Podosomes are dispensable for osteoclast differentiation and migration

European Journal of Cell Biology

Volumn 92, Issue 4-5, 2013, Pages 139-149

  Touaitahuata, Heiani ^a,b   Planus, Emmanuelle ^c,d   Albiges Rizo, Corinne ^c,d   Blangy, Anne ^a,b   Pawlak, Geraldine ^a,b,d  

^a Centre National de la Recherche Scientifique   (France)

^b UNIV MONTPELLIER   (France)

^c INSTITUT ALBERT BONNIOT   (France)

^d UNIV GRENOBLE ALPES   (France)

Author keywords

Actin; Adhesion; Cofilin; Integrin; Manganese; MMP14; MT1 MMP; Myeloid; Osteoclast; Podosome

Indexed keywords

INTEGRIN; SCLEROPROTEIN;

ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; HUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PODOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RIGIDITY;

ACRYLIC RESINS; ACTINS; AGAR; ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL-MATRIX JUNCTIONS; CELLS, CULTURED; CULTURE MEDIA; DIMETHYLPOLYSILOXANES; EXTRACELLULAR MATRIX; INTEGRINS; MICE; MICE, INBRED C57BL; OSTEOCLASTS; SRC-FAMILY KINASES; VINCULIN;

EID: 84877606554     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2013.03.001     Document Type: Article

References (48)

1. Albiges-Rizo C., Destaing O., Fourcade B., Planus E., Block M.R. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 2009, 122:3037-3049.
2. Blangy A., Touaitahuata H., Cres G., Pawlak G. Cofilin activation during podosome belt formation in osteoclasts. PLoS ONE 2012, 7:e45909.
3. Brazier H., Pawlak G., Vives V., Blangy A. The Rho GTPase Wrch1 regulates osteoclast precursor adhesion and migration. Int. J. Biochem. Cell Biol. 2009, 41:1391-1401.
4. Brazier H., Stephens S., Ory S., Fort P., Morrison N., Blangy A. Expression profile of RhoGTPases and RhoGEFs during RANKL-stimulated osteoclastogenesis: identification of essential genes in osteoclasts. J. Bone Miner. Res. 2006, 21:1387-1398.
5. Brown X.Q., Ookawa K., Wong J.Y. Evaluation of polydimethylsiloxane scaffolds with physiologically-relevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 2005, 26:3123-3129.
6. Chabadel A., Banon-Rodriguez I., Cluet D., Rudkin B.B., Wehrle-Haller B., Genot E., Jurdic P., Anton I.M., Saltel F. CD44 and beta3 integrin organize two functionally distinct actin-based domains in osteoclasts. Mol. Biol. Cell 2007, 18:4899-4910.
7. Chen J., Salas A., Springer T.A. Bistable regulation of integrin adhesiveness by a bipolar metal ion cluster. Nat. Struct. Biol. 2003, 10:995-1001.
8. Collin O., Na S., Chowdhury F., Hong M., Shin M.E., Wang F., Wang N. Self-organized podosomes are dynamic mechanosensors. Curr. Biol. 2008, 18:1288-1294.
9. Collin O., Tracqui P., Stephanou A., Usson Y., Clement-Lacroix J., Planus E. Spatiotemporal dynamics of actin-rich adhesion microdomains: influence of substrate flexibility. J. Cell Sci. 2006, 119:1914-1925.
10. Damljanovic V., Lagerholm B.C., Jacobson K. Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 2005, 39:847-851.
11. de Vries T.J., Schoenmaker T., Beertsen W., van der Neut R., Everts V. Effect of CD44 deficiency on in vitro and in vivo osteoclast formation. J. Cell. Biochem. 2005, 94:954-966.
12. Destaing O., Saltel F., Geminard J.C., Jurdic P., Bard F. Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 2003, 14:407-416.
13. Destaing O., Sanjay A., Itzstein C., Horne W.C., Toomre D., De Camilli P., Baron R. The tyrosine kinase activity of c-Src regulates actin dynamics and organization of podosomes in osteoclasts. Mol. Biol. Cell 2008, 19:394-404.
14. Engler A.J., Griffin M.A., Sen S., Bonnemann C.G., Sweeney H.L., Discher D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 2004, 166:877-887.
15. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
16. Evans E., Kinoshita K., Simon S., Leung A. Long-lived, high-strength states of ICAM-1 bonds to beta2 integrin, I: Lifetimes of bonds to recombinant alphaLbeta2 under force. Biophys. J. 2010, 98:1458-1466.
17. Friedl P., Weigelin B. Interstitial leukocyte migration and immune function. Nat. Immunol. 2008, 9:960-969.
18. Fu Q., Rahaman M.N., Bal B.S., Brown R.F. Preparation and in vitro evaluation of bioactive glass (13-93) scaffolds with oriented microstructures for repair and regeneration of load-bearing bones. J. Biomed. Mater. Res. A 2010, 93:1380-1390.
19. Gowen M., Lazner F., Dodds R., Kapadia R., Feild J., Tavaria M., Bertoncello I., Drake F., Zavarselk S., Tellis I., Hertzog P., Debouck C., Kola I. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J. Bone Miner. Res. 1999, 14:1654-1663.
20. Guiet R., Verollet C., Lamsoul I., Cougoule C., Poincloux R., Labrousse A., Calderwood D.A., Glogauer M., Lutz P.G., Maridonneau-Parini I. Macrophage mesenchymal migration requires podosome stabilization by filamin A. J. Biol. Chem. 2012, 287:13051-13062.
21. Hu S., Planus E., Georgess D., Place C., Wang X., Albiges-Rizo C., Jurdic P., Geminard J.C. Podosome rings generate forces that drive saltatory osteoclast migration. Mol. Biol. Cell 2011, 22:3120-3126.
22. Ishii M., Kikuta J., Shimazu Y., Meier-Schellersheim M., Germain R.N. Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo. J. Exp. Med. 2010, 207:2793-2798.
23. Jang I., Jeon B.T., Jeong E.A., Kim E.J., Kang D., Lee J.S., Jeong B.G., Kim J.H., Choi B.H., Lee J.E., Kim J.W., Choi J.Y., Roh G.S. Pak1/LIMK1/cofilin pathway contributes to tumor migration and invasion in human non-small cell lung carcinomas and cell lines. Korean J. Physiol. Pharmacol. 2012, 16:159-165.
24. Khatiwala C.B., Peyton S.R., Putnam A.J. Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. Am. J. Physiol. Cell Physiol. 2006, 290:C1640-C1650.
25. Kim K., Lee S.H., Ha Kim J., Choi Y., Kim N. NFATc1 induces osteoclast fusion via up-regulation of Atp6v0d2 and the dendritic cell-specific transmembrane protein (DC-STAMP). Mol. Endocrinol. (Baltimore, MD) 2008, 22:176-185.
26. Kirstein B., Chambers T.J., Fuller K. Secretion of tartrate-resistant acid phosphatase by osteoclasts correlates with resorptive behavior. J. Cell. Biochem. 2006, 98:1085-1094.
27. Kotani M., Kikuta J., Klauschen F., Chino T., Kobayashi Y., Yasuda H., Tamai K., Miyawaki A., Kanagawa O., Tomura M., Ishii M. Systemic circulation and bone recruitment of osteoclast precursors tracked by using fluorescent imaging techniques. J. Immunol. 2013, 190:605-612.
28. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D.R., Fassler R., Sixt M. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453:51-55.
29. Luxenburg C., Geblinger D., Klein E., Anderson K., Hanein D., Geiger B., Addadi L. The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS ONE 2007, 2:e179.
30. McHugh K.P., Hodivala-Dilke K., Zheng M.H., Namba N., Lam J., Novack D., Feng X., Ross F.P., Hynes R.O., Teitelbaum S.L. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J. Clin. Invest. 2000, 105:433-440.
31. Mochizuki A., Takami M., Miyamoto Y., Nakamaki T., Tomoyasu S., Kadono Y., Tanaka S., Inoue T., Kamijo R. Cell adhesion signaling regulates RANK expression in osteoclast precursors. PLoS ONE 2012, 7:e48795.
32. Mould A.P., Askari J.A., Barton S., Kline A.D., McEwan P.A., Craig S.E., Humphries M.J. Integrin activation involves a conformational change in the alpha 1 helix of the beta subunit A-domain. J. Biol. Chem. 2002, 277:19800-19805.
33. Novack D.V., Faccio R. Osteoclast motility: putting the brakes on bone resorption. Ageing Res. Rev. 2009, 10:54-61.
34. Okamoto K., Takayanagi H. Osteoclasts in arthritis and Th17 cell development. Int. Immunopharmacol. 2011, 11:543-548.
35. Orr A.W., Ginsberg M.H., Shattil S.J., Deckmyn H., Schwartz M.A. Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 2006, 17:4686-4697.
36. Ory S., Brazier H., Blangy A. Identification of a bipartite focal adhesion localization signal in RhoU/Wrch-1, a Rho family GTPase that regulates cell adhesion and migration. Biol. Cell. 2007, 99:701-716.
37. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13661-13665.
38. Roodman G.D. Cell biology of the osteoclast. Exp. Hematol. 1999, 27:1229-1241.
39. Saltel F., Chabadel A., Zhao Y., Lafage-Proust M.H., Clezardin P., Jurdic P., Bonnelye E. Transmigration: a new property of mature multinucleated osteoclasts. J. Bone Miner. Res. 2006, 21:1913-1923.
40. Saltel F., Destaing O., Bard F., Eichert D., Jurdic P. Apatite-mediated actin dynamics in resorbing osteoclasts. Mol. Biol. Cell 2004, 15:5231-5241.
41. Schmidt S., Nakchbandi I., Ruppert R., Kawelke N., Hess M.W., Pfaller K., Jurdic P., Fassler R., Moser M. Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J. Cell Biol. 2011, 192:883-897.
42. Takayanagi H., Kim S., Koga T., Nishina H., Isshiki M., Yoshida H., Saiura A., Isobe M., Yokochi T., Inoue J., Wagner E.F., Mak T.W., Kodama T., Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 2002, 3:889-901.
43. Van Goethem E., Poincloux R., Gauffre F., Maridonneau-Parini I., Le Cabec V. Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. 2010, 184:1049-1061.
44. van Helden S.F., Krooshoop D.J., Broers K.C., Raymakers R.A., Figdor C.G., van Leeuwen F.N. A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J. Immunol. 2006, 177:1567-1574.
45. Vives V., Laurin M., Cres G., Larrousse P., Morichaud Z., Noel D., Cote J.F., Blangy A. The Rac1 exchange factor Dock5 is essential for bone resorption by osteoclasts. J. Bone Miner. Res. 2011, 26:1099-1110.
46. Wakkach A., Mansour A., Dacquin R., Coste E., Jurdic P., Carle G.F., Blin-Wakkach C. Bone marrow microenvironment controls the in vivo differentiation of murine dendritic cells into osteoclasts. Blood 2008, 112:5074-5083.
47. Yagi M., Ninomiya K., Fujita N., Suzuki T., Iwasaki R., Morita K., Hosogane N., Matsuo K., Toyama Y., Suda T., Miyamoto T. Induction of DC-STAMP by alternative activation and downstream signaling mechanisms. J. Bone Miner. Res. 2007, 22:992-1001.
48. Zhou Y., Su J., Shi L., Liao Q., Su Q. DADS downregulates the Rac1-ROCK1/PAK1-LIMK1-ADF/cofilin signaling pathway, inhibiting cell migration and invasion. Oncol. Rep. 2013, 29:605-612.