The actin cytoskeleton in cancer cell motility

Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465

Rafelski SM, Theriot JA (2004) Crawling toward a unified model of cell motility: spatial and temporal regulation of actin dynamics. Annu Rev Biochem 73:209–239

Zigmond SH, Gerald PS (2004) Beginning and ending an actin filament: control at the barbed end. In: current topics in developmental biology, vol 63. Academic Press, pp 145–188

Goode BL, Eck MJ (2007) Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76:593–627

Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19:541–564

Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36:451–477

Wang W, Eddy R, Condeelis J (2007) The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 7:429–440

Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

Logan MR, Mandato CA (2006) Regulation of the actin cytoskeleton by PIP2 in cytokinesis. Biol Cell 98:377–388

Wear MA, Cooper JA (2004) Capping protein: new insights into mechanism and regulation. Trends Biochem Sci 29:418–428

Yarmola EG, Bubb MR (2006) Profilin: emerging concepts and lingering misconceptions. Trends Biochem Sci 31:197–205

Takenawa T, Suetsugu S (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8:37–48

Suetsugu S, Miki H, Takenawa T (1998) The essential role of profilin in the assembly of actin for microspike formation. Embo J 17:6516–6526

Dominguez R (2007) The beta-thymosin/WH2 fold: multifunctionality and structure. Ann N Y Acad Sci 1112:86–94

Carlier MF, Hertzog M, Didry D, Renault L, Cantrelle FX, van Heijenoort C, Knossow M, Guittet E (2007) Structure, function, and evolution of the beta-thymosin/WH2 (WASP-Homology2) actin-binding module. Ann N Y Acad Sci 1112:67–75

Scita G, Confalonieri S, Lappalainen P, Suetsugu S (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18:52–60

Buday L, Downward J (2007) Roles of cortactin in tumor pathogenesis. Biochim Biophys Acta 1775:263–273

Peng J, Wallar BJ, Flanders A, Swiatek PJ, Alberts AS (2003) Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 (mDia2) as an effector for Cdc42. Curr Biol 13:534–545

Wallar BJ, Deward AD, Resau JH, Alberts AS (2007) RhoB and the mammalian Diaphanous-related formin mDia2 in endosome trafficking. Exp Cell Res 313:560–571

Eisenmann KM, Harris ES, Kitchen SM, Holman HA, Higgs HN, Alberts AS (2007) Dia-interacting protein modulates formin-mediated actin assembly at the cell cortex. Curr Biol 17:579–591

Pellegrin S, Mellor H (2005) The Rho family GTPase Rif induces filopodia through mDia2. Curr Biol 15:129–133

Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. Embo J 16:3044–3056

Zigmond SH (2004) Formin-induced nucleation of actin filaments. Curr Opin Cell Biol 16:99–105

Tehrani S, Tomasevic N, Weed S, Sakowicz R, Cooper JA (2007) Src phosphorylation of cortactin enhances actin assembly. Proc Natl Acad Sci U S A 104:11933–11938

Scott RW, Olson MF (2007) LIM kinases: function, regulation and association with human disease. J Mol Med 85:555–568

Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, Dotti CG (2003) RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162:1267–1279

Takeya R, Taniguchi K, Narumiya S, Sumimoto H (2008) The mammalian formin FHOD1 is activated through phosphorylation by ROCK and mediates thrombin-induced stress fibre formation in endothelial cells. Embo J 27:618–628

Schirenbeck A, Arasada R, Bretschneider T, Schleicher M, Faix J (2005) Formins and VASPs may co-operate in the formation of filopodia. Biochem Soc Trans 33:1256–1259

Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9:1110–1121

Adams JC (2004) Roles of fascin in cell adhesion and motility. Curr Opin Cell Biol 16:590–596

Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006) Role of fascin in filopodial protrusion. J Cell Biol 174:863–875

O’Connell CB, Tyska MJ, Mooseker MS (2007) Myosin at work: motor adaptations for a variety of cellular functions. Biochim Biophys Acta 1773:615–630

Gunning PW, Schevzov G, Kee AJ, Hardeman EC (2005) Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol 15:333–341

Ichetovkin I, Grant W, Condeelis J (2002) Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr Biol 12:79–84

DesMarais V, Macaluso F, Condeelis J, Bailly M (2004) Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 117:3499–3510

van Rheenen J, Song X, van Roosmalen W, Cammer M, Chen X, Desmarais V, Yip SC, Backer JM, Eddy RJ, Condeelis JS (2007) EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol 179:1247–1259

El-Sibai M, Nalbant P, Pang H, Flinn RJ, Sarmiento C, Macaluso F, Cammer M, Condeelis JS, Hahn KM, Backer JM (2007) Cdc42 is required for EGF-stimulated protrusion and motility in MTLn3 carcinoma cells. J Cell Sci 120:3465–3474

Yip SC, El-Sibai M, Coniglio SJ, Mouneimne G, Eddy RJ, Drees BE, Neilsen PO, Goswami S, Symons M, Condeelis JS, Backer JM (2007) The distinct roles of Ras and Rac in PI 3-kinase-dependent protrusion during EGF-stimulated cell migration. J Cell Sci 120:3138–3146

Wang W, Goswami S, Lapidus K, Wells AL, Wyckoff JB, Sahai E, Singer RH, Segall JE, Condeelis JS (2004) Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 64:8585–8594

Steffen A, Faix J, Resch GP, Linkner J, Wehland J, Small JV, Rottner K, Stradal TEB (2006) Filopodia Formation in the Absence of Functional WAVE- and Arp2/3-Complexes. Mol Biol Cell 17:2581–2591

Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109:509–521

Vale RD, Milligan RA (2000) The way things move: looking under the hood of molecular motor proteins. Science 288:88–95

Somlyo AP, Somlyo AV (2000) Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 522(Pt 2):177–185

Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho- kinase). J Biol Chem 271:20246–20249

Murata-Hori M, Suizu F, Iwasaki T, Kikuchi A, Hosoya H (1999) ZIP kinase identified as a novel myosin regulatory light chain kinase in HeLa cells. FEBS Lett 451:81–84

Leung T, Chen XQ, Tan I, Manser E, Lim L (1998) Myotonic dystrophy kinase-related Cdc42-binding kinase acts as a Cdc42 effector in promoting cytoskeletal reorganization. Mol Cell Biol 18:130–140

Wilkinson S, Paterson HF, Marshall CJ (2005) Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat Cell Biol 7:255–261

Wilson DP, Sutherland C, Borman MA, Deng JT, Macdonald JA, Walsh MP (2005) Integrin-linked kinase is responsible for Ca2+-independent myosin diphosphorylation and contraction of vascular smooth muscle. Biochem J 392:641–648

Cohen O, Feinstein E, Kimchi A (1997) DAP-kinase is a Ca2+/calmodulin-dependent, cytoskeletal-associated protein kinase, with cell death-inducing functions that depend on its catalytic activity. Embo J 16:998–1008

Kawai T, Nomura F, Hoshino K, Copeland NG, Gilbert DJ, Jenkins NA, Akira S (1999) Death-associated protein kinase 2 is a new calcium/calmodulin-dependent protein kinase that signals apoptosis through its catalytic activity. Oncogene 18:3471–3480

Sanjo H, Kawai T, Akira S (1998) DRAKs, novel serine/threonine kinases related to death-associated protein kinase that trigger apoptosis. J Biol Chem 273:29066–29071

Ramos E, Wysolmerski RB, Masaracchia RA (1997) Myosin phosphorylation by human cdc42-dependent S6/H4 kinase/gammaPAK from placenta and lymphoid cells. Recept Signal Transduct 7:99–110

Zeng Q, Lagunoff D, Masaracchia R, Goeckeler Z, Cote G, Wysolmerski R (2000) Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J Cell Sci 113(Pt 3):471–482

Guerriero V Jr., Russo MA, Olson NJ, Putkey JA, Means AR (1986) Domain organization of chicken gizzard myosin light chain kinase deduced from a cloned cDNA. Biochemistry 25:8372–8381

Ito M, Nakano T, Erdodi F, Hartshorne DJ (2004) Myosin phosphatase: structure, regulation and function. Mol Cell Biochem 259:197–209

Okamoto R, Kato T, Mizoguchi A, Takahashi N, Nakakuki T, Mizutani H, Isaka N, Imanaka-Yoshida K, Kaibuchi K, Lu Z, Mabuchi K, Tao T, Hartshorne DJ, Nakano T, Ito M (2006) Characterization and function of MYPT2, a target subunit of myosin phosphatase in heart. Cell Signal 18:1408–1416

Feng J, Ito M, Ichikawa K, Isaka N, Nishikawa M, Hartshorne DJ, Nakano T (1999) Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J Biol Chem 274:37385–37390

Terrak M, Kerff F, Langsetmo K, Tao T, Dominguez R (2004) Structural basis of protein phosphatase 1 regulation. Nature 429:780–784

Tan I, Ng CH, Lim L, Leung T (2001) Phosphorylation of a novel myosin binding subunit of protein phosphatase 1 reveals a conserved mechanism in the regulation of actin cytoskeleton. J Biol Chem 276:21209–21216

Muranyi A, MacDonald JA, Deng JT, Wilson DP, Haystead TA, Walsh MP, Erdodi F, Kiss E, Wu Y, Hartshorne DJ (2002) Phosphorylation of the myosin phosphatase target subunit by integrin-linked kinase. Biochem J 366:211–216

Kiss E, Muranyi A, Csortos C, Gergely P, Ito M, Hartshorne DJ, Erdodi F (2002) Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem J 365:79–87

Borman MA, MacDonald JA, Muranyi A, Hartshorne DJ, Haystead TAJ (2002) Smooth muscle myosin phosphatase-associated kinase induces Ca2+ sensitization via myosin phosphatase inhibition. J Biol Chem 277:23441–23446

Muranyi A, Zhang R, Liu F, Hirano K, Ito M, Epstein HF, Hartshorne DJ (2001) Myotonic dystrophy protein kinase phosphorylates the myosin phosphatase targeting subunit and inhibits myosin phosphatase activity. FEBS Lett 493:80–84

Velasco G, Armstrong C, Morrice N, Frame S, Cohen P (2002) Phosphorylation of the regulatory subunit of smooth muscle protein phosphatase 1M at Thr850 induces its dissociation from myosin. FEBS Lett 527:101–104

Li L, Eto M, Lee MR, Morita F, Yazawa M, Kitazawa T (1998) Possible involvement of the novel CPI-17 protein in protein kinase C signal transduction of rabbit arterial smooth muscle. J Physiol 508(Pt 3):871–881

Eto M, Kitazawa T, Matsuzawa F, Aikawa S, Kirkbride JA, Isozumi N, Nishimura Y, Brautigan DL, Ohki SY (2007) Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor. Structure 15:1591–1602

Koyama M, Ito M, Feng J, Seko T, Shiraki K, Takase K, Hartshorne DJ, Nakano T (2000) Phosphorylation of CPI-17, an inhibitory phosphoprotein of smooth muscle myosin phosphatase, by Rho-kinase. FEBS Lett 475:197–200

MacDonald JA, Eto M, Borman MA, Brautigan DL, Haystead TA (2001) Dual Ser and Thr phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by MYPT-associated kinase. FEBS Lett 493:91–94

Deng JT, Sutherland C, Brautigan DL, Eto M, Walsh MP (2002) Phosphorylation of the myosin phosphatase inhibitors, CPI-17 and PHI-1, by integrin-linked kinase. Biochem J 367:517–524

Eto M, Karginov A, Brautigan DL (1999) A novel phosphoprotein inhibitor of protein type-1 phosphatase holoenzymes. Biochemistry 38:16952–16957

Erdodi F, Kiss E, Walsh MP, Stefansson B, Deng JT, Eto M, Brautigan DL, Hartshorne DJ (2003) Phosphorylation of protein phosphatase type-1 inhibitory proteins by integrin-linked kinase and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun 306:382–387

Jin H, Sperka T, Herrlich P, Morrison H (2006) Tumorigenic transformation by CPI-17 through inhibition of a merlin phosphatase. Nature 442:576–579

Somlyo AP, Somlyo AV (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83:1325–1358

Garrett SC, Varney KM, Weber DJ, Bresnick AR (2006) S100A4, a mediator of metastasis. J Biol Chem 281:677–680

Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP, Lukanidin EM (1994) Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269:19679–19682

Li ZH, Bresnick AR (2006) The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res 66:5173–5180

Watanabe Y, Usada N, Minami H, Morita T, Tsugane S, Ishikawa R, Kohama K, Tomida Y, Hidaka H (1993) Calvasculin, as a factor affecting the microfilament assemblies in rat fibroblasts transfected by src gene. FEBS Lett 324:51–55

Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K, Endo H (1994) Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin. J Cell Biol 124:757–768

Stehn JR, Schevzov G, O’Neill GM, Gunning PW (2006) Specialisation of the tropomyosin composition of actin filaments provides new potential targets for chemotherapy. Curr Cancer Drug Targets 6:245–256

Bryce NS, Schevzov G, Ferguson V, Percival JM, Lin JJC, Matsumura F, Bamburg JR, Jeffrey PL, Hardeman EC, Gunning P, Weinberger RP (2003) Specification of actin filament function and molecular composition by tropomyosin isoforms. Mol Biol Cell 14:1002–1016

Fanning AS, Wolenski JS, Mooseker MS, Izant JG (1994) Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil Cytoskeleton 29:29–45

Adami R, Cintio O, Trombetta G, Choquet D, Grazi E (2003) On the stiffness of the natural actin filament decorated with alexa fluor tropomyosin. Biophys Chem 104:469–476

Ono S, Ono K (2002) Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J Cell Biol 156:1065–1076

Ishikawa R, Yamashiro S, Matsumura F (1989) Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon. J Biol Chem 264:7490–7497

Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305:1782–1786

DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE (2002) Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115:4649–4660

Soderling SH, Scott JD (2006) WAVE signalling: from biochemistry to biology. Biochem Soc Trans 34:73–76

Nimnual AS, Taylor LJ, Bar-Sagi D (2003) Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5:236–241

Hooper S, Marshall JF, Sahai E (2006) Tumor cell migration in three dimensions. Meth Enzymol 406:625–643

Buccione R, Orth JD, McNiven MA (2004) Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5:647–657

Linder S (2007) The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17:107–117

Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, Segall J, Eddy R, Miki H, Takenawa T, Condeelis J (2005) Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168:441–452

Yamaguchi H, Pixley F, Condeelis J (2006) Invadopodia and podosomes in tumor invasion. Eur J Cell Biol 85:213–218

Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610

Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9:893–904

Lidke DS, Lidke KA, Rieger B, Jovin TM, Arndt-Jovin DJ (2005) Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J Cell Biol 170:619–626

Zaru R, Mollahan P, Watts C (2008) 3-Phosphoinositide-dependent kinase 1 deficiency perturbs toll-like receptor signaling events and actin cytoskeleton dynamics in dendritic cells. J Biol Chem 283:929–939

Pinner S, Sahai E (2008) PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 10:127–137

Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ (2005) Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435:365–369

Trinkaus JP (1973) Surface activity and locomotion of Fundulus deep cells during blastula and gastrula stages. Dev Biol 30:69–103

Blaser H, Reichman-Fried M, Castanon I, Dumstrei K, Marlow FL, Kawakami K, Solnica-Krezel L, Heisenberg CP, Raz E (2006) Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 11:613–627

Lecuit T, Lenne P-F (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 8:633–644

Pinner S, Sahai E (2008) PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 10:127–137

Sahai E, Marshall CJ (2003) Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5:711–719

Charras GT, Coughlin M, Mitchison TJ, Mahadevan L (2007) Life and times of a cellular bleb. Biophys J 94:1836–1853

Wyckoff JB, Pinner SE, Gschmeissner S, Condeelis JS, Sahai E (2006) ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol 16:1515–1523

Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, Matsumura F (2000) Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150:797–806

Totsukawa G, Wu Y, Sasaki Y, Hartshorne DJ, Yamakita Y, Yamashiro S, Matsumura F (2004) Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J Cell Biol 164:427–439

Chen BH, Tzen JT, Bresnick AR, Chen HC (2002) Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J Biol Chem 277:33857–33863

Niggli V, Schmid M, Nievergelt A (2006) Differential roles of Rho-kinase and myosin light chain kinase in regulating shape, adhesion, and migration of HT1080 fibrosarcoma cells. Biochem Biophys Res Commun 343:602–608

Lee WS, Seo G, Shin HJ, Yun SH, Yun H, Choi N, Lee J, Son D, Cho J, Kim J, Cho YB, Chun HK, Lee WY (2008) Identification of differentially expressed genes in microsatellite stable HNPCC and sporadic colon cancer. J Surg Res 144:29–35

Minamiya Y, Nakagawa T, Saito H, Matsuzaki I, Taguchi K, Ito M, Ogawa J (2005) Increased expression of myosin light chain kinase mRNA is related to metastasis in non-small cell lung cancer. Tumour Biol 26:153–157

Ye LH, Wu LY, Guo W, Ma HT, Zhang XD (2006) [Screening of a sub-clone of human breast cancer cells with high metastasis potential]. Zhonghua Yi Xue Za Zhi 86:61–65

Kucharczak J, Pannequin J, Camby I, Decaestecker C, Kiss R, Martinez J (2001) Gastrin induces over-expression of genes involved in human U373 glioblastoma cell migration. Oncogene 20:7021–7028

Tohtong R, Phattarasakul K, Jiraviriyakul A, Sutthiphongchai T (2003) Dependence of metastatic cancer cell invasion on MLCK-catalyzed phosphorylation of myosin regulatory light chain. Prostate Cancer Prostatic Dis 6:212–216

Kaneko K, Satoh K, Masamune A, Satoh A, Shimosegawa T (2002) Myosin light chain kinase inhibitors can block invasion and adhesion of human pancreatic cancer cell lines. Pancreas 24:34–41

Nguyen Q-D, Faivre S, Bruyneel E, Rivat C, Seto M, Endo T, Mareel M, Emami S, Gespach C (2002) RhoA- and RhoD-dependent regulatory switch of G{alpha} subunit signaling by PAR-1 receptors in cellular invasion. FASEB J 16:565–576

Hagerty L, Weitzel DH, Chambers J, Fortner CN, Brush MH, Loiselle D, Hosoya H, Haystead TA (2007) ROCK1 phosphorylates and activates zipper-interacting protein kinase. J Biol Chem 282:4884–4893

MacDonald JA, Borman MA, Muranyi A, Somlyo AV, Hartshorne DJ, Haystead TAJ (2001) Identification of the endogenous smooth muscle myosin phosphatase-associated kinase. Proc Natl Acad Sci 98:2419–2424

Sahai E (2005) Mechanisms of cancer cell invasion. Curr Opin Genet Dev 15:87–96

Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker E-B, Friedl P (2003) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160:267–277

Woodley DT, Yamauchi M, Wynn KC, Mechanic G, Briggaman RA (1991) Collagen telopeptides (Cross-Linking Sites) play a role in collagen gel lattice contraction. J Investig Dermatol 97:580–585

Sahai E (2007) Illuminating the metastatic process. Nat Rev Cancer 7:737–749

Condeelis J, Segall JE (2003) Intravital imaging of cell movement in tumours. Nat Rev Cancer 3:921–930

Makale M (2007) Intravital imaging and cell invasion. Meth Enzymol 426:375–401

MacDonald IC, Groom AC, Chambers AF (2002) Cancer spread and micrometastasis development: quantitative approaches for in vivo models. Bioessays 24:885–893

Friedl P, Wolf K (2003) Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem Soc Symp 70:277–285

Friedl P, Borgmann S, Brocker EB (2001) Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement. J Leukoc Biol 70:491–509

Wang W, Mouneimne G, Sidani M, Wyckoff J, Chen X, Makris A, Goswami S, Bresnick AR, Condeelis JS (2006) The activity status of cofilin is directly related to invasion, intravasation, and metastasis of mammary tumors. J Cell Biol 173:395–404

Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH, Wrana JL (2003) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:1775–1779

Sahai E, Garcia-Medina R, Pouyssegur J, Vial E (2007) Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J Cell Biol 176:35–42

Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9:1392–1400