Rho GTPase signalling in cell migration

Current Opinion in Cell Biology

Volumn 36, Issue , 2015, Pages 103-112

  Ridley, Anne J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; ACTIN;

ACTIN POLYMERIZATION; CANCER CELL; CELL ADHESION; CELL JUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL MOTION; CHEMICAL MODIFICATION; CONTACT INHIBITION; ENDOTHELIUM; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FARNESYLATION; FOCAL ADHESION; GERANYLGERANYLATION; HUMAN; INTRACELLULAR SIGNALING; LAMELLIPODIUM; LEUKOCYTE; MICROTUBULE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; ANIMAL; CELL COMMUNICATION; METABOLISM; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; CELL COMMUNICATION; CELL MOVEMENT; HUMANS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84941283246     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.08.005     Document Type: Review

References (111)

1. Mayor R., Theveneau E. The neural crest. Development 2013, 140:2247-2251.
2. Spano D., Heck C., De Antonellis P., Christofori G., Zollo M. Molecular networks that regulate cancer metastasis. Semin Cancer Biol 2012, 22:234-249.
3. Griffith J.W., Luster A.D. Targeting cells in motion: migrating toward improved therapies. Eur J Immunol 2013, 43:1430-1435.
4. Friedl P., Locker J., Sahai E., Segall J.E. Classifying collective cancer cell invasion. Nat Cell Biol 2012, 14:777-783.
5. Paluch E.K., Raz E. The role and regulation of blebs in cell migration. Curr Opin Cell Biol 2013, 25:582-590.
6. Charras G., Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol 2014, 15:813-824.
7. Batson J., Astin J.W., Nobes C.D. Regulation of contact inhibition of locomotion by Eph-ephrin signalling. J Microsc 2013, 251:232-241.
8. Graziano B.R., Weiner O.D. Self-organization of protrusions and polarity during eukaryotic chemotaxis. Curr Opin Cell Biol 2014, 30:60-67.
9. Ridley A.J., Comoglio P.M., Hall A. Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol Cell Biol 1995, 15:1110-1122.
10. Boureux A., Vignal E., Faure S., Fort P. Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol 2007, 24:203-216.
11. Petrie R.J., Gavara N., Chadwick R.S., Yamada K.M. Nonpolarized signaling reveals two distinct modes of 3D cell migration. J Cell Biol 2012, 197:439-455.
12. Tal O., Lim H.Y., Gurevich I., Milo I., Shipony Z., Ng L.G., Angeli V., Shakhar G. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J Exp Med 2011, 208:2141-2153.
13. Montell D.J., Yoon W.H., Starz-Gaiano M. Group choreography: mechanisms orchestrating the collective movement of border cells. Nat Rev Mol Cell Biol 2012, 13:631-645.
14. Lawson C.D., Burridge K. The on off relationship of Rho and Rac during integrin-mediated adhesion and cell migration. Small GTPases 2014, 5:e27958.
15. Faroudi M., Hons M., Zachacz A., Dumont C., Lyck R., Stein J.V., Tybulewicz V.L. Critical roles for Rac GTPases in T-cell migration to and within lymph nodes. Blood 2010, 116:5536-5547.
16. Goicoechea S.M., Awadia S., Garcia-Mata R. I'm coming to GEF you: regulation of RhoGEFs during cell migration. Cell Adh Migr 2014, 8:535-549.
17. D'Amico G., Robinson S.D., Germain M., Reynolds L.E., Thomas G.J., Elia G., Saunders G., Fruttiger M., Tybulewicz V., Mavria G., et al. Endothelial-Rac1 is not required for tumor angiogenesis unless αvβ3-integrin is absent. PLoS ONE 2010, 5:e9766.
18. Law A.L., Vehlow A., Kotini M., Dodgson L., Soong D., Theveneau E., Bodo C., Taylor E., Navarro C., Perera U., et al. Lamellipodin and the Scar/WAVE complex cooperate to promote cell migration in vivo. J Cell Biol 2013, 203:673-689.
19. Michael M., Vehlow A., Navarro C. Krause M: c-Abl, lamellipodin, and Ena/VASP proteins cooperate in dorsal ruffling of fibroblasts and axonal morphogenesis. Curr Biol 2010, 20:783-791.
20. Kuhn S., Geyer M. Formins as effector proteins of Rho GTPases. Small GTPases 2014, 5:e29513.
21. Krause M., Gautreau A. Steering cell migration: lamellipodium dynamics and the regulation of directional persistence. Nat Rev Mol Cell Biol 2014, 15:577-590.
22. Havrylenko S., Noguera P., Abou-Ghali M., Manzi J., Faqir F., Lamora A., Guerin C., Blanchoin L., Plastino J. WAVE binds Ena/VASP for enhanced Arp2/3 complex-based actin assembly. Mol Biol Cell 2015, 26:55-65.
23. Machacek M., Hodgson L., Welch C., Elliott H., Pertz O., Nalbant P., Abell A., Johnson G.L., Hahn K.M., Danuser G. Coordination of Rho GTPase activities during cell protrusion. Nature 2009, 461:99-103.
24. Heasman S.J., Carlin L.M., Cox S., Ng T., Ridley A.J. Coordinated RhoA signaling at the leading edge and uropod is required for T cell transendothelial migration. J Cell Biol 2010, 190:553-563.
25. Zawistowski J.S., Sabouri-Ghomi M., Danuser G., Hahn K.M., Hodgson L. A RhoC biosensor reveals differences in the activation kinetics of RhoA and RhoC in migrating cells. PLoS ONE 2013, 8:e79877.
26. Suraneni P., Rubinstein B., Unruh J.R., Durnin M., Hanein D., Li R. The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J Cell Biol 2012, 197:239-251.
27. Wu C., Asokan S.B., Berginski M.E., Haynes E.M., Sharpless N.E., Griffith J.D., Gomez S.M., Bear J.E. Arp2/3 is critical for lamellipodia and response to extracellular matrix cues but is dispensable for chemotaxis. Cell 2012, 148:973-987.
28. Li A., Ma Y., Yu X., Mort R.L., Lindsay C.R., Stevenson D., Strathdee D., Insall R.H., Chernoff J., Snapper S.B., et al. Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod-driven motility and cell-cycle progression. Dev Cell 2011, 21:722-734.
29. Kurisu S., Takenawa T. WASP and WAVE family proteins: friends or foes in cancer invasion?. Cancer Sci 2010, 101:2093-2104.
30. Spence H.J., Timpson P., Tang H.R., Insall R.H., Machesky L.M. Scar/WAVE3 contributes to motility and plasticity of lamellipodial dynamics but not invasion in three dimensions. Biochem J 2012, 448:35-42.
31. Sweeney M.O., Collins A., Padrick S.B., Goode B.L. A novel role for WAVE1 in controlling actin network growth rate and architecture. Mol Biol Cell 2015, 26:495-505.
32. Veltman D.M., King J.S., Machesky L.M., Insall R.H. SCAR knockouts in Dictyostelium: WASP assumes SCAR's position and upstream regulators in pseudopods. J Cell Biol 2012, 198:501-508.
33. Rane C.K., Minden A. P21 activated kinases: structure, regulation, and functions. Small GTPases 2014, 5:e28003.
34. Wilson E., Leszczynska K., Poulter N.S., Edelmann F., Salisbury V.A., Noy P.J., Bacon A., Rappoport J.Z., Heath J.K., Bicknell R., et al. RhoJ interacts with the GITPIX complex and regulates focal adhesion disassembly. J Cell Sci 2014, 127:3039-3051.
35. Kaur S., Leszczynska K., Abraham S., Scarcia M., Hiltbrunner S., Marshall C.J., Mavria G., Bicknell R., Heath V.L. RhoJ/TCL regulates endothelial motility and tube formation and modulates actomyosin contractility and focal adhesion numbers. Arterioscler Thromb Vasc Biol 2011, 31:657-664.
36. Vignal E., De Toledo M., Comunale F., Ladopoulou A., Gauthier-Rouviere C., Blangy A., Fort P. Characterization of TCL, a new GTPase of the rho family related to TC10 and Cdc42. J Biol Chem 2000, 275:36457-36464.
37. Gad A.K., Nehru V., Ruusala A., Aspenstrom P. RhoD regulates cytoskeletal dynamics via the actin nucleation-promoting factor WASp homologue associated with actin Golgi membranes and microtubules. Mol Biol Cell 2012, 23:4807-4819.
38. Troeger A., Williams D.A. Hematopoietic-specific Rho GTPases Rac2 and RhoH and human blood disorders. Exp Cell Res 2013, 319:2375-2383.
39. Etienne-Manneville S. Cdc42 the centre of polarity. J Cell Sci 2004, 117:1291-1300.
40. Vega F.M., Fruhwirth G., Ng T., Ridley A.J. RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J Cell Biol 2011, 193:655-665.
41. Bravo-Cordero J.J., Magalhaes M.A., Eddy R.J., Hodgson L., Condeelis J. Functions of cofilin in cell locomotion and invasion. Nat Rev Mol Cell Biol 2013, 14:405-415.
42. Bravo-Cordero J.J., 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, 21:635-644.
43. Jackson B., Peyrollier K., Pedersen E., Basse A., Karlsson R., Wang Z., Lefever T., Ochsenbein A.M., Schmidt G., Aktories K., et al. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol Biol Cell 2011, 22:593-605.
44. Konigs V., Jennings R., Vogl T., Horsthemke M., Bachg A.C., Xu Y., Grobe K., Brakebusch C., Schwab A., Bahler M., et al. Mouse macrophages completely lacking Rho subfamily GTPases (RhoA, RhoB, and RhoC) have severe lamellipodial retraction defects, but robust chemotactic navigation and altered motility. J Biol Chem 2014, 289:30772-30784.
45. Fan L., Mellor H. The small Rho GTPase Rif and actin cytoskeletal remodelling. Biochem Soc Trans 2012, 40:268-272.
46. Dang I., Gorelik R., Sousa-Blin C., Derivery E., Guerin C., Linkner J., Nemethova M., Dumortier J.G., Giger F.A., Chipysheva T.A., et al. Inhibitory signalling to the Arp2/3 complex steers cell migration. Nature 2013, 503:281-284.
47. Yamazaki D., Itoh T., Miki H. Takenawa T: srGAP1 regulates lamellipodial dynamics and cell migratory behavior by modulating Rac1 activity. Mol Biol Cell 2013, 24:3393-3405.
48. Petrie R.J., Yamada K.M. At the leading edge of three-dimensional cell migration. J Cell Sci 2012, 125:5917-5926.
49. Kutys M.L., Yamada K.M. An extracellular-matrix-specific GEFGAP interaction regulates Rho GTPase crosstalk for 3D collagen migration. Nat Cell Biol 2014, 16:909-917.
50. Sanz-Moreno V., Gadea G., Ahn J., Paterson H., Marra P., Pinner S., Sahai E., Marshall C.J. Rac activation and inactivation control plasticity of tumor cell movement. Cell 2008, 135:510-523.
51. Azzarelli R., Guillemot F., Pacary E. Function and regulation of Rnd proteins in cortical projection neuron migration. Front Neurosci 2015, 9:19.
52. Pacary E., Heng J., Azzarelli R., Riou P., Castro D., Lebel-Potter M., Parras C., Bell D.M., Ridley A.J., Parsons M., et al. Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 2011, 69:1069-1084.
53. Riou P., Villalonga P., Ridley A.J. Rnd proteins: multifunctional regulators of the cytoskeleton and cell cycle progression. Bioessays 2010, 32:986-992.
54. Tang J., Ip J.P., Ye T., Ng Y.P., Yung W.H., Wu Z., Fang W., Fu A.K., Ip N.Y. Cdk5-dependent Mst3 phosphorylation and activity regulate neuronal migration through RhoA inhibition. J Neurosci 2014, 34:7425-7436.
55. Hwang J., Pallas D.C. STRIPAK complexes: structure, biological function, and involvement in human diseases. Int J Biochem Cell Biol 2014, 47:118-148.
56. Louvi A., Nishimura S., Gunel M. Ccm3, a gene associated with cerebral cavernous malformations, is required for neuronal migration. Development 2014, 141:1404-1415.
57. Azzarelli R., Pacary E., Garg R., Garcez P., van den Berg D., Riou P., Ridley A.J., Friedel R.H., Parsons M., Guillemot F. An antagonistic interaction between PlexinB2 and Rnd3 controls RhoA activity and cortical neuron migration. Nat Commun 2014, 5:3405.
58. Davis J.R., Luchici A., Mosis F., Thackery J., Salazar J.A., Mao Y., Dunn G.A., Betz T., Miodownik M., Stramer B.M. Inter-cellular forces orchestrate contact inhibition of locomotion. Cell 2015, 161:361-373.
59. Davis J.R., Huang C.Y., Zanet J., Harrison S., Rosten E., Cox S., Soong D.Y., Dunn G.A., Stramer B.M. Emergence of embryonic pattern through contact inhibition of locomotion. Development 2012, 139:4555-4560.
60. Mayor R., Theveneau E. The role of the non-canonical Wnt-planar cell polarity pathway in neural crest migration. Biochem J 2014, 457:19-26.
61. Moore R., Theveneau E., Pozzi S., Alexandre P., Richardson J., Merks A., Parsons M., Kashef J., Linker C., Mayor R. Par3 controls neural crest migration by promoting microtubule catastrophe during contact inhibition of locomotion. Development 2013, 140:4763-4775.
62. Wojnacki J., Quassollo G., Marzolo M.P., Caceres A. Rho: GTPases at the crossroad of signaling networks in mammals: impact of Rho-GTPases on microtubule organization and dynamics. Small GTPases 2014, 5:e28430.
63. Beaty B.T., Condeelis J. Digging a little deeper: the stages of invadopodium formation and maturation. Eur J Cell Biol 2014, 93:438-444.
64. Spuul P., Ciufici P., Veillat V., Leclercq A., Daubon T., Kramer I.J., Genot E. Importance of RhoGTPases in formation, characteristics, and functions of invadosomes. Small GTPases 2014, 5:e28195.
65. Tang H., Li A., Bi J., Veltman D.M., Zech T., Spence H.J., Yu X., Timpson P., Insall R.H., Frame M.C., et al. Loss of Scar/WAVE complex promotes N-WASP- and FAK-dependent invasion. Curr Biol 2013, 23:107-117.
66. Moshfegh Y., Bravo-Cordero J.J., Miskolci V., Condeelis J., Hodgson L. A Trio-Rac1-Pak1 signalling axis drives invadopodia disassembly. Nat Cell Biol 2014, 16:574-586.
67. Orgaz J.L., Sanz-Moreno V. Emerging molecular targets in melanoma invasion and metastasis. Pigment Cell Melanoma Res 2013, 26:39-57.
68. Bornschlogl T. How filopodia pull: what we know about the mechanics and dynamics of filopodia. Cytoskeleton (Hoboken) 2013, 70:590-603.
69. Khurana S., George S.P. The role of actin bundling proteins in the assembly of filopodia in epithelial cells. Cell Adh Migr 2011, 5:409-420.
70. Wakayama Y., Fukuhara S., Ando K., Matsuda M., Mochizuki N. Cdc42 mediates Bmp-induced sprouting angiogenesis through Fmnl3-driven assembly of endothelial filopodia in zebrafish. Dev Cell 2015, 32:109-122.
71. Fairchild C.L., Barna M. Specialized filopodia: at the 'tip' of morphogen transport and vertebrate tissue patterning. Curr Opin Genet Dev 2014, 27:67-73.
72. Stanganello E., Hagemann A.I., Mattes B., Sinner C., Meyen D., Weber S., Schug A., Raz E., Scholpp S. Filopodia-based Wnt transport during vertebrate tissue patterning. Nat Commun 2015, 6:5846.
73. Koizumi K., Takano K., Kaneyasu A., Watanabe-Takano H., Tokuda E., Abe T., Watanabe N., Takenawa T., Endo T. RhoD activated by fibroblast growth factor induces cytoneme-like cellular protrusions through mDia3C. Mol Biol Cell 2012, 23:4647-4661.
74. Arjonen A., Kaukonen R., Ivaska J. Filopodia and adhesion in cancer cell motility. Cell Adh Migr 2011, 5:421-430.
75. Jayo A., Parsons M., Adams J.C. A novel Rho-dependent pathway that drives interaction of fascin-1 with p-Lin-11/Isl-1/Mec-3 kinase (LIMK) 1/2 to promote fascin-1/actin binding and filopodia stability. BMC Biol 2012, 10:72.
76. Boer E.F., Howell E.D., Schilling T.F., Jette C.A., Stewart R.A. Fascin1-dependent filopodia are required for directional migration of a subset of neural crest cells. PLoS Genet 2015, 11:e1004946.
77. Meyen D., Tarbashevich K., Banisch T.U., Wittwer C., Reichman-Fried M., Maugis B., Grimaldi C., Messerschmidt E.M., Raz E. Dynamic filopodia are required for chemokine-dependent intracellular polarization during guided cell migration in vivo. Elife 2015, 4.
78. Phng L.K., Stanchi F., Gerhardt H. Filopodia are dispensable for endothelial tip cell guidance. Development 2013, 140:4031-4040.
79. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat Rev Mol Cell Biol 2008, 9:730-736.
80. Narumiya S., Tanji M., Ishizaki T. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 2009, 28:65-76.
81. Zatulovskiy E., Tyson R., Bretschneider T., Kay R.R. Bleb-driven chemotaxis of Dictyostelium cells. J Cell Biol 2014, 204:1027-1044.
82. Ruprecht V., Wieser S., Callan-Jones A., Smutny M., Morita H., Sako K., Barone V., Ritsch-Marte M., Sixt M., Voituriez R., et al. Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell 2015, 160:673-685.
83. Xiang S.Y., Dusaban S.S., Brown J.H. Lysophospholipid receptor activation of RhoA and lipid signaling pathways. Biochim Biophys Acta 2013, 1831:213-222.
84. Niggli V. Insights into the mechanism for dictating polarity in migrating T-cells. Int Rev Cell Mol Biol 2014, 312:201-270.
85. Row R.H., Maitre J.L., Martin B.L., Stockinger P., Heisenberg C.P., Kimelman D. Completion of the epithelial to mesenchymal transition in zebrafish mesoderm requires Spadetail. Dev Biol 2011, 354:102-110.
86. Kardash E., Reichman-Fried M., Maitre J.L., Boldajipour B., Papusheva E., Messerschmidt E.M., Heisenberg C.P., Raz E. A role for Rho GTPases and cellcell adhesion in single-cell motility in vivo. Nat Cell Biol 2010, 12:47-53. sup pp 111.
87. Tarbashevich K., Reichman-Fried M., Grimaldi C., Raz E. Chemokine-dependent pH elevation at the cell front sustains polarity in directionally migrating zebrafish germ cells. Curr Biol 2015, 25:1096-1103.
88. Sanz-Moreno V., Gaggioli C., Yeo M., Albrengues J., Wallberg F., Viros A., Hooper S., Mitter R., Feral C.C., Cook M., et al. ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell 2011, 20:229-245.
89. Orgaz J.L., Pandya P., Dalmeida R., Karagiannis P., Sanchez-Laorden B., Viros A., Albrengues J., Nestle F.O., Ridley A.J., Gaggioli C., et al. Diverse matrix metalloproteinase functions regulate cancer amoeboid migration. Nat Commun 2014, 5:4255.
90. Navarro-Lerida I., Pellinen T., Sanchez S.A., Guadamillas M.C., Wang Y., Mirtti T., Calvo E., Del Pozo M.A. Rac1 nucleocytoplasmic shuttling drives nuclear shape changes and tumor invasion. Dev Cell 2015, 32:318-334.
91. Etienne-Manneville S. Neighborly relations during collective migration. Curr Opin Cell Biol 2014, 30:51-59.
92. Cai D., Chen S.C., Prasad M., He L., Wang X., Choesmel-Cadamuro V., Sawyer J.K., Danuser G., Montell D.J. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014, 157:1146-1159.
93. Wang X., He L., Wu Y.I., Hahn K.M., Montell D.J. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol 2010, 12:591-597.
94. Theveneau E., Mayor R. Can mesenchymal cells undergo collective cell migration? The case of the neural crest. Cell Adh Migr 2011, 5:490-498.
95. Fort P., Guemar L., Vignal E., Morin N., Notarnicola C., de Santa Barbara P., Faure S. Activity of the RhoU/Wrch1 GTPase is critical for cranial neural crest cell migration. Dev Biol 2011, 350:451-463.
96. Abraham S., Yeo M., Montero-Balaguer M., Paterson H., Dejana E., Marshall C.J., Mavria G. VE-Cadherin-mediated cellcell interaction suppresses sprouting via signaling to MLC2 phosphorylation. Curr Biol 2009, 19:668-674.
97. Schaker K., Bartsch S., Patry C., Stoll S.J., Hillebrands J.L., Wieland T., Kroll J. The bipartite rac1 guanine nucleotide exchange factor engulfment and cell motility 1/dedicator of cytokinesis 180 (elmo1/dock180) protects endothelial cells from apoptosis in blood vessel development. J Biol Chem 2015, 290:6408-6418.
98. Theveneau E., Marchant L., Kuriyama S., Gull M., Moepps B., Parsons M., Mayor R. Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 2010, 19:39-53.
99. Oubaha M., Lin M.I., Margaron Y., Filion D., Price E.N., Zon L.I., Cote J.F., Gratton J.P. Formation of a PKCζ/β-catenin complex in endothelial cells promotes angiopoietin-1-induced collective directional migration and angiogenic sprouting. Blood 2012, 120:3371-3381.
100. Camand E., Peglion F., Osmani N., Sanson M., Etienne-Manneville S. N-cadherin expression level modulates integrin-mediated polarity and strongly impacts on the speed and directionality of glial cell migration. J Cell Sci 2012, 125:844-857.
101. Hidalgo-Carcedo C., Hooper S., Chaudhry S.I., Williamson P., Harrington K., Leitinger B., Sahai E. Collective cell migration requires suppression of actomyosin at cellcell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat Cell Biol 2011, 13:49-58.
102. Kim C., Yang H., Fukushima Y., Saw P.E., Lee J., Park J.S., Park I., Jung J., Kataoka H., Lee D., et al. Vascular RhoJ is an effective and selective target for tumor angiogenesis and vascular disruption. Cancer Cell 2014, 25:102-117.
103. Wimmer R., Cseh B., Maier B., Scherrer K., Baccarini M. Angiogenic sprouting requires the fine tuning of endothelial cell cohesion by the Raf-1/Rok-α complex. Dev Cell 2012, 22:158-171.
104. Richardson B.E., Lehmann R. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 2010, 11:37-49.
105. Nourshargh S., Hordijk P.L., Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010, 11:366-378.
106. Sumagin R., Parkos C.A. Epithelial adhesion molecules and the regulation of intestinal homeostasis during neutrophil transepithelial migration. Tissue Barriers 2015, 3:e969100.
107. Reymond N., d'Agua B.B., Ridley A.J. Crossing the endothelial barrier during metastasis. Nat Rev Cancer 2013, 13:858-870.
108. Heemskerk N., van Rijssel J., van Buul J.D. Rho-GTPase signaling in leukocyte extravasation: an endothelial point of view. Cell Adh Migr 2014, 8:67-75.
109. Cain R.J., Vanhaesebroeck B., Ridley A.J. The PI3K p110α isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J Cell Biol 2010, 188:863-876.
110. Manes T.D., Pober J.S. TCR-driven transendothelial migration of human effector memory CD4T cells involves Vav, Rac, and myosin IIA. J Immunol 2013, 190:3079-3088.
111. Lorentzen A., Bamber J., Sadok A., Elson-Schwab I., Marshall C.J. An ezrin-rich, rigid uropod-like structure directs movement of amoeboid blebbing cells. J Cell Sci 2011, 124:1256-1267.