Tumor-targeted prodrug ICT2588 demonstrates therapeutic activity against solid tumors and reduced potential for cardiovascular toxicity

Molecular Pharmaceutics

Volumn 11, Issue 4, 2014, Pages 1294-1300

  Gill, Jason H ^a,b   Loadman, Paul M ^a   Shnyder, Steven D ^a   Cooper, Patricia ^a   Atkinson, Jennifer M ^a   Ribeiro Morais, Goreti ^a   Patterson, Laurence H ^a   Falconer, Robert A ^a  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

cancer therapy; drug delivery; matrix metalloproteinase; nanotherapeutic; peptide conjugate; vascular disrupting agent

Indexed keywords

ANTINEOPLASTIC AGENT; AZADEMETHYLCOLCHICINE; COLCHICINE DERIVATIVE; COMBRETASTATIN A4 PHOSPHATE; DOXORUBICIN; FLUOROURACIL; ICT 2588; MATRIX METALLOPROTEINASE 14; PACLITAXEL; PRODRUG; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; COLCHICINE; ICT2588; OLIGOPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CARDIOTOXICITY; CARDIOVASCULAR TOXICITY; COLORECTAL TUMOR; CONTROLLED STUDY; DRUG ACTIVATION; DRUG STABILITY; FEMALE; HUMAN; HUMAN TISSUE; LIVER HOMOGENATE; LUNG HOMOGENATE; LUNG NON SMALL CELL CANCER; MAXIMUM PERMISSIBLE DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN DEGRADATION; SINGLE DRUG DOSE; SOLID TUMOR; TUMOR VOLUME; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CARDIOVASCULAR SYSTEM; DRUG EFFECTS; NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; CARDIOVASCULAR SYSTEM; COLCHICINE; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; NEOPLASMS; OLIGOPEPTIDES; PRODRUGS; VON WILLEBRAND FACTOR;

EID: 84898001922     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp400760b     Document Type: Article

References (43)

1. Collins, I.; Workman, P. New approaches to molecular cancer therapeutics Nat. Chem. Biol. 2006, 2 (12) 689-700
2. Hoelder, S.; Clarke, P. A.; Workman, P. Discovery of small molecule cancer drugs: successes, challenges and opportunities Mol. Oncol. 2012, 6 (2) 155-76
3. Torti, D.; Trusolino, L. Oncogene addiction as a foundational rationale for targeted anti-cancer therapy: promises and perils EMBO J. 2011, 3 (11) 623-36
4. Rebucci, M.; Michiels, C. Molecular aspects of cancer cell resistance to chemotherapy Biochem. Pharmacol. 2013, 85 (9) 1219-26
5. Atkinson, J. M.; Falconer, R. A.; Edwards, D. R.; Pennington, C. J.; Siller, C. S.; Shnyder, S. D.; Bibby, M. C.; Patterson, L. H.; Loadman, P. M.; Gill, J. H. Development of a novel tumor-targeted vascular disrupting agent activated by membrane-type matrix metalloproteinases Cancer Res. 2010, 70 (17) 6902-12
6. Denmeade, S. R.; Isaacs, J. T. Engineering enzymatically activated ″molecular grenades″ for cancer Oncotarget 2012, 3 (7) 666-7
7. Denmeade, S. R.; Mhaka, A. M.; Rosen, D. M.; Brennen, W. N.; Dalrymple, S.; Dach, I.; Olesen, C.; Gurel, B.; Demarzo, A. M.; Wilding, G.; Carducci, M. A.; Dionne, C. A.; Moller, J. V.; Nissen, P.; Christensen, S. B.; Isaacs, J. T. Engineering a prostate-specific membrane antigen-activated tumor endothelial cell prodrug for cancer therapy Sci. Trans. Med. 2012, 4 (140) 140ra86
8. Sotiropoulou, G.; Pampalakis, G. Targeting the kallikrein-related peptidases for drug development Trends Pharmacol. Sci. 2012, 33 (12) 623-34
9. Sounni, N. E.; Noel, A. Targeting the tumor microenvironment for cancer therapy Clin. Chem. 2013, 59 (1) 85-93
10. Weis, S. M.; Cheresh, D. A. Tumor angiogenesis: molecular pathways and therapeutic targets Nat. Med. 2011, 17 (11) 1359-70
11. Kanthou, C.; Tozer, G. M. Microtubule depolymerizing vascular disrupting agents: novel therapeutic agents for oncology and other pathologies Int. J. Exp. Pathol. 2009, 90 (3) 284-94
12. Lippert, J. W., 3rd Vascular disrupting agents Bioorg. Med. Chem. 2007, 15 (2) 605-15
13. Mita, M. M.; Sargsyan, L.; Mita, A. C.; Spear, M. Vascular-disrupting agents in oncology Expert Opin. Invest. Drugs 2013, 22 (3) 317-28
14. Tozer, G. M.; Kanthou, C.; Baguley, B. C. Disrupting tumour blood vessels Nat. Rev. Cancer 2005, 5 (6) 423-35
15. Mason, R. P.; Zhao, D.; Liu, L.; Trawick, M. L.; Pinney, K. G. A perspective on vascular disrupting agents that interact with tubulin: preclinical tumor imaging and biological assessment Integr. Biol. 2011, 3 (4) 375-87
16. Reyes-Aldasoro, C. C.; Wilson, I.; Prise, V. E.; Barber, P. R.; Ameer-Beg, M.; Vojnovic, B.; Cunningham, V. J.; Tozer, G. M. Estimation of apparent tumor vascular permeability from multiphoton fluorescence microscopic images of P22 rat sarcomas in vivo Microcirculation 2008, 15 (1) 65-79
17. Subbiah, I. M.; Lenihan, D. J.; Tsimberidou, A. M. Cardiovascular toxicity profiles of vascular-disrupting agents Oncologist 2011, 16 (8) 1120-30
18. van Heeckeren, W. J.; Bhakta, S.; Ortiz, J.; Duerk, J.; Cooney, M. M.; Dowlati, A.; McCrae, K.; Remick, S. C. Promise of new vascular-disrupting agents balanced with cardiac toxicity: is it time for oncologists to get to know their cardiologists? J. Clin. Oncol. 2006, 24 (10) 1485-8
19. Bosslet, K.; Straub, R.; Blumrich, M.; Czech, J.; Gerken, M.; Sperker, B.; Kroemer, H. K.; Gesson, J. P.; Koch, M.; Monneret, C. Elucidation of the mechanism enabling tumor selective prodrug monotherapy Cancer Res. 1998, 58 (6) 1195-201
20. Cao, Q.; Li, Z. B.; Chen, K.; Wu, Z.; He, L.; Neamati, N.; Chen, X. Evaluation of biodistribution and anti-tumor effect of a dimeric RGD peptide-paclitaxel conjugate in mice with breast cancer Eur. J. Nuc. Med. Mol. Imaging 2008, 35 (8) 1489-98
21. Atkinson, J. M.; Siller, C. S.; Gill, J. H. Tumour endoproteases: the cutting edge of cancer drug delivery? Br. J. Pharmacol. 2008, 153 (7) 1344-52
22. Mahato, R.; Tai, W.; Cheng, K. Prodrugs for improving tumor targetability and efficiency Adv. Drug Delivery Rev. 2011, 63 (8) 659-70
23. Kratz, F.; Warnecke, A. Finding the optimal balance: challenges of improving conventional cancer chemotherapy using suitable combinations with nano-sized drug delivery systems J. Controlled Release 2012, 164 (2) 221-35
24. Rautio, J.; Kumpulainen, H.; Heimbach, T.; Oliyai, R.; Oh, D.; Jarvinen, T.; Savolainen, J. Prodrugs: design and clinical applications Nat. Rev. Drug Discovery 2008, 7 (3) 255-70
25. Devy, L.; Huang, L.; Naa, L.; Yanamandra, N.; Pieters, H.; Frans, N.; Chang, E.; Tao, Q.; Vanhove, M.; Lejeune, A.; van Gool, R.; Sexton, D. J.; Kuang, G.; Rank, D.; Hogan, S.; Pazmany, C.; Ma, Y. L.; Schoonbroodt, S.; Nixon, A. E.; Ladner, R. C.; Hoet, R.; Henderikx, P.; Tenhoor, C.; Rabbani, S. A.; Valentino, M. L.; Wood, C. R.; Dransfield, D. T. Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis Cancer Res. 2009, 69 (4) 1517-26
26. Handsley, M. M.; Edwards, D. R. Metalloproteinases and their inhibitors in tumor angiogenesis Int. J. Cancer 2005, 115 (6) 849-60
27. Kaimal, R.; Aljumaily, R.; Tressel, S. L.; Pradhan, R. V.; Covic, L.; Kuliopulos, A.; Zarwan, C.; Kim, Y. B.; Sharifi, S.; Agarwal, A. Selective blockade of matrix metalloprotease-14 with a monoclonal antibody abrogates invasion, angiogenesis, and tumor growth in ovarian cancer Cancer Res. 2013, 73 (8) 2457-67
28. Sabeh, F.; Ota, I.; Holmbeck, K.; Birkedal-Hansen, H.; Soloway, P.; Balbin, M.; Lopez-Otin, C.; Shapiro, S.; Inada, M.; Krane, S.; Allen, E.; Chung, D.; Weiss, S. J. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP J. Cell Biol. 2004, 167 (4) 769-81
29. Sounni, N. E.; Devy, L.; Hajitou, A.; Frankenne, F.; Munaut, C.; Gilles, C.; Deroanne, C.; Thompson, E. W.; Foidart, J. M.; Noel, A. MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression FASEB J. 2002, 16 (6) 555-64
30. Ueda, J.; Kajita, M.; Suenaga, N.; Fujii, K.; Seiki, M. Sequence-specific silencing of MT1-MMP expression suppresses tumor cell migration and invasion: importance of MT1-MMP as a therapeutic target for invasive tumors Oncogene 2003, 22 (54) 8716-22
31. Kridel, S. J.; Sawai, H.; Ratnikov, B. I.; Chen, E. I.; Li, W.; Godzik, A.; Strongin, A. Y.; Smith, J. W. A unique substrate binding mode discriminates membrane type-1 matrix metalloproteinase from other matrix metalloproteinases J. Biol. Chem. 2002, 277 (26) 23788-93
32. Gill, J. H.; Loadman, P. M.; Falconer, R. A.; Patterson, L. H.; Atkinson, J. M.; Bibby, M. C. MMP Activated Vascular Disrupting Agents, EP20120160556, 2008
33. Ansari, C.; Tikhomirov, G. A.; Hong, S. H.; Falconer, R. A.; Loadman, P. M.; Gill, J. H.; Castaneda, R.; Hazard, F. K.; Tong, L.; Lenkov, O. D.; Felsher, D. W.; Rao, J.; Daldrup-Link, H. E. Development of Novel Tumor-Targeted Theranostic Nanoparticles Activated by Membrane-Type Matrix Metalloproteinases for Combined Cancer Magnetic Resonance Imaging and Therapy Small 2014, 10, 566-75
34. Brott, D.; Gould, S.; Jones, H.; Schofield, J.; Prior, H.; Valentin, J. P.; Bjurstrom, S.; Kenne, K.; Schuppe-Koistinen, I.; Katein, A.; Foster-Brown, L.; Betton, G.; Richardson, R.; Evans, G. Louden, C. Biomarkers of drug-induced vascular injury Toxicol. Appl. Pharmacol. 2005, 207 (2 Suppl) 441-5
35. Constans, J.; Conri, C. Circulating markers of endothelial function in cardiovascular disease Clin. Chim. Acta 2006, 368 (1-2) 33-47
36. Smith, B. W.; Strakova, J.; King, J. L.; Erdman, J. W.; O'Brien, W. D. Validated sandwich ELISA for the quantification of Von Willebrand factor in rabbit plasma Biomarker Insights 2010, 5, 119-27
37. Seemann, I.; te Poele, J. A.; Song, J. Y.; Hoving, S.; Russell, N. S.; Stewart, F. A. Radiation- and anthracycline-induced cardiac toxicity and the influence of ErbB2 blocking agents Breast Cancer Res. Treat. 2013, 141 (3) 385-95
38. Atkinson, J. M.; Pennington, C. J.; Martin, S. W.; Anikin, V. A.; Mearns, A. J.; Loadman, P. M.; Edwards, D. R.; Gill, J. H. Membrane type matrix metalloproteinases (MMPs) show differential expression in non-small cell lung cancer (NSCLC) compared to normal lung: correlation of MMP-14 mRNA expression and proteolytic activity Eur. J. Cancer 2007, 43 (11) 1764-71
39. Nuttall, R. K.; Pennington, C. J.; Taplin, J.; Wheal, A.; Yong, V. W.; Forsyth, P. A.; Edwards, D. R. Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells Mol. Cancer Res. 2003, 1 (5) 333-45
40. Workman, P.; Aboagye, E. O.; Balkwill, F.; Balmain, A.; Bruder, G.; Chaplin, D. J.; Double, J. A.; Everitt, J.; Farningham, D. A.; Glennie, M. J.; Kelland, L. R.; Robinson, V.; Stratford, I. J.; Tozer, G. M.; Watson, S.; Wedge, S. R.; Eccles, S. A. Committee of the National Cancer Research, I. Guidelines for the welfare and use of animals in cancer research Br. J. Cancer 2010, 102 (11) 1555-77
41. Drew, A. F.; Blick, T. J.; Lafleur, M. A.; Tim, E. L.; Robbie, M. J.; Rice, G. E.; Quinn, M. A.; Thompson, E. W. Correlation of tumor- and stromal-derived MT1-MMP expression with progression of human ovarian tumors in SCID mice Gynecol. Oncol. 2004, 95 (3) 437-48
42. Szabova, L.; Chrysovergis, K.; Yamada, S. S.; Holmbeck, K. MT1-MMP is required for efficient tumor dissemination in experimental metastatic disease Oncogene 2008, 27 (23) 3274-81
43. Desai, V. G.; Herman, E. H.; Moland, C. L.; Branham, W. S.; Lewis, S. M.; Davis, K. J.; George, N. I.; Lee, T.; Kerr, S.; Fuscoe, J. C. Development of doxorubicin-induced chronic cardiotoxicity in the B6C3F1 mouse model Toxicol. Appl. Pharmacol. 2013, 266 (1) 109-21