Combination-targeting to multiple endothelial cell adhesion molecules modulates binding, endocytosis, and in vivo biodistribution of drug nanocarriers and their therapeutic cargoes

Journal of Controlled Release

Volumn 188, Issue , 2014, Pages 87-98

  Papademetriou, Iason ^a   Tsinas, Zois ^a   Hsu, Janet ^a   Muro, Silvia ^a,b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Combination targeting; Endocytosis; Endothelial cell adhesion molecules; In vivo biodistribution; Lysosomal enzyme delivery; Targeted nanocarriers

Indexed keywords

BIOMOLECULES; CAMS; ENDOTHELIAL CELLS; MOLECULES;

COMBINATION TARGETING; ENDOCYTOSIS; IN-VIVO; LYSOSOMAL ENZYMES; NANO-CARRIERS;

DISEASE CONTROL;

CD31 ANTIGEN; CELL ADHESION MOLECULE; INTERCELLULAR ADHESION MOLECULE 1; NANOCARRIER; SPHINGOMYELIN PHOSPHODIESTERASE; VASCULAR CELL ADHESION MOLECULE 1; DRUG CARRIER; NANOPARTICLE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOTHELIUM CELL; IN VIVO STUDY; INTERNALIZATION; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; DRUG DELIVERY SYSTEM; HUMAN; LYSOSOME; METABOLISM; TISSUE DISTRIBUTION;

ANIMALS; ANTIGENS, CD31; CELL LINE; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LYSOSOMES; MICE, INBRED C57BL; NANOPARTICLES; TISSUE DISTRIBUTION; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84903746928     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.06.008     Document Type: Article

References (55)

1. P. Debbage Targeted drugs and nanomedicine: present and future Curr. Pharm. Des. 15 2009 153 172
2. R. Duncan, and S.C. Richardson Endocytosis and intracellular trafficking as gateways for nanomedicine delivery: opportunities and challenges Mol. Pharm. 9 2012 2380 2402
3. A.S. Hoffman The origins and evolution of "controlled" drug delivery systems J. Control. Release 132 2008 153 163
4. S. Muro Challenges in design and characterization of ligand-targeted drug delivery systems J. Control. Release 164 2012 125 137
5. S. Parveen, R. Misra, and S.K. Sahoo Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging Nanomedicine 8 2012 147 166
6. V.P. Torchilin Multifunctional nanocarriers Adv. Drug Deliv. Rev. 58 2006 1532 1555 (Pubitemid 44822608)
7. R. Weissleder, K. Kelly, E.Y. Sun, T. Shtatland, and L. Josephson Cell-specific targeting of nanoparticles by multivalent attachment of small molecules Nat. Biotechnol. 23 2005 1418 1423 (Pubitemid 41679395)
8. I.T. Papademetriou, C. Garnacho, E.H. Schuchman, and S. Muro In vivo performance of polymer nanocarriers dually-targeted to epitopes of the same or different receptors Biomaterials 34 2013 3459 3466
9. D. Sun, S. Nakao, F. Xie, S. Zandi, A. Schering, and A. Hafezi-Moghadam Superior sensitivity of novel molecular imaging probe: simultaneously targeting two types of endothelial injury markers FASEB J. 24 2010 1532 1540
10. J.K. Willmann, A.M. Lutz, R. Paulmurugan, M.R. Patel, P. Chu, J. Rosenberg, and S.S. Gambhir Dual-targeted contrast agent for US assessment of tumor angiogenesis in vivo Radiology 248 2008 936 944
11. S. Veeranarayanan, A.C. Poulose, M.S. Mohamed, S.H. Varghese, Y. Nagaoka, Y. Yoshida, T. Maekawa, and D.S. Kumar Synergistic targeting of cancer and associated angiogenesis using triple-targeted dual-drug silica nanoformulations for theragnostics Small 8 2012 3476 3489
12. Q. Xu, Y. Liu, S. Su, W. Li, C. Chen, and Y. Wu Anti-tumor activity of paclitaxel through dual-targeting carrier of cyclic RGD and transferrin conjugated hyperbranched copolymer nanoparticles Biomaterials 33 2012 1627 1639
13. X. Ying, H. Wen, W.L. Lu, J. Du, J. Guo, W. Tian, Y. Men, Y. Zhang, R.J. Li, T.Y. Yang, D.W. Shang, J.N. Lou, L.R. Zhang, and Q. Zhang Dual-targeting daunorubicin liposomes improve the therapeutic efficacy of brain glioma in animals J. Control. Release 141 2010 183 192
14. Y. Zhang, C. Zhu, and W.M. Pardridge Antisense gene therapy of brain cancer with an artificial virus gene delivery system Mol. Ther. 6 2002 67 72 (Pubitemid 36124272)
15. A.O. Eniola, and D.A. Hammer In vitro characterization of leukocyte mimetic for targeting therapeutics to the endothelium using two receptors Biomaterials 26 2005 7136 7144 (Pubitemid 41095536)
16. J.M. Saul, A.V. Annapragada, and R.V. Bellamkonda A dual-ligand approach for enhancing targeting selectivity of therapeutic nanocarriers J. Control. Release 114 2006 277 287 (Pubitemid 44310813)
17. A.O. Eniola, P.J. Willcox, and D.A. Hammer Interplay between rolling and firm adhesion elucidated with a cell-free system engineered with two distinct receptor-ligand pairs Biophys. J. 85 2003 2720 2731 (Pubitemid 37210818)
18. E.A. Ferrante, J.E. Pickard, J. Rychak, A. Klibanov, and K. Ley Dual targeting improves microbubble contrast agent adhesion to VCAM-1 and P-selectin under flow J. Control. Release 140 2009 100 107
19. R.C. Gunawan, D. Almeda, and D.T. Auguste Complementary targeting of liposomes to IL-1alpha and TNF-alpha activated endothelial cells via the transient expression of VCAM1 and E-selectin Biomaterials 32 2011 9848 9853
20. R.C. Gunawan, and D.T. Auguste The role of antibody synergy and membrane fluidity in the vascular targeting of immunoliposomes Biomaterials 31 2009 900 907
21. S.H. Ha, A. Carson, A. Agarwal, N.A. Kotov, and K. Kim Detection and monitoring of the multiple inflammatory responses by photoacoustic molecular imaging using selectively targeted gold nanorods Biomed. Opt. Express 2 2011 645 657
22. M.A. McAteer, K. Mankia, N. Ruparelia, A. Jefferson, H.B. Nugent, L.A. Stork, K.M. Channon, J.E. Schneider, and R.P. Choudhury A leukocyte-mimetic magnetic resonance imaging contrast agent homes rapidly to activated endothelium and tracks with atherosclerotic lesion macrophage content Arterioscler. Thromb. Vasc. Biol. 32 2012 1427 1435
23. G.P. Robbins, R.L. Saunders, J.B. Haun, J. Rawson, M.J. Therien, and D.A. Hammer Tunable leuko-polymersomes that adhere specifically to inflammatory markers Langmuir 26 2010 14089 14096
24. G.E. Weller, F.S. Villanueva, E.M. Tom, and W.R. Wagner Targeted ultrasound contrast agents: in vitro assessment of endothelial dysfunction and multi-targeting to ICAM-1 and sialyl Lewisx Biotechnol. Bioeng. 92 2005 780 788 (Pubitemid 41772473)
25. D. Serrano, and S. Muro Endothelial cell adhesion molecules and drug delivery applications H. Aranda-Espinoza, Mechanobiology of the Endothelium 2014 CRC Press Boca Raton
26. M.A. McAteer, J.E. Schneider, Z.A. Ali, N. Warrick, C.A. Bursill, C. von zur Muhlen, D.R. Greaves, S. Neubauer, K.M. Channon, and R.P. Choudhury Magnetic resonance imaging of endothelial adhesion molecules in mouse atherosclerosis using dual-targeted microparticles of iron oxide Arterioscler. Thromb. Vasc. Biol. 28 2008 77 83
27. D.A. Hammer, G.P. Robbins, J.B. Haun, J.J. Lin, W. Qi, L.A. Smith, P.P. Ghoroghchian, M.J. Therien, and F.S. Bates Leuko-polymersomes Faraday Discuss. 139 2008 129 141 (discussion 213-128, 419-120)
28. R. Rothlein, and T.A. Springer The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester J. Exp. Med. 163 1986 1132 1149 (Pubitemid 16000413)
29. P.J. Newman, M.C. Berndt, J. Gorski, G.C. White, S. Lyman, C. Paddock, and W.A. Muller PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily Science 247 1990 1219 1222
30. D.R. Phillips, and P.P. Agin Platelet plasma-membrane glycoproteins - evidence for presence of nonequivalent disulfide bonds using non-reduced-reduced 2-dimensional gel-electrophoresis J. Biol. Chem. 252 1977 2121 2126 (Pubitemid 8077399)
31. L. Osborn, C. Hession, R. Tizard, C. Vassallo, S. Luhowskyj, G. Chi-Rosso, and R. Lobb Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes Cell 59 1989 1203 1211 (Pubitemid 20024630)
32. P. Lorenzon, E. Vecile, E. Nardon, E. Ferrero, J.M. Harlan, F. Tedesco, and A. Dobrina Endothelial cell E- and P-selectin and vascular cell adhesion molecule-1 function as signaling receptors J. Cell Biol. 142 1998 1381 1391 (Pubitemid 28429118)
33. C. Garnacho, S.M. Albelda, V.R. Muzykantov, and S. Muro Differential intra-endothelial delivery of polymer nanocarriers targeted to distinct PECAM-1 epitopes J. Control. Release 130 2008 226 233
34. S. Muro, C. Garnacho, J.A. Champion, J. Leferovich, C. Gajewski, E.H. Schuchman, S. Mitragotri, and V.R. Muzykantov Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers Mol. Ther. 16 2008 1450 1458
35. S. Muro, R. Wiewrodt, A. Thomas, L. Koniaris, S.M. Albelda, V.R. Muzykantov, and M. Koval A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1 J. Cell Sci. 116 2003 1599 1609 (Pubitemid 36527505)
36. I. Ricard, M.D. Payet, and G. Dupuis VCAM-1 is internalized by a clathrin-related pathway in human endothelial cells but its alpha(4)beta(1) integrin counter-receptor remains associated with the plasma membrane in human T lymphocytes Eur. J. Immunol. 28 1998 1708 1718 (Pubitemid 28221176)
37. H. Hillaireau, and P. Couvreur Nanocarriers' entry into the cell: relevance to drug delivery Cell. Mol. Life Sci. 66 2009 2873 2896
38. J. Papademetriou, C. Garnacho, D. Serrano, T. Bhowmick, E.H. Schuchman, and S. Muro Comparative binding, endocytosis, and biodistribution of antibodies and antibody-coated carriers for targeted delivery of lysosomal enzymes to ICAM-1 versus transferrin receptor J. Inherit. Metab. Dis. 36 2013 467 477
39. X. He, S.R. Miranda, X. Xiong, A. Dagan, S. Gatt, and E.H. Schuchman Characterization of human acid sphingomyelinase purified from the media of overexpressing Chinese hamster ovary cells Biochim. Biophys. Acta 1432 1999 251 264 (Pubitemid 29304533)
40. J. Hsu, D. Serrano, T. Bhowmick, K. Kumar, Y. Shen, Y.C. Kuo, C. Garnacho, and S. Muro Enhanced endothelial delivery and biochemical effects of alpha-galactosidase by ICAM-1-targeted nanocarriers for Fabry disease J. Control. Release 149 2011 323 331
41. J.M. Warram, A.G. Sorace, R. Saini, H.R. Umphrey, K.R. Zinn, and K. Hoyt A triple-targeted ultrasound contrast agent provides improved localization to tumor vasculature J. Ultrasound Med. 30 2011 921 931
42. E.H. Schuchman, and R.J. Desnick Niemann-Pick disease types A and B: acid sphingomyelinase deficiencies C. Scriver, A. Beaudet, W. Sly, D. Valle, B. Childs, K. Kinzler, B. Vogelstein, F. Bunz, K.M. Gibson, G. Mitchell, The metabolic and molecular bases of inherited disease 2001 McGraw-Hill New York 3589 3610
43. S. Muro New biotechnological and nanomedicine strategies for treatment of lysosomal storage disorders Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2 2010 189 204
44. C. Garnacho, R. Dhami, E. Simone, T. Dziubla, J. Leferovich, E.H. Schuchman, V. Muzykantov, and S. Muro Delivery of acid sphingomyelinase in normal and Niemann-Pick disease mice using intercellular adhesion molecule-1-targeted polymer nanocarriers J. Pharmacol. Exp. Ther. 325 2008 400 408 (Pubitemid 351574785)
45. G. Liu, S.M. Vogel, X. Gao, K. Javaid, G. Hu, S.M. Danilov, A.B. Malik, and R.D. Minishall Scr phosphorylation of endothelial cell surface intercellular adhesion molecule-1 mediates neutrophil adhesion and contributes to the mechanism of lung inflammation Arterioscler. Thromb. Vasc. Biol. 31 2011 1342 1350
46. A.M. Chacko, M. Nayak, C.F. Greineder, H.M. Delissier, and V.R. Muzycantov Collaborative enhancement of antibody binding to distinct PECAM-1 epitopes modulates endothelial targeting PLoS One 7 2012 e34958
47. A.G. Kumar, X.Y. Dai, C.A. Kozak, M.P. Mims, A.M. Gotto, and C.M. Ballantyne Murine VCAM-1 - molecular-cloning, mapping, and analysis of a truncated form J. Immunol. 153 1994 4088 4098 (Pubitemid 24322576)
48. S. Lee, I.H. Yoon, A. Yoon, J.M. Cook-Mills, C.G. Park, and J. Chung An antibody to the sixth Ig-like domain of VCAM-1 inhibits leukocyte transendothelialmigration without affecting adhesion J. Immunol. 189 2012 4592 4601
49. A. Frey, K.T. Giannasca, R. Weltzin, P.J. Giannasca, H. Reggio, W.I. Lencer, and M.R. Neutra Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting J. Exp. Med. 184 1996 1045 1059 (Pubitemid 26313562)
50. T.M. Carlos, and J.M. Harlan Leukocyte-endothelial adhesion molecules Blood 84 1994 2068 2101 (Pubitemid 24296363)
51. J.P. Couty, C. Rampon, M. Leveque, M.P. Laran-Chich, S. Bourdoulous, J. Greenwood, and P.O. Couraud PECAM-1 engagement counteracts ICAM-1-induced signaling in brain vascular endothelial cells J. Neurochem. 103 2007 793 801 (Pubitemid 47498026)
52. W.Y. Liao, H.J. Li, M.Y. Chang, A.C. Tang, A.S. Hoffman, and P.C. Hsieh Comprehensive characterizations of nanoparticle biodistribution following systemic injection in mice Nanoscale 5 2013 11079 11086
53. V.R. Muzykantov, R. Radhakrishnan, and D.M. Eckmann Dynamic factors controlling targeting nanocarriers to vascular endothelium Curr. Drug Metab. 13 2012 70 81
54. J. Han, B.J. Zern, V.V. Shuvaev, P.F. Davies, S. Muro, and V. Muzykantov Acute and chronic shear stress differently regulate endothelial internalization of nanocarriers targeted to platelet-endothelial cell adhesion molecule-1 ACS Nano 6 2012 8824 8836
55. L.H. Romer, N.V. McLean, H.C. Yan, M. Daise, J. Sun, and H.M. DeLisser IFN-gamma and TNF-alpha induce redistribution of PECAM-1 (CD31) on human endothelial cells J. Immunol. 154 1995 6582 6592