WNT signaling and chondrocytes: From cell fate determination to osteoarthritis physiopathology

Journal of Receptors and Signal Transduction

Volumn 34, Issue 2, 2014, Pages 73-80

  Sassi, Nadia ^a   Laadhar, Lilia ^a   Allouche, Mohamed ^b   Achek, Asma ^a   Kallel Sellami, Mariem ^a   Makni, Sondès ^a   Sellami, Slaheddine ^a  

^a LA RABTA HOSPITAL   (Tunisia)

^b CHARLES NICOLLE HOSPITAL   (Tunisia)

Author keywords

Articular cartilage; Chondrocyte; Collagens; Osteoarthritis; WNT signaling

Indexed keywords

BETA CATENIN; CALCIUM; COLLAGEN; CYCLINE; INTERLEUKIN 1; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MATRIX METALLOPROTEINASE; PROTEIN C JUN; UNCLASSIFIED DRUG; WNT 5 PROTEIN; WNT 7 PROTEIN; WNT PROTEIN;

ADULTHOOD; ARTICULAR CARTILAGE; CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL POLARITY; CHONDROGENESIS; EXPERIMENTAL MODEL; HUMAN; IN VITRO STUDY; NONHUMAN; OSSIFICATION; OSTEOARTHRITIS; PATHOPHYSIOLOGY; PROTEIN INTERACTION; REVIEW; WNT SIGNALING PATHWAY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CHONDROCYTES; HUMANS; OSTEOARTHRITIS; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84897897086     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.3109/10799893.2013.863919     Document Type: Review

References (106)

1. Guinamp C, Pap T, Schadel J, et al. Gene therapy in osteoarthritis. Joint Bone Spine 2000;67:570-1.
2. Nagase H, Kashiwagi M. Aggrecanases and cartilage matrix degradation. Arthritis Res 2003;5:94-103.
3. Laadhar L, Zitouni M, Kallel-Sellami M, et al. Physiopathology of osteoarthritis From normal cartilage to osteoarthritic cartilage: risk factors and inflammatory mechanisms. Rev Med Interne 2007;28: 531-6.
4. Poole AR, Kobayashi M, Yasuda T, et al. Type II collagen degradation and its regulation in articular cartilage in osteoarthritis. Ann Rheum Dis 2002;61:78-81.
5. Van Beuningen HM, Stoop R, Buma P, et al. Phenotypic differences in murine chondrocyte cell lines from mature articular cartilage. Osteoarthritis Cartilage 2002;10:977-86.
6. Hartmann C. Skeletal development-WNTs are in control. Mol Cells 2007;24:177-84.
7. Ladher RK, Church VL, Allen S, et al. Cloning and expression of the WNT antagonists Sfrp-2 and Frzb during Chick development. Dev Biol 2000;218:183-98.
8. Chen M, Zhu M, Awad H, et al. Inhibition of beta-catenin signalling causes defects in postnatal cartilage development. J Cell Science 2008;121:1455-65.
9. Yuasa T, Otani T, Koike T, et al. WNT/beta-catenin signalling stimulates matrix catabolic genes and activity in articular chondrocytes: its possible role in joint degeneration. Lab Invest 2008;88: 264-74.
10. Laughlin J, Dowling B, Chapman K, et al. Functional variant within the secreted frizzled-related protein 3 gene are associated with hip osteoarthritis in females. Proc Natl Acad Sci U S A 2004;101: 9757-62.
11. Lories RJ, Peeters J, Bakker A, et al. Articular cartilage and biomechanical properties of the long bones in Frzb-knockout mice. Arthritis Rheum 2007;56:4095-103.
12. Lane NE, Nevitt MC, Lui LY, et al. WNT signaling antagonists are potential prognostic biomarkers for the progression of radiographic hip osteoarthritis in elderly Caucasian women. Arthritis Rheum 2007;56:3319-25.
13. Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982;31:99-109.
14. Rijsewijk F, Schuermann M, Wagenaar E, et al. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 1987;50:649-57.
15. The WNT gene homepage. Available from: http://www.stanford. edu/group/nusselab/cgi-bin/wnt/.
16. LAllemain G. Role of the WNT pathway in oncogenesis. Bull Cancer 2006;93:88-97.
17. GenBank. Available from: http://www.ncbi.nlm.nih.gov/gene/ 34009.
18. Willert K, Brown JD, Danenberg E, et al. WNT proteins are lipidmodified and can act as stem cell growth factors. Nature 2003;22 423(6938):448-52.
19. He X, Semenov M, Tamai K, Zeng X. LDL receptor-related proteins 5 and 6 in WNT/b-catenin signaling: arrows point the way. Development 2004;131:1663-77.
20. Bhanot P, Brink M, Samos CH, et al. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature 1996;382:225-30.
21. Yang-Snyder J, Miller JR, Brown JD, et al. A frizzled homolog functions in a vertebrate WNT signaling pathway. Curr Biol 1996;6: 1302-6.
22. Foord SM, Bonner TI, Neubig RR, et al. International Union of Pharmacology. XLVI G protein-coupled receptor list. Pharmacol Rev 2005;57:279-88.
23. Wong HC, Bourdelas A, Krauss A, et al. Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled. Mol Cell 2003;12:1251-60.
24. Kelly OG, Pinson KI, Skarnes WC. The WNT co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004; 131:2803-15.
25. Mao J, Wang J, Liu B, et al. Low-density lipoprotein receptorrelated protein-5 binds to Axin and regulates the canonical WNT signaling pathway. Mol Cell 2001;7:801-9.
26. Hoang B, Moos Jr M, Vukicevic S, Luyten FP. Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J Biol Chem 1996;271:26131-7.
27. Rattner A, Hsieh JC, Smallwood PM, et al. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc Natl Acad Sci USA 1997;94: 2859-63.
28. Hsieh JC, Kodjabachian L, Rebbert ML, et al. A new secreted protein that binds to WNT proteins and inhibits their activities. Nature 1999;398:431-6.
29. Itasaki N, Jones CM, Mercurio S, et al. Wise, a context dependent activator and inhibitor of WNT signaling. Development 2003;130: 4295-305.
30. Li X, Zhang Y, Kang H, et al. Sclerostin binds to LRP5/6 and antagonizes canonical WNT signaling. J Biol Chem 2005;280: 19883-7.
31. Semenov M, Tamai K, He X. SOST is a ligand for LRP5/LRP6 and a WNT signaling inhibitor. J Biol Chem 2005;280:26770-5.
32. Glinka A, Wu W, Delius H, et al. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998;391:357-62.
33. Mao B, Niehrs C. Kremen2 modulates Dickkopf2 activity during WNT/LRP6 signaling. Gene 2003;302:179-83.
34. Noordermeer J, Klingensmith J, Perrimon N, Nusse R. Dishevelled and armadillo act in the wingless signaling pathway in Drosophila. Nature 1994;367:80-3.
35. Zeng L, Fagotto F, Zhang T, et al. The mouse Fused locus encodes Axin, an inhibitor of the WNT signaling pathway that regulates embryonic axis formation. Cell 1997, 11;90:181-92.
36. Su LK, Vogelstein B, Kinzler KW. Association of the APC tumor suppressor protein with catenins. Science 1993;262:1734-7.
37. Rubinfeld B, Albert I, Porfiri E, et al. Binding of GSK3b to the APC-b-catenin complex and regulation of complex assembly. Science 1996;272:1023-6.
38. Munemitsu S, Albert I, Souza B, et al. Regulation of intracellular b-catenin levels by the adenomatous polyposis coli (APC) tumorsuppressor protein. Proc Natl Acad Sci USA 1995;92:3046-50.
39. Adler PN, Lee H. Frizzled signaling and cell-cell interactions in planar polarity. Curr Opin Cell Biol 2001;13:635-40.
40. Boutros M, Mlodzik M. Dishevelled: at the crossroads of divergent intracellular signaling pathways. Mech Dev 1999;83:27-37.
41. Kuhl M, Sheldahl LC, Park M, et al. The WNT/Ca2+ pathway: a new vertebrate WNT signaling pathway takes shape. Trends Genet 2000;16:279-83.
42. Miller JR, Hocking AM, Brown JD, Moon RT. Mechanism and function of signal transduction by the WNT/beta-catenin and WNT/ Ca2+ pathways. Oncogene 1999;18:7860-72.
43. Behrens J, von Kries JP, Kuhl M, et al. Functional interaction of b-catenin with the transcription factor LEF-1. Nature 1996;382: 638-42.
44. Wu X, Tu X, Joeng KS, et al. Rac1 activation controls nuclear localization of b-catenin during canonical WNT signaling. Cell 2008;133:340-53.
45. Van de Wetering M, Cavallo R, Dooijes D, et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 1997;88:789-99.
46. Brunner E, Peter O, Schweizer L, Basler K. Pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 1997;385:829-33.
47. Brannon M, Brown JD, Bates R, et al. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 1999;126:3159-70.
48. Billin AN, Thirlwell H, Ayer DE. b-catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol Cell Biol 2000;20:6882-90.
49. Cavallo RA, Cox RT, Moline MM, et al. Drosophila Tcf and Groucho interact to repress Wingless signaling activity. Nature 1998;395:604-8.
50. Roose J, Molenaar M, Peterson J, et al. The Xenopus WNT effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 1998;395:608-12.
51. Levanon D, Goldstein RE, Bernstein Y, et al. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc Natl Acad Sci USA 1998;95:11590-5.
52. Daniels DL, Weis WI. b-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in WNT mediated transcription activation. Nat Struct Mol Biol 2005;12:364-71.
53. Belenkaya TY, Han C, Standley HJ, et al. Pygopus encodes a nuclear protein essential for wingless/WNT signaling. Development 2002;129:4089-101.
54. Kramps T, Peter O, Brunner E, et al. WNT/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear b-catenin-TCF complex. Cell 2002;109:47-60.
55. Parker DS, Jemison J, Cadigan KM. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 2002;129:2565-76.
56. Thompson B, Townsley F, Rosin-Arbesfeld R, et al. A new nuclear component of the WNT signaling pathway. Nat Cell Biol 2002;4: 367-73.
57. Soliman MA, Riabowol K. After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem Sci 2007;32:509-19.
58. Hecht A, Vleminckx K, Stemmler MP, et al. The p300/CBP acetyltransferases function as transcriptional coactivators of b-catenin in vertebrates. EMBO J 2000;19:1839-50.
59. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with b-catenin to activate gene expression. J Cell Biol 2000;149:249-54.
60. Ogryzko VV, Schiltz RL, Russanova V, et al. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996;87:953-9.
61. Goldman PS, Tran VK, Goodman RH. The multifunctional role of the co-activator CBP in transcriptional regulation. Recent Prog Horm Res 1997;52:103-19.
62. Staal FJT, Clevers HC. WNT signalling and haematopoiesis: a WNT-WNT situation. Nat Rev Immunol 2005;5:21-30.
63. Hinoi T, Yamamoto H, Kishida M, et al. Complex formation of adenomatous polyposis coli gene product and axin facilitates glycogen synthase kinase-3 beta-dependent phosphorylation of beta-catenin and down-regulates beta-catenin. J Biol Chem 2000; 275:34399-406.
64. Hens JR, Wilson KM, Dann P, et al. TOPGAL mice show that the canonical WNT signaling pathway is active during bone development and growth and is activated by mechanical loading in vitro. J Bone Miner Res 2005;20:1103-13.
65. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, et al. WNT/betacatenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem 2006;281:31720-8.
66. Jackson A, Vayssiere B, Garcia T, et al. Gene array analysis of WNT-regulated genes in C3H10T1/2 cells. Bone 2005;36:585-98.
67. Hecht A, Litterst CM, Huber O, Kemler R. Functional characterization of multiple transactivating elements in b-catenin, some of which interact with the TATA-binding protein in vitro. J Biol Chem 1999;274:18017-25.
68. Barker N, Hurlstone A, Musisi H, et al. The chromatin remodelling factor Brg-1 interacts with b-catenin to promote target gene activation. EMBO J 2001;20:4935-43.
69. Bauer A, Huber O, Kemler R. Pontin52, an interaction partner of b-catenin, binds to the TATA box binding protein. Proc Natl Acad Sci USA 1998;95:14787-92.
70. Bauer A, Chauvet S, Huber O, et al. Pontin52 and reptin52 function as antagonistic regulators of b-catenin signaling activity. EMBO J 2000;19:6121-30.
71. Ishitani T, Kishida S, Hyodo-Miura J, et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the WNT-5a/ Ca(2+) pathway to antagonize WNT/beta-catenin signaling. Mol Cell Biol 2003;23:131-9.
72. Mlodzik M. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet 2002;21:564-71
73. Torres MA, Yang-Snyder JA, Purcell SM, et al. Activities of the WNT-1 class of secreted signaling factors are antagonized by the WNT-5A class and by a dominant negative cadherin in early Xenopus development. J Cell Biol 1996;133:1123-37.
74. Teo JL, Kahn M. The WNT signaling pathway in cellular proliferation and differentiation: a tale of two coactivators. Adv Drug Deliv Rev 2010;62:1149-55.
75. Liu F, Kohlmeier S, Wang CY. WNT signaling and skeletal development. Cell Signal 2008;20:999-1009.
76. Wang Y, Nathans J. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 2007;134:647-58.
77. Wen S, Zhu H, Lu W, et al. Planar cell polarity pathway genes and risk for spina bifida. Am J Med Genet A 2010;152A: 299-304.
78. Copp AJ, Greene ND. Genetics and development of neural tube defects. J Pathol 2010;220:217-30.
79. Habas R, Dawid IB, He X. Coactivation of Rac and Rho by WNT/ Frizzled signaling is required for vertebrate gastrulation. Genes Dev 2003;17:295-309.
80. Park M, Moon RT. The planar cell-polarity gene stbm regulates cell behavior and cell fate in vertebrate embryos. Nat Cell Biol 2002;4: 20-5.
81. Saneyoshi T, Kume S, Amasaki Y, Mikoshiba K. The WNT/ calcium pathway activates NF-AT and promotes ventral cell fate in Xenopus embryos. Nature 2002;417:295-9.
82. Wang HY, Malbon CC. WNT signaling, Ca2+, and cyclic GMP: visualizing Frizzled functions. Science 2003;300:1529-30.
83. Kohn AD, Moon RT. WNT and calcium signaling: b-Cateninindependent pathways. Cell Calcium 2005;38:439-46.
84. Reinhold M, Naski M. Direct interactions of Runx2 and canonical WNT signaling induce FGF18. J Biol Chem 2007;282:3653-63.
85. Tufan AC, Daumer KM, DeLise AM, Tuan RS. AP-1 transcription factor complex is a target of signals from both WNT-7a and N-cadherin-dependent. Expr Cell Res 2002;273:197-203.
86. Hartmann C, Tabin CJ. Dual roles of WNT signaling during chondrogenesis in the chicken limb. Development 2000;127: 3141-59.
87. Yang Y, Topol L, Lee H, Wu J. WNT5a and WNT5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 2003;130:1003-15.
88. Kawakami Y, Wada N, Nishimatsu S, et al. Involvement of WNT-5a in chondrogenic pattern formation in the chick limb bud. Dev, Growth Diff 1999;41:29-40.
89. Tamamura Y, Otani T, Kanatani N, et al. Developmental regulation of WNT-beta catenin signals is required for growth plate assembly cartilage integrity and endochondral ossification. J Biol Chem 2005;280:19185-95.
90. Gaur T, Rich L, Lengner CJ, et al. Secreted frizzled related protein 1 regulates WNT signaling for BMP2 induced chondrocyte differentiation. J Cell Physiol 2006;208:87-96.
91. Akiyama H, Lyons JP, Mori-Akiyama Y, et al. Interactions between Sox9 and b-catenin control chondrocyte differentiation. Genes Dev 2004;18:1072-87.
92. Sen M. WNT signalling in rheumatoid arthritis. Rheumatology (Oxford) 2005;44:708-13.
93. Hwang SG, Ryu JH, Kim IC, et al. Regulation of beta-catenin signaling and maintenance of chondrocyte differentiation by ubiquitin dependent proteosomal degradation of alpha-catenin. J Biol Chem 2004;279:26597-604.
94. Sandell LJ, Aigner T. Articular cartilage and changes in arthritis. An introduction: cell biology of osteoarthritis. Arthritis Res 2001; 3:107-13.
95. Ryu JH, Chun JS. Opposing roles of WNT-5A and WNT-11 in interleukin-1b regulation of type ii collagen expression in articular chondrocytes. J Biol Chem 2006;281:22039-47.
96. Ryu JH, Kim SJ, Kim SH, et al. Regulation of the chondrocyte phenotype by b-catenin. Development 2002;129:5541-50.
97. Sassi N, Laadhar L, Allouche M, et al. WNT signaling is involved in human articular chondrocyte de-differentiation in vitro. Biotech Histochem. 2013 Aug 1. [Epub ahead of print].
98. Hwang SG, Yu SS, Lee SW, Chun JS. WNT-7a causes loss of differentiated phenotype and inhibits apoptosis of articular chondrocytes via different mechanisms. J Biol Chem 2004;280: 12758-65.
99. Hwang SG, Yu SS, Lee SW, Chun JS. WNT 3a regulates chondrocytes differentiation via c-Jun/AP1 pathway. FEBS Letters 2005;579:4837-42.
100. Day TF, Guo X, Garrett-Beal L, Yang Y. WNT beta-catenin signaling in mesenchymal progenitor controls osteoblast and chondrocyte differentiation during vertebrates skeletogenesis. Dev Cell 2005;8:739-50.
101. DellAccio F, De Bari C, Luyten F. Molecular markers predictive of the capacity of expanded human articular chondrocytes to form stable cartilage in vivo. Arthritis Rheum 2001;44: 1608-19.
102. Weng LH, Wang CJ, Ko JY, et al. Control of Dkk-1 ameliorates chondrocyte apoptosis cartilage destruction and subchondral bone deterioration in osteoarthritic knees. Arthritis Rheum 2010;62: 1393-402.
103. Zhu M, Chen M, Zuscik M, et al. Inhibition of beta-catenin signaling in articular chondrocytes results in articular cartilage destruction. Arthritis Rheum 2008;7:2053-64.
104. Sassi N, Laadhar L, Allouche M, et al. The roles of canonical and non canonical WNT signaling in human de-differentiated articular chondrocytes. Biotech Histochem. 2013 Aug 1. [Epub ahead of print].
105. Weng LH, Wang CJ, Ko JY, et al. Inflammation induction of Dickkopf-1 mediates chondrocyte apoptosis in osteoarthritic joint. Osteoarthritis Cartilage 2009;17:933-43.
106. Sassi N, Laadhar L, Driss M, et al. The role of the Notch pathway in healthy and osteoarthritic articular cartilage: from experimental models to ex vivo studies. Arthritis Res Ther 2011; 13:208.