Invadosomes in their natural habitat

European Journal of Cell Biology

Volumn 93, Issue 10-12, 2014, Pages 367-379

  Génot, Elisabeth ^a,b,c   Gligorijevic, Bojana ^d,e  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CENTRE DE RECHERCHE CARDIO THORACIQUE DE BORDEAUX   (France)

^c INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e Temple University   (United States)

Author keywords

Cancer; Cell locomotion; Cell migration; Cell motility; Confocal; Development; In situ; In vivo; Invadopodia; Invadosomes; Invasion; Microenvironment; Microscopy; Multiphoton; Podosomes; Protrusions

Indexed keywords

F ACTIN;

ASCIDIACEA; CAENORHABDITIS ELEGANS; CANCER CELL; CELL ORGANELLE; CHEMOTAXIS; DICTYOSTELIUM DISCOIDEUM; EXTRACELLULAR MATRIX; EXTRAVASATION; IN VITRO STUDY; INVADOSOME; MACROPHAGE; METASTASIS; MOLECULAR DYNAMICS; NEURAL CREST; NONHUMAN; OSTEOCLAST ACTIVITY; OSTEOLYSIS; PATHOPHYSIOLOGY; SHORT SURVEY; SIGNAL TRANSDUCTION; VASCULAR BIOLOGY; ZEBRA FISH;

CAENORHABDITIS ELEGANS; DANIO RERIO; MURINAE;

EID: 84939263309     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2014.10.002     Document Type: Short Survey

References (120)

1. Albinsson S., Sward K. Targeting smooth muscle microRNAs for therapeutic benefit in vascular disease. Pharmacol. Res. 2013, 75:28-36.
2. Alexander N.R., Branch K.M., Parekh A., Clark E.S., Iwueke I.C., Guelcher S.A., Weaver A.M. Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 2009, 18:1295-1299.
3. Annes J.P., Munger J.S., Rifkin D.B. Making sense of latent TGFβ activation. J. Cell Sci. 2003, 116:217-224.
4. Artym V.V., Zhang Y., Seillier-Moiseiwitsch F., Yamada K.M., Mueller S.C. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 2006, 66:3034-3043.
5. 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. 2008, 69:747-752.
6. Baker B.M., Chec C.S. Deconstructing the third dimension - how 3D culture microenvironments alter cellular cues. J. Cell Sci. 2012, 125:1-10.
7. Beaty B.T., Sharma V.P., Bravo-Cordero J.J., Simpson M.A., Eddy R.J., Koleske A.J., Condeelis J. β1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol. Biol. Cell 2013, 24:1661-1675.
8. Beaty B.T., Condeelis J. Digging a little deeper: the stages of invadopodium formation and maturation. Eur. J. Cell Biol. 2014, pii:S0171-9335(14)00090-9, (this issue).
9. Boettger N.B., Kostin S., Schneider J., Kruger M., Hein L., Brain T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J. Clin. Invest. 2009, 119:2634-2647.
10. Burgstaller G., Gimona M. Actin cytoskeleton remodelling via local inhibition of contractility at discrete microdomains. J. Cell. Sci. 2004, 117:223-231.
11. Burgstaller G., Gimona M. Podosome-mediated matrix resorption and cell motility in vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H3001-H3005.
12. Calle Y., Jones G.E., Jagger C., Fuller K., Blundell M.P., Chow J., Chambers T., Thrasher A.J. WASp deficiency in mice results in failure to form osteoclast sealing zones and defects in bone resorption. Blood 2004, 103:3552-3561.
13. Calle Y., Burns S., Thrasher A.J., Jones G.E. The leukocyte podosome. Eur. J. Cell Biol. 2006, 85:151-157.
14. Carmona-Fontaine C., Matthews R.K., Kuriyama S., Moreno M., Dunn G.A., Parsons M., Stern C.D., Mayor R. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 2008, 456:957-961.
15. Condeelis J., Segall J.E. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 2003, 3:921-930.
16. Conway E.M., Collen D., Carmeliet P. Molecular mechanisms of blood vessel growth. Cardiovasc. Res. 2001, 49:507-521.
17. Cordes K.R., Sheehy N.T., White M.P., Berry E.C., Morton S.U., Muth A.N., Lee T.H., Miano J.M., Ivey K.N., Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
18. Chen W.T. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 1989, 251:167-185.
19. Clark E.S., Whigham A.S., Yarbrough W.G., Weaver A.M. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 2007, 67:4227-4235.
20. 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.
21. Cooley J., Whitaker S., Sweeney S., Fraser S., Davidson B. Cytoskeletal polarity mediates localized induction of the heart progenitor lineage. Nat. Cell Biol. 2011, 13:952-957.
22. Coopman P.J., Do M.T., Thompson E.W., Mueller S.C. Phagocytosis of crosslinked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin. Cancer Res. 1998, 4:507-515.
23. David-Pfeuty T., Singer S.J. Altered distributions of the cytoskeletal proteins vinculin and α-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proc. Natl Acad. Sci. U.S.A. 1980, 77:6687-6691.
24. Davidson B. Ciona intestinalis as a model for cardiac development. Semin. Cell Dev. Biol. 2007, 18:16-26.
25. Deryugina E.I., Quigley J.P. Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis. Histochem. Cell Biol. 2008, 130:1119-1130.
26. 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.
27. Diaz B., Shani G., Pass I., Anderson D., Quintavalle M., Courtneidge S.A. Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci. Signal. 2009, 2:ra53.
28. Diaz B., Yuen A., Iizuka S., Higashiyama S., Courtneidge S.A. Notch increases the shedding of HB-EGF by ADAM12 to potentiate invadopodia formation in hypoxia. J. Cell Biol. 2013, 201:279-292.
29. Dora K.A. Coordination of vasomotor responses by the endothelium. Circ. J. 2010, 74:226-232.
30. Dumartin L., Quemener C., Laklai H., Herbert J., Bicknell R., Bousquet C., Pyronnet S., Castronovo V., Schilling M.K., Bikfalvi A., Hagedorn M. Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 2010, 138:1595-1606.
31. Eckert M.A., Lwin T.M., Chang A.T., Kim J., Danis E., Ohno-Machado L., Yang J. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 2011, 19:372-386.
32. Elia L., Quintavalle M., Zhang J., Contu R., Cossu L., Latronico M.V., Peterson K.L., Indolfi C., Catalucci D., Chen J., Courtneidge S.A., Condorelli G. The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ. 2009, 16:1590-1598.
33. Entenberg D., Wyckoff J., Gligorijevic B., Roussos E.T., Verkhusha V.V., Pollard J., Condeelis J. Setup and use of a two-laser multiphoton microscope for multichannel intravital fluorescence imaging. Nat. Protoc. 2011, 6:1500-1520.
34. Fukui Y., de Hostos E.L., Inoue S. Dynamics of GFP-coronin and eupodia in live Dictyostelium observed with real-time confocal optics. Biol. Bull. 1997, 193:224-225.
35. Fukui Y., Inoue S. Amoeboid movement anchored by eupodia, new actin-rich knobby feet in Dictyostelium. Cell Motil. Cytoskeleton 1997, 36:339-354.
36. Gacche R.N., Meshram R.J. Targeting tumor micro-environment for design and development of novel anti-angiogenic agents arresting tumor growth. Prog. Biophys. Mol. Biol. 2013, 113:333-354.
37. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 9:1392-1400.
38. Gil-Henn H., Patsialou A., Wang Y., Warren M.S., Condeelis J.S., Koleske A.J. Arg/Abl2 promotes invasion and attenuates proliferation of breast cancer in vivo. Oncogene 2013, 32:2622-2630.
39. Gligorijevic B., Wyckoff J., Yamaguchi H., Wang Y., Condeelis J. N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. J. Cell Sci. 2012, 125:724-734.
40. Goicoechea S.M., García-Mata R., Staub J., Valdivia A., Sharek L., McCulloch C.G., Hwang R.F., Urrutia R., Yeh J.J., Kim H.J., Otey C.A. Palladin promotes invasion of pancreatic cancer cells by enhancing invadopodia formation in cancer-associated fibroblasts. Oncogene 2014, 33:1265-1273.
41. Hagedorn E.J., Yashiro H., Ziel J.W., Ihara S., Wang Z., Sherwood D.R. Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. Dev. Cell 2009, 17:187-198.
42. Hagedorn E.J., Ziel J.W., Morrissey M.A., Linden L.M., Wang Z., Chi Q., Johnson S.A., Sherwood D.R. The netrin receptor DCC focuses invadopodia driven basement membrane transmigration in vivo. J. Cell Biol. 2013, 201:903-913.
43. Heissig B., Hattori K., Friedrich M., Rafii S., Werb Z. Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr. Opin. Hematol. 2003, 10:136-141.
44. Hiramatsu R., Matsuoka T., Kimura-Yoshida C., Han S., Mochida K., Adachi T., Takayama S., Matsuo I. External mechanical cues trigger the establishment of the anterior-posterior axis in early mouse embryos. Dev. Cell 2013, 27:131-144.
45. Hoshino D., Branch K.M., Weaver A.M. Signaling inputs to invadopodia and podosomes. J. Cell Sci. 2013, 126:2979-2989.
46. Hotary K., Li X.Y., Allen E., Stevens S.L., Weiss S.J. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 2006, 20:2673-2686.
47. Juin A., Planus E., Guillemot F., Horakova P., Albiges-Rizo C., Genot E., Rosenbaum J., Moreau V., Saltel F. Extracellular matrix rigidity controls podosome induction in microvascular endothelial cells. Biol. Cell 2013, 105:46-57.
48. Kaverina I., Stradal T.E., 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, 116:4915-4924.
49. Kaufmann S., Kuphal S., Schubert T., Bosserhoff A.K. Functional implication of Netrin expression in malignant melanoma. Cell Oncol. 2009, 31(6):415-422.
50. Kienast Y., von Baumgarten L., Fuhrmann M., Klinkert W.E.F., Goldbrunner R., Herms J., Winkler F. Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 2010, 16:116-123.
51. Labernardie A., Thibault C., Vieu C., Maridonneau-Parini I., Charrière G.M. Dynamics of podosome stiffness revealed by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21016-21021.
52. Li A., Dawson J.C., Forero-Vargas M., Spence H.J., Yu X.Z., Konig I., Anderson K., Machesky L.M. The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr. Biol. 2010, 20:339-345.
53. Lin E.Y., Jones J.G., Li P., Zhu L., Whitney K.D., Muller W.J., Pollard J.W. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 2003, 163:2112-2126.
54. 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, 96:9648-9653.
55. Linder S., Wiesner C., Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 2011, 27:185-211.
56. Mader C.C., Oser M., Magalhaes M.A., Bravo-Cordero J.J., Condeelis J., Koleske A.J., Gil-Henn H. An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res. 2011, 71:1730-1741.
57. Magalhaes M.A.O., Larson D.R., Mader C.C., Bravo-Cordero J.J., Gil-Henn H., Oser M., Chen X., Koleske A.J., Condeelis J. Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J. Cell Biol. 2011, 195:903-920.
58. Marques I.J., Weiss F.U., Vlecken D.H., Nitsche C., Bakkers J., Lagendijk A.K., Partecke L.I., Heidecke C., Lerch M., Bagowski C.P. Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer 2009, 9:128.
59. Matus D.Q., Li X.-Y., Durbin S., Agarwal D., Chi Q., Weiss S.J., Sherwood D.R. Identification of novel regulators of cell invasion across basement membrane in vivo. Sci. Signal 2010, 4:ra35.
60. Meyer A.S., Hughes-Alford S.K., Kay J.E., Castillo A., Wells A., Gertler F.B., Lauffenburger D.A. 2D protrusion but not motility predicts growth factor-induced cancer cell migration in 3D collagen. J. Cell. Biol. 2012, 197:721-729.
61. Michiels C. Endothelial cell functions. J. Cell Phys. 2003, 196:430-443.
62. Morrissey M.A., Hagedorn E.J., Sherwood D.R. Cell Invasion through basement membrane: The netrin receptor DCC guides the way. Worm 2013, 2:e26169.
63. Murphy D.A., Diaz B., Bromann P.A., Tsai J.H., Kawakami Y., Maurer J., Stewart R.A., Izpisua-Belmonte J.C., Courtneidge S.A. A Src-Tks5 pathway is required for neural crest cell migration during embryonic development. PLoS ONE 2011, 6:e22499.
64. Murphy D.A., Courtneidge S.A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 2011, 12:413-426.
65. Nakaya Y., Sukowati E.W., Wu Y., Sheng G. RhoA and microtubule dynamics control basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 2008, 10:765-775.
66. Parekh A., Ruppender N.S., Branch K.M., Sewell-Loftin M.K., Lin J., Boyer P.D., Candiello J.E., Merryman W.D., Guelcher S.A., Weaver A.M. Sensing and modulation of invadopodia across a wide range of rigidities. Biophys. J. 2011, 100:573-582.
67. Patel A., Dash P.R. Formation of atypical podosomes in extravillous trophoblasts regulates extracellular matrix degradation. Eur. J. Cell Biol. 2012, 91:171-179.
68. Patsialou A., Bravo-Cordero J.J., Wang Y., Entenberg D., Liu H., Clarke M., Condeelis J.S. Intravital multiphoton imaging reveals multicellular streaming as a crucial component of in vivo cell migration in human breast tumors. Intravital 2013, 2. 10.4161/intv.25294.
69. Patsialou A., Wyckoff J., Wang Y., Goswami S., Stanley E.R., Condeelis J.S. Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor. Cancer Res. 2009, 69:9498-9506.
70. Quintavalle M., Elia L., Condorelli G., Courtneidge S.A. MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J. Cell Biol. 2010, 189:13-22.
71. Rajendran P., Rengarajan T., Thangavel J., Nishigaki Y., Sakthisekaran D., Sethi G., Nishigaki I. The vascular endothelium and human diseases. Int. J. Biol. Sci. 2013, 9:1057-1069.
72. Rensen S.S.M., Doevendans P.A.F.M., van Eys G.J.J.M. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth. Heart J. 2007, 15:100-108.
73. Rivero F., Dislich H., Glockner G., Noegel A.A. The Dictyostelium discoideum family of Rho-related proteins. Nucleic Acids Res. 2001, 29:1068-1079.
74. Rodrigues S., De Wever O., Bruyneel E., Rooney R.J., Gespach C. Opposing roles of netrin-1 and the dependence receptor DCC in cancer cell invasion, tumor growth and metastasis. Oncogene 2007, 26:5615-5625.
75. Ross R., Glomset J.A. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 1973, 180:1332-1339.
76. Rottiers P., Saltel F., Daubon T., Chaigne-Delalande B., Tridon V., Billottet C., Reuzeau E., Genot E. TGFβ-induced endothelial podosomes mediate basement membrane collagen degradation in arterial vessels. J. Cell Sci. 2009, 122:4311-4318.
77. Rowe R.G., Weiss S.J. Breaching the basement membrane: who, when and how?. Trends Cell Biol. 2008, 18:560-574.
78. Osiak A.E., Zenner G., Linder S. Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp. Cell Res. 2005, 307:342-353.
79. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., Allen E., Chung D., Weiss S.J. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 2004, 167:769-781.
80. Saltel F., Daubon T., Juin A., Ganuza I.E., Veillat V., Genot E. Invadosomes: intriguing structures with promise. Eur. J. Cell Biol. 2011, 90:100-107.
81. Sarmiento C., Wang W., Dovas A., Yamaguchi H., Sidani M., El-Sibai M., DesMarais V., Holman H.A., Kitchen S., Backer J.M., Alberts A., Condeelis J. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J. Cell Biol. 2008, 180:1245-1260.
82. Sato Y., Rifkin D.B. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-β 1-like molecule byplasmin during co-culture. J. Cell Biol. 1989, 109:309-315.
83. Schoumacher M., Goldman R.D., Louvard D., Vignjevic D.M. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 2010, 189:541-556.
84. Seano G., Chiaverina G., Gagliardi P.A., di Blasio L., Puliafito A., Bouvard C., Sessa R., Tarone G., Sorokin L., Helley D., Jain R.K., Serini G., Bussolino F., Primo L. Endothelial podosome rosettes regulate vascular branching in tumor angiogenesis. Nat. Cell Bio. 2014, 16:931-941.
85. Seiler C., Davuluri G., Abrams J., Byfield F.J., Janmey P.A., Pack M. Smooth muscle tension induces invasive remodeling of the zebrafish intestine. PLoS Biol. 2012, 10:e1001386.
86. Shaye D.D., Greenwald I. OrthoList: a compendium of C. elegans genes with human orthologs. PLoS ONE 2011, 6:e20085.
87. Sherwood D.R., Butler J.A., Kramer J.M., Sternberg P.W. FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 2005, 121:951-962.
88. Shimizu A., Nakayama H., Wang P., Konig C., Akino T., Sandlund J., Coma S., Italiano J.E., Mammoto A., Bielenberg D.R., Klagsbrun M. Netrin-1 promotes glioblastoma cell invasiveness and angiogenesis by multiple pathways including activation of RhoA, cathepsin B, and cAMP-response element-binding protein. J. Biol. Chem. 2013, 288:2210-2222.
89. Sho E., Sho M., Singh T.M., Nanjo H., Komatsu M., Xu C., Masuda H., Zarins C.K. Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix. Exp. Mol. Pathol. 2002, 73:142-153.
90. Singh J., Aaronson S.A., Mlodzik M. Drosophila Abelson kinase mediates cell invasion and proliferation through two distinct MAPK pathways. Oncogene 2010, 29:4033-4045.
91. Stoletov K., Montel V., Lester R.D., Gonias S.L., Klemke R. High-resolution imaging of the dynamic tumor cell-vascular interface in transparent zebrafish. PNAS 2007, 104:17406-107411.
92. Stoletov K., Kato S., Zardouzian E., Kelber J., Yang J., Shattil S., Klemke R. Visualizing extravasation dynamics of metastatic tumor cells. J. Cell Sci. 2010, 123:2332-23341.
93. Stylli S.S., Kaye A.H., Lock P. Invadopodia: at the cutting edge of tumour invasion. J. Clin. Neurosci. 2008, 15:725-737.
94. Sutoh M., Hashimoto Y., Yoneyama T., Yamamoto H., Hatakeyama S., Koie T., Okamoto A., Yamaya K., Saitoh H., Funyu T., Nakamura T., Sato T., Ohyama C., Tsuboi S. Invadopodia formation by bladder tumor cells. Oncol. Res. 2010, 19:85-92.
95. Tat J., Liu M., Wen X. Zebrafish cancer and metastasis models for in vivo drug discovery. Drug Discov. Today Technol. 2013, 3:e83-e89.
96. Tatin F., Varon C., Genot 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, 119:769-781.
97. Tarone G., Cirillo D., Giancotti F.G., Comoglio P.M., Marchisio P.C. Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp. Cell Res. 1985, 159:141-157.
98. Teng T., Xie X., Walker S., White D.T., Mumm J.S., Cowell J.K. Evaluating human cancer cell metastasis in zebrafish. BMC Cancer 2013, 13:453.
99. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 2003, 15:740-746.
100. Tolde O., Rosel D., Vesely P., Folk P., Brabek J. The structure of invadopodia in a complex 3D environment. Eur. J. Cell Biol. 2010, 89:674-680.
101. Van den Dries K., Meddens M.B., de Keijzer S., Shekhar S., Subramaniam V., Figdor C.G., Cambi A. Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat. Commun. 2013, 4:1412-1416.
102. 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.
103. Van Goethem R.G., Balor S., Charriere G.M., Poincloux R., Labrousse A., Maridonneau-Parini I., Le Cabec V. Macrophage podosomes go 3D. Eur. J. Cell Biol. 2011, 90:224-236.
104. Van Haastert P.J., Devreotes P.N. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell. Biol. 2004, 5:626-634.
105. Varon C., Tatin F., Moreau V., Van Obberghen-Schilling E., Fernandez-Sauze S., Reuzeau E., Kramer I., Genot E. Transforming growth factor β induces rosettes of podosomes in primary aortic endothelial cells. Mol. Cell. Biol. 2006, 26:3582-3594.
106. Vidal M., Warner S., Read R., Cagan R.L. Differing Src signaling levels have distinct outcomes in drosophila. Cancer Res. 2007, 67:10278-10285.
107. Wallace K.N., Dolan A.C., Seiler C., Smith E.M., Yusuff S., Chaille-Arnold L., Judson B., Sierk R., Yengo C., Sweeney H.L., Pack M. Mutation of smooth muscle myosin causes epithelial invasion and cystic expansion of the zebrafish intestine. Dev. Cell 2005, 8:717-726.
108. Wang Y., McNiven M.A. Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 2012, 196:375-385.
109. Wang W., Wyckoff J.B., Frohlich V.C., Oleynikov Y., Hüttelmaier S., Zavadil J., Cermak L., Bottinger E.P., Singer R.H., White J.G., Segall J.E., Condeelis J.S. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res. 2002, 62:6278-6288.
110. Weis S., Cui J., Barnes L., Cheresh D. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J. Cell Biol. 2004, 167:223-229.
111. Wiesner C., Le-Cabec V., El Azzouzi K., Maridonneau-Parini I., Linder S. Podosomes in space: macrophage migration and matrix degradation in 2D and 3D settings. Cell Adh. Migr. 2014, 8:0-12.
112. Wilson B.D., Ii M., Park K.W., Suli A., Sorensen L.K., Larrieu-Lahargue F., Urness L.D., Suh W., Asai J., Kock G.A., Thorne T., Silver M., Thomas K.R., Chien C.B., Losordo D.W., Li D.Y. Netrins promote developmental and therapeutic angiogenesis. Science 2006, 313:640-644.
113. Wyckoff J., Wang W., Lin E.Y., Wang Y., Pixley F., Stanley E.R., Graf T., Pollard J.W., Segall J., Condeelis J. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004, 64:7022-7029.
114. Wyckoff J.B., Jones J.G., Condeelis J.S., Segall J.E. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 2000, 60:2504-2511.
115. Xin M., Small E.M., Sutherland L.B., Qi X., McAnally J., Plato C.F., Richardson J.A., Bassel-Duby R., Olson E.N. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev. 2009, 23:2166-2178.
116. Yamaguchi H., Lorenz M., Kempiak S., Sarmiento C., Coniglio S., Symons M., Segall J., Eddy R., Miki H., Takenawa T., Condeelis J. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 2005, 168:441-452.
117. Yamaguchi H., Pixley F., Condeelis J. Invadopodia and podosomes in tumor invasion. Eur. J. Cell Biol. 2006, 85:213-218.
118. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927L 939.
119. Yu X., Zech T., McDonald L., Gonzalez E.G., Li A., Macpherson I., Schwarz J.P., Spence H., Futó K., Timpson P., Nixon C., Ma Y., Anton I.M., Visegrády B., Insall R.H., Oien K., Blyth K., Norman J.C., Machesky L.M. N-WASP coordinates the delivery and F-actin - mediated capture of MT1-MMP at invasive pseudopods. J. Cell Biol. 2012, 199:527-544.
120. Yurchenco P.D., Amenta P.S., Patton B.L. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 2004, 22:521-538.