αvβ5/β6 integrin suppression leads to a stimulation of α2β1 dependent cell migration resistant to PI3K/Akt inhibition

Experimental Cell Research

Volumn 315, Issue 11, 2009, Pages 1840-1849

  Defilles, Céline ^a   Lissitzky, Jean Claude ^a   Montero, Marie Pierre ^a   André, Frédéric ^a   Prévot, Charles ^a   Delamarre, Estelle ^a   Marrakchi, Naziha ^b   Luis, José ^a   Rigot, Véronique ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b PASTEUR INSTITUTE OF TUNIS   (Tunisia)

Author keywords

Cell migration; Colon adenocarcinoma; Crosstalk; Integrin signaling; Integrins; PI3K; PKC

Indexed keywords

ALPHAVBETA5 INTEGRIN; ALPHAVBETA6 INTEGRIN; COLLAGEN TYPE 1; FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SMALL INTERFERING RNA; VERY LATE ACTIVATION ANTIGEN 2; INTEGRIN; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE INHIBITOR; TUMOR ANTIGEN; VITRONECTIN RECEPTOR;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE REARRANGEMENT; GENE REPRESSION; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; CELL MOTION; DRUG ANTAGONISM; DRUG EFFECT; FOCAL ADHESION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; CELL MOVEMENT; COLLAGEN TYPE I; FOCAL ADHESIONS; HUMANS; INTEGRIN ALPHA2BETA1; INTEGRINS; ONCOGENE PROTEIN V-AKT; PROTEIN KINASE INHIBITORS; RECEPTORS, VITRONECTIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 65749096676     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.03.014     Document Type: Article

References (47)

1. Chen X., and Gumbiner B.M. Crosstalk between different adhesion molecules. Curr. Opin. Cell Biol. 18 (2006) 572-578
2. Lunt S.J., Chaudary N., and Hill R.P. The tumor microenvironment and metastatic disease. Clin. Exp. Metastasis. (2008)
3. Berrier A.L., and Yamada K.M. Cell-matrix adhesion. J. Cell. Physiol. 213 (2007) 565-573
4. Beer A.J., Niemeyer M., Carlsen J., Sarbia M., Nahrig J., Watzlowik P., Wester H.J., Harbeck N., and Schwaiger M. Patterns of alphavbeta3 expression in primary and metastatic human breast cancer as shown by 18F-Galacto-RGD PET. J. Nucl. Med. 49 (2008) 255-259
5. Hofmann U.B., Westphal J.R., Waas E.T., Becker J.C., Ruiter D.J., and van Muijen G.N. Coexpression of integrin alpha(v)beta3 and matrix metalloproteinase-2 (MMP-2) coincides with MMP-2 activation: correlation with melanoma progression. J. Invest. Dermatol. 115 (2000) 625-632
6. McGary E.C., Lev D.C., and Bar-Eli M. Cellular adhesion pathways and metastatic potential of human melanoma. Cancer Biol. Ther. 1 (2002) 459-465
7. Kikkawa H., Kaihou M., Horaguchi N., Uchida T., Imafuku H., Takiguchi A., Yamazaki Y., Koike C., Kuruto R., Kakiuchi T., Tsukada H., Takada Y., Matsuura N., and Oku N. Role of integrin alpha(v)beta3 in the early phase of liver metastasis: PET and IVM analyses. Clin. Exp. Metastasis. 19 (2002) 717-725
8. Enns A., Korb T., Schluter K., Gassmann P., Spiegel H.U., Senninger N., Mitjans F., and Haier J. Alphavbeta5-integrins mediate early steps of metastasis formation. Eur. J. Cancer 41 (2005) 1065-1072
9. Reynolds T. Updates to staging system reflect advances in imaging, understanding. J. Natl. Cancer Inst. 94 (2002) 1664-1666
10. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69 (1992) 11-25
11. Wu W.S., Wu J.R., and Hu C.T. Signal cross talks for sustained MAPK activation and cell migration: the potential role of reactive oxygen species. Cancer Metastasis. Rev. 27 (2008) 303-314
12. Hehlgans S., Haase M., and Cordes N. Signalling via integrins: implications for cell survival and anticancer strategies. Biochim. Biophys. Acta 1775 (2007) 163-180
13. Kenny L.M., Coombes R.C., Oulie I., Contractor K.B., Miller M., Spinks T.J., McParland B., Cohen P.S., Hui A.M., Palmieri C., Osman S., Glaser M., Turton D., Al-Nahhas A., and Aboagye E.O. Phase I trial of the positron-emitting Arg-Gly-Asp (RGD) peptide radioligand 18F-AH111585 in breast cancer patients. J. Nucl. Med. 49 (2008) 879-886
14. Conway C.L., Walker I., Bell A., Roberts D.J., Brown S.B., and Vernon D.I. In vivo and in vitro characterisation of a protoporphyrin IX-cyclic RGD peptide conjugate for use in photodynamic therapy. Photochem. Photobiol. Sci. 7 (2008) 290-298
15. Rosenow F., Ossig R., Thormeyer D., Gasmann P., Schluter K., Brunner G., Haier J., and Eble J.A. Integrins as antimetastatic targets of RGD-independent snake venom components in liver metastasis [corrected]. Neoplasia 10 (2008) 168-176
16. Brooks P.C., Stromblad S., Sanders L.C., von Schalscha T.L., Aimes R.T., Stetler-Stevenson W.G., Quigley J.P., and Cheresh D.A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85 (1996) 683-693
17. Silletti S., Kessler T., Goldberg J., Boger D.L., and Cheresh D.A. Disruption of matrix metalloproteinase 2 binding to integrin alpha vbeta 3 by an organic molecule inhibits angiogenesis and tumor growth in vivo. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 119-124
18. Canonici A., Steelant W., Rigot V., Khomitch-Baud A., Boutaghou-Cherid H., Bruyneel E., Van Roy F., Garrouste F., Pommier G., and Andre F. Insulin-like growth factor-I receptor, E-cadherin and alpha v integrin form a dynamic complex under the control of alpha-catenin. Int. J. Cancer 122 (2008) 572-582
19. Gimond C., van Der Flier A., van Delft S., Brakebusch C., Kuikman I., Collard J.G., Fassler R., and Sonnenberg A. Induction of cell scattering by expression of beta1 integrins in beta1-deficient epithelial cells requires activation of members of the rho family of GTPases and downregulation of cadherin and catenin function. J. Cell Biol. 147 (1999) 1325-1340
20. Sakamoto Y., Ogita H., Hirota T., Kawakatsu T., Fukuyama T., Yasumi M., Kanzaki N., Ozaki M., and Takai Y. Interaction of integrin alpha(v)beta3 with nectin. Implication in cross-talk between cell-matrix and cell-cell junctions. J. Biol. Chem. 281 (2006) 19631-19644
21. Diaz-Gonzalez F., Forsyth J., Steiner B., and Ginsberg M.H. Trans-dominant inhibition of integrin function. Mol. Biol. Cell 7 (1996) 1939-1951
22. Pijuan-Thompson V., and Gladson C.L. Ligation of integrin alpha5beta1 is required for internalization of vitronectin by integrin alphavbeta3. J. Biol. Chem. 272 (1997) 2736-2743
23. Simon K.O., Nutt E.M., Abraham D.G., Rodan G.A., and Duong L.T. The alphavbeta3 integrin regulates alpha5beta1-mediated cell migration toward fibronectin. J. Biol. Chem. 272 (1997) 29380-29389
24. Blystone S.D., Slater S.E., Williams M.P., Crow M.T., and Brown E.J. A molecular mechanism of integrin crosstalk: alphavbeta3 suppression of calcium/calmodulin-dependent protein kinase II regulates alpha5beta1 function. J. Cell Biol. 145 (1999) 889-897
25. Riederer M.A., Ginsberg M.H., and Steiner B. Blockade of platelet GPIIB-IIIA (integrin alphaII(b)beta(3)) in flowing human blood leads to passivation of prothrombotic surfaces. Thromb. Haemost. 88 (2002) 858-864
26. Perruzzi C.A., de Fougerolles A.R., Koteliansky V.E., Whelan M.C., Westlin W.F., and Senger D.R. Functional overlap and cooperativity among alphav and beta1 integrin subfamilies during skin angiogenesis. J. Invest. Dermatol. 120 (2003) 1100-1109
27. Van de Walle G.R., Schoolmeester A., Iserbyt B.F., Cosemans J.M., Heemskerk J.W., Hoylaerts M.F., Nurden A., Vanhoorelbeke K., and Deckmyn H. Activation of alphaIIbbeta3 is a sufficient but also an imperative prerequisite for activation of alpha2beta1 on platelets. Blood 109 (2007) 595-602
28. Orr A.W., Ginsberg M.H., Shattil S.J., Deckmyn H., and Schwartz M.A. Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 17 (2006) 4686-4697
29. Baciu P.C., Suleiman E.A., Deryugina E.I., and Strongin A.Y. Membrane type-1 matrix metalloproteinase (MT1-MMP) processing of pro-alphav integrin regulates cross-talk between alphavbeta3 and alpha2beta1 integrins in breast carcinoma cells. Exp. Cell Res. 291 (2003) 167-175
30. Blystone S.D., Graham I.L., Lindberg F.P., and Brown E.J. Integrin alpha v beta 3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor alpha 5 beta 1. J. Cell Biol. 127 (1994) 1129-1137
31. Lehmann M., Rabenandrasana C., Tamura R., Lissitzky J.C., Quaranta V., Pichon J., and Marvaldi J. A monoclonal antibody inhibits adhesion to fibronectin and vitronectin of a colon carcinoma cell line and recognizes the integrins alpha v beta 3, alpha v beta 5, and alpha v beta 6. Cancer Res. 54 (1994) 2102-2107
32. Calvete J.J., Fox J.W., Agelan A., Niewiarowski S., and Marcinkiewicz C. The presence of the WGD motif in CC8 heterodimeric disintegrin increases its inhibitory effect on alphaII(b)beta3, alpha(v)beta3, and alpha5beta1 integrins. Biochemistry 41 (2002) 2014-2021
33. Olfa K.Z., Jose L., Salma D., Amine B., Najet S.A., Nicolas A., Maxime L., Raoudha Z., Kamel M., Jacques M., Jean-Marc S., Mohamed el A., and Naziha M. Lebestatin, a disintegrin from Macrovipera venom, inhibits integrin-mediated cell adhesion, migration and angiogenesis. Lab. Invest. 85 (2005) 1507-1516
34. Monferran S., Skuli N., Delmas C., Favre G., Bonnet J., Cohen-Jonathan-Moyal E., and Toulas C. Alphavbeta3 and alphavbeta5 integrins control glioma cell response to ionising radiation through ILK and RhoB. Int. J. Cancer 123 (2008) 357-364
35. Rigot V., Lehmann M., Andre F., Daemi N., Marvaldi J., and Luis J. Integrin ligation and PKC activation are required for migration of colon carcinoma cells. J. Cell. Sci. 111 Pt 20 (1998) 3119-3127
36. Conesa M., Prat A., Mort J.S., Marvaldi J., Lissitzky J.C., and Seidah N.G. Down-regulation of alpha v/beta 3 integrin via misrouting to lysosomes by overexpression of a beta 3Lamp1 fusion protein. Biochem. J. 370 (2003) 703-711
37. Nejjari M., Berthet V., Rigot V., Laforest S., Jacquier M.F., Seidah N.G., Remy L., Bruyneel E., Scoazec J.Y., Marvaldi J., and Luis J. Inhibition of proprotein convertases enhances cell migration and metastases development of human colon carcinoma cells in a rat model. Am. J. Pathol. 164 (2004) 1925-1933
38. Agrez M.V., Bates R.C., Boyd A.W., and Burns G.F. Arg-Gly-Asp-containing peptides expose novel collagen receptors on fibroblasts: implications for wound healing. Cell Regul. 2 (1991) 1035-1044
39. Andre F., Rigot V., Remacle-Bonnet M., Luis J., Pommier G., and Marvaldi J. Protein kinases C-gamma and -delta are involved in insulin-like growth factor I-induced migration of colonic epithelial cells. Gastroenterology 116 (1999) 64-77
40. Pacifici R., Roman J., Kimble R., Civitelli R., Brownfield C.M., and Bizzarri C. Ligand binding to monocyte alpha 5 beta 1 integrin activates the alpha 2 beta 1 receptor via the alpha 5 subunit cytoplasmic domain and protein kinase C. J. Immunol. 153 (1994) 2222-2233
41. Abair T.D., Sundaramoorthy M., Chen D., Heino J., Ivaska J., Hudson B.G., Sanders C.R., Pozzi A., and Zent R. Cross-talk between integrins alpha1beta1 and alpha2beta1 in renal epithelial cells. Exp. Cell Res. (2008)
42. Masson-Gadais B., Pierres A., Benoliel A.M., Bongrand P., and Lissitzky J.C. Integrin (alpha) and beta subunit contribution to the kinetic properties of (alpha)2beta1 collagen receptors on human keratinocytes analyzed under hydrodynamic conditions. J. Cell. Sci. 112 Pt 14 (1999) 2335-2345
43. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 296 (2002) 1655-1657
44. Hay N. The Akt-mTOR tango and its relevance to cancer. Cancer Cell. 8 (2005) 179-183
45. Luo B.H., Carman C.V., and Springer T.A. Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25 (2007) 619-647
46. Servant G., Weiner O.D., Herzmark P., Balla T., Sedat J.W., and Bourne H.R. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287 (2000) 1037-1040
47. Hedjazifar S., Jenndahl L.E., Shimokawa H., and Baeckstrom D. PKB mediates c-erbB2-induced epithelial beta1 integrin conformational inactivation through Rho-independent F-actin rearrangements. Exp. Cell. Res. 307 (2005) 259-275