Inhibition of adhesion, migration and of α5β1 integrin in the HCT-116 colorectal cancer cells treated with the ruthenium drug NAMI-A

Journal of Inorganic Biochemistry

Volumn 160, Issue , 2016, Pages 225-235

  Pelillo, Chiara ^a   Mollica, Hilaria ^a   Eble, Johannes A ^b   Grosche, Julius ^b   Herzog, Lea ^b   Codan, Barbara ^c   Sava, Gianni ^a,c   Bergamo, Alberta ^a  

^a Callerio Foundation   (Italy)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Colorectal cancer; Integrins; Metastasis; Ruthenium

Indexed keywords

ANTINEOPLASTIC AGENT; BLOCKING ANTIBODY; FIBRONECTIN; FOCAL ADHESION KINASE; IMIDAZOLIUM IMIDAZOLEDIMETHYLSULFOXIDETETRACHLORORUTHENATE; RUTHENIUM DERIVATIVE; SCLEROPROTEIN; SMALL INTERFERING RNA; TYROSINE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; DIMETHYL SULFOXIDE; FOCAL ADHESION KINASE 1; IMIDAZOLIUM-BIS(IMIDAZOLE)DIMETHYLSULFOXIDEIMIDAZOTETRACHLORORUTHENATE(III); NEUTRALIZING ANTIBODY; ORGANOMETALLIC COMPOUND; PTK2 PROTEIN, HUMAN; RUTHENIUM;

ARTICLE; AUTOPHOSPHORYLATION; BINDING SITE; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; COLORECTAL CANCER; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; HCT116 CELL LINE; IN VITRO STUDY; METASTASIS; METASTASIS INHIBITION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CELL MOTION; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HCT 116 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION;

ANTIBODIES, NEUTRALIZING; ANTINEOPLASTIC AGENTS; CELL ADHESION; CELL MOVEMENT; CELL SURVIVAL; DIMETHYL SULFOXIDE; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMANS; INTEGRIN ALPHA5BETA1; ORGANOMETALLIC COMPOUNDS; PHOSPHORYLATION; RNA, SMALL INTERFERING; RUTHENIUM;

EID: 84959491932     PISSN: 01620134     EISSN: 18733344     Source Type: Journal    
DOI: 10.1016/j.jinorgbio.2016.02.025     Document Type: Article

References (56)

1. G. Sava, I. Capozzi, K. Clerici, R. Gagliardi, E. Alessio, and G. Mestroni Pharmacological control of lung metastases of solid tumours by a novel ruthenium complex Clin. Exp. Metastasis 16 1998 371 379
2. G. Sava, S. Zorzet, C. Turrin, F. Vita, M. Soranzo, G. Zabucchi, M. Cocchietto, A. Bergamo, S. DiGiovine, G. Pezzoni, L. Sartor, and S. Garbisa Dual Action of NAMI-A in inhibition of solid tumor metastasis: selective targeting of metastatic cells and binding to collagen Clin. Cancer Res. 9 2003 1898 1905
3. B. Gava, S. Zorzet, P. Spessotto, M. Cocchietto, and G. Sava Inhibition of B16 melanoma metastases with the ruthenium complex imidazolium trans-imidazoledimethylsulfoxide-tetrachlororuthenate and down-regulation of tumor cell invasion J. Pharmacol. Exp. Ther. 317 2006 284 291
4. D. Wang, and S.J. Lippard Cellular processing of platinum anticancer drugs Nat. Rev. Drug Discov. 4 2005 307 320
5. D. Pluim, R.C. van Waardenburg, J.H. Beijnen, and J.H. Schellens Cytotoxicity of the organic ruthenium anticancer drug NAMI-A is correlated with DNA binding in four different human tumor cell lines Cancer Chemother. Pharmacol. 54 2004 71 78
6. L. Brescacin Modulazione di mediatori determinant per la progression metastatica con il complesso di rutenio NAMI-A Phd thesis 2007 University of Padua
7. S. Zorzet, A. Bergamo, M. Cocchietto, A. Sorc, B. Gava, E. Alessio, E. Iengo, and G. Sava Lack of in vitro cytotoxicity, associated to increased G(2)-M cell fraction and inhibition of matrigel invasion, may predict in vivo-selective antimetastasis activity of ruthenium complexes J. Pharmacol. Exp. Ther. 295 2000 927 933
8. A. Vacca, M. Bruno, A. Boccarelli, M. Coluccia, D. Ribatti, A. Bergamo, S. Garbisa, L. Sartor, and G. Sava Inhibition of endothelial cell functions and of angiogenesis by the metastasis inhibitor NAMI-A Br. J. Cancer 86 2002 993 998
9. S. Pacor, S. Zorzet, M. Cocchietto, M. Bacac, M. Vadori, C. Turrin, B. Gava, A. Castellarin, and G. Sava Intratumoral NAMI-A treatment triggers metastasis reduction, which correlates to CD44 regulation and tumor infiltrating lymphocyte recruitment J. Pharmacol. Exp. Ther. 310 2004 737 744
10. C. Casarsa, M.T. Mischis, and G. Sava TGFbeta1 regulation and collagen-release-independent connective tissue re-modelling by the ruthenium complex NAMI-A in solid tumours J. Inorg. Biochem. 98 2004 1648 1654
11. J.B. Aitken, S. Antony, C.M. Weekley, B. Lai, L. Spiccia, and H.H. Harris Distinct cellular fates for KP1019 and NAMI-A determined by X-ray fluorescence imaging of single cells Metallomics 4 2012 1051 1056
12. F. Frausin, V. Scarcia, M. Cocchietto, A. Furlani, B. Serli, E. Alessio, and G. Sava Free exchange across cells, and echistatin-sensitive membrane target for the metastasis inhibitor NAMI-A (imidazolium trans-imidazole dimethyl sulfoxide tetrachlororuthenate) on KB tumor cells J. Pharmacol. Exp. Ther. 313 2005 227 233
13. M. Groessl, O. Zava, and P.J. Dyson Cellular uptake and subcellular distribution of ruthenium-based metallodrugs under clinical investigation versus cisplatin Metallomics 3 2011 591 599
14. G. Sava, F. Frausin, M. Cocchietto, F. Vita, E. Podda, P. Spessotto, A. Furlani, V. Scarcia, and G. Zabucchi Actin-dependent tumour cell adhesion after short-term exposure to the antimetastasis ruthenium complex NAMI-A Eur. J. Cancer 40 2004 1383 1396
15. A. Bergamo, and G. Sava Ruthenium complexes can target determinants of tumour malignancy Dalton Trans. 13 2007 1267 1272
16. M. Millard, S. Odde, and N. Neamati Integrin Targeted Therapeutics Theranostics 1 2011 154 188
17. K. Legate, S. Wickström, and R. Fässler Genetic and cell biological analysis of integrin outside-in signalling Genes Dev. 23 2009 397 418
18. J. Xiong, H.E. Balcioglu, and E.H. Danen Integrin signaling in control of tumor growth and progression Int. J. Biochem. Cell Biol. 45 2013 1012 1015
19. F. Aoudjit, and K. Vuori Integrin Signaling in cancer cell survival and chemoresistance Chemother. Res. Pract. 2012 2012 283181
20. D. Lane, N. Goncharenko-Khaider, C. Rancourt, and A. Piché Ovarian cancer ascites protects from TRAIL-induced cell death through αvβ5 integrin-mediated focal adhesion kinase and Akt activation Oncogene 29 2010 3519 3531
21. M. Fornaro, J. Plescia, S. Chheang, G. Tallini, Y.M. Zhu, M. King, D.C. Altieri, and R.R. Languino Fibronectin protects prostate cancer cells from tumor necrosis factor-α-induced apoptosis via the AKT/survivin pathway J. Biol. Chem. 278 2003 50402 50411
22. K.H. Shain, T.H. Landowski, and W.S. Dalton Adhesion-mediated intracellular redistribution of c-Fas-associated death domain-like IL-1-converting enzyme-like inhibitory protein-long confers resistance to CD95-induced apoptosis in hematopoietic cancer cell lines J. Immunol. 168 2002 2544 2553
23. D.E. White, and W.J. Muller Multifaceted roles of integrins in breast cancer metastasis J. Mammary Gland Biol. Neoplasia 12 2007 135 142
24. T. Shibue, and R.A. Weinberg Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs Proc. Natl. Acad. Sci. U. S. A. 106 2009 10290 10295
25. H. Janouskova, A.M. Ray, F. Noulet, I. Lelong-Rebel, L. Choulier, F. Schaffner, M. Lehmen, S. Martin, J. Teisinger, and M. Dontenwill Activation of p53 pathway by Nutlin-3a inhibits the expression of the therapeutic target α5 integrin in colon cancer cells Cancer Lett. 336 2013 307 318
26. J. Roman, J.D. Ritzenthaler, and S. Roser-Page α5β1-integrin expression is essential for tumor progression in experimental lung cancer Am. J. Respir. Cell Mol. Biol. 43 2010 684 691
27. K. Sawada, C. Ohyagi-Hara, T. Kimura, and K. Morishige Integrin inhibitors as a therapeutic agent for ovarian cancer J. Oncol. 2012 2012 915140
28. Y. Jia, Z.Z. Zeng, S.M. Markwart, K.F. Rockwood, K.M. Ignatoski, S.P. Ethier, and D.L. Livant Integrin fibronectin receptors in matrix metalloproteinase 1-dependent invasion by breast cancer and mammary epithelial cells Cancer Res. 64 2004 8674 8681
29. F. Schaffner, A.M. Ray, and M. Dontenwill Integrin α5β1, the fibronectin receptor, as a pertinent therapeutic target in solid tumors Cancer 5 2013 27 47
30. P. Khalili, A. Arakelian, G. Chen, M. Plunkett, I. Beck, G.C. Parry, F. Donate, D.E. Shaw, A.P. Mazar, and S.A. Rabbani A non-RGD-based integrin binding peptide (ATN-161) blocks breast cancer growth and metastasis in vivo Mol. Cancer Ther. 5 2006 2271 2280
31. O. Stoeltzing, W. Liu, N. Reinmuth, F. Fan, G.C. Parry, A.A. Parikh, M.F. McCarty, C.D. Bucana, A.P. Mazar, and L.M. Ellis Inhibition of integrin alpha5beta1 function with a small peptide (ATN-161) plus continuous 5-FU infusion reduces colorectal liver metastases and improves survival in mice Int. J. Cancer 104 2003 496 503
32. M.E. Cianfrocca, K.A. Kimmel, J. Gallo, T. Cardoso, M.M. Brown, G. Hudes, N. Lewis, L. Weiner, G.N. Lam, S.C. Brown, D.E. Shaw, A.P. Mazar, and R.B. Cohen Phase 1 trial of the antiangiogenic peptide ATN-161 (Ac-PHSCN-NH(2)), a beta integrin antagonist, in patients with solid tumours Br. J. Cancer 94 2006 1621 1626
33. A.D. Ricart, A.W. Tolcher, G. Liu, K. Holen, G. Schwartz, M. Albertini, G. Weiss, S. Yazji, C. Ng, and G. Wilding Volociximab, a chimeric monoclonal antibody that specifically binds alpha5beta1 integrin: a phase I, pharmacokinetic, and biological correlative study Clin. Cancer Res. 14 2008 7924 7929
34. C. Pelillo, A. Bergamo, H. Mollica, M. Bestagno, and G. Sava Colorectal cancer metastases settle in the hepatic microenvironment through α5β1 J. Cell. Biochem. 116 2015 2385 2396
35. G. Mestroni, E. Alessio, G. Sava, New salts of anionic complexes of Ru(III) as antimetastatic and antineoplastic gents. International Patent PCT C 07F 15/00A61K 31/28, WO 98/00431, (1998).
36. W. Kueng, E. Silber, and U. Eppenberger Quantification of cells cultured on 96-well plates Anal. Biochem. 182 1989 16 19
37. P. Skehan, R. Storeng, D. Scudiero, A. Monks, J. McMahon, D. Vistica, J.T. Warren, H. Bokesch, S. Kenney, and M.R. Boyd New colorimetric cytotoxicity assay for anticancer-drug screening J. Natl. Cancer Inst. 82 1990 1107 1112
38. M.C. Alley, D.A. Scudiero, A. Monks, M.L. Hursey, M.J. Czerwinski, D.L. Fine, B.J. Abbott, J.G. Mayo, R.H. Schoemaker, and M.R. Boyd Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay Cancer Res. 40 1988 589 601
39. B. Codan, G. Del Favero, V. Martinelli, C.S. Long, L. Mestroni, and O. Sbaizero Exploring the elasticity and adhesion behaviour of cardiac fibroblast by atomic force microscopy indentation Mater. Sci. Eng. C 40 2014 427 434
40. R. Limame, A. Wouters, B. Pauwels, E. Fransen, M. Peeters, F. Lardon, O. De Wever, and P. Pauwels Comparative analysis of dynamic cell viability, migration and invasion assessments by novel real-time technology and classic endpoint assays PLoS One 7 2012 e46536
41. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)) method Methods 25 2001 402 408
42. C. Ramakers, J.M. Ruijter, R.H. Deprez, and A.F. Moorman Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data Neurosci. Lett. 339 2003 62 66
43. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding Anal. Biochem. 72 1976 248 254
44. E. Hahn, G. Wick, D. Pencev, and R. Timpl Distribution of basement membrane proteins in normal and fibrotic liver: collagen type IV, laminin, and fibronectin Gut 21 1980 63 71
45. K.R. Cutroneo, S.L. White, J.F. Chiu, and H.P. Ehrlich Tissue fibrosis and carcinogenesis: divergent or successive pathways dictate multiple molecular therapeutic targets for oligo decoy therapies J. Cell. Biochem. 97 2006 1161 1174
46. 4(DMSO)Im], a novel selective antimetastatic agent, on the survival time of mice with p388 leukemia, p388/DDP subline and MCa mammary carcinoma Metal-Based Drugs 2 1995 195 199
47. M.J. Humphries Integrin structure Biochem. Soc. Trans. 28 2000 311 339
48. J.L. Guan, J.E. Trevithick, and R.O. Hynes Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein Cell. Regul. 2 1991 951 964
49. L. Kornberg, H.S. Earp, J.T. Parsons, M. Schaller, and R.L. Juliano Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase J. Biol. Chem. 267 1992 23439 23442
50. Q. Shi, and D. Boettiger a novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397 Mol. Biol. Cell 14 2003 4305 4315
51. K.E. Michael, D.W. Dumbauld, K.L. Burns, S.K. Hanks, and A.J. Garcia Focal adhesion kinase modulates cell adhesion strengthening via integrin activation Mol. Biol. Cell 20 2009 2508 2519
52. J.T. Parsons Focal adhesion kinase: the first ten years J. Cell Sci. 116 2003 1409 1416
53. D.J. Webb, J.T. Parsons, and A.F. Horwitz Adhesion assembly, disassembly and turnover in migrating cells - over and over and over again Nat. Cell Biol. 4 2002 E97 E100
54. S. Fulda, A.M. Gorman, O. Hori, and A. Samali Cellular Stress Responses: Cell Survival and Cell Death Int. J. Cell. Biol. 2010 2010 214074
55. J.M. Rademaker-Lakhai, D. van den Bongard, D. Pluim, J.H. Beijen, and J.H. Schellens A phase I and pharmacological study with imidazolium-trans-DMSO-imidazole-tetrachlororuthenate, a novel ruthenium anticancer agent Clin. Cancer Res. 10 2004 3717 3727
56. S. Leijen, S.A. Burgers, P. Baas, D. Pluim, M. Tibben, E. van Werkhoven, E. Alessio, G. Sava, J.H. Beijen, and J.H. Schellens Phase I/II study with ruthenium compound NAMI-A and gemcitabine in patients with non-small cell lung cancer after first line therapy Investig. New Drugs 33 2015 201 214