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Review

Application of PLGA nano/microparticle delivery systems for immunomodulation and prevention of allotransplant rejection

, , , , ORCID Icon & ORCID Icon
Pages 767-780 | Received 25 Aug 2019, Accepted 24 Mar 2020, Published online: 04 Apr 2020

References

  • Watson C, Dark J. Organ transplantation: historical perspective and current practice. Br J Anaesth. 2012;108(suppl_1):i29–i42.
  • Quinby WC. The function of the kidney when deprived of its nerves. J Exp Med. 1916;23(4):535.
  • Simonsen M, Buemann J, Gammeltoft A, et al. Biological incompatibility in kidney transplantation in dogs: I. Experimental and morphological investigations. Acta Pathologica Microbiologica Scand. 1953;32(1):1–35.
  • Murray J, Lang S, Miller B, et al. Prolonged functional survival of renal autotransplants in the dog. Surg Gynecology Obstetrics. 1956;103(1):15.
  • Hume DM, Merrill JP, Miller BF, et al. Experiences with renal homotransplantation in the human: report of nine cases. J Clin Invest. 1955;34(2):327–382.
  • Ratcliffe P, Dudley C, Higgins R, et al. Randomised controlled trial of steroid withdrawal in renal transplant recipients receiving triple immunosuppression. Lancet. 1996;348(9028):643–648.
  • Calne R, Williams R. Liver transplantation in man—I, observations on technique and organization in five cases. Br Med J. 1968;4(5630):535–540.
  • Calne R, Evans D, Herbertson B, et al. Survival after renal transplantation in man: an interim report on 54 consecutive transplants. Br Med J. 1968;2(5602):404.
  • Lower RR, Stofer RC, Shumway NE. A study of pulmonary valve autotransplantation. Surgery. 1960;48(6):1090–1100.
  • Coulson AS, Zeitman VH, Stinson EB, et al. Immunodepressive serum treatment of acute heart transplant rejection. Br Med J. 1976;1(6012):749.
  • Allan JS, Madsen JC. Recent advances in the immunology of chronic rejection. Curr Opin Nephrol Hypertens. 2002;11(3):315–321.
  • Denton MD, Magee CC, Sayegh MH. Immunosuppressive strategies in transplantation. Lancet. 1999;353(9158):1083–1091.
  • Timm S, Otto C, Begrich D, et al. Immunogenicity of parathyroid allografts in the rat: immunosuppressive dosages effective in passenger leukocyte-rich small bowel transplants are not effective in parathyroid gland transplants with few passenger leukocytes. Langenbecks Arch Surg. 2004;389(1):46–52.
  • Kerman RH, Orosz CC, Lorber MI. Clinical relevance of anti-HLA antibodies pre and post transplant. Am J Med Sci. 1997;313(5):275–278.
  • Singh N, Pirsch J, Samaniego M. Antibody-mediated rejection: treatment alternatives and outcomes. Transplantation Rev. 2009;23(1):34–46.
  • Rocha PN, Plumb TJ, Crowley SD, et al. Effector mechanisms in transplant rejection. Immunol Rev. 2003;196(1):51–64.
  • Libby P, Pober JS. Chronic rejection. Immunity. 2001;14(4):387–397.
  • Racusen LC. Immunopathology of organ transplantation. Springer Semin Immunopathol 2003;25:141–165.
  • Fairchild RL. The Yin and Yang of IFN‐γ in Allograft Rejection. Am J Transplant. 2003;3(8):913–914.
  • Chapman J. Optimizing the long-term outcome of renal transplants: opportunities created by sirolimus. Transplant proc. 2003;35(S3):67S–72S.
  • Savikko J, von Willebrand E, Häyry P. Leflunomide analogue FK778 is vasculoprotective independent of its immunosuppressive effect: potential applications for restenosis and chronic rejection. Transplantation. 2003;76(3):455–458.
  • Toungouz M, Donckier V, Goldman M. Tolerance induction in clinical transplantation: the pending questions. Transplantation. 2003;75(9):58S–60S.
  • Wood KJ, Bushell A, Hester J. Regulatory immune cells in transplantation. Nat Rev Immunol. 2012;12(6):417.
  • Brown K, Sacks S, Wong W. Coexpression of donor peptide/recipient MHC complex and intact donor MHC: evidence for a link between the direct and indirect pathways. Am J Transplant. 2011;11(4):826–831.
  • Shoskes DA, Wood KJ. Indirect presentation of MHC antigens in transplantation. Immunol Today. 1994;15(1):32–38.
  • Illigens BM, Yamada A, Fedoseyeva EV, et al. The relative contribution of direct and indirect antigen recognition pathways to the alloresponse and graft rejection depends upon the nature of the transplant. Hum Immunol. 2002;63(10):912–925.
  • Herrera OB, Golshayan D, Tibbott R, et al. A novel pathway of alloantigen presentation by dendritic cells. J Immunol. 2004;173(8):4828–4837.
  • Afzali B, Lechler R, Hernandez‐Fuentes M. Allorecognition and the alloresponse: clinical implications. Tissue Antigens. 2007;69(6):545–556.
  • Italia JL, Bhardwaj V, Kumar MR. Disease, destination, dose and delivery aspects of ciclosporin: the state of the art. Drug Discov Today. 2006;11(17–18):846–854.
  • Kino T, Hatanaka H, Miyata S, et al. FK-506, a novel immunosuppressant isolated from a Streptomyces. J Antibiot (Tokyo). 1987;40(9):1256–1265.
  • Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol. 2009;4(2):481–508.
  • Ayres R, Dousset B, Wixon S, et al. Peripheral neurotoxicity with tacrolimus. Lancet. 1994;343(8901):862–863.
  • Platz K-P, Mueller AR, Blumhardt G, et al. Nephrotoxicity following orthotopic liver transplantation. A comparison between cyclosporine and FK506. Transplantation. 1994;58(2):170–178.
  • Saunders RN, Metcalfe MS, Nicholson ML. Rapamycin in transplantation: a review of the evidence. Kidney Int. 2001;59(1):3–16.
  • R, Turnquist HR, Taner T, et al. Use of rapamycin in the induction of tolerogenic dendritic cells. In: Dendritic Cells. Springer, 2009. p. 215–232.
  • Hackstein H, Taner T, Zahorchak AF, et al. Rapamycin inhibits IL-4—induced dendritic cell maturation in vitro and dendritic cell mobilization and function in vivo. Blood. 2003;101(11):4457–4463.
  • Turnquist HR, Raimondi G, Zahorchak AF, et al. Rapamycin-conditioned dendritic cells are poor stimulators of allogeneic CD4+ T cells, but enrich for antigen-specific Foxp3+ T regulatory cells and promote organ transplant tolerance. J Immunol. 2007;178(11):7018–7031.
  • Jhunjhunwala S, Balmert SC, Raimondi G, et al. Controlled release formulations of IL-2, TGF-β1 and rapamycin for the induction of regulatory T cells. J Control Release. 2012;159(1):78–84.
  • Battaglia M, Stabilini A, Draghici E, et al. Rapamycin and interleukin-10 treatment induces T regulatory type 1 cells that mediate antigen-specific transplantation tolerance. Diabetes. 2006;55(1):40–49.
  • Strauss L, Whiteside TL, Knights A, et al. Selective survival of naturally occurring human CD4+ CD25+ Foxp3+ regulatory T cells cultured with rapamycin. J Immunol. 2007;178(1):320–329.
  • Battaglia M, Stabilini A, Migliavacca B, et al. Rapamycin promotes expansion of functional CD4+ CD25+ FOXP3+ regulatory T cells of both healthy subjects and type 1 diabetic patients. J Immunol. 2006;177(12):8338–8347.
  • Battaglia M, Stabilini A, Roncarolo M-G. Rapamycin selectively expands CD4+ CD25+ FoxP3+ regulatory T cells. Blood. 2005;105(12):4743–4748.
  • Lee H, Huh K, Kim Y, et al., editors. Sirolimus-induced pneumonitis after renal transplantation: a single-center experience. Transplant proc. 2012;44(1):161–163.
  • Pinsky B, Takemoto S, Lentine K, et al. Transplant outcomes and economic costs associated with patient noncompliance to immunosuppression. Am J Transplant. 2009;9(11):2597–2606.
  • Dew MA, DiMartini AF, Dabbs ADV, et al. Rates and risk factors for nonadherence to the medical regimen after adult solid organ transplantation. Transplantation. 2007;83(7):858–873.
  • Bosma OH, Vermeulen KM, Verschuuren EA, et al. Adherence to immunosuppression in adult lung transplant recipients: prevalence and risk factors. J Heart Lung Transplant. 2011;30(11):1275–1280.
  • Fisher JD, Acharya AP, Little SR. Micro and nanoparticle drug delivery systems for preventing allotransplant rejection. Clin Immunol. 2015;160(1):24–35.
  • Ruiz P, Maldonado P, Hidalgo Y, et al. Transplant tolerance: new insights and strategies for long-term allograft acceptance. Clin Dev Immunol. 2013;210506.
  • Hubbell JA, Thomas SN, Swartz MA. Materials engineering for immunomodulation. Nature. 2009;462(7272):449.
  • Danhier F, Ansorena E, Silva JM, et al. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release. 2012;161(2):505–522.
  • Kohane DS. Microparticles and nanoparticles for drug delivery. Biotechnol Bioeng. 2007;96(2):203–209.
  • Liu Y, Ghassemi AH, Hennink WE, et al. The microclimate pH in poly (D, L-lactide-co-hydroxymethyl glycolide) microspheres during biodegradation. Biomaterials. 2012;33(30):7584–7593.
  • Stanković M, Tomar J, Hiemstra C, et al. Tailored protein release from biodegradable poly (ε-caprolactone-PEG)-b-poly (ε-caprolactone) multiblock-copolymer implants. Eur J Pharm Biopharm. 2014;87(2):329–337.
  • Balmert SC, Little SR. Biomimetic delivery with micro‐and nanoparticles. Adv Mater. 2012;24(28):3757–3778.
  • Champion JA, Walker A, Mitragotri S. Role of particle size in phagocytosis of polymeric microspheres. Pharm Res. 2008;25(8):1815–1821.
  • Moon JJ, Huang B, Irvine DJ. Engineering nano‐and microparticles to tune immunity. Adv Mater. 2012;24(28):3724–3746.
  • Ghassemi A, Van Steenbergen M, Talsma H, et al. Preparation and characterization of protein loaded microspheres based on a hydroxylated aliphatic polyester, poly (lactic-co-hydroxymethyl glycolic acid). J Control Release. 2009;138(1):57–63.
  • Kunjachan S, Gremse F, Theek B, et al. Noninvasive optical imaging of nanomedicine biodistribution. ACS Nano. 2012;7(1):252–262.
  • Hou Y, Liu Y, Chen Z, et al. Manufacture of IRDye800CW-coupled Fe 3 O 4 nanoparticles and their applications in cell labeling and in vivo imaging. J Nanobiotechnology. 2010;8(1):25.
  • Sánchez A, Seoane R, Quireza O, et al. In vivo study of the tissue distribution and immunosuppressive response of cyclosporin a-loaded polyester micro-and nanospheres. Drug Deliv. 1995;2(1):21–28.
  • Sanchez A, Alonso MJ. Poly (D, L-lactide-co-glycolide) micro and nanospheres as a way to prolong blood. Eur J Pharm Biopharm. 1995;41(1):31–37.
  • Yoshikawa H, Seebach S. Lymphotropic delivery of cyclosporin A by intramuscular injection of biodegradable microspheres in mice. Biol Pharm Bull. 1996;19(11):1527–1529.
  • Miyamoto Y, Uno T, Yamamoto H, et al. Pharmacokinetic and immunosuppressive effects of tacrolimus‐loaded biodegradable microspheres. Liver Transpl. 2004;10(3):392–396.
  • Wang Q, Uno T, Miyamoto Y, et al. Biodegradable microsphere‐loaded tacrolimus enhanced the effect on mice islet allograft and reduced the adverse effect on insulin secretion. Am J Transplant. 2004;4(5):721–727.
  • Lamprecht A, Yamamoto H, Takeuchi H, et al. Nanoparticles enhance therapeutic efficiency by selectively increased local drug dose in experimental colitis in rats. J Pharmacol Exp Ther. 2005;315(1):196–202.
  • Meer Y, Pellequer Y, Lamprecht A. Nanoparticles in inflammatory bowel disease: particle targeting versus pH-sensitive delivery. Int J Pharm. 2006;316(1–2):138–143.
  • Lamprecht A, Yamamoto H, Takeuchi H, et al. A pH-sensitive microsphere system for the colon delivery of tacrolimus containing nanoparticles. J Control Release. 2005;104(2):337–346.
  • Glowacki AJ, Gottardi R, Yoshizawa S, et al. Strategies to direct the enrichment, expansion, and recruitment of regulatory cells for the treatment of disease. Ann Biomed Eng. 2015;43(3):593–602.
  • Jhunjhunwala S, Raimondi G, Thomson AW, et al. Delivery of rapamycin to dendritic cells using degradable microparticles. J Control Release. 2009;133(3):191–197.
  • Haddadi A, Elamanchili P, Lavasanifar A, et al. Delivery of rapamycin by PLGA nanoparticles enhances its suppressive activity on dendritic cells. J Biomed Mater Res A. 2008;84(4):885–898.
  • Das S, Haddadi A, Veniamin S, et al. Delivery of rapamycin‐loaded nanoparticle down regulates ICAM‐1 expression and maintains an immunosuppressive profile in human CD34+ progenitor‐derived dendritic cells. J Biomed Mater Res A. 2008;85(4):983–992.
  • Shirali A, Look M, Du W, et al. Nanoparticle delivery of mycophenolic acid upregulates PD‐L1 on dendritic cells to prolong murine allograft survival. Am J Transplant. 2011;11(12):2582–2592.
  • Metcalfe SM, Watson TJ, Shurey S, et al. Leukemia inhibitory factor is linked to regulatory transplantation tolerance. Transplantation. 2005;79(6):726–730.
  • Gao W, Thompson L, Zhou Q, et al. Treg versus Th17 lymphocyte lineages are cross-regulated by LIF versus IL-6. Cell Cycle. 2009;8(9):1444–1450.
  • Park J, Gao W, Whiston R, et al. Modulation of CD4+ T lymphocyte lineage outcomes with targeted, nanoparticle-mediated cytokine delivery. Mol Pharm. 2010;8(1):143–152.
  • Dong H, Fahmy TM, Metcalfe SM, et al. Immuno-isolation of pancreatic islet allografts using pegylated nanotherapy leads to long-term normoglycemia in full MHC mismatch recipient mice. PloS One. 2012;7(12):e50265.
  • Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10(9):942.
  • Lee I, Wang L, Wells AD, et al. Recruitment of Foxp3+ T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J Exp Med. 2005;201(7):1037–1044.
  • Jhunjhunwala S, Raimondi G, Glowacki AJ, et al. Bioinspired controlled release of CCL22 recruits regulatory T cells in vivo. Adv Mater. 2012;24(35):4735–4738.
  • Stephan MT, Stephan SB, Bak P, et al. Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles. Biomaterials. 2012;33(23):5776–5787.
  • Stephan MT, Moon JJ, Um SH, et al. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat Med. 2010;16(9):1035.
  • Steenblock ER, Fahmy TM. A comprehensive platform for ex vivo T-cell expansion based on biodegradable polymeric artificial antigen-presenting cells. Mol Ther. 2008;16(4):765–772.
  • Oelke M, Maus MV, Didiano D, et al. Ex vivo induction and expansion of antigen-specific cytotoxic T cells by HLA-Ig–coated artificial antigen-presenting cells. Nat Med. 2003;9(5):619.
  • Steenblock ER, Fadel T, Labowsky M, et al. An artificial antigen-presenting cell with paracrine delivery of IL-2 impacts the magnitude and direction of the T cell response. J Biol Chem. 2011;286(40):34883–34892.
  • Labowsky M, Fahmy T. Effect of cell surface deformation on synaptic factor accumulation during the early stages of T cell activation. Chem Eng Sci. 2013;90:275–283.
  • Labowsky M, Fahmy T. Diffusive transfer between two intensely interacting cells with limited surface kinetics. Chem Eng Sci. 2012;74:114–123.
  • Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science. 2004;303(5665):1818–1822.
  • Zhang Y, Chan HF, Leong KW. Advanced materials and processing for drug delivery: the past and the future. Adv Drug Deliv Rev. 2013;65(1):104–120.
  • Verma RK, Garg S. Drug delivery technologies and future directions. Pharm Technol. 2001;25(2):1–14.
  • Venkatpurwar V, Rhodes S, Oien K, et al. Drug-not carrier-dependent haematological and biochemical changes in a repeated dose study of cyclosporine encapsulated polyester nano-and micro-particles: size does not matter. Toxicology. 2015;330:9–18.
  • Kojima R, Yoshida T, Tasaki H, et al. Release mechanisms of tacrolimus-loaded PLGA and PLA microspheres and immunosuppressive effects of the microspheres in a rat heart transplantation model. Int J Pharm. 2015;492(1–2):20–27.
  • Bryant J, Hlavaty KA, Zhang X, et al. Nanoparticle delivery of donor antigens for transplant tolerance in allogeneic islet transplantation. Biomaterials. 2014;35(31):8887–8894.
  • Solhjou Z, Uehara M, Bahmani B, et al. Novel application of localized nanodelivery of anti–interleukin‐6 protects organ transplant from ischemia–reperfusion injuries. Am J Transplant. 2017;17(9):2326–2337.
  • Uehara M, Bahmani B, Jiang L, et al. Nanodelivery of mycophenolate mofetil to the organ improves transplant vasculopathy. ACS Nano. 2019;13(11):12393–12407.
  • Lewis JS, Roche C, Zhang Y, et al. Combinatorial delivery of immunosuppressive factors to dendritic cells using dual-sized microspheres. J Mat Chem B. 2014;2(17):2562–2574.
  • Tasciotti E, Cabrera FJ, Evangelopoulos M, et al. The emerging role of nanotechnology in cell and organ transplantation. Transplantation. 2016;100(8):1629.
  • Farina M, Alexander JF, Thekkedath U, et al. Cell encapsulation: overcoming barriers in cell transplantation in diabetes and beyond. Adv Drug Deliv Rev. 2019;139:92–115.
  • Li J, Yue S, Zhao Q, et al. Glucose cntrol in islet transplanted mice using long acting liraglutide nanoparticles. Nanosci Nanotechnol Lett. 2019;11(3):398–405.
  • Mistry NP, Desai JL, Thakkar HP. Formulation and evaluation of tacrolimus‐loaded galactosylated Poly (lactic‐co‐glycolic acid) nanoparticles for liver targeting. J Pharm Pharmacol. 2015;67(10):1337–1348.
  • Zamorano-Leon JJ, Hernandez-Fisac I, Guerrero S, et al. New strategy of tacrolimus administration in animal model based on tacrolimus-loaded microspheres. Transpl Immunol. 2016;36:9–13.
  • Italia J, Bhatt D, Bhardwaj V, et al. PLGA nanoparticles for oral delivery of cyclosporine: nephrotoxicity and pharmacokinetic studies in comparison to Sandimmune Neoral®. J Control Release. 2007;119(2):197–206.
  • Kapoor DN, Bhatia A, Kaur R, et al. PLGA: a unique polymer for drug delivery. Ther Deliv. 2015;6(1):41–58.
  • Sharma S, Parmar A, Kori S, et al. PLGA-based nanoparticles: a new paradigm in biomedical applications. Trends Analyt Chem. 2016;80:30–40.
  • Houchin M, Topp E. Chemical degradation of peptides and proteins in PLGA: a review of reactions and mechanisms. J Pharm Sci. 2008;97(7):2395–2404.
  • Jain A, Jain A, Gulbake A, et al. Peptide and protein delivery using new drug delivery systems. Critical Reviews™ in Therapeutic Drug Carrier Systems. 2013;30(4):293–329.
  • Astete CE, Sabliov CM. Synthesis and characterization of PLGA nanoparticles. J Biomater Sci Polym Ed. 2006;17(3):247–289.
  • Biondi M, Ungaro F, Quaglia F, et al. Controlled drug delivery in tissue engineering. Adv Drug Deliv Rev. 2008;60(2):229–242.
  • Ballestrero A, Boy D, Moran E, et al. Immunotherapy with dendritic cells for cancer. Adv Drug Deliv Rev. 2008;60(2):173–183.
  • Sah H. Protein behavior at the water/methylene chloride interface. J Pharm Sci. 1999;88(12):1320–1325.
  • Veronese FM. Peptide and protein PEGylation: a review of problems and solutions. Biomaterials. 2001;22(5):405–417.
  • Vasita R, Shanmugam K, Katti DS. Degradation behavior of electrospun microfibers of blends of poly (lactide-co-glycolide) and Pluronic® F-108. Polym Degrad Stab. 2010;95(9):1605–1613.
  • Danhier F, Feron O, Préat V. To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release. 2010;148(2):135–146.
  • Tabatabaei Mirakabad FS, Nejati-Koshki K, Akbarzadeh A, et al. PLGA-based nanoparticles as cancer drug delivery systems. Asian Pac J Cancer Prev. 2014;15(2):517–535.
  • Rao JP, Geckeler KE. Polymer nanoparticles: preparation techniques and size-control parameters. Prog Polym Sci. 2011;36(7):887–913.
  • Sah H, Thoma LA, Desu HR, et al. Concepts and practices used to develop functional PLGA-based nanoparticulate systems. Int J Nanomedicine. 2013;8:747.
  • Fredenberg S, Wahlgren M, Reslow M, et al. The mechanisms of drug release in poly (lactic-co-glycolic acid)-based drug delivery systems—a review. Int J Pharm. 2011;415(1–2):34–52.

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