Immunoglobulin Fc-fused, neuropilin-1-specific peptide shows efficient tumor tissue penetration and inhibits tumor growth via anti-angiogenesis

Journal of Controlled Release

Volumn 216, Issue , 2015, Pages 56-68

  Kim, Ye Jin ^a   Bae, Jeomil ^a   Shin, Tae Hwan ^a   Kang, Se Hun ^b   Jeong, Moonkyoung ^c   Han, Yunho ^c   Park, Ji Ho ^c   Kim, Seok Ki ^b   Kim, Yong Sung ^a  

^a Ajou University   (South Korea)

^b National Cancer Center   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Anti angiogenesis; Antibody therapy; Fc fusion peptide; Tumor penetration; Tumor targeting, Neuropilin 1

Indexed keywords

ANTIBODIES; DISEASES; ENDOTHELIAL CELLS; GLYCOPROTEINS; MAMMALS; MONOCLONAL ANTIBODIES; PEPTIDES; TISSUE;

ANGIOGENESIS; ANTIBODY THERAPY; FUSION PEPTIDES; TUMOR PENETRATION; TUMOR TARGETING;

TUMORS;

ANGIOGENESIS INHIBITOR; CETUXIMAB; DOXORUBICIN; IMMUNOGLOBULIN FC TPP1 FUSION PROTEIN; NEUROPILIN 1; NEUROPILIN 2; SEMAPHORIN 3A; UNCLASSIFIED DRUG; UVOMORULIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2; ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIBIOTIC; CADHERIN; IMMUNOGLOBULIN FC FRAGMENT; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BINDING AFFINITY; BLOOD VESSEL PERMEABILITY; BREAST METASTASIS; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DOWN REGULATION; DRUG CLEARANCE; DRUG HALF LIFE; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR INVASION; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BINDING SITE; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; METABOLISM; NEOPLASMS, EXPERIMENTAL; PERMEABILITY;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS; BINDING SITES; CADHERINS; CETUXIMAB; DOWN-REGULATION; DOXORUBICIN; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; MICE; MICE, INBRED BALB C; NEOPLASMS, EXPERIMENTAL; NEUROPILIN-1; PERMEABILITY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84940210504     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.08.016     Document Type: Article

References (50)

1. F. Marcucci, M. Bellone, C. Rumio, and A. Corti Approaches to improve tumor accumulation and interactions between monoclonal antibodies and immune cells MAbs 5 2013 34 46
2. V.P. Chauhan, T. Stylianopoulos, Y. Boucher, and R.K. Jain Delivery of molecular and nanoscale medicine to tumors: transport barriers and strategies Annu. Rev. Chem. Biomol. Eng. 2 2011 281 298
3. G.M. Thurber, M.M. Schmidt, and K.D. Wittrup Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance Adv. Drug Deliv. Rev. 60 2008 1421 1434
4. I.A. Khawar, J.H. Kim, and H.J. Kuh Improving drug delivery to solid tumors: priming the tumor microenvironment J. Control. Release 201C 2015 78 89
5. I. Beyer, R. van Rensburg, R. Strauss, Z. Li, H. Wang, J. Persson, R. Yumul, Q. Feng, H. Song, J. Bartek, P. Fender, and A. Lieber Epithelial junction opener JO-1 improves monoclonal antibody therapy of cancer Cancer Res. 71 2011 7080 7090
6. M.W. Parker, H.F. Guo, X. Li, A.D. Linkugel, and C.W. Vander Kooi Function of members of the neuropilin family as essential pleiotropic cell surface receptors Biochemistry 51 2012 9437 9446
7. G.J. Prud'homme, and Y. Glinka Neuropilins are multifunctional coreceptors involved in tumor initiation, growth, metastasis and immunity Oncotarget 3 2012 921 939
8. B. Chaudhary, Y.S. Khaled, B.J. Ammori, and E. Elkord Neuropilin 1: function and therapeutic potential in cancer Cancer Immunol. Immunother. 63 2014 81 99
9. T. Kadonosono, A. Yamano, T. Goto, T. Tsubaki, M. Niibori, T. Kuchimaru, and S. Kizaka-Kondoh Cell penetrating peptides improve tumor delivery of cargos through neuropilin-1-dependent extravasation J. Control. Release 201 2015 14 21
10. L.M. Acevedo, S. Barillas, S.M. Weis, J.R. Gothert, and D.A. Cheresh Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor Blood 111 2008 2674 2680
11. L. Treps, A. Le Guelte, and J. Gavard Emerging roles of Semaphorins in the regulation of epithelial and endothelial junctions Tissue Barriers 1 2013 e23272
12. K.N. Sugahara, T. Teesalu, P.P. Karmali, V.R. Kotamraju, L. Agemy, D.R. Greenwald, and E. Ruoslahti Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs Science 328 2010 1031 1035
13. T. Teesalu, K.N. Sugahara, V.R. Kotamraju, and E. Ruoslahti C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration Proc. Natl. Acad. Sci. U. S. A. 106 2009 16157 16162
14. T.H. Shin, E.S. Sung, Y.J. Kim, K.S. Kim, S.H. Kim, S.K. Kim, Y.D. Lee, and Y.S. Kim Enhancement of the tumor penetration of monoclonal antibody by fusion of a neuropilin-targeting peptide improves the antitumor efficacy Mol. Cancer Ther. 13 2014 651 661
15. H.L. Goel, and A.M. Mercurio VEGF targets the tumour cell Nat. Rev. Cancer 13 2013 871 882
16. H. Jia, L. Cheng, M. Tickner, A. Bagherzadeh, D. Selwood, and I. Zachary Neuropilin-1 antagonism in human carcinoma cells inhibits migration and enhances chemosensitivity Br. J. Cancer 102 2010 541 552
17. M.A. von Wronski, N. Raju, R. Pillai, N.J. Bogdan, E.R. Marinelli, P. Nanjappan, K. Ramalingam, T. Arunachalam, S. Eaton, K.E. Linder, F. Yan, S. Pochon, M.F. Tweedle, and A.D. Nunn Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor J. Biol. Chem. 281 2006 5702 5710
18. A. Starzec, P. Ladam, R. Vassy, S. Badache, N. Bouchemal, A. Navaza, C.H. du Penhoat, and G.Y. Perret Structure-function analysis of the antiangiogenic ATWLPPR peptide inhibiting VEGF(165) binding to neuropilin-1 and molecular dynamics simulations of the ATWLPPR/neuropilin-1 complex Peptides 28 2007 2397 2402
19. M.W. Parker, A.D. Linkugel, and C.W. Vander Kooi Effect of C-terminal sequence on competitive semaphorin binding to neuropilin-1 J. Mol. Biol. 425 2013 4405 4414
20. L. Roth, L. Agemy, V.R. Kotamraju, G. Braun, T. Teesalu, K.N. Sugahara, J. Hamzah, and E. Ruoslahti Transtumoral targeting enabled by a novel neuropilin-binding peptide Oncogene 31 2012 3754 3763
21. H. Jia, R. Aqil, L. Cheng, C. Chapman, S. Shaikh, A. Jarvis, A.W. Chan, B. Hartzoulakis, I.M. Evans, A. Frolov, J. Martin, P. Frankel, S. Djordevic, I.C. Zachary, and D.L. Selwood N-terminal modification of VEGF-A C terminus-derived peptides delineates structural features involved in neuropilin-1 binding and functional activity Chembiochem 15 2014 1161 1170
22. Q. Pan, Y. Chanthery, W.C. Liang, S. Stawicki, J. Mak, N. Rathore, R.K. Tong, J. Kowalski, S.F. Yee, G. Pacheco, S. Ross, Z. Cheng, J. Le Couter, G. Plowman, F. Peale, A.W. Koch, Y. Wu, A. Bagri, M. Tessier-Lavigne, and R.J. Watts Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth Cancer Cell 11 2007 53 67
23. M. Caunt, J. Mak, W.C. Liang, S. Stawicki, Q. Pan, R.K. Tong, J. Kowalski, C. Ho, H.B. Reslan, J. Ross, L. Berry, I. Kasman, C. Zlot, Z. Cheng, J. Le Couter, E.H. Filvaroff, G. Plowman, F. Peale, D. French, R. Carano, A.W. Koch, Y. Wu, R.J. Watts, M. Tessier-Lavigne, and A. Bagri Blocking neuropilin-2 function inhibits tumor cell metastasis Cancer Cell 13 2008 331 342
24. C.H. Lee, K.J. Park, E.S. Sung, A. Kim, J.D. Choi, J.S. Kim, S.H. Kim, M.H. Kwon, and Y.S. Kim Engineering of a human kringle domain into agonistic and antagonistic binding proteins functioning in vitro and in vivo Proc. Natl. Acad. Sci. U. S. A. 107 2010 9567 9571
25. D.K. Choi, J. Bae, S.M. Shin, J.Y. Shin, S. Kim, and Y.S. Kim A general strategy for generating intact, full-length IgG antibodies that penetrate into the cytosol of living cells MAbs 6 2014 1402 1414
26. H.J. Choi, Y.J. Kim, S. Lee, and Y.S. Kim A heterodimeric Fc-based bispecific antibody simultaneously targeting VEGFR-2 and Met exhibits potent anti-tumor activity Mol. Cancer Ther. 12 2013 2748 2759
27. L. Tang, N.P. Gabrielson, F.M. Uckun, T.M. Fan, and J. Cheng Size-dependent tumor penetration and in vivo efficacy of monodisperse drug-silica nanoconjugates Mol. Pharm. 10 2013 883 892
28. S. Moktan, E. Perkins, F. Kratz, and D. Raucher Thermal targeting of an acid-sensitive doxorubicin conjugate of elastin-like polypeptide enhances the therapeutic efficacy compared with the parent compound in vivo Mol. Cancer Ther. 11 2012 1547 1556
29. S. Yoon, Y.H. Kim, S.H. Kang, S.K. Kim, H.K. Lee, H. Kim, J. Chung, and I.H. Kim Bispecific Her2 × cotinine antibody in combination with cotinine-(histidine)2-iodine for the pre-targeting of Her2-positive breast cancer xenografts J. Cancer Res. Clin. Oncol. 140 2014 227 233
30. L.A. Khawli, P. Hu, and A.L. Epstein NHS76/PEP2, a fully human vasopermeability-enhancing agent to increase the uptake and efficacy of cancer chemotherapy Clin. Cancer Res. 11 2005 3084 3093
31. A. Kim, M.J. Kim, Y. Yang, J.W. Kim, Y.I. Yeom, and J.S. Lim Suppression of NF-kappaB activity by NDRG2 expression attenuates the invasive potential of highly malignant tumor cells Carcinogenesis 30 2009 927 936
32. J. Luchino, M. Hocine, M.C. Amoureux, B. Gibert, A. Bernet, A. Royet, I. Treilleux, P. Lecine, J.P. Borg, P. Mehlen, S. Chauvet, and F. Mann Semaphorin 3E suppresses tumor cell death triggered by the plexin D1 dependence receptor in metastatic breast cancers Cancer Cell 24 2013 673 685
33. M.W. Parker, P. Xu, X. Li, and C.W. Vander Kooi Structural basis for the selective vascular endothelial growth factor-A (VEGF-A) binding to neuropilin-1 J. Biol. Chem. 287 2012 11082 11089
34. C.W. Vander Kooi, M.A. Jusino, B. Perman, D.B. Neau, H.D. Bellamy, and D.J. Leahy Structural basis for ligand and heparin binding to neuropilin B domains Proc. Natl. Acad. Sci. U. S. A. 104 2007 6152 6157
35. H.B. Pang, G.B. Braun, T. Friman, P. Aza-Blanc, M.E. Ruidiaz, K.N. Sugahara, T. Teesalu, and E. Ruoslahti An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability Nat. Commun. 5 2014 4904
36. B.A. Appleton, P. Wu, J. Maloney, J. Yin, W.C. Liang, S. Stawicki, K. Mortara, K.K. Bowman, J.M. Elliott, W. Desmarais, J.F. Bazan, A. Bagri, M. Tessier-Lavigne, A.W. Koch, Y. Wu, R.J. Watts, and C. Wiesmann Structural studies of neuropilin/antibody complexes provide insights into semaphorin and VEGF binding EMBO J. 26 2007 4902 4912
37. A. Le Guelte, E.M. Galan-Moya, J. Dwyer, L. Treps, G. Kettler, J.K. Hebda, S. Dubois, C. Auffray, H. Chneiweiss, N. Bidere, and J. Gavard Semaphorin 3A elevates endothelial cell permeability through PP2A inactivation J. Cell Sci. 125 2012 4137 4146
38. L. Wang, D. Mukhopadhyay, and X. Xu C terminus of RGS-GAIP-interacting protein conveys neuropilin-1-mediated signaling during angiogenesis FASEB J. 20 2006 1513 1515
39. J.K. Kim, M. Firan, C.G. Radu, C.H. Kim, V. Ghetie, and E.S. Ward Mapping the site on human IgG for binding of the MHC class I-related receptor, FcRn Eur. J. Immunol. 29 1999 2819 2825
40. Y. Xin, S. Bai, L.A. Damico-Beyer, D. Jin, W.C. Liang, Y. Wu, F.P. Theil, A. Joshi, Y. Lu, J. Lowe, M. Maia, R.K. Brachmann, and H. Xiang Anti-neuropilin-1 (MNRP1685A): unexpected pharmacokinetic differences across species, from preclinical models to humans Pharm. Res. 29 2012 2512 2521
41. H. Kawamura, X. Li, S.J. Harper, D.O. Bates, and L. Claesson-Welsh Vascular endothelial growth factor (VEGF)-A165b is a weak in vitro agonist for VEGF receptor-2 due to lack of coreceptor binding and deficient regulation of kinase activity Cancer Res. 68 2008 4683 4692
42. L. Claesson-Welsh, and M. Welsh VEGFA and tumour angiogenesis J. Intern. Med. 273 2013 114 127
43. Y. Kang, and J. Massague Epithelial-mesenchymal transitions: twist in development and metastasis Cell 118 2004 277 279
44. B. Herzog, C. Pellet-Many, G. Britton, B. Hartzoulakis, and I.C. Zachary VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation Mol. Biol. Cell 22 2011 2766 2776
45. T.M. Hong, Y.L. Chen, Y.Y. Wu, A. Yuan, Y.C. Chao, Y.C. Chung, M.H. Wu, S.C. Yang, S.H. Pan, J.Y. Shih, W.K. Chan, and P.C. Yang Targeting neuropilin 1 as an antitumor strategy in lung cancer Clin. Cancer Res. 13 2007 4759 4768
46. K.N. Sugahara, G.B. Braun, T.H. de Mendoza, V.R. Kotamraju, R.P. French, A.M. Lowy, T. Teesalu, and E. Ruoslahti Tumor-penetrating iRGD peptide inhibits metastasis Mol. Cancer Ther. 14 2015 120 128
47. A. Raza, M.J. Franklin, and A.Z. Dudek Pericytes and vessel maturation during tumor angiogenesis and metastasis Am. J. Hematol. 85 2010 593 598
48. S.L. Lee, P. Rouhi, L. Dahl Jensen, D. Zhang, H. Ji, G. Hauptmann, P. Ingham, and Y. Cao Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model Proc. Natl. Acad. Sci. U. S. A. 106 2009 19485 19490
49. I.K. Choi, R. Strauss, M. Richter, C.O. Yun, and A. Lieber Strategies to increase drug penetration in solid tumors Front. Oncol. 3 2013 193
50. J.R. Wild, C.A. Staton, K. Chapple, and B.M. Corfe Neuropilins: expression and roles in the epithelium Int. J. Exp. Pathol. 93 2012 81 103