Exploiting shape, cellular-hitchhiking and antibodies to target nanoparticles to lung endothelium: Synergy between physical, chemical and biological approaches

Biomaterials

Volumn 68, Issue , 2015, Pages 1-8

  Anselmo, Aaron C ^a   Kumar, Sunny ^a   Gupta, Vivek ^b   Pearce, Austin M ^a   Ragusa, Analisa ^a   Muzykantov, Vladimir ^c   Mitragotri, Samir ^a  

^a University of California   (United States)

^b KECK GRADUATE INSTITUTE   (United States)

^c University of Pennsylvania   (United States)

Author keywords

Cell mediated drug delivery; Cellular hitchhiking; Erythrocytes; Nanoparticles; Red blood cells; Shape

Indexed keywords

ANTIBODIES; BIOLOGICAL ORGANS; BLOOD; CELLS; CHEMICAL MODIFICATION; CYTOLOGY; IMMUNE SYSTEM; TISSUE;

CELLULAR HITCHHIKING; CHEMICAL AND BIOLOGICALS; ERYTHROCYTES; HYDROPHILIC COATINGS; NANOPARTICLE GEOMETRIES; RED BLOOD CELL; ROD-SHAPED PARTICLES; SHAPE;

NANOPARTICLES;

IMMUNOGLOBULIN G; INTERCELLULAR ADHESION MOLECULE 1 ANTIBODY; NANOPARTICLE; INTERCELLULAR ADHESION MOLECULE 1; MONOCLONAL ANTIBODY; NANOTUBE;

ACCUMULATION RATIO; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOLOGICAL FUNCTIONS; CELLULAR HITCHHIKING; COATED PARTICLE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG DELIVERY SYSTEM; ERYTHROCYTE; FEMALE; IMMUNE SYSTEM; LIVER; LUNG; LUNG ENDOTHELIUM; MOUSE; NANOPARTICLE SHAPE; NONHUMAN; PARAMETERS; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; SPLEEN; SURFACE PROPERTY; ANIMAL; ANTIBODY SPECIFICITY; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; ENDOTHELIUM; IMMUNOLOGY; MATERIALS TESTING; PARTICLE SIZE; TISSUE DISTRIBUTION; ULTRASTRUCTURE;

ANIMALS; ANTIBODIES, MONOCLONAL; CELLS, CULTURED; ENDOTHELIUM; ERYTHROCYTES; FEMALE; INTERCELLULAR ADHESION MOLECULE-1; LUNG; MATERIALS TESTING; MICE; MICE, INBRED BALB C; NANOTUBES; ORGAN SPECIFICITY; PARTICLE SIZE; TISSUE DISTRIBUTION;

EID: 84939628491     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.07.043     Document Type: Article

References (58)

1. Petros R.A., DeSimone J.M. Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 2010, 9:615-627.
2. Wang A.Z., Langer R., Farokhzad O.C. Nanoparticle delivery of cancer drugs. Annu. Rev. Med. 2012, 63:185-198.
3. Peer D., Karp J.M., Hong S., Farokhzad O.C., Margalit R., Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2007, 2:751-760.
4. Ruoslahti E. Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv. Mater. 2012, 24:3747-3756.
5. Moghimi S.M., Hunter A.C., Murray J.C. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 2001, 53:283-318.
6. Owens D.E., Peppas N.A. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 2006, 307:93-102.
7. Torchilin V.P., Trubetskoy V.S. Which polymers can make nanoparticulate drug carriers long-circulating?. Adv. Drug Deliv. Rev. 1995, 16:141-155.
8. Farokhzad O.C., Cheng J., Teply B.A., Sherifi I., Jon S., Kantoff P.W., et al. Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo. Proc. Natl. Acad. Sci. 2006, 103:6315-6320.
9. Decuzzi P, Godin B, Tanaka T, Lee SY, Chiappini C, Liu X, et al, Size and shape effects in the biodistribution of intravascularly injected particles, Journal of Controlled Release Official Journal of the Controlled Release Society.141:320-7.
10. Merkel T.J., Jones S.W., Herlihy K.P., Kersey F.R., Shields A.R., Napier M., et al. Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proc. Natl. Acad. Sci. 2011, 108:586-591.
11. Yoo J.W., Irvine D.J., Discher D.E., Mitragotri S. Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat. Rev. Drug Discov. 2011, 10:521-535.
12. Anselmo A.C., Mitragotri S. An overview of clinical and commercial impact of drug delivery systems. J. Control. Release 2014, 190:15-28.
13. Anselmo A.C., Mitragotri S. A review of clinical translation of inorganic nanoparticles. AAPS J. 2015, 10.1208/s12248-015-9780-2.
14. Cheng Z., Al Zaki A., Hui J.Z., Muzykantov V.R., Tsourkas A. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science 2012, 338:903-910.
15. Gref R., Minamitake Y., Peracchia M.T., Trubetskoy V., Torchilin V., Langer R. Biodegradable long-circulating polymeric nanospheres. Science 1994, 263:1600-1603.
16. Otsuka H., Nagasaki Y., Kataoka K. PEGylated nanoparticles for biological and pharmaceutical applications. Adv. drug Deliv. Rev. 2003, 55:403-419.
17. Brannon-Peppas L., Blanchette J.O. Nanoparticle and targeted systems for cancer therapy. Adv. Drug Deliv. Rev. 2012, 64:206-212.
18. Howard M., Zern B.J., Anselmo A.C., Shuvaev V.V., Mitragotri S., Muzykantov V. Vascular targeting of nanocarriers: perplexing aspects of the seemingly straightforward paradigm. ACS Nano 2014, 8:4100-4132.
19. Abu Lila A.S., Kiwada H., Ishida T. The accelerated blood clearance (ABC) phenomenon: clinical challenge and approaches to manage. J. Control. Release Off. J. Control. Release Soc. 2013, 172:38-47.
20. Ishida T., Maeda R., Ichihara M., Irimura K., Kiwada H. Accelerated clearance of PEGylated liposomes in rats after repeated injections. J. Control. Release 2003, 88:35-42.
21. Laverman P., Carstens M.G., Boerman O.C., Dams E.T.M., Oyen W.J., van Rooijen N., et al. Factors affecting the accelerated blood clearance of polyethylene glycol-liposomes upon repeated injection. J. Pharmacol. Exp. Ther. 2001, 298:607-612.
22. Schrama D., Reisfeld R.A., Becker J.C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov. 2006, 5:147-159.
23. Jahn E.-M., Schneider C.K. How to systematically evaluate immunogenicity of therapeutic proteins-regulatory considerations. New Biotechnol. 2009, 25:280-286.
24. Shankar G., Pendley C., Stein K.E. A risk-based bioanalytical strategy for the assessment of antibody immune responses against biological drugs. Nat. Biotechnol. 2007, 25:555-561.
25. Muro S., Garnacho C., Champion J.A., Leferovich J., Gajewski C., Schuchman E.H., et al. Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Mol. Ther. 2008, 16:1450-1458.
26. Kolhar P., Anselmo A.C., Gupta V., Pant K., Prabhakarpandian B., Ruoslahti E., et al. Using shape effects to target antibody-coated nanoparticles to lung and brain endothelium. Proc. Natl. Acad. Sci. 2013, 110:10753-10758.
27. Anselmo A.C., Zhang M., Kumar S., Vogus D.R., Menegatti S., Helgeson M.E., et al. Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis, and targeting. ACS Nano 2015, 9:3169-3177.
28. Geng Y., Dalhaimer P., Cai S., Tsai R., Tewari M., Minko T., et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2007, 2:249-255.
29. Doshi N., Zahr A.S., Bhaskar S., Lahann J., Mitragotri S. Red blood cell-mimicking synthetic biomaterial particles. Proc. Natl. Acad. Sci. 2009, 106:21495-21499.
30. Anselmo A.C., Modery-Pawlowski C.L., Menegatti S., Kumar S., Vogus D.R., Tian L.L., et al. Platelet-like nanoparticles: mimicking shape, flexibility, and surface biology of platelets to target vascular injuries. ACS Nano 2014, 8:11243-11253.
31. Hu C.-M.J., Zhang L., Aryal S., Cheung C., Fang R.H., Zhang L. Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform. Proc. Natl. Acad. Sci. 2011, 108:10980-10985.
32. Parodi A., Quattrocchi N., van de Ven A.L., Chiappini C., Evangelopoulos M., Martinez J.O., et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 2013, 8:61-68.
33. Rodriguez P.L., Harada T., Christian D.A., Pantano D.A., Tsai R.K., Discher D.E. Minimal" self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 2013, 339:971-975.
34. Anselmo A.C., Mitragotri S. Cell-mediated delivery of nanoparticles: taking advantage of circulatory cells to target nanoparticles. J. Control. Release 2014, 190:531-541.
35. Champion J.A., Katare Y.K., Mitragotri S. Making polymeric micro-and nanoparticles of complex shapes. Proc. Natl. Acad. Sci. 2007, 104:11901-11904.
36. Chambers E., Mitragotri S. Long circulating nanoparticles via adhesion on red blood cells: mechanism and extended circulation. Exp. Biol. Med. (Maywood) 2007, 232:958-966.
37. Anselmo A.C., Gupta V., Zern B.J., Pan D., Zakrewsky M., Muzykantov V., et al. Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano 2013, 7:11129-11137.
38. Chambers E., Mitragotri S. Prolonged circulation of large polymeric nanoparticles by non-covalent adsorption on erythrocytes. J. Control. Release 2004, 100:111-119.
39. Yoon J.-Y., Kim J.-H., Kim W.-S. Interpretation of protein adsorption phenomena onto functional microspheres. Colloids Surfaces B Biointerfaces 1998, 12:15-22.
40. Yoon J.-Y., Park H.-Y., Kim J.-H., Kim W.-S. Adsorption of BSA on highly carboxylated microspheres-quantitative effects of surface functional groups and interaction forces. J. Colloid Interface Sci. 1996, 177:613-620.
41. Szarka R.J., Wang N., Gordon L., Nation P., Smith R.H. A murine model of pulmonary damage induced by lipopolysaccharide via intranasal instillation. J. Immunol. Methods 1997, 202:49-57.
42. Beck-Schimmer B., Schimmer R.C., Warner R.L., Schmal H., Nordblom G., Flory C.M., et al. Expression of lung vascular and airway ICAM-1 after exposure to bacterial lipopolysaccharide. Am. J. Respir. Cell Mol. Biol. 1997, 17:344-352.
43. Anselmo A.C., Gilbert J.B., Kumar S., Gupta V., Cohen R.E., Rubner M.F., et al. Monocyte-mediated delivery of polymeric backpacks to inflamed tissues: a generalized strategy to deliver drugs to treat inflammation. J. Control. Release 2015, 199:29-36.
44. Shuvaev V.V., Ilies M.A., Simone E., Zaitsev S., Kim Y., Cai S., et al. Endothelial targeting of antibody-decorated polymeric filomicelles. ACS Nano 2011, 5:6991-6999.
45. Rossin R., Muro S., Welch M.J., Muzykantov V.R., Schuster D.P. In vivo imaging of 64Cu-labeled polymer nanoparticles targeted to the lung endothelium. J. Nucl. Med. 2008, 49:103-111.
46. Muzykantov V.R., Sakharov D.V., Smirnov M.D., Samokhin G.P., Smirnov V.N. Immunotargeting of erythrocytes-bound streptokinase provides local lysis of a fibrin clot. Biochim Biophys Acta (BBA) Gen. Subj. 1986, 884:355-362.
47. Muzykantov V.R. Drug delivery carriers on the fringes: natural red blood cells versus synthetic multilayered capsules. Expert Opin. Drug Deliv. 2013, 10:1-4.
48. Ganguly K., Krasik T., Medinilla S., Bdeir K., Cines D.B., Muzykantov V.R., et al. Blood clearance and activity of erythrocyte-coupled fibrinolytics. J. Pharmacol. Exp. Ther. 2005, 312:1106-1113.
49. Danielyan K., Ganguly K., Ding B.-S., Atochin D., Zaitsev S., Murciano J.-C., et al. Cerebrovascular thromboprophylaxis in mice by erythrocyte-coupled tissue-type plasminogen activator. Circulation 2008, 118:1442-1449.
50. Zaitsev S., Kowalska M.A., Neyman M., Carnemolla R., Tliba S., Ding B.S., et al. Targeting recombinant thrombomodulin fusion protein to red blood cells provides multifaceted thromboprophylaxis. Blood 2012, 119:4779-4785.
51. Shi G., Mukthavaram R., Kesari S., Simberg D. Distearoyl anchor-painted erythrocytes with prolonged ligand retention and circulation properties in vivo. Adv. Healthc. Mater. 2014, 3:142-148.
52. Doshi N., Prabhakarpandian B., Rea-Ramsey A., Pant K., Sundaram S., Mitragotri S. Flow and adhesion of drug carriers in blood vessels depend on their shape: a study using model synthetic microvascular networks. J. Control. Release 2010, 146:196-200.
53. Zern B.J., Chacko A.-M., Liu J., Greineder C.F., Blankemeyer E.R., Radhakrishnan R., et al. Reduction of nanoparticle avidity enhances the selectivity of vascular targeting and PET detection of pulmonary inflammation. ACS Nano 2013, 7:2461-2469.
54. Murciano J.-C., Muro S., Koniaris L., Christofidou-Solomidou M., Harshaw D.W., Albelda S.M., et al. ICAM-directed vascular immunotargeting of antithrombotic agents to the endothelial luminal surface. Blood 2003, 101:3977-3984.
55. Calderon A.J., Bhowmick T., Leferovich J., Burman B., Pichette B., Muzykantov V., et al. Optimizing endothelial targeting by modulating the antibody density and particle concentration of anti-ICAM coated carriers. J. Control. Release 2011, 150:37-44.
56. Papademetriou I.T., Garnacho C., Schuchman E.H., Muro S. In vivo performance of polymer nanocarriers dually-targeted to epitopes of the same or different receptors. Biomaterials 2013, 34:3459-3466.
57. Champion J.A., Mitragotri S. Role of target geometry in phagocytosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:4930-4934.
58. Albanese A., Tang P.S., Chan W.C. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 2012, 14:1-16.