Breuer B., Kresse H. Biosynthesis and properties of a further member of the small chondroitin/dermatan sulfate proteoglycan family. J Biol Chem. 1990 Dec 15;265(35):22023–22028. [PubMed] [Google Scholar]
  28. Scott J. E. Proteoglycan-fibrillar collagen interactions. Biochem J. 1988 Jun 1;252(2):313–323. doi: 10.1042/bj2520313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Shively J. E., Conrad H. E. Nearest neighbor analysis of heparin: identification and quantitation of the products formed by selective depolymerization procedures. Biochemistry. 1976 Sep 7;15(18):3943–3950. doi: 10.1021/bi00663a006. [DOI] [PubMed] [Google Scholar]
  31. Staprans I., Piel C. F., Felts J. M. Analysis of selected plasma constituents in continuous ambulatory peritoneal dialysis effluent. Am J Kidney Dis. 1986 Jun;7(6):490–494. doi: 10.1016/s0272-6386(86)80190-1. [DOI] [PubMed] [Google Scholar]
  32. Steinhauer H. B., Schollmeyer P. Prostaglandin-mediated loss of proteins during peritonitis in continuous ambulatory peritoneal dialysis. Kidney Int. 1986 Feb;29(2):584–590. doi: 10.1038/ki.1986.38. [DOI] [PubMed] [Google Scholar]
  33. Stylianou E., Jenner L. A., Davies M., Coles G. A., Williams J. D. Isolation, culture and characterization of human peritoneal mesothelial cells. Kidney Int. 1990 Jun;37(6):1563–1570. doi: 10.1038/ki.1990.150. [DOI] [PubMed] [Google Scholar]
  34. Thomas G. J., Jenner L., Mason R. M., Davies M. Human glomerular epithelial cell proteoglycans. Arch Biochem Biophys. 1990 Apr;278(1):11–20. doi: 10.1016/0003-9861(90)90224-m. [DOI] [PubMed] [Google Scholar]
  35. Thomas G. J., Mason R. M., Davies M. Characterization of proteoglycans synthesized by human adult glomerular mesangial cells in culture. Biochem J. 1991 Jul 1;277(Pt 1):81–88. doi: 10.1042/bj2770081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Topley N., Brown Z., Jörres A., Westwick J., Davies M., Coles G. A., Williams J. D. Human peritoneal mesothelial cells synthesize interleukin-8. Synergistic induction by interleukin-1 beta and tumor necrosis factor-alpha. Am J Pathol. 1993 Jun;142(6):1876–1886. [PMC free article] [PubMed] [Google Scholar]
  37. Verger C., Luger A., Moore H. L., Nolph K. D. Acute changes in peritoneal morphology and transport properties with infectious peritonitis and mechanical injury. Kidney Int. 1983 Jun;23(6):823–831. doi: 10.1038/ki.1983.101. [DOI] [PubMed] [Google Scholar]
  38. Vogel K. G., Paulsson M., Heinegård D. Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem J. 1984 Nov 1;223(3):587–597. doi: 10.1042/bj2230587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vogel K. G., Trotter J. A. The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Coll Relat Res. 1987 Jun;7(2):105–114. doi: 10.1016/s0174-173x(87)80002-x. [DOI] [PubMed] [Google Scholar]
  40. Westergren-Thorsson G., Hernnäs J., Särnstrand B., Oldberg A., Heinegård D., Malmström A. Altered expression of small proteoglycans, collagen, and transforming growth factor-beta 1 in developing bleomycin-induced pulmonary fibrosis in rats. J Clin Invest. 1993 Aug;92(2):632–637. doi: 10.1172/JCI116631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Winnemöller M., Schmidt G., Kresse H. Influence of decorin on fibroblast adhesion to fibronectin. Eur J Cell Biol. 1991 Feb;54(1):10–17. [PubMed] [Google Scholar]
  42. Winnemöller M., Schön P., Vischer P., Kresse H. Interactions between thrombospondin and the small proteoglycan decorin: interference with cell attachment. Eur J Cell Biol. 1992 Oct;59(1):47–55. [PubMed] [Google Scholar]
  43. Woods A., Couchman J. R., Hök M. Heparan sulfate proteoglycans of rat embryo fibroblasts. A hydrophobic form may link cytoskeleton and matrix components. J Biol Chem. 1985 Sep 5;260(19):10872–10879. [PubMed] [Google Scholar]
  44. Yamagata T., Saito H., Habuchi O., Suzuki S. Purification and properties of bacterial chondroitinases and chondrosulfatases. J Biol Chem. 1968 Apr 10;243(7):1523–1535. [PubMed] [Google Scholar]
  45. Yamaguchi Y., Mann D. M., Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature. 1990 Jul 19;346(6281):281–284. doi: 10.1038/346281a0. [DOI] [PubMed] [Google Scholar]
  46. Yamamoto T., Nagase M., Hishida A., Honda N. Specific increases in urinary excretion of anti-DNA antibodies in lupus mice induced by lysozyme administration: further evidence for DNA-anti-DNA immune complexes in the pathogenesis of nephritis. Clin Exp Immunol. 1993 Jan;91(1):115–120. doi: 10.1111/j.1365-2249.1993.tb03364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yanagishita M., Hascall V. C. Characterization of low buoyant density dermatan sulfate proteoglycans synthesized by rat ovarian granulosa cells in culture. J Biol Chem. 1983 Nov 10;258(21):12847–12856. [PubMed] [Google Scholar]
  48. Yung S., Coles G. A., Williams J. D., Davies M. The source and possible significance of hyaluronan in the peritoneal cavity. Kidney Int. 1994 Aug;46(2):527–533. doi: 10.1038/ki.1994.304. [DOI] [PubMed] [Google Scholar]

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