Development of a chimeric recombinant disintegrin as a cost-effective anti-cancer agent with promising translational potential

Toxicon

Volumn 59, Issue 4, 2012, Pages 472-486

  Minea, Radu ^a,b   Helchowski, Corey ^a,b   Rubino, Barbara ^a,b   Brodmann, Kyle ^a,b   Swenson, Stephen ^a,b   Markland Jr , Francis ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Breast cancer; Engineered bacterial system; Liposomal delivery of recombinant proteins; Recombinant disintegrins; Snake venom disintegrins

Indexed keywords

ANTINEOPLASTIC AGENT; DISINTEGRIN; DISULFIDE; LIPOSOME; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VICROSTATIN;

ACTIN FILAMENT; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIUM CULTURE; BINDING AFFINITY; BINDING KINETICS; BREAST CARCINOMA; CANCER CELL; CANCER INHIBITION; CANCER MODEL; CANCER SURVIVAL; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DRUG ACCUMULATION; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENCY; DRUG TOLERABILITY; ENCAPSULATION; ENDOTHELIUM CELL; ESCHERICHIA COLI; ESCHERICHIA COLI ORIGAMI B; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPOSOMAL DELIVERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; COST-BENEFIT ANALYSIS; DISEASE MODELS, ANIMAL; DISINTEGRINS; DRUG EVALUATION, PRECLINICAL; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENE FUSION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOTOXINS; LIPOSOMES; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE ALIGNMENT;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VIPERIDAE;

EID: 84857045307     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2011.02.020     Document Type: Article

References (61)

1. Albrecht-Buehler G. The phagokinetic tracks of 3T3 cells. Cell 1977, 11:395-404.
2. Baluk P., Hashizume H., McDonald D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 2005, 15:102-111.
3. Barker P.L., Bullens S., Bunting S., Burdick D.J., Chan K.S., Deisher T., Eigenbrot C., Gadek T.R., Gantzos R., Lipari M.T., et al. Cyclic RGD peptide analogues as antiplatelet antithrombotics. J. Med. Chem. 1992, 35:2040-2048.
4. Bissell M.J., Rizki A., Mian I.S. Tissue architecture: the ultimate regulator of breast epithelial function. Curr. Opin. Cell Biol. 2003, 15:753-762.
5. Bowersox J.C., Sorgente N. Chemotaxis of aortic endothelial cells in response to fibronectin. Cancer Res. 1982, 42:2547-2551.
6. Carrington J.C., Dougherty W.G. A viral cleavage site cassette: identification of amino acid sequences required for tobacco etch virus polyprotein processing. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:3391-3395.
7. Contois L., Akalu A., Brooks P.C. Integrins as " functional hubs" in the regulation of pathological angiogenesis. Semin. Cancer Biol 2009.
8. Dechantsreiter M.A., Planker E., Matha B., Lohof E., Holzemann G., Jonczyk A., Goodman S.L., Kessler H. N-methylated cyclic RGD peptides as highly active and selective alpha(V)beta(3) integrin antagonists. J. Med. Chem. 1999, 42:3033-3040.
9. Desgrosellier J.S., Barnes L.A., Shields D.J., Huang M., Lau S.K., Prevost N., Tarin D., Shattil S.J., Cheresh D.A. An integrin alpha(v)beta(3)-c-Src oncogenic unit promotes anchorage-independence and tumor progression. Nat. Med 2009.
10. Ebos J.M., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009, 15:232-239.
11. Ellis L.M., Reardon D.A. Cancer: the nuances of therapy. Nature 2009, 458:290-292.
12. Folkman J. Angiogenesis: an organizing principle for drug discovery?. Nat. Rev. Drug Discov. 2007, 6:273-286.
13. Fujii Y., Okuda D., Fujimoto Z., Horii K., Morita T., Mizuno H. Crystal structure of trimestatin, a disintegrin containing a cell adhesion recognition motif RGD. J. Mol. Biol. 2003, 332:1115-1122.
14. Gold H.K., Yasuda T., Jang I.K., Guerrero J.L., Fallon J.T., Leinbach R.C., Collen D. Animal models for arterial thrombolysis and prevention of reocclusion. Erythrocyte-rich versus platelet-rich thrombus. Circulation 1991, 83:IV26-40.
15. Golubkov V., Hawes D., Markland F.S. Anti-angiogenic activity of contortrostatin, a disintegrin from Agkistrodon contortrix contortrix snake venom. Angiogenesis 2003, 6:213-224.
16. Goodman S.L., Holzemann G., Sulyok G.A., Kessler H. Nanomolar small molecule inhibitors for alphav(beta)6, alphav(beta)5, and alphav(beta)3 integrins. J. Med. Chem. 2002, 45:1045-1051.
17. Gould R.J., Polokoff M.A., Friedman P.A., Huang T.F., Holt J.C., Cook J.J., Niewiarowski S. Disintegrins: a family of integrin inhibitory proteins from viper venoms. Proc. Soc. Exp. Biol. Med. 1990, 195:168-171.
18. Hamano Y., Zeisberg M., Sugimoto H., Lively J.C., Maeshima Y., Yang C., Hynes R.O., Werb Z., Sudhakar A., Kalluri R. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 2003, 3:589-601.
19. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
20. Hariharan S., Gustafson D., Holden S., McConkey D., Davis D., Morrow M., Basche M., Gore L., Zang C., O'Bryant C.L., Baron A., Gallemann D., Colevas D., Eckhardt S.G. Assessment of the biological and pharmacological effects of the alpha nu beta3 and alpha nu beta5 integrin receptor antagonist, cilengitide (EMD 121974), in patients with advanced solid tumors. Ann. Oncol. 2007, 18:1400-1407.
21. Hood J.D., Cheresh D.A. Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2002, 2:91-100.
22. Huang T.F., Yeh C.H., Wu W.B. Viper venom components affecting angiogenesis. Haemostasis 2001, 31:192-206.
23. Ivaska J., Heino J. Interplay between cell adhesion and growth factor receptors: from the plasma membrane to the endosomes. Cell Tissue Res 2009.
24. Jurasz P., Alonso-Escolano D., Radomski M.W. Platelet-cancer interactions: mechanisms and pharmacology of tumour cell-induced platelet aggregation. Br. J. Pharmacol. 2004, 143:819-826.
25. Kang I.C., Kim D.S., Jang Y., Chung K.H. Suppressive mechanism of salmosin, a novel disintegrin in B16 melanoma cell metastasis. Biochem. Biophys. Res. Commun. 2000, 275:169-173.
26. Kim S., Bell K., Mousa S.A., Varner J.A. Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am. J. Pathol. 2000, 156:1345-1362.
27. Kim S., Harris M., Varner J.A. Regulation of integrin alpha vbeta 3-mediated endothelial cell migration and angiogenesis by integrin alpha5beta1 and protein kinase A. J. Biol. Chem. 2000, 275:33920-33928.
28. Kim S.I., Kim K.S., Kim H.S., Kim D.S., Jang Y., Chung K.H., Park Y.S. Inhibitory effect of the salmosin gene transferred by cationic liposomes on the progression of B16BL6 tumors. Cancer Research 2003, 63:6458-6462.
29. LaVallie E.R., DiBlasio E.A., Kovacic S., Grant K.L., Schendel P.F., McCoy J.M. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnol. (N Y) 1993, 11:187-193.
30. Mahabeleshwar G.H., Chen J., Feng W., Somanath P.R., Razorenova O.V., Byzova T.V. Integrin affinity modulation in angiogenesis. Cell Cycle 2008, 7:335-347.
31. Mahabeleshwar G.H., Feng W., Phillips D.R., Byzova T.V. Integrin signaling is critical for pathological angiogenesis. J. Exp. Med. 2006, 203:2495-2507.
32. Marcinkiewicz C., Weinreb P.H., Calvete J.J., Kisiel D.G., Mousa S.A., Tuszynski G.P., Lobb R.R. Obtustatin: a potent selective inhibitor of alpha1beta1 integrin in vitro and angiogenesis in vivo. Cancer Res. 2003, 63:2020-2023.
33. Mas-Moruno C., Rechenmacher F., Kessler H. Cilengitide: The first anti-angiogenic small molecule drug candidate design, Synthesis and clinical Evaluation. Anticancer Agents Med. Chem 2011.
34. McLane M.A., Joerger T., Mahmoud A. Disintegrins in health and disease. Front. Biosci. 2008, 13:6617-6637.
35. McLane M.A., Marcinkiewicz C., Vijay-Kumar S., Wierzbicka-Patynowski I., Niewiarowski S. Viper venom disintegrins and related molecules. Proc. Soc. Exp. Biol. Med. 1998, 219:109-119.
36. McQuade P., Knight L.C., Welch M.J. Evaluation of 64Cu- and 125I-radiolabeled bitistatin as potential agents for targeting alpha v beta 3 integrins in tumor angiogenesis. Bioconjug. Chem. 2004, 15:988-996.
37. Minea R., Swenson S., Costa F., Chen T.C., Markland F.S. Development of a novel recombinant disintegrin, contortrostatin, as an effective anti-tumor and anti-angiogenic agent. Pathophysiol. Haemost. Thromb. 2005, 34:177-183.
38. Mizejewski G.J. Role of integrins in cancer: survey of expression patterns. Proc. Soc. Exp. Biol. Med. 1999, 222:124-138.
39. Moiseeva N., Bau R., Swenson S.D., Markland F.S., Choe J.Y., Liu Z.J., Allaire M. Structure of acostatin, a dimeric disintegrin from Southern copperhead (Agkistrodon contortrix contortrix), at 1.7 A resolution. Acta Crystallogr. D. Biol. Crystallogr. 2008, 64:466-470.
40. Nash G.F., Turner L.F., Scully M.F., Kakkar A.K. Platelets and cancer. Lancet Oncol. 2002, 3:425-430.
41. Nemeth J.A., Nakada M.T., Trikha M., Lang Z., Gordon M.S., Jayson G.C., Corringham R., Prabhakar U., Davis H.M., Beckman R.A. Alpha-v integrins as therapeutic targets in oncology. Cancer Invest. 2007, 25:632-646.
42. Osborne C.K., Hobbs K., Clark G.M. Effect of Estrogens and Antiestrogens on growth of human breast cancer cells in Athymic nude mice. Cancer Res. 1985, 45:584-590.
43. Ouyang C., Huang T.F. Potent platelet aggregation inhibitor from Trimeresurus gramineus snake venom. Biochim. Biophys. Acta 1983, 757:332-341.
44. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., Inoue M., Bergers G., Hanahan D., Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15:220-231.
45. Park S.H., Raines R.T. Fluorescence polarization assay to quantify protein-protein interactions. Methods Mol. Biol. 2004, 261:161-166.
46. Ramos O.H., Kauskot A., Cominetti M.R., Bechyne I., Salla Pontes C.L., Chareyre F., Manent J., Vassy R., Giovannini M., Legrand C., Selistre-de-Araujo H.S., Crepin M., Bonnefoy A. A novel alpha(v)beta (3)-blocking disintegrin containing the RGD motive, DisBa-01, inhibits bFGF-induced angiogenesis and melanoma metastasis. Clin. Exp. Metastasis. 2008, 25:53-64.
47. Reardon D.A., Nabors L.B., Stupp R., Mikkelsen T. Cilengitide: an integrin-targeting arginine-glycine-aspartic acid peptide with promising activity for glioblastoma multiforme. Expert Opin. Investig. Drugs 2008, 17:1225-1235.
48. Reynolds L.E., Wyder L., Lively J.C., Taverna D., Robinson S.D., Huang X., Sheppard D., Hynes R.O., Hodivala-Dilke K.M. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 2002, 8:27-34.
49. Saudek V., Atkinson R.A., Pelton J.T. Three-dimensional structure of echistatin, the smallest active RGD protein. Biochemistry 1991, 30:7369-7372.
50. Schmitmeier S., Markland F.S., Schonthal A.H., Chen T.C. Potent mimicry of fibronectin-induced intracellular signaling in glioma cells by the homodimeric snake venom disintegrin contortrostatin. Neurosurgery 2005, 57:141-153. discussion 141-153.
51. Serini G., Valdembri D., Bussolino F. Integrins and angiogenesis: a sticky business. Exp. Cell Res. 2006, 312:651-658.
52. Shebuski R.J., Ramjit D.R., Sitko G.R., Lumma P.K., Garsky V.M. Prevention of canine coronary artery thrombosis with echistatin, a potent inhibitor of platelet aggregation from the venom of the viper, Echis carinatus. Thromb. Haemost. 1990, 64:576-581.
53. Silva R., D'Amico G., Hodivala-Dilke K.M., Reynolds L.E. Integrins: the keys to unlocking angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1703-1713.
54. Swenson S., Costa F., Minea R., Sherwin R.P., Ernst W., Fujii G., Yang D., Markland F.S. Intravenous liposomal delivery of the snake venom disintegrin contortrostatin limits breast cancer progression. Mol. Cancer Ther. 2004, 3:499-511.
55. Trikha M., De Clerck Y.A., Markland F.S. Contortrostatin, a snake venom disintegrin, inhibits beta 1 integrin-mediated human metastatic melanoma cell adhesion and blocks experimental metastasis. Cancer Res. 1994, 54:4993-4998.
56. Trikha M., Rote W.E., Manley P.J., Lucchesi B.R., Markland F.S. Purification and characterization of platelet aggregation inhibitors from snake venoms. Thromb. Res. 1994, 73:39-52.
57. Tucker G.C. Integrins: molecular targets in cancer therapy. Curr. Oncol. Rep. 2006, 8:96-103.
58. Wierzbicka-Patynowski I., Niewiarowski S., Marcinkiewicz C., Calvete J.J., Marcinkiewicz M.M., McLane M.A. Structural requirements of echistatin for the recognition of alpha(v)beta(3) and alpha(5)beta(1) integrins. J. Biol. Chem. 1999, 274:37809-37814.
59. Zetter B.R. Migration of capillary endothelial cells is stimulated by tumour-derived factors. Nature 1980, 285:41-43.
60. Zhou Q., Nakada M.T., Arnold C., Markland F.S. Contortrostatin, a dimeric disintegrin from Agkistrodon contortrix contortrix, inhibits angiogenesis. Angiogenesis 1999, 3:259-269.
61. Zhou Q., Nakada M.T., Brooks P.C., Swenson S.D., Ritter M.R., Argounova S., Arnold C., Markland F.S. Contortrostatin, a homodimeric disintegrin, binds to integrin alphavbeta5. Biochem. Biophys. Res. Commun. 2000, 267:350-355.