Inhibition of Gsk3β in cartilage induces osteoarthritic features through activation of the canonical Wnt signaling pathway

Osteoarthritis and Cartilage

Volumn 19, Issue 11, 2011, Pages 1363-1372

  Miclea, R L ^a   Siebelt, M ^b   Finos, L ^a   Goeman, J J ^a   Lowik C W G M ^a   Oostdijk, W ^a   Weinans, H ^b   Wit, J M ^a   Robanus Maandag, E C ^a   Karperien, M ^c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Cartilage degradation; Chondrocyte; Gsk3 ; Metalloproteinase; Wnt

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOSAMINOGLYCAN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; EX VIVO STUDY; IN VIVO STUDY; MALE; METATARSAL BONE; MOUSE; NONHUMAN; OSTEOARTHRITIS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; BIOLOGICAL MARKERS; CARTILAGE, ARTICULAR; CHONDROCYTES; EXTRACELLULAR MATRIX; GLYCOGEN SYNTHASE KINASE 3; GLYCOSAMINOGLYCANS; HINDLIMB; MICE; PEPTIDE HYDROLASES; PROTEIN ARRAY ANALYSIS; RATS; WNT SIGNALING PATHWAY;

EID: 80053654387     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2011.07.014     Document Type: Article

References (43)

1. Pacifici M., Koyama E., Iwamoto M. Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res C Embryo Today 2005, 75(3):237-248.
2. Aigner T., Zien A., Gehrsitz A., Gebhard P.M., McKenna L. Anabolic and catabolic gene expression pattern analysis in normal versus osteoarthritic cartilage using complementary DNA-array technology. Arthritis Rheum 2001, 44(12):2777-2789.
3. Zhu M., Chen M., Zuscik M., Wu Q., Wang Y.J., Rosier R.N., et al. Inhibition of beta-catenin signaling in articular chondrocytes results in articular cartilage destruction. Arthritis Rheum 2008, 58(7):2053-2064.
4. Zhu M., Tang D., Wu Q., Hao S., Chen M., Xie C., et al. Activation of beta-catenin signaling in articular chondrocytes leads to osteoarthritis-like phenotype in adult beta-catenin conditional activation mice. J Bone Miner Res 2009, 24(1):12-21.
5. Miclea R.L., Karperien M., Bosch C.A., van der Horst.G., van der Valk M.A., Kobayashi T., et al. Adenomatous polyposis coli-mediated control of beta-catenin is essential for both chondrogenic and osteogenic differentiation of skeletal precursors. BMC Dev Biol 2009, 9(1):26.
6. Chun J.S., Oh H., Yang S., Park M. Wnt signaling in cartilage development and degeneration. BMB Rep 2008, 41(7):485-494.
7. Doble B.W., Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003, 116(Pt 7):1175-1186.
8. Kapadia R.M., Guntur A.R., Reinhold M.I., Naski M.C. Glycogen synthase kinase 3 controls endochondral bone development: contribution of fibroblast growth factor 18. Dev Biol 2005, 285(2):496-507.
9. Engler T.A., Henry J.R., Malhotra S., Cunningham B., Furness K., Brozinick J., et al. Substituted 3-imidazo[1,2-a]pyridin-3-yl- 4-(1,2,3,4-tetrahydro-[1,4]diazepino-[6,7,1-hi]indol-7-yl)pyrrole-2,5-diones as highly selective and potent inhibitors of glycogen synthase kinase-3. J Med Chem 2004, 47(16):3934-3937.
10. van der Horst G., van der Werf S.M., Farih-Sips H., van Bezooijen R.L., Lowik C.W., Karperien M. Downregulation of Wnt signaling by increased expression of Dickkopf-1 and -2 is a prerequisite for late-stage osteoblast differentiation of KS483 cells. J Bone Miner Res 2005, 20(10):1867-1877.
11. Smink J.J., Buchholz I.M., Hamers N., van Tilburg C.M., Christis C., Sakkers R.J., et al. Short-term glucocorticoid treatment of piglets causes changes in growth plate morphology and angiogenesis. Osteoarthritis Cartilage 2003, 11(12):864-871.
12. Hoogendam J., Parlevliet E., Miclea R., Lowik C.W., Wit J.M., Karperien M. Novel early target genes of parathyroid hormone-related peptide in chondrocytes. Endocrinology 2006, 147(6):3141-3152.
13. Jonnalagadda S., Srinivasan R. Principal components analysis based methodology to identify differentially expressed genes in time-course microarray data. BMC Bioinformatics 2008, 9:267.
14. Huang d.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
15. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4(5):3.
16. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 2000, 25(1):25-29.
17. Palmer A.W., Guldberg R.E., Levenston M.E. Analysis of cartilage matrix fixed charge density and three-dimensional morphology via contrast-enhanced microcomputed tomography. Proc Natl Acad Sci U S A 2006, 103(51):19255-19260.
18. Cai Y., Mohseny A.B., Karperien M., Hogendoorn P.C., Zhou G., Cleton-Jansen A.M. Inactive Wnt/beta-catenin pathway in conventional high-grade osteosarcoma. J Pathol 2010, 220(1):24-33.
19. Mushtaq T., Bijman P., Ahmed S.F., Farquharson C. Insulin-like growth factor-I augments chondrocyte hypertrophy and reverses glucocorticoid-mediated growth retardation in fetal mice metatarsal cultures. Endocrinology 2004, 145(5):2478-2486.
20. Wu Q., Huang J.H., Sampson E.R., Kim K.O., Zuscik M.J., O'Keefe R.J., et al. Smurf2 induces degradation of GSK-3beta and upregulates beta-catenin in chondrocytes: a potential mechanism for Smurf2-induced degeneration of articular cartilage. Exp Cell Res 2009, 315(14):2386-2398.
21. Choi Y.A., Kang S.S., Jin E.J. BMP-2 treatment of C3H10T1/2 mesenchymal cells blocks MMP-9 activity during chondrocyte commitment. Cell Biol Int 2009, 33(8):887-892.
22. Takenaka K., Kise Y., Miki H. GSK3beta positively regulates Hedgehog signaling through Sufu in mammalian cells. Biochem Biophys Res Commun 2007, 353(2):501-508.
23. Katoh M., Katoh M. Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 2006, 5(9):1059-1064.
24. Day T.F., Yang Y. Wnt and hedgehog signaling pathways in bone development. J Bone Joint Surg Am 2008, 90(Suppl 1):19-24.
25. Ornitz D.M. FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev 2005, 16(2):205-213.
26. Mercader N., Fischer S., Neumann C.J. Prdm1 acts downstream of a sequential RA, Wnt and Fgf signaling cascade during zebrafish forelimb induction. Development 2006, 133(15):2805-2815.
27. ten Berge D., Brugmann S.A., Helms J.A., Nusse R. Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development. Development 2008, 135(19):3247-3257.
28. Rousset R., Mack J.A., Wharton K.A., Axelrod J.D., Cadigan K.M., Fish M.P., et al. Naked cuticle targets dishevelled to antagonize Wnt signal transduction. Genes Dev 2001, 15(6):658-671.
29. Jukkola T., Sinjushina N., Partanen J. Drapc1 expression during mouse embryonic development. Gene Expr Patterns 2004, 4(6):755-762.
30. Zeng W., Wharton K.A., Mack J.A., Wang K., Gadbaw M., Suyama K., et al. Naked cuticle encodes an inducible antagonist of Wnt signalling. Nature 2000, 403(6771):789-795.
31. Moon R.T., Bowerman B., Boutros M., Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science 2002, 296(5573):1644-1646.
32. Jho E.H., Zhang T., Domon C., Joo C.K., Freund J.N., Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002, 22(4):1172-1183.
33. Sandell L.J., Aigner T. Articular cartilage and changes in arthritis. An introduction: cell biology of osteoarthritis. Arthritis Res 2001, 3(2):107-113.
34. Mohtai M., Smith R.L., Schurman D.J., Tsuji Y., Torti F.M., Hutchinson N.I., et al. Expression of 92-kD type IV collagenase/gelatinase (gelatinase B) in osteoarthritic cartilage and its induction in normal human articular cartilage by interleukin 1. J Clin Invest 1993, 92(1):179-185.
35. Pfander D., Cramer T., Weseloh G., Pullig O., Schuppan D., Bauer M., et al. Hepatocyte growth factor in human osteoarthritic cartilage. Osteoarthritis Cartilage 1999, 7(6):548-559.
36. Tsuchiya A., Yano M., Tocharus J., Kojima H., Fukumoto M., Kawaichi M., et al. Expression of mouse HtrA1 serine protease in normal bone and cartilage and its upregulation in joint cartilage damaged by experimental arthritis. Bone 2005, 37(3):323-336.
37. Meng J., Ma X., Ma D., Xu C. Microarray analysis of differential gene expression in temporomandibular joint condylar cartilage after experimentally induced osteoarthritis. Osteoarthritis Cartilage 2005, 13(12):1115-1125.
38. Velasco J., Zarrabeitia M.T., Prieto J.R., Perez-Castrillon J.L., Perez-Aguilar M.D., Perez-Nunez M.I., et al. Wnt pathway genes in osteoporosis and osteoarthritis: differential expression and genetic association study. Osteoporos Int 2009.
39. Hu S.I., Carozza M., Klein M., Nantermet P., Luk D., Crowl R.M. Human HtrA, an evolutionarily conserved serine protease identified as a differentially expressed gene product in osteoarthritic cartilage. J Biol Chem 1998, 273(51):34406-34412.
40. Dankbar B., Neugebauer K., Wunrau C., Tibesku C.O., Skwara A., Pap T., et al. Hepatocyte growth factor induction of macrophage chemoattractant protein-1 and osteophyte-inducing factors in osteoarthritis. J Orthop Res 2007, 25(5):569-577.
41. van der Weyden L., Wei L., Luo J., Yang X., Birk D.E., Adams D.J., et al. Functional knockout of the matrilin-3 gene causes premature chondrocyte maturation to hypertrophy and increases bone mineral density and osteoarthritis. Am J Pathol 2006, 169(2):515-527.
42. Gebauer M., Saas J., Haag J., Dietz U., Takigawa M., Bartnik E., et al. Repression of anti-proliferative factor Tob1 in osteoarthritic cartilage. Arthritis Res Ther 2005, 7(2):R274-R284.
43. Lories R.J., Peeters J., Bakker A., Tylzanowski P., Derese I., Schrooten J., et al. Articular cartilage and biomechanical properties of the long bones in Frzb-knockout mice. Arthritis Rheum 2007, 56(12):4095-4103.