Podosome organization drives osteoclast-mediated bone resorption

Cell Adhesion and Migration

Volumn 8, Issue 3, 2014, Pages 192-204

  Georgess, Dan ^a   Machuca Gayet, Irma ^a   Blangy, Anne ^b   Jurdic, Pierre ^a  

^a UNIVERSITÉ DE LYON   (France)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

Actin; Actin rings; Bone degradation; Migration; Osteoclasts; Podosomes; Sealing zone

Indexed keywords

INTEGRIN; RAC PROTEIN; RHO FACTOR;

ACIDIFICATION; BONE DEFECT; CELL ADHESION; CELL FUNCTION; CELL LINEAGE; CELL MIGRATION; CELL STRUCTURE; CELL SURVIVAL; DYNAMICS; HUMAN; MOLECULE; MONOCYTE; MULTINUCLEAR CELL; MUSCLE CONTRACTILITY; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PODOSOME; POLARIZATION; POLYMERIZATION; PROTEIN DEGRADATION; REGULATORY MECHANISM; REVIEW; ACTIN FILAMENT; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ACTIN CYTOSKELETON; ANIMALS; BONE RESORPTION; CELL ADHESION; CELL DIFFERENTIATION; HUMANS; OSTEOCLASTS;

EID: 84901422239     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.27840     Document Type: Review

References (130)

1. Bartl R. Osteoporosis: diagnosis, prevention, therapy. New York: Springer, 2009.
2. Harre U, Schett G. Bone research in 2012: the ups and downs of bone in health and rheumatic disease. Nat Rev Rheumatol 2013; 9:67-8; PMID:23296393; http://dx.doi.org/10.1038/nrrheum.2012.219
3. Harre U, Georgess D, Bang H, Bozec A, Axmann R, Ossipova E, Jakobsson PJ, Baum W, Nimmerjahn F, Szarka E, et al. Induction of osteoclastogenesis and bone loss by human autoantibodies against citrullinated vimentin. J Clin Invest 2012; 122:1791-802; PMID:22505457; http://dx.doi.org/10.1172/JCI60975
4. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365:2205-19; PMID:22150039; http://dx.doi.org/10.1056/NEJMra1004965
5. Lazner F, Gowen M, Pavasovic D, Kola I. Osteopetrosis and osteoporosis: two sides of the same coin. Hum Mol Genet 1999; 8:1839-46; PMID:10469835; http://dx.doi.org/10.1093/hmg/8.10.1839
6. Geissmann F. The origin of dendritic cells. Nat Immunol 2007; 8:558-60; PMID:17514208; http://dx.doi.org/10.1038/ni0607-558
7. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 1998; 93:165-76; PMID:9568710; http://dx.doi.org/10.1016/S0092-8674(00)81569-X
8. Fuller K, Wong B, Fox S, Choi Y, Chambers TJ. TRANCE is necessary and sufficient for osteoblastmediated activation of bone resorption in osteoclasts. J Exp Med 1998; 188:997-1001; PMID:9730902; http://dx.doi.org/10.1084/jem.188.5.997
9. Matsuzaki K, Udagawa N, Takahashi N, Yamaguchi K, Yasuda H, Shima N, Morinaga T, Toyama Y, Yabe Y, Higashio K, et al. Osteoclast differentiation factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochem Biophys Res Commun 1998; 246:199-204; PMID:9600092; http://dx.doi.org/10.1006/bbrc.1998.8586
10. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, Tomoyasu A, Yano K, Goto M, Murakami A, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 1998; 95:3597-602; PMID:9520411; http://dx.doi.org/10.1073/pnas.95.7.3597
11. Gallois A, Lachuer J, Yvert G, Wierinckx A, Brunet F, Rabourdin-Combe C, Delprat C, Jurdic P, Mazzorana M. Genome-wide expression analyses establish dendritic cells as a new osteoclast precursor able to generate bone-resorbing cells more efficiently than monocytes. J Bone Miner Res 2010; 25:661-72; PMID:19775202; http://dx.doi.org/10.1359/jbmr.090829
12. Rivollier A, Mazzorana M, Tebib J, Piperno M, Aitsiselmi T, Rabourdin-Combe C, Jurdic P, Servet-Delprat C. Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood 2004; 104:4029-37; PMID:15308576; http://dx.doi.org/10.1182/blood-2004-01-0041
13. Servet-Delprat C, Arnaud S, Jurdic P, Nataf S, Grasset MF, Soulas C, Domenget C, Destaing O, Rivollier A, Perret M, et al. Flt3+ macrophage precursors commit sequentially to osteoclasts, dendritic cells and microglia. BMC Immunol 2002; 3:15; PMID:12398794; http://dx.doi.org/10.1186/1471-2172-3-15
14. Speziani C, Rivollier A, Gallois A, Coury F, Mazzorana M, Azocar O, Flacher M, Bella C, Tebib J, Jurdic P, et al. Murine dendritic cell transdifferentiation into osteoclasts is differentially regulated by innate and adaptive cytokines. Eur J Immunol 2007; 37:747-57; PMID:17304626; http://dx.doi.org/10.1002/eji.200636534
15. Wakkach A, Mansour A, Dacquin R, Coste E, Jurdic P, Carle GF, Blin-Wakkach C. Bone marrow microenvironment controls the in vivo differentiation of murine dendritic cells into osteoclasts. Blood 2008; 112:5074-83; PMID:18768394; http://dx.doi.org/10.1182/blood-2008-01-132787
16. Horowitz MC, Lorenzo JA. The origins of osteoclasts. Curr Opin Rheumatol 2004; 16:464-8; PMID:15201612; http://dx.doi.org/10.1097/01.bor.0000127825.05580.eb
17. Jacome-Galarza CE, Lee SK, Lorenzo JA, Aguila HL. Identification, characterization, and isolation of a common progenitor for osteoclasts, macrophages, and dendritic cells from murine bone marrow and periphery. J Bone Miner Res 2013; 28:1203-13; PMID:23165930; http://dx.doi.org/10.1002/jbmr.1822
18. Otero K, Shinohara M, Zhao H, Cella M, Gilfillan S, Colucci A, Faccio R, Ross FP, Teitelbaum SL, Takayanagi H, et al. TREM2 and β-catenin regulate bone homeostasis by controlling the rate of osteoclastogenesis. J Immunol 2012; 188:2612-21; PMID:22312126; http://dx.doi.org/10.4049/jimmunol.1102836
19. Zhao B, Ivashkiv LB. Negative regulation of osteoclastogenesis and bone resorption by cytokines and transcriptional repressors. Arthritis Res Ther 2011; 13:234; PMID:21861861; http://dx.doi.org/10.1186/ar3379
20. Nakashima T, Takayanagi H. New regulation mechanisms of osteoclast differentiation. Ann N Y Acad Sci 2011; 1240:E13-8; PMID:22360322; http://dx.doi.org/10.1111/j.1749-6632.2011.06373.x
21. Takayanagi H. The role of NFAT in osteoclast formation. Ann N Y Acad Sci 2007; 1116:227-37; PMID:18083930; http://dx.doi.org/10.1196/annals.1402.071
22. Dougall WC, Glaccum M, Charrier K, Rohrbach K, Brasel K, De Smedt T, Daro E, Smith J, Tometsko ME, Maliszewski CR, et al. RANK is essential for osteoclast and lymph node development. Genes Dev 1999; 13:2412-24; PMID:10500098; http://dx.doi.org/10.1101/gad.13.18.2412
23. Pettit AR, Ji H, von Stechow D, Müller R, Goldring SR, Choi Y, Benoist C, Gravallese EM. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 2001; 159:1689-99; PMID:11696430; http://dx.doi.org/10.1016/S0002-9440(10)63016-7
24. O'Brien CA, Nakashima T, Takayanagi H. Osteocyte control of osteoclastogenesis. Bone 2013; 54:258-63; PMID:22939943; http://dx.doi.org/10.1016/j.bone.2012.08.121
25. Coxon FP, Taylor A. Vesicular trafficking in osteoclasts. Semin Cell Dev Biol 2008; 19:424-33; PMID:18768162; http://dx.doi.org/10.1016/j.semcdb.2008.08.004
26. Mulari M, Vääräniemi J, Väänänen HK. Intracellular membrane trafficking in bone resorbing osteoclasts. Microsc Res Tech 2003; 61:496-503; PMID:12879417; http://dx.doi.org/10.1002/jemt.10371
27. Yadav VK, Oury F, Tanaka KF, Thomas T, Wang Y, Cremers S, Hen R, Krust A, Chambon P, Karsenty G. Leptin-dependent serotonin control of appetite: temporal specificity, transcriptional regulation, and therapeutic implications. J Exp Med 2011; 208:41-52; PMID:21187319; http://dx.doi.org/10.1084/jem.20101940
28. Abu-Amer Y, Ross FP, Schlesinger P, Tondravi MM, Teitelbaum SL. Substrate recognition by osteoclast precursors induces C-src/microtubule association. J Cell Biol 1997; 137:247-58; PMID:9105052; http://dx.doi.org/10.1083/jcb.137.1.247
29. Mulari MT, Zhao H, Lakkakorpi PT, Väänänen HK. Osteoclast ruff led border has distinct subdomains for secretion and degraded matrix uptake. Traffic 2003; 4:113-25; PMID:12559037; http://dx.doi.org/10.1034/j.1600-0854.2003.40206.x
30. Karsdal MA, Henriksen K, Sørensen MG, Gram J, Schaller S, Dziegiel MH, Heegaard AM, Christophersen P, Martin TJ, Christiansen C, et al. Acidification of the osteoclastic resorption compartment provides insight into the coupling of bone formation to bone resorption. Am J Pathol 2005; 166:467-76; PMID:15681830; http://dx.doi.org/10.1016/S0002-9440(10)62269-9
31. Rousselle AV, Heymann D. Osteoclastic acidification pathways during bone resorption. Bone 2002; 30:533-40; PMID:11934642; http://dx.doi.org/10.1016/S8756-3282(02)00672-5
32. Silver IA, Murrills RJ, Etherington DJ. Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 1988; 175:266-76; PMID:3360056; http://dx.doi.org/10.1016/0014-4827(88)90191-7
33. Baron R, Neff L, Louvard D, Courtoy PJ. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruff led border. J Cell Biol 1985; 101:2210-22; PMID:3905822; http://dx.doi.org/10.1083/jcb.101.6.2210
34. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 2010; 142:296-308; PMID:20655470; http://dx.doi.org/10.1016/j.cell.2010.06.003
35. Linder S, Wiesner C, Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 2011; 27:185-211; PMID:21801014; http://dx.doi.org/10.1146/annurev-cellbio-092910-154216
36. Rottiers P, Saltel F, Daubon T, Chaigne-Delalande B, Tridon V, Billottet C, Reuzeau E, Génot E. TGFbeta-induced endothelial podosomes mediate basement membrane collagen degradation in arterial vessels. J Cell Sci 2009; 122:4311-8; PMID:19887587; http://dx.doi.org/10.1242/jcs.057448
37. Saltel F, Daubon T, Juin A, Ganuza IE, Veillat V, Génot E. Invadosomes: intriguing structures with promise. Eur J Cell Biol 2011; 90:100-7; PMID:20605056; http://dx.doi.org/10.1016/j.ejcb.2010.05.011
38. Jurdic P, Saltel F, Chabadel A, Destaing O. Podosome and sealing zone: specificity of the osteoclast model. Eur J Cell Biol 2006; 85:195-202; PMID:16546562; http://dx.doi.org/10.1016/j.ejcb.2005.09.008
39. Destaing O, Saltel F, Géminard JC, Jurdic P, Bard F. Podosomes display actin turnover and dynamic selforganization in osteoclasts expressing actin-green fluorescent protein. Mol Biol Cell 2003; 14:407-16; PMID:12589043; http://dx.doi.org/10.1091/mbc.E02-07-0389
40. Labernadie A, Thibault C, Vieu C, Maridonneau- Parini I, Charrière GM. Dynamics of podosome stiffness revealed by atomic force microscopy. Proc Natl Acad Sci U S A 2010; 107:21016-21; PMID:21081699; http://dx.doi.org/10.1073/pnas.1007835107
41. Linder S, Wiesner C, Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 2011; 27:185-211; PMID:21801014; http://dx.doi.org/10.1146/annurev-cellbio-092910-154216
42. 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; PMID:17264882; http://dx.doi.org/10.1371/journal.pone.0000179
43. Schmidt S, Nakchbandi I, Ruppert R, Kawelke N, Hess MW, Pfaller K, Jurdic P, Fässler R, Moser M. Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J Cell Biol 2011; 192:883-97; PMID:21357746; http://dx.doi.org/10.1083/jcb.201007141
44. Gluckman E, Esperou H, Devergie A, Traineau R, Leverger G, Schaison G. Pediatric bone marrow transplantation for leukemia and aplastic anemia. Report of 222 cases transplanted in a single center. Nouv Rev Fr Hematol 1989; 31:111-4; PMID:2671924
45. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, Rayburn H, Crowley D, Ullman-Culleré M, Ross FP, Coller BS, Teitelbaum S, Hynes RO. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 1999; 103:229-38; PMID:9916135; http://dx.doi.org/10.1172/JCI5487
46. McHugh KP, Hodivala-Dilke K, Zheng MH, Namba N, Lam J, Novack D, Feng X, Ross FP, Hynes RO, Teitelbaum SL. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 2000; 105:433-40; PMID:10683372; http://dx.doi.org/10.1172/JCI8905
47. Faccio R, Novack DV, Zallone A, Ross FP, Teitelbaum SL. Dynamic changes in the osteoclast cytoskeleton in response to growth factors and cell attachment are controlled by beta3 integrin. J Cell Biol 2003; 162:499-509; PMID:12900398; http://dx.doi.org/10.1083/jcb.200212082
48. Destaing O, Planus E, Bouvard D, Oddou C, Badowski C, Bossy V, Raducanu A, Fourcade B, Albiges-Rizo C, Block MR. β1A integrin is a master regulator of invadosome organization and function. Mol Biol Cell 2010; 21:4108-19; PMID:20926684; http://dx.doi.org/10.1091/mbc.E10-07-0580
49. Nesbitt S, Nesbit A, Helfrich M, Horton M. Biochemical characterization of human osteoclast integrins. Osteoclasts express alpha v beta 3, alpha 2 beta 1, and alpha v beta 1 integrins. J Biol Chem 1993; 268:16737-45; PMID:8344953
50. Calderwood DA. Integrin activation. J Cell Sci 2004; 117:657-66; PMID:14754902; http://dx.doi.org/10.1242/jcs.01014
51. Zou W, Izawa T, Zhu T, Chappel J, Otero K, Monkley SJ, Critchley DR, Petrich BG, Morozov A, Ginsberg MH, et al. Talin1 and Rap1 are critical for osteoclast function. Mol Cell Biol 2013; 33:830-44; PMID:23230271; http://dx.doi.org/10.1128/MCB.00790-12
52. Winkler J, Lünsdorf H, Jockusch BM. Energy-filtered electron microscopy reveals that talin is a highly flexible protein composed of a series of globular domains. Eur J Biochem 1997; 243:430-6; PMID:9030769; http://dx.doi.org/10.1111/j.1432-1033.1997.0430a.x
53. Papagrigoriou E, Gingras AR, Barsukov IL, Bate N, Fillingham IJ, Patel B, Frank R, Ziegler WH, Roberts GC, Critchley DR, et al. Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle. EMBO J 2004; 23:2942-51; PMID:15272303; http://dx.doi.org/10.1038/sj.emboj.7600285
54. Jockusch BM, Rüdiger M. Crosstalk between cell adhesion molecules: vinculin as a paradigm for regulation by conformation. Trends Cell Biol 1996; 6:311-5; PMID:15157439; http://dx.doi.org/10.1016/0962-8924(96)10022-2
55. Turner CE, Glenney JR Jr., Burridge K. Paxillin: a new vinculin-binding protein present in focal adhesions. J Cell Biol 1990; 111:1059-68; PMID:2118142; http://dx.doi.org/10.1083/jcb.111.3.1059
56. Wu H, Parsons JT. Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J Cell Biol 1993; 120:1417-26; PMID:7680654; http://dx.doi.org/10.1083/jcb.120.6.1417
57. Calle Y, Chou HC, Thrasher AJ, Jones GE. Wiskott-Aldrich syndrome protein and the cytoskeletal dynamics of dendritic cells. J Pathol 2004; 204:460-9; PMID:15495215; http://dx.doi.org/10.1002/path.1651
58. Monypenny J, Chou HC, Bañón-Rodríguez I, Thrasher AJ, Antón IM, Jones GE, Calle Y. Role of WASP in cell polarity and podosome dynamics of myeloid cells. Eur J Cell Biol 2011; 90:198-204; PMID:20609498; http://dx.doi.org/10.1016/j.ejcb.2010.05.009
59. Kinley AW, Weed SA, Weaver AM, Karginov AV, Bissonette E, Cooper JA, Parsons JT. Cortactin interacts with WIP in regulating Arp2/3 activation and membrane protrusion. Curr Biol 2003; 13:384-93; PMID:12620186; http://dx.doi.org/10.1016/S0960-9822(03)00107-6
60. Antón IM, Jones GE, Wandosell F, Geha R, Ramesh N. WASP-interacting protein (WIP): working in polymerisation and much more. Trends Cell Biol 2007; 17:555-62; PMID:17949983; http://dx.doi.org/10.1016/j.tcb.2007.08.005
61. Krzewski K, Chen X, Orange JS, Strominger JL. Formation of a WIP-, WASp-, actin-, and myosin IIA-containing multiprotein complex in activated NK cells and its alteration by KIR inhibitory signaling. J Cell Biol 2006; 173:121-32; PMID:16606694; http://dx.doi.org/10.1083/jcb.200509076
62. de la Fuente MA, Sasahara Y, Calamito M, Antón IM, Elkhal A, Gallego MD, Suresh K, Siminovitch K, Ochs HD, Anderson KC, et al. WIP is a chaperone for Wiskott-Aldrich syndrome protein (WASP). Proc Natl Acad Sci U S A 2007; 104:926-31; PMID:17213309; http://dx.doi.org/10.1073/pnas.0610275104
63. Chabadel A, Bañon-Rodríguez I, Cluet D, Rudkin BB, Wehrle-Haller B, Genot E, Jurdic P, Anton IM, Saltel F. CD44 and beta3 integrin organize two functionally distinct actin-based domains in osteoclasts. Mol Biol Cell 2007; 18:4899-910; PMID:17898081; http://dx.doi.org/10.1091/mbc.E07-04-0378
64. Goodison S, Urquidi V, Tarin D. CD44 cell adhesion molecules. Mol Pathol 1999; 52:189-96; PMID:10694938; http://dx.doi.org/10.1136/mp.52.4.189
65. Destaing O, Sanjay A, Itzstein C, Horne WC, 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; PMID:17978100; http://dx.doi.org/10.1091/mbc.E07-03-0227
66. Mersich AT, Miller MR, Chkourko H, Blystone SD. The formin FRL1 (FMNL1) is an essential component of macrophage podosomes. Cytoskeleton (Hoboken) 2010; 67:573-85; PMID:20617518; http://dx.doi.org/10.1002/cm.20468
67. Luxenburg C, Winograd-Katz S, Addadi L, Geiger B. Involvement of actin polymerization in podosome dynamics. J Cell Sci 2012; 125:1666-72; PMID:22328507; http://dx.doi.org/10.1242/jcs.075903
68. Wanger M, Keiser T, Neuhaus JM, Wegner A. The actin treadmill. Can J Biochem Cell Biol 1985; 63:414-21; PMID:3899328
69. Yin HL, Albrecht JH, Fattoum A. Identification of gelsolin, a Ca2+-dependent regulatory protein of actin gel-sol transformation, and its intracellular distribution in a variety of cells and tissues. J Cell Biol 1981; 91:901-6; PMID:6276414; http://dx.doi.org/10.1083/jcb.91.3.901
70. Southwick FS. Gelsolin and ADF/cofilin enhance the actin dynamics of motile cells. Proc Natl Acad Sci U S A 2000; 97:6936-8; PMID:10860951; http://dx.doi.org/10.1073/pnas.97.13.6936
71. Zallone AZ, Teti A, Primavera MV, Naldini L, Marchisio PC. Osteoclasts and monocytes have similar cytoskeletal structures and adhesion property in vitro. J Anat 1983; 137:57-70; PMID:6355036
72. Marchisio PC, Cirillo D, Naldini L, Primavera MV, Teti A, Zambonin-Zallone A. Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J Cell Biol 1984; 99:1696-705; PMID:6436255; http://dx.doi.org/10.1083/jcb.99.5.1696
73. Duong LT, Lakkakorpi P, Nakamura I, Rodan GA. Integrins and signaling in osteoclast function. Matrix Biol 2000; 19:97-105; PMID:10842093; http://dx.doi.org/10.1016/S0945-053X(00)00051-2
74. Chellaiah M, Kizer N, Silva M, Alvarez U, Kwiatkowski D, Hruska KA. Gelsolin deficiency blocks podosome assembly and produces increased bone mass and strength. J Cell Biol 2000; 148:665-78; PMID:10684249; http://dx.doi.org/10.1083/jcb.148.4.665
75. Touaitahuata H, Planus E, Albiges-Rizo C, Blangy A, Pawlak G. Podosomes are dispensable for osteoclast differentiation and migration. Eur J Cell Biol 2013; 92:139-49; PMID:23598086; http://dx.doi.org/10.1016/j.ejcb.2013.03.001
76. Blangy A, Touaitahuata H, Cres G, Pawlak G. Cofilin activation during podosome belt formation in osteoclasts. PLoS One 2012; 7:e45909; PMID:23049890; http://dx.doi.org/10.1371/journal.pone.0045909
77. van den Dries K, Meddens MBM, de Keijzer S, Shekhar S, Subramaniam V, Figdor CG, Cambi A. Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat Commun 2013; 4:1412; PMID:23361003; http://dx.doi.org/10.1038/ncomms2402
78. Hu S, Biben T, Wang X, Jurdic P, Géminard JC. Internal dynamics of actin structures involved in the cell motility and adhesion: Modeling of the podosomes at the molecular level. J Theor Biol 2011; 270:25-30; PMID:21075123; http://dx.doi.org/10.1016/j.jtbi.2010.11.014
79. Moreau V, Tatin F, Varon C, Génot E. Actin can reorganize into podosomes in aortic endothelial cells, a process controlled by Cdc42 and RhoA. Mol Cell Biol 2003; 23:6809-22; PMID:12972601; http://dx.doi.org/10.1128/MCB.23.19.6809-6822.2003
80. Kaverina I, Stradal TE, Gimona M. Podosome formation in cultured A7r5 vascular smooth muscle cells requires Arp2/3-dependent de-novo actin polymerization at discrete microdomains. J Cell Sci 2003; 116:4915-24; PMID:14625385; http://dx.doi.org/10.1242/jcs.00818
81. Calle Y, Burns S, Thrasher AJ, Jones GE. The leukocyte podosome. Eur J Cell Biol 2006; 85:151-7; PMID:16546557; http://dx.doi.org/10.1016/j.ejcb.2005.09.003
82. Linder S, Nelson D, Weiss M, Aepfelbacher M. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci U S A 1999; 96:9648-53; PMID:10449748; http://dx.doi.org/10.1073/pnas.96.17.9648
83. Hammarfjord O, Falet H, Gurniak C, Hartwig JH, Wallin RP. Gelsolin-independent podosome formation in dendritic cells. PLoS One 2011; 6:e21615; PMID:21779330; http://dx.doi.org/10.1371/journal.pone.0021615
84. Cougoule C, Van Goethem E, Le Cabec V, Lafouresse F, Dupré L, Mehraj V, Mège JL, Lastrucci C, Maridonneau-Parini I. Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and to migrate in 3D environments. Eur J Cell Biol 2012; 91:938-49; PMID:22999511; http://dx.doi.org/10.1016/j.ejcb.2012.07.002
85. Bhuwania R, Cornfine S, Fang Z, Krüger M, Luna EJ, Linder S. Supervillin couples myosindependent contractility to podosomes and enables their turnover. J Cell Sci 2012; 125:2300-14; PMID:22344260; http://dx.doi.org/10.1242/jcs.100032
86. Bañón-Rodríguez I, Monypenny J, Ragazzini C, Franco A, Calle Y, Jones GE, Antón IM. The cortactin-binding domain of WIP is essential for podosome formation and extracellular matrix degradation by murine dendritic cells. Eur J Cell Biol 2011; 90:213-23; PMID:20952093; http://dx.doi.org/10.1016/j.ejcb.2010.09.001
87. Linder S, Hüfner K, Wintergerst U, Aepfelbacher M. Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J Cell Sci 2000; 113:4165-76; PMID:11069762
88. Destaing O, Saltel F, Gilquin B, Chabadel A, Khochbin S, Ory S, Jurdic P. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 2005; 118:2901-11; PMID:15976449; http://dx.doi.org/10.1242/jcs.02425
89. Biosse Duplan M, Zalli D, Stephens S, Zenger S, Neff L, Oelkers JM, Lai FP, Horne W, Rottner K, Baron R. Microtubule dynamic instability controls podosome patterning in osteoclasts through EB1, cortactin, and Src. Mol Cell Biol 2014; 34:16-29; PMID:24144981; http://dx.doi.org/10.1128/MCB.00578-13
90. Saltel F, Destaing O, Bard F, Eichert D, Jurdic P. Apatite-mediated actin dynamics in resorbing osteoclasts. Mol Biol Cell 2004; 15:5231-41; PMID:15371537; http://dx.doi.org/10.1091/mbc.E04-06-0522
91. Luxenburg C, Addadi L, Geiger B. The molecular dynamics of osteoclast adhesions. Eur J Cell Biol 2006; 85:203-11; PMID:16360241; http://dx.doi.org/10.1016/j.ejcb.2005.11.002
92. Luxenburg C, Parsons JT, Addadi L, Geiger B. Involvement of the Src-cortactin pathway in podosome formation and turnover during polarization of cultured osteoclasts. J Cell Sci 2006; 119:4878-88; PMID:17105771; http://dx.doi.org/10.1242/jcs.03271
93. Fuller K, Ross JL, Szewczyk KA, Moss R, Chambers TJ. Bone is not essential for osteoclast activation. PLoS One 2010; 5:e12837; PMID:20862258; http://dx.doi.org/10.1371/journal.pone.0012837
94. Luxenburg C, Winograd-Katz S, Addadi L, Geiger B. Involvement of actin polymerization in podosome dynamics. J Cell Sci 2012; 125:1666-72; PMID:22328507; http://dx.doi.org/10.1242/jcs.075903
95. Hu S, Planus E, Georgess D, Place C, Wang X, Albiges-Rizo C, Jurdic P, Géminard JC. Podosome rings generate forces that drive saltatory osteoclast migration. Mol Biol Cell 2011; 22:3120-6; PMID:21737683; http://dx.doi.org/10.1091/mbc.E11-01-0086
96. van den Dries K, Meddens MB, de Keijzer S, Shekhar S, Subramaniam V, Figdor CG, Cambi A. Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat Commun 2013; 4:1412; PMID:23361003; http://dx.doi.org/10.1038/ncomms2402
97. Georgess D, Mazzorana M, Terrado J, Delprat C, Chamot C, Guasch RM, Pérez-Roger I, Jurdic P, Machuca-Gayet I. Comparative transcriptomics reveal RhoE as a novel regulator of actin dynamics in bone-resorbing osteoclasts. Mol Biol Cell 2013; (Forthcoming); PMID:24284899; http://dx.doi.org/10.1091/mbc.E13-07-0363
98. Luxenburg C, Parsons JT, Addadi L, Geiger B. Involvement of the Src-cortactin pathway in podosome formation and turnover during polarization of cultured osteoclasts. J Cell Sci 2006; 119:4878-88; PMID:17105771; http://dx.doi.org/10.1242/jcs.03271
99. Soriano P, Montgomery C, Geske R, Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 1991; 64:693-702; PMID:1997203; http://dx.doi.org/10.1016/0092-8674(91)90499-O
100. Zou W, Kitaura H, Reeve J, Long F, Tybulewicz VL, Shattil SJ, Ginsberg MH, Ross FP, Teitelbaum SL. Syk, c-Src, the alphavbeta3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J Cell Biol 2007; 176:877-88; PMID:17353363; http://dx.doi.org/10.1083/jcb.200611083
101. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, Neff L, Sanjay A, Bruzzaniti A, De Camilli P, Baron R, et al. Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 2007; 178:1053-64; PMID:17846174; http://dx.doi.org/10.1083/jcb.200701148
102. Purev E, Neff L, Horne WC, Baron R. c-Cbl and Cbl-b act redundantly to protect osteoclasts from apoptosis and to displace HDAC6 from beta-tubulin, stabilizing microtubules and podosomes. Mol Biol Cell 2009; 20:4021-30; PMID:19641021; http://dx.doi.org/10.1091/mbc.E09-03-0248
103. Bruzzaniti A, Neff L, Sanjay A, Horne WC, De Camilli P, Baron R. Dynamin forms a Src kinasesensitive complex with Cbl and regulates podosomes and osteoclast activity. Mol Biol Cell 2005; 16:3301-13; PMID:15872089; http://dx.doi.org/10.1091/mbc.E04-12-1117
104. Bruzzaniti A, Neff L, Sandoval A, Du L, Horne WC, Baron R. Dynamin reduces Pyk2 Y402 phosphorylation and SRC binding in osteoclasts. Mol Cell Biol 2009; 29:3644-56; PMID:19380485; http://dx.doi.org/10.1128/MCB.00851-08
105. Faccio R, Teitelbaum SL, Fujikawa K, Chappel J, Zallone A, Tybulewicz VL, Ross FP, Swat W. Vav3 regulates osteoclast function and bone mass. Nat Med 2005; 11:284-90; PMID:15711558; http://dx.doi.org/10.1038/nm1194
106. Lowell CA, Soriano P. Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev 1996; 10:1845-57; PMID:8756343; http://dx.doi.org/10.1101/gad.10.15.1845
107. Horne WC, Neff L, Chatterjee D, Lomri A, Levy JB, Baron R. Osteoclasts express high levels of pp60csrc in association with intracellular membranes. J Cell Biol 1992; 119:1003-13; PMID:1385441; http://dx.doi.org/10.1083/jcb.119.4.1003
108. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS. Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 2004; 24:5269-80; PMID:15169891; http://dx.doi.org/10.1128/MCB.24.12.5269-5280.2004
109. Vérollet C, Gallois A, Dacquin R, Lastrucci C, Pandruvada SN, Ortega N, Poincloux R, Behar A, Cougoule C, Lowell C, et al. Hck contributes to bone homeostasis by controlling the recruitment of osteoclast precursors. FASEB J 2013; 27:3608-18; PMID:23742809; http://dx.doi.org/10.1096/fj.13-232736
110. Horne WC, Sanjay A, Bruzzaniti A, Baron R. The role(s) of Src kinase and Cbl proteins in the regulation of osteoclast differentiation and function. Immunol Rev 2005; 208:106-25; PMID:16313344; http://dx.doi.org/10.1111/j.0105-2896.2005.00335.x
111. Granot-Attas S, Luxenburg C, Finkelshtein E, Elson A. Protein tyrosine phosphatase epsilon regulates integrin-mediated podosome stability in osteoclasts by activating Src. Mol Biol Cell 2009; 20:4324-34; PMID:19692574; http://dx.doi.org/10.1091/mbc.E08-11-1158
112. Shivtiel S, Kollet O, Lapid K, Schajnovitz A, Goichberg P, Kalinkovich A, Shezen E, Tesio M, Netzer N, Petit I, et al. CD45 regulates retention, motility, and numbers of hematopoietic progenitors, and affects osteoclast remodeling of metaphyseal trabecules. J Exp Med 2008; 205:2381-95; PMID:18779349; http://dx.doi.org/10.1084/jem.20080072
113. Takeshita S, Namba N, Zhao JJ, Jiang Y, Genant HK, Silva MJ, Brodt MD, Helgason CD, Kalesnikoff J, Rauh MJ, et al. SHIP-deficient mice are severely osteoporotic due to increased numbers of hyperresorptive osteoclasts. Nat Med 2002; 8:943-9; PMID:12161749; http://dx.doi.org/10.1038/nm752
114. Hall A. Rho family GTPases. Biochem Soc Trans 2012; 40:1378-82; PMID:23176484; http://dx.doi.org/10.1042/BST20120103
115. Vega FM, Ridley AJ. Rho GTPases in cancer cell biology. FEBS Lett 2008; 582:2093-101; PMID:18460342; http://dx.doi.org/10.1016/j.febslet.2008.04.039
116. Zhang D, Udagawa N, Nakamura I, Murakami H, Saito S, Yamasaki K, Shibasaki Y, Morii N, Narumiya S, Takahashi N, et al. The small GTPbinding protein, rho p21, is involved in bone resorption by regulating cytoskeletal organization in osteoclasts. J Cell Sci 1995; 108:2285-92; PMID:7673348
117. Chellaiah MA, Soga N, Swanson S, McAllister S, Alvarez U, Wang D, Dowdy SF, Hruska KA. Rho-A is critical for osteoclast podosome organization, motility, and bone resorption. J Biol Chem 2000; 275:11993-2002; PMID:10766830; http://dx.doi.org/10.1074/jbc.275.16.11993
118. Ory S, Munari-Silem Y, Fort P, 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 2000; 113:1177-88; PMID:10704369
119. Wang Y, Lebowitz D, Sun C, Thang H, Grynpas MD, Glogauer M. Identifying the relative contributions of Rac1 and Rac2 to osteoclastogenesis. J Bone Miner Res 2008; 23:260-70; PMID:17922611; http://dx.doi.org/10.1359/jbmr.071013
120. Croke M, Ross FP, Korhonen M, Williams DA, Zou W, Teitelbaum SL. Rac deletion in osteoclasts causes severe osteopetrosis. J Cell Sci 2011; 124:3811-21; PMID:22114304; http://dx.doi.org/10.1242/jcs.086280
121. Razzouk S, Lieberherr M, Cournot G. Rac-GTPase, osteoclast cytoskeleton and bone resorption. Eur J Cell Biol 1999; 78:249-55; PMID:10350213; http://dx.doi.org/10.1016/S0171-9335(99)80058-2
122. Vives V, Laurin M, Cres G, Larrousse P, Morichaud Z, Noel D, Côté JF, Blangy A. The Rac1 exchange factor Dock5 is essential for bone resorption by osteoclasts. J Bone Miner Res 2011; 26:1099-110; PMID:21542010; http://dx.doi.org/10.1002/jbmr.282
123. Vives V, Laurin M, Cres G, Larrousse P, Morichaud Z, Noel D, Côté JF, Blangy A. The Rac1 exchange factor Dock5 is essential for bone resorption by osteoclasts. J Bone Miner Res 2011; 26:1099-110; PMID:21542010; http://dx.doi.org/10.1002/jbmr.282
124. Nagai Y, Osawa K, Fukushima H, Tamura Y, Aoki K, Ohya K, Yasuda H, Hikiji H, Takahashi M, Seta Y, et al. p130Cas, Crk-associated substrate, plays important roles in osteoclastic bone resorption. J Bone Miner Res 2013; 28:2449-62; PMID:23526406; http://dx.doi.org/10.1002/jbmr.1936
125. Susa M, Luong-Nguyen N-H, Cappellen D, Zamurovic N, Gamse R. Human primary osteoclasts: in vitro generation and applications as pharmacological and clinical assay. J Transl Med 2004; 2:6; PMID:15025786; http://dx.doi.org/10.1186/1479-5876-2-6
126. Novack DV, Faccio R. Osteoclast motility: putting the brakes on bone resorption. Ageing Res Rev 2011; 10:54-61; PMID:19788940; http://dx.doi.org/10.1016/j.arr.2009.09.005
127. Hefti T, Frischherz M, Spencer ND, Hall H, Schlottig F. A comparison of osteoclast resorption pits on bone with titanium and zirconia surfaces. Biomaterials 2010; 31:7321-31; PMID:20609470; http://dx.doi.org/10.1016/j.biomaterials.2010.06.009
128. Schilling AF, Linhart W, Filke S, Gebauer M, Schinke T, Rueger JM, Amling M. Resorbability of bone substitute biomaterials by human osteoclasts. Biomaterials 2004; 25:3963-72; PMID:15046886; http://dx.doi.org/10.1016/j.biomaterials.2003.10.079
129. Kikuta J, Wada Y, Kowada T, Wang Z, Sun-Wada GH, Nishiyama I, Mizukami S, Maiya N, Yasuda H, Kumanogoh A, et al. Dynamic visualization of RANKL and Th17-mediated osteoclast function. J Clin Invest 2013; 123:866-73; PMID:23321670
130. Coxon FP, Taylor A. Vesicular trafficking in osteoclasts. Semin Cell Dev Biol 2008; 19:424-33; PMID:18768162; http://dx.doi.org/10.1016/j.semcdb.2008.08.004