Chondroitin sulphate sulphation motif expression in the ontogeny of the intervertebral disc

European Cells and Materials

Volumn 21, Issue , 2011, Pages 1-14

  Hayes, A J ^a   Hughes, C E ^a   Ralphs, J R ^a   Caterson, B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Ageing; Chondroitin sulphate; Development; Differentiation; Growth; Growth plate; Intervertebral disc; Sulphation motif; Vertebral body

Indexed keywords

CHONDROITIN SULFATE; EPITOPE; PROTEOGLYCAN;

AGED; AGING; ANIMAL TISSUE; ANNULUS PULPOSUS; ARTICLE; CARTILAGE CELL; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; EXTRACELLULAR MATRIX; GROWTH; GROWTH PLATE; HISTOGENESIS; INTERVERTEBRAL DISK; NONHUMAN; NOTOCHORD; NUCLEUS PULPOSUS; PERICHONDRIUM; RAT; SULFATION; TISSUE DIFFERENTIATION; VERTEBRA BODY;

EID: 79551516146     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v021a01     Document Type: Article

References (59)

1. Alliston T (2010) Chondroitin sulphate and growth factor signalling in the skeleton: possible links to MPS VI. J Pediatr Rehabil Med 3: 129-138.
2. Aszodi A, Chan D, Hunziker E, Bateman JF, Fässler, R (1988) Collagen II is essential for the removal of the notochord and the formation of intervertebral discs. J Cell Biol 143: 1399-1412.
3. Benjamin M, Ralphs JR (1999) The tendon/ligamentbone junction. In "Biology of the Synovial Joint" (Archer CW, Benjamin M, Caterson B Ralphs JR, eds) Harwood Academic Publishers, Taylor and Francis, Abingdon, UK, pp 361-373.
4. Bogduk N (2005) Clinical anatomy of the lumbar spine and sacrum. 4th ed. Churchill Livingstone, London.
5. Bowman K, Bertozzi CB (1999) Carbohydrate sulfotransferases: mediators of extra cellular communication. Chem Biol 6: 9-22.
6. Campbell SC, Schwartz NB (1988) Kinetics of intracellular processing of chondroitin sulphate proteoglycan core protein and other matrix components. J Cell Biol 106: 2191-2202.
7. 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: 411-417.
8. Cortes M., Baria AT, Schwartz NB (2009) Sulfation of chondroitin sulphate proteoglycans is necessary for proper Indian hedgehog signalling in the developing growth plate. Development 136: 1697-1706.
9. Couchman JR (2010) Transmembrane signalling proteoglycans. Ann Rev Cell Dev Biol, in press.
10. Deepa SS, Umehara Y, Higashiyama S, Itoh N and Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulphate E with various heparinbinding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277: 43707-43716.
11. Dziewiatkowski, D.D (1962) Intracellular synthesis of chondroitin sulphate. Cell Biol 13: 359-364.
12. Gandhi NS, Mancera RL (2008) The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des 72: 455-482.
13. Gibson G, Lin DL, Caterson B, Foster B (1996) Type X collagen is colocalised with a proteoglycan epitope to form distinct morphological structures in bovine growth cartilage. Bone 19: 307-315.
14. Götz W, Barnert S, Bertagnoli R, Miosge N, Kresse H, Herken R (1997) Immunohistochemical localisation of the small proteoglycans decorin and biglycan in human intervertebral discs. Cell Tissue Res 289: 185-190.
15. Gualeni B, Facchini M, De Leonardis F, Tenni R, Cetta G, Viola M, Passi A, Superti-Furga A, Forlino A, Rossi A (2010) Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling. Matrix Biol, in press.
16. Handel TM, Johnson Z, Crown SE, Lau ES, Sweeney M, Proudfoot AE (2005) Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu Rev Biochem 74: 385-410.
17. Hardingham T (1994) The sulphation pattern in chondroitin sulphate chains investigated by chondroitinase ABC and ACII digestion and reactivity with monoclonal antibodies. Carbohydrate Res 255: 241-254.
18. Hayes AJ, Benjamin JR, Ralphs JR. (2001) Extracellular matrix in development of the intervertebral disc. Matrix Biol 20: 107-121.
19. Hayes AJ, Tudor D, Nowell MA, Caterson B and Hughes CE (2008) Chondroitin sulphate sulfation motifs as putative biomarkers for isolation of articular cartilage progenitor cells. J Histochem Cytochem 56: 125-138.
20. Inkinen RI, Lammi MJ, Lehmonen S, Puustjärvi K, Kääpä E and Tammi MI (1998) Relative increase of biglycan and decorin and altered chondroitin sulphate epitopes in the degenerating human intervertebral disc. J Rheumatol 25: 506-514.
21. Johnson WEB, Eisenstein SM, Roberts S (2001) Cell cluster formation in degenerate lumbar intervertebral discs is associated with increased cell proliferation. Conn Tiss Res 42:197-207.
22. Kamiya N, Watanabe H, Habuchi H, Takagi H, Shinomura T, Shimizu K, Kimata K (2006) Versican/PGM regulates chondrogenesis as an extracellular matrix molecule crucial for mesenchymal condensation. J Biol Chem 281: 2390-2400.
23. Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K, and Miyasaka M (2002) Oversulfated chondroitin/dermatan sulfates containing GlcAβ1/IdoAα1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J Biol Chem 277: 12921-12930.
24. Kirsch T, Koyama E, Liu M, Golub EE, Pacifici M (2002) Syndecan-3 is a selective regulator of chondrocyte proliferation. J Biol Chem 277: 42171-42177.
25. Klüppel M, Wight TN, Chan C, Hinek A, Wrana JL (2005) Maintenance of chondroitin sulphation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132: 3989-4003.
26. Kosher RA (1998) Syndecan-3 in limb skeletal development. Microsc Res. Techn 43: 123-130.
27. Kronenberg HM (2007) The role of the perichondrium in fetal bone development. Ann NY Acad Sci 1116: 59-64.
28. Mark MP, Butler WT, Ruch JV (1989) Transient expression of a chondroitin sulfate-related epitope during cartilage histomorphogenesis in the axial skeleton of fetal rats. Dev Biol 133: 475-488.
29. Mark MP, Baker JR, Kimata K, Ruch JV (1990) Regulated changes in chondroitin sulfation during embryogenesis: an immunohistochemical approach. Int J Dev Biol 24: 191-204.
30. Melrose J, Smith S, Ghosh P (2000) Differential expression of proteoglycan epitopes by ovine intervertebral disc cells. J Anat 197: 189-198.
31. Melrose J, Smith S, Ghosh P, Whitelock J (2003) Perlecan, the multidomain heparin sulphate proteoglycan of basement membranes, is also a prominent components of the cartilaginous primordial in the developing human foetal spine. J Histochem Cytochem 51:1331-1341.
32. Melrose J, Hayes AJ, Whitelock JM, Little CB (2008) Perlecan, the "jack of all trades" proteoglycan of cartilaginous weight-bearing connective tissues. Bioessays 30: 457-469.
33. Merry CLR, Astrautsove SA (2008) Glycans in evolution and development. Workshop on glycoscience and development. EMBO Rep 9: 716-622.
34. Milz S, Aktas T, Putz R Benjamin M (2006) Expression of extracellular matrix molecules typical of articular cartilage in the human scapholunate interosseous ligament. J Anat 208: 671-679.
35. Nandini CD, Mikami T, Ohta M, Itoh N, Akiyama-Nambu F, Sugahara K (2004) Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J Biol Chem 279: 50799-50809.
36. Peacock A (1951a) Observations on the pre-natal development of the intervertebral disc in man. J Anat 85: 260-274.
37. Peacock A (1951b) Observations on the post-natal structure of the intervertebral disc in man. J Anat 86: 162-179.
38. Pelton RW, Dickinson ME, Moses HL, Hogan BLM (1990) In situ hybridisation analysis of TGFβ3 RNA expression during mouse development: comparative studies with TGFβ1 and β2. Development. 110: 609-620.
39. Raman R, Sasisekharan V, Sassisekharan R (2005) Structural insights into biological roles of proteinglycosaminoglycan interactions. Chem Biol 12: 267-277.
40. Risbud MV, Schaer TP, Shapiro IM (2010) Toward an understanding of the role of notochordal cells in the adult intervertebral disc: from discord to accord. Dev Dyn 239: 2141-2148.
41. Roberts S, Caterson B, Evans H, Eisenstein SM (1994) Proteoglycan components of the intervertebral disc and cartilage endplate: an immunolocalisation study of animal and human tissues. Histochem J 26: 402-411.
42. Rufai A, Benjamin M, Ralphs JR (1995) The development of fibrocartilage in the rat intervertebral disc. Anat Embryol 192: 53-62.
43. Sasisekharen R, Raman R, Prabhakar V (2006) Glycomics approach to structure-function relationships of glycosaminoglycans. Annu Rev Biomed Eng 8: 181-231.
44. Schmid P, Cox D, Bilbe, G, Maier R, McMaster GK (1991) Differential expression of TGFβ1, β2 and β3 genes during mouse embryogenesis. Development. 111: 117-130.
45. Sharp CA, Roberts S, Evans H, Brown SJ (2009) Disc cell clusters in pathological human intervertebral discs are associated with increased stress protein immunolabelling. Eur Spine J 18: 1587-1594.
46. Shimazu A, Nah HD, Kirsch T, Koyama E, Leatherman JL, Golden EB, Kosher RA Pacifici M (1996) Syndecan-3 and the control of chondrocyte proliferation during endochondral ossification. Exp Cell Res 229: 126-136.
47. Shimo T, Gentili C, Iwamoto M, Wu C, Koyama E, Pacifici M (2004) Indian hedgehog and syndecan-3 coregulate chondrocyte proliferation and function during chick limb skeletogenesis. Dev Dyn 229: 607-617.
48. Smith SM, West LA, Govindraj P, Zhang X, Ornitz DM, Hassell JR (2007) Heparan and chondroitin sulphate on growth plate perlecan mediate binding and delivery of FGF-2 to FGF receptors. Matrix Biol 26: 175-184.
49. Sorrell JM, Caterson B (1989) Detection of age-related changes in the distribution of keratan sulfates and chondroitin sulfates in developing chick limbs: an immunocytochemical study. Development 106: 657-663.
50. Sorrell JM, Lintala AM, Mahmoodian F, Caterson B (1988) Epitope-specific changes in chondroitin sulphate/dermatan sulphate proteoglycans as markers in the lymphopoietic and granulopoietic compartments of developing bursae of Fabricius. J Immunol 140: 4263-4270.
51. Sorrell JM, Mahmoodian F, Schafer IA, Davis B, Caterson B (1990) Identification of monoclonal antibodies that recognize novel epitopes in native chondroitin/dermatan sulphate glycosaminoglycan chains: their use in mapping functionally distinct domains of human skin. J Histochem Cytochem 38: 393-402.
52. Sorrell JM, Carrino DA, Caplan AI (1996) Regulated expression of chondroitin sulfates at sites of epithelialmesenchymal interaction: spatio-temporal patterning identified with anti-chondroitin sulphate monoclonal antibodies. Int J Devel Neurosci 14: 233-248.
53. Thorp FK, Dorfman A (1963) The occurrence of intracellular chondroitin sulphate. J Cell Biol 18: 13-17.
54. Tiedemann K, Olander B, Eklund E, Todorova L, Bengtsson M, Maccarana M, Westergren-Thorsson G, Malmström A (2005) Regulation of the chondroitin/dermatan fine structure by transforming growth factor-β1 through effects on polymer-modifying enzymes. Glycobiology 15: 1277-1285.
55. Tolonen J, Grönblad M, Vanharanta H, Virri J, Guyer RD, Rytömaa T, Karaharju EO (2006) Growth factor expression in degenerated intervertebral disc tissue. An immunohistochemical analysis of transforming growth factor beta, fibroblast growth factor and platelet-derived growth factor. Eur Spine J 15: 588-596.
56. Urban J., Maroudas A (1980) The chemistry of the intervertebral disc in relation to its physiological function. Clin Rheum Dis 6: 51-76.
57. Visco DM, Johnstone B, Hill MA, Jolly GA, Caterson B (1993) Immunohistochemical analysis of 3-B-3(-) and 7-D-4 epitope expression in canine osteoarthritis. Arthritis Rheum 36: 1718-1725.
58. Walmsley R (1953) The development and growth of the intervertebral disc. Edinburgh Med J 60: 341-364.
59. Watanabe H, Yamada Y, Kimata K (1998) Roles of aggrecan, a large chondroitin sulphate proteoglycan, in cartilage structure and function. J Biochem 124: 687-693.