NGR-based strategies for targeting delivery of chemotherapeutics to tumor vasculature

Anti-Cancer Agents in Medicinal Chemistry

Volumn 12, Issue 3, 2012, Pages 239-246

  Zou, Mingming ^a   Zhang, Lei ^a   Xie, Yuanchao ^a   Xu, Wenfang ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Angiogenesis; APN; Chemotherapeutics; isoDGR; NGR peptides; Targeted delivery; v 3 integrin

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; ARGININE; ASPARAGINE; CARBOPLATIN; CHROMOGRANIN A; CISPLATIN; CONTRAST MEDIUM; CYTOKINE; DOCETAXEL; DOXORUBICIN; FLOXURIDINE; FLUOROURACIL; GEMCITABINE; GLYCINE; MELPHALAN; MICROSOMAL AMINOPEPTIDASE; PACLITAXEL; RECOMBINANT ALPHA2A INTERFERON; RECOMBINANT ENDOSTATIN; RECOMBINANT GAMMA INTERFERON; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BINDING AFFINITY; BINDING SITE; BLOOD BRAIN BARRIER; CANCER INHIBITION; CELL ADHESION; CELL PROLIFERATION; CHEMICAL STRUCTURE; CLINICAL EFFECTIVENESS; DEAMINATION; DENDRITIC CELL; DNA PROTEIN COMPLEX; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; HUMAN; HYDROLYSIS; IC 50; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM TOLERATED DOSE; NONHUMAN; PHARMACOKINETICS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN MOTIF; REVIEW; TUMOR LOCALIZATION; TUMOR REGRESSION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; VIRUS PARTICLE;

EID: 84863285169     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/187152012800228751     Document Type: Review

References (59)

1. Luan, Y.; Xu, W., The structure and main functions of aminopeptidase N. Curr Med Chem, 2007, 14 (6), 639-647.
2. Bhagwat, S.V.; Lahdenranta, J.; Giordano, R.; Arap, W.; Pasqualini, R.; Shapiro, L.H., CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood, 2001, 97 (3), 652-659.
3. Arap, W.; Pasqualini, R.; Ruoslahti, E., Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science, 1998, 279 (5349), 377-380.
4. Allen, T.M., Ligand-targeted therapeutics in anticancer therapy. Nat. Rev. Cancer, 2002, 2 (10), 750-763.
5. Zhang, Z.; Hatta, H.; Tanabe, K.; Nishimoto, S., A new class of 5- fluoro-2'-deoxyuridine prodrugs conjugated with a tumor-homing cyclic peptide CNGRC by ester linkers: synthesis, reactivity, and tumor-cell-selective cytotoxicity. Pharm. Res., 2005, 22 (3), 381-389.
6. Ndinguri, M.W.; Solipuram, R.; Gambrell, R.P.; Aggarwal, S.; Hammer, R.P., Peptide targeting of platinum anti-cancer drugs. Bioconjug. Chem., 2009, 20 (10), 1869-1878.
7. 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 proapoptotic peptides. Nat. Med., 1999, 5 (9), 1032-1038.
8. Curnis, F.; Sacchi, A.; Borgna, L.; Magni, F.; Gasparri, A.; Corti, A., Enhancement of tumor necrosis factor alpha antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat. Biotechnol., 2000, 18 (11), 1185-1190.
9. Grifman, M.; Trepel, M.; Speece, P.; Gilbert, L.B.; Arap, W.; Pasqualini, R.; Weitzman, M.D., Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol. Ther., 2001, 3 (6), 964-975.
10. Mizuguchi, H.; Koizumi, N.; Hosono, T.; Utoguchi, N.; Watanabe, Y.; Kay, M.A.; Hayakawa, T., A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther., 2001, 8 (9), 730-735.
11. Chen, Y.; Wu, J.J.; Huang, L., Nanoparticles targeted with NGR motif deliver c-myc siRNA and doxorubicin for anticancer therapy. Mol. Ther., 2010, 18 (4), 828-834.
12. Corti, A.; Ponzoni, M., Tumor vascular targeting with tumor necrosis factor alpha and chemotherapeutic drugs. Ann. N. Y. Acad. Sci., 2004, 1028 (1),104-112.
13. Mukhopadhyay, S.; Barnés, C.M.; Haskel, A.; Short, S.M.; Barnes, K.R.; Lippard, S.J., Conjugated Platinum (IV) Peptide Complexes for Targeting Angiogenic Tumor Vasculature. Bioconjugate. Chem., 2007, 19 (1), 39-49.
14. Zhang, Z.; Hatta, H.; Ito, T.; Nishimoto, S., Synthesis and photochemical properties of photoactivated antitumor prodrugs releasing 5-fluorouracil. Org. Biomol. Chem., 2005, 3 (4), 592-596.
15. Koivunen, E.; Gay, D.A.; Ruoslahti, E., Selection of peptides binding to the alpha 5 beta 1 integrin from phage display library. J. Biol. Chem., 1993, 268 (27), 20205-20210.
16. Koivunen, E.; Wang, B.; Ruoslahti, E., Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Nat. Biotechnol., 1995, 13 (3), 265-270.
17. Colombo, G.; Curnis, F.; De Mori, G.M.; Gasparri, A.; Longoni, C.; Sacchi, A.; Longhi, R.; Corti, A., Structure-activity relationships of linear and cyclic peptides containing the NGR tumor-homing motif. J. Biol. Chem., 2002, 277 (49), 47891-47897.
18. Curnis, F.; Longhi, R.; Crippa, L.; Cattaneo, A.; Dondossola, E.; Bachi, A.; Corti, A., Spontaneous formation of L-isoaspartate and gain of function in fibronectin. J. Biol. Chem., 2006, 281 (47), 36466-36476.
19. Spitaleri, A.; Mari, S.; Curnis, F.; Traversari, C.; Longhi, R.; Bordignon, C.; Corti, A.; Rizzardi, G.P.; Musco, G., Structural basis for the interaction of isoDGR with the RGD-binding site of alphavbeta3 integrin. J. Biol. Chem., 2008, 283 (28), 19757-19768.
20. Tyler-Cross, R.; Schirch, V., Effects of amino acid sequence, buffers, and ionic strength on the rate and mechanism of deamidation of asparagine residues in small peptides. J. Biol. Chem., 1991, 266 (33), 22549-22556.
21. Corti, A.; Curnis, F.; Arap, W.; Pasqualini, R., The neovasculature homing motif NGR: more than meets the eye. Blood, 2008, 112 (7), 2628-2635.
22. Corti, A.; Curnis, F., Isoaspartate-dependent molecular switches for integrin-ligand recognition. J. Cell Sci., 2011, 124 (Pt 4), 515-522.
23. Curnis, F.; Sacchi, A.; Gasparri, A.; Longhi, R.; Bachi, A.; Doglioni, C.; Bordignon, C.; Traversari, C.; Rizzardi, G.P.; Corti, A., Isoaspartate-glycine-arginine: a new tumor vasculaturetargeting motif. Cancer Res., 2008, 68 (17), 7073-7082.
24. Curnis, F.; Cattaneo, A.; Longhi, R.; Sacchi, A.; Gasparri, A.M.; Pastorino, F.; Di Matteo, P.; Traversari, C.; Bachi, A.; Ponzoni, M.; Rizzardi, G.P.; Corti, A., Critical role of flanking residues in NGRto- isoDGR transition and CD13/integrin receptor switching. J. Biol. Chem., 2010, 285 (12), 9114-9123.
25. van Hensbergen, Y.; Broxterman, H.J.; Elderkamp, Y.W.; Lankelma, J.; Beers, J.C.; Heijn, M.; Boven, E.; Hoekman, K.; Pinedo, H.M., A doxorubicin-CNGRC-peptide conjugate with prodrug properties. Biochem. Pharmacol., 2002, 63 (5), 897-908.
26. Pastorino, F.; Brignole, C.; Marimpietri, D.; Cilli, M.; Gambini, C.; Ribatti, D.; Longhi, R.; Allen, T.M.; Corti, A.; Ponzoni, M., Vascular damage and anti-angiogenic effects of tumor vesseltargeted liposomal chemotherapy. Cancer Res., 2003, 63 (21), 7400-7409.
27. Pastorino, F.; Brignole, C.; Di Paolo, D.; Nico, B.; Pezzolo, A.; Marimpietri, D.; Pagnan, G.; Piccardi, F.; Cilli, M.; Longhi, R.; Ribatti, D.; Corti, A.; Allen, T.M.; Ponzoni, M., Targeting liposomal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy. Cancer Res., 2006, 66 (20), 10073-10082.
28. Garde, S.V.; Forte, A.J.; Ge, M.; Lepekhin, E.A.; Panchal, C.J.; Rabbani, S.A.; Wu, J.J., Binding and internalization of NGRpeptide- targeted liposomal doxorubicin (TVT-DOX) in CD13- expressing cells and its antitumor effects. Anticancer Drugs, 2007, 18 (10), 1189-1200.
29. Wang, X.; Wang, Y.G.; Chen, X.M.; Wang, J.C.; Zhang, X.; Zhang, Q., NGR-modified micelles enhance their interaction with CD13-overexpressing tumor and endothelial cells. J. Controlled Rel., 2009, 139 (1), 56-62.
30. Negussie, A.H.; Miller, J.L.; Reddy, G.; Drake, S.K.; Wood, B.J.; Dreher, M.R., Synthesis and in vitro evaluation of cyclic NGR peptide targeted thermally sensitive liposome. J. Controlled Rel., 2010, 143 (2), 265-273.
31. Pastorino, F.; Di Paolo, D.; Piccardi, F.; Nico, B.; Ribatti, D.; Daga, A.; Baio, G.; Neumaier, C.E.; Brignole, C.; Loi, M.; Marimpietri, D.; Pagnan, G.; Cilli, M.; Lepekhin, E.A.; Garde, S.V.; Longhi, R.; Corti, A.; Allen, T.M.; Wu, J.J.; Ponzoni, M., Enhanced antitumor efficacy of clinical-grade vasculaturetargeted liposomal doxorubicin. Clin. Cancer Res., 2008, 14 (22), 7320-7329.
32. Murase, Y.; Asai, T.; Katanasaka, Y.; Sugiyama, T.; Shimizu, K.; Maeda, N.; Oku, N., A novel DDS strategy, "dual-targeting", and its application for antineovascular therapy. Cancer Lett., 2010, 287 (2), 165-171.
33. Zhao, B.J.; Ke, X.Y.; Huang, Y.; Chen, X.M.; Zhao, X.; Zhao, B.X.; Lu, W.L.; Lou, J.N.; Zhang, X.; Zhang, Q., The antiangiogenic efficacy of NGR-modified PEG-DSPE micelles containing paclitaxel (NGR-M-PTX) for the treatment of glioma in rats. J. Drug Target, 2011, 19 (5), 382-390.
34. Ferrero, E.; Zocchi, M.R.; Magni, E.; Panzeri, M.C.; Curnis, F.; Rugarli, C.; Ferrero, M.E.; Corti, A., Roles of tumor necrosis factor p55 and p75 receptors in TNF-alpha-induced vascular permeability. Am. J. Physiol. Cell Physiol., 2001, 281 (4), C1173-1179.
35. Eggermont, A.M.; Schraffordt Koops, H.; Lienard, D.; Kroon, B.B.; van Geel, A.N.; Hoekstra, H.J.; Lejeune, F.J., Isolated limb perfusion with high-dose tumor necrosis factor-alpha in combination with interferon-gamma and melphalan for nonresectable extremity soft tissue sarcomas: a multicenter trial. J. Clin. Oncol., 1996, 14 (10), 2653-2665.
36. Grunhagen, D.J.; Brunstein, F.; ten Hagen, T.L.; van Geel, A.N.; de Wilt, J.H.; Eggermont, A.M., TNF-based isolated limb perfusion: a decade of experience with antivascular therapy in the management of locally advanced extremity soft tissue sarcomas. Cancer Treat. Res., 2004, 120 (10),65-79.
37. 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 (3), 867-874.
38. Curnis, F.; Sacchi, A.; Corti, A., Improving chemotherapeutic drug penetration in tumors by vascular targeting and barrier alteration. J. Clin. Invest., 2002, 110 (4), 475-482.
39. Sacchi, A.; Gasparri, A.; Gallo-Stampino, C.; Toma, S.; Curnis, F.; Corti, A., Synergistic antitumor activity of cisplatin, paclitaxel, and gemcitabine with tumor vasculature-targeted tumor necrosis factoralpha. Clin. Cancer Res., 2006, 12 (1), 175-182.
40. Gregorc, V.; Santoro, A.; Bennicelli, E.; Punt, C.J.; Citterio, G.; Timmer-Bonte, J.N.; Caligaris Cappio, F.; Lambiase, A.; Bordignon, C.; van Herpen, C.M., Phase Ib study of NGR-hTNF, a selective vascular targeting agent, administered at low doses in combination with doxorubicin to patients with advanced solid tumours. Br. J. Cancer, 2009, 101 (2), 219-224.
41. Gregorc, V.; De Braud, F.G.; De Pas, T.M.; Scalamogna, R.; Citterio, G.; Milani, A.; Boselli, S.; Catania, C.; Donadoni, G.; Rossoni, G.; Ghio, D.; Spitaleri, G.; Ammannati, C.; Colombi, S.; Caligaris-Cappio, F.; Lambiase, A.; Bordignon, C., Phase I study of NGR-hTNF, a selective vascular targeting agent, in combination with cisplatin in refractory solid tumors. Clin. Cancer Res., 2011, 17 (7), 1964-1972.
42. Silver, R.T.; Woolf, S.H.; Hehlmann, R.; Appelbaum, F.R.; Anderson, J.; Bennett, C.; Goldman, J.M.; Guilhot, F.; Kantarjian, H.M.; Lichtin, A.E.; Talpaz, M.; Tura, S., An evidence-based analysis of the effect of busulfan, hydroxyurea, interferon, and allogeneic bone marrow transplantation in treating the chronic phase of chronic myeloid leukemia: developed for the American Society of Hematology. Blood, 1999, 94 (5), 1517-1536.
43. Wadler, S., The role of interferons in the treatment of solid tumors. Cancer, 1992, 70 (4 Suppl), 949-958.
44. Caraceni, A.; Gangeri, L.; Martini, C.; Belli, F.; Brunelli, C.; Baldini, M.; Mascheroni, L.; Lenisa, L.; Cascinelli, N., Neurotoxicity of interferon-alpha in melanoma therapy: results from a randomized controlled trial. Cancer, 1998, 83 (3), 482-489.
45. Meng, J.; Yan, Z.; Wu, J.; Li, L.; Xue, X.; Li, M.; Li, W.; Hao, Q.; Wan, Y.; Qin, X.; Zhang, C.; You, Y.; Han, W.; Zhang, Y., Highyield expression, purification and characterization of tumortargeted IFN-alpha2a. Cytotherapy, 2007, 9 (1), 60-68.
46. Sacchi, A.; Gasparri, A.; Curnis, F.; Bellone, M.; Corti, A., Crucial role for interferon gamma in the synergism between tumor vasculature-targeted tumor necrosis factor alpha (NGR-TNF) and doxorubicin. Cancer Res., 2004, 64 (19), 7150-7155.
47. Dondossola, E.; Gasparri, A.M.; Colombo, B.; Sacchi, A.; Curnis, F.; Corti, A., Chromogranin A restricts drug penetration and limits the ability of NGR-TNF to enhance chemotherapeutic efficacy. Cancer Res., 2011, 71 (17), 5881-5890.
48. Bieker, R.; Kessler, T.; Schwoppe, C.; Padro, T.; Persigehl, T.; Bremer, C.; Dreischaluck, J.; Kolkmeyer, A.; Heindel, W.; Mesters, R.M.; Berdel, W.E., Infarction of tumor vessels by NGRpeptide- directed targeting of tissue factor: experimental results and first-in-man experience. Blood, 2009, 113 (20), 5019-5027.
49. Curnis, F.; Gasparri, A.; Sacchi, A.; Cattaneo, A.; Magni, F.; Corti, A., Targeted delivery of IFNgamma to tumor vessels uncouples antitumor from counterregulatory mechanisms. Cancer Res., 2005, 65 (7), 2906-2913.
50. Zhang, B.; Gao, B.; Dong, S.; Zhang, Y.; Wu, Y., Anti-tumor efficacy and pre-clinical immunogenicity of IFNalpha2a-NGR. Regul. Toxicol. Pharmacol., 2011, 60 (1), 73-78.
51. Lu, L.I.; Wang, X.; Wang, L.; Zhang, B.; Yan, S.; Zhao, X.; Li, W.; Cui, M.; Gao, M.; Zhang, Y.; Wu, Y., Pharmacokinetics of rh- IFNalpha-2a-NGR, a tumor targeted-therapy candidate, following intramuscular administration to mice, rats and monkeys. Pharmazie, 2011, 66 (9), 690-693.
52. Yokoyama, Y.; Ramakrishnan, S., Addition of an aminopeptidase N-binding sequence to human endostatin improves inhibition of ovarian carcinoma growth. Cancer, 2005, 104 (2), 321-331.
53. Mastrobattista, E.; Bravo, S.A.; van der Aa, M.; Crommelin, D.J.A., Nonviral gene delivery systems: from simple transfection agents to artificial viruses. Drug Discovery Today: Technologies, 2005, 2 (1), 103-109.
54. Moffatt, S.; Cristiano, R.J., Uptake characteristics of NGR-coupled stealth PEI/pDNA nanoparticles loaded with PLGA-PEG-PLGA tri-block copolymer for targeted delivery to human monocytederived dendritic cells. Int. J. Pharm., 2006, 321 (12), 143-154.
55. Liu, L.; Anderson, W.F.; Beart, R.W.; Gordon, E.M.; Hall, F.L., Incorporation of tumor vasculature targeting motifs into moloney murine leukemia virus env escort proteins enhances retrovirus binding and transduction of human endothelial cells. J. Virol., 2000, 74 (11), 5320-5328.
56. Jullienne, B.; Vigant, F.; Muth, E.; Chaligne, R.; Bouquet, C.; Giraudier, S.; Perricaudet, M.; Benihoud, K., Efficient delivery of angiostatin K1-5 into tumors following insertion of an NGR peptide into adenovirus capsid. Gene Ther., 2009, 16 (12), 1405-1415.
57. Zhou, T.; Jia, X.; Li, H.; Wang, J.; Zhang, H.; A, Y.; Zhang, Z., New tumor-targeted nanosized delivery carrier for oligonucleotides: characteristics in vitro and in vivo. Int. J. Nanomedicine, 2011, 6, 1527-1534.
58. [von Wallbrunn, A.; Waldeck, J.; Holtke, C.; Zuhlsdorf, M.; Mesters, R.; Heindel, W.; Schafers, M.; Bremer, C., In vivo optical imaging of CD13/APN-expression in tumor xenografts. J. Biomed. Opt., 2008, 13 (1), 011007.
59. Wang, R.E.; Niu, Y.; Wu, H.; Amin, M.N.; Cai, J., Development of NGR peptide-based agents for tumor imaging. Am. J. Nucl. Med. Mol. Imaging., 2011, 1 (1), 36-46.