Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1996 Sep 15;318(Pt 3):779–784. doi: 10.1042/bj3180779

Presence of pro-forms of decorin and biglycan in human articular cartilage.

P J Roughley 1, R J White 1, J S Mort 1
PMCID: PMC1217686  PMID: 8836119

Abstract

The proteoglycans decorin and biglycan in extracts of human articular cartilage were analysed by SDS/PAGE and immunoblotting, using antisera raised to peptide sequences present in the pro-regions and the mature core proteins. In adult cartilage, both pro-forms and mature processed forms of the proteoglycan core protein were observed for both decorin and biglycan. In the case of biglycan, it was also shown that additional proteolytic processing takes place after removal of the propeptide and that this accounts for the presence of non-glycanated forms of the molecule. For both decorin and biglycan, the relative abundance of the pro-forms was much less in the juvenile than the adult. Different adult connective tissues, including meniscus, tendon and intervertebral disc were also examined for the presence of pro-forms of the proteoglycans. While the mature form of decorin was present at a similar level in extracts of all tissues examined, the pro-form was only detected in the articular cartilage. In the case of biglycan, the abundance of the mature form was more varied, with high levels in articular cartilage, intermediate levels in meniscus and the annulus fibrosus of the intervertebral disc, low levels in the nucleus pulposus of the intervertebral disc, and non-detectable levels in the patellar tendon. The pro-form of biglycan was detected in the disc tissue extracts, albeit at a lower level than in articular cartilage, but was not detected in the meniscus or tendon. The proportion of the pro-form relative to the mature form of biglycan was, however, higher in the nucleus pulposus of the intervertebral disc than in articular cartilage. Thus, the persistence of pro-forms of both decorin and biglycan is a feature of the extracellular matrix of some connective tissues, although their abundance is both tissue- and age-dependent, with adult articular cartilage being a particularly rich source.

Full Text

The Full Text of this article is available as a PDF (291.0 KB).

Selected References

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

  1. Abramson S. R., Woessner J. F., Jr cDNA sequence for rat dermatan sulfate proteoglycan-II (decorin). Biochim Biophys Acta. 1992 Sep 24;1132(2):225–227. doi: 10.1016/0167-4781(92)90019-v. [DOI] [PubMed] [Google Scholar]
  2. Bernatowicz M. S., Matsueda G. R. Preparation of peptide-protein immunogens using N-succinimidyl bromoacetate as a heterobifunctional crosslinking reagent. Anal Biochem. 1986 May 15;155(1):95–102. doi: 10.1016/0003-2697(86)90231-9. [DOI] [PubMed] [Google Scholar]
  3. Bianco P., Fisher L. W., Young M. F., Termine J. D., Robey P. G. Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J Histochem Cytochem. 1990 Nov;38(11):1549–1563. doi: 10.1177/38.11.2212616. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Dreher K. L., Asundi V., Matzura D., Cowan K. Vascular smooth muscle biglycan represents a highly conserved proteoglycan within the arterial wall. Eur J Cell Biol. 1990 Dec;53(2):296–304. [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. Hedbom E., Heinegård D. Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J Biol Chem. 1993 Dec 25;268(36):27307–27312. [PubMed] [Google Scholar]
  11. Hughes C. E., Caterson B., White R. J., Roughley P. J., Mort J. S. Monoclonal antibodies recognizing protease-generated neoepitopes from cartilage proteoglycan degradation. Application to studies of human link protein cleavage by stromelysin. J Biol Chem. 1992 Aug 15;267(23):16011–16014. [PubMed] [Google Scholar]
  12. Johnstone B., Markopoulos M., Neame P., Caterson B. Identification and characterization of glycanated and non-glycanated forms of biglycan and decorin in the human intervertebral disc. Biochem J. 1993 Jun 15;292(Pt 3):661–666. doi: 10.1042/bj2920661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kamo I., Kikuchi A., Nonaka I., Yamada E., Kondo J. Haemopoietic activity associated with biglycan like proteoglycan. Biochem Biophys Res Commun. 1993 Sep 15;195(2):1119–1126. doi: 10.1006/bbrc.1993.2160. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Kresse H., Hausser H., Schönherr E. Small proteoglycans. Experientia. 1993 May 15;49(5):403–416. doi: 10.1007/BF01923585. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Li W., Vergnes J. P., Cornuet P. K., Hassell J. R. cDNA clone to chick corneal chondroitin/dermatan sulfate proteoglycan reveals identity to decorin. Arch Biochem Biophys. 1992 Jul;296(1):190–197. doi: 10.1016/0003-9861(92)90562-b. [DOI] [PubMed] [Google Scholar]
  19. Marcum J. A., Thompson M. A. The amino-terminal region of a proteochondroitin core protein, secreted by aortic smooth muscle cells, shares sequence homology with the pre-propeptide region of the biglycan core protein from human bone. Biochem Biophys Res Commun. 1991 Mar 15;175(2):706–712. doi: 10.1016/0006-291x(91)91623-k. [DOI] [PubMed] [Google Scholar]
  20. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. Rada J. A., Cornuet P. K., Hassell J. R. Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res. 1993 Jun;56(6):635–648. doi: 10.1006/exer.1993.1081. [DOI] [PubMed] [Google Scholar]
  25. Rosenberg L. C., Choi H. U., Tang L. H., Johnson T. L., Pal S., Webber C., Reiner A., Poole A. R. Isolation of dermatan sulfate proteoglycans from mature bovine articular cartilages. J Biol Chem. 1985 May 25;260(10):6304–6313. [PubMed] [Google Scholar]
  26. Roughley P. J., White R. J. Age-related changes in the structure of the proteoglycan subunits from human articular cartilage. J Biol Chem. 1980 Jan 10;255(1):217–224. [PubMed] [Google Scholar]
  27. Roughley P. J., White R. J. Dermatan sulphate proteoglycans of human articular cartilage. The properties of dermatan sulphate proteoglycans I and II. Biochem J. 1989 Sep 15;262(3):823–827. doi: 10.1042/bj2620823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Roughley P. J., White R. J., Magny M. C., Liu J., Pearce R. H., Mort J. S. Non-proteoglycan forms of biglycan increase with age in human articular cartilage. Biochem J. 1993 Oct 15;295(Pt 2):421–426. doi: 10.1042/bj2950421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sawhney R. S., Hering T. M., Sandell L. J. Biosynthesis of small proteoglycan II (decorin) by chondrocytes and evidence for a procore protein. J Biol Chem. 1991 May 15;266(14):9231–9240. [PubMed] [Google Scholar]
  30. Schechter I., Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun. 1967 Apr 20;27(2):157–162. doi: 10.1016/s0006-291x(67)80055-x. [DOI] [PubMed] [Google Scholar]
  31. Scholzen T., Solursh M., Suzuki S., Reiter R., Morgan J. L., Buchberg A. M., Siracusa L. D., Iozzo R. V. The murine decorin. Complete cDNA cloning, genomic organization, chromosomal assignment, and expression during organogenesis and tissue differentiation. J Biol Chem. 1994 Nov 11;269(45):28270–28281. [PubMed] [Google Scholar]
  32. Svensson L., Heinegård D., Oldberg A. Decorin-binding sites for collagen type I are mainly located in leucine-rich repeats 4-5. J Biol Chem. 1995 Sep 1;270(35):20712–20716. doi: 10.1074/jbc.270.35.20712. [DOI] [PubMed] [Google Scholar]
  33. Torok M. A., Evans S. A., Marcum J. A. cDNA sequence for bovine biglycan (PGI) protein core. Biochim Biophys Acta. 1993 Apr 29;1173(1):81–84. doi: 10.1016/0167-4781(93)90247-b. [DOI] [PubMed] [Google Scholar]
  34. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wegrowski Y., Pillarisetti J., Danielson K. G., Suzuki S., Iozzo R. V. The murine biglycan: complete cDNA cloning, genomic organization, promoter function, and expression. Genomics. 1995 Nov 1;30(1):8–17. doi: 10.1006/geno.1995.0002. [DOI] [PubMed] [Google Scholar]
  36. Yeo T. K., Torok M. A., Kraus H. L., Evans S. A., Zhou Y., Marcum J. A. Distribution of biglycan and its propeptide form in rat and bovine aortic tissue. J Vasc Res. 1995 May-Jun;32(3):175–182. doi: 10.1159/000159091. [DOI] [PubMed] [Google Scholar]
  37. Zhan Q., Burrows R., Cintron C. Cloning and in situ hybridization of rabbit decorin in corneal tissues. Invest Ophthalmol Vis Sci. 1995 Jan;36(1):206–215. [PubMed] [Google Scholar]
  38. Zhu X. L., Radhakrishnamurthy B., Xu J. H., Srinivasan S. R., Berenson G. S. N-terminal sequence of a core protein from a biglycan isolated from bovine aorta. Connect Tissue Res. 1995;31(2):125–132. doi: 10.3109/03008209509028400. [DOI] [PubMed] [Google Scholar]
  39. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES