Rho GTPases in osteoclasts: Orchestrators of podosome arrangement

European Journal of Cell Biology

Volumn 87, Issue 8-9, 2008, Pages 469-477

  Ory, Stéphane ^a   Brazier, Hélène ^a   Pawlak, Géraldine ^a,b   Blangy, Anne ^a  

^a CNRS   (France)

^b INSTITUT ALBERT BONNIOT   (France)

Author keywords

Osteoclast; Podosome; Rho GTPases; RhoU; Sealing zone; WASP; Wrch 1

Indexed keywords

F ACTIN; INTEGRIN; PROTEIN CDC42; PROTEIN KINASE; PROTEINASE; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN;

ACTIN POLYMERIZATION; BONE MARROW CELL; CELL ADHESION; CELL ISOLATION; CELL LINEAGE; CELL MIGRATION; CELL STRUCTURE; DENDRITIC CELL; EXTRACELLULAR MATRIX; MACROPHAGE; MESENCHYME CELL; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PODOSOME; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; STRESS FIBER;

ANIMALS; CELL ADHESION; HUMANS; MICROFILAMENTS; MODELS, BIOLOGICAL; OSTEOCLASTS; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 49249104668     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2008.03.002     Document Type: Short Survey

References (74)

1. Abo A., Qu J., Cammarano M.S., Dan C., Fritsch A., Baud V., Belisle B., and Minden A. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J. 17 (1998) 6527-6540
2. Aktories K., and Barbieri J.T. Bacterial cytotoxins: targeting eukaryotic switches. Nat. Rev. Microbiol. 3 (2005) 397-410
3. Arthur W.T., Petch L.A., and Burridge K. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10 (2000) 719-722
4. Berger C.E., Rathod H., Gillespie J.I., Horrocks B.R., and Datta H.K. Scanning electrochemical microscopy at the surface of bone-resorbing osteoclasts: evidence for steady-state disposal and intracellular functional compartmentalization of calcium. J. Bone Miner. Res. 16 (2001) 2092-2102
5. Berzat A.C., Buss J.E., Chenette E.J., Weinbaum C.A., Shutes A., Der C.J., Minden A., and Cox A.D. Transforming activity of the Rho family GTPase, Wrch-1, a Wnt-regulated Cdc42 homolog, is dependent on a novel carboxyl-terminal palmitoylation motif. J. Biol. Chem. 280 (2005) 33055-33065
6. Bhadriraju K., Yang M., Alom Ruiz S., Pirone D., Tan J., and Chen C.S. Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp. Cell Res. 313 (2007) 3616-3623
7. Boureux A., Vignal E., Faure S., and Fort P. Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol. Biol. Evol. 24 (2007) 203-216
8. Brazier H., Stephens S., Ory S., Fort P., Morrison N., and Blangy A. Expression profile of RhoGTPases and RhoGEFs during RANKL-stimulated osteoclastogenesis: identification of essential genes in osteoclasts. J. Bone Miner. Res. 21 (2006) 1387-1398
9. Brown M.C., Cary L.A., Jamieson J.S., Cooper J.A., and Turner C.E. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol. Biol. Cell 16 (2005) 4316-4328
10. Burns S., Thrasher A.J., Blundell M.P., Machesky L., and Jones G.E. Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98 (2001) 1142-1149
11. Burns S., Cory G.O., Vainchenker W., and Thrasher A.J. Mechanisms of WASp-mediated hematologic and immunologic disease. Blood 104 (2004) 3454-3462
12. Burridge K., and Wennerberg K. Rho and Rac take center stage. Cell 116 (2004) 167-179
13. Butler B., and Blystone S.D. Tyrosine phosphorylation of beta3 integrin provides a binding site for Pyk2. J. Biol. Chem. 280 (2005) 14556-14562
14. Calle Y., Jones G.E., Jagger C., Fuller K., Blundell M.P., Chow J., Chambers T., and Thrasher A.J. WASp deficiency in mice results in failure to form osteoclast sealing zones and defects in bone resorption. Blood 103 (2004) 3552-3561
15. Chabadel A., Banon-Rodriguez I., Cluet D., Rudkin B.B., Wehrle-Haller B., Genot E., Jurdic P., Anton I.M., and Saltel F. CD44 and beta3 integrin organize two functionally distinct actin-based domains in osteoclasts. Mol. Biol. Cell 18 (2007) 4899-4910
16. Chellaiah M.A. Regulation of actin ring formation by rho GTPases in osteoclasts. J. Biol. Chem. 280 (2005) 32930-32943
17. Chellaiah M.A., Soga N., Swanson S., McAllister S., Alvarez U., Wang D., Dowdy S.F., and Hruska K.A. Rho-A is critical for osteoclast podosome organization, motility, and bone resorption. J. Biol. Chem. 275 (2000) 11993-12002
18. Chellaiah M.A., Biswas R.S., Rittling S.R., Denhardt D.T., and Hruska K.A. Rho-dependent Rho kinase activation increases CD44 surface expression and bone resorption in osteoclasts. J. Biol. Chem. 278 (2003) 29086-29097
19. Chellaiah M.A., Kizer N., Biswas R., Alvarez U., Strauss-Schoenberger J., Rifas L., Rittling S.R., Denhardt D.T., and Hruska K.A. Osteopontin deficiency produces osteoclast dysfunction due to reduced CD44 surface expression. Mol. Biol. Cell 14 (2003) 173-189
20. Chellaiah M.A., Kuppuswamy D., Lasky L., and Linder S. Phosphorylation of a Wiscott-Aldrich syndrome protein-associated signal complex is critical in osteoclast bone resorption. J. Biol. Chem. 282 (2007) 10104-10116
21. Chou H.C., Anton I.M., Holt M.R., Curcio C., Lanzardo S., Worth A., Burns S., Thrasher A.J., Jones G.E., and Calle Y. WIP regulates the stability and localization of WASP to podosomes in migrating dendritic cells. Curr. Biol. 16 (2006) 2337-2344
22. Chuang Y.Y., Valster A., Coniglio S.J., Backer J.M., and Symons M. The atypical Rho family GTPase Wrch-1 regulates focal adhesion formation and cell migration. J. Cell Sci. 120 (2007) 1927-1934
23. Collin O., Tracqui P., Stephanou A., Usson Y., Clement-Lacroix J., and Planus E. Spatiotemporal dynamics of actin-rich adhesion microdomains: influence of substrate flexibility. J. Cell Sci. 119 (2006) 1914-1925
24. David-Pfeuty T., and Singer S.J. Altered distributions of the cytoskeletal proteins vinculin and alpha-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proc. Natl. Acad. Sci. USA 77 (1980) 6687-6691
25. de la Fuente M.A., Sasahara Y., Calamito M., Anton I.M., Elkhal A., Gallego M.D., Suresh K., Siminovitch K., Ochs H.D., Anderson K.C., Rosen F.S., Geha R.S., and Ramesh N. WIP is a chaperone for Wiskott-Aldrich syndrome protein (WASP). Proc. Natl. Acad. Sci. USA 104 (2007) 926-931
26. de Rooij J., Kerstens A., Danuser G., Schwartz M.A., and Waterman-Storer C.M. Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 171 (2005) 153-164
27. Destaing O., Saltel F., Geminard J.C., Jurdic P., and Bard F. Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14 (2003) 407-416
28. Destaing O., Saltel F., Gilquin B., Chabadel A., Khochbin S., Ory S., and Jurdic P. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 118 (2005) 2901-2911
29. Destaing O., Sanjay A., Itzstein C., Horne W.C., Toomre D., Camilli P.D., and Baron R. The tyrosine kinase activity of c-Src regulates actin dynamics and organization of podosomes in osteoclasts. Mol. Biol. Cell 19 (2008) 394-404
30. Duong L.T., Lakkakorpi P.T., Nakamura I., Machwate M., Nagy R.M., and Rodan G.A. PYK2 in osteoclasts is an adhesion kinase, localized in the sealing zone, activated by ligation of alpha(v)beta3 integrin, and phosphorylated by src kinase. J. Clin. Invest. 102 (1998) 881-892
31. Faccio R., Grano M., Colucci S., Villa A., Giannelli G., Quaranta V., and Zallone A. Localization and possible role of two different alpha v beta 3 integrin conformations in resting and resorbing osteoclasts. J. Cell Sci. 115 (2002) 2919-2929
32. Faccio R., Novack D.V., Zallone A., Ross F.P., and Teitelbaum S.L. Dynamic changes in the osteoclast cytoskeleton in response to growth factors and cell attachment are controlled by beta3 integrin. J. Cell Biol. 162 (2003) 499-509
33. Faccio R., Teitelbaum S.L., Fujikawa K., Chappel J., Zallone A., Tybulewicz V.L., Ross F.P., and Swat W. Vav3 regulates osteoclast function and bone mass. Nature Med. 11 (2005) 284-290
34. Fincham V.J., Chudleigh A., and Frame M.C. Regulation of p190 Rho-GAP by v-Src is linked to cytoskeletal disruption during transformation. J. Cell Sci. 112 (1999) 947-956
35. Flevaris P., Stojanovic A., Gong H., Chishti A., Welch E., and Du X. A molecular switch that controls cell spreading and retraction. J. Cell Biol. 179 (2007) 553-565
36. Fukata M., Nakagawa M., and Kaibuchi K. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr. Opin. Cell Biol. 15 (2003) 590-597
37. Gil-Henn H., Destaing O., Sims N.A., Aoki K., Alles N., Neff L., Sanjay A., Bruzzaniti A., De Camilli P., Baron R., and Schlessinger J. Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J. Cell Biol. 178 (2007) 1053-1064
38. Gringel A., Walz D., Rosenberger G., Minden A., Kutsche K., Kopp P., and Linder S. PAK4 and alphaPIX determine podosome size and number in macrophages through localized actin regulation. J. Cell. Physiol. 209 (2006) 568-579
39. Gupton S.L., and Waterman-Storer C.M. Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125 (2006) 1361-1374
40. Hayer S., Steiner G., Gortz B., Reiter E., Tohidast-Akrad M., Amling M., Hoffmann O., Redlich K., Zwerina J., Skriner K., Hilberg F., Wagner E.F., Smolen J.S., and Schett G. CD44 is a determinant of inflammatory bone loss. J. Exp. Med. 201 (2005) 903-914
41. Jurdic P., Saltel F., Chabadel A., and Destaing O. Podosome and sealing zone: specificity of the osteoclast model. Eur. J. Cell Biol. 85 (2006) 195-202
42. Kulkarni S., Goll D.E., and Fox J.E. Calpain cleaves RhoA generating a dominant-negative form that inhibits integrin-induced actin filament assembly and cell spreading. Int. J. Biol. Chem. Cell Biol. 277 (2002) 24435-24441
43. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17 (2007) 107-117
44. Linder S., and Aepfelbacher M. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13 (2003) 376-385
45. Linder S., Nelson D., Weiss M., and Aepfelbacher M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96 (1999) 9648-9653
46. Linder S., Higgs H., Hufner K., Schwarz K., Pannicke U., and Aepfelbacher M. The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J. Immunol. 165 (2000) 221-225
47. Luxenburg C., Geblinger D., Klein E., Anderson K., Hanein D., Geiger B., and Addadi L. The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS ONE 2 (2007) e179
48. Marchisio P.C., Cirillo D., Naldini L., Primavera M.V., Teti A., and Zambonin-Zallone A. Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J. Cell Biol. 99 (1984) 1696-1705
49. Marzia M., Chiusaroli R., Neff L., Kim N.Y., Chishti A.H., Baron R., and Horne W.C. Calpain is required for normal osteoclast function and is down-regulated by calcitonin. J. Biol. Chem. 281 (2006) 9745-9754
50. McHugh K.P., Hodivala-Dilke K., Zheng M.H., Namba N., Lam J., Novack D., Feng X., Ross F.P., Hynes R.O., and Teitelbaum S.L. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J. Clin. Invest. 105 (2000) 433-440
51. Meller N., Merlot S., and Guda C. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118 (2005) 4937-4946
52. Miyauchi A., Hruska K.A., Greenfield E.M., Duncan R., Alvarez J., Barattolo R., Colucci S., Zambonin-Zallone A., Teitelbaum S.L., and Teti A. Osteoclast cytosolic calcium, regulated by voltage-gated calcium channels and extracellular calcium, controls podosome assembly and bone resorption. J. Cell Biol. 111 (1990) 2543-2552
53. Moore C.A., Parkin C.A., Bidet Y., and Ingham P.W. A role for the myoblast city homologues Dock1 and Dock5 and the adaptor proteins Crk and Crk-like in zebrafish myoblast fusion. Development 134 (2007) 3145-3153
54. Ory S., Munari-Silem Y., Fort P., and Jurdic P. Rho and Rac exert antagonistic functions on spreading of macrophage-derived multinucleated cells and are not required for actin fiber formation. J. Cell Sci. 113 (2000) 1177-1188
55. Ory S., Brazier H., and 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 99 (2007) 701-716
56. Pfaff M., and Jurdic P. Podosomes in osteoclast-like cells: structural analysis and cooperative roles of paxillin, proline-rich tyrosine kinase 2 (Pyk2) and integrin alphaVbeta3. J. Cell Sci. 114 (2001) 2775-2786
57. Raftopoulou M., and Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 265 (2004) 23-32
58. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., and Kirschner M.W. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97 (1999) 221-231
59. Ross F.P., and Teitelbaum S.L. alphavbeta3 and macrophage colony-stimulating factor: partners in osteoclast biology. Immunol. Rev. 208 (2005) 88-105
60. Rossman K.L., Der C.J., and Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6 (2005) 167-180
61. Ruusala A., and Aspenström P. The atypical Rho GTPase Wrch1 collaborates with the nonreceptor tyrosine kinases Pyk2 and Src in regulating cytoskeletal dynamics. Mol. Cell. Biol. 28 (2008) 1802-1814
62. Saltel F., Destaing O., Bard F., Eichert D., and Jurdic P. Apatite-mediated actin dynamics in resorbing osteoclasts. Mol. Biol. Cell 15 (2004) 5231-5241
63. Sanjay A., Houghton A., Neff L., DiDomenico E., Bardelay C., Antoine E., Levy J., Gailit J., Bowtell D., Horne W.C., and Baron R. Cbl associates with Pyk2 and Src to regulate Src kinase activity, alpha(v)beta(3) integrin-mediated signaling, cell adhesion, and osteoclast motility. J. Cell Biol. 152 (2001) 181-195
64. Saras J., Wollberg P., and Aspenström P. Wrch1 is a GTPase-deficient Cdc42-like protein with unusual binding characteristics and cellular effects. Exp. Cell Res. 299 (2004) 356-369
65. Shutes A., Berzat A.C., Cox A.D., and Der C.J. Atypical mechanism of regulation of the Wrch-1 Rho family small GTPase. Curr. Biol. 14 (2004) 2052-2056
66. Solon J., Levental I., Sengupta K., Georges P.C., and Janmey P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93 (2007) 4453-4461
67. Soriano P., Montgomery C., Geske R., and Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64 (1991) 693-702
68. Tarone G., Cirillo D., Giancotti F.G., Comoglio P.M., and Marchisio P.C. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp. Cell Res. 159 (1985) 141-157
69. ten Klooster J.P., Jaffer Z.M., Chernoff J., and Hordijk P.L. Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J. Cell Biol. 172 (2006) 759-769
70. Turner M., and Billadeau D.D. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2 (2002) 476-486
71. 2+ channel TRPV5 is essential for proper osteoclastic bone resorption. Proc. Natl. Acad. Sci. USA 102 (2005) 17507-17512
72. Zhang D., Udagawa N., Nakamura I., Murakami H., Saito S., Yamasaki K., Shibasaki Y., Morii N., Narumiya S., Takahashi N., and Suda T. The small GTP-binding protein, rho p21, is involved in bone resorption by regulating cytoskeletal organization in osteoclasts. J. Cell Sci. 108 (1995) 2285-2292
73. Zicha D., Allen W.E., Brickell P.M., Kinnon C., Dunn G.A., Jones G.E., and Thrasher A.J. Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome. Br. J. Haematol. 101 (1998) 659-665
74. Zrihan-Licht S., Fu Y., Settleman J., Schinkmann K., Shaw L., Keydar I., Avraham S., and Avraham H. RAFTK/Pyk2 tyrosine kinase mediates the association of p190 RhoGAP with RasGAP and is involved in breast cancer cell invasion. Oncogene 19 (2000) 1318-1328