NGR peptide ligands for targeting CD13/APN identified through peptide array screening resemble fibronectin sequences

ACS Combinatorial Science

Volumn 14, Issue 11, 2012, Pages 590-599

  Soudy, Rania ^a   Ahmed, Sahar ^a   Kaur, Kamaljit ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

aminopeptidase N CD13; NGR sequence; peptide array cell binding; tumor targeting

Indexed keywords

FIBRONECTIN; LIGAND; MICROSOMAL AMINOPEPTIDASE; NGR PEPTIDE; OLIGOPEPTIDE;

ARTICLE; METABOLISM;

ANTIGENS, CD13; FIBRONECTINS; LIGANDS; OLIGOPEPTIDES;

EID: 84869063107     PISSN: 21568952     EISSN: None     Source Type: Journal    
DOI: 10.1021/co300055s     Document Type: Article

References (52)

1. Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Targeting of drugs and nanoparticles to tumors J. Cell Biol. 2010, 188, 759-768
2. Liu, Z.; Wu, K. Peptides homing to tumor vasculature: Imaging and therapeutics for cancer Recent Pat. Anti-Cancer Drug Discovery 2008, 3, 202-208
3. Chen, K.; Chen, X. Integrin targeted delivery of chemotherapeutics Theranostics 2011, 1, 189-200
4. Brooks, P. C.; Clark, R. A. F.; Cheresh, D. A. Requirement of vascular integrin alpha v beta 3 for angiogenesis Science 1994, 264, 569-571
5. Wickström, M.; Larsson, R.; Nygren, P.; Gullbo, J. Aminopeptidase N (CD13) as a target for cancer chemotherapy Cancer Sci. 2011, 102, 501-508
6. Hicklin, D. J.; Ellis, L. M. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis J. Clin. Oncol. 2005, 23, 1011-1027 (Pubitemid 46202320)
7. Veikkola, T.; Karkkainen, M.; Claesson-Welsh, L.; Alitalo, K. Regulation of angiogenesis via vascular endothelial growth factor receptors Cancer Res. 2000, 60, 203-212 (Pubitemid 30070735)
8. Silletti, S.; Kessler, T.; Goldberg, J.; Boger, D. L.; Cheresh, D. A. Disruption of matrix metalloproteinase 2 binding to integrin αvβ3 by an organic molecule inhibits angiogenesis and tumor growth in vivo Proc. Natl. Acad. Sci. 2001, 98, 119-124 (Pubitemid 32095873)
9. Desgrosellier, J. S.; Cheresh, D. A. Integrins in cancer: Biological implications and therapeutic opportunities Nat. Rev. Cancer 2010, 10, 9-22
10. Allen, T. M. Ligand-targeted therapeutics in anticancer therapy Nat. Rev. Cancer 2002, 2, 750-763 (Pubitemid 37328910)
11. Mina-Osorio, P. The moonlighting enzyme CD13: Old and new functions to target Trends Mol. Med. 2008, 14, 361-371
12. Fukasawa, K.; Fujii, H.; Saitoh, Y.; Koizumi, K.; Aozuka, Y.; Sekine, K.; Yamada, M.; Saiki, I.; Nishikawa, K. Aminopeptidase N (APN/CD13) is selectively expressed in vascular endothelial cells and plays multiple roles in angiogenesis Cancer Lett. 2006, 243, 135-143 (Pubitemid 44508648)
13. 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 (Pubitemid 34126966)
14. Matteo, P. D.; Arrigoni, G. L.; Alberici, L.; Corti, A.; Gallo-Stampino, C.; Traversari, C.; Doglioni, C.; Rizzardi, G.-P. Enhanced expression of CD13 in vessels of inflammatory and neoplastic tissues J. Histochem. Cytochem. 2011, 59, 47-59
15. Pasqualini, R.; Koivunen, E.; Kain, R.; Lahdenranta, J.; Sakamoto, M.; Stryhn, A.; Ashmun, R. A.; Shapiro, L. H.; Arap, W.; Ruoslahti, E. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis Cancer Res. 2000, 60, 722-727 (Pubitemid 30094573)
16. Pasqualini, R.; Koivunen, E.; Ruoslahti, E. A peptide isolated from phage display libraries is a structural and functional mimic of an RGD-binding site on integrins J. Cell Biol. 1995, 130, 1189-1196
17. Arap, W.; Pasqualini, R.; Ruoslahti, E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model Science 1998, 279, 377-380 (Pubitemid 28063372)
18. 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, 1185-1190
19. 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, 964-975 (Pubitemid 32611306)
20. 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 vessel-targeted liposomal chemotherapy Cancer Res. 2003, 63, 7400-7409 (Pubitemid 37413482)
21. Di Matteo, P.; Curnis, F.; Longhi, R.; Colombo, G.; Sacchi, A.; Crippa, L.; Protti, M. P.; Ponzoni, M.; Toma, S.; Corti, A. Immunogenic and structural properties of the Asn-Gly-Arg (NGR) tumor neovasculature-homing motif Mol. Immunol. 2006, 43, 1509-1518
22. Corti, A.; Curnis, F.; Arap, W.; Pasqualini, R. The neovasculature homing motif NGR: More than meets the eye Blood 2008, 112, 2628-2635
23. van Hensbergen, Y.; Broxterman, H. J.; Elderkamp, Y. W.; Lankelma, J.; Beers, J. C. C.; Heijn, M.; Boven, E.; Hoekman, K.; Pinedo, H. M. A doxorubicin-CNGRC-peptide conjugate with prodrug properties Biochem. Pharmacol. 2002, 63, 897-908 (Pubitemid 34243003)
24. Ndinguri, M. W.; Solipuram, R.; Gambrell, R. P.; Aggarwal, S.; Hammer, R. P. Peptide targeting of platinum anti-cancer drugs Bioconjug. Chem. 2009, 20, 1869-1878
25. 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 (Pubitemid 29439574)
26. Santoro, A.; Pressiani, T.; Citterio, G.; Rossoni, G.; Donadoni, G.; Pozzi, F.; Rimassa, L.; Personeni, N.; Bozzarelli, S.; Colombi, S.; De Braud, F. G.; Caligaris-Cappio, F.; Lambiase, A.; Bordignon, C. Activity and safety of NGR-hTNF, a selective vascular-targeting agent, in previously treated patients with advanced hepatocellular carcinoma Br. J. Cancer 2010, 103, 837-844
27. Santoro, A.; Rimassa, L.; Sobrero, A. F.; Citterio, G.; Sclafani, F.; Carnaghi, C.; Pessino, A.; Caprioni, F.; Andretta, V.; Tronconi, M. C.; Finocchiaro, G.; Rossoni, G.; Zanoni, A.; Miggiano, C.; Rizzardi, G.-P.; Traversari, C.; Caligaris-Cappio, F.; Lambiase, A.; Bordignon, C. Phase II study of NGR-hTNF, a selective vascular targeting agent, in patients with metastatic colorectal cancer after failure of standard therapy Eur. J. Cancer 2010, 46, 2746-2752
28. 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 Release 2010, 143, 265-273
29. Metaferia, B. B.; Rittler, M.; Gheeya, J. S.; Lee, A.; Hempel, H.; Plaza, A.; Stetler-Stevenson, W. G.; Bewley, C. A.; Khan, J. Synthesis of novel cyclic NGR/RGD peptide analogs via on resin click chemistry Bioorg. Med. Chem. Lett. 2010, 20, 7337-7340
30. Colombo, G.; Curnis, F.; De Mori, G. M. S.; 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, 47891-47897 (Pubitemid 36159317)
31. Plesniak, L. A.; Salzameda, B.; Hinderberger, H.; Regan, E.; Kahn, J.; Mills, S. A.; Teriete, P.; Yao, Y.; Jennings, P.; Marassi, F.; Adams, J. A. Structure and activity of CPNGRC: A modified CD13/APN peptidic homing motif Chem. Biol. Drug Des. 2010, 75, 551-562
32. 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 NGR-to-isoDGR transition and CD13/integrin receptor switching J. Biol. Chem. 2010, 285, 9114-9123
33. Ahmed, S.; Mathews, A. S.; Byeon, N.; Lavasanifar, A.; Kaur, K. Peptide Arrays for Screening Cancer Specific Peptides Anal. Chem. 2010, 82, 7533-7541
34. Hwang, R.; Varner, J. The role of integrins in tumor angiogenesis Hematol. Oncol. Clin. North Am. 2004, 18, 991-1006 (Pubitemid 39335755)
35. Haubner, R.; Weber, W. A.; Beer, A. J.; Vabuliene, E.; Reim, D.; Sarbia, M.; Becker, K.-F.; Goebel, M.; Hein, R.; Wester, H.-J.; Kessler, H.; Schwaiger, M. Noninvasive visualization of the activated αvβ3 integrin in cancer patients by positron emission tomography and [18F]galacto-RGD PLoS Med. 2005, 2, e70
36. Sugahara, K. N.; Teesalu, T.; Karmali, P. P.; Kotamraju, V. R.; Agemy, L.; Greenwald, D. R.; Ruoslahti, E. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs Science 2010, 328, 1031-1035
37. 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, 20205-20210 (Pubitemid 23278923)
38. Lau, D. H.; Guo, L.; Liu, R.; Song, A.; Shao, C.; Lam, K. S. Identifying peptide ligands for cell surface receptors using cell-growth-on-bead assay and one-bead one-compound combinatorial library Biotechnol. Lett. 2002, 24, 497-500 (Pubitemid 34263656)
39. 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, 36466-36476 (Pubitemid 46041380)
40. Shim, J. S.; Kim, J. H.; Cho, H. Y.; Yum, Y. N.; Kim, S. H.; Park, H.-J.; Shim, B. S.; Choi, S. H.; Kwon, H. J. Irreversible inhibition of CD13/aminopeptidase N by the antiangiogenic agent curcumin Chem. Biol. 2003, 10, 695-704 (Pubitemid 37089844)
41. Okochi, M.; Nomura, S.; Kaga, C.; Honda, H. Peptide array-based screening of human mesenchymal stem cell-adhesive peptides derived from fibronectin type III domain Biochem. Biophys. Res. Commun. 2008, 371, 85-89
42. Jiang, W.; Jin, G.; Ma, D.; Wang, F.; Fu, T.; Chen, X.; Chen, X.; Jia, K.; Marikar, F. M.; Hua, Z. Modification of cyclic NGR tumor neovasculature-homing motif sequence to human plasminogen kringle 5 improves inhibition of tumor growth PLoS One 2012, 7, e37132
43. 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 αvβ3 integrin J. Biol. Chem. 2008, 283, 19757-19768
44. Berditchevski, F.; Zutter, M. M.; Hemler, M. E. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins) Mol. Biol. Cell 1996, 7, 193-207 (Pubitemid 26064366)
45. Aozuka, Y.; Koizumi, K.; Saitoh, Y.; Ueda, Y.; Sakurai, H.; Saiki, I. Anti-tumor angiogenesis effect of aminopeptidase inhibitor bestatin against B16-BL6 melanoma cells orthotopically implanted into syngeneic mice Cancer Lett. 2004, 216, 35-42 (Pubitemid 39410494)
46. Bauvois, B.; Puiffe, M.-L.; Bongui, J.-B.; Paillat, S.; Monneret, C.; Dauzonne, D. Synthesis and biological evaluation of novel flavone-8-acetic acid derivatives as reversible inhibitors of aminopeptidase N/CD13 J. Med. Chem. 2003, 46, 3900-3913 (Pubitemid 37034139)
47. Bocquier, A. A.; Potts, J. R.; Pickford, A. R.; Campbell, I. D. Solution structure of a pair of modules from the gelatin-binding domain of fibronectin Structure 1999, 7, 1451-S3
48. Fucile, G.; Garcia, C.; Carlsson, J.; Sunnerhagen, M.; Christendat, D. Structural and biochemical investigation of two Arabidopsis shikimate kinases: The heat-inducible isoform is thermostable Protein Sci. 2011, 20, 1125-1136
49. Williams, M. J.; Phan, I.; Harvey, T. S.; Rostagno, A.; Gold, L. I.; Campbell, I. D. Solution structure of a pair of fibronectin type 1 modules with fibrin binding activity J. Mol. Biol. 1994, 235, 1302-1311 (Pubitemid 24148932)
50. Leahy, D. J.; Aukhil, I.; Erickson, H. P. 2.0 Å Crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region Cell 1996, 84, 155-164
51. Soliman, W.; Wang, L.; Bhattacharjee, S.; Kaur, K. Structure-activity relationships of an antimicrobial peptide plantaricin S from two-peptide class IIb bacteriocins J. Med. Chem. 2011, 54, 2399-2408
52. Kocbek, P.; Obermajer, N.; Cegnar, M.; Kos, J.; Kristl, J. Targeting cancer cells using PLGA nanoparticles surface modified with monoclonal antibody J. Controlled Release 2007, 120, 18-26 (Pubitemid 46874614)