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. 1998 Mar 1;330(Pt 2):753–757. doi: 10.1042/bj3300753

Age-related changes in the structure of the keratan sulphate chains attached to fibromodulin isolated from articular cartilage.

R M Lauder 1, T N Huckerby 1, I A Nieduszynski 1, A H Plaas 1
PMCID: PMC1219201  PMID: 9480886

Abstract

Bovine articular cartilage fibromodulin has been isolated from animals aged 3 months to 8 years, and the attached keratan sulphate (KS) chains digested with keratanase II. The oligosaccharides generated have been reduced, examined by high-pH anion-exchange chromatography and their structures identified by comparison with standards. It has been shown that in fibromodulin from young articular cartilage, the KS chains do not possess either non-reducing terminal (alpha2-6)-linked N-acetylneuraminic acid or fucose (alpha1-3)-linked to sulphated N-acetylglucosamine residues. However, an age-related increase has been observed in the abundance of both (alpha2-6)-linked N-acetylneuraminic acid and (alpha1-3)-linked fucose, neither of which is found in KS isolated from non-articular cartilage, irrespective of the age of the source. Interestingly, the KS chain length remains constant as a function of age, which possibly relates to a role in collagen fibril assembly. In addition, no significant age-related changes were identified in levels of galactose sulphation.

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Selected References

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  1. Bengtsson E., Neame P. J., Heinegård D., Sommarin Y. The primary structure of a basic leucine-rich repeat protein, PRELP, found in connective tissues. J Biol Chem. 1995 Oct 27;270(43):25639–25644. doi: 10.1074/jbc.270.43.25639. [DOI] [PubMed] [Google Scholar]
  2. Bhavanandan V. P., Meyer K. Studies on keratosulfates. Methylation, desulfation, and acid hydrolysis studies on old human rib cartilage keratosulfate. J Biol Chem. 1968 Mar 10;243(5):1052–1059. [PubMed] [Google Scholar]
  3. Blochberger T. C., Vergnes J. P., Hempel J., Hassell J. R. cDNA to chick lumican (corneal keratan sulfate proteoglycan) reveals homology to the small interstitial proteoglycan gene family and expression in muscle and intestine. J Biol Chem. 1992 Jan 5;267(1):347–352. [PubMed] [Google Scholar]
  4. Brown G. M., Nieduszynski I. A., Morris H. G., Abram B. L., Huckerby T. N., Block J. A. Skeletal keratan sulphate structural analysis using keratanase II digestion followed by high-performance anion-exchange chromatography. Glycobiology. 1995 May;5(3):311–317. doi: 10.1093/glycob/5.3.311. [DOI] [PubMed] [Google Scholar]
  5. Corpuz L. M., Funderburgh J. L., Funderburgh M. L., Bottomley G. S., Prakash S., Conrad G. W. Molecular cloning and tissue distribution of keratocan. Bovine corneal keratan sulfate proteoglycan 37A. J Biol Chem. 1996 Apr 19;271(16):9759–9763. doi: 10.1074/jbc.271.16.9759. [DOI] [PubMed] [Google Scholar]
  6. Cs-Szabó G., Roughley P. J., Plaas A. H., Glant T. T. Large and small proteoglycans of osteoarthritic and rheumatoid articular cartilage. Arthritis Rheum. 1995 May;38(5):660–668. doi: 10.1002/art.1780380514. [DOI] [PubMed] [Google Scholar]
  7. Dickenson J. M., Huckerby T. N., Nieduszynski I. A. A non-reducing terminal fragment from tracheal cartilage keratan sulphate chains contains alpha (2-3)-linked N-acetylneuraminic acid. Biochem J. 1991 Sep 15;278(Pt 3):779–785. doi: 10.1042/bj2780779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dickenson J. M., Huckerby T. N., Nieduszynski I. A. Skeletal keratan sulphate chains isolated from bovine intervertebral disc may terminate in alpha(2----6)-linked N-acetylneuraminic acid. Biochem J. 1992 Feb 15;282(Pt 1):267–271. doi: 10.1042/bj2820267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dudhia J., Davidson C. M., Wells T. M., Vynios D. H., Hardingham T. E., Bayliss M. T. Age-related changes in the content of the C-terminal region of aggrecan in human articular cartilage. Biochem J. 1996 Feb 1;313(Pt 3):933–940. doi: 10.1042/bj3130933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Funderburgh J. L., Funderburgh M. L., Brown S. J., Vergnes J. P., Hassell J. R., Mann M. M., Conrad G. W. Sequence and structural implications of a bovine corneal keratan sulfate proteoglycan core protein. Protein 37B represents bovine lumican and proteins 37A and 25 are unique. J Biol Chem. 1993 Jun 5;268(16):11874–11880. [PubMed] [Google Scholar]
  12. Funderburgh J. L., Funderburgh M. L., Mann M. M., Conrad G. W. Arterial lumican. Properties of a corneal-type keratan sulfate proteoglycan from bovine aorta. J Biol Chem. 1991 Dec 25;266(36):24773–24777. [PubMed] [Google Scholar]
  13. Gelberg H., Healy L., Whiteley H., Miller L. A., Vimr E. In vivo enzymatic removal of alpha 2-->6-linked sialic acid from the glomerular filtration barrier results in podocyte charge alteration and glomerular injury. Lab Invest. 1996 May;74(5):907–920. [PubMed] [Google Scholar]
  14. Hedbom E., Heinegård D. Interaction of a 59-kDa connective tissue matrix protein with collagen I and collagen II. J Biol Chem. 1989 Apr 25;264(12):6898–6905. [PubMed] [Google Scholar]
  15. Hedlund H., Mengarelli-Widholm S., Heinegård D., Reinholt F. P., Svensson O. Fibromodulin distribution and association with collagen. Matrix Biol. 1994 Apr;14(3):227–232. doi: 10.1016/0945-053x(94)90186-4. [DOI] [PubMed] [Google Scholar]
  16. Heinegård D., Larsson T., Sommarin Y., Franzén A., Paulsson M., Hedbom E. Two novel matrix proteins isolated from articular cartilage show wide distributions among connective tissues. J Biol Chem. 1986 Oct 15;261(29):13866–13872. [PubMed] [Google Scholar]
  17. Huckerby T. N., Nieduszynski I. A., Brown G. M., Cockin G. H. A full assignment of proton resonances for an alpha(1-3)-linked fucose residue in keratan sulphate from bovine articular cartilage. Glycoconj J. 1991 Feb;8(1):39–44. doi: 10.1007/BF00731641. [DOI] [PubMed] [Google Scholar]
  18. Johnstone B., Bayliss M. T. The large proteoglycans of the human intervertebral disc. Changes in their biosynthesis and structure with age, topography, and pathology. Spine (Phila Pa 1976) 1995 Mar 15;20(6):674–684. doi: 10.1097/00007632-199503150-00008. [DOI] [PubMed] [Google Scholar]
  19. Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. doi: 10.1016/0968-0004(94)90090-6. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Larsson T., Sommarin Y., Paulsson M., Antonsson P., Hedbom E., Wendel M., Heinegård D. Cartilage matrix proteins. A basic 36-kDa protein with a restricted distribution to cartilage and bone. J Biol Chem. 1991 Oct 25;266(30):20428–20433. [PubMed] [Google Scholar]
  22. Lauder R. M., Huckerby T. N., Nieduszynski I. A. Structure of the keratan sulphate chains attached to fibromodulin isolated from bovine tracheal cartilage. Oligosaccharides generated by keratanase digestion. Biochem J. 1994 Sep 1;302(Pt 2):417–423. doi: 10.1042/bj3020417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lauder R. M., Huckerby T. N., Nieduszynski I. A. The structure of the keratan sulphate chains attached to fibromodulin from human articular cartilage. Glycoconj J. 1997 Aug;14(5):651–660. doi: 10.1023/a:1018552913584. [DOI] [PubMed] [Google Scholar]
  24. Lauder R. M., Huckerby T. N., Nieduszynski I. A. The structure of the keratan sulphate chains attached to fibromodulin isolated from articular cartilage. Eur J Biochem. 1996 Dec 1;242(2):402–409. doi: 10.1111/j.1432-1033.1996.0402r.x. [DOI] [PubMed] [Google Scholar]
  25. Lauder R. M., Huckerby T. N., Nieduszynski I. A. The structure of the keratan sulphate chains attached to fibromodulin isolated from bovine tracheal cartilage: oligosaccharides generated by keratanase II digestion. Glycoconj J. 1995 Oct;12(5):651–659. doi: 10.1007/BF00731261. [DOI] [PubMed] [Google Scholar]
  26. Melching L. I., Roughley P. J. The synthesis of dermatan sulphate proteoglycans by fetal and adult human articular cartilage. Biochem J. 1989 Jul 15;261(2):501–508. doi: 10.1042/bj2610501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neame P. J., Sommarin Y., Boynton R. E., Heinegård D. The structure of a 38-kDa leucine-rich protein (chondroadherin) isolated from bovine cartilage. J Biol Chem. 1994 Aug 26;269(34):21547–21554. [PubMed] [Google Scholar]
  28. Nieduszynski I. A., Huckerby T. N., Dickenson J. M., Brown G. M., Tai G. H., Morris H. G., Eady S. There are two major types of skeletal keratan sulphates. Biochem J. 1990 Oct 1;271(1):243–245. doi: 10.1042/bj2710243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Noyori K., Jasin H. E. Inhibition of human fibroblast adhesion by cartilage surface proteoglycans. Arthritis Rheum. 1994 Nov;37(11):1656–1663. doi: 10.1002/art.1780371115. [DOI] [PubMed] [Google Scholar]
  30. Oldberg A., Antonsson P., Lindblom K., Heinegård D. A collagen-binding 59-kd protein (fibromodulin) is structurally related to the small interstitial proteoglycans PG-S1 and PG-S2 (decorin). EMBO J. 1989 Sep;8(9):2601–2604. doi: 10.1002/j.1460-2075.1989.tb08399.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Plaas A. H., Ison A. L., Ackland J. Synthesis of small proteoglycans substituted with keratan sulfate by rabbit articular chondrocytes. J Biol Chem. 1989 Aug 25;264(24):14447–14454. [PubMed] [Google Scholar]
  32. Plaas A. H., Neame P. J., Nivens C. M., Reiss L. Identification of the keratan sulfate attachment sites on bovine fibromodulin. J Biol Chem. 1990 Nov 25;265(33):20634–20640. [PubMed] [Google Scholar]
  33. Poppe L., Stuike-Prill R., Meyer B., van Halbeek H. The solution conformation of sialyl-alpha (2----6)-lactose studied by modern NMR techniques and Monte Carlo simulations. J Biomol NMR. 1992 Mar;2(2):109–136. doi: 10.1007/BF01875524. [DOI] [PubMed] [Google Scholar]
  34. Roughley P. J., Melching L. I., Recklies A. D. Changes in the expression of decorin and biglycan in human articular cartilage with age and regulation by TGF-beta. Matrix Biol. 1994 Jan;14(1):51–59. doi: 10.1016/0945-053x(94)90029-9. [DOI] [PubMed] [Google Scholar]
  35. Roughley P. J., White R. J., Cs-Szabó G., Mort J. S. Changes with age in the structure of fibromodulin in human articular cartilage. Osteoarthritis Cartilage. 1996 Sep;4(3):153–161. doi: 10.1016/s1063-4584(96)80011-2. [DOI] [PubMed] [Google Scholar]
  36. SENO N., MEYER K., ANDERSON B., HOFFMAN P. VARIATIONS IN KERATOSULFATES. J Biol Chem. 1965 Mar;240:1005–1010. [PubMed] [Google Scholar]
  37. Sampaio L. de O., Bayliss M. T., Hardingham T. E., Muir H. Dermatan sulphate proteoglycan from human articular cartilage. Variation in its content with age and its structural comparison with a small chondroitin sulphate proteoglycan from pig laryngeal cartilage. Biochem J. 1988 Sep 15;254(3):757–764. doi: 10.1042/bj2540757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sata T., Roth J., Zuber C., Stamm B., Heitz P. U. Expression of alpha 2,6-linked sialic acid residues in neoplastic but not in normal human colonic mucosa. A lectin-gold cytochemical study with Sambucus nigra and Maackia amurensis lectins. Am J Pathol. 1991 Dec;139(6):1435–1448. [PMC free article] [PubMed] [Google Scholar]
  39. Scott J. E., Parry D. A. Control of collagen fibril diameters in tissues. Int J Biol Macromol. 1992 Oct;14(5):292–293. doi: 10.1016/s0141-8130(05)80043-1. [DOI] [PubMed] [Google Scholar]
  40. Shinomura T., Kimata K. Proteoglycan-Lb, a small dermatan sulfate proteoglycan expressed in embryonic chick epiphyseal cartilage, is structurally related to osteoinductive factor. J Biol Chem. 1992 Jan 15;267(2):1265–1270. [PubMed] [Google Scholar]
  41. Tai G. H., Huckerby T. N., Nieduszynski I. A. N.m.r. spectroscopic studies of fucose-containing oligosaccharides derived from keratanase digestion of articular cartilage keratan sulphates. Influence of fucose residues on keratanase cleavage. Biochem J. 1993 May 1;291(Pt 3):889–894. doi: 10.1042/bj2910889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vierbuchen M. J., Fruechtnicht W., Brackrock S., Krause K. T., Zienkiewicz T. J. Quantitative lectin-histochemical and immunohistochemical studies on the occurrence of alpha(2,3)- and alpha(2,6)-linked sialic acid residues in colorectal carcinomas. Relation to clinicopathologic features. Cancer. 1995 Sep 1;76(5):727–735. doi: 10.1002/1097-0142(19950901)76:5<727::aid-cncr2820760504>3.0.co;2-r. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Wachtel E., Maroudas A., Schneiderman R. Age-related changes in collagen packing of human articular cartilage. Biochim Biophys Acta. 1995 Feb 23;1243(2):239–243. doi: 10.1016/0304-4165(94)00134-j. [DOI] [PubMed] [Google Scholar]

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