Single cell tracking assay reveals an opposite effect of selective small non-peptidic α5β1 or αvβ3/β5 integrin antagonists in U87MG glioma cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 9, 2014, Pages 2978-2987

  Ray, Anne Marie ^a   Schaffner, Florence ^a   Janouskova, Hana ^a   Noulet, Fanny ^a   Rognan, Didier ^a   Lelong Rebel, Isabelle ^a   Choulier, Laurence ^a   Blandin, Anne Florence ^a   Lehmann, Maxime ^a   Martin, Sophie ^a   Kapp, Tobias ^b   Neubauer, Stefanie ^b   Rechenmacher, Florian ^b   Kessler, Horst ^b,c   Dontenwill, Monique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Cell adhesion; Cell migration; Small antagonist; 5 1 integrin; v 3 5 integrin

Indexed keywords

ALPHA5BETA1 INTEGRIN ANTAGONIST; ALPHAVBETA3 INTEGRIN ANTAGONIST; BETA3 INTEGRIN; BETA5 INTEGRIN ANTAGONIST; FIBRONECTIN; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; VITRONECTIN; VITRONECTIN RECEPTOR;

ARTICLE; CELL ADHESION; CELL ASSAY; CELL MIGRATION; CELL TRACKING; CONTROLLED STUDY; GLIOMA CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; WOUND HEALING;

CELL ADHESION; CELL MIGRATION; SMALL ANTAGONIST; Α5Β1 INTEGRIN; ΑVΒ3/Β5 INTEGRIN;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; DRUG SCREENING ASSAYS, ANTITUMOR; GLIOMA; HUMANS; INTEGRIN ALPHA5BETA1; INTEGRIN ALPHAVBETA3; INTEGRIN BETA CHAINS; NEOPLASM PROTEINS;

EID: 84904878299     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.04.024     Document Type: Article

References (46)

1. C.G. Gahmberg, S.C. Fagerholm, S.M. Nurmi, T. Chavakis, S. Marchesan, and M. Gronholm Regulation of integrin activity and signalling Biochim. Biophys. Acta 1790 2009 431 444
2. G.M. D'Abaco, and A.H. Kaye Integrins: molecular determinants of glioma invasion J. Clin. Neurosci. 14 2007 1041 1048 (Pubitemid 47588943)
3. A. Huttenlocher, and A.R. Horwitz Integrins in cell migration Cold Spring Harb. Perspect. Biol. 3 2011 a005074
4. C. Margadant, H.N. Monsuur, J.C. Norman, and A. Sonnenberg Mechanisms of integrin activation and trafficking Curr. Opin. Cell Biol. 23 2011 607 614
5. S.L. Goodman, and M. Picard Integrins as therapeutic targets Trends Pharmacol. Sci. 33 2012 405 412
6. J.S. Desgrosellier, and D.A. Cheresh Integrins in cancer: biological implications and therapeutic opportunities Nat. Rev. 10 2010 9 22
7. H. Janouskova, A. Maglott, D.Y. Leger, C. Bossert, F. Noulet, E. Guerin, D. Guenot, S. Pinel, P. Chastagner, F. Plenat, N. Entz-Werle, J. Lehmann-Che, J. Godet, S. Martin, J. Teisinger, and M. Dontenwill Integrin alpha5beta1 plays a critical role in resistance to temozolomide by interfering with the p53 pathway in high-grade glioma Cancer Res. 72 2012 3463 3470
8. F. Schaffner, A. Ray, and M. Dontenwill Integrin α5β1, the fibronectin receptor, as a pertinent therapeutic target in solid tumors Cancers 5 2013 27 47
9. C. Colin, N. Baeza, C. Bartoli, F. Fina, N. Eudes, I. Nanni, P.M. Martin, L. Ouafik, and D. Figarella-Branger Identification of genes differentially expressed in glioblastoma versus pilocytic astrocytoma using suppression subtractive hybridization Oncogene 25 2006 2818 2826
10. O. Rossier, V. Octeau, J.B. Sibarita, C. Leduc, B. Tessier, D. Nair, V. Gatterdam, O. Destaing, C. Albiges-Rizo, R. Tampe, L. Cognet, D. Choquet, B. Lounis, and G. Giannone Integrins beta1 and beta3 exhibit distinct dynamic nanoscale organizations inside focal adhesions Nat. Cell Biol. 14 2012 1057 1067
11. M.R. Morgan, A. Byron, M.J. Humphries, and M.D. Bass Giving off mixed signals - distinct functions of alpha5beta1 and alphavbeta3 integrins in regulating cell behaviour IUBMB Life 61 2009 731 738
12. E.H. Danen, P. Sonneveld, C. Brakebusch, R. Fassler, and A. Sonnenberg The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis J. Cell Biol. 159 2002 1071 1086 (Pubitemid 36055761)
13. C. Mas-Moruno, F. Rechenmacher, and H. Kessler Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation Anti Cancer Agents Med. Chem. 10 2010 753 768
14. P.T. Caswell, S. Vadrevu, and J.C. Norman Integrins: masters and slaves of endocytic transport Nat. Rev. Mol. Cell Biol. 10 2009 843 853
15. L. Marinelli, A. Meyer, D. Heckmann, A. Lavecchia, E. Novellino, and H. Kessler Ligand binding analysis for human alpha5beta1 integrin: strategies for designing new alpha5beta1 integrin antagonists J. Med. Chem. 48 2005 4204 4207 (Pubitemid 40884920)
16. M. Nagae, S. Re, E. Mihara, T. Nogi, Y. Sugita, and J. Takagi Crystal structure of alpha5beta1 integrin ectodomain: atomic details of the fibronectin receptor J. Cell Biol. 197 2012 131 140
17. D. Heckmann, A. Meyer, L. Marinelli, G. Zahn, R. Stragies, and H. Kessler Probing integrin selectivity: rational design of highly active and selective ligands for the alpha5beta1 and alphavbeta3 integrin receptor Angew. Chem. Int. Ed. 46 2007 3571 3574 (Pubitemid 46973460)
18. D. Heckmann, A. Meyer, B. Laufer, G. Zahn, R. Stragies, and H. Kessler Rational design of highly active and selective ligands for the alpha5beta1 integrin receptor Chembiochem 9 2008 1397 1407
19. D. Heckmann, and H. Kessler Design and chemical synthesis of integrin ligands Methods Enzymol. 426 2007 463 503
20. F. Rechenmacher, S. Neubauer, J. Polleux, C. Mas-Moruno, M. De Simone, E.A. Cavalcanti-Adam, J.P. Spatz, R. Fassler, and H. Kessler Functionalizing alphavbeta3- or alpha5beta1-selective integrin antagonists for surface coating: a method to discriminate integrin subtypes in vitro Angew. Chem. Int. Ed. 52 2013 1572 1575
21. A.O. Frank, E. Otto, C. Mas-Moruno, H.B. Schiller, L. Marinelli, S. Cosconati, A. Bochen, D. Vossmeyer, G. Zahn, R. Stragies, E. Novellino, and H. Kessler Conformational control of integrin-subtype selectivity in isoDGR peptide motifs: a biological switch Angew. Chem. Int. Ed. 49 2010 9278 9281
22. F. Rechenmacher, S. Neubauer, C. Mas-Moruno, P.M. Dorfner, J. Polleux, J. Guasch, B. Conings, H.G. Boyen, A. Bochen, T.R. Sobahi, R. Burgkart, J.P. Spatz, R. Fassler, and H. Kessler A molecular toolkit for the functionalization of titanium-based biomaterials that selectively control integrin-mediated cell adhesion Chemistry 19 2013 9218 9223 (Weinheim an der Bergstrasse, Germany)
23. M. Lehmann, C. Rabenandrasana, R. Tamura, J.C. Lissitzky, V. Quaranta, J. Pichon, and J. Marvaldi 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
24. D. Cox, M. Brennan, and N. Moran Integrins as therapeutic targets: lessons and opportunities Nat. Rev. Drug Discov. 9 2010 804 820
25. P. Friedl, J. Locker, E. Sahai, and J.E. Segall Classifying collective cancer cell invasion Nat. Cell Biol. 14 2012 777 783
26. E. Camand, F. Peglion, N. Osmani, M. Sanson, and S. Etienne-Manneville N-cadherin expression level modulates integrin-mediated polarity and strongly impacts on the speed and directionality of glial cell migration J. Cell Sci. 125 2012 844 857
27. M. Reffay, M.C. Parrini, O. Cochet-Escartin, B. Ladoux, A. Buguin, S. Coscoy, F. Amblard, J. Camonis, and P. Silberzan Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells Nat. Cell Biol. 16 2014 217 223
28. A.P. Mould, Analyzing integrin-dependent adhesion, Current protocols in cell biology/editorial board, Juan S. Bonifacino... [et al.], Chapter 9 (2011) Unit 9 4.
29. R. Stragies, F. Osterkamp, G. Zischinsky, D. Vossmeyer, H. Kalkhof, U. Reimer, and G. Zahn Design and synthesis of a new class of selective integrin alpha5beta1 antagonists J. Med. Chem. 50 2007 3786 3794 (Pubitemid 47292042)
30. A. Tolomelli, L. Gentilucci, E. Mosconi, A. Viola, S.D. Dattoli, M. Baiula, S. Spampinato, L. Belvisi, and M. Civera Development of isoxazoline-containing peptidomimetics as dual alphavbeta3 and alpha5beta1 integrin ligands Chem. Med. Chem. 6 2011 2264 2272
31. B. Delouvrie, K. Al-Kadhimi, J.C. Arnould, S.T. Barry, D.A. Cross, M. Didelot, P.R. Gavine, H. Germain, C.S. Harris, A.M. Hughes, D.A. Jude, J. Kendrew, C. Lambert-van der Brempt, J.J. Lohmann, M. Menard, A.A. Mortlock, M. Pass, C. Rooney, M. Vautier, J.L. Vincent, and N. Warin Structure-activity relationship of a series of non peptidic RGD integrin antagonists targeting alpha5beta1: part 1 Bioorg. Med. Chem. Lett. 22 2012 4111 4116
32. B. Delouvrie, K. Al-Kadhimi, J.C. Arnould, S.T. Barry, D.A. Cross, M. Didelot, P.R. Gavine, H. Germain, C.S. Harris, A.M. Hughes, D.A. Jude, J. Kendrew, C. Lambert-van der Brempt, J.J. Lohmann, M. Menard, A.A. Mortlock, M. Pass, C. Rooney, M. Vautier, J.L. Vincent, and N. Warin Structure-activity relationship of a series of non peptidic RGD integrin antagonists targeting alpha5beta1: part 2 Bioorg. Med. Chem. Lett. 22 2012 4117 4121
33. A.P. Mould, J.A. Askari, S. Aota, K.M. Yamada, A. Irie, Y. Takada, H.J. Mardon, and M.J. Humphries Defining the topology of integrin alpha5beta1-fibronectin interactions using inhibitory anti-alpha5 and anti-beta1 monoclonal antibodies. Evidence that the synergy sequence of fibronectin is recognized by the amino-terminal repeats of the alpha5 subunit J. Biol. Chem. 272 1997 17283 17292 (Pubitemid 27311152)
34. A.M. Gonzalez, J. Claiborne, and J.C. Jones Integrin cross-talk in endothelial cells is regulated by protein kinase A and protein phosphatase 1 J. Biol. Chem. 283 2008 31849 31860
35. J.S. Bauer, C.L. Schreiner, F.G. Giancotti, E. Ruoslahti, and R.L. Juliano Motility of fibronectin receptor-deficient cells on fibronectin and vitronectin: collaborative interactions among integrins J. Cell Biol. 116 1992 477 487
36. P. Roca-Cusachs, N.C. Gauthier, A. Del Rio, and M.P. Sheetz Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction Proc. Natl. Acad. Sci. U. S. A. 106 2009 16245 16250
37. A. Stachurska, J. Elbanowski, and H.M. Kowalczynska Role of alpha5beta1 and alphavbeta3 integrins in relation to adhesion and spreading dynamics of prostate cancer cells interacting with fibronectin under in vitro conditions Cell Biol. Int. 36 2012 883 892
38. D.P. White, P.T. Caswell, and J.C. Norman alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration J. Cell Biol. 177 2007 515 525 (Pubitemid 46718279)
39. A.I. Jeanes, P. Wang, P. Moreno-Layseca, N. Paul, J. Cheung, R. Tsang, N. Akhtar, F.M. Foster, K. Brennan, and C.H. Streuli Specific beta-containing integrins exert differential control on proliferation and two-dimensional collective cell migration in mammary epithelial cells J. Biol. Chem. 287 2012 24103 24112
40. C. Margadant, M. Kreft, D.J. de Groot, J.C. Norman, and A. Sonnenberg Distinct roles of talin and kindlin in regulating integrin alpha5beta1 function and trafficking Curr. Biol. 22 2012 1554 1563
41. D.C. Worth, K. Hodivala-Dilke, S.D. Robinson, S.J. King, P.E. Morton, F.B. Gertler, M.J. Humphries, and M. Parsons Alpha v beta3 integrin spatially regulates VASP and RIAM to control adhesion dynamics and migration J. Cell Biol. 189 2010 369 383
42. P.T. Caswell, M. Chan, A.J. Lindsay, M.W. McCaffrey, D. Boettiger, and J.C. Norman Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments J. Cell Biol. 183 2008 143 155
43. J.P. Xiong, T. Stehle, R. Zhang, A. Joachimiak, M. Frech, S.L. Goodman, and M.A. Arnaout Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand Science (New York, N.Y.) 296 2002 151 155 (Pubitemid 34280076)
44. A.P. Mould, E.J. Symonds, P.A. Buckley, J.G. Grossmann, P.A. McEwan, S.J. Barton, J.A. Askari, S.E. Craig, J. Bella, and M.J. Humphries Structure of an integrin-ligand complex deduced from solution x-ray scattering and site-directed mutagenesis J. Biol. Chem. 278 2003 39993 39999 (Pubitemid 37248564)
45. J. Takagi, K. Strokovich, T.A. Springer, and T. Walz Structure of integrin alpha5beta1 in complex with fibronectin EMBO J. 22 2003 4607 4615 (Pubitemid 37162897)
46. H.B. Schiller, M.R. Hermann, J. Polleux, T. Vignaud, S. Zanivan, C.C. Friedel, Z. Sun, A. Raducanu, K.E. Gottschalk, M. Thery, M. Mann, and R. Fassler Beta1- and alphav-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments Nat. Cell Biol. 15 2013 625 636