Integrin-Specific Control of Focal Adhesion Kinase and RhoA Regulates Membrane Protrusion and Invasion

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Costa, Patricia ^a   Scales, Tim M E ^a   Ivaska, Johanna ^b,c   Parsons, Maddy ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; FIBRONECTIN; FOCAL ADHESION KINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST METASTASIS; CELL CULTURE; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; HUMAN; HUMAN CELL; MEMBRANE PROTRUSION; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ACTINS; ACTOMYOSIN; ANTIGENS, CD29; CARCINOMA; CELL ADHESION; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMAGING, THREE-DIMENSIONAL; INTEGRIN BETA3; NEOPLASM INVASIVENESS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84883606862     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074659     Document Type: Article

References (53)

1. Rathinam R, Alahari SK, (2010) Important role of integrins in the cancer biology. Cancer Metastasis Rev 29: 223-237.
2. Zaidel-Bar R, Geiger B, (2010) The switchable integrin adhesome. Journal of cell science 123: 1385-1388.
3. Ridley AJ, (2011) Life at the leading edge. Cell 145: 1012-1022.
4. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, Rayburn H, Crowley D, et al. (1999) Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 103: 229-238.
5. Fassler R, Meyer M, (1995) Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev 9: 1896-1908.
6. Guo W, Giancotti FG, (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 5: 816-826.
7. White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, et al. (2004) Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 6: 159-170.
8. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139: 891-906.
9. Butcher DT, Alliston T, Weaver VM, (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9: 108-122.
10. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, et al. (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nature cell biology 9: 1392-1400.
11. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, et al. (2008) Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. The Journal of cell biology 183: 143-155.
12. Wolf K, Friedl P, (2009) Mapping proteolytic cancer cell-extracellular matrix interfaces. Clinical & experimental metastasis 26: 289-298.
13. Kappert K, Meyborg H, Baumann B, Furundzija V, Kaufmann J, et al. (2009) Integrin cleavage facilitates cell surface-associated proteolysis required for vascular smooth muscle cell invasion. Int J Biochem Cell Biol 41: 1511-1517.
14. Sakai K, Nakamura T, Suzuki Y, Imizu T, Matsumoto K, (2011) 3-D collagen-dependent cell surface expression of MT1-MMP and MMP-2 activation regardless of integrin beta1 function and matrix stiffness. Biochemical and biophysical research communications 412: 98-103.
15. Morozevich G, Kozlova N, Cheglakov I, Ushakova N, Berman A, (2009) Integrin alpha5beta1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity. Cell Cycle 8: 2219-2225.
16. Sameni M, Dosescu J, Yamada KM, Sloane BF, Cavallo-Medved D, (2008) Functional live-cell imaging demonstrates that beta1-integrin promotes type IV collagen degradation by breast and prostate cancer cells. Mol Imaging 7: 199-213.
17. Takino T, Saeki H, Miyamori H, Kudo T, Sato H, (2007) Inhibition of membrane-type 1 matrix metalloproteinase at cell-matrix adhesions. Cancer research 67: 11621-11629.
18. Brakebusch C, Wennerberg K, Krell HW, Weidle UH, Sallmyr A, et al. (1999) Beta1 integrin promotes but is not essential for metastasis of ras-myc transformed fibroblasts. Oncogene 18: 3852-3861.
19. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, et al. (2002) Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 8: 27-34.
20. Parsons M, Messent AJ, Humphries JD, Deakin NO, Humphries MJ, (2008) Quantification of integrin receptor agonism by fluorescence lifetime imaging. J Cell Sci 121: 265-271.
21. Worth DC, Hodivala-Dilke K, Robinson SD, King SJ, Morton PE, et al. (2010) Alpha v beta3 integrin spatially regulates VASP and RIAM to control adhesion dynamics and migration. The Journal of cell biology 189: 369-383.
22. Lichtner RB, Howlett AR, Lerch M, Xuan JA, Brink J, et al. (1998) Negative cooperativity between alpha 3 beta 1 and alpha 2 beta 1 integrins in human mammary carcinoma MDA MB 231 cells. Exp Cell Res 240: 368-376.
23. Calderwood DA, Tai V, Di Paolo G, De Camilli P, Ginsberg MH, (2004) Competition for talin results in trans-dominant inhibition of integrin activation. J Biol Chem 279: 28889-28895.
24. Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO, (1998) Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. The Journal of cell biology 142: 1357-1369.
25. King SJ, Worth DC, Scales TM, Monypenny J, Jones GE, et al. (2011) beta1 integrins regulate fibroblast chemotaxis through control of N-WASP stability. EMBO J 30: 1705-1718.
26. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, et al. (2011) Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 146: 148-163.
27. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, et al. (2004) TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851.
28. Kalluri R, Zeisberg M, (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401.
29. Nystrom ML, Thomas GJ, Stone M, Mackenzie IC, Hart IR, et al. (2005) Development of a quantitative method to analyse tumour cell invasion in organotypic culture. J Pathol 205: 468-475.
30. Ramsay AG, Keppler MD, Jazayeri M, Thomas GJ, Parsons M, et al. (2007) HS1-associated protein X-1 regulates carcinoma cell migration and invasion via clathrin-mediated endocytosis of integrin alphavbeta6. Cancer research 67: 5275-5284.
31. Starnes TW, Cortesio CL, Huttenlocher A, (2011) Imaging podosome dynamics and matrix degradation. Methods Mol Biol 769: 111-136.
32. Scales TM, Jayo A, Obara B, Holt MR, Hotchin NA,et al. (2012) alpha3beta1 integrins regulate CD151 complex assembly and membrane dynamics in carcinoma cells within 3D environments. Oncogene.
33. Danen EH, van Rheenen J, Franken W, Huveneers S, Sonneveld P, et al. (2005) Integrins control motile strategy through a Rho-cofilin pathway. The Journal of cell biology 169: 515-526.
34. Bradley WD, Hernandez SE, Settleman J, Koleske AJ, (2006) Integrin signaling through Arg activates p190RhoGAP by promoting its binding to p120RasGAP and recruitment to the membrane. Molecular biology of the cell 17: 4827-4836.
35. Huveneers S, Danen EH, (2009) Adhesion signaling- crosstalk between integrins, Src and Rho. Journal of cell science 122: 1059-1069.
36. Narumiya S, Tanji M, Ishizaki T, (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 28: 65-76.
37. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, et al. (2003) Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. The Journal of cell biology 162: 223-232.
38. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, et al. (2008) Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456: 957-961.
39. Yu HG, Nam JO, Miller NL, Tanjoni I, Walsh C, et al. (2011) p190RhoGEF (Rgnef) promotes colon carcinoma tumor progression via interaction with focal adhesion kinase. Cancer research 71: 360-370.
40. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, et al. (2008) PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. The Journal of cell biology 180: 187-203.
41. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, et al. (2008) WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. The Journal of cell biology 180: 1245-1260.
42. Zhao J, Guan JL, (2009) Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 28: 35-49.
43. Zhai J, Lin H, Nie Z, Wu J, Canete-Soler R, et al. (2003) Direct interaction of focal adhesion kinase with p190RhoGEF. J Biol Chem 278: 24865-24873.
44. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, et al. (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282: 14845-14852.
45. Papusheva E, Mello de Queiroz F, Dalous J, Han Y, Esposito A, et al. (2009) Dynamic conformational changes in the FERM domain of FAK are involved in focal-adhesion behavior during cell spreading and motility. Journal of cell science 122: 656-666.
46. Chan KT, Cortesio CL, Huttenlocher A, (2009) FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. The Journal of cell biology 185: 357-370.
47. Stokes JB, Adair SJ, Slack-Davis JK, Walters DM, Tilghman RW, et al. (2011) Inhibition of focal adhesion kinase by PF-562,271 inhibits the growth and metastasis of pancreatic cancer concomitant with altering the tumor microenvironment. Mol Cancer Ther 10: 2135-2145.
48. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
49. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, et al. (2002) High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13: 803-813.
50. Baldassarre M, Pompeo A, Beznoussenko G, Castaldi C, Cortellino S, et al. (2003) Dynamin participates in focal extracellular matrix degradation by invasive cells. Molecular biology of the cell 14: 1074-1084.
51. Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larrain J, et al. (2008) Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. Development 135: 1771-1780.
52. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi JP, Nevo J, et al. (2012) Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 30: 1436-1448.
53. Koskinen K, Vainio PJ, Smith DJ, Pihlavisto M, Yla-Herttuala S, et al. (2004) Granulocyte transmigration through the endothelium is regulated by the oxidase activity of vascular adhesion protein-1 (VAP-1). Blood 103: 3388-3395.