Combinatorial effects of doxorubicin and retargeted tissue factor by intratumoral entrapment of doxorubicin and proapoptotic increase of tumor vascular infarction

Oncotarget

Volumn 7, Issue 50, 2016, Pages 82458-82472

  Stucke Ring, Janine ^a   Ronnacker, Julian ^a   Brand, Caroline ^a   Höltke, Carsten ^a   Schliemann, Christoph ^a   Kessler, Torsten ^a   Schmidt, Lars Henning ^a   Harrach, Saliha ^a   Mantke, Verena ^a   Hintelmann, Heike ^a   Hartmann, Wolfgang ^b   Wardelmann, Eva ^b   Lenz, Georg ^a   Wünsch, Bernhard ^c   Müller Tidow, Carsten ^d   Mesters, Rolf M ^a   Schwöppe, Christian ^a   Berdel, Wolfgang E ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

Author keywords

Doxorubicin tumor entrapment; Retargeted tissue factor; Vascular infarction; Vascular targeting

Indexed keywords

ANTINEOPLASTIC AGENT; DOXORUBICIN; GLYCYLASPARAGINYLGLYCYLARGINYLALANYLHISTIDYLALANINE; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; THROMBOPLASTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; ASSAY; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG HALF LIFE; ENDOTHELIUM CELL; FACTOR X ASSAY; FEMALE; FIBROSARCOMA; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM PLASMA CONCENTRATION; MELANOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR CELL; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BLOOD CLOTTING; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOLOGY; SKIN TUMOR; TUMOR CELL LINE; TUMOR VOLUME; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOOD COAGULATION; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; FEMALE; FIBROSARCOMA; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MELANOMA; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLSERINES; SKIN NEOPLASMS; THROMBOPLASTIN; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85004072329     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12559     Document Type: Article

References (44)

1. Denekamp J: Endothelial cell proliferation as a novel approach to targeting tumour therapy. Br J Cancer. 1982; 45:136-139.
2. Huang X, Molema G, King S, Watkins L, Edgington TS, Thorpe PE. Tumor infarction in mice by antibody-directed targeting of tissue factor to tumor vasculature. Science. 1997; 275:547-550.
3. Pasqualini R, Koivunen E, Kain R, Lahdenranta J, Sakamoto M, Stryhn A, Ashmun RA, Shapiro LH, Arap W, Ruoshlahti E. Aminopeptidase N is a receptor for tumorhoming peptides and a target for inhibiting angiogenesis. Cancer Res. 2000; 60:722-727.
4. Kessler T, Schwöppe C, Liersch R, Schliemann C, Hintelmann H, Bieker R, Berdel WE, Mesters RM. Generation of fusion proteins for selective occlusion of tumor vessels. Curr Drug Discov Technol. 2008; 5:1-8.
5. Bieker R, Kessler T, Schwöppe C, Padró T, Persigehl T, Bremer C, Dreischalück J, Kolkmeyer A, Heindel W, Mesters RM, Berdel WE: Infarction of tumor vessels by NGR-peptide directed targeting of tissue factor. Experimental results and first-in-man experience. Blood. 2009; 113:5019-5027.
6. Schwöppe C, Kessler T, Persigehl T, Liersch R, Hintelmann H, Dreischalück J, Ring J, Bremer C, Heindel W, Mesters RM, Berdel WE. Tissue-factor fusion proteins induce occlusion of tumor vessels. Thrombosis Res. 2010; 125:S143-S150.
7. Schwöppe C, Zerbst C, Fröhlich M, Schliemann C, Kessler T, Liersch R, Overkamp L, Holtmeier R, Stypmann J, Dreiling A, König S, Höltke C, Lücke M, et al. Anticancer therapy by tumor vessel infarction with polyethylene glycol conjugated tissue factor. J Med Chem. 2013; 56:2337-2347.
8. Persigehl T, Ring J, Bremer C, Heindel W, Holtmeier R, Stypmann J, Claesener M, Hermann S, Schäfers M, Zerbst C, Schliemann C, Mesters RM, Berdel WE, et al. Non-invasive monitoring of tumor-vessel infarction by retargeted truncated tissue factor tTF-NGR using multimodal imaging. Angiogenesis. 2014; 17:235-246.
9. Takimoto CH. Topoisomerase interactive agents. In: Cancer-Principles Practice of Oncology (DeVita VT, Hellman S, Rosenberg SA, eds.) Lippingcott, Philadelphia, 7th edition, 2005; 375-390.
10. Karuktsis KK, Thompson EHZ, Whiles JA, Rosenfeld RJ. Deciphering the fluorescence of daunomycin and doxorubicin. Biophys Chem. 1998; 73:249-263.
11. Dachary-Prigent J, Toti F, Satta N, Pasquet J-M, Uzan A, Freyssinet J-M. Physiopathological significance of catalytic phospholipids in the generation of thrombin. Semin Thromb Hemost. 1996; 22:157-164.
12. Bach R, Gentry R, Nemerson Y: Factor VII binding to tissue factor in reconstituted phospholipid vesicles: induction of cooperativity by phosphatidylserine. Biochemistry. 1986; 25:4007-4020.
13. Blankenberg FG, Katsikis PD, Tait JF, Davis RE, Naumovski L, Ohtsuki K, Kopiwoda S, Abrams MJ, Darkes M, Robbins RC, Maecker HT, Strauss HW. In vivo detection and imaging of phosphatidylserine expression during programmed cell death. Proc Natl Acad Sci USA. 1998; 95:6349-6354.
14. Hu S, Kiesewetter DO, Zhu L, Guo N, Gao H, Liu G, Hida N, Lang L, Niu G, Chen X. Longitudinal PET imaging of doxorubicin-induced cell death with 18F-annexin V. Mol Imaging Biol. 2012; 14:762-770.
15. He J, Luster TA, Thorpe PE. Radiation-enhanced vascular targeting of human lung cancers in mice with a monoclonal antibody that binds anionic phospholipids. Clin Cancer Res. 2007; 13:5211-5218.
16. Bombeli T, Karsan A, Tait JF, Harlan JM. Apoptotic vascular endothelial cells become procoagulant. Blood. 1997; 89:2429-2442.
17. Swystun LL, Shin LYY, Beaudin S, Liaw PC. Chemotherapeutic agents doxorubicin and epirubicin induce procoagulant phenotype on endothelial cells and blood monocytes. J Thromb Haemost. 2009; 7:619-626.
18. Lysov Z, Swyston LL, Kuruvilla S, Arnold A, Liaw PC. Lung cancer chemotherapy agents increase procoagulant activity via protein disulfide isomerase-dependent tssue factor decryption. Blood Coagul Fibrinolysis. 2015; 26:36-45.
19. Brand C, Dencks S, Schmitz G, Mühlmeister M, Stypmann J, Ross R, Hintelmann H, Schliemann C, Müller-Tidow C, Mesters RM, Berdel WE, Schwöppe C. Low-energy ultrasound treatment improves regional tumor vessel infarction by retargeted tissue factor. J Ultrasound Med. 2015; 34:1227-1236.
20. Carmeliet P, Jain RK: Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473:298-307.
21. Faintuch BL, Oliveira EA, Targino RC, Moro AM: Radiolabeled NGR phage display peptide sequence for tumor targeting. Appl Radiation Isotopes. 2014; 86:41-45.
22. Kim D-W, Kim WH, Kim MH, Kim CG: Synthesis and evaluation of novel Tc-99m labeled NGR-containig hexapeptides as tumor imaging agents. J Label Compd Radiopharm. 2015; 58:30-35.
23. Li G, Wang X, Zong S, Wang J, Conti PS, Chen K: MicroPET imaging of CD13 expression using a 64Culabeled dimeric NGR peptide based on sacophagine cage. Mol Pharmaceutics. 2014; 11:3938-3946.
24. Ma W, Li G, Wang J, Yang W, Zhang Y, Conti PS, Chen K. In vivo NIRF imaging-guided delivery of a novel NGRVEGI fusion protein for targeting tumor vasculature. Amino Acids. 2014; 46:2721-2732.
25. Mate G, Kertesz I, Enyedi KN, Mezö G, Angyal J, Vasas N, Kis A, Szabo E, Emri M, Biro T, Galuska L, Trencsenyi G. In vivo imaging of aminopeptidase N (CD13) receptors in experimental renal tumors using the novel radiotracer 68Ga-NOTA-c(NGR). Eur J Pharm Sci. 2015; 69:61-71.
26. Oostendorp M, Douma K, Hackeng TM, Dirksen A, Post MJ, van Zandvoort MAMJ, Backes WH. Quantitative molecular magnetic resonance imaging of tumor angiogenesis using cNGR-labeled paramagnetic quantum dots. Cancer Res. 2008; 68:7676-7683.
27. Shao Y, Liang W, Kang F, Yang W, Ma X, Li G, Zong S, Chen K, Wang J. A direct comparison of tumor angiogenesis with 68Ga-labeled NGR and RGD peptides in HT-1080 tumor xenografts using microPET imaging. Amino Acids. 2014; 46:2355-2364.
28. Shi J, Wang L, Zhang J, Ma R, Gao J, Liu Y, Zhang C, Zhang Z. A tumor-targeting near-infrared laser-triggered drug delivery system based on GO@Ag nanoparticles for chemo-photothermal therapy and x-ray imaging. Biomaterials. 2014; 35:5847-5861.
29. von Wallbrunn A, Waldeck J, Höltke C, Zühlsdorf M, Mesters R, Heindel W, Schäfers M, Bremer C. In vivo optical imaging of CD13/APN-expression in tumor xenografts. J Biomedical Optics. 2008; 13:011007.
30. Zhang J, Lu X, Wan N, Hua Z, Wang Z, Huang H, Yang M, Wang F. 68Ga-DOTA-NGR as a novel molecular probe for APN-positive tumor imaging using MicroPET. Nucl Med Biol. 2014; 41:268-275.
31. Pathuri G, Hedrick AF, Awasthi V, Ihnat MA, Gali H. Evaluation of 99mTc-probestin for imaging APN expressing tumors by SPECT. Bioorg Med Chem Lett. 2013; 23: 5049-5052.
32. Oostendorp M, Douma K, Wagenaar A, Slenter JM, Hackeng TM, van Zandvoort MA, Post MJ, Backes WH. Molecular magnetic resonance imaging of myocardial angiogenesis after acute myocardial infarction. Circulation. 2010; 121:775-783.
33. http://www.proteinatlas.org/ENSG00000166825-ANPEP/tissue
34. Banner DW, D'Arcy A, Chène C, Winkler FK, Guha A, Konigsberg WH, Nemerson Y, Kirchhofer D. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature. 1996; 380:41-46.
35. Dennis MS, Jin H, Dugger D, Yang R, McFarland L, Ogasawara A, Williams S, Cole MJ, Ross S, Schwall R. Imaging tumors with an albumin-binding Fab, a novel tumor-targeting agent. Cancer Res. 2007; 67:254-261.
36. Di Matteo P, Curnis F, Longhi R, Colombo G, Sacchi A, Crippa L, Protti MP, Ponzoni M, Toma S, Corti A. Immunogenic and structural properties of the Asn-Gly-Arg (NGR) tumor neovasculature-homing motif. Mol Immunol. 2008; 43:1509-1518.
37. Corti A, Curnis F, Arap W, Pasqualini R: The neovasculature homing motif NGR. more than meets the eye. Blood. 2008; 112:2628-2635.
38. 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.
39. Brooks PC, Clark RA, Cheresh DA. Requirement of vascular Integrin alpha V beta 3 for angiogenesis. Science. 1994; 264:569-571.
40. Koivunen E, Wang B, Ruoslahti E. Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Biotechnology (N Y). 1995; 13:265-270.
41. Kessler T, Bieker R, Padró T, Schwöppe C, Persigehl T, Bremer C, Kreuter M, Berdel WE, Mesters RM. Inhibition of tumor growth by RGD peptide-directed delivery of truncated tissue factor to the tumor vasculature. Clin Cancer Res. 2005; 11:6317-6324.
42. Liu C, Huang H, Donate F, Dickinson C, Santucci R, El-Sheikh A, Vessella R, Edgington TS. Prostate-specific membrane antigen directed selective thrombotic infarction of tumors. Cancer Res. 2002; 62:5470-5475.
43. Schellenberger EA, Bogdanov A, Petrovsky A, Ntziachristos V, Weissleder R, Josephson L. Optical Imaging of Apoptosis as a Biomarker of Tumor Response to Chemotherapy. Neoplasia. 2003; 5:187-192.
44. Ruf W, Rehemtulla A, Morrissey JH, Edgington TS. Phospholipid-independent and-dependent interactions required for tissue factor receptor and cofactor function. J Biol Chem. 1991; 266:2158-2166, (erratum J Biol Chem 1991; 266:16256).