Cdc42 and Tks5: A minimal and universal molecular signature for functional invadosomes

Cell Adhesion and Migration

Volumn 8, Issue 3, 2014, Pages 280-292

  Di Martino, Julie ^a,b   Paysan, Lisa ^a,b   Gest, Caroline ^a,b   Lagrée, Valérie ^a,b   Juin, Amélie ^a,b,c   Saltel, Frédéric ^a,b   Moreau, Violaine ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

Actin cytoskeleton; Cdc42; Invadosomes; Invasion; Src; Tks5

Indexed keywords

PROTEIN; PROTEIN CDC42; PROTEIN TYROSINE KINASE; TKS5 PROTEIN; UNCLASSIFIED DRUG; FISH PROTEIN, MOUSE; PHOSPHOPROTEIN; SH3PXD2A PROTEIN, HUMAN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

3T3 CELL LINE; ACTIN FILAMENT; ARTICLE; CELL ORGANELLE; CELL TYPE; ENDOTHELIUM CELL; FEMALE; GENE OVEREXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; INVADOSOME; PROTEIN DEGRADATION; ANIMAL; CELL MOTION; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL MOVEMENT; EXTRACELLULAR MATRIX; HUMANS; MICE; MICROSCOPY, FLUORESCENCE; NIH 3T3 CELLS; PHOSPHOPROTEINS;

EID: 84907553011     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.28833     Document Type: Article

References (71)

1. Hoshino D, Branch KM, Weaver AM. Signaling inputs to invadopodia and podosomes. J Cell Sci 2013; 126:2979-89; PMID:23843616; http://dx.doi.org/10.1242/jcs.079475
2. Tatin F, Varon C, Génot E, Moreau V. A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci 2006; 119:769-81; PMID:16449321; http://dx.doi.org/10.1242/jcs.02787
3. Tatin F, Grise F, Reuzeau E, Genot E, Moreau V. Sodium fluoride induces podosome formation in endothelial cells. Biol Cell 2010; 102:489-98; PMID:20504277; http://dx.doi.org/10.1042/BC20100030
4. 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
5. Hai CM, Hahne P, Harrington EO, Gimona M. Conventional protein kinase C mediates phorbol-dibutyrate-induced cytoskeletal remodeling in a7r5 smooth muscle cells. Exp Cell Res 2002; 280:64-74; PMID:12372340; http://dx.doi.org/10.1006/excr.2002.5592
6. Osiak AE, Zenner G, Linder S. Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp Cell Res 2005; 307:342-53; PMID:15894313; http://dx.doi.org/10.1016/j.yexcr.2005.03.035
7. Varon C, Tatin F, Moreau V, Van Obberghen-Schilling E, Fernandez-Sauze S, Reuzeau E, Kramer I, Génot E. Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol Cell Biol 2006; 26:3582-94; PMID:16611998; http://dx.doi.org/10.1128/MCB.26.9.3582-3594.2006
8. Billottet C, Rottiers P, Tatin F, Varon C, Reuzeau E, Maître JL, Saltel F, Moreau V, Génot E. Regulatory signals for endothelial podosome formation. Eur J Cell Biol 2008; 87:543-54; PMID:18397815; http://dx.doi.org/10.1016/j.ejcb.2008.02.006
9. Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, Ohno-Machado L, Yang J. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 2011; 19:372-86; PMID:21397860; http://dx.doi.org/10.1016/j.ccr.2011.01.036
10. Pignatelli J, Tumbarello DA, Schmidt RP, Turner CE. Hic-5 promotes invadopodia formation and invasion during TGF-β-induced epithelial-mesenchymal transition. J Cell Biol 2012; 197:421-37; PMID:22529104; http://dx.doi.org/10.1083/jcb.201108143
11. Juin A, Billottet C, Moreau V, Destaing O, Albiges-Rizo C, Rosenbaum J, Génot E, Saltel F. Physiological type I collagen organization induces the formation of a novel class of linear invadosomes. Mol Biol Cell 2012; 23:297-309; PMID:22114353; http://dx.doi.org/10.1091/mbc.E11-07-0594
12. Yamaguchi H, Oikawa T. Membrane lipids in invadopodia and podosomes: key structures for cancer invasion and metastasis. Oncotarget 2010; 1:320-8; PMID:21307399
13. 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
14. Burns S, Thrasher AJ, Blundell MP, Machesky L, Jones GE. Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 2001; 98:1142-9; PMID:11493463; http://dx.doi.org/10.1182/blood.V98.4.1142
15. Mizutani K, Miki H, He H, Maruta H, Takenawa T. Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res 2002; 62:669-74; PMID:11830518
16. Lizárraga F, Poincloux R, Romao M, Montagnac G, Le Dez G, Bonne I, Rigaill G, Raposo G, Chavrier P. Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res 2009; 69:2792-800; PMID:19276357; http://dx.doi.org/10.1158/0008-5472.CAN-08-3709
17. Gardberg M, Kaipio K, Lehtinen L, Mikkonen P, Heuser VD, Talvinen K, Iljin K, Kampf C, Uhlen M, Grénman R, et al. FHOD1, a formin upregulated in epithelial-mesenchymal transition, participates in cancer cell migration and invasion. PLoS One 2013; 8:e74923; PMID:24086398; http://dx.doi.org/10.1371/journal.pone.0074923
18. Lagal V, Abrivard M, Gonzalez V, Perazzi A, Popli S, Verzeroli E, Tardieux I. Spire-1 a novel contributor of invadosome and associated invasive properties. J Cell Sci 2013; (Forthcoming)
19. Zhang D, Udagawa N, Nakamura I, Murakami H, Saito S, Yamasaki K, Shibasaki Y, Morii N, Narumiya S, Takahashi N, et al. The small GTP-binding protein, rho p21, is involved in bone resorption by regulating cytoskeletal organization in osteoclasts. J Cell Sci 1995; 108:2285-92; PMID:7673348
20. 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
21. Cougoule C, Carréno S, Castandet J, Labrousse A, Astarie-Dequeker C, Poincloux R, Le Cabec V, Maridonneau-Parini I. Activation of the lysosome-associated p61Hck isoform triggers the biogenesis of podosomes. Traffic 2005; 6:682-94; PMID:15998323; http://dx.doi.org/10.1111/j.1600-0854.2005.00307.x
22. Kuroiwa M, Oneyama C, Nada S, Okada M. The guanine nucleotide exchange factor Arhgef5 plays crucial roles in Src-induced podosome formation. J Cell Sci 2011; 124:1726-38; PMID:21525037; http://dx.doi.org/10.1242/jcs.080291
23. Goicoechea SM, Garcia-Mata R, Staub J, Valdivia A, Sharek L, McCulloch CG, Hwang RF, Urrutia R, Yeh JJ, Kim HJ, et al. Palladin promotes invasion of pancreatic cancer cells by enhancing invadopodia formation in cancer-associated fibroblasts. Oncogene 2014; 33:1265-73; PMID:23524582
24. Wheeler AP, Smith SD, Ridley AJ. CSF-1 and PI 3-kinase regulate podosome distribution and assembly in macrophages. Cell Motil Cytoskeleton 2006; 63:132-40; PMID:16421924; http://dx.doi.org/10.1002/cm.20111
25. Tarone G, Cirillo D, Giancotti FG, Comoglio PM, Marchisio PC. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp Cell Res 1985; 159:141-57; PMID:2411576; http://dx.doi.org/10.1016/S0014-4827(85)80044-6
26. Mader CC, Oser M, Magalhaes MA, Bravo-Cordero JJ, Condeelis J, Koleske AJ, Gil-Henn H. An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res 2011; 71:1730-41; PMID:21257711; http://dx.doi.org/10.1158/0008-5472.CAN-10-1432
27. Seiler C, Davuluri G, Abrams J, Byfield FJ, Janmey PA, Pack M. Smooth muscle tension induces invasive remodeling of the zebrafish intestine. PLoS Biol 2012; 10:e1001386; PMID:22973180; http://dx.doi.org/10.1371/journal.pbio.1001386
28. Lock P, Abram CL, Gibson T, Courtneidge SA. A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J 1998; 17:4346-57; PMID:9687503; http://dx.doi.org/10.1093/emboj/17.15.4346
29. Abram CL, Seals DF, Pass I, Salinsky D, Maurer L, Roth TM, Courtneidge SA. The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J Biol Chem 2003; 278:16844-51; PMID:12615925; http://dx.doi.org/10.1074/jbc.M300267200
30. Seals DF, Azucena EF Jr., Pass I, Tesfay L, Gordon R, Woodrow M, Resau JH, Courtneidge SA. The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 2005; 7:155-65; PMID:15710328; http://dx.doi.org/10.1016/j.ccr.2005.01.006
31. 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
32. Van Goethem E, Guiet R, Balor S, Charrière GM, Poincloux R, Labrousse A, Maridonneau-Parini I, Le Cabec V. Macrophage podosomes go 3D. Eur J Cell Biol 2011; 90:224-36; PMID:20801545; http://dx.doi.org/10.1016/j.ejcb.2010.07.011
33. Vikesaa J, Hansen TV, Jønson L, Borup R, Wewer UM, Christiansen J, Nielsen FC. RNA-binding IMPs promote cell adhesion and invadopodia formation. EMBO J 2006; 25:1456-68; PMID:16541107; http://dx.doi.org/10.1038/sj.emboj.7601039
34. Destaing O, Block MR, Planus E, Albiges-Rizo C. Invadosome regulation by adhesion signaling. Curr Opin Cell Biol 2011; 23:597-606; PMID:21550788; http://dx.doi.org/10.1016/j.ceb.2011.04.002
35. 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
36. Liu S, Yamashita H, Weidow B, Weaver AM, Quaranta V. Laminin-332-beta1 integrin interactions negatively regulate invadopodia. J Cell Physiol 2010; 223:134-42; PMID:20039268
37. Branch KM, Hoshino D, Weaver AM. Adhesion rings surround invadopodia and promote maturation. Biol Open 2012; 1:711-22; PMID:23213464; http://dx.doi.org/10.1242/bio.20121867
38. 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
39. Attanasio F, Caldieri G, Giacchetti G, van Horssen R, Wieringa B, Buccione R. Novel invadopodia components revealed by differential proteomic analysis. Eur J Cell Biol 2011; 90:115-27; PMID:20609496; http://dx.doi.org/10.1016/j.ejcb.2010.05.004
40. Cervero P, Himmel M, Krüger M, Linder S. Proteomic analysis of podosome fractions from macrophages reveals similarities to spreading initiation centres. Eur J Cell Biol 2012; 91:908-22; PMID:22721921; http://dx.doi.org/10.1016/j.ejcb.2012.05.005
41. Dutartre H, Davoust J, Gorvel JP, Chavrier P. Cytokinesis arrest and redistribution of actin-cytoskeleton regulatory components in cells expressing the Rho GTPase CDC42Hs. J Cell Sci 1996; 109:367-77; PMID:8838660
42. Burger KL, Davis AL, Isom S, Mishra N, Seals DF. The podosome marker protein Tks5 regulates macrophage invasive behavior. Cytoskeleton (Hoboken) 2011; 68:694-711; PMID:22021214; http://dx.doi.org/10.1002/cm.20545
43. Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995; 81:53-62; PMID:7536630; http://dx.doi.org/10.1016/0092-8674(95)90370-4
44. Kozma R, Ahmed S, Best A, Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 1995; 15:1942-52; PMID:7891688
45. Oikawa T, Okamura H, Dietrich F, Senju Y, Takenawa T, Suetsugu S. IRSp53 mediates podosome formation via VASP in NIH-Src cells. PLoS One 2013; 8:e60528; PMID:23555988; http://dx.doi.org/10.1371/journal.pone.0060528
46. Wang L, Zheng Y. Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol 2007; 17:58-64; PMID:17161947; http://dx.doi.org/10.1016/j.tcb.2006.11.009
47. Ridley AJ. Life at the leading edge. Cell 2011; 145:1012-22; PMID:21703446; http://dx.doi.org/10.1016/j.cell.2011.06.010
48. Ayala I, Giacchetti G, Caldieri G, Attanasio F, Mariggiò S, Tetè S, Polishchuk R, Castronovo V, Buccione R. Faciogenital dysplasia protein Fgd1 regulates invadopodia biogenesis and extracellular matrix degradation and is up-regulated in prostate and breast cancer. Cancer Res 2009; 69:747-52; PMID:19141649; http://dx.doi.org/10.1158/0008-5472.CAN-08-1980
49. Daubon T, Buccione R, Génot E. The Aarskog-Scott syndrome protein Fgd1 regulates podosome formation and extracellular matrix remodeling in transforming growth factor β-stimulated aortic endothelial cells. Mol Cell Biol 2011; 31:4430-41; PMID:21911474; http://dx.doi.org/10.1128/MCB.05474-11
50. Gringel A, Walz D, Rosenberger G, Minden A, Kutsche K, Kopp P, Linder S. PAK4 and alphaPIX determine podosome size and number in macrophages through localized actin regulation. J Cell Physiol 2006; 209:568-79; PMID:16897755; http://dx.doi.org/10.1002/jcp.20777
51. Razidlo GL, Schroeder B, Chen J, Billadeau DD, McNiven MA. Vav1 as a central regulator of invadopodia assembly. Curr Biol 2014; 24:86-93; PMID:24332539; http://dx.doi.org/10.1016/j.cub.2013.11.013
52. Webb BA, Eves R, Crawley SW, Zhou S, Côté GP, Mak AS. PAK1 induces podosome formation in A7r5 vascular smooth muscle cells in a PAK-interacting exchange factor-dependent manner. Am J Physiol Cell Physiol 2005; 289:C898-907; PMID:15944209; http://dx.doi.org/10.1152/ajpcell.00095.2005
53. van Helden SF, Hordijk PL. Podosome regulation by Rho GTPases in myeloid cells. Eur J Cell Biol 2011; 90:189-97; PMID:20573421; http://dx.doi.org/10.1016/j.ejcb.2010.05.008
54. Itzstein C, Coxon FP, Rogers MJ. The regulation of osteoclast function and bone resorption by small GTPases. Small GTPases 2011; 2:117-30; PMID:21776413; http://dx.doi.org/10.4161/sgtp.2.3.16453
55. Brazier H, Pawlak G, Vives V, Blangy A. The Rho GTPase Wrch1 regulates osteoclast precursor adhesion and migration. Int J Biochem Cell Biol 2009; 41:1391-401; PMID:19135548; http://dx.doi.org/10.1016/j.biocel.2008.12.007
56. Bravo-Cordero JJ, Oser M, Chen X, Eddy R, Hodgson L, Condeelis J. A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr Biol 2011; 21:635-44; PMID:21474314; http://dx.doi.org/10.1016/j.cub.2011.03.039
57. Kwiatkowska A, Didier S, Fortin S, Chuang Y, White T, Berens ME, Rushing E, Eschbacher J, Tran NL, Chan A, et al. The small GTPase RhoG mediates glioblastoma cell invasion. Mol Cancer 2012; 11:65; PMID:22966858; http://dx.doi.org/10.1186/1476-4598-11-65
58. Georgess D, Mazzorana M, Terrado J, Delprat C, Chamot C, Guasch RM, Perez-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
59. Oikawa T, Oyama M, Kozuka-Hata H, Uehara S, Udagawa N, Saya H, Matsuo K. Tks5-dependent formation of circumferential podosomes/invadopodia mediates cell-cell fusion. J Cell Biol 2012; 197:553-68; PMID:22584907; http://dx.doi.org/10.1083/jcb.201111116
60. Crimaldi L, Courtneidge SA, Gimona M. Tks5 recruits AFAP-110, p190RhoGAP, and cortactin for podosome formation. Exp Cell Res 2009; 315:2581-92; PMID:19540230; http://dx.doi.org/10.1016/j.yexcr.2009.06.012
61. Thompson O, Kleino I, Crimaldi L, Gimona M, Saksela K, Winder SJ. Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS One 2008; 3:e3638; PMID:18982058; http://dx.doi.org/10.1371/journal.pone.0003638
62. Murphy DA, Diaz B, Bromann PA, Tsai JH, Kawakami Y, Maurer J, Stewart RA, Izpisúa-Belmonte JC, Courtneidge SAA. A Src-Tks5 pathway is required for neural crest cell migration during embryonic development. PLoS One 2011; 6:e22499; PMID:21799874; http://dx.doi.org/10.1371/journal.pone.0022499
63. Juin A, Planus E, Guillemot F, Horakova P, Albiges-Rizo C, Génot E, Rosenbaum J, Moreau V, Saltel F. Extracellular matrix rigidity controls podosome induction in microvascular endothelial cells. Biol Cell 2013; 105:46-57; PMID:23106484; http://dx.doi.org/10.1111/boc.201200037
64. Stylli SS, Stacey TT, Verhagen AM, Xu SS, Pass I, Courtneidge SA, Lock P. Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation. J Cell Sci 2009; 122:2727-40; PMID:19596797; http://dx.doi.org/10.1242/jcs.046680
65. Burger KL, Learman BS, Boucherle AK, Sirintrapun SJ, Isom S, Diaz B, Courtneidge SA, Seals DF. Src-dependent Tks5 phosphorylation regulates invado-podia-associated invasion in prostate cancer cells. Prostate 2014; 74:134-48; PMID:24174371
66. Oikawa T, Itoh T, Takenawa T. Sequential signals toward podosome formation in NIH-src cells. J Cell Biol 2008; 182:157-69; PMID:18606851; http://dx.doi.org/10.1083/jcb.200801042
67. Parsons SJ, Parsons JT. Src family kinases, key regulators of signal transduction. Oncogene 2004; 23:7906-9; PMID:15489908; http://dx.doi.org/10.1038/sj.onc.1208160
68. Hoshino D, Jourquin J, Emmons SW, Miller T, Goldgof M, Costello K, Tyson DR, Brown B, Lu Y, Prasad NK, et al. Network analysis of the focal adhesion to invadopodia transition identifies a PI3K-PKCα invasive signaling axis. Sci Signal 2012; 5:ra66; PMID:22969158; http://dx.doi.org/10.1126/scisignal.2002964
69. Belsches AP, Haskell MD, Parsons SJ. Role of c-Src tyrosine kinase in EGF-induced mitogenesis. Front Biosci 1997; 2:d501-18; PMID:9331427
70. 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
71. Yu CH, Rafiq NB, Krishnasamy A, Hartman KL, Jones GE, Bershadsky AD, Sheetz MP. Integrin-matrix clusters form podosome-like adhesions in the absence of traction forces. Cell Rep 2013; 5:1456-68; PMID:24290759; http://dx.doi.org/10.1016/j.celrep.2013.10.040