Tumors and Tumor-Like Lesions of the Hepatobiliary Tract pp 3323-3350 | Cite as
Mechanisms of Invasion and Metastasis: Cell Migration and Chemotaxis
Abstract
For the acquisition of active motility, cancer cells must undergo a shape change to acquire a polarized phenotype, similar to locomoting leukocytes. Polarity of motile cells is characterized by a leading front and a rear region. Polarity of normal and neoplastic cells depends on a distinct cortical actin skeleton and the generation of various cell junctions. Several cytoskeletal proteins promote polarity in normal and transformed cells, including Hugl-1, radixin, and claudin-1. Cell surface proteins interacting with other cells and matrix transmit signals to the machinery which generates polarity and motility. The motile response of polarized tumor cells is associated with the biogenesis of several types of cell projections, including blebs, pseudopods, lamellipodia, filopodia, and cytonemes. The function of these projections in cell migration critically depends on a complex cytoskeletal machinery. The expression of polarity- and motility-associated proteins in normal and neoplastic cells is subject to epigenetic modifications, specifically to numerous types of microRNAs. Motility and migration are induced by two basic forms of chemical stimulation, i.e., chemokinesis (induced random motility) and chemotaxis (induced directed motility). Several chemokinetic and chemotactic factors have been identified in cancers.
Keywords
Hepatocyte Growth Factor Tumor Cell Migration Tumor Cell Motility Focal Adhesion Protein Apicobasal PolarityReferences
- Ackerman MA, Shriver M, Perry NA, Hu LY, Kontrogianni-Konstantopoulos A (2014) Obscurins: Goliaths and Davids take over non-muscle tissues. PLoS One 9:e88162CrossRefGoogle Scholar
- Ady JW, Desir S, Thayanithy V, Vogel RI, Moreira AL, Downey RJ, Fong Y, Manova-Todorova K, Moore MA, Lou E (2014) Intercellular communication in malignant pleural mesothelioma: properties of tunneling nanotubes. Front Physiol 5:400PubMedPubMedCentralCrossRefGoogle Scholar
- Ahmad T, Mukherjee S, Pattnaik B, Kumar M, Singh S, Kumar M, Rehman R, Tiwari BK, Jha KA, Barhanpurkar AP et al (2014) Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy. EMBO J 33:994–1010PubMedPubMedCentralGoogle Scholar
- Akhshi TK, Wernike D, Piekny A (2014) Microtubules and actin work together to polarize cells for division and migration. Cytoskeleton (Hoboken) 71:1–23CrossRefGoogle Scholar
- An JH, Kim JW, Jang SM, Kim CH, Kang EJ, Choi KH (2011) Gelsolin negatively regulates the activity of tumor suppressor p53 through their physical interaction in hepatocarcinoma HepG2 cells. Biochem Biophys Res Commun 412:44–49PubMedCrossRefGoogle Scholar
- Angus L, Moleirnho S, Herron L, Sinha A, Zhang X, Niestrata M, Dholakia K, Prystowsky MB et al (2012) Willin/FRMD6 expression activates the Hippo signaling pathway kinases in mammals and antagonizes oncogenic YAP. Oncogene 31:238–250PubMedCrossRefGoogle Scholar
- Arjonen A, Kaukonen R, Ivaska J (2011) Filopodia and adhesion in cancer cell motility. Cell Adhes Migr 5:421–430CrossRefGoogle Scholar
- Austefjord MW, Gerdes HH, Wang X (2014) Tunneling nanotubes: diversity in morphology and structure. Commun Integr Biol 7:e27934PubMedPubMedCentralCrossRefGoogle Scholar
- Bae YH, Ding Z, Das T, Wells A, Gertler F, Roy P (2010) Profilin1 regulates PI(3,4)P2 and lamellipodin accumulation at the leading edge thus influencing motility of MDA-MB-231 cells. Proc Natl Acad Sci U S A 107:21547–21552PubMedPubMedCentralCrossRefGoogle Scholar
- Baehs S, Herbst A, Thieme SE, Perschl C, Behrens A, Scheel S, Jung A, Brabletz T et al (2009) Dickkopf-4 is frequently down-regulated and inhibits growth of colorectal cancer cells. Cancer Lett 276:152–159PubMedCrossRefGoogle Scholar
- Ballestrem C, Wehrle-Haller B, Hinz B, Imhof BA (2000) Actin-dependent lamellipodia formation and microtubule-dependent tail retraction control-directed cell migration. Mol Cell Biol 11:2999–3012CrossRefGoogle Scholar
- Barzik M, McClain LM, Gupton SL, Gertler FB (2014) Ena/VASP regulates mDia2-initiated filopodial length, dynamics, and function. Mol Biol Cell 25:2604–2619PubMedPubMedCentralCrossRefGoogle Scholar
- Baum B, Kunda P (2005) Actin nucleation: spire – actin nucleator in a class of its own. Curr Biol 15:R305–R308PubMedCrossRefGoogle Scholar
- Bernard O (2007) Lim kinases, regulators of actin dynamics. Int J Biochem Cell Biol 39:1071–1076PubMedCrossRefGoogle Scholar
- Bisi S, Disanza A, Malinverno C, Frittoli E, Palamidessi A, Scita G (2013) Membrane and actin dynamics interplay at lamellipodia leading edge. Curr Opin Cell Biol 25:565–573PubMedCrossRefGoogle Scholar
- Blood CH, Zetter BR (1993) Laminin regulates a tumor cell chemotaxis receptor through the laminin-binding integrin subunit alpha 6. Cancer Res 53:2661–2666PubMedGoogle Scholar
- Boeda B, Etienne-Manneville S (2015) Spectrin binding motifs regulate Scribble cortical dynamics and polarity function. Elife. doi:10.7554/eLife.04726PubMedPubMedCentralGoogle Scholar
- Boer EF, Howell ED, Schilling TF, Jette CA, Stewart RA (2015) Fascin1-dependent filopodia are required for directional migration of a subset of neural crest cells. PLoS Genet 11:e1004946PubMedPubMedCentralCrossRefGoogle Scholar
- Bozzuto G, Ruggiweri P, Molinari A (2010) Molecular aspects of tumor cell migration and invasion. Ann Iast Super Sanita 46:66–80Google Scholar
- Bradbury P, Fabry B, O’Neill GM (2012) Occupy tissue. The movement in cancer metastasis. Cell Adhes Migr 6:424–432CrossRefGoogle Scholar
- Brauckhoff A, Malz M, Tschaharganeh D, Malek N, Weber A, Riener MO, Soll C, Samarin J et al (2011) Nuclear expression of the ubiquitin ligase seven in absentia homolog (SIAH)-1 induces proliferation and migration of liver cancer cells. J Hepatol 55:1049–1057PubMedCrossRefGoogle Scholar
- Bunthot S, Obchoei S, Kraiklang R, Pirojkul C, Wongkham S, Wongkham C (2012) Overexpression of claudin-4 in cholangiocarcinoma tissues and its possible role in tumor metastasis. Asian Pac J Cancer Prev 13(Suppl):71–76PubMedGoogle Scholar
- Cao Y, Chang H, Li L, Cheng RC, Fan XN (2007) Alterations of adhesion molecule expression and cellular polarity in hepatocellular carcinoma. Histopathology 51:528–538PubMedCrossRefGoogle Scholar
- Cao T, Li H, Hu Y, Ma D, Cai X (2014) miR-144 suppresses the proliferation and metastasis of hepatocellular carcinoma by targeting E2F3. Tumour Biol 35:10759–10764PubMedCrossRefGoogle Scholar
- Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ (2010) Exosome release of b-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 190:1079–1091PubMedPubMedCentralCrossRefGoogle Scholar
- Chakraborty S, Lakshmanan M, Swa HL, Chen J, Zhang X, Ong YS, Loo LS, Akincilar SC, Gunaratne J, Tergaonkar V et al (2015) An oncogenic role of Agrin in regulating focal adhesion integrity in hepatocellular carcinoma. Nat Commun 6:6184PubMedPubMedCentralCrossRefGoogle Scholar
- Chan J, Ko FC, Yeung YS, Ng IO, Yam JW (2011) Integrin-linked kinase overexpression and its oncogenic role in promoting tumorigenicity of hepatocellular carcinoma. PLoS One 6:e16984PubMedPubMedCentralCrossRefGoogle Scholar
- Chang TM, Hung WC (2012) Transcriptional repression of TWIST1 gene by Prospero-related homeobox 1 inhibits invasiveness of hepatocellular carcinoma cells. FEBS Lett 586:3746–3752PubMedCrossRefGoogle Scholar
- Chang YC, Zhang H, Brennan ML, Wu J (2013) Crystal structure of lamellipodin implicates diverse functions in actin polymerization and Ras signaling. Protein Cell 4:211–219PubMedPubMedCentralCrossRefGoogle Scholar
- Chen CK, Sawaya MR, Phillips ML, Reisler E, Quinlan ME (2012) Multiple forms of Spire-actin complexes and their functional consequences. J Biol Chem 287:10684–10692PubMedPubMedCentralCrossRefGoogle Scholar
- Chen H, Miao R, Fan J, Han Z, Wu J, Qiu G, Tang H, Peng Z (2013a) Decreased expression of miR-126 correlates with metastatic recurrence of hepatocellular carcinoma. Clin Exp Metastasis 30:651–658PubMedCrossRefGoogle Scholar
- Chen YW, Chu HC, Ze-Chiang L, Shiah WJ, Chou CP, Klimstra DS, Lewis BC (2013b) p16 stimulates CDC42-dependent migration of hepatocellular carcinoma cells. PLoS One 8:e69389PubMedPubMedCentralCrossRefGoogle Scholar
- Chen YL, Wang TH, Hsu HC, Yuan RH, Jeng YM (2013c) Overexpression of CTHRC1 in hepatocellular carcinoma promotes tumor invasion and predicts poor prognosis. PLoS One 8:e70324PubMedPubMedCentralCrossRefGoogle Scholar
- Chen XJ, Squarr AJ, Stephan R, Chen B, Higgins TE, Barry DJ, Martin MC, Rosen MK, Bogdan S, Way M (2014) Ena/VASP proteins cooperate with the WAVE complex to regulate the actin cytoskeleton. Dev Cell 30:569–584PubMedPubMedCentralCrossRefGoogle Scholar
- Chen X, Bo L, Zhao X, Chen Q (2015) MicroRNA-133a inhibits cell proliferation, colony formation ability, migration and invasion by targeting matrix metalloproteinase 9 in hepatocellular carcinoma. Mol Med Rep. doi:10.3892/mmr.2015.3232Google Scholar
- Cheng IK, Tsang BC, Lai KP, Ching AK, Chan AW, To KF, Lai PB, Wong N (2012) GEF-H1 over-expression in hepatocellular carcinoma promotes cell motility via activation of RhoA signaling. J Pathol. doi:10.1002/path.4084PubMedCentralGoogle Scholar
- Chuma et al. (2004) http://www.ncbi.nlm.nih.gov/pubmed/15464244
- Cramer LP (1999) Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. Biochem Soc Symp 65:173–205PubMedGoogle Scholar
- Dagouassat M, Suffee N, Hlawaty H, Haddad O, Charni F, Laguillier C, Vassy R, Martin L, Schischmanoff PO, Gattegno L et al (2010) Monocyte chemoattractant protein-1 (MCP-1)/CCL2 secreted by hepatic myofibroblasts promotes migration and invasion of human hepatoma cells. Int J Cancer 126:1095–1108PubMedGoogle Scholar
- Dai W, Wang C, Wang F, Wang Y, Shen M, Chen K, Cheng P, Zhang Y, Yang J, Zhu R, Zhang H, Li J, Zheng Y et al (2014) Anti-miR-197 inhibits migration in HCC cells by targeting KAI 1/CD82. Biochem Biophys Res Commun 446:541–548PubMedCrossRefGoogle Scholar
- Dang I, Gorelik R, Sousa-Blin C, Derivery E, Guérin C, Linkner J, Nemethova M, Dumortier JG et al (2013) Inhibitory signaling to the Arp2/3 complex steers cell migration. Nature 503:281–284PubMedGoogle Scholar
- De Vreede G, Schoenfled JD, Windler SL, Morrison H, Lu H, Bilder D (2014) The Scribble module regulates retromer-dependent endocytic trafficking during epithelial polarization. Development 141:2796–2802PubMedPubMedCentralCrossRefGoogle Scholar
- Deakin NO, Ballestrem C, Turner CE (2012) Paxillin and Hic-5 interaction with vinculin is differentially regulated by Rac1 and RhoA. PLoS One 7:e37990PubMedPubMedCentralCrossRefGoogle Scholar
- Dillenburg-Pilla P, Patel V, Mikelis CM, Zarate-Bladés CR, Doçi CL, Amornphimoltham P, Wang Z, Martin D, Leelahavanichkul K et al (2015) SDF-1/CXCL12 induces directional cell migration and spontaneous metastasis via a CXCR4/Gαi/mTORC1 axis. FASEB J 29:1056–1068Google Scholar
- Ding J, Huang S, Wu S, Zhao Y, Liang L, Yan M, Ge C, Yao J, Chen T, Wand D, Wang H, Gu J, Yao M, Li J, Tu H et al (2010) Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol 12:390–399PubMedCrossRefGoogle Scholar
- Ding J, Huang S, Wang Y, Tian Q, Zha R, Shi H, Wang Q, Ge C, Chen T, Zhao Y et al (2013) Genome-wide screening revealed that miR-195 targets the TNF-a/NF-kB pathway by downregulating IKKa and TAB3 in hepatocellular carcinoma. Hepatology 58:654–666PubMedCrossRefGoogle Scholar
- Donthamsetty S, Have VS, Mars WM, Bowen WC, Orr A, Haynes MM, Wu C, Michalopoulos GK (2013) Role of PINCH and its partner tumor suppressor Rsu-1 in regulating liver size and tumorigenesis. PLoS One 8:e74625PubMedPubMedCentralCrossRefGoogle Scholar
- Dütting S, Brachs S, Mielenz D (2011) Fraternal twins – Swiprosin-1/EFhd2 and Swiprosin-2/EFhd1, two homologous EF-hand containing calcium binding adaptor proteins with distinct functions. Cell Commun Signal 9:2PubMedPubMedCentralCrossRefGoogle Scholar
- Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer zu Brickwedde MK, Ohno S, Vestweber D (2001) The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J 20:3738–3748PubMedPubMedCentralCrossRefGoogle Scholar
- Elsum I, Yates L, Humbert PO, Richardson HE (2012) The Scribble-Dlg-Lgl polarity module in development and cancer: from flies to man. Essays Biochem 53:141–168PubMedCrossRefGoogle Scholar
- Fairchild CL, Barna M (2014) Specialized filopodia: at the ‘tip’ of morphogen transport and vertebrate tissue patterning. Curr Opin Genet Dev 27:67–73PubMedCrossRefGoogle Scholar
- Faix J, Rottner K (2006) The making of filopodia. Curr Opin Cell Biol 18:18–25PubMedCrossRefGoogle Scholar
- Faix J, Breitsprecher D, Stradal TE, Rottner K (2009) Filopodia: complex models for simple rods. Int J Biochem Cell Biol 41:1656–1664PubMedCrossRefGoogle Scholar
- Fan Q, He M, Deng X, Wu WK, Zhao L, Tang J, Wen G, Sun X, Liu Y (2013) Depression of c-Fos caused by microRNA-139 down-regulation contributes to the metastasis of human hepatocellular carcinoma. Cell Biochem Funct 31:319–324PubMedCrossRefGoogle Scholar
- Fang CM, Xu YH (2001) Down-regulated expression of atypical PKC-binding domain deleted asip isoforms in human hepatocellular carcinomas. Cell Res 11:223–229PubMedCrossRefGoogle Scholar
- Fang S, Lorick KL, Jensen JP, Weissman AM (2003) RING finger ubiquitin protein ligases: implications for tumorigenesis, metastasis and for molecular targets in cancer. Semin Cancer Biol 13:5–14PubMedCrossRefGoogle Scholar
- Fang Y, Xue JL, Shen Q, Chen J, Tian L (2012) MicroRNA-7 inhibits tumor growth and metastasis by targeting the phosphoinositide 3-kinase/Akt pathway in hepatocellular carcinoma. Hepatology 55:1852–1862PubMedCrossRefGoogle Scholar
- Fang KP, Zhang JL, Ren YH, Qian YB (2014) Talin-1 correlates with reduced invasion and migration in human hepatocellular carcinoma cells. Asian Pac J Cancer Prev 15:2655–2661PubMedCrossRefGoogle Scholar
- Fu BH, Wu ZZ, Dong C (2004) Integrin beta1 mediates hepatocellular carcinoma cells chemotaxis to laminin. Hepatobiliary Pancreat Dis Int 3:548–551PubMedGoogle Scholar
- Fu BH, Wu ZZ, Qin J (2010) Effects of integrins on laminin chemotaxis by hepatocellular carcinoma cells. Mol Biol Rep 37:1665–1670PubMedCrossRefGoogle Scholar
- Fu BH, Wu ZZ, Qin J (2011) Effects of integrin α6β1 on migration of hepatocellular carcinoma cells. Mol Biol Rep 38:3271–3276PubMedCrossRefGoogle Scholar
- Fu D, Lippincott-Schwartz J, Arias IM (2013) Increased mitochondrial fusion and autophagy help isolated hepatocytes repolarize in collagen sandwich cultures. Autophagy 9:2154–2155PubMedCrossRefGoogle Scholar
- Fukuda T, Chen K, Shi X, Wu C (2003) PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and survival. J Biol Chem 278:51324–51333PubMedCrossRefGoogle Scholar
- Fukuda K, Gupta S, Chen K, Wu C, Qin J (2009) The pseudoactive site of ILK is essential for its binding to alpha-Parvin and localization to focal adhesions. Mol Cell 36:819–830PubMedPubMedCentralCrossRefGoogle Scholar
- Fukuda K, Bledska K, Yang J, Pererea HD, Plow EF, Qin J (2014) Molecular basis of kindlin-2 binding to integrin-linked kinase pseudokinase for regulating cell adhesion. J Biol Chem 289:28363–28375PubMedPubMedCentralCrossRefGoogle Scholar
- Gagliardi PA, di Blasio L, Puliafito A, Seano G, Sessa R, Chianale F, Leung T, Bussolino F, Primo L (2014) PDK1-mediated activation of MRCKα regulates directional cell migration and lamellipodia retraction. J Cell Biol 206:415–434PubMedPubMedCentralCrossRefGoogle Scholar
- Galkina SI, Fedorova NV, Stadnichuk VI, Sud’ina GF (2013) Membrane tubulovesicular extensions (cytonemes): secretory and adhesive cellular organelles. Cell Adh Migr 7:174–186PubMedPubMedCentralCrossRefGoogle Scholar
- Galkina SI, Fedorova NV, Serebryakova MV, Arifulin EA, Stadnichuk VI, Gaponova TV, Baratova LA, Sud’ina GF (2015) Inhibition of the GTPase dynamin or actin depolymerization initiates outward plasma membrane tubulation/vesiculation (cytoneme formation) in neutrophils. Biol Cell. doi:10.1111/boc.201400063PubMedGoogle Scholar
- Gallagher KL, Benfey PN (2005) Not just another hole in the wall: understanding intercellular protein trafficking. Genes Dev 19:189–195PubMedCrossRefGoogle Scholar
- Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, Langen R, McMahon HT (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25:2898–2910PubMedPubMedCentralCrossRefGoogle Scholar
- Gang Z, Ya-Lin K, Dong-Qing W, Yu L, Li R, Hong-Yi Z (2013) Combining cortactin and CTTN detection with clinicopathologic features increases effectiveness of survival predictions for patients with resectable hepatocellular carcinoma. Clin Lab 59:1343–1352PubMedGoogle Scholar
- Gardberg M, Kaipio K, Lehtinen L, Mikkonen P, Heuser VD, Talvinen K, Iljin K, Kampf C et al (2013) FHOD1, a formin upregulated in epithelial-mesenchymal transition, participates in cancer cell migration and invasion. PLoS One 8:e74923PubMedPubMedCentralCrossRefGoogle Scholar
- Genda et al. (1999) http://www.ncbi.nlm.nih.gov/pubmed/10498656
- Gertler F, Condeelis J (2011) Metastasis: tumor cells becoming MENAcing. Trends Cell Biol 21:81–90PubMedCrossRefGoogle Scholar
- Ghatak S, Morgner J, Wickström SA (2013) ILK: a pseudokinase with a unique function in the integrin-actin linkage. Biochem Soc Trans 41:995–1001PubMedCrossRefGoogle Scholar
- Goetz SC, Ocbina PJ, Anderson KV (2009) The primary cilium as a Hedgehog signal transduction machine. Methods Cell Biol 94:199–222PubMedPubMedCentralCrossRefGoogle Scholar
- Grise F, Bidaud A, Moreau V (2009) Rho GTPases in hepatocellular carcinoma. Biochim Biophys Acta 1795:137–151PubMedGoogle Scholar
- Gross SR (2013) Actin binding proteins: their ups and downs in metastatic life. Cell Adh Migr 7:199–213PubMedPubMedCentralCrossRefGoogle Scholar
- Gunn-Moore FJ, Welsh GI, Herron LR, Brannigan F, Venkateswarlu K, Gillespie S et al (2005) A novel 4.1 ezrin radixin moesin (FERM)-containing, ‘Willin’. FEBS Lett 579:5089–5094PubMedCrossRefGoogle Scholar
- Gupton SL, Gertler FB (2007) Filopodia: the fingers that do the walking. Sci STKE 2007(400):re5PubMedCrossRefGoogle Scholar
- Hager MH, Morley S, Bielenberg DR, Gao S, Morello M, Holcomb IN, Liu W, Mouneimne G et al (2012) DIAPH3 governs the cellular transition to the amoeboid tumour phenotype. EMBO Mol Med 4:743–760PubMedPubMedCentralCrossRefGoogle Scholar
- Halaoui R, McCaffey L (2014) Rewiring cell polarity signaling in cancer. Oncogene. doi:10.1038/onc.2014.59PubMedGoogle Scholar
- Hall A (2009) The cytoskeleton and cancer. Cancer Metastasis Rev 28:5–14PubMedCrossRefGoogle Scholar
- Harris HJ, Clerte C, Farquhar MJ, Goodall M, Hu K, Rassam P, Dosset P, Wilson GK, Balfe P, Ijzendoorn SC, Milhiet PE et al (2013) Hepatoma polarization limits CD81 and hepatitis C virus dynamics. Cell Microbiol 15:430–445PubMedCrossRefGoogle Scholar
- Hayashi Y, Osanai M, Lee GH (2011) Fascin-1 expression correlates with repression of E-cadherin expression in hepatocellular carcinoma cells and augments their invasiveness in combination with matrix metalloproteinases. Cancer Sci 102:1228–1235PubMedCrossRefGoogle Scholar
- Helgeson LA, Prendergast JG, Wagner AR, Rodnick-Smith M, Nolen BJ (2014) Interactions with actin monomers, actin filaments, and Arp2/3 complex define the roles of WASP family proteins and cortactin in coordinately regulating branched actin networks. J Biol Chem 289:28856–28869PubMedPubMedCentralCrossRefGoogle Scholar
- Hirose et al. (2002) http://www.ncbi.nlm.nih.gov/pubmed/12045219
- Hoffmann AK, Nai X, Linder S (2014) Daam1 is a regulator of filopodia formation and phagocytic uptake of Borrelia burgdorferi by primary human macrophages. FASEB J 28:3075–3089PubMedCrossRefGoogle Scholar
- Honda S, Shirotani-Ikejima H, Tadokoro S, Tomiyama Y, Miyata T (2013) The integrin-linked kinase-PINCH-parvin complex supports integrin aIIbb3 activation. PLoS One 8:e85498PubMedPubMedCentralCrossRefGoogle Scholar
- Horita Y, Ohashi K, Mukai M, Inoue M, Mizuno K (2008) Suppression of the invasive capacity of rat ascites hepatoma cells by knockdown of Slingshot or LIM kinase. J Biol Chem 283:6013–6021PubMedCrossRefGoogle Scholar
- Hsieh SY, He JR, Hsu CY, Chen WJ, Bera R, Lin KY, Shih TC, Yu MC, Lin YJ et al (2011) Neuregulin/erythroblastic leukemia viral oncogene homolog 3 autocrine loop contributes to invasion and early recurrence of human hepatoma. Hepatology 53:504–516PubMedCrossRefGoogle Scholar
- Hu Y, Fang C, Xu Y (2005) The effect of isoforms of the cell polarity protein, human ASIP, on the cell cycle and Fas/FasL-mediated apoptosis in human hepatoma cells. Cell Mol Life Sci 62:1974–1983PubMedCrossRefGoogle Scholar
- Hu CT, Cheng CC, Pan SM, Wu JR, Wu WS (2013) PKC mediates fluctuant ERK-paxillin signaling for hepatocyte growth factor-induced migration of hepatoma cell HepG2. Cell Signal 25:1457–1467PubMedCrossRefGoogle Scholar
- Hua M, Zhang W, Li W, Li X, Liu B, Lu X, Zhang H (2012) Molecular mechanisms regulating the establishment of hepatocyte polarity during human hepatic progenitor cell differentiation into a functional hepatocyte-like phenotype. J Cell Sci 125:5800–5810PubMedCrossRefGoogle Scholar
- Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K (2003) JNK phosphorylates paxillin and regulates cell migration. Nature 424:219–223PubMedCrossRefGoogle Scholar
- Huang C, Jacobson K, Schaller MD (2004) A role for JNK-paxillin signalling in cell migration. Cell Cycle 3:4–6PubMedGoogle Scholar
- Huang X, Ji J, Xue H, Zhang F, Han X, Cai Y, Zhang J, Ji G (2012) Fascin and cortactin expression is correlated with a poor prognosis in hepatocellular carcinoma. Eur J Gastroenterol Hepatol 24:633–639PubMedCrossRefGoogle Scholar
- Huh YH, Kim SH, Chung KH, Oh S, Kwon MS, Choi HW, Rhee S, Ryu JH, Park ZY et al (2013) Swiprosin-1 modulates actin dynamics by regulating the F-actin accessibility to cofilin. Cell Mol Life Sci 70:4841–4854PubMedPubMedCentralCrossRefGoogle Scholar
- Hyeon J, Ahn S, Lee JJ, Song DH, Park CK (2013) Expression of fibroblast growth factor 19 is associated with recurrence and poor prognosis of hepatocellular carcinoma. Dig Dis Sci 58:1916–1922PubMedCrossRefGoogle Scholar
- Iguchi T, Aishima S, Umeda K, Sanefuji K, Sugimachi K, Gion T, Taketomi A, Maehara Y, Tsuneyoshi M (2009) Fascin expression in progression and prognosis in hepatocellular carcinoma. J Surg Oncol 100:575–579PubMedCrossRefGoogle Scholar
- Insall R (2013) The interaction between pseudopods and extracellular signalling during chemotaxis and directed migration. Curr Opin Cell Biol 25:526–531PubMedCrossRefGoogle Scholar
- Ip YC, Cheung ST, Lee YT, Ho JC, Fan ST (2007) Inhibition of hepatocellular carcinoma invasion by suppression of claudin-10 in HLE cells. Mol Cancer Ther 6:2858–2867PubMedCrossRefGoogle Scholar
- Ishino K, Kaeyama, Shibanuma M, Nose K (2000) Specific decrease in the level of Hic-5, a focal adhesion protein, during immortalization of mouse embryonic fibroblasts, and its association with focal adhesion kinase. J Cell Biochem 76:411PubMedCrossRefGoogle Scholar
- Ishiuchi T, Takeichi M (2011) Willin and Par3 cooperatively regulate epithelial apical constriction through aPKC-mediated ROCK phosphorylation. Nat Cell Biol 13:860–866PubMedCrossRefGoogle Scholar
- Ito M, Hagiyama M, Mimae T, Inoue T, Kato T, Yoneshige A, Nakanishi J, Kondo T, Okada M, Ito A (2014) α-Parvin, a pseudopodial constituent, promotes cell motility and is associated with lymph node metastasis of lobular breast carcinoma. Breast Cancer Res Treat 144:59–69PubMedCrossRefGoogle Scholar
- Jan YJ, Ko BS, Liu TA, Wu YM, Liang SM, Chen SC, Wang J, Liou JY (2013) Expression of partitioning defective 3 (par-3) for predicting extrahepatic metastasis and survival with hepatocellular carcinoma. Int J Mol Sci 14:1684–1697PubMedPubMedCentralCrossRefGoogle Scholar
- Ji Y, Li B, Zhu Z, Guo X, He W, Fan Z, Zhang W (2015) Overexpression of WAVE3 promotes tumor invasiveness and confers an unfavorable prognosis in human hepatocellular carcinoma. Biomed Pharmacother 69:409–415PubMedCrossRefGoogle Scholar
- Jia CC, Wang TT, Liu W, Fu BS, Hua X, Wang GY, Li TJ, Li X, Wu XY, Tai Y et al (2013) Cancer-associated fibroblasts from hepatocellular carcinoma promote malignant cell proliferation by HGF secretion. PLoS One 8:e63243PubMedPubMedCentralCrossRefGoogle Scholar
- Jia D, Jing Y, Zhang Z, Liu L, Ding J, Zhao F, Ge C, Wang Q, Chen T, Yao M, Li J, Gu J, He X (2014) Amplification of MPZL1/PZR promotes tumor cell migration Src-mediated phosphorylation of cortactin in hepatocellular carcinoma. Cell Res 24:204–207PubMedCrossRefGoogle Scholar
- Jin KM, Lu M, Liu FF, Gu J, Du XJ, Xing BC (2013) N-WASP is highly expressed in hepatocellular carcinoma and associated with poor prognosis. Surgery 153:518–525PubMedCrossRefGoogle Scholar
- Johnson HE, King SJ, Asokan SB, Rotty JD, Bear JE, Haugh JM (2015) F-actin bundles direct the initiation and orientation of lamellipodia through adhesion-based signaling. J Cell Biol 208:443–455Google Scholar
- Kanamori H, Kawakami T, Effendi K, Yamazaki K, Mori T, Ebinuma H, Masugi Y, Du W, Nagasaka K, Ogiwara A et al (2011) Identification by differential tissue proteome analysis of talin-1 as a novel molecular marker of progression of hepatocellular carcinoma. Oncology 80:406–415PubMedCrossRefGoogle Scholar
- Kang YK, Hong SW, Lee H, Kim WH (2010) Prognostic implications of ezrin expression in human hepatocellular carcinoma. Mol Carcinog 49:798–804PubMedGoogle Scholar
- Kang YH, Ji NY, Lee CI, Lee HG, Kim JW, Yeom YI, Kim DG, Yoon SK, Kim JW et al (2011) ESM-1 silencing decreased cell survival, migration, and invasion and modulated cell cycle progression in hepatocellular carcinoma. Amino Acids 40:1003–1013PubMedCrossRefGoogle Scholar
- Kashyap A, Zimmerman T, Ergül N, Bosserhoff A, Hartman U, Alla V, Bataille F, Galle PR, Strand S, Strand D (2013) The human Lgll polarity gene, Hugl-2, induces MET and suppresses Snail tumorigenesis. Oncogene 32:1396–1407PubMedCrossRefGoogle Scholar
- Kaufmann R, Rahn S, Pollrich K, Hertel J, Dittmar Y, Hommann M, Henklein P, Biskup C, Westermann M, Hollenberg MD et al (2007) Thrombin-mediated hepatocellular carcinoma cell migration: cooperative action via proteinase-activated receptors 1 and 4. J Cell Physiol 211:699–707PubMedCrossRefGoogle Scholar
- Kaufmann R, Oettel C, Horn A, Halbhuber KJ, Eitner A, Krieg R, Katenkamp K, Henklein P et al (2009) Met receptor tyrosine kinase transactivation is involved in proteinase-activated receptor-2-mediated hepatocellular carcinoma cell invasion. Carcinogenesis 30:1487–1496PubMedCrossRefGoogle Scholar
- Keller HU, Zimmermann A (1986) Shape changes and chemokinesis of Walker 256 carcinosarcoma cells in response to colchicine, vinblastine, nocodazole and taxol. Invasion Metastasis 6:33–43PubMedGoogle Scholar
- Keller HU, Zimmermann A, Niggli V (1989) Diacylglycerols and the protein kinase inhibitor H-7 suppress cell polarity and locomotion of Walker 256 carcinosarcoma cells. Int J Cancer 44:934–939PubMedCrossRefGoogle Scholar
- Keller H, Niggli V, Zimmermann A (1991) Diversity of motile responses of human neutrophil granulocytes: functional meaning and cytoskeletal basis. Adv Exp Med Biol 297:23–37PubMedCrossRefGoogle Scholar
- Kelley LC, Hayes KE, Ammer AG, Martin KH, Weed SA (2010) Cortactin phosphorylated by ERK1/2 localizes to sites of dynamic actin regulation and is required for carcinoma lamellipodia persistence. PLoS One 5:e13847PubMedPubMedCentralCrossRefGoogle Scholar
- Khanduja N, Kuhn JR (2014) Processive acceleration of actin barbed end assembly by N-WASP. Mol Biol Cell 25:55–65PubMedPubMedCentralCrossRefGoogle Scholar
- Kim MS, Yoo NJ, Lee SH (2011) Absence of paxillin gene mutation in lung cancer and other common solid cancers. Tumori 97:211–213PubMedGoogle Scholar
- Kirkbride KC, Sung BH, Sinha S, Weaver AM (2011) Cortactin: a multifunctional regulator of cellular invasiveness. Cell Adh Migr 5:187–198PubMedPubMedCentralCrossRefGoogle Scholar
- Klemke RL, Jiang X, Choi S, Kelber JA (2013) Proteomic and biochemical methods to study the cytoskeletome. Methods Mol Biol 1046:203–218PubMedCrossRefGoogle Scholar
- Koestler SA, Steffen A, Nemethova M, Winterhoff M, Luo N, Holleboom JM, Krupp J et al (2013) Arp2/3 complex is essential for actin network treadmilling as a well as for targeting of capping protein and cofilin. Mol Biol Cell 24:2861–2875PubMedPubMedCentralCrossRefGoogle Scholar
- Kojima H, Nies AT, König J, Hagmann W, Spring H, Uemura M, Fukui H, Keppler D (2003) Changes in the expression and localization of hepatocellular transporters and radixin in primary biliary cirrhosis. J Hepatol 39:693–702PubMedCrossRefGoogle Scholar
- Kojima T, Murata M, Yamamoto T, Lan M, Imamura M, Son S, Takano KI, Yamaguchi H et al (2009) Tight junction proteins and signal transduction pathways in hepatocytes. Histol Histopathol 24:1463–1472PubMedGoogle Scholar
- Kominsky SL (2006) Claudins: emerging targets for cancer therapy. Expert Rev Mol Med 8:1–11PubMedCrossRefGoogle Scholar
- Korhan P, Erdal E, Atabey N (2014) MiR-181a-5p is downregulated in hepatocellular carcinoma and suppresses motility, invasion and branching-morphogenesis by directly targeting c-Met. Biochem Biophys Res Commun 450:1304–1312PubMedCrossRefGoogle Scholar
- Kornberg TB (2014a) Cytonemes and the dispersion of morphogens. Wiley Interdisc Rev Dev Biol 3:445–463CrossRefGoogle Scholar
- Kornberg TB (2014b) The contrasting roles of primary cilia and cytonemes in Hh signaling. Dev Biol 394:1–5PubMedPubMedCentralCrossRefGoogle Scholar
- Kornberg TB, Roy S (2014) Cytonemes as specialized signaling filopodia. Development 141:729–736PubMedPubMedCentralCrossRefGoogle Scholar
- Krause M, Leslie JD, Stewart M, Lafuente EM, Valderrama F, Jagannathan R, Strasser GA et al (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev Cell 7:571–583PubMedCrossRefGoogle Scholar
- Kurisu S, Takenawa T (2009) The WASP and WAVE family proteins. Genome Biol 10:226PubMedPubMedCentralCrossRefGoogle Scholar
- Kwon MS, Park KR, Kim YD, Na BR, Kim HR, Choi HJ, Piragyte I, Jeon H, Chung KH et al (2013) Swiprosin-1 is a novel actin bundling protein that regulates cell spreading and migration. PLoS One 8:e71626PubMedPubMedCentralCrossRefGoogle Scholar
- Lai TY, Su CC, Kuo WW, Yeh YL, Kuo WH, Tsai FJ, Tsai CH, Weng YJ, Huang CY et al (2011) b-catenin plays a key role in metastasis of human hepatocellular carcinoma. Oncol Rep 26:415–422PubMedGoogle Scholar
- Las G, Shirihai OS (2014) Miro1: new wheels for transferring mitochondria. EMBO J 33:939–941PubMedPubMedCentralCrossRefGoogle Scholar
- Law AL, Vehlow A, Kotini M, Dodgson L, Soong D, Theveneau E, Bodo C, Taylor E et al (2013) Lamellipodin and the Scar/WAVE complex cooperate to promote cell migration in vivo. J Cell Biol 203:673–689PubMedPubMedCentralCrossRefGoogle Scholar
- Lee JY (2014) New and old roles of plasmodesmata in immunity and parallels to tunneling nanotubes. Plant Sci 221–222:13–20PubMedCrossRefGoogle Scholar
- Lee JM, Yang J, Newell P, Singh S, Parwani A, Friedman SL, Nejak-Bowen KN et al (2014) Beta-catenin signaling in hepatocellular cancer: implications in inflammation, fibrosis, and proliferation. Cancer Lett 343:90–97PubMedCrossRefGoogle Scholar
- Legate KR, Montanez E, Kudlacek O, Fässler R (2006) ILK, PINCH and parvin: the tIPP of integrin signaling. Nat Rev Mol Cell Biol 7:20–31PubMedCrossRefGoogle Scholar
- Lemmers C, Michel D, Lane-Guermonprez L, Delgrossi MH, Médina E, Arsanto JP, Le Bivic A (2004) CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol Biol Cell 15:1324–1333PubMedPubMedCentralCrossRefGoogle Scholar
- Leong GR, Goulding KR, Amin N, Richardson HE, Brumby AM (2009) Scribble mutants promote aPKC abd JNK-dependent epithelial neoplasia independently of Crumbs. BMC Biol 7:62PubMedPubMedCentralCrossRefGoogle Scholar
- Li HG, Xie DR, Shen XM, Li HH, Zeng H, Zeng YJ (2005) Clinicopathlogical of expression of paxillin, syndecan-1 and EMMPRIN in hepatocellular carcinoma. World J Gastroenterol 11:1445–1451PubMedPubMedCentralCrossRefGoogle Scholar
- Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y, Zheng X (2009) miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 275:44–53PubMedCrossRefGoogle Scholar
- Li QJ, Zhou L, Yang F, Wang GX, Zheng H, Wang DS, He Y, Dou KF (2012) MicroRNA-10b promotes migration and invasion through CADM1 in human hepatocellular carcinoma cells. Tumour Biol 33:1455–1465PubMedCrossRefGoogle Scholar
- Li Y, Zhou B, Dai J, Liu R, Han ZG (2013) Aberrant upregulation of LRRC1 contributes to human hepatocellular carcinoma. Mol Biol Rep 40:4543–4551PubMedCrossRefGoogle Scholar
- Li Q, Ding C, Chen C, Zhang Z, Xiao H, Xie F, Lei L, Chen Y, Mao B, Jiang M, Li J et al (2014a) miR-224 promotes cell migration and invasion by targeting homeobox D 10 gene in human hepatocellular carcinoma. J Gastroenterol Hepatol 29:835–842PubMedCrossRefGoogle Scholar
- Li T, Xie J, Shen C, Cheng D, Shi Y, Wu Z, Zhan Q, Deng X, Chen H, Shen B, Peng C, Li H, Zhu Z (2014b) miR-150-5p inhibits hepatoma cell migration and invasion by targeting MMP14. PLoS One 9:e15577Google Scholar
- Li P, Mao X, Ren Y, Liu P (2015a) Epithelial cell polarity determinant CRB3 in cancer development. Int J Biol Sci 11:31–37PubMedPubMedCentralCrossRefGoogle Scholar
- Li J, Fang L, Yu W, Wang Y (2015b) MicroRNA-125b suppresses the migration and invasion of hepatocellular carcinoma cells by targeting transcriptional coactivator with PDZ-binding motif. Oncol Lett 9:1971–1975PubMedPubMedCentralGoogle Scholar
- Li Y, Xu D, Bao C, Zhang Y, Chen D, Zhao F, Ding J, Liang L, Wang Q, Liu L, Li J, Yao M, Huang S, He X (2015c) MicroRNA-135b, a HSF1 target, promotes tumor invasion and metastasis by regulating RECK and EVI5 in hepatocellular carcinoma. Oncotarget 6:2421–2433PubMedCrossRefGoogle Scholar
- Liang L, Guan J, Zeng Y, Wang J, Li X, Zhang X, Ding Y (2011) Down-regulation of formin-like 2 predicts poor prognosis in hepatocellular carcinoma. Hum Pathol 42:1603–1612PubMedCrossRefGoogle Scholar
- Liao CH, Yeh CT, Huang YH, Wu SM, Chi HC, Tsai MM, Tsai CY, Liao CJ, Tseng YH et al (2011) Dickkopf 4 positively regulated by the thyroid hormone receptor surpasses cell invasion in human hepatoma cells. Hepatology 55:910–920CrossRefGoogle Scholar
- Liao CG, Kong LM, Zhou P, Yang XL, Huang JG, Zhang HL, Lu N (2014) miR-10b is overexpressed in hepatocellular carcinoma and promotes cell proliferation, migration and invasion through RhoC, uPAR and MMps. J Transl Med 12:234PubMedPubMedCentralCrossRefGoogle Scholar
- Lim YS, Tang BL (2012) Intracellular organelle trafficking by membranous nanotube connections: a possible new role in cellular rejuvenation? Cell Commun Adhes 19:39–44PubMedCrossRefGoogle Scholar
- Lin L, Yang XM, Li J, Zhang YL, Qin W, Zhang ZG (2014) Microfilament regulatory protein MENA increases activity of RhoA and promotes metastasis of hepatocellular carcinoma. Exp Cell Res 327:113–122PubMedCrossRefGoogle Scholar
- Lipkowitz S, Weissman AM (2011) RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat Rev Cancer 11:629–643PubMedPubMedCentralCrossRefGoogle Scholar
- Liu L, Zhu XD, Wang WQ, Shen Y, Qin Y, Ren ZG, Sun HC, Tang ZY (2010) Activation of beta-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis. Clin Cancer Res 16:2740–2750PubMedCrossRefGoogle Scholar
- Liu Y, Zhang JB, Qin Y, Wang W, Wie L, Teng Y, Guo L, Zhang B, Lin Z, Liu J, Ren ZG et al (2013a) PROX1 promotes hepatocellular carcinoma metastasis via up-regulating hypoxia-inducible factor 1a expression and protein stability. Hepatology 58:692–705PubMedCrossRefGoogle Scholar
- Liu FY, Deng YL, Li Y, Zeng D, Zhou ZZ, Tian DA, Liu M (2013b) Down-regulated KLF17 expression is associated with tumor invasion and poor prognosis in hepatocellular carcinoma. Med Oncol 30:425PubMedCrossRefGoogle Scholar
- Liu Z, Tu K, Liu Q (2014a) Effects of microRNA-30a on migration, invasion and prognosis of hepatocellular carcinoma. FEBS Lett 588:3089–3097PubMedCrossRefGoogle Scholar
- Liu W, Xu C, Wan H, Liu C, Wen C, Lu H, Wan F (2014b) MicroRNA-206 overexpression promotes apoptosis, induces cell cycle arrest and inhibits the migration of human hepatocellular carcinoma HepG2 cells. Int J Mol Med 34:420–428PubMedPubMedCentralGoogle Scholar
- Liu Y, Ding Y, Huang J, Wang S, Ni W, Guan J, Li Q, Zhang Y, Ding Y, Chen B, Chen B et al (2014c) MiR-141 suppresses the migration and invasion of HCC cells by targeting Tiam1. PLoS One 9:e88393PubMedPubMedCentralCrossRefGoogle Scholar
- Lou E, Fujisawa S, Barlas A, Romin Y, Manova-Todorova K, Moore MA, Subramanian S (2012) Tunnelling nanotubes: a new paradigm for studying intercellular communication and therapeutics in cancer. Commun Integr Biol 5:399–403PubMedPubMedCentralCrossRefGoogle Scholar
- Lu X, Feng X, Man X, Yang G, Tang L, Du D, Zhang F, Yuan H, Huang Q, Zhang Z et al (2009) Aberrant splicing of Hugl-1 is associated with hepatocellular carcinoma progression. Clin Cancer Res 15:3287–3296PubMedCrossRefGoogle Scholar
- Lynch J, Meehan MH, Crean J, Copeland J, Stallings RL, Bray IM (2013) Metastasis suppressor microRNA-335 targets the formin family of actin nucleators. PLoS One 8:e78428PubMedPubMedCentralCrossRefGoogle Scholar
- Ma Y, She XG, Ming YZ, Wan QQ, Ye QF (2015) MicroRNA-144 suppresses tumorigenesis of hepatocellular carcinoma by targeting AKT3. Mol Med Rep 11:1378–1383PubMedGoogle Scholar
- MacGrath SM, Koleske AJ (2012) Cortactin in cell migration and cancer at a glance. J Cell Sci 125:1621–1666PubMedPubMedCentralCrossRefGoogle Scholar
- Maegdefrau U, Bosserhoff AK (2012) BMP activated Smad signaling strongly promotes migration and invasion of hepatocellular carcinoma cells. Exp Mol Pathol 92:74–81PubMedCrossRefGoogle Scholar
- Malz M, Aulmann A, Samarin J, Bissinger M, Longerich T, Schmitt S, Schirmacher P et al (2012) Nuclear accumulation of seven in absentia homologue-2 supports motility and proliferation of liver cancer cells. Int J Cancer 131:2016–2026PubMedCrossRefGoogle Scholar
- Mao TL, Chu JS, Jeng YM, Lai PL, Hsu HC (2001) Expression of mutant nuclear beta-catenin correlates with non-invasive hepatocellular carcinoma, absence of portal vein spread, and good prognosis. J Pathol 193:95–101PubMedCrossRefGoogle Scholar
- Mao X, Li P, Ren Y, Li J, Zhou C, Yang J, Liu P (2015) Cell polarity protein CRB3 is an independent favorable prognostic factor for clear cell renal cell carcinoma. Int J Oncol 46:657–666PubMedGoogle Scholar
- Mariano C, Sasaki H, Brites D, Brito MA (2011) A look at tricellulin and its role in tight junction formation and maintenance. Eur J Cell Biol 90:787–796PubMedCrossRefGoogle Scholar
- Mattila PK, Lappalainen P (2008) Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9:446–454PubMedCrossRefGoogle Scholar
- McCaffrey LM, Macara IG (2011) Epithelial organization, cell polarity and tumorigenesis. Trends Cell Biol 21:727–735PubMedCrossRefGoogle Scholar
- Médina E, Lemmers C, Lane-Guermonprez L, Le Bivic A (2002) Role of the Crumbs complex in the regulation of junction formation in Drosophila and mammalian epithelial cells. Biol Cell 94:305–313PubMedCrossRefGoogle Scholar
- Megger DA, Bracht T, Kohl M, Ahrens M, Naboulsi W, Weber F, Hoffmann AC, Stephan C, Kuhlmann K, Eisneacher M et al (2013) Proteomic differences between hepatocellular carcinoma and nontumorous liver tissue investigated by a combined gel-based and label-free quantitative proteomics study. Mol Cell Proteomics 12:2006–2020PubMedPubMedCentralCrossRefGoogle Scholar
- Mellor H (2010) The role of formins in filopodia formation. Biochim Biophys Acta 1803:191–200PubMedCrossRefGoogle Scholar
- Michael M, Vehlow A, Navarro C, Krause M (2010) C-Abl, lamellipodin, and Ena/VASP proteins cooperate in dorsal ruffling of fibroblasts and axonal morphogenesis. Curr Biol 20:783–791PubMedPubMedCentralCrossRefGoogle Scholar
- Miki H, Takenawa T (2003) Regulation of actin dynamics by WASP family proteins. J Biochem 134:309–313PubMedCrossRefGoogle Scholar
- Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E, Voth GA, Unger VM (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149:137–145PubMedPubMedCentralCrossRefGoogle Scholar
- Mishima A, Suzuki A, Enaka M, Hirose T, Mizuno K, Ohnishi T, Mohri H, Ishigatsubo Y, Ohno S (2002) Over-expression of PAR-3 suppresses contact-mediated inhibition of cell migration in MDCK cells. Genes Cells 7:581–596PubMedCrossRefGoogle Scholar
- Misra A, Rajmohan R, Lim RP, Bhattacharyya S, Thanabalu T (2010) The mammalian verprolin, WIRE induces filopodia independent of N-WASP through IRSp53. Exp Cell Res 316:2810–2824PubMedCrossRefGoogle Scholar
- Morimura S, Suzuki K, Takahashi K (2009) BetaPIX and GIT1 regulates HGF-induced lamellipodia formation and WAVE2 transport. Biochem Biophys Res Commun 382:614–619PubMedCrossRefGoogle Scholar
- Müsch A (2014) The unique polarity phenotype of hepatocytes. Exp Cell Res 328:276–283PubMedPubMedCentralCrossRefGoogle Scholar
- Nakanishi et al. (1999) http://www.ncbi.nlm.nih.gov/pubmed/10763917
- Nance J, Zallen JA (2011) Elaborating polarity: PAR proteins and the cytoskeleton. Development 138:799–809PubMedPubMedCentralCrossRefGoogle Scholar
- Narumiya S, Ishizaki T, Watanabe N (1997) Rho effectors and reorganization of actin cytoskeleton. FEBS Lett 410:68–72PubMedCrossRefGoogle Scholar
- Ng L, Poon RT, Yau S, Chow A, Lam C, Li HS, Yau TC, Law WL, Pang R (2013) Suppression of actopaxin impairs hepatocellular carcinoma metastasis through modulation of cell migration and invasion. Hepatology 58:667–679PubMedCrossRefGoogle Scholar
- Ni F, Zhao H, Cui H, Wu Z, Chen L, Hu Z, Guo C, Liu Y, Chen Z, Wang X, Chen D, Wei H, Wang S (2015) MicroRNA-362-5p promotes tumor growth and metastasis by targeting CYLD in hepatocellular carcinoma. Cancer Lett 356:809–818PubMedCrossRefGoogle Scholar
- Niggli V, Zimmermann A, Keller H (1996) Inhibition of protein kinase C-dependent protein phsophorylation correlates with increased polarity and locomotion in Walker 256 carcinosarcoma cells. Int J Cancer 65:473–478PubMedCrossRefGoogle Scholar
- Nishiyama M, Ozturk M, Frohlich M, Mafune K, Steele G, Wands JR (1990) Expression of human alpha-actinin in human hepatocellular carcinoma. Cancer Res 50:6291–6294PubMedGoogle Scholar
- Nozawa YI, Lin C, Chuang PT (2013) Hedgehog signaling from the primary cilium to the nucleus: an emerging picture of ciliary localization, trafficking and transduction. Curr Opin Genet Dev 23:429–437PubMedPubMedCentralCrossRefGoogle Scholar
- Ogata R (1998) Type IV collagen and laminin enhance the motility, adhesion, and proliferation of hepatoma cells. Kurume Med J 45:11–20PubMedCrossRefGoogle Scholar
- Ohta Y, Suzuki N, Nakamura S, Hartwig JH, Stossel TP (1999) The small GTPase RalA targets filamin to induce filopodia. Proc Natl Acad Sci U S A 96:2122–2128PubMedPubMedCentralCrossRefGoogle Scholar
- Ohta Y, Hartwig JH, Stossel TP (2006) FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodeling. Nat Cell Biol 8:803–814PubMedCrossRefGoogle Scholar
- Ozen E, Gozukizil A, ERdal E, Uren A, Bottaro DP, Tabey N (2012) Heparin inhibits hepatocyte growth factor induced motility and invasion of hepatocellular carcinoma cells through early growth response protein 1. PLoS One 7:e42717PubMedPubMedCentralCrossRefGoogle Scholar
- Paliouras GN, Naujokas MA, Park M (2009) Pak4, a novel Gab1 binding partner, modulates cell migration and invasion by the Met receptor. Mol Cell Biol 29:3018–3032PubMedPubMedCentralCrossRefGoogle Scholar
- Paluch EK, Raz E (2013) The role and regulation of blebs in cell migration. Curr Opin Cell Biol 25:582–590PubMedPubMedCentralCrossRefGoogle Scholar
- Pang EY, Bai AH, To KF, Sy SM, Wong NL, Lai PB, Squire JA, Wong N (2007) Identification of PFTAIRE protein kinase 1, a novel cell division cycle-2 related gene, in the motile phenotype of hepatocellular carcinoma cells. Hepatology 46:436–445PubMedCrossRefGoogle Scholar
- Pang F, Zha R, Zhao Y, Wang Q, Chen D, Zhang Z, Chen T, Yao M, Gu J, He X (2014) MiR-525-3p enhances the migration and invasion of liver cancer cells by downregulating ZNF395. Plosone 9:e90867Google Scholar
- Park CH, Rha SY, Ahn JB, Shin SJ, Kwon WS, Kim TS, An S, Kim NK, Yang WI, Chung HC (2014) PINCH-2 presents functional copy number variation and suppresses migration of colon cancer cells by paracrine activity. Int J Cancer. doi:10.1002/ijc.29273Google Scholar
- Peng H, Talebzadeh-Farrooji M, Osborne MJ, Prokop JW, McDonald PC, Karar J et al (2014) LIMD2 is a small LIM-only protein overexpressed in metastatic lesions that regulates cell motility and tumor progression by directly binding to and activating the integrin-linked kinase. Cancer Res 74:1390–1403PubMedPubMedCentralCrossRefGoogle Scholar
- Perry NA, Ackerman MA, Shriver M, Hu LY, Kontrogianni-Konstantopoulos A (2013) Obscurins: unassuming giants enter the spotlight. IUBMB Life 65:479–486PubMedPubMedCentralCrossRefGoogle Scholar
- Persad S, Dedhar S (2003) The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metastasis Rev 22:375–384PubMedCrossRefGoogle Scholar
- Qazi AS, Sun M, Huang Y, Wei Y, Tang J (2011) Subcellular proteomics: determination of specific location and expression levels of lymphatic metastasis associated proteins in hepatocellular carcinoma by subcellular fractionation. Biomed Pharmacother 65:407–416PubMedCrossRefGoogle Scholar
- Qin J, Wu C (2012) ILK: a pseudokinase in the center stage of cell-matrix adhesion and signaling. Curr Opin Cell Biol 24:607–613PubMedPubMedCentralCrossRefGoogle Scholar
- Qin X, Zhang H, Zhou X, Wang C, Zhang H, Zhang X, Ye L (2007) Proliferation and migration mediated by Dkk-1/Wnt/beta-catenin cascade in a model of hepatocellular carcinoma cells. Transl Res 150:281–294PubMedCrossRefGoogle Scholar
- Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y, Long M, Turner JR (2010) Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21:1200–1213PubMedPubMedCentralCrossRefGoogle Scholar
- Razumilava N, Gradilone SA, Smoot RL, Mertens JC, Bronk SF, Sirica AE, Gores GJ (2014) Noncanonical Hedgehog signaling contributes to chemotaxis in cholangiocarcinoma. J Hepatol 60:599–605PubMedCrossRefGoogle Scholar
- Reglero-Real N, Alvarez-Varela A, Cernuda-Morollon E, Feito J, Marcos-Ramiro B, Fernandez-Martin L, Gomez-Lechon MJ et al (2014) Apicobasal polarity controls lymphocyte adhesion to hepatic epithelial cells. Cell Rep 8:1879–1893PubMedCrossRefGoogle Scholar
- Ren K, Jin H, Bian C, He H, Liu X, Zhang S, Wang Y, Shao RG (2008) MR-1 modulates proliferation and migration of human hepatoma HepG2 cells through myosin light chains-2 (MLC2)/foacl adhesion kinase (FAK)/Akt signaling pathway. J Biol Chem 283:35598–35605PubMedCrossRefGoogle Scholar
- Rogers KW, Schier AF (2011) Morphogen gradients: from generation to interpretation. Annu Rev Cell Dev Biol 27:377–407PubMedCrossRefGoogle Scholar
- Roussos ET, Wang Y, Wyckoff JB, Sellers RS, Wang W, Li J, Pollard JW, Gertler FB (2010) Mena deficiency delays tumor progression and decreases metastasis in polyoma middle-T transgenic mouse mammary tumors. Breast Cancer Res 12:R101PubMedPubMedCentralCrossRefGoogle Scholar
- Roy S, Kornberg TB (2015) Paracrine signaling mediated at cell-cell contacts. Bioessays 37:25–33PubMedCrossRefGoogle Scholar
- Rustom A (2009) Hen or egg?: some thoughts on tunneling nanotubes. Ann N Y Acad Sci 1178:129–136PubMedCrossRefGoogle Scholar
- Salvi A, Sabelli C, Moncini S, Venturin M, Arici B, Riva P, Portolani N, Giulini SM et al (2009) Micro-RNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J 276:2966–2982PubMedCrossRefGoogle Scholar
- Sang H, Li T, Li H, Liu J (2013) Down-regulation of gab1 inhibits cell proliferation and migration in hilar cholangiocarcinoma. PLoS One 8:e81347PubMedPubMedCentralCrossRefGoogle Scholar
- Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M, Desmarais V et al (2008) WASP family members and formin protein coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 180:1245–1260PubMedPubMedCentralCrossRefGoogle Scholar
- Schoedel KE, Tyner VZ, Kim TH, Michalopoulos GK, Mars WM (2003) HGF, MET, and matrix-related proteases in hepatocellular carcinoma, fibrolamellar variant, cirrhotic and normal liver. Mod Pathol 16:14–21PubMedCrossRefGoogle Scholar
- Sepulveda JL, Gkretsi V, Wu C (2005) Assembly and signaling of adhesion complexes. Curr Top Dev Biol 68:183–225PubMedCrossRefGoogle Scholar
- Sheng Y, Li J, Zou C, Wang S, Cao Y, Zhang J, Huang A, Tang H (2014) Downregulation of miR-101-3p by hepatitis B virus promotes proliferation and migration of hepatocellular carcinoma cells by targeting Rab5a. Arch Virol 159:2397–2410PubMedCrossRefGoogle Scholar
- Shi J, Yang L, Wang Z, Wang L, Zhou J, Wang X, Shi G, Ding Z, Ke A, Dai Z, Qiu S, Tang Q, Gao Q, Fan J (2015) CC chemokine receptor-like 1 functions as a tumour suppressor by impairing CCR7-related chemotaxis in hepatocellular carcinoma. J Pathol 235:546–558PubMedCrossRefGoogle Scholar
- Shih YT, Wang MC, Peng HH, Chen TF, Chen L, Chang JY, Chiu JJ (2012) Modulation of chemotactic and pro-inflammatory activities of endothelial progenitor cells by hepatocellular carcinoma. Cell Signal 24:779–793PubMedCrossRefGoogle Scholar
- Shih YT, Wang MC, Zhou J, Peng HH, Lee DY, Chiu JJ (2015) Endothelial progenitors promote hepatocarcinoma intrahepatic metastasis through monocyte chemotactic protein-1 induction of microRNA-21. Gut 64:1132–1147Google Scholar
- Shim JH, Chung YH, Kim JA, Lee D, Kim KM, Lim YS, Lee HC, Lee YS, Yu E et al (2012) Clinical implications of arrest-defective protein 1 expression in hepatocellular carcinoma: a novel predictor of microvascular invasion. Dig Dis 30:603–608PubMedCrossRefGoogle Scholar
- Shriver M, Stroka KM, Vitolo MI, Martin S, Huso DL, Konstantopoulos K, Kontrogianni-Konstantopoulos A (2014) Loss of giant obscurins from breast epithelium promotes epithelial-to-mesenchymal transition, tumorigenicity and metastasis. Oncogene. doi:10.1038/onc.2014.358PubMedCentralGoogle Scholar
- Slim CL, van Ijzendoorn SC, Lazaro-Diéguez F, Müsch A (2014) The special case of hepatocytes: unique tissue architecture calls for a distinct mode of cell division. Bioarchitecture 4:47–52PubMedPubMedCentralCrossRefGoogle Scholar
- Snyder JC, Rochelle LK, Marion S, Lyerly HK, Barak LS, Caron MG (2015) Lgr4 and Lgr5 drive the formation of long actin-rich cytoneme-like membrane protrusions. J Cell Sci 128:1230–1240PubMedPubMedCentralCrossRefGoogle Scholar
- Song Z, Li R, You N, Tao K, Dou K (2010) Loss of heterozygosity of the tumor suppressor gene Tg737 in the side population cells of hepatocellularcarcinomas is associated with poor prognosis. Mol Biol Rep 37:4091–4101PubMedCrossRefGoogle Scholar
- Stanchi F, Grashoff C, Nguemeni Yonga CF, Grall D, Fässler R, Van Obberghen-Schilling E (2009) Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focal-adhesion maturation. J Cell Sci 122:1800–1811PubMedCrossRefGoogle Scholar
- Stiegler AL, Draheim KM, Li X, Chayen NE, Calderwood DA, Boggon TJ (2012) Structural basis for paxillin binding and focal adhesion targeting of b-parvin. J Biol Chem 287:32566–32577PubMedPubMedCentralCrossRefGoogle Scholar
- Suda J, Zhu L, Karvar S (2011) Phosphorylation of radixin regulates cell polarity and Mrp-2 distribution in hepatocytes. Am J Physiol Cell Physiol 300:C416–C424PubMedCrossRefGoogle Scholar
- Suda J, Rockey DC, Karvar S (2014) Phosphorylation dynamics of radixin in hypoxia-induced hepatocyte injury. Am J Physiol Gastrointest Liver Physiol. doi:10.1152/ajpgi.00369.2014PubMedGoogle Scholar
- Sun Z, Han Q, Zhou N, Wang S, Lu S, Bai C, Zhao RC (2013) MicroRNA-9 enhances migration and invasion through KLF17 in hepatocellular carcinoma. Mol Oncol 7:884–894PubMedCrossRefGoogle Scholar
- Sun Z, Meng C, Wang S, Zhou N, Guan M, Bai C, Lu S, Han Q, Zao RC (2014) MicroRNA-1246 enhances migration and invasion through CADM1 in hepatocellular carcinoma. BMC Cancer 14:616PubMedPubMedCentralCrossRefGoogle Scholar
- Sutton A, Friand V, Papy-Garcia D, Dagouassat M, Martin L, Vassy R, Haddad O, Sainte-Catherine O, Kraemer M et al (2007) Glycosaminoglycans and their synthetic mimetics inhibit RANTES-induced migration and invasion of human hepatome cells. Mol Cancer Ther 6:2948–2958PubMedCrossRefGoogle Scholar
- Tan S, Li R, Ding K, Lobie PE, Zhu T (2011) miR-198 inhibits migration and invasion of hepatocellular carcinoma cells by targeting the HGF/c-MET pathway. FEBS Lett 585:2229–2234PubMedCrossRefGoogle Scholar
- Tan VY, Lewis SJ, Adams JC, Martin RM (2013) Association of fascin-1 with mortality, disease progression and metastasis in carcinomas: a systematic review and meta-analysis. BMC Med 11:52PubMedPubMedCentralCrossRefGoogle Scholar
- Tanaka K (2000) Formin family proteins in cytoskeletal control. Biochem Biophys Res Commun 267:479–481PubMedCrossRefGoogle Scholar
- Tao YM, Liu Z, Liu HL (2013) Dickkopf-1 (DKK1) promotes invasion and metastasis of hepatocellular carcinoma. Dig Liver Dis 45:251–257PubMedCrossRefGoogle Scholar
- Thayanithy V, Dickson EL, Steer C, Subramanian S, Lou E (2014) Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl Res 164:359–365PubMedPubMedCentralCrossRefGoogle Scholar
- Tian Q, Liang L, Ding J, Zha R, Shi H, Wang Q, Huang S, Guo W, Ge C, Chen T et al (2012) MicroRNA-550a acts as a pro-metastatic gene and directly targets cytoplasmic polyadenylation element-binding protein 4 in hepatocellular carcinoma. PLoS One 7:e48958PubMedPubMedCentralCrossRefGoogle Scholar
- Tsai MH, Wu CC, Peng PH, Liang Y, Hsiao YC, Chien KY, Chen JT, Lin SJ, Tang RP, Hsieh LL, Yu JS (2012) Identification of secretory gelsolin as a plasma biomarker associated with distant organ metastasis of colorectal cancer. J Mol Med (Berl) 90:187–200CrossRefGoogle Scholar
- Tsao CM, Yan MD, Shih YL, Yu PN, Kuo CC, Lin WC, Li HJ, Lin YW (2012) SOX1 functions as a tumor suppressor by antagonizing the WNT/b-catenin signaling pathway in hepatocellular carcinoma. Hepatology 56:2277–2287PubMedCrossRefGoogle Scholar
- Tu Y, Li F, Goicoechea S, Wu C (1999) The LIM-only protein PINCH directly interacts with integrin-linked kinase and is recruited to integrin-rich sites in spreading cells. Mol Cell Biol 19:2425–2434PubMedPubMedCentralCrossRefGoogle Scholar
- Tyson RA, Zatulovskiy E, Kay RR, Bretschneider T (2014) How blebs and pseudopods cooperate during chemotaxis. Proc Natl Acad Sci U S A 111:11703–11708PubMedPubMedCentralCrossRefGoogle Scholar
- Vaira V, Faversani A, Dohi T, Montorsi M, Augello C, Gatti S, Altieri DC, Bosari S (2012) miR-296 regulation of a cell polarity-cell plasticity module controls tumor progression. Oncogene 31:27–38PubMedCrossRefGoogle Scholar
- Valente S, Rossi R, Resta L, Pasquinelli G (2015) Exploring the human mesenchymal stem cell tubule communication network through electron microscopy. Ultrastruct Pathol 39:88–94Google Scholar
- Van Haastert PJ (2010) Chemotaxis: insights from the extending pseudopod. J Cell Sci 123:3031–3037PubMedCrossRefGoogle Scholar
- Van Haastert PJ, Veltman DM (2007) Chemotaxis: navigating by multiple signaling pathways. Sci STKE 2007:440Google Scholar
- Vannier C, Pesty A, San-Roman MJ, Schmidt AA (2013) The Bin/amphiphysin/Rvs (BAR) domain protein endophilin B2 interacts with plectin and controls perinuclear cytoskeletal architecture. J Biol Chem 288:27619–27637PubMedPubMedCentralCrossRefGoogle Scholar
- Vehlow A, Soong D, Vizcay-Barrena G, Bodo C, Law AL, Perera U, Krause M (2013) Endophilin, lamellipodin, and Mena cooperate to regulate F-actin-dependent EGF-receptor endocytosis. EMBO J 32:2722–2734PubMedPubMedCentralCrossRefGoogle Scholar
- Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006) Role of fascin in filopodial protrusion. J Cell Biol 174:863–875PubMedPubMedCentralCrossRefGoogle Scholar
- Vitriol EA, Wise AL, Berginski ME, Bamburg JR, Zheng JQ (2013) Instantaneous inactivation of cofilin reveals its function of F-actin disassembly in lamellipodia. Mol Biol Cell 24:2238–2247PubMedPubMedCentralCrossRefGoogle Scholar
- Wang X, Gerdes HH (2015) Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ. doi:10.1038/cdd.2014.211Google Scholar
- Wang W, Soroka CJ, Mennone A, Rahner C, Harry K, Pypaert M, Boyer JL (2006) Radixin is required to maintain apical canalicular membrane structure and function in rat hepatocytes. Gastroenterology 131:878–884PubMedPubMedCentralCrossRefGoogle Scholar
- Wang H, Wu K, Sun Y, Li Y, Wu M, Qiao Q, Wie Y, Han ZG, Cai B (2012) STC2 is upregulated in hepatocellular carcinoma and promotes cell proliferation and migration in vitro. BMB Rep 45:629–634PubMedPubMedCentralCrossRefGoogle Scholar
- Wang ZG, Jia MK, Cao H, Bian P, Fang XD (2013a) Knockdown of coronin-1C disrupts Rac1 activation and impairs tumorigenic potential in hepatocellular carcinoma cells. Oncol Rep 29:1066–1072PubMedGoogle Scholar
- Wang R, Zhao N, Li S, Fang JH, Chen MX, Yang J, Jia WH, Yuan Y, Zhuang SM (2013b) MicroRNA-195 suppresses angiogenesis and metastasis of hepatocellular carcinoma by inhibiting the expression of VEGF, VAV2 and CDC42. Hepatology 58:642–653PubMedCrossRefGoogle Scholar
- Wang T, Yanger K, Stanger BZ, Cassio D, Bi E (2014) Cytokinesis defines a spatial landmark for hepatocyte polarization and apical lumen formation. J Cell Sci 127:2483–2492PubMedPubMedCentralCrossRefGoogle Scholar
- Wang G, Sun Y, He Y, Ji C, Hu B, Sun Y (2015) miR-26a promoted by interferon-alpha inhibits hepatocellular carcinoma proliferation and migration by blocking EZH2. Genet Test Mol Biomarkers 19:30–36PubMedCrossRefGoogle Scholar
- Weaver AM (2008) Cortactin in tumor invasiveness. Cancer Lett 265:157–166PubMedPubMedCentralCrossRefGoogle Scholar
- Webb DJ, Brown CM, Horwitz AF (2003) Illuminating adhesion complexes in migrating cells: moving toward a bright future. Curr Opin Cell Biol 15:614–620PubMedCrossRefGoogle Scholar
- Weed SA, Parsons JT (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20:6418–6434PubMedCrossRefGoogle Scholar
- Wehrle-Haller B, Imhof BA (2003) Actin, microtubules and focal adhesion dynamics during cell migration. Int J Biochem Cell Biol 35:39–50PubMedCrossRefGoogle Scholar
- Wells A (ed) (2006) Cell motility in cancer invasion and metastasis. Series: Cancer metastasis – biology and treatment, vol 8. Spinger, LondonGoogle Scholar
- Wong CC, Wong CM, Ko FC, Chan LK, Ching YP, Yam JW, Ng IO (2008) Deleted in liver cancer 1 (DLC1) negatively regulates Rho/ROCK/MLC pathway in hepatocellular carcinoma. PLoS One 3:e2779PubMedPubMedCentralCrossRefGoogle Scholar
- Wong CC, Wong CM, Tung EK, Man K, Ng IO (2009) Rho-kinase 2 is frequently overexpressed in hepatocellular carcinoma and involved in tumor invasion. Hepatology 49:1583–1594PubMedCrossRefGoogle Scholar
- Wong CC, Wong CM, Au SL, Ng IO (2010) RhoGTPases and Rho-effectors in hepatocelular carcinoma metastasis: ROCK N’Rho move it. Liver Int 30:642–656PubMedCrossRefGoogle Scholar
- Wozniak MA, Modzelewska K, Kwong L, Keely PJ (2004) Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692:103–119PubMedCrossRefGoogle Scholar
- Wu C (2004) The PINCH-ILK-parvin complexes: assembly, functions and regulation. Biochim Biophys Acta 1692:55–62PubMedCrossRefGoogle Scholar
- Wu L, Peng CW, Hou JX, Zhang YH, Chen C, Chen LD, Li Y (2010) Coronin-1C is a novel biomarker for hepatocellular carcinoma invasive progression identified by proteomics analysis and clinical validation. J Exp Clin Cancer Res 29:17PubMedPubMedCentralCrossRefGoogle Scholar
- Wu L, Cai C, Wang X, Liu M, Li X, Tang H (2011) MicroRNA-142-3p, a new regulator of RAC1, suppresses the migration and invasion of hepatocellular carcinoma cells. FEBS Lett 585:1322–1330PubMedCrossRefGoogle Scholar
- Xie Q, Liu KD, Hu MY, Zhou K (2001) SF/HGF-c-Met autocrine and paracrine promote metastasis of hepatocellular carcinoma. World J Gastroenterol 7:816–820PubMedPubMedCentralCrossRefGoogle Scholar
- Xie B, Xing R, Chen P, Gou Y, Li S, Xiao J, Dong J (2010) Down-regulation of c-Met expression inhibits human HCC cells growth and invasion by RNA interference. J Surg Res 162:231–238PubMedCrossRefGoogle Scholar
- Xieraili M, Yasen M, Mogushi K, Obulhasim G, Mayinuer A, Aihara A, Tanaka S, Mizushima H, Tanaka H, Arii S (2012) Villin 1 is a predictive factor for the recurrence of high serum alpha-fetoprotein-associated hepatocellular carcinoma after hepatectomy. Cancer Sci 103:1493–1501PubMedCrossRefGoogle Scholar
- Xu C, Liu S, Fu H, Li S, Tie Y, Zhu J, Xing R, Jin Y, Sun Z, Zheng X (2010) MicroRNA-193b regulates proliferation, migration and invasion in human hepatocellular carcinoma cells. Eur J Cancer 46:2828–2836PubMedCrossRefGoogle Scholar
- Yamaguchi H, Condeelis J (2007) Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773:642–652PubMedCrossRefGoogle Scholar
- Yamaji S, Suzuki A, Kanamori H, Mishima W, Yoshimi R, Takasaki H, Takabayashi M et al (2004) Affixin interacts with alpha-actinin and mediates integrin signaling for reorganization of F-actin induced by initial cell-substrate interaction. J Cell Biol 165:539–551PubMedPubMedCentralCrossRefGoogle Scholar
- Yang et al. (2006) http://www.ncbi.nlm.nih.gov/pubmed/17020969
- Yang F, Yin Y, Wang F, Wang Y, Zhang L, Tang Y, Sun S (2010) miR-17-5p promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology 51:1614–1623PubMedCrossRefGoogle Scholar
- Yang Z, Tsuchiya H, Zhang Y, Hartnett ME, Wang L (2013a) MicroRNA-433 inhibits liver cancer cell migration by repressing the protein expression and function of cAMP response element-binding protein. J Biol Chem 288:28893–28899PubMedPubMedCentralCrossRefGoogle Scholar
- Yang X, Liang L, Zhang XF, Jia HL, Qin Y, Zhu XC, Gao XM, Qiao P, Zheng Y et al (2013b) MicroRNA-26a suppresses tumor growth and metastasis of human hepatocellular carcinoma by targeting interleukin-6-Stat3 pathway. Hepatology 58:158–170PubMedCrossRefGoogle Scholar
- Yeh YT, Dai HY, Chien CY (2014) Amplification of MPZL1/PZR gene in hepatocellular carcinoma. Hepatobiliary Surg Nutr 3:87–90PubMedPubMedCentralGoogle Scholar
- Yin HL, Kwiatkowski DJ, Mole JE, Cole FS (1984) Structure and biosynthesis of cytoplasmic and secreted variants of gelsolin. J Biol Chem 259:5271–5276PubMedGoogle Scholar
- Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ (2010) Claudin-1 acts through c-Abl-protein kinase Cdelta (PKCdelta) signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 285:226–233PubMedCrossRefGoogle Scholar
- Yoshioka K, Matsumura F, Akedo H, Itoh K (1998) Small GTP-binding protein Rho stimulates the actomyosin system, leading to invasion of tumor cells. J Biol Chem 273:5146–5154PubMedCrossRefGoogle Scholar
- You N, Liu W, Tang L, Zhong X, Ji R, Zhang N, Wang D, He Y, Dou K, Tao K (2012) Tg737 signaling is required for hypoxia-enhanced invasion and migration in hepatoma cells. J Exp Clin Cancer Res 31:75PubMedPubMedCentralCrossRefGoogle Scholar
- Yu LX, Zhou L, Li M, Li ZW, Wang DS, Zhang SG (2013) The Notch1/cyclooxygenase-2/Snail/E-cadherin pathway is associated with hypoxia-induced hepatocellular carcinoma cell invasion and migration. Oncol Rep 29:362–370PubMedGoogle Scholar
- Yu L, Ding GF, He C, Sun L, Jiang Y, Zhu L (2014) MicroRNA-424 is down-regulated in hepatocellular carcinoma and suppresses cell migration and invasion through c-Myb. PLoS One 9:e91661PubMedPubMedCentralCrossRefGoogle Scholar
- Yuan BZ, Zhou X, Zimonjic DB, Durkin ME, Popescu NC (2003) Amplification and overxpression of the EMS 1 oncogene, a possible prognostic marker, in human hepatocellular carcinoma. J Mol Diagn 5:48–53PubMedPubMedCentralCrossRefGoogle Scholar
- Zhang JL, Qian YB, Zhu LX, Xiong QR (2011) Talin1, a valuable marker for diagnosis and prognostic assessment of human hepatocellular carcinomas. Asian Pac J Cancer Prev 12:3265–3269PubMedGoogle Scholar
- Zhang Y, Takahashi S, Tasaka A, Yoshima T, Ochi H, Chayama K (2013) Involvement of microRNA-224 in cell proliferation, migration, invasion, and anti-apoptosis in hepatocellular carcinoma. J Gastroenterol Hepatol 28:565–575PubMedCrossRefGoogle Scholar
- Zhang N, Duan WD, Leng JJ, Zhou L, Wang X, Xu YZ, Wang XD, Zhang AQ, Dong JH (2015a) STAT3 regulates the migration and invasion of a stem-like subpopulation through microRNA-21 and multiple targets in hepatocellular carcinoma. Oncol Rep 33:1493–1498PubMedGoogle Scholar
- Zhang JG, Shi Y, Hong DF, Ong M, Huang D, Wang CY, Zhao G (2015b) MiR-148b suppresses cell proliferation and invasion in hepatocellular carcinoma by targeting WNT1/β-catenin pathway. Sci Rep 5:8087PubMedPubMedCentralCrossRefGoogle Scholar
- Zhao G, Huang ZM, Kong YL, Wen DQ, Li Y, Ren L, Zhang HY (2013) Cortactin is a sensitive biomarker relative to the poor prognosis of human hepatocellular carcinoma. World J Surg Oncol 11:74PubMedPubMedCentralCrossRefGoogle Scholar
- Zheng F, Liao YJ, Cai MY, Liu YH, Liu TH, Chen SP, Bian XW, Guan XY, Lin MC, Zeng YX, Kung HF, Xie D (2012) The putative tumour suppressor microRNA-124 modulates hepatocellular carcinoma cell aggressiveness by repressing ROCK2 and EZH2. Gut 61:278–289PubMedCrossRefGoogle Scholar
- Zhou Z, Deng H, Yan W, Huang H, Deng Y, Li Y, Tian D (2012) Expression of metadherin/AEG-1 gene is positively related to orientation chemotaxis and adhesion of human hepatocellular carcinoma cell lines of different metastatic potentials. J Huazhong Univ Sci Technol Med Sci 32:353–357PubMedCrossRefGoogle Scholar
- Zhou L, Yang ZX, Song WJ, Li QJ, Yang F, Wang DS, Zhang N, Dou KF (2013) MicroRNA-21 regulates the migration and invasion of a stem-like population in hepatocellular carcinoma. Int J Oncol 43:661–669PubMedGoogle Scholar
- Zhou HC, Fang JH, Luo X, Zhang L, Yang J, Zhang C, Zhuang SM (2014) Downregulation of microRNA-100 enhances the ICMT-Rac1 signaling and promotes metastasis of hepatocellular carcinoma cells. Oncotarget 5:12177–12188PubMedPubMedCentralCrossRefGoogle Scholar
- Zhu K, Dai Z, Pan Q, Wang Z, Yang GH, Yu L, Ding ZB, Shi GM, Ke AW, Yang XR et al (2011) Metadherin promotes hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin Cancer Res 17:7294–7302PubMedCrossRefGoogle Scholar
- Zimmermann J, Falcke M (2014) Formation of transient lamellipodia. PLoS One 9:e87638PubMedPubMedCentralCrossRefGoogle Scholar
- Zimmermann A, Keller HU (1987) Locomotion of tumor cells as an element of invasion and metastasis. Biomed Pharmacother 41:337–344PubMedGoogle Scholar
- Zimmermann A, Keller H (1992) Effects of staurosporine, K252a and other structurally related protein kinase inhibitors on shape and locomotion of Walker carcinosarcoma cells. Br J Cancer 66:1077–1082PubMedPubMedCentralCrossRefGoogle Scholar
- Zimmermann A, Keller H (1993) Shape changes and chemokinesis of Walker carcinosarcoma cells: effects pf protein kinase inhibitors (HA-1004, polymyxin B, sangivamycin and taxoxifen) and an inhibitor of diacylglycerol kinase (R 59022). Anticancer Res 13:347–354PubMedGoogle Scholar
- Zimmermann A, Gehr P, Keller HU (1988) Diacylglycerol-induced shape changes, movements and altered F-actin distribution in human neutrophils. J Cell Sci 90:657–666PubMedGoogle Scholar