Autocrine stimulation of osteoblast activity by Wnt5a in response to TNF-α in human mesenchymal stem cells

Biochemical and Biophysical Research Communications

Volumn 430, Issue 3, 2013, Pages 1072-1077

  Briolay, A ^a   Lencel, P ^b   Bessueille, L ^a   Caverzasio, J ^c   Buchet, R ^a   Magne, D ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DU LITTORAL CÔTE D OPALE   (France)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Alkaline phosphatase; Ankylosing spondylitis; Inflammation; Mineralization; Osteoblast; TNF ; Wnt

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; ALKALINE PHOSPHATASE; BETA CATENIN; CYCLOOXYGENASE 2; DICKKOPF 1 PROTEIN; LITHIUM CHLORIDE; OSTEOCALCIN; TUMOR NECROSIS FACTOR ALPHA; WNT10B PROTEIN; WNT5A PROTEIN;

ADULT; ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MESENCHYMAL STEM CELL; MINERALIZATION; NUCLEOTIDE SEQUENCE; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL;

ADULT; ALKALINE PHOSPHATASE; BETA CATENIN; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; INDOLES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LITHIUM CHLORIDE; MALE; MALEIMIDES; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; OSTEOGENESIS; PROTO-ONCOGENE PROTEINS; SPONDYLITIS, ANKYLOSING; TUMOR NECROSIS FACTOR-ALPHA; WNT PROTEINS;

EID: 84872500712     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.036     Document Type: Article

References (42)

1. Walsh N.C., Crotti T.N., Goldring S.R., Gravallese E.M. Rheumatic diseases: the effects of inflammation on bone. Immunol. Rev. 2005, 208:228-251.
2. Ding J., Ghali O., Lencel P., Broux O., Chauveau C., Devedjian J.C., Hardouin P., Magne D. TNF-alpha and IL-1beta inhibit RUNX2 and collagen expression but increase alkaline phosphatase activity and mineralization in human mesenchymal stem cells. Life Sci. 2009, 84:499-504.
3. Kaneki H., Guo R., Chen D., Yao Z., Schwarz E.M., Zhang Y.E., Boyce B.F., Xing L. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J. Biol. Chem. 2006, 281:4326-4333.
4. Sieper J., Braun J., Rudwaleit M., Boonen A., Zink A. Ankylosing spondylitis: an overview. Ann. Rheum. Dis. 2002, 61(Suppl. 3):iii8-18.
5. Schett G., Rudwaleit M. Can we stop progression of ankylosing spondylitis?. Best. Pract. Res. Clin. Rheumatol. 2010, 24:363-371.
6. Lencel P., Delplace S., Pilet P., Leterme D., Miellot F., Sourice S., Caudrillier A., Hardouin P., Guicheux J., Magne D. Cell-specific effects of TNF-α and IL-1β on alkaline phosphatase: implication for syndesmophyte formation and vascular calcification. Lab. Invest. 2011, 91:1434-1442.
7. Pedersen S.J., Sørensen I.J., Lambert R.G., Hermann K.G., Garnero P., Johansen J.S., Madsen O.R., Hansen A., Hansen M.S., Thamsborg G., Andersen L.S., Majgaard O., Loft A.G., Erlendsson J., Asmussen K.H., Jurik A.G., Møller J., Hasselquist M., Mikkelsen D., Østergaard M. Radiographic progression is associated with resolution of systemic inflammation in patients with axial spondylarthritis treated with tumor necrosis factor α inhibitors: a study of radiographic progression, inflammation on magnetic resonance imaging, and circulating biomarkers of inflammation, angiogenesis, and cartilage and bone turnover. Arthritis Rheum. 2011, 63:3789-3800.
8. Gerstenfeld L.C., Cho T.J., Kon T., Aizawa T., Tsay A., Fitch J., Barnes G.L., Graves D.T., Einhorn T.A. Impaired fracture healing in the absence of TNF-alpha signaling: the role of TNF-alpha in endochondral cartilage resorption. J. Bone Miner. Res. 2003, 18:1584-1592.
9. Gerstenfeld L.C., Cho T.J., Kon T., Aizawa T., Cruceta J., Graves B.D., Einhorn T.A. Impaired intramembranous bone formation during bone repair in the absence of tumor necrosis factor-alpha signaling. Cells Tissues Organs 2001, 169:285-294.
10. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D., Korb A., Smolen J., Hoffmann M., Scheinecker C., van der Heide D., Landewe R., Lacey D., Richards W.G., Schett G. Dickkopf-1 is a master regulator of joint remodeling. Nat. Med. 2007, 13:156-163.
11. Gaur T., Wixted J.J., Hussain S., O'Connell S.L., Morgan E.F., Ayers D.C., Komm B.S., Bodine P.V., Stein G.S., Lian J.B. Secreted frizzled related protein 1 is a target to improve fracture healing. J. Cell. Physiol. 2009, 220:174-181.
12. Komatsu D.E., Mary M.N., Schroeder R.J., Robling A.G., Turner C.H., Warden S.J. Modulation of Wnt signaling influences fracture repair. J. Orthop. Res. 2010, 28:928-936.
13. Agholme F., Isaksson H., Kuhstoss S., Aspenberg P. The effects of Dickkopf-1 antibody on metaphyseal bone and implant fixation under different loading conditions. Bone 2011, 48:988-996.
14. Pinzone J.J., Hall B.M., Thudi N.K., Vonau M., Qiang Y.W., Rosol T.J., Shaughnessy J.D. The role of Dickkopf-1 in bone development, homeostasis, and disease. Blood 2009, 113:517-525.
15. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 2005, 8:739-750.
16. Morvan F., Boulukos K., Clément-Lacroix P., Roman Roman S., Suc-Royer I., Vayssière B., Ammann P., Martin P., Pinho S., Pognonec P., Mollat P., Niehrs C., Baron R., Rawadi G. Deletion of a single allele of the Dkk1 gene leads to an increase in bone formation and bone mass. J. Bone Miner. Res. 2006, 21:934-945.
17. Heiland G.R., Zwerina K., Baum W., Kireva T., Distler J.H., Grisanti M., Asuncion F., Li X., Ominsky M., Richards W., Schett G., Zwerina J. Neutralisation of Dkk-1 protects from systemic bone loss during inflammation and reduces sclerostin expression. Ann. Rheum. Dis. 2010, 69:2152-2159.
18. Heiland G.R., Appel H., Poddubnyy D., Zwerina J., Hueber A., Haibel H., Baraliakos X., Listing J., Rudwaleit M., Schett G., Sieper J. High level of functional dickkopf-1 predicts protection from syndesmophyte formation in patients with ankylosing spondylitis. Ann. Rheum. Dis. 2012, 71:572-574.
19. Andrade A.C., Nilsson O., Barnes K.M., Baron J. Wnt gene expression in the post-natal growth plate: regulation with chondrocyte differentiation. Bone 2007, 40:1361-1369.
20. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl. Acad. Sci. USA 2005, 102:3324-3329.
21. Zhong Z., Zylstra-Diegel C.R., Schumacher C.A., Baker J.J., Carpenter A.C., Rao S., Yao W., Guan M., Helms J.A., Lane N.E., Lang R.A., Williams B.O. Wntless functions in mature osteoblasts to regulate bone mass. Proc. Natl. Acad. Sci. USA 2012, 109:E2197-2204.
22. Matzelle M.M., Gallant M.A., Condon K.W., Walsh N.C., Manning C.A., Stein G.S., Lian J.B., Burr D.B., Gravallese E.M. Resolution of inflammation induces osteoblast function and regulates the Wnt signaling pathway. Arthritis Rheum. 2012, 64:1540-1550.
23. Gustafson B., Smith U. Cytokines promote Wnt signaling and inflammation and impair the normal differentiation and lipid accumulation in 3T3-L1 preadipocytes. J. Biol. Chem. 2006, 281:9507-9516.
24. Guo J., Jin J., Cooper L.F. Dissection of sets of genes that control the character of wnt5a-deficient mouse calvarial cells. Bone 2008, 43:961-971.
25. Takada I., Mihara M., Suzawa M., Ohtake F., Kobayashi S., Igarashi M., Youn M.Y., Takeyama K., Nakamura T., Mezaki Y., Takezawa S., Yogiashi Y., Kitagawa H., Yamada G., Takada S., Minami Y., Shibuya H., Matsumoto K., Kato S. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat. Cell Biol. 2007, 9:1273-1285.
26. Sen M., Lauterbach K., El-Gabalawy H., Firestein G.S., Corr M., Carson D.A. Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 2000, 97:2791-2796.
27. Hadjiargyrou M., Lombardo F., Zhao S., Ahrens W., Joo J., Ahn H., Jurman M., White D.W., Rubin C.T. Transcriptional profiling of bone regeneration. Insight into the molecular complexity of wound repair. J. Biol. Chem. 2002, 277:30177-30182.
28. Olivares-Navarrete R., Hyzy S.L., Park J.H., Dunn G.R., Haithcock D.A., Wasilewski C.E., Boyan B.D., Schwartz Z. Mediation of osteogenic differentiation of human mesenchymal stem cells on titanium surfaces by a Wnt-integrin feedback loop. Biomaterials 2011, 32:6399-6411.
29. Caverzasio J., Manen D. Essential role of Wnt3a-mediated activation of mitogen-activated protein kinase p38 for the stimulation of alkaline phosphatase activity and matrix mineralization in C3H10T1/2 mesenchymal cells. Endocrinology 2007, 148:5323-5330.
30. Lencel P., Delplace S., Hardouin P., Magne D. TNF-α stimulates alkaline phosphatase and mineralization through PPARγ inhibition in human osteoblasts. Bone 2011, 48:242-249.
31. Lu Z., Wang G., Dunstan C.R., Zreiqat H. Short-term exposure to tumor necrosis factor-alpha enables human osteoblasts to direct adipose tissue-derived mesenchymal stem cells into osteogenic differentiation. Stem Cells Dev. 2012, 21:2420-2429.
32. Vincent C., Findlay D.M., Welldon K.J., Wijenayaka A.R., Zheng T.S., Haynes D.R., Fazzalari N.L., Evdokiou A., Atkins G.J. Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogen-activated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J. Bone Miner. Res. 2009, 24:1434-1449.
33. Krause U., Harris S., Green A., Ylostalo J., Zeitouni S., Lee N., Gregory C.A. Pharmaceutical modulation of canonical Wnt signaling in multipotent stromal cells for improved osteoinductive therapy. Proc. Natl. Acad. Sci. USA 2010, 107:4147-4152.
34. Sonomoto K., Yamaoka K., Oshita K., Fukuyo S., Zhang X., Nakano K., Okada Y., Tanaka Y. Interleukin-1β induces differentiation of human mesenchymal stem cells into osteoblasts via the Wnt-5a/receptor tyrosine kinase-like orphan receptor 2 pathway. Arthritis Rheum. 2012, 64:3355-3363.
35. Heath D.J., Chantry A.D., Buckle C.H., Coulton L., Shaughnessy J.D., Evans H.R., Snowden J.A., Stover D.R., Vanderkerken K., Croucher P.I. Inhibiting Dickkopf-1 (Dkk1) removes suppression of bone formation and prevents the development of osteolytic bone disease in multiple myeloma. J. Bone Miner. Res. 2009, 24:425-436.
36. Fulciniti M., Tassone P., Hideshima T., Vallet S., Nanjappa P., Ettenberg S.A., Shen Z., Patel N., Tai Y.T., Chauhan D., Mitsiades C., Prabhala R., Raje N., Anderson K.C., Stover D.R., Munshi N.C. Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma. Blood 2009, 114:371-379.
37. Kim J.B., Leucht P., Lam K., Luppen C., Ten Berge D., Nusse R., Helms J.A. Bone regeneration is regulated by wnt signaling. J. Bone Miner. Res. 2007, 22:1913-1923.
38. Pereira C., Schaer D.J., Bachli E.B., Kurrer M.O., Schoedon G. Wnt5A/CaMKII signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler. Thromb. Vasc. Biol. 2008, 28:504-510.
39. Kim J., Kim D.W., Ha Y., Ihm M.H., Kim H., Song K., Lee I. Wnt5a induces endothelial inflammation via beta-catenin-independent signaling. J. Immunol. 2010, 185:1274-1282.
40. Baksh D., Boland G.M., Tuan R.S. Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J. Cell. Biochem. 2007, 101:1109-1124.
41. Bilkovski R., Schulte D.M., Oberhauser F., Gomolka M., Udelhoven M., Hettich M.M., Roth B., Heidenreich A., Gutschow C., Krone W., Laudes M. Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J. Biol. Chem. 2010, 285:6170-6178.
42. Maeda K., Kobayashi Y., Udagawa N., Uehara S., Ishihara A., Mizoguchi T., Kikuchi Y., Takada I., Kato S., Kani S., Nishita M., Marumo K., Martin T.J., Minami Y., Takahashi N. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat. Med. 2012, 18:405-412.