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ORIGINAL RESEARCH

PLGA-Chitosan Encapsulated IL-10 Nanoparticles Modulate Chlamydia Inflammation in Mice

, ORCID Icon, , , , & show all
Pages 1287-1301 | Received 29 Jul 2023, Accepted 12 Dec 2023, Published online: 08 Feb 2024

References

  • Gonzalez-Chavez A, Elizondo-Argueta S, Gutierrez-Reyes G, Leon-Pedroza JI. Pathophysiological implications between chronic inflammation and the development of diabetes and obesity. Cir Cir. 2011;79(2):209–216.
  • Harvey AE, Lashinger LM, Hursting SD. The growing challenge of obesity and cancer: an inflammatory issue. Ann N Y Acad Sci. 2011;1229:45–52. doi:10.1111/j.1749-6632.2011.06096.x
  • Chen L, Deng H, Cui H, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018;9(6):7204–7218. doi:10.18632/oncotarget.23208
  • Wortmann M, Skorubskaya E, Peters AS, Hakimi M, Bockler D, Dihlmann S. Necrotic cell debris induces a NF-kappaB-driven inflammasome response in vascular smooth muscle cells derived from abdominal aortic aneurysms (AAA-SMC). Biochem Biophys Res Commun. 2019;511(2):343–349. doi:10.1016/j.bbrc.2019.02.051
  • Abdulkhaleq LA, Assi MA, Abdullah R, Zamri-Saad M, Taufiq-Yap YH, Hezmee MNM. The crucial roles of inflammatory mediators in inflammation: a review. Vet World. 2018;11(5):627–635. doi:10.14202/vetworld.2018.627-635
  • Slaats J, Ten Oever J, van de Veerdonk FL, Netea MG. IL-1beta/IL-6/CRP and IL-18/ferritin: distinct inflammatory programs in infections. PLoS Pathog. 2016;12(12):e1005973. doi:10.1371/journal.ppat.1005973
  • Lin L, Curtin JA, Regis E, et al. A systems immunology approach to investigate cytokine responses to viruses and bacteria and their association with disease. Sci Rep. 2022;12(1):13463. doi:10.1038/s41598-022-16509-4
  • Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature. 2011;473(7347):317–325. doi:10.1038/nature10146
  • Charo IF, Taub R. Anti-inflammatory therapeutics for the treatment of atherosclerosis. Nat Rev Drug Discov. 2011;10(5):365–376. doi:10.1038/nrd3444
  • Delbaere Q, Chapet N, Huet F, et al. Anti-inflammatory drug candidates for prevention and treatment of cardiovascular diseases. Pharmaceuticals. 2023;16(1):78. doi:10.3390/ph16010078
  • Yilma AN, Singh SR, Fairley SJ, Taha MA, Dennis VA. The anti-inflammatory cytokine, interleukin-10, inhibits inflammatory mediators in human epithelial cells and mouse macrophages exposed to live and UV-inactivated chlamydia trachomatis. Mediators Inflamm. 2012;2012:520174. doi:10.1155/2012/520174
  • Wang X, Coradin T, Helary C. Modulating inflammation in a cutaneous chronic wound model by IL-10 released from collagen-silica nanocomposites via gene delivery. Biomater Sci. 2018;6(2):398–406. doi:10.1039/c7bm01024a
  • Saraiva M, Vieira P, O’Garra A. Biology and therapeutic potential of interleukin-10.. J Exp Med. 2020;217(1). doi:10.1084/jem.20190418
  • Trifunovic J, Miller L, Debeljak Z, Horvat V. Pathologic patterns of interleukin 10 expression–a review. Biochem Med. 2015;25(1):36–48. doi:10.11613/BM.2015.004
  • Watanabe S, Alexander M, Misharin AV, Budinger GRS. The role of macrophages in the resolution of inflammation. J Clin Invest. 2019;129(7):2619–2628. doi:10.1172/JCI124615
  • Minton K. IL-10 targets macrophage metabolism. Nat Rev Immunol. 2017;17(6):345. doi:10.1038/nri.2017.57
  • Mittal SK, Cho KJ, Ishido S, Roche PA. Interleukin 10 (IL-10)-mediated Immunosuppression: MARCH-I INDUCTION REGULATES ANTIGEN PRESENTATION BY MACROPHAGES BUT NOT DENDRITIC CELLS. J Biol Chem. 2015;290(45):27158–27167. doi:10.1074/jbc.M115.682708
  • Perez-Hernandez J, Chiurchiu V, Perruche S, You S. Regulation of T-cell immune responses by pro-resolving lipid mediators. Front Immunol. 2021;12:768133. doi:10.3389/fimmu.2021.768133
  • de Gruijter NM, Jebson B, Rosser EC. Cytokine production by human B cells: role in health and autoimmune disease. Clin Exp Immunol. 2022;210(3):253–262. doi:10.1093/cei/uxac090
  • Wang X, Wong K, Ouyang W, Rutz S. Targeting IL-10 family cytokines for the treatment of human diseases. Cold Spring Harb Perspect Biol. 2019;11:2.
  • Silva JR, Sales NS, Silva MO, et al. Expression of a soluble IL-10 receptor enhances the therapeutic effects of a papillomavirus-associated antitumor vaccine in a murine model. Cancer Immunol Immunother. 2019;68(5):753–763. doi:10.1007/s00262-018-02297-2
  • Wang SB, Deng YQ, Ren J, Xiao BK, Liu Z, Tao ZZ. Exogenous interleukin-10 alleviates allergic inflammation but inhibits local interleukin-10 expression in a mouse allergic rhinitis model. BMC Immunol. 2014;15(1):9. doi:10.1186/1471-2172-15-9
  • Rojas JM, Avia M, Martin V, Sevilla N. IL-10: a multifunctional cytokine in viral infections. Review J Immunol Res. 2017;2017:6104054. doi:10.1155/2017/6104054
  • Sung YK, Kim SW. Recent advances in polymeric drug delivery systems. Biomater Res. 2020;24(1):12. doi:10.1186/s40824-020-00190-7
  • Leonard M, De Boisseson MR, Hubert P, Dalencon F, Dellacherie E. Hydrophobically modified alginate hydrogels as protein carriers with specific controlled release properties. J Control Release. 2004;98(3):395–405. doi:10.1016/j.jconrel.2004.05.009
  • McClements DJ. Encapsulation, protection, and delivery of bioactive proteins and peptides using nanoparticle and microparticle systems: a review. Adv Colloid Interface Sci. 2018;253:1–22. doi:10.1016/j.cis.2018.02.002
  • Maskrey BH, Megson IL, Whitfield PD, Rossi AG. Mechanisms of resolution of inflammation: a focus on cardiovascular disease. Arterioscler Thromb Vasc Biol. 2011;31(5):1001–1006. doi:10.1161/ATVBAHA.110.213850
  • Xiang W, Yu N, Lei A, et al. Insights into host cell cytokines in chlamydia infection. Front Immunol. 2021;12:639834. doi:10.3389/fimmu.2021.639834
  • Redpath SA, Fonseca NM, Perona-Wright G. Protection and pathology during parasite infection: IL-10 strikes the balance. Parasite Immunol. 2014;36(6):233–252. doi:10.1111/pim.12113
  • Kumar R, Ng S, Engwerda C. The role of IL-10 in Malaria: a double edged sword review. Front Immunol. 2019;10:229. doi:10.3389/fimmu.2019.00229
  • Yilma AN, Singh SR, Dixit S, Dennis VA. Anti-inflammatory effects of silver-polyvinyl pyrrolidone (Ag-PVP) nanoparticles in mouse macrophages infected with live Chlamydia trachomatis. Int J Nanomed. 2013;8:2421–2432. doi:10.2147/IJN.S44090
  • Duncan SA, Sahu R, Dixit S, Singh SR, Dennis VA. Suppressors of Cytokine Signaling (SOCS)1 and SOCS3 proteins are mediators of interleukin-10 modulation of inflammatory responses induced by Chlamydia muridarum and Its Major Outer Membrane Protein (MOMP) in mouse J774 macrophages. Mediators Inflamm. 2020;2020:7461742. doi:10.1155/2020/7461742
  • Pirooznia N, Hasannia S, Lotfi AS, Ghanei M. Encapsulation of alpha-1 antitrypsin in PLGA nanoparticles: in vitro characterization as an effective aerosol formulation in pulmonary diseases. J Nanobiotechnology. 2012;10:20. doi:10.1186/1477-3155-10-20
  • Jarudilokkul S, Tongthammachat A, Boonamnuayvittaya V. Preparation of chitosan nanoparticles for encapsulation and release of protein. Korean J Chem Eng. 2011;28(5):1247–1251. doi:10.1007/s11814-010-0485-z
  • Amidi M, Mastrobattista E, Jiskoot W, Hennink WE. Chitosan-based delivery systems for protein therapeutics and antigens. Adv Drug Deliv Rev. 2010;62(1):59–82. doi:10.1016/j.addr.2009.11.009
  • de Sousa Victor R, Marcelo da Cunha Santos A, Viana de Sousa B, de Araujo Neves G, Navarro de Lima Santana L, Rodrigues Menezes R. A review on chitosan’s uses as biomaterial: tissue engineering, drug delivery systems and cancer treatment. Materials. 2020;13:21.
  • Duncan SA, Dixit S, Sahu R, et al. Prolonged Release and Functionality of Interleukin-10 Encapsulated within PLA-PEG Nanoparticles. Nanomaterials. 2019;9:8.
  • Sahu R, Dixit S, Verma R, et al. Encapsulation of Recombinant MOMP in Extended-Releasing PLGA 85:15 nanoparticles confer protective immunity against a chlamydia muridarum genital challenge and re-challenge. Original Res Front Immunol. 2021;12(1197):660932. doi:10.3389/fimmu.2021.660932
  • Sahu R, Dixit S, Verma R, et al. A nanovaccine formulation of Chlamydia recombinant MOMP encapsulated in PLGA 85:15 nanoparticles augments CD4(+) effector (CD44(high) CD62L(low)) and memory (CD44(high) CD62L(high)) T-cells in immunized mice. Nanomedicine. 2020;29:102257. doi:10.1016/j.nano.2020.102257
  • Fairley SJ, Singh SR, Yilma AN, et al. Chlamydia trachomatis recombinant MOMP encapsulated in PLGA nanoparticles triggers primarily T helper 1 cellular and antibody immune responses in mice: a desirable candidate nanovaccine. Int J Nanomed. 2013;8:2085–2099. doi:10.2147/IJN.S44155
  • Taha MA, Singh SR, Dennis VA. Biodegradable PLGA85/15 nanoparticles as a delivery vehicle for Chlamydia trachomatis recombinant MOMP-187 peptide. Nanotechnology. 2012;23(32):325101. doi:10.1088/0957-4484/23/32/325101
  • Dixit S, Singh SR, Yilma AN, Agee RD, Taha M, Dennis VA. Poly(lactic acid)-poly(ethylene glycol) nanoparticles provide sustained delivery of a Chlamydia trachomatis recombinant MOMP peptide and potentiate systemic adaptive immune responses in mice. Nanomedicine. 2014;10(6):1311–1321. doi:10.1016/j.nano.2014.02.009
  • Tucureanu MM, Rebleanu D, Constantinescu CA, et al. Lipopolysaccharide-induced inflammation in monocytes/macrophages is blocked by liposomal delivery of G(i)-protein inhibitor. Int J Nanomed. 2018;13:63–76. doi:10.2147/IJN.S150918
  • Verma R, Sahu R, Dixit S, et al. The Chlamydia M278 major outer membrane peptide encapsulated in the poly(lactic acid)-Poly(ethylene glycol) nanoparticulate self-adjuvanting delivery system protects mice against a chlamydia muridarum genital tract challenge by stimulating robust systemic and local mucosal immune responses. Front Immunol. 2018;9:2369. doi:10.3389/fimmu.2018.02369
  • Dixit S, Sahu R, Verma R, et al. Caveolin-mediated endocytosis of the Chlamydia M278 outer membrane peptide encapsulated in poly(lactic acid)-Poly(ethylene glycol) nanoparticles by mouse primary dendritic cells enhances specific immune effectors mediated by MHC class II and CD4(+) T cells. Biomaterials. 2018;159:130–145. doi:10.1016/j.biomaterials.2017.12.019
  • Saxena A, Khosraviani S, Noel S, Mohan D, Donner T, Hamad AR. Interleukin-10 paradox: a potent immunoregulatory cytokine that has been difficult to harness for immunotherapy. Research support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Review. Cytokine. 2015;74(1):27–34. doi:10.1016/j.cyto.2014.10.031
  • Park J, Gao W, Whiston R, Strom TB, Metcalfe S, Fahmy TM. Modulation of CD4+ T lymphocyte lineage outcomes with targeted, nanoparticle-mediated cytokine delivery. Mol Pharm. 2011;8(1):143–152. doi:10.1021/mp100203a
  • Akagi T, Baba M, Akashi M. Biodegradable Nanoparticles as Vaccine Adjuvants and Delivery Systems: regulation of Immune Responses by Nanoparticle-Based Vaccine. In: Kunugi S, Yamaoka T, editors. Polymers in Nanomedicine. Springer Berlin Heidelberg; 2011.
  • Han J, Zhao D, Li D, Wang X, Jin Z, Zhao K. Polymer-based nanomaterials and applications for vaccines and drugs. Polymers. 2018;10(1):31. doi:10.3390/polym10010031
  • Yang Y, Chen J, Li H, et al. Porcine interleukin-2 gene encapsulated in chitosan nanoparticles enhances immune response of mice to piglet paratyphoid vaccine. Comp Immunol Microbiol Infect Dis. 2007;30(1):19–32. doi:10.1016/j.cimid.2006.09.006
  • Elmowafy EM, Tiboni M, Soliman ME. Biocompatibility, biodegradation and biomedical applications of poly(lactic acid)/poly(lactic-co-glycolic acid) micro and nanoparticles. J Pharm Invest. 2019;49(4):347–380. doi:10.1007/s40005-019-00439-x
  • Adepu S, Ramakrishna S. Controlled drug delivery systems: current status and future directions. Molecules. 2021;26:19.
  • Kamaly N, Yameen B, Wu J, Farokhzad OC. Degradable controlled-release polymers and polymeric nanoparticles: mechanisms of controlling drug release. Chem Rev. 2016;116(4):2602–2663. doi:10.1021/acs.chemrev.5b00346
  • Boyoglu S, Vig K, Pillai S, et al. Enhanced delivery and expression of a nanoencapsulated DNA vaccine vector for respiratory syncytial virus. Nanomedicine. 2009;5(4):463–472. doi:10.1016/j.nano.2009.02.004
  • Hamdy S, Molavi O, Ma Z, et al. Co-delivery of cancer-associated antigen and Toll-like receptor 4 ligand in PLGA nanoparticles induces potent CD8+ T cell-mediated anti-tumor immunity. Vaccine. 2008;26(39):5046–5057. doi:10.1016/j.vaccine.2008.07.035
  • Verma AK, Pandey RP, Chanchal A, Siddiqui I, Sharma P. Encapsulation of antigenic secretory proteins of mycobacterium tuberculosis in biopolymeric nanoparticles for possible aerosol delivery system. J Bionanosci. 2011;5(1):88–95. doi:10.1166/jbns.2011.1042
  • Carvalho V, Castanheira P, Madureira P, et al. Self-assembled dextrin nanogel as protein carrier: controlled release and biological activity of IL-10. Biotechnol Bioeng. 2011;108(8):1977–1986. doi:10.1002/bit.23125
  • Carvalho V, Castanheira P, Faria TQ, et al. Biological activity of heterologous murine interleukin-10 and preliminary studies on the use of a dextrin nanogel as a delivery system. Int J Pharm. 2010;400(1–2):234–242. doi:10.1016/j.ijpharm.2010.08.040
  • Kole S, Shin SM, Kwak IS, Cho SH, Jung SJ. Efficacy of Chitosan-PLGA encapsulated trivalent oral vaccine against viral haemorrhagic septicemia virus, Streptococcus parauberis, and Miamiensis avidus in olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2022;127:843–854. doi:10.1016/j.fsi.2022.07.029
  • Zielinska A, Carreiro F, Oliveira AM, et al. Polymeric nanoparticles: production, characterization, toxicology and ecotoxicology. Molecules. 2020;25:16.
  • Gustafson HH, Holt-Casper D, Grainger DW, Ghandehari H. Nanoparticle uptake: the phagocyte problem. Nano Today. 2015;10(4):487–510. doi:10.1016/j.nantod.2015.06.006
  • Zhang J, Saltzman M. Engineering biodegradable nanoparticles for drug and gene delivery. Chem Eng Prog. 2013;109(3):25–30.
  • Sales-Junior PA, Guzman F, Vargas MI, et al. Use of biodegradable PLGA microspheres as a slow release delivery system for the Boophilus microplus synthetic vaccine SBm7462. Vet Immunol Immunopathol. 2005;107(3–4):281–290. doi:10.1016/j.vetimm.2005.05.004
  • Aranaz I, Alcantara AR, Civera MC, et al. Chitosan: an overview of its properties and applications. Polymers. 2021;13:19.
  • Hirano T. IL-6 in inflammation, autoimmunity and cancer. Int Immunol. 2021;33(3):127–148. doi:10.1093/intimm/dxaa078
  • Mbongue JC, Vanterpool E, Firek A, Langridge WHR. Lipopolysaccharide-induced immunological tolerance in monocyte-derived dendritic cells. Immuno. 2022;2(3):482–500.