Proteoglycans of the intervertebral disc

The Intervertebral Disc: Molecular and Structural Studies of the Disc in Health and Disease

Volumn , Issue , 2014, Pages 53-77

  Melrose, James ^a   Roughley, Peter ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b SHRINERS HOSPITAL FOR CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84930725599     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7091-1535-0_4     Document Type: Chapter

References (202)

1. Adams MA, Roughley PJ (2006) What is intervertebral disc degeneration, and what causes it? Spine (Phila Pa 1976) 31:2151-2161
2. Agrawal A, Guttapalli A, Narayan S, Albert TJ, Shapiro IM, Risbud MV (2007) Normoxic stabilization of HIF-1alpha drives glycolytic metabolism and regulates aggrecan gene expression in nucleus pulposus cells of the rat intervertebral disk. Am J Physiol Cell Physiol 293:C621-C631
3. Akeda K, An HS, Pichika R, Patel K, Muehleman C, Nakagawa K, Uchida A, Masuda K (2007) The expression of NG2 proteoglycan in the human intervertebral disc. Spine (Phila Pa 1976) 32: 306-314
4. Ameye L, Young MF (2002) Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12:107R-116R
5. Antonsson P, Heinegard D, Oldberg A (1991) Posttranslational modifications offibromodulin. J Biol Chem 266:16859-16861
6. Antonsson P, Heinegard D, Oldberg A (1993) Structure and deduced amino acid sequence of the humanfibromodulin gene. Biochim Biophys Acta 1174:204-206
7. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y (1999) Perlecan is essential for cartilage and cephalic development. Nat Genet 23:354-358
8. Arikawa-Hirasawa E, Wilcox WR, Le AH, Silverman N, Govindraj P, Hassell JR, Yamada Y (2001a) Dyssegmental dysplasia, Silverman-Handmaker type, is caused by functional null mutations of the perlecan gene. Nat Genet 27:431-434
9. Arikawa-Hirasawa E, Wilcox WR, Yamada Y (2001b) Dyssegmental dysplasia, Silverman-Handmaker type: unexpected role of perlecan in cartilage development. Am J Med Genet 106:254-257
10. Arikawa-Hirasawa E, Le AH, Nishino I, Nonaka I, Ho NC, Francomano CA, Govindraj P, Hassell JR, Devaney JM, Spranger J, Stevenson RE, Iannaccone S, Dalakas MC, Yamada Y (2002) Structural and functional mutations of the perlecan gene cause Schwartz-Jampel syndrome, with myotonic myopathy and chondrodysplasia. Am J Hum Genet 70:1368-1375
11. Barry FP, Neame PJ, Sasse J, Pearson D (1994) Length variation in the keratan sulfate domain of mammalian aggrecan. Matrix Biol 14:323-328
12. Barry FP, Rosenberg LC, Gaw JU, Koob TJ, Neame PJ (1995) N-and O-linked keratan sulfate on the hyaluronan binding region of aggrecan from mature and immature bovine cartilage. J Biol Chem 270:20516-20524
13. Bengtsson E, Neame PJ, Heinegard D, Sommarin Y (1995) The primary structure of a basic leucine-rich repeat protein, PRELP, found in connective tissues. J Biol Chem 270:25639-25644
14. Bengtsson E, Aspberg A, Heinegard D, Sommarin Y, Spillmann D (2000) The amino-terminal part of PRELP binds to heparin and heparan sulfate. J Biol Chem 275:40695-40702
15. Bengtsson E, Morgelin M, Sasaki T, Timpl R, Heinegard D, Aspberg A (2002) The leucine-rich repeat protein PRELP binds perlecan and collagens and may function as a basement membrane anchor. J Biol Chem 277:15061-15068
16. Bix G, Fu J, Gonzalez EM, Macro L, Barker A, Campbell S, Zutter MM, Santoro SA, Kim JK, Hook M, Reed CC, Iozzo RV (2004) Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through alpha2beta1 integrin. J Cell Biol 166:97-109
17. Bix G, Iozzo RA, Woodall B, Burrows M, McQuillan A, Campbell S, Fields GB, Iozzo RV (2007) Endorepellin, the C-terminal angiostatic module of perlecan, enhances collagen-platelet responses via the alpha2beta1-integrin receptor. Blood 109:3745-3748
18. Botsford DJ, Esses SI, Ogilvie-Harris DJ (1994) In vivo diurnal variation in intervertebral disc volume and morphology. Spine (Phila Pa 1976) 19:935-940
19. Bredrup C, Knappskog PM, Majewski J, Rodahl E, Boman H (2005) Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Invest Ophthalmol Vis Sci 46:420-426
20. Brown GM, Huckerby TN, Bayliss MT, Nieduszynski IA (1998) Human aggrecan keratan sulfate undergoes structural changes during adolescent development. J Biol Chem 273:26408-26414
21. Camper L, Heinegard D, Lundgren-Akerlund E (1997) Integrin alpha-2beta1 is a receptor for the cartilage matrix protein chondroadherin. J Cell Biol 138:1159-1167
22. Caterson B (2012) Fell-Muir lecture: chondroitin sulphate glycosaminoglycans: fun for some and confusion for others. Int J Exp Pathol 93:1-10
23. Caterson B, Mahmoodian F, Sorrell JM, Hardingham TE, Bayliss MT, Carney SL, Ratcliffe A, Muir H (1990) Modulation of native chondroitin sulphate structure in tissue development and in disease. J Cell Sci 97(Pt 3):411-417
24. Chakravarti S (2002) Functions of lumican andfibromodulin: lessons from knockout mice. Glycoconj J 19:287-293
25. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H (1998) Lumican regulates collagenfibril assembly: skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141: 1277-1286
26. Chen ZT, Wang IJ, Shih YF, Lin LL (2009) The association of haplotype at the lumican gene with high myopia susceptibility in Taiwanese patients. Ophthalmology 116:1920-1927
27. Chen S, Oldberg A, Chakravarti S, Birk DE (2010) Fibromodulin regulates collagenfibrillogenesis during peripheral corneal development. Dev Dyn 239:844-854
28. Chuang CY, Lord MS, Melrose J, Rees MD, Knox SM, Freeman C, Iozzo RV, Whitelock JM (2010) Heparan sulfate-dependent signaling offibroblast growth factor 18 by chondrocyte-derived perlecan. Biochemistry 49:5524-5532
29. Cohen IR, Grassel S, Murdoch AD, Iozzo RV (1993) Structural characterization of the complete human perlecan gene and its promoter. Proc Natl Acad Sci USA 90:10404-10408
30. Corsi A, Xu T, Chen XD, Boyde A, Liang J, Mankani M, Sommer B, Iozzo RV, Eichstetter I, Robey PG, Bianco P, Young MF (2002) Phenotypic effects of biglycan deficiency are linked to collagenfibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res 17:1180-1189
31. Cummings RD (2009) The repertoire of glycan determinants in the human glycome. Mol Biosyst 5:1087-1104
32. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV (1997) Targeted disruption of decorin leads to abnormal collagenfibril morphology and skin fragility. J Cell Biol 136:729-743
33. Danielson KG, Siracusa LD, Donovan PJ, Iozzo RV (1999) Decorin, epiphycan, and lumican genes are closely linked on murine chromosome 10 and are deleted in lethal steel mutants. Mamm Genome 10:201-203
34. Day JM, Olin AI, Murdoch AD, Canfield A, Sasaki T, Timpl R, Hardingham TE, Aspberg A (2004) Alternative splicing in the aggrecan G3 domain influences binding interactions with tenascin-C and other extracellular matrix proteins. J Biol Chem 279: 12511-12518
35. Doege K, Sasaki M, Horigan E, Hassell JR, Yamada Y (1987) Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J Biol Chem 262:17757-17767
36. Doege KJ, Sasaki M, Kimura T, Yamada Y (1991) Complete coding sequence and deduced primary structure of the human cartilage large aggregating proteoglycan, aggrecan. Human-specific repeats, and additional alternatively spliced forms. J Biol Chem 266:894-902
37. Doege KJ, Coulter SN, Meek LM, Maslen K, Wood JG (1997) A human-specific polymorphism in the coding region of the aggrecan gene. Variable number of tandem repeats produce a range of core protein sizes in the general population. J Biol Chem 272: 13974-13979
38. Dours-Zimmermann MT, Zimmermann DR (1994) A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican. J Biol Chem 269:32992-32998
39. Durigova M, Nagase H, Mort JS, Roughley PJ (2011a) MMPs are less efficient than ADAMTS5 in cleaving aggrecan core protein. Matrix Biol 30:145-153
40. Durigova M, Troeberg L, Nagase H, Roughley PJ, Mort JS (2011b) Involvement of ADAMTS5 and hyaluronidase in aggrecan degradation and release from OSM-stimulated cartilage. Eur Cell Mater 21:31-45
41. Elsaid KA, Jay GD, Warman ML, Rhee DK, Chichester CO (2005) Association of articular cartilage degradation and loss of boundarylubricating ability of synovialfluid following injury and inflammatory arthritis. Arthritis Rheum 52:1746-1755
42. Ezura Y, Chakravarti S, Oldberg A, Chervoneva I, Birk DE (2000) Differential expression of lumican andfibromodulin regulate collagenfibrillogenesis in developing mouse tendons. J Cell Biol 151:779-788
43. Faivre L, Prieur AM, Le Merrer M, Hayem F, Penet C, Woo P, Hofer M, Dagoneau N, Sermet I, Munnich A, Cormier-Daire V (2000) Clinical variability and genetic homogeneity of the camptodactylyarthropathy-coxa vara-pericarditis syndrome. Am J Med Genet 95:233-236
44. Flannery C, Stanescu V, Morgelin M, Boynton R, Gordy J, Sandy J (1992) Variability in the G3 domain content of bovine aggrecan from cartilage extracts and chondrocyte cultures. Arch Biochem Biophys 297:52-60
45. Flannery CR, Hughes CE, Schumacher BL, Tudor D, Aydelotte MB, Kuettner KE, Caterson B (1999) Articular cartilage superficial zone protein (SZP) is homologous to megakaryocyte stimulating factor precursor and is a multifunctional proteoglycan with potential growth-promoting, cytoprotective, and lubricating properties in cartilage metabolism. Biochem Biophys Res Commun 254:535-541
46. Fosang AJ, Hardingham TE (1989) Isolation of the N-terminal globular protein domains from cartilage proteoglycans. Identification of G2 domain and its lack of interaction with hyaluronate and link protein. Biochem J 261:801-809
47. Fosang AJ, Neame PJ, Last K, Hardingham TE, Murphy G, Hamilton JA (1992) The interglobular domain of cartilage aggrecan is cleaved by PUMP, gelatinases, and cathepsin B. J Biol Chem 267: 19470-19474
48. Fransson LA, Belting M, Cheng F, Jonsson M, Mani K, Sandgren S (2004) Novel aspects of glypican glycobiology. Cell Mol Life Sci 61:1016-1024
49. Fulop C, Walcz E, Valyon M, Glant TT (1993) Expression of alternatively spliced epidermal growth factor-like domains in aggrecans of different species. Evidence for a novel module. J Biol Chem 268:17377-17383
50. Gendron C, Kashiwagi M, Lim NH, Enghild JJ, Thogersen IB, Hughes C, Caterson B, Nagase H (2007) Proteolytic activities of human ADAMTS-5: comparative studies with ADAMTS-4. J Biol Chem 282:18294-18306
51. Geng Y, McQuillan D, Roughley PJ (2006) SLRP interaction can protect collagenfibrils from cleavage by collagenases. Matrix Biol 25:484-491
52. Girardin EP, Hajmohammadi S, Birmele B, Helisch A, Shworak NW, de Agostini AI (2005) Synthesis of anticoagulantly active heparan sulfate proteoglycans by glomerular epithelial cells involves multiple 3-O-sulfotransferase isoforms and a limiting precursor pool. J Biol Chem 280:38059-38070
53. Gleghorn L, Ramesar R, Beighton P, Wallis G (2005) A mutation in the variable repeat region of the aggrecan gene (AGC1) causes a form of spondyloepiphyseal dysplasia associated with severe, premature osteoarthritis. Am J Hum Genet 77:484-490
54. Gogate SS, Nasser R, Shapiro IM, Risbud MV (2011) Hypoxic regulation of beta-1,3-glucuronyltransferase 1 expression in nucleus pulposus cells of the rat intervertebral disc: role of hypoxia-inducible factor proteins. Arthritis Rheum 63:1950-1960
55. Goldberg M, Septier D, Oldberg A, Young MF, Ameye LG (2006) Fibromodulin-deficient mice display impaired collagenfibrillogenesis in predentin as well as altered dentin mineralization and enamel formation. J Histochem Cytochem 54:525-537
56. Gonzalez EM, Reed CC, Bix G, Fu J, Zhang Y, Gopalakrishnan B, Greenspan DS, Iozzo RV (2005) BMP-1/Tolloid-like metalloproteases process endorepellin, the angiostatic C-terminal fragment of perlecan. J Biol Chem 280:7080-7087
57. Grover J, Roughley PJ (1993) Versican gene expression in human articular cartilage and comparison of mRNA splicing variation with aggrecan. Biochem J 291(Pt 2):361-367
58. Grover J, Roughley PJ (1998) Characterization of the human proline/ arginine-rich end leucine-rich repeat protein (PRELP) gene promoter and identification of a repressor element. Biochem J 336(Pt 1):77-82
59. Grover J, Roughley PJ (2001) Characterization and expression of murine PRELP. Matrix Biol 20:555-564
60. Grover J, Chen XN, Korenberg JR, Roughley PJ (1995) The human lumican gene. Organization, chromosomal location, and expression in articular cartilage. J Biol Chem 270:21942-21949
61. Grover J, Chen XN, Korenberg JR, Recklies AD, Roughley PJ (1996) The gene organization, chromosome location, and expression of a 55-kDa matrix protein (PRELP) of human articular cartilage. Genomics 38:109-117
62. Grover J, Chen XN, Korenberg JR, Roughley PJ (1997) The structure and chromosome location of the human chondroadherin gene (CHAD). Genomics 45:379-385
63. Gruber HE, Ingram JA, Hoelscher GL, Zinchenko N, Hanley EN Jr, Sun Y (2009) Asporin, a susceptibility gene in osteoarthritis, is expressed at higher levels in the more degenerate human intervertebral disc. Arthritis Res Ther 11:R47
64. Haglund L, Ouellet J, Roughley P (2009) Variation in chondroadherin abundance and fragmentation in the human scoliotic disc. Spine (Phila Pa 1976) 34:1513-1518
65. Haglund L, Tillgren V, Addis L, Wenglen C, Recklies A, Heinegard D (2011) Identification and characterization of the integrin alpha-2beta1 binding motif in chondroadherin mediating cell attachment. J Biol Chem 286:3925-3934
66. Hasegawa K, Yoneda M, Kuwabara H, Miyaishi O, Itano N, Ohno A, Zako M, Isogai Z (2007) Versican, a major hyaluronan-binding component in the dermis, loses its hyaluronan-binding ability in solar elastosis. J Invest Dermatol 127:1657-1663
67. Hayes A, Lord MS, Smith SM, Smith MM, Whitelock JM, Weiss AS, Melrose J (2011a) Colocalization in vivo and association in vitro of perlecan and elastin. Histochem Cell Biol 136:437-475
68. Hayes AJ, Hughes CE, Ralphs JR, Caterson B (2011b) Chondroitin sulphate sulphation motif expression in the ontogeny of the intervertebral disc. Eur Cell Mater 21:1-14
69. Hayes AJ, Smith SM, Gibson MA, Melrose J (2011c) Comparative immunolocalisation of the elastinfibre associated proteinsfibrillin-1, LTBP2 and MAGP-1 with components of the collagenous and proteoglycan matrix of the foetal human IVD. Spine (Phila Pa 1976) 36:E1365-E1372
70. Hayes AJ, Smith SM, Melrose J (2013) Comparative immunolocalisation offibrillin-1 and perlecan in the human foetal and HS deficient Hspg2 exon 3 null mutant mouse intervertebral disc. Histochem Cell Biol 139:1-11
71. Heathfield TF, Onnerfjord P, Dahlberg L, Heinegard D (2004) Cleavage offibromodulin in cartilage explants involves removal of the N-terminal tyrosine sulfate-rich region by proteolysis at a site that is sensitive to matrix metalloproteinase-13. J Biol Chem 279:6286-6295
72. Hedbom E, Heinegard D (1993) Binding offibromodulin and decorin to separate sites onfibrillar collagens. J Biol Chem 268:27307-27312
73. Heegaard AM, Corsi A, Danielsen CC, Nielsen KL, Jorgensen HL, Riminucci M, Young MF, Bianco P (2007) Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation 115:2731-2738
74. Henry SP, Takanosu M, Boyd TC, Mayne PM, Eberspaecher H, Zhou W, de Crombrugghe B, Hook M, Mayne R (2001) Expression pattern and gene characterization of asporin. A newly discovered member of the leucine-rich repeat protein family. J Biol Chem 276: 12212-12221
75. Hirai M, Horiguchi M, Ohbayashi T, Kita T, Chien KR, Nakamura T (2007) Latent TGF-beta-binding protein 2 binds to DANCE/fibulin-5 and regulates elasticfiber assembly. EMBO J 26:3283-3295
76. Hirani R, Hanssen E, Gibson MA (2007) LTBP-2 specifically interacts with the amino-terminal region offibrillin-1 and competes with LTBP-1 for binding to this microfibrillar protein. Matrix Biol 26: 213-223
77. Hiyama A, Gajghate S, Sakai D, Mochida J, Shapiro IM, Risbud MV (2009) Activation of TonEBP by calcium controls {beta}1,3-glucuronosyltransferase-I expression, a key regulator of glycosaminoglycan synthesis in cells of the intervertebral disc. J Biol Chem 284:9824-9834
78. Hocking AM, Shinomura T, McQuillan DJ (1998) Leucine-rich repeat glycoproteins of the extracellular matrix. Matrix Biol 17:1-19
79. Humphries DE, Stevens RL (1992) Regulation of the gene that encodes the peptide core of heparin proteoglycan and other proteoglycans that are stored in the secretory granules of hematopoietic cells. Adv Exp Med Biol 313:59-67
80. Imai K, Hiramatsu A, Fukushima D, Pierschbacher MD, Okada Y (1997) Degradation of decorin by matrix metalloproteinases: identification of the cleavage sites, kinetic analyses and transforming growth factor-beta1 release. Biochem J 322(Pt 3):809-814
81. Iozzo RV (1994) Perlecan: A gem of a proteoglycan. Matrix Biol 14:203-208
82. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609-652
83. Iozzo RV, Schaefer L (2010) Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 277:3864-3875
84. Iozzo RV, Naso MF, Cannizzaro LA, Wasmuth JJ, McPherson JD (1992) Mapping of the versican proteoglycan gene (CSPG2) to the long arm of human chromosome 5 (5q12-5q14). Genomics 14:845-851
85. Iozzo R, Goldoni S, Berendsen AD, Young MF (2011) Small leucine rich proteoglycans. In: Mecham R (ed) The extracellular matrix: an overview, Biology of extracellular matrix. Springer, Berlin/ Heidelberg, pp 197-231
86. Ito K, Shinomura T, Zako M, Ujita M, Kimata K (1995) Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J Biol Chem 270:958-965
87. Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71:481-539
88. Jay GD, Harris DA, Cha CJ (2001a) Boundary lubrication by lubricin is mediated by O-linked beta(1-3)Gal-GalNAc oligosaccharides. Glycoconj J 18:807-815
89. Jay GD, Tantravahi U, Britt DE, Barrach HJ, Cha CJ (2001b) Homology of lubricin and superficial zone protein (SZP): products of megakaryocyte stimulating factor (MSF) gene expression by human synovialfibroblasts and articular chondrocytes localized to chromosome 1q25. J Orthop Res 19:677-687
90. Jepsen KJ, Wu F, Peragallo JH, Paul J, Roberts L, Ezura Y, Oldberg A, Birk DE, Chakravarti S (2002) A syndrome of joint laxity and impaired tendon integrity in lumican-andfibromodulin-deficient mice. J Biol Chem 277:35532-35540
91. Johnson WE, Caterson B, Eisenstein SM, Hynds DL, Snow DM, Roberts S (2002) Human intervertebral disc aggrecan inhibits nerve growth in vitro. Arthritis Rheum 46:2658-2664
92. Johnson WE, Caterson B, Eisenstein SM, Roberts S (2005) Human intervertebral disc aggrecan inhibits endothelial cell adhesion and cell migration in vitro. Spine (Phila Pa 1976) 30:1139-1147
93. Kalamajski S, Oldberg A (2009) Homologous sequence in lumican andfibromodulin leucine-rich repeat 5-7 competes for collagen binding. J Biol Chem 284:534-539
94. Kalamajski S, Oldberg A (2010) The role of small leucine-rich proteoglycans in collagenfibrillogenesis. Matrix Biol 29:248-253
95. Kalamajski S, Aspberg A, Lindblom K, Heinegard D, Oldberg A (2009) Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization. Biochem J 423:53-59
96. Kallunki P, Tryggvason K (1992) Human basement membrane heparan sulfate proteoglycan core protein: A 467-kD protein containing multiple domains resembling elements of the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J Cell Biol 116:559-571
97. Karniski LP (2001) Mutations in the diastrophic dysplasia sulfate transporter (DTDST) gene: correlation between sulfate transport activity and chondrodysplasia phenotype. Hum Mol Genet 10:1485-1490
98. Kawaguchi Y, Osada R, Kanamori M, Ishihara H, Ohmori K, Matsui H, Kimura T (1999) Association between an aggrecan gene polymorphism and lumbar disc degeneration. Spine (Phila Pa 1976) 24: 2456-2460
99. Kloeckener-Gruissem B, Bartholdi D, Abdou MT, Zimmermann DR, Berger W (2006) Identification of the genetic defect in the original Wagner syndrome family. Mol Vis 12:350-355
100. Kluppel M, Wight TN, Chan C, Hinek A, Wrana JL (2005) Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132:3989-4003
101. Korenberg JR, Chen XN, Doege K, Grover J, Roughley PJ (1993) Assignment of the human aggrecan gene (AGC1) to 15q26 usingfluorescence in situ hybridization analysis. Genomics 16:546-548
102. Kurima K, Warman ML, Krishnan S, Domowicz M, Krueger RC Jr, Deyrup A, Schwartz NB (1998) A member of a family of sulfateactivating enzymes causes murine brachymorphism. Proc Natl Acad Sci USA 95:8681-8685
103. Li H, Schwartz NB, Vertel BM (1993) cDNA cloning of chick cartilage chondroitin sulfate (aggrecan) core protein and identification of a stop codon in the aggrecan gene associated with the chondrodystrophy, nanomelia. J Biol Chem 268:23504-23511
104. Li Y, Aoki T, Mori Y, Ahmad M, Miyamori H, Takino T, Sato H (2004) Cleavage of lumican by membrane-type matrix metalloproteinase-1 abrogates this proteoglycan-mediated suppression of tumor cell colony formation in soft agar. Cancer Res 64:7058-7064
105. Lorenzo P, Aspberg A, Onnerfjord P, Bayliss MT, Neame PJ, Heinegard D (2001) Identification and characterization of asporin. A novel member of the leucine-rich repeat protein family closely related to decorin and biglycan. J Biol Chem 276:12201-12211
106. Majava M, Bishop PN, Hagg P, Scott PG, Rice A, Inglehearn C, Hammond CJ, Spector TD, Ala-Kokko L, Mannikko M (2007) Novel mutations in the small leucine-rich repeat protein/proteoglycan (SLRP) genes in high myopia. Hum Mutat 28:336-344
107. Mansson B, Wenglen C, Morgelin M, Saxne T, Heinegard D (2001) Association of chondroadherin with collagen type II. J Biol Chem 276:32883-32888
108. Marcelino J, Carpten JD, Suwairi WM, Gutierrez OM, Schwartz S, Robbins C, Sood R, Makalowska I, Baxevanis A, Johnstone B, Laxer RM, Zemel L, Kim CA, Herd JK, Ihle J, Williams C, Johnson M, Raman V, Alonso LG, Brunoni D, Gerstein A, Papadopoulos N, Bahabri SA, Trent JM, Warman ML (1999) CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathycoxa vara-pericarditis syndrome. Nat Genet 23:319-322
109. Margolis RU, Margolis RK (1994) Aggrecan-versican-neurocan family proteoglycans. Methods Enzymol 245:105-126
110. McBride OW, Fisher LW, Young MF (1990) Localization of PGI (biglycan, BGN) and PGII (decorin, DCN, PG-40) genes on human chromosomes Xq13-qter and 12q, respectively. Genomics 6:219-225
111. Melrose J, Ghosh P, Taylor TK (2001) A comparative analysis of the differential spatial and temporal distributions of the large (aggrecan, versican) and small (decorin, biglycan,fibromodulin) proteoglycans of the intervertebral disc. J Anat 198:3-15
112. Melrose J, Roughley P, Knox S, Smith S, Lord M, Whitelock J (2006) The structure, location, and function of perlecan, a prominent pericellular proteoglycan of fetal, postnatal, and mature hyaline cartilages. J Biol Chem 281:36905-36914
113. Melrose J, Smith SM, Fuller ES, Young AA, Roughley PJ, Dart A, Little CB (2007) Biglycan andfibromodulin fragmentation correlates with temporal and spatial annular remodelling in experimentally injured ovine intervertebral discs. Eur Spine J 16:2193-2205
114. Melrose J, Fuller ES, Roughley PJ, Smith MM, Kerr B, Hughes CE, Caterson B, Little CB (2008a) Fragmentation of decorin, biglycan, lumican and keratocan is elevated in degenerate human meniscus, knee and hip articular cartilages compared with age-matched macroscopically normal and control tissues. Arthritis Res Ther 10:R79
115. Melrose J, Hayes AJ, Whitelock JM, Little CB (2008b) Perlecan, the "jack of all trades" proteoglycan of cartilaginous weight-bearing connective tissues. Bioessays 30:457-469
116. Merberg D, Fitz LJ, Temple P, Giannotti J, Murtha P, Fitzgerald M, Scaltreto H, Kelleher K, Preissner K, Kriz R, Jacobs K, Turner K (1993) A comparison of vitronectin and megakaryocyte stimulating factor. In: Rosenblatt S, Kost C, Wegerhoff J, Mosher DF, Preissner KT (eds) Biology of vitronectins and their Receptors. Elsevier, Amsterdam, pp 45-54
117. Mimura T, Han KY, Onguchi T, Chang JH, Kim TI, Kojima T, Zhou Z, Azar DT (2009) MT1-MMP-mediated cleavage of decorin in corneal angiogenesis. J Vasc Res 46:541-550
118. Monfort J, Tardif G, Reboul P, Mineau F, Roughley P, Pelletier JP, Martel-Pelletier J (2006) Degradation of small leucine-rich repeat proteoglycans by matrix metalloprotease-13: identification of a new biglycan cleavage site. Arthritis Res Ther 8:R26
119. Morgelin M, Paulsson M, Hardingham TE, Heinegard D, Engel J (1988) Cartilage proteoglycans. Assembly with hyaluronate and link protein as studied by electron microscopy. Biochem J 253:175-185
120. Mukhopadhyay A, Nikopoulos K, Maugeri A, de Brouwer AP, van Nouhuys CE, Boon CJ, Perveen R, Zegers HA, Wittebol-Post D, van den Biesen PR, van der Velde-Visser SD, Brunner HG, Black GC, Hoyng CB, Cremers FP (2006) Erosive vitreoretinopathy and wagner disease are caused by intronic mutations in CSPG2/Versican that result in an imbalance of splice variants. Invest Ophthalmol Vis Sci 47:3565-3572
121. Muragaki Y, Nishimura I, Henney A, Ninomiya Y, Olsen BR (1990) The alpha 1 (IX) collagen gene gives rise to two different transcripts in both mouse embryonic and human fetal RNA. Proc Natl Acad Sci USA 87:2400-2404
122. Murdoch AD, Iozzo RV (1993) Perlecan: The multidomain heparan sulphate proteoglycan of basement membrane and extracellular matrix. Virchows Arch A Pathol Anat Histopathol 423:237-242
123. Murdoch AD, Dodge GR, Cohen I, Tuan RS, Iozzo RV (1992) Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J Biol Chem 267:8544-8557
124. Nareyeck G, Seidler DG, Troyer D, Rauterberg J, Kresse H, Schonherr E (2004) Differential interactions of decorin and decorin mutants with type I and type VI collagens. Eur J Biochem 271:3389-3398
125. Naso MF, Zimmermann DR, Iozzo RV (1994) Characterization of the complete genomic structure of the human versican gene and functional analysis of its promoter. J Biol Chem 269:32999-33008
126. Neame PJ, Barry FP (1993) The link proteins. Experientia 49:393-402
127. Neame PJ, Sommarin Y, Boynton RE, Heinegard D (1994) The structure of a 38-kDa leucine-rich protein (chondroadherin) isolated from bovine cartilage. J Biol Chem 269:21547-21554
128. Neame PJ, Kay CJ, McQuillan DJ, Beales MP, Hassell JR (2000) Independent modulation of collagenfibrillogenesis by decorin and lumican. Cell Mol Life Sci 57:859-863
129. Nilsson B, De Luca S, Lohmander S, Hascall VC (1982) Structures of N-linked and O-linked oligosaccharides on proteoglycan monomer isolated from the Swarm rat chondrosarcoma. J Biol Chem 257:10920-10927
130. Noonan DM, Fulle A, Valente P, Cai S, Horigan E, Sasaki M, Yamada Y, Hassell JR (1991) The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J Biol Chem 266:22939-22947
131. Oldberg A, Antonsson P, Lindblom K, Heinegard D (1989) A collagenbinding 59-kd protein (fibromodulin) is structurally related to the small interstitial proteoglycans PG-S1 and PG-S2 (decorin). EMBO J 8:2601-2604
132. Olin AI, Morgelin M, Sasaki T, Timpl R, Heinegard D, Aspberg A (2001) The proteoglycans aggrecan and Versican form networks withfibulin-2 through their lectin domain binding. J Biol Chem 276:1253-1261
133. Onnerfjord P, Heathfield TF, Heinegard D (2004) Identification of tyrosine sulfation in extracellular leucine-rich repeat proteins using mass spectrometry. J Biol Chem 279:26-33
134. Orgel JP, Eid A, Antipova O, Bella J, Scott JE (2009) Decorin core protein (decoron) shape complements collagenfibril surface structure and mediates its binding. PLoS One 4:e7028
135. Parsi MK, Adams JR, Whitelock J, Gibson MA (2010) LTBP-2 has multiple heparin/heparan sulfate binding sites. Matrix Biol 29:393-401
136. Plaas AH, Neame PJ, Nivens CM, Reiss L (1990) Identification of the keratan sulfate attachment sites on bovinefibromodulin. J Biol Chem 265:20634-20640
137. Rhee DK, Marcelino J, Al-Mayouf S, Schelling DK, Bartels CF, Cui Y, Laxer R, Goldbach-Mansky R, Warman ML (2005a) Consequences of disease-causing mutations on lubricin protein synthesis, secretion, and post-translational processing. J Biol Chem 280: 31325-31332
138. Rhee DK, Marcelino J, Baker M, Gong Y, Smits P, Lefebvre V, Jay GD, Stewart M, Wang H, Warman ML, Carpten JD (2005b) The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest 115:622-631
139. Ricciardelli C, Sakko AJ, Ween MP, Russell DL, Horsfall DJ (2009) The biological role and regulation of versican levels in cancer. Cancer Metastasis Rev 28:233-245
140. Roberts CR, Mort JS, Roughley PJ (1987) Treatment of cartilage proteoglycan aggregate with hydrogen peroxide. Relationship between observed degradation products and those that occur naturally during aging. Biochem J 247:349-357
141. Roberts S, Caterson B, Menage J, Evans EH, Jaffray DC, Eisenstein SM (2000) Matrix metalloproteinases and aggrecanase: their role in disorders of the human intervertebral disc. Spine (Phila Pa 1976) 25:3005-3013
142. Rossi M, Morita H, Sormunen R, Airenne S, Kreivi M, Wang L, Fukai N, Olsen BR, Tryggvason K, Soininen R (2003) Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J 22:236-245
143. Roughley PJ (2004) Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine (Phila Pa 1976) 29:2691-2699
144. Roughley PJ (2006) The structure and function of cartilage proteoglycans. Eur Cell Mater 12:92-101
145. Roughley PJ, White RJ (1980) Age-related changes in the structure of the proteoglycan subunits from human articular cartilage. J Biol Chem 255:217-224
146. Roughley PJ, White RJ (1989) Dermatan sulphate proteoglycans of human articular cartilage. The properties of dermatan sulphate proteoglycans I and II. Biochem J 262:823-827
147. Roughley PJ, White RJ, Cs-Szabo G, Mort JS (1996a) Changes with age in the structure offibromodulin in human articular cartilage. Osteoarthritis Cartilage 4:153-161
148. Roughley PJ, White RJ, Mort JS (1996b) Presence of pro-forms of decorin and biglycan in human articular cartilage. Biochem J 318(Pt 3):779-784
149. Roughley PJ, Melching LI, Heathfield TF, Pearce RH, Mort JS (2006) The structure and degradation of aggrecan in human intervertebral disc. Eur Spine J 15(Suppl 3):S326-S332
150. Sandy JD, Flannery CR, Boynton RE, Neame PJ (1990) Isolation and characterization of disulfide-bonded peptides from the three globular domains of aggregating cartilage proteoglycan. J Biol Chem 265:21108-21113
151. Sandy JD, Westling J, Kenagy RD, Iruela-Arispe ML, Verscharen C, Rodriguez-Mazaneque JC, Zimmermann DR, Lemire JM, Fischer JW, Wight TN, Clowes AW (2001) Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276:13372-13378
152. Schumacher BL, Block JA, Schmid TM, Aydelotte MB, Kuettner KE (1994) A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. Arch Biochem Biophys 311:144-152
153. Scott JE (1996) Proteodermatan and proteokeratan sulfate (decorin, lumican/fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagen. Biochemistry 35:8795-8799
154. Scott JE (2003) Elasticity in extracellular matrix 'shape modules' of tendon, cartilage, etc. A sliding proteoglycan-filament model. J Physiol 553:335-343
155. Scott JE, Stockwell RA (2006) Cartilage elasticity resides in shape module decoran and aggrecan sumps of dampingfluid: implications in osteoarthrosis. J Physiol 574:643-650
156. Scott IC, Imamura Y, Pappano WN, Troedel JM, Recklies AD, Roughley PJ, Greenspan DS (2000) Bone morphogenetic protein-1 processes probiglycan. J Biol Chem 275:30504-30511
157. Scott PG, McEwan PA, Dodd CM, Bergmann EM, Bishop PN, Bella J (2004) Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc Natl Acad Sci USA 101:15633-15638
158. Shen Z, Gantcheva S, Mansson B, Heinegard D, Sommarin Y (1998) Chondroadherin expression changes in skeletal development. Biochem J 330(Pt 1):549-557
159. Shi S, Ciurli C, Cartman A, Pidoux I, Poole AR, Zhang Y (2003) Experimental immunity to the G1 domain of the proteoglycan versican induces spondylitis and sacroiliitis, of a kind seen in human spondylarthropathies. Arthritis Rheum 48:2903-2915
160. Shi S, Grothe S, Zhang Y, O'Connor-McCourt MD, Poole AR, Roughley PJ, Mort JS (2004) Link protein has greater affinity for versican than aggrecan. J Biol Chem 279:12060-12066
161. Shine KM, Spector M (2008) The presence and distribution of lubricin in the caprine intervertebral disc. J Orthop Res 26:1398-1406
162. Shine KM, Simson JA, Spector M (2009) Lubricin distribution in the human intervertebral disc. J Bone Joint Surg Am 91:2205-2212
163. Sivan SS, Tsitron E, Wachtel E, Roughley PJ, Sakkee N, van der Ham F, DeGroot J, Roberts S, Maroudas A (2006) Aggrecan turnover in human intervertebral disc as determined by the racemization of aspartic acid. J Biol Chem 281:13009-13014
164. Smith SM, Whitelock JM, Iozzo RV, Little CB, Melrose J (2009) Topographical variation in the distributions of versican, aggrecan and perlecan in the foetal human spine reflects their diverse functional roles in spinal development. Histochem Cell Biol 132: 491-503
165. Smith SM, Shu C, Melrose J (2010) Comparative immunolocalisation of perlecan with collagen II and aggrecan in human foetal, newborn and adult ovine joint tissues demonstrates perlecan as an early developmental chondrogenic marker. Histochem Cell Biol 134:251-263
166. Song YQ, Cheung KM, Ho DW, Poon SC, Chiba K, Kawaguchi Y, Hirose Y, Alini M, Grad S, Yee AF, Leong JC, Luk KD, Yip SP, Karppinen J, Cheah KS, Sham P, Ikegawa S, Chan D (2008) Association of the asporin D14 allele with lumbar-disc degeneration in Asians. Am J Hum Genet 82:744-747
167. Spicer AP, Joo A, Bowling RA Jr (2003) A hyaluronan binding link protein gene family whose members are physically linked adjacent to chondroitin sulfate proteoglycan core protein genes: The missing links. J Biol Chem 278:21083-21091
168. Stallcup WB (2002) The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31:423-435
169. Superti-Furga A, Hastbacka J, Rossi A, van der Harten JJ, Wilcox WR, Cohn DH, Rimoin DL, Steinmann B, Lander ES, Gitzelmann R (1996) A family of chondrodysplasias caused by mutations in the diastrophic dysplasia sulfate transporter gene and associated with impaired sulfation of proteoglycans. Ann N Y Acad Sci 785:195-201
170. Svensson L, Aszodi A, Reinholt FP, Fassler R, Heinegard D, Oldberg A (1999) Fibromodulin-null mice have abnormal collagenfibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem 274:9636-9647
171. Svensson L, Narlid I, Oldberg A (2000) Fibromodulin and lumican bind to the same region on collagen type Ifibrils. FEBS Lett 470:178-182
172. Swann DA, Sotman S, Dixon M, Brooks C (1977) The isolation and partial characterization of the major glycoprotein (LGP-I) from the articular lubricating fraction from bovine synovialfluid. Biochem J 161:473-485
173. Swann DA, Hendren RB, Radin EL, Sotman SL, Duda EA (1981a) The lubricating activity of synovialfluid glycoproteins. Arthritis Rheum 24:22-30
174. Swann DA, Slayter HS, Silver FH (1981b) The molecular structure of lubricating glycoprotein-I, the boundary lubricant for articular cartilage. J Biol Chem 256:5921-5925
175. Sztrolovics R, Chen XN, Grover J, Roughley PJ, Korenberg JR (1994) Localization of the humanfibromodulin gene (FMOD) to chromosome 1q32 and completion of the cDNA sequence. Genomics 23:715-717
176. Sztrolovics R, Alini M, Roughley PJ, Mort JS (1997) Aggrecan degradation in human intervertebral disc and articular cartilage. Biochem J 326(Pt 1):235-241
177. Sztrolovics R, Grover J, Cs-Szabo G, Shi SL, Zhang Y, Mort JS, Roughley PJ (2002) The characterization of versican and its message in human articular cartilage and intervertebral disc. J Orthop Res 20:257-266
178. Tillgren V, Onnerfjord P, Haglund L, Heinegard D (2009) The tyrosine sulfate-rich domains of the LRR proteinsfibromodulin and osteoadherin bind motifs of basic clusters in a variety of heparinbinding proteins, including bioactive factors. J Biol Chem 284: 28543-28553
179. Tkachenko E, Rhodes JM, Simons M (2005) Syndecans: new kids on the signaling block. Circ Res 96:488-500
180. Tomoeda M, Yamada S, Shirai H, Ozawa Y, Yanagita M, Murakami S (2008) PLAP-1/asporin inhibits activation of BMP receptor via its leucine-rich repeat motif. Biochem Biophys Res Commun 371:191-196
181. Tompson SW, Merriman B, Funari VA, Fresquet M, Lachman RS, Rimoin DL, Nelson SF, Briggs MD, Cohn DH, Krakow D (2009) A recessive skeletal dysplasia, SEMD aggrecan type, results from a missense mutation affecting the C-type lectin domain of aggrecan. Am J Hum Genet 84:72-79
182. Tortorella MD, Liu RQ, Burn T, Newton RC, Arner E (2002) Characterization of human aggrecanase 2 (ADAM-TS5): substrate specificity studies and comparison with aggrecanase 1 (ADAM-TS4). Matrix Biol 21:499-511
183. Tsai TT, Danielson KG, Guttapalli A, Oguz E, Albert TJ, Shapiro IM, Risbud MV (2006) TonEBP/OREBP is a regulator of nucleus pulposus cell function and survival in the intervertebral disc. J Biol Chem 281:25416-25424
184. Turnbull JE (2010) Heparan sulfate glycomics: towards systems biology strategies. Biochem Soc Trans 38:1356-1360
185. Valhmu WB, Palmer GD, Rivers PA, Ebara S, Cheng JF, Fischer S, Ratcliffe A (1995) Structure of the human aggrecan gene: exonintron organization and association with the protein domains. Biochem J 309(Pt 2):535-542
186. Vehvilainen P, Hyytiainen M, Keski-Oja J (2009) Matrix association of latent TGF-beta binding protein-2 (LTBP-2) is dependent onfibrillin-1. J Cell Physiol 221:586-593
187. Vlodavsky I, Friedmann Y, Elkin M, Aingorn H, Atzmon R, Ishai-Michaeli R, Bitan M, Pappo O, Peretz T, Michal I, Spector L, Pecker I (1999) Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat Med 5:793-802
188. von Marschall Z, Fisher LW (2010) Decorin is processed by three isoforms of bone morphogenetic protein-1 (BMP1). Biochem Biophys Res Commun 391:1374-1378
189. Wang IJ, Chiang TH, Shih YF, Hsiao CK, Lu SC, Hou YC, Lin LL (2006) The association of single nucleotide polymorphisms in the 5 ¢-regulatory region of the lumican gene with susceptibility to high myopia in Taiwan. Mol Vis 12:852-857
190. Wang J, Markova D, Anderson DG, Zheng Z, Shapiro IM, Risbud MV (2011) TNF-alpha and IL-1beta promote a disintegrin-like and metalloprotease with thrombospondin type I motif-5-mediated aggrecan degradation through syndecan-4 in intervertebral disc. J Biol Chem 286:39738-39749
191. Watanabe H, Kimata K, Line S, Strong D, Gao LY, Kozak CA, Yamada Y (1994) Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat Genet 7:154-157
192. Watanabe H, Cheung SC, Itano N, Kimata K, Yamada Y (1997) Identification of hyaluronan-binding domains of aggrecan. J Biol Chem 272:28057-28065
193. Watanabe H, Yamada Y, Kimata K (1998) Roles of aggrecan, a large chondroitin sulfate proteoglycan, in cartilage structure and function. J Biochem 124:687-693
194. Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA (1996) The degradation of human endothelial cell-derived perlecan and release of bound basicfibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J Biol Chem 271:10079-10086
195. Whitelock JM, Melrose J, Iozzo RV (2008) Diverse cell signaling events modulated by perlecan. Biochemistry 47:11174-11183
196. Wiberg C, Heinegard D, Wenglen C, Timpl R, Morgelin M (2002) Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures. J Biol Chem 277:49120-49126
197. Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, Bonadio J, Boskey A, Heegaard AM, Sommer B, Satomura K, Dominguez P, Zhao C, Kulkarni AB, Robey PG, Young MF (1998) Targeted disruption of the biglycan gene leads to an osteoporosislike phenotype in mice. Nat Genet 20:78-82
198. Yamada S, Tomoeda M, Ozawa Y, Yoneda S, Terashima Y, Ikezawa K, Ikegawa S, Saito M, Toyosawa S, Murakami S (2007) PLAP-1/ asporin, a novel negative regulator of periodontal ligament mineralization. J Biol Chem 282:23070-23080
199. Yang BL, Yang BB, Erwin M, Ang LC, Finkelstein J, Yee AJ (2003) Versican G3 domain enhances cellular adhesion and proliferation of bovine intervertebral disc cells cultured in vitro. Life Sci 73:3399-3413
200. Young AA, Smith MM, Smith SM, Cake MA, Ghosh P, Read RA, Melrose J, Sonnabend DH, Roughley PJ, Little CB (2005) Regional assessment of articular cartilage gene expression and small proteoglycan metabolism in an animal model of osteoarthritis. Arthritis Res Ther 7:R852-R861
201. Zheng J, Luo W, Tanzer ML (1998) Aggrecan synthesis and secretion. A paradigm for molecular and cellular coordination of multiglobular protein folding and intracellular trafficking. J Biol Chem 273:12999-13006
202. Zimmermann DR, Ruoslahti E (1989) Multiple domains of the largefibroblast proteoglycan, versican. EMBO J 8:2975-2981