Regulation of UDP-glucose dehydrogenase is sufficient to modulate hyaluronan production and release, control sulfated GAG synthesis, and promote chondrogenesis

Journal of Cellular Physiology

Volumn 226, Issue 3, 2011, Pages 749-761

  Clarkin, Claire E ^a   Allen, Steve ^a   Kuiper, Nikki J ^b   Wheeler, Benjamin T ^a   Wheeler Jones, Caroline P ^a   Pitsillides, Andrew A ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b KEELE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; GLYCOSAMINOGLYCAN; HYALURONIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE EXTRACELLULAR SIGNAL REGULATED KINASE KINASE; PHOSPHOTRANSFERASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE;

ARTICLE; BONE MARROW; CARTILAGE; CHICK; CHONDROGENESIS; EMBRYO; ENZYME INHIBITION; ENZYME REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; SULFATION; SYNTHESIS;

ANIMALS; CHICKENS; CHONDROGENESIS; CHONDROITIN SULFATES; ELECTROPHORESIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSAMINOGLYCANS; HYALURONIC ACID; JOINTS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE;

EID: 78650656657     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22393     Document Type: Article

References (55)

1. Ab-Rahim S, Selvaratnam L, Kamarul T. 2008. The effect of TGF-beta1 and beta-estradiol on glycosaminoglycan and type II collagen distribution in articular chondrocyte cultures. Cell Biol Int 32: 841-847.
2. Alexopoulos LG, Williams GM, Upton ML, Setton LA, Guilak F. 2005. Osteoarthritic changes in the biphasic mechanical properties of the chondrocyte pericellular matrix in articular cartilage. J Biomech 38: 509-517.
3. Alexopoulos LG, Youn I, Bonaldo P, Guilak F. 2009. Developmental and osteoarthritic changes in Col6a1-knockout mice: Biomechanics of type VI collagen in the cartilage pericellular matrix. Arthritis Rheum 60: 771-779.
4. Bain J, Plater L, Elliott M, Shpiro N, Hastie JC, Mclauchlan H, Klevernic I, Arthur JSC, Alessi DR, Cohen P. 2007. The selectivity of protein kinase inhibitors: A further update. Biochem J 403: 297-315.
5. Bastow ER, Lamb KJ, Lewthwaite JC, Osborne AC, Kavanagh E, Wheeler-Jones CPD, Pitsillides AA. 2005. Selective activation of the MEK-ERK pathway is regulated by mechanical stimuli in forming joints and promotes pericellular matrix formation. J Biol Chem 280: 11749-11758.
6. Bayliss MT, Ali SY. 1978. Age-related changes in the composition and structure of human articular-cartilage proteoglycans. Biochem J 176: 683-693.
7. Beauchef G, Kypriotou M, Chadjichristos C, Widom RL, Porée B, Renard E, Moslemi S, Wegrowski Y, Maquart F-X, Pujol J-P, Galéra P. 2005. c-Krox down-regulates the expression of UDP-glucose dehydrogenase in chondrocytes. Biochem Biophys Res Comm 333: 1123-1131.
8. Bobick BE, Kulyk WM. 2008. Regulation of cartilage formation and maturation by mitogen-activated protein kinase signaling. Birth Defect Res Part C Embryo Today Rev 84: 131-154.
9. Bontemps Y, Vuillermoz B, Antonicelli F, Perreau C, Danan J-L, Maquart F-X, Wegrowski Y. 2003. Specific protein-1 Is a universal regulator of UDP-glucose dehydrogenase expression: Its positive involvement in transforming growth factor {beta} signalling and inhibition in hypoxia. J Biol Chem 278: 21566-21575.
10. Calabro A, Benavides M, Tammi M, Hascall VC, Midura RJ. 2000a. Microanalysis of enzyme digests of hyaluronan and chondroitin/dermatan sulfate by fluorophore-assisted carbohydrate electrophoresis (FACE). Glycobiology 10: 273-281.
11. Calabro A, Hascall VC, Midura RJ. 2000b. Adaptation of FACE methodology for microanalysis of total hyaluronan and chondroitin sulfate composition from cartilage. Glycobiology 10: 283-293.
12. Calabro A, Midura R, Wang A, West L, Plaas A, Hascall VC. 2001. Fluorophore-assisted carbohydrate electrophoresis (FACE) of glycosaminoglycans. Osteoarthritis Cartilage 9: S16-S22.
13. De Luca G, Castellani A. 1984. Regulatory aspects of glycosaminoglycan biosynthesis. Acta Biol Hung 35: 109-121.
14. Dowthwaite GP, Ward AC, Flannely J, Suswillo RFL, Flannery CR, Archer CW, Pitsillides AA. 1999. The effect of mechanical strain on hyaluronan metabolism in embryonic fibrocartilage cells. Matrix Biol 18: 523-532.
15. Ferrari D, Kosher RA. 2002. Dlx5 is a positive regulator of chondrocyte differentiation during endochondral ossification. Dev Biol 252: 257-270.
16. Ferrari D, Lichtler AC, Pan Z, Dealy CN, Upholt WB, Kosher RA. 1998. Ectopic expression of Msx-2 in posterior limb bud mesoderm impairs limb morphogenesis while inducing BMP-4 expression, inhibiting cell proliferation, and promoting apoptosis. Dev Biol 197: 12-24.
17. Fisher MC, Li Y, Seghatoleslami MR, Dealy CN, Kosher RA. 2006. Heparan sulfate proteoglycans including syndecan-3 modulate BMP activity during limb cartilage differentiation. Matrix Biol 25: 27-39.
18. Fosang AJ, Hey NJ, Carney SL, Hardingham TE. 1990. An ELISA plate-based assay for hyaluronan using biotinylated proteoglycan G1 domain (HA-binding region). Matrix 10: 306-313.
19. García-García MJ, Anderson KV. 2003. Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation. Cell 114: 727-737.
20. Gay SW, Kosher RA. 1984. Uniform cartilage differentiation in micromass cultures prepared from a relatively homogeneous population of chondrogenic progenitor cells of the chick limb bud: Effect of prostaglandins. J Exp Zool 232: 317-326.
21. Ginsburg V, Weissbach A, Maxwell ES. 1958. Formation of glucuronic acid from uridinediphosphate glucuronic acid. Biochim Biophys Acta 28: 649-650.
22. Grande-Allen KJ, Griffin BP, Ratliff NB, Cosgrove DM, Vesely I. 2003. Glycosaminoglycan profiles of myxomatous mitral leaflets and chordae parallel the severity of mechanical alterations. J Am Col Cardiol 42: 271-277.
23. Guilak F, Alexopoulos LG, Upton ML, Youn I, Choi JB, Cao L, Setton LA, Haider MA. 2006. The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Ann NY Acad Sci 1068: 498-512.
24. Guo N, Kanter D, Funderburgh ML, Mann MM, Du Y, Funderburgh JL. 2007. A Rapid transient increase in hyaluronan synthase-2 mRNA initiates secretion of hyaluronan by corneal keratocytes in response to transforming growth factor beta. J Biol Chem 282: 12475-12483.
25. Hacker U, Lin X, Perrimon N. 1997. The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development 124: 3565-3573.
26. Hardingham T, Bayliss M. 1990. Proteoglycans of articular cartilage: Changes in aging and in joint disease. Semin Arthritis Rheum 20: 12-33.
27. Hickery MS, Bayliss MT, Dudhia J, Lewthwaite JC, Edwards JCW, Pitsillides AA. 2003. Age-related changes in the response of human articular cartilage to IL-1 alpha and transforming growth factor beta (TGF-beta): Chondrocytes exhibit diminished sensitivity to TGF-beta. J Biol Chem 278: 53063-53071.
28. Hwang H-Y, Robert Horvitz H. 2002. The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated. Proc Natl Acad Sci USA 99: 14224-14229.
29. Hwang H-Y, Olson SK, Esko JD, Robert Horvitz H. 2003. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 423: 439-443.
30. Karousou EG, Militsopoulou M, Porta G, De Luca G, Hascall VC, Passi A. 2004. Polyacrylamide gel electrophoresis of fluorophore-labeled hyaluronan and chondroitin sulfate disaccharides: Application to the analysis in cells and tissues. Electrophoresis 25: 2919-2925.
31. Kavanagh E, Church VL, Osborne AC, Lamb KJ, Archer C, Francis-West PH, Pitsillides AA. 2006. Differential regulation of GDF-5 and FGF-2/4 by immobilisation in ovo exposes distinct roles in joint formation. Dev Dyn 235: 826-834.
32. Kosher RA, Savage MP. 1981. Glycosaminoglycan synthesis by the apical ectodermal ridge of chick limb bud. Nature 291: 231-232.
33. Lewthwaite JC, Bastow ER, Lamb KJ, Blenis J, Wheeler-Jones CPD, Pitsillides AA. 2006. A specific mechanomodulatory role for p38 MAPK in embryonic joint articular surface cell MEK-ERK pathway regulation. J Biol Chem 281: 11011-11018.
34. Li Y, Toole BP, Dealy CN, Kosher RA. 2007. Hyaluronan in limb morphogenesis. Dev Biol 305: 411-420.
35. Lorenzo P, Bayliss MT, Heinegård D. 2004. Altered patterns and synthesis of extracellular matrix macromolecules in early osteoarthritis. Matrix Biol 23: 381-391.
36. Maleski MP, Knudson CB. 1996. Hyaluronan-mediated aggregation of limb bud mesenchyme and mesenchymal condensation during chondrogenesis. Exp Cell Res 225: 55-66.
37. Maneix L, Beauchef G, Servent A, Wegrowski Y, Maquart FX, Boujrad N, Flouriot G, Pujol JP, Boumediene K, Galera P, Moslemi S. 2008. 17-beta-Oestradiol up-regulates the expression of a functional UDP-glucose dehydrogenase in articular chondrocytes: Comparison with effects of cytokines and growth factors. Rheumatology 47: 281-288.
38. Meran S, Thomas DW, Stephens P, Enoch S, Martin J, Steadman R, Phillips AO. 2008. Hyaluronan facilitates transforming growth factor-beta1-mediated fibroblast proliferation. J Biol Chem 283: 6530-6545.
39. Müller G, Hanschke M. 1996. Quantitative and qualitative analyses of proteoglycans in cartilage extracts by precipitation with 1, 9-dimethylmethylene blue. Connect Tissue Res 33: 243-248.
40. Ogihara Y, Suda N, Hammond VE, Senior PV, Beck F, Yanagishita M. 2001. Biosynthesis of proteoglycan in bone and cartilage of parathyroid hormone-related protein knockout mice. J Bone Miner Metab 19: 4-12.
41. Oh C-D, Chang S-H, Yoon Y-M, Lee S-J, Lee Y-S, Kang S-S, Chun J-S. 2000. Opposing role of mitogen-activated protein kinase subtypes, Erk-1/2 and p38, in the regulation of chondrogenesis of mesenchymes. J Biol Chem 275: 5613-5619.
42. Pitsillides AA, Will RK, Bayliss MT, Edwards JCW. 1994. Circulating and synovial fluid hyaluronan levels. Effects of intra articular corticosteroid on the concentration and the rate of turnover. Arthrit Rheum 37: 1030-1038.
43. Pitsillides A, Archer C, Prehm P, Bayliss M, Edwards J. 1995. Alterations in hyaluronan synthesis during developing joint cavitation. J Histochem Cytochem 43: 263-273.
44. Plaas AHK, Wong-Palms S, Roughley PJ, Midura RJ, Hascall VC. 1997. Chemical and immunological assay of the non reducing terminal residues of chondroitin sulfate from human aggrecan. J Biol Chem 272: 20603-20610.
45. Roughley P, White R. 1980. Age-related changes in the structure of the proteoglycan subunits from human articular cartilage. J Biol Chem 255: 217-224.
46. Sharma A.L.D.W, Richardson JB, Roberts S, Kuiper N.J. 2007. Glycosaminoglycan profiles of repair tissue formed following autologous chondrocyte implantation differ from control cartilage. Arthritis Res Ther 9: R79.
47. Stuhlmeier KM, Pollaschek C. 2004. Differential effect of transforming growth factor beta (TGF-beta) on the genes encoding hyaluronan synthases and utilization of the p38 MAPK pathway in TGF-beta-induced hyaluronan synthase 1 activation. J Biol Chem 279: 8753-8760.
48. Syeda F, Grosjean J, Houliston RA, Keogh RJ, Carter TD, Paleolog E, Wheeler-Jones CPD. 2006. Cyclooxygenase-2 induction and prostacyclin release by protease-activated receptors in endothelial cells require cooperation between mitogen-activated protein kinase and NF-kappa B pathways. J Biol Chem 281: 11792-11804.
49. Varon C, Ezan J, Reuzeau E, Basoni C, Kramer I. 2008. TGFbeta1 regulates endothelial cell spreading and hypertrophy through a Rac-p38-mediated pathway. Biol Cell 100: 537-550.
50. Vigetti D, Ori M, Viola M, Genasetti A, Karousou E, Rizzi M, Pallotti F, Nardi I, Hascall VC, De Luca G, Passi A. 2006. Molecular cloning and characterization of UDP-glucose dehydrogenase from the amphibian Xenopus laevis and its involvement in hyaluronan synthesis. J Biol Chem 281: 8254-8263.
51. Walsh EC, Stainier DYR. 2001. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293: 1670-1673.
52. Wang QG, El Haj AJ, Kuiper NJ. 2008. Glycosaminoglycans in the pericellular matrix of chondrons and chondrocytes. J Anat 213: 266-273.
53. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. 2008. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell 31: 918-924.
54. Yoshida S, Nagase M, Shibata S, Fujita T. 2008. Podocyte injury induced by albumin overload in vivo and in vitro: Involvement of TGF-beta and p38 MAPK. Nephron Exp Nephrol 108: 57-68.
55. Yu L, Hébert MC, Zhang YE. 2002. TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO 21: 3749-3759.