Anticancer therapy by tumor vessel infarction with polyethylene glycol conjugated retargeted tissue factor

Journal of Medicinal Chemistry

Volumn 56, Issue 6, 2013, Pages 2337-2347

  Schwöppe, Christian ^a   Zerbst, Caroline ^a   Fröhlich, Max ^a   Schliemann, Christoph ^a   Kessler, Torsten ^a   Liersch, Ruediger ^a   Overkamp, Laura ^a   Holtmeier, Richard ^a   Stypmann, Jörg ^a   Dreiling, Alena ^a   König, Simone ^a   Höltke, Carsten ^a   Lücke, Martin ^a   Müller Tidow, Carsten ^a   Mesters, Rolf M ^a   Berdel, Wolfgang E ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; POLYETHYLENE GLYCOL CONJUGATED TRUNCATED TISSUE FACTOR ASPARAGINE GLYCINE ARGININE MOTIF FUSION PROTEIN; TRUNCATED TISSUE FACTOR ASPARAGINE GLYCINE ARGININE MOTIF FUSION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; RANDOMIZED CONTROLLED TRIAL; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD VESSELS; CELL LINE, TUMOR; FEMALE; FIBROSARCOMA; HUMANS; MICE; MODELS, MOLECULAR; OLIGOPEPTIDES; POLYETHYLENE GLYCOLS; PROTEIN CONFORMATION; THROMBOPLASTIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84875709977     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm301669z     Document Type: Article

References (49)

1. Folkman, J. Angiogenesis in cancer, vascular, reumatoid and other disease Nat. Med. 1995, 1, 27-31
2. Ferrara, N.; Alitalo, K. Clinical applications of angiogenic growth factors and their inhibitors Nat. Med. 1999, 5, 1359-1364
3. Chung, A. S.; Lee, J.; Ferrara, N. Targeting the tumour vasculature: Insights from physiological angiogenesis Nat. Rev. Cancer 2010, 10, 505-514
4. Ebos, J. M.; Kerbel, R. S. Antiangiogenic therapy: Impact on invasion, disease progression, and metastasis Nat. Rev. Clin. Oncol. 2011, 8, 210-221 (erratum 8: 316)
5. Tozer, G. M.; Kanthou, C.; Baguley, B. C. Disrupting tumour blood vessels Nat. Rev. Cancer 2005, 5, 423-435
6. Chaplin, D. J.; Dougherty, G. J.; Siemann, D. W. Vascular disrupting agents. In Antiangiogenic Cancer Therapy; Davis, D. W.; Herbst, R; Abbruzzese, J. L., Eds.; CRC Press: Boca Raton, FL, 2008; pp 329-364.
7. Denekamp, J. Endothelial cell proliferation as a novel approach to targeting tumour therapy Br. J. Cancer 1982, 45, 136-139
8. Neri, D.; Bicknell, R. Tumour vascular targeting Nat. Rev. Cancer 2005, 5, 436-446
9. Kessler, T.; Fehrmann, F.; Bieker, R.; Berdel, W. E.; Mesters, R. M. Vascular endothelial growth factor and its receptor as drug targets in hematological malignancies Curr. Drug Targets 2007, 8, 257-268
10. Rettig, W. J.; Garin-Chesa, P.; Healey, J. H.; Su, S. L.; Jaffe, E. A.; Old, L. J. Identification of endosialin, a cell surface glycoprotein of vascular endothelial cells in human cancer Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 10832-10836
11. Kessler, T. A.; Pfeifer, A.; Silletti, S.; Mesters, R. M.; Berdel, W. E.; Verma, I.; Cheresh, D. Matrix metalloproteinase/integrin interactions as target for anti-angiogenic treatment strategies Ann. Hematol. 2002, 81 (Suppl 2) S69-S70
12. Brooks, P. C.; Clark, R. A.; Cheresh, D. A. Requirement of vascular integrin alpha V beta 3 for angiogenesis Science 1994, 264, 569-571
13. Koivunen, E.; Wang, B.; Ruoslahti, E. Phage libraries displaying cyclic peptides with different ring sizes: Ligand specificities of the RGD-directed integrins Biotechnology 1995, 13, 265-270
14. 1 integrins Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 13612-13617
15. Burg, M. A.; Pasqualini, R.; Arap, W.; Ruoslahti, E.; Stallcup, W. B. NG2 proteoglycan-binding peptides target tumor neovasculature Cancer Res. 1999, 59, 2869-2874
16. Arap, W.; Pasqualini, R.; Ruoslahti, E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model Science 1998, 279, 377-380
17. Ellerby, H. M.; Arap, W.; Ellerby, L. M.; Kain, R.; Andrusiak, R.; Rio, G. D.; Krajewski, S.; Lombardo, C. R.; Rao, R.; Ruoslahti, E.; Bredesen, D. E.; Pasqualini, R. Anti-cancer activity of targeted pro-apoptotic peptides Nat. Med. 1999, 5, 1032-1038
18. Hood, J. D.; Bednarski, M.; Frausto, R.; Guccione, S.; Reisfeld, R. A.; Xiang, R.; Cheresh, D. A. Tumor regression by targeted gene delivery to the neovasculature Science 2002, 296, 2404-2407
19. Ran, S.; He, J.; Xianming, H.; Soares, M.; Scothorn, D.; Thorpe, P. E. Antitumor effects of a monoclonal antibody that binds anionic phospholipids on the surface of tumor blood vessels in mice Clin. Cancer Res. 2005, 11, 1551-1562
20. Ruoslahti, E. Targeting tumor vasculature with homing peptides from phage display Semin. Cancer Biol. 2000, 10, 435-442
21. Huang, X.; Molema, G.; King, S.; Watkins, L.; Edgington, T. S.; Thorpe, P. E. Tumor infarction in mice by antibody-directed targeting of tissue factor to tumor vasculature Science 1997, 275, 547-550
22. Morrissey, J. H.; Macik, B. G.; Neuenschwander, P. F.; Comp, P. C. Quantitation of activated factor VII levels in plasma using a tissue factor mutant selectively deficient in promoting factor VII activation Blood 1993, 81, 734-744
23. Nilsson, F.; Kosmehl, H.; Zardi, L.; Neri, D. Targeted delivery of tissue factor to the ED-B domain of fibronectin, a marker of angiogenesis, mediates the infarction of solid tumors in mice Cancer Res. 2001, 61, 711-716
24. Liu, C.; Huang, H.; Donate, F.; Dickinson, C.; Santucci, R.; El-Sheikh, A.; Vessella, R.; Edgington, T. S. Prostate-specific membrane antigen directed selective thrombotic infarction of tumors Cancer Res. 2002, 62, 5470-5475
25. Ran, S.; Gao, B.; Duffy, S.; Watkins, L.; Rote, N.; Thorpe, P. E. Infarction of solid Hodgkin's tumors in mice by antibody-directed targeting of tissue factor to tumor vasculature Cancer Res. 1998, 58, 4646-4653
26. Kessler, T.; Bieker, R.; Padró, T.; Schwöppe, C.; Persigehl, T.; Bremer, C.; Kreuter, M.; Berdel, W. E.; Mesters, R. M. Inhibition of tumor growth by RGD peptide-directed delivery of truncated tissue factor to the tumor vasculature Clin. Cancer Res. 2005, 11, 6317-6324
27. Dienst, A.; Grunow, A.; Unruh, M.; Rabausch, B.; Nör, J. E.; Fries, J. W. U.; Gottstein, C. Specific occlusion of murine and human tumor vasculature by VCAM-1-targeted recombinant fusion proteins J. Natl. Cancer Inst. 2005, 97, 733-747
28. Pasqualini, R.; Koivunen, E.; Kain, R.; Lahdenranta, J.; Sakamoto, M.; Stryhn, A.; Ashmun, R. A.; Shapiro, L. H.; Arap, W.; Ruoshlahti, E. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis Cancer Res. 2000, 60, 722-727
29. Guzman-Rojas, L.; Rangel, R.; Salameh, A.; Edwards, J. K.; Dondossola, E.; Kim, Y.-G.; Saghatelian, A.; Giordano, R. J.; Kolonin, M. G.; Staquicini, F. I.; Koivunen, E.; Sidman, R. L.; Arap, W.; Pasqualini, R. Cooperative effects of aminopeptidase N (CD13) expressed by nonmalignant and cancer cells within the tumor microenvironment Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 1637-1642
30. Curnis, F.; Arrigoni, G.; Sacchi, A.; Fischetti, L.; Arap, W.; Pasqualini, R.; Corti, A. Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells Cancer Res. 2002, 62, 867-874
31. Corti, A.; Curnis, F.; Arap, W.; Pasqualini, R. The neovasculature homing motif NGR: More than meets the eye Blood 2008, 112, 2628-2635
32. Curnis, F.; Longhi, R.; Crippa, L.; Cattaneo, A.; Dondossola, E.; Bachi, A.; Corti, A. Sponaneous formation of L-isoaspartate and gain of function in fibronectin J. Biol. Chem. 2006, 281, 36466-36476
33. Gregory, V.; Zucali, P. A.; Santoro, A.; Ceresoli, G. L.; Citterio, G.; De Pas, T. M.; Zilembo, N.; De Vincenzo, F.; Simonelli, M.; Rossoni, G.; Spreafico, A.; Vigano, M. G.; Fontana, F.; De Braud, F. G.; Bajetta, E.; Caligaris-Cappio, F.; Bruzzi, P.; Lambiase, A.; Bordignon, C. Phase II study of asparagine-glycine-arginine-human tumor necrosis factor α, a selective vascular targeting agent, in previously treated patients with malignant pleural mesothelioma J. Clin. Oncol. 2010, 28, 2604-2611
34. Kessler, T.; Schwöppe, C.; Liersch, R.; Schliemann, C.; Hintelmann, H.; Bieker, R.; Berdel, W. E.; Mesters, R. M. Generation of fusion proteins for selective occlusion of tumor vessels Curr. Drug Discovery Technol. 2008, 5, 1-8
35. Bieker, R.; Kessler, T.; Schwöppe, C.; Padró, T.; Persigehl, T.; Bremer, C.; Dreischalück, J.; Kolkmeyer, A.; Heindel, W.; Mesters, R. M.; Berdel, W. E. Infarction of tumor vessels by NGR-peptide directed targeting of tissue factor. Experimental results and first-in-man experience Blood 2009, 113, 5019-5027
36. Schwöppe, C.; Kessler, T.; Persigehl, T.; Liersch, R.; Hintelmann, H.; Dreischalück, J.; Ring, J.; Bremer, C.; Heindel, W.; Mesters, R. M.; Berdel, W. E. Tissue-factor fusion proteins induce occlusion of tumor vessels Thromb. Res 2010, 125 (Suppl. 2) S143-S150
37. Dreischalück, J.; Schwöppe, C.; Spieker, T.; Kessler, T.; Tiemann, K.; Liersch, R.; Schliemann, C.; Kreuter, M.; Kolkmeyer, A.; Hintelmann, H.; Mesters, R. M.; Berdel, W. E. Vascular infarction by subcutaneous application of tissue factor targeted to tumor vessels with NGR-peptides: Activity and toxicity profile Int. J. Oncol. 2010, 37, 1389-1397
38. Pasut, G.; Veronese, F. M. PEG conjugates in clinical development or use as anticancer agents: An overview Adv. Drug Delivery Rev. 2009, 61, 1177-1188
39. Jevsevar, S.; Kunstelj, M.; Porekar, V. G. PEGylation of therapeutic proteins Biotechnol. J. 2010, 5, 113-128
40. Pasut, G.; Veronese, F. M. State of the art in PEGylation: The great versatility achieved after forty years of research J. Controlled Release 2012, 161, 461-472
41. Dennis, M. S.; Jin, H.; Dugger, D.; Yang, R.; McFarland, L.; Ogasawara, A.; Williams, S.; Cole, M. J.; Ross, S.; Schwall, R. Imaging tumors with an albumin-binding Fab, a novel tumor-targeting agent Cancer Res. 2007, 67, 254-261
42. Banner, D. W.; D'Arcy, A.; Chène, C.; Winkler, F. K.; Guha, A.; Konigsberg, W. H.; Nemerson, Y.; Kirchhofer, D. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor Nature 1996, 380, 41-46
43. Von Maltzahn, G.; Park, J.-H.; Lin, K. Y.; Singh, N.; Schwöppe, C.; Mesters, R.; Berdel, W. E.; Ruoslahti, E.; Sailor, M. J.; Bhatia, S. N. Nanoparticles that communicate in vivo to amplify tumour targeting Nat. Mater. 2011, 10, 545-552
44. Sorina Morar, A.; Schrimsher, J. L.; Chavez, M. D. PEGylation of proteins: A structural approach BioPharm Int. 2006, 19, 1
45. Ruf, W.; Rehemtulla, A.; Morrissey, J. H.; Edgington, T. S. Phospholipid-independent and -dependent interactions required for tissue factor receptor and cofactor function J. Biol. Chem. 1991, 266, 2158-2166
46. Erratum: J. Biol. Chem. 1991, 266, 16256.
47. Hanes, C. S. Studies on plant amylases: The effect of starch concentration upon the velocity of hydrolysis by the amylase of germinated barley Biochem. J. 1932, 26, 1406-1421
48. Lohmaier, S.; Ghanem, A.; Veltmann, C.; Sommer, T.; Bruce, M.; Tiemann, K. In vitro and in vivo studies on continuous echo-contrast application strategies using SonoVue in a newly developed rotating pump setup Ultrasound Med. Biol. 2004, 30, 1145-1151
49. Tiemann, K.; Veltmann, C.; Ghanem, A.; Lohmaier, S.; Bruce, M.; Kuntz-Hehner, S.; Pohl, C.; Ehlgen, A.; Schlosser, T.; Omran, H.; Becher, H. The impact of emission power on the destruction of echo contrast agents and on the origin of tissue harmonic signals using power pulse-inversion imaging Ultrasound Med. Biol. 2001, 27, 1525-1533