Abstract
Antioxidant enzymes (AOEs) catalase and superoxide dismutase (SOD) detoxify harmful reactive oxygen species, but the therapeutic utility of AOEs is hindered by inadequate delivery. AOE modification by poly-ethylene glycol (PEG) and encapsulation in PEG-coated liposomes increases the AOE bioavailability and enhances protective effects in animal models. Pluronic-based micelles formed with AOEs show even more potent protective effects. Furthermore, polymeric nanocarriers (PNCs) based on PEG-copolymers protect encapsulated AOEs from proteolysis and improve delivery to the target cells, such as the endothelium lining the vascular lumen. Antibodies to endothelial determinants conjugated to AOEs or AOE carriers provide targeting and intracellular delivery. Targeted liposomes, protein conjugates and magnetic nanoparticles deliver AOEs to sites of vascular oxidative stress in the cardiovascular, pulmonary and nervous systems. Further advances in nanodevices for AOE delivery will provide a basis for the translation of this approach in the clinical domain.
Papers of special note have been highlighted as: ▪ of interest ▪▪ of considerable interest
Bibliography
- 1 Christofidou-Solomidou M, Muzykantov VR. Antioxidant strategies in respiratory medicine. Treat. Respir. Med.5(1),47–78 (2006).
- 2 Muzykantov VR. Targeting of superoxide dismutase and catalase to vascular endothelium. J. Control. Release71(1),1–21 (2001).
- 3 Yi X, Zimmerman MC, Yang R, Tong J, Vinogradov S, Kabanov AV. Pluronic-modified superoxide dismutase 1 attenuates angiotensin II-induced increase in intracellular superoxide in neurons. Free Radic. Biol. Med.49(4),548–558 (2010).
- 4 Muzykantov VR. Delivery of antioxidant enzyme proteins to the lung. Antioxid. Redox Signal.3(1),39–62 (2001).
- 5 Suarna C, Wu BJ, Choy K et al. Protective effect of vitamin E supplements on experimental atherosclerosis is modest and depends on preexisting vitamin E deficiency. Free Radic. Biol. Med.41(5),722–730 (2006).
- 6 Siekmeier R, Steffen C, Marz W. Role of oxidants and antioxidants in atherosclerosis: results of in vitro and in vivo investigations. J. Cardiovasc. Pharmacol. Ther.12(4),265–282 (2007).
- 7 Thomson MJ, Puntmann V, Kaski JC. Atherosclerosis and oxidant stress: the end of the road for antioxidant vitamin treatment? Cardiovasc. Drugs Ther.21(3),195–210 (2007).
- 8 Dziubla TD, Muro S, Muzykantov VR, Koval M. Nanoscale antioxidant therapeutics. In: Oxidative Stress, Disease and Cancer. Singh KK (Ed.). Imperial College Press, London, UK (2006).
- 9 Delles C, Miller WH, Dominiczak AF. Targeting reactive oxygen species in hypertension. Antioxid. Redox Signal.10(6),1061–1077 (2008).
- 10 Ratnam DV, Ankola DD, Bhardwaj V, Sahana DK, Kumar MN. Role of antioxidants in prophylaxis and therapy: A pharmaceutical perspective. J. Control. Release113(3),189–207 (2006).
- 11 Muzykantov VR, Atochina EN, Ischiropoulos H, Danilov SM, Fisher AB. Immunotargeting of antioxidant enzyme to the pulmonary endothelium. Proc. Natl Acad. Sci. USA93(11),5213–5218 (1996).
- 12 Muzykantov VR, Christofidou-Solomidou M, Balyasnikova I et al. Streptavidin facilitates internalization and pulmonary targeting of an anti-endothelial cell antibody (platelet-endothelial cell adhesion molecule 1): a strategy for vascular immunotargeting of drugs. Proc. Natl Acad. Sci. USA96(5),2379–2384 (1999).
- 13 Nowak K, Weih S, Metzger R et al. Immunotargeting of catalase to lung endothelium via anti-angiotensin-converting enzyme antibodies attenuates ischemia-reperfusion injury of the lung in vivo. Am. J. Physiol. Lung Cell Mol. Physiol.293(1),L162–L169 (2007).
- 14 Shuvaev VV, Tliba S, Nakada M, Albelda SM, Muzykantov VR. Platelet-endothelial cell adhesion molecule-1-directed endothelial targeting of superoxide dismutase alleviates oxidative stress caused by either extracellular or intracellular superoxide. J. Pharmacol. Exp. Ther.323(2),450–457 (2007).
- 15 Shuvaev VV, Christofidou-Solomidou M, Bhora F et al. Targeted detoxification of selected reactive oxygen species in the vascular endothelium. J. Pharmacol. Exp. Ther.331(2),404–411 (2009).
- 16 Shuvaev VV, Han J, Yu KJ et al. PECAM-targeted delivery of SOD inhibits endothelial inflammatory response. FASEB J.25(1),348–357 (2010).
- 17 Kozower BD, Christofidou-Solomidou M, Sweitzer TD et al. Immunotargeting of catalase to the pulmonary endothelium alleviates oxidative stress and reduces acute lung transplantation injury. Nat. Biotechnol.21(4),392–398 (2003).
- 18 Christofidou-Solomidou M, Scherpereel A, Wiewrodt R et al. PECAM-directed delivery of catalase to endothelium protects against pulmonary vascular oxidative stress. Am. J. Physiol. Lung Cell Mol. Physiol.285(2),L283–292 (2003).
- 19 Muro S, Wiewrodt R, Thomas A et al. A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J. Cell Sci.116(Pt 8),1599–1609 (2003).
- 20 Wiewrodt R, Thomas AP, Cipelletti L et al. Size-dependent intracellular immunotargeting of therapeutic cargoes into endothelial cells. Blood99(3),912–922 (2002).
- 21 Muro S, Cui X, Gajewski C, Murciano JC, Muzykantov VR, Koval M. Slow intracellular trafficking of catalase nanoparticles targeted to ICAM-1 protects endothelial cells from oxidative stress. Am. J. Physiol. Cell Physiol.285(5),C1339–C1347 (2003).
- 22 Muro S, Gajewski C, Koval M, Muzykantov VR. ICAM-1 recycling in endothelial cells: a novel pathway for sustained intracellular delivery and prolonged effects of drugs. Blood105(2),650–658 (2005).
- 23 Stenesh J. Biochemistry. Plenum, NY, USA (1998).
- 24 Papi A, Chicca M, Pandit A, Caramori G, Geoffrey JL, Steven DS. Oxidants and antioxidants/Antioxidants, Nonenzymatic. In: Encyclopedia of Respiratory Medicine. Academic Press, Oxford, UK, 266–271 (2006).
- 25 Quideau S, Deffieux D, Douat-Casassus C, Pouysegu L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem. Int. Ed. Engl.50(3),586–621 (2011).
- 26 Sandur SK, Ichikawa H, Pandey MK et al. Role of pro-oxidants and antioxidants in the anti-inflammatory and apoptotic effects of curcumin (diferuloylmethane). Free Radic. Biol. Med.43(4),568–580 (2007).
- 27 Darvesh AS, Aggarwal BB, Bishayee A. Curcumin and liver cancer: a review. Curr. Pharm. Biotechnol. (2011) (Epub ahead of print).
- 28 Pezzuto JM. The phenomenon of resveratrol: redefining the virtues of promiscuity. Ann. NY Acad. Sci.1215(1),123–130 (2011).
- 29 Freeman BA, Young SL, Crapo JD. Liposome-mediated augmentation of superoxide dismutase in endothelial cells prevents oxygen injury. J. Biol. Chem.258(20),12534–12542 (1983).
- 30 Chorny M, Hood E, Levy RJ, Muzykantov VR. Endothelial delivery of antioxidant enzymes loaded into non-polymeric magnetic nanoparticles. J. Control. Release146(1),144–151 (2010).▪ Nonsolvent, nonshear preparation of magnetically active nanocarriers efficiently load active catalase or SOD, provide proteins with protection from proteolysis and protect cells from oxidative damage from hydrogen peroxide in vitro.
- 31 Batrakova EV, Li S, Reynolds AD et al. A macrophage-nanozyme delivery system for Parkinson’s disease. Bioconjug. Chem.18(5),1498–1506 (2007).
- 32 Vertegel AA, Reukov V, Maximov V. Enzyme-nanoparticle conjugates for biomedical applications. Methods Mol. Biol.679,165–182 (2011).
- 33 Nagami H, Yoshimoto N, Umakoshi H, Shimanouchi T, Kuboi R. Liposome-assisted activity of superoxide dismutase under oxidative stress. J. Biosci. Bioeng.99(4),423–428 (2005).
- 34 Stone WL, Smith M. Therapeutic uses of antioxidant liposomes. Mol. Biotechnol.27(3),217–230 (2004).
- 35 Gonnet M, Lethuaut L, Boury F. New trends in encapsulation of liposoluble vitamins. J. Control. Release146(3),276–290 (2010).
- 36 Alipour M, Omri A, Smith MG, Suntres ZE. Prophylactic effect of liposomal N-acetylcysteine against LPS-induced liver injuries. J. Endo. Res.13(5),297–304 (2007).
- 37 Mitsopoulos P, Omri A, Alipour M, Vermeulen N, Smith MG, Suntres ZE. Effectiveness of liposomal-N-acetylcysteine against LPS-induced lung injuries in rodents. Int. J. Pharma.363(1–2),106–111 (2008).▪▪ Liposomal delivery of antioxidants provided protection against LPS in multiple lung injury measures.
- 38 Fan J, Shek PN, Suntres ZE, Li YH, Oreopoulos GD, Rotstein OD. Liposomal antioxidants provide prolonged protection against acute respiratory distress syndrome. Surgery128(2),332–338 (2000).
- 39 Mukhopadhyay S, Mukherjee S, Stone WL, Smith M, Das SK. Role of MAPK/AP-1 signaling pathway in the protection of CEES-induced lung injury by antioxidant liposome. Toxicology261(3),143–151 (2009).
- 40 Bansal SS, Goel M, Aqil F, Vadhanam MV, Gupta RC. Advanced drug-delivery systems of curcumin for cancer chemoprevention. Cancer Prev. Res. (Phila).4(8),1158–1171 (2011).
- 41 Thangapazham RL, Puri A, Tele S, Blumenthal R, Maheshwari RK. Evaluation of a nanotechnology-based carrier for delivery of curcumin in prostate cancer cells. Int. J. Oncol.32(5),1119–1123 (2008).
- 42 Hung CF, Chen JK, Liao MH, Lo HM, Fang JY. Development and evaluation of emulsion-liposome blends for resveratrol delivery. J. Nanosci. Nanotechnol.6(9–10),2950–2958 (2006).
- 43 Narayanan NK, Nargi D, Randolph C, Narayanan BA. Liposome encapsulation of curcumin and resveratrol in combination reduces prostate cancer incidence in PTEN knockout mice. Int. J. Cancer125(1),1–8 (2009).
- 44 Williams SR, Lepene BS, Thatcher CD, Long TE. Synthesis and characterization of poly(ethylene glycol)-glutathione conjugate self-assembled nanoparticles for antioxidant delivery. Biomacromolecules10(1),155–161 (2009).
- 45 Tanswell AK, Freeman BA. Liposome-entrapped antioxidant enzymes prevent lethal O2 toxicity in the newborn rat. J. Appl. Physiol.63(1),347–352 (1987).
- 46 Briscoe P, Caniggia I, Graves A et al. Delivery of superoxide dismutase to pulmonary epithelium via pH-sensitive liposomes. Am. J. Physiol.268(3 Pt 1),L374–380 (1995).
- 47 Laursen JB, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, Harrison DG. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation95(3),588–593 (1997).
- 48 Corvo LM, Jorge JCS, van’t Hof R, Cruz MEM, Crommelin DJA, Storm G. Superoxide dismutase entrapped in long-circulating liposomes: formulation design and therapeutic activity in rat adjuvant arthritis. Biochim. Biophys. Acta1564(1),227–236 (2002).
- 49 Gaspar MM, Martins MB, Corvo ML, Cruz ME. Design and characterization of enzymosomes with surface-exposed superoxide dismutase. Biochim. Biophys. Acta1609(2),211–217 (2003).
- 50 Gaspar MM, Boerman OC, Laverman P, Corvo ML, Storm G, Cruz ME. Enzymosomes with surface-exposed superoxide dismutase: in vivo behaviour and therapeutic activity in a model of adjuvant arthritis. J. Control. Release117(2),186–195 (2007).
- 51 Brynskikh AM, Zhao Y, Mosley RL et al. Macrophage delivery of therapeutic nanozymes in a murine model of Parkinson’s disease. Nanomedicine5(3),379–396 (2010).
- 52 Rosenbaugh EG, Roat JW, Gao L et al. The attenuation of central angiotensin II-dependent pressor response and intra-neuronal signaling by intracarotid injection of nanoformulated copper/zinc superoxide dismutase. Biomaterials31(19),5218–5226 (2010).
- 53 Batrakova EV, Li S, Miller DW, Kabanov AV. Pluronic P85 increases permeability of a broad spectrum of drugs in polarized BBMEC and Caco-2 cell monolayers. Pharm. Res.16(9),1366–1372 (1999).
- 54 Batrakova EV, Miller DW, Li S, Alakhov VY, Kabanov AV, Elmquist WF. Pluronic P85 enhances the delivery of digoxin to the brain: in vitro and in vivo studies. J. Pharmacol. Exp. Ther.296(2),551–557 (2001).
- 55 Batrakova EV, Zhang Y, Li Y et al. Effects of pluronic P85 on GLUT1 and MCT1 transporters in the blood-brain barrier. Pharm. Res.21(11),1993–2000 (2004).
- 56 Chorny M, Fishbein I, Alferiev I, Levy RJ. Magnetically responsive biodegradable nanoparticles enhance adenoviral gene transfer in cultured smooth muscle and endothelial cells. Mol. Pharm.6(5),1380–1387 (2009).
- 57 Shuvaev VV, Tliba S, Pick J et al. Modulation of endothelial targeting by size of antibody-antioxidant enzyme conjugates. J. Control. Release149(3),236–241 (2011).
- 58 Villano D, Fernandez-Pachon MS, Moya ML, Troncoso AM, Garcia-Parrilla MC. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta71(1),230–235 (2007).
- 59 Rock CL, Jacob RA, Bowen PE. Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E, and the carotenoids. J. Am. Diet Assoc.96(7),693–702; quiz 703–694 (1996).
- 60 de la Lastra CA, Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem. Soc. Trans.35(Pt 5),1156–1160 (2007).
- 61 Wattamwar PP, Hardas SS, Butterfield DA, Anderson KW, Dziubla TD. Tuning of the pro-oxidant and antioxidant activity of trolox through the controlled release from biodegradable poly(trolox ester) polymers. Acta Biomaterialia (2011) (In Press).
- 62 Kumar V, Prud’Homme RK. Thermodynamic limits on drug loading in nanoparticle cores. J. Pharm. Sci.97(11),4904–4914 (2008).
- 63 De Villiers MM, Aramwit P, Kwon GS. Nanotechnology in Drug Delivery. Springer, AAPS Press, NY and VA, USA (2009).
- 64 Gref R, Minamitake Y, Peracchia MT, Trubetskoy V, Torchilin V, Langer R. Biodegradable long-circulating polymeric nanospheres. Science263(5153),1600–1603 (1994).
- 65 Leonarduzzi G, Testa G, Sottero B, Gamba P, Poli G. Design and development of nanovehicle-based delivery systems for preventive or therapeutic supplementation with flavonoids. Curr. Med. Chem.17(1),74–95.
- 66 Kumar V, Hong SY, Maciag AE et al. Stabilization of the nitric oxide (NO) prodrugs and anticancer leads, PABA/NO and double JS-K, through incorporation into PEG-protected nanoparticles. Mol. Pharm.7(1),291–298 (2010).
- 67 Wattamwar PP, Mo YQ, Wan R, Palli R, Zhang QW, Dziubla TD. Antioxidant activity of degradable polymer poly(trolox ester) to suppress oxidative stress injury in the cells. Adv. Func. Mater.20(1),147–154 (2010).
- 68 Fleming C, Maldjian A, Da Costa D et al. A carbohydrate-antioxidant hybrid polymer reduces oxidative damage in spermatozoa and enhances fertility. Nat. Chem. Biol.1(5),270–274 (2005).
- 69 Spizzirri UG, Iemma F, Puoci F et al. Synthesis of antioxidant polymers by grafting of gallic acid and catechin on gelatin. Biomacromolecules10(7),1923–1930 (2009).
- 70 Wang Y, Singh A, Xu P, Pindrus MA, Blasioli DJ, Kaplan DL. Expansion and osteogenic differentiation of bone marrow-derived mesenchymal stem cells on a vitamin C functionalized polymer. Biomaterials27(17),3265–3273 (2006).
- 71 Dziubla TD, Karim A, Muzykantov VR. Polymer nanocarriers protecting active enzyme cargo against proteolysis. J. Control. Release102(2),427–439 (2005).
- 72 Giovagnoli S, Luca G, Casaburi I et al. Long-term delivery of superoxide dismutase and catalase entrapped in poly(lactide-co-glycolide) microspheres: In vitro effects on isolated neonatal porcine pancreatic cell clusters. J. Control. Release107(1),65–77 (2005).
- 73 Seshadri G, Sy JC, Brown M et al. The delivery of superoxide dismutase encapsulated in polyketal microparticles to rat myocardium and protection from myocardial ischemia-reperfusion injury. Biomaterials31(6),1372–1379 (2010).
- 74 Fiore VF, Lofton MC, Roser-Page S et al. Polyketal microparticles for therapeutic delivery to the lung. Biomaterials31(5),810–817 (2010).
- 75 Dziubla TD, Shuvaev VV, Hong NK et al. Endothelial targeting of semi-permeable polymer nanocarriers for enzyme therapies. Biomaterials29(2),215–227 (2008).▪▪ Degradable polymer nanocarriers modified to accommodate endothelial targeting antibodies successfully load active catalase, bind to endothelial cells and impart antioxidant protection.
- 76 Reddy MK, Wu L, Kou W, Ghorpade A, Labhasetwar V. Superoxide dismutase-loaded PLGA nanoparticles protect cultured human neurons under oxidative stress. Appl. Biochem. Biotechnol.151(2–3),565–577 (2008).
- 77 Reddy MK, Labhasetwar V. Nanoparticle-mediated delivery of superoxide dismutase to the brain: an effective strategy to reduce ischemia-reperfusion injury. FASEB J.23(5),1384–1395 (2009).
- 78 Muro S, Dziubla T, Qiu W et al. Endothelial targeting of high-affinity multivalent polymer nanocarriers directed to intercellular adhesion molecule 1. J. Pharmacol. Exp. Ther.317(3),1161–1169 (2006).
- 79 Yan M, Du JJ, Gu Z et al. A novel intracellular protein delivery platform based on single-protein nanocapsules. Nat. Nanotechnol.5(1),48–53 (2010).▪ Novel biodegradable protein delivery nanocapsules.
- 80 Kim D, Kim E, Kim J et al. Direct synthesis of polymer nanocapsules with a noncovalently tailorable surface. Angew. Chem. Int. Ed.46(19),3471–3474 (2007).
- 81 Kim E, Kim D, Jung H et al. Facile, Template-Free Synthesis of Stimuli-Responsive Polymer Nanocapsules for Targeted Drug Delivery. Angew. Chem. Int. Ed.49(26),4405–4408 (2010).
- 82 Photos PJ, Bacakova L, Discher B, Bates FS, Discher DE. Polymer vesicles in vivo: correlations with PEG molecular weight. J. Control. Release90(3),323–334 (2003).
- 83 Saad M, Garbuzenko OB, Ber E et al. Receptor targeted polymers, dendrimers, liposomes: which nanocarrier is the most efficient for tumor-specific treatment and imaging? J. Control. Release130(2),107–114 (2008).
- 84 Dziubla TD, Karim A, Muzykantov VR. Polymer nanocarriers protecting active enzyme cargo against proteolysis. J. Control. Release102(2),427–439 (2005).
- 85 Ahmed F, Discher DE. Self-porating polymersomes of PEG-PLA and PEG-PCL: hydrolysis-triggered controlled release vesicles. J. Control. Release96(1),37–53 (2004).
- 86 Zarif L. Elongated supramolecular assemblies in drug delivery. J. Control. Release81(1–2),7–23 (2002).
- 87 Bianco A, Kostarelos K, Prato M. Opportunities and challenges of carbon-based nanomaterials for cancer therapy. Expert Opin. Drug Deliv.5(3),331–342 (2008).
- 88 Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc. Natl Acad. Sci. USA103(13),4930–4934 (2006).▪▪ Demonstrates that the effect of high aspect ratio and shape on inhibition of phagocytosis of drug-delivery particles is possible by minimizing the size-normalized curvature of particles.
- 89 Muro S, Garnacho C, Champion JA 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.16(8),1450–1458 (2008).
- 90 Xu S, Nie Z, Seo M et al. Generation of monodisperse particles by using microfluidics: control over size, shape, and composition. Angew. Chem. Int. Ed. Engl.44(5),724–728 (2005).
- 91 Dendukuri D, Pregibon DC, Collins J, Hatton TA, Doyle PS. Continuous-flow lithography for high-throughput microparticle synthesis. Nat. Mater.5(5),365–369 (2006).
- 92 Gratton SE, Pohlhaus PD, Lee J, Guo J, Cho MJ, Desimone JM. Nanofabricated particles for engineered drug therapies: a preliminary biodistribution study of PRINT nanoparticles. J. Control. Release121(1–2),10–18 (2007).▪ Investigates cellular internalization pathways of varied size, shape and surface charge of nanofabricated particles.
- 93 Rolland JP, Maynor BW, Euliss LE, Exner AE, Denison GM, DeSimone JM. Direct fabrication and harvesting of monodisperse, shape-specific nanobiomaterials. J. Am. Chem. Soc.127(28),10096–10100 (2005).
- 94 Gratton SE, Napier ME, Ropp PA, Tian S, Desimone JM. Microfabricated particles for engineered drug therapies: elucidation into the mechanisms of cellular internalization of PRINT particles. Pharm. Res.25(12),2845–2852 (2008).
- 95 Lee JC, Bermudez H, Discher BM et al. Preparation, stability, and in vitro performance of vesicles made with diblock copolymers. Biotechnol. Bioeng.73(2),135–145 (2001).
- 96 Discher DE, Eisenberg A. Polymer vesicles. Science297(5583),967–973 (2002).
- 97 Lee JC, Wong DT, Discher DE. Direct measures of large, anisotropic strains in deformation of the erythrocyte cytoskeleton. Biophys. J.77(2),853–864 (1999).
- 98 Dalhaimer P, Bates FS, Discher DE. Single molecule visualization of stable, stiffness-tunable, flow-conforming worm micelles. Macromolecules36(18),6873–6877 (2003).
- 99 Simone EA, Dziubla TD, Colon-Gonzalez F, Discher DE, Muzykantov VR. Effect of polymer amphiphilicity on loading of a therapeutic enzyme into protective filamentous and spherical polymer nanocarriers. Biomacromolecules8(12),3914–3921 (2007).
- 100 Simone EA, Dziubla TD, Discher DE, Muzykantov VR. Filamentous polymer nanocarriers of tunable stiffness that encapsulate the therapeutic enzyme catalase. Biomacromolecules10(6),1324–1330 (2009).
- 101 Petros RA, Ropp PA, DeSimone JM. Reductively labile PRINT particles for the delivery of doxorubicin to HeLa cells. J. Am. Chem. Soc.130(15),5008–5009 (2008).
- 102 Kelly JY, DeSimone JM. Shape-specific, monodisperse nano-molding of protein particles. J. Am. Chem. Soc.130(16),5438–5439 (2008).
- 103 Castillo J, Curley J, Hotz J et al. Glucocorticoids prolong rat sciatic nerve blockade in vivo from bupivacaine microspheres. Anesthesiology85(5),1157–1166 (1996).
- 104 Hickey T, Kreutzer D, Burgess DJ, Moussy F. Dexamethasone/PLGA microspheres for continuous delivery of an anti-inflammatory drug for implantable medical devices. Biomaterials23(7),1649–1656 (2002).
- 105 Simone EA, Dziubla TD, Arguiri E et al. Loading PEG-catalase into filamentous and spherical polymer nanocarriers. Pharm. Res.26(1),250–260 (2009).
- 106 Kumar N, Ravikumar MN, Domb AJ. Biodegradable block copolymers. Adv. Drug Deliv. Rev.53(1),23–44 (2001).
- 107 Shive MS, Anderson JM. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv. Drug Deliv. Rev.28(1),5–24 (1997).
- 108 Siepmann J, Gopferich A. Mathematical modeling of bioerodible, polymeric drug delivery systems. Adv. Drug Deliv. Rev.48(2–3),229–247 (2001).
- 109 Hanes J, Chiba M, Langer R. Synthesis and characterization of degradable anhydride-co-imide terpolymers containing trimellitylimido-L-tyrosine: novel polymers for drug delivery. Macromolecules29(16),5279–5287 (1996).
- 110 Leong KW, Brott BC, Langer R. Bioerodible polyanhydrides as drug-carrier matrices. I: Characterization, degradation, and release characteristics. J. Biomed. Mater. Res.19(8),941–955 (1985).
- 111 Tabata Y, Gutta S, Langer R. Controlled delivery systems for proteins using polyanhydride microspheres. Pharm. Res.10(4),487–496 (1993).
- 112 Carino GP, Jacob JS, Mathiowitz E. Nanosphere based oral insulin delivery. J. Control. Release65(1–2),261–269 (2000).
- 113 Fu J, Wu C. Laser light scattering of the degradation of poly(sebacic anhydride) nanoparticles. J. Polymer Sci. B Polymer Phys.39(6),703–708 (2001).
- 114 Pfeifer BA, Burdick JA, Langer R. Formulation and surface modification of poly(ester-anhydride) micro- and nanospheres. Biomaterials26(2),117–124 (2005).
- 115 Li S, Garreau H, Vert M. Structure-property relationships in the case of the degradation of solid aliphatic poly-(α-hydroxy acids) in aqueous media part 3 influence of the morphology of poly(L-lactic acid). J. Mat. Sci.1(4),198–206 (1990).
- 116 Li S, Garreau H, Vert M: Structure-property relationships in the case of the degradation of solid aliphatic poly-(α-hydroxy acids) in aqueous media. Part 1 Poly(DL-lactic acid). J. Mat. Sci.1(3),123 (1990).
- 117 Vert M, Li SM, Garreau H. Attempts to map the structure and degradation characteristics of aliphatic polyesters derived from lactic and glycolic acids. J. Biomater. Sci. Polym. Ed.6(7),639–649 (1994).
- 118 Geng Y, Discher DE. Hydrolytic degradation of poly(ethylene oxide)-block-polycaprolactone worm micelles. J. Am. Chem. Soc.127(37),12780–12781 (2005).
- 119 Shih C. A graphical method for the determination of the mode of hydrolysis of biodegradable polymers. Pharm. Res.12(12),2036–2060 (1995).
- 120 Ahmed F, Pakunlu RI, Srinivas G et al. Shrinkage of a rapidly growing tumor by drug-loaded polymersomes: pH-triggered release through copolymer degradation. Mol. Pharm.3(3),340–350 (2006).
- 121 Gopferich A. Mechanisms of polymer degradation and erosion. Biomaterials17(2),103–114 (1996).
- 122 Li S, Molina I, Martinez MB, Vert M. Hydrolytic and enzymatic degradations of physically crosslinked hydrogels prepared from PLA/PEO/PLA triblock copolymers. J. Mater. Sci. Mater. Med.13(1),81–86 (2002).
- 123 MacDonald RT, McCarthy SP, Gross RA. Enzymatic degradability of poly(lactide): effects of chain stereochemistry and material crystallinity. Macromolecules29(23),7356–7361 (1996).
- 124 Tokiwa Y, Jarerat A. Biodegradation of poly(L-lactide). Biotechnol. Lett.26(10),771–777 (2004).
- 125 Klibanov AL, Maruyama K, Torchilin VP, Huang L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett.268(1),235–237 (1990).
- 126 Bermudez H, Brannan AK, Hammer DA, Bates FS, Discher DE. Molecular weight dependence of polymersome membrane structure, elasticity, and stability. Macromolecules35(21),8203–8208 (2002).
- 127 Geng Y, Dalhaimer P, Cai S et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nano.2(4),249–255 (2007).
- 128 Bedu-Addo FK, Tang P, Xu Y, Huang L. Interaction of polyethyleneglycol-phospholipid conjugates with cholesterol-phosphatidylcholine mixtures: sterically stabilized liposome formulations. Pharm. Res.13(5),718–724 (1996).
- 129 Koval M, Preiter K, Adles C, Stahl PD, Steinberg TH. Size of IgG-opsonized particles determines macrophage response during internalization. Exp. Cell Res.242(1),265–273 (1998).
- 130 Brewer JM, Tetley L, Richmond J, Liew FY, Alexander J. Lipid vesicle size determines the Th1 or Th2 response to entrapped antigen. J. Immunol.161(8),4000–4007 (1998).
- 131 Romero EL, Morilla MJ, Regts J, Koning GA, Scherphof GL. On the mechanism of hepatic transendothelial passage of large liposomes. FEBS Lett.448(1),193–196 (1999).
- 132 Champion JA, Mitragotri S. Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res.26(1),244–249 (2008).
- 133 Izumisawa T, Hattori Y, Date M, Toma K, Maitani Y. Cell line-dependent internalization pathways determine DNA transfection efficiency of decaarginine-PEG-lipid. Int. J. Pharm.404(1–2),264–270 (2010).
- 134 Shi F, Wasungu L, Nomden A et al. Interference of poly(ethylene glycol)-lipid analogues with cationic-lipid-mediated delivery of oligonucleotides; role of lipid exchangeability and non-lamellar transitions. Biochem. J.366(Pt 1),333–341 (2002).
- 135 Aoki H, Fujita M, Sun CQ, Fuji K, Miyajima K. High-efficiency entrapment of superoxide dismutase into cationic liposomes containing synthetic aminoglycolipid. Chem. Pharm. Bull.45(8),1327–1331 (1997).
- 136 Atochina EN, Balyasnikova IV, Danilov SM, Granger DN, Fisher AB, Muzykantov VR. Immunotargeting of catalase to ACE or ICAM-1 protects perfused rat lungs against oxidative stress. Am. J. Physiol.275(4 Pt 1),L806–817 (1998).
- 137 Deneke SM. Thiol-based antioxidants. Curr. Top. Cell Regul.36,151–180 (2000).
- 138 Pedersen PJ, Adolph SK, Subramanian AK et al. Liposomal formulation of retinoids designed for enzyme triggered release. J. Med. Chem.53(9),3782–3792 (2010).
- 139 Trapasso E, Cosco D, Celia C, Fresta M, Paolino D. Retinoids: new use by innovative drug-delivery systems. Expert Opin. Drug Deliv.6(5),465–483 (2009).
- 140 Wegmann Jr, Krucker M, Bachmann S et al. Characterization of lycopene nanoparticles combining solid-state and suspended-state NMR spectroscopy. J. Agricult. Food Chem.50(26),7510–7514 (2002).
- 141 Palozza P, Muzzalupo R, Trombino S, Valdannini A, Picci N. Solubilization and stabilization of [beta]-carotene in niosomes: delivery to cultured cells. Chem. Phys. Lipids139(1),32–42 (2006).
- 142 Robb EL, Page MM, Wiens BE, Stuart JA. Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochem. Biophys. Res. Comm.367(2),406–412 (2008).
- 143 Mignet N, Seguin J, Romano MR et al. Development of a liposomal formulation of the natural flavonoid fisetin. Int. J. Pharm. (2011) (In Press).
- 144 Yuan Z-p, Chen L-j, Fan L-y et al. Liposomal quercetin efficiently suppresses growth of solid tumors in murine models. Clin. Cancer Res.12(10),3193–3199 (2006).
- 145 Gao L, Liu G, Wang X, Liu F, Xu Y, Ma J. Preparation of a chemically stable quercetin formulation using nanosuspension technology. Int. J. Pharm.404(1–2),231–237 (2010).
- 146 Nilsson L, Löf D, BergenstÃ¥hl Br. Phenolic acid nanoparticle formation in iron-containing aqueous solutions. J. Agricult. Food Chem.56(23),11453–11457 (2008).
- 147 Coimbra M, Isacchi B, van Bloois L et al. Improving solubility and chemical stability of natural compounds for medicinal use by incorporation into liposomes. Int. J. Pharm. (2011) (In Press).
- 148 Teskac K, Kristl J. The evidence for solid lipid nanoparticles mediated cell uptake of resveratrol. Int. J. Pharm.390(1),61–69 (2009).
- 149 Frozza RL, Bernardi A, Paese K et al. Characterization of trans-resveratrol-loaded lipid-core nanocapsules and tissue distribution studies in rats. J. Biomed. Nanotechnol.6(6),694–703 (2011).
- 150 Lee W-C, Tsai T-H. Preparation and characterization of liposomal coenzyme Q10 for in vivo topical application. Int. J. Pharm.395(1–2),78–83 (2010).
- 151 Beg S, Javed S, Kohli K. Bioavailability enhancement of coenzyme Q10: an extensive review of patents. Recent Pat. Drug Deliv. Formul.4(3),245–255 (2010).
- 152 Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv. Drug Deliv. Rev.61(6),428–437 (2009).
- 153 Carnemolla R, Shuvaev VV, Muzykantov VR. Targeting antioxidant and antithrombotic biotherapeutics to endothelium. Semin. Thromb. Hemost.36(3),332–342 (2010).
- 154 Harush-Frenkel O, Altschuler Y, Benita S. Nanoparticle-cell interactions: drug delivery implications. Crit. Rev. Ther. Drug Carrier Syst.25(6),485–544 (2008).
- 155 Sun X, Zhang N. Cationic polymer optimization for efficient gene delivery. Mini Rev. Med. Chem.10(2),108–125 (2010).
- 156 Simone EA, Dziubla TD, Muzykantov VR. Polymeric carriers: role of geometry in drug delivery. Expert Opin. Drug Deliv.5(12),1283–1300 (2008).▪ Recent review on the role that the size, shape and surface modifications play on polymer carriers in vitro and in vivo localization and drug delivery.
- 157 Tao L, Hu W, Liu Y, Huang G, Sumer BD, Gao J. Shape-specific polymeric nanomedicine: emerging opportunities and challenges. Exp. Biol. Med.236(1),20–29 (2011).
- 158 Caldorera-Moore M, Guimard N, Shi L, Roy K. Designer nanoparticles: incorporating size, shape and triggered release into nanoscale drug carriers. Expert Opin. Drug Deliv.7(4),479–495 (2010).
- 159 Hillaireau H, Couvreur P. Nanocarriers’ entry into the cell: relevance to drug delivery. Cell Mol. Life Sci.66(17),2873–2896 (2009).
- 160 Siepmann J, Peppas NA. Modeling of drug release from delivery systems based on hydroxypropyl methylcellulose (HPMC). Adv. Drug Deliv. Rev.48(2–3),139–157 (2001).
- 161 Gao W, Chan JM, Farokhzad OC. pH-Responsive nanoparticles for drug delivery. Mol. Pharm.7(6),1913–1920 (2010).
- 162 Yoo JW, Chambers E, Mitragotri S. Factors that control the circulation time of nanoparticles in blood: challenges, solutions and future prospects. Curr. Pharm. Des.16(21),2298–2307 (2010).