Engineered exosome as a biological nanoplatform for drug delivery of Rosmarinic acid to improve implantation in mice with induced endometritis

References

• Aghaeepour N, Ganio EA, Mcilwain D, Tsai AS, Tingle M, Van Gassen S, Gaudilliere DK, Baca Q, McNeil L, Okada R, et al. 2017. An immune clock of human pregnancy. Sci Immunol. 2(15):2946. doi: 10.1126/sciimmunol.aan2946.
   Web of Science ®Google Scholar
• Alagawany M, Abd El-Hack ME, Farag MR, Gopi M, Karthik K, Malik YS, Dhama K. 2017. Rosmarinic acid: modes of action, medicinal values and health benefits. Anim Health Res Rev. 18(2):167–176. doi: 10.1017/S1466252317000081.
   PubMed Web of Science ®Google Scholar
• Antimisiaris SG, Mourtas S, Marazioti A. 2018. Exosomes and exosome-inspired vesicles for targeted drug delivery. Pharmaceutics. 10(4):218. doi: 10.3390/pharmaceutics10040218.
   PubMed Web of Science ®Google Scholar
• Araujo-Abad S, Saceda M, de Juan Romero C. 2022. Biomedical application of small extracellular vesicles in cancer treatment. Adv Drug Deliv Rev. 182:114117. doi: 10.1016/j.addr.2022.114117.
   PubMed Web of Science ®Google Scholar
• Arici A, Oral E, Bahtiyar O, Engin O, Seli E, Jones EE. 1997. Leukaemia inhibitory factor expression in human follicular fluid and ovarian cells. Hum Reprod. 12(6):1233–1239. doi: 10.1093/humrep/12.6.1233.
   PubMed Web of Science ®Google Scholar
• Barile L, Vassalli G. 2017. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 174:63–78. doi: 10.1016/j.pharmthera.2017.02.020.
   PubMed Web of Science ®Google Scholar
• Bischof P, Campana A. 2000. Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol. 14(5):801–814. doi: 10.1053/beog.2000.0120.
   PubMed Web of Science ®Google Scholar
• Bouet PE, El Hachem H, Monceau E, Gariépy G, Kadoch IJ, Sylvestre C. 2016. Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis. Fertil Steril. 105(1):106–110. doi: 10.1016/j.fertnstert.2015.09.025.
   PubMed Web of Science ®Google Scholar
• Burnett LA, Nowak RA. 2016. Exosomes mediate embryo and maternal interactions at implantation and during pregnancy. Front Biosci (Schol Ed)). 8(1):79–96. doi: 10.2741/s448.
   PubMedGoogle Scholar
• Cheng J, Sha Z, Li J, Li B, Luo X, Zhang Z, Zhou Y, Chen S, Wang Y. 2023. Progress on the role of estrogen and progesterone signaling in mouse embryo implantation and decidualization. Reprod Sci. 30(6):1746–1757. doi: 10.1007/s43032-023-01169-0.
   PubMed Web of Science ®Google Scholar
• Christiansen OB, Nielsen HS, Kolte AM. 2006. Future directions of failed implantation and recurrent miscarriage research. Reprod Biomed Online. 13(1):71–83. doi: 10.1016/S1472-6483(10)62018-4.
   PubMed Web of Science ®Google Scholar
• Cicinelli E, Matteo M, Tinelli R, Pinto V, Marinaccio M, Indraccolo U, De Ziegler D, Resta L. 2014. Chronic endometritis due to common bacteria is prevalent in women with recurrent miscarriage as confirmed by improved pregnancy outcome after antibiotic treatment. Reprod Sci. 21(5):640–647. doi: 10.1177/1933719113508817.
   PubMed Web of Science ®Google Scholar
• Coughlan C, Ledger W, Wang Q, Liu F, Demirol A, Gurgan T, Cutting R, Ong K, Sallam H, Li TC, et al. 2014. Recurrent implantation failure: definition and management. Reprod Biomed Online. 28(1):14–38. doi: 10.1016/j.rbmo.2013.08.011.
   PubMed Web of Science ®Google Scholar
• Croy BA, Esadeg S, Chantakru S, van den Heuvel M, Paffaro VA, He H, Black GP, Ashkar AA, Kiso Y, Zhang J, et al. 2003. Update on pathways regulating the activation of uterine natural killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. J Reprod Immunol. 59(2):175–191. doi: 10.1016/S0165-0378(03)00046-9.
   PubMed Web of Science ®Google Scholar
• Deb K, Reese J, Paria BC. 2006. Methodologies to study implantation in mice. Placenta Tropho. 1:9–34. doi: 10.1385/1-59259-983-4:007.
   Google Scholar
• Duan L, Xu X, Xu L, Chen H, Li X, Alahdal M, Xiao Y, Liang Y, Xia J. 2021. Exosome-mediated drug delivery for cell-free therapy of osteoarthritis. Curr Med Chem. 28(31):6458–6483. doi: 10.2174/0929867327666201118161232.
   PubMed Web of Science ®Google Scholar
• Governini L, Luongo FP, Haxhiu A, Piomboni P, Luddi A. 2021. Main actors behind the endometrial receptivity and successful implantation. Tissue Cell. 73:101656. doi: 10.1016/j.tice.2021.101656.
   PubMed Web of Science ®Google Scholar
• Gurunathan S, Kang MH, Jeyaraj M, Qasim M, Kim JH. 2021. Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells. 8(4):462. doi: 10.3390/cells8040307.
   Web of Science ®Google Scholar
• Guzeloglu-Kayisli O, Kayisli UA, Taylor HS. 2009. The role of growth factors and cytokines during implantation: endocrine and paracrine interactions. Semin Reprod Med. 27(1):62– 79. doi: 10.1055/s-0028-1108011.
   PubMed Web of Science ®Google Scholar
• Hajipour H, Ghorbani M, Kahroba H, Mahmoodzadeh F, Emameh RZ, Taheri RA. 2019. Arginyl-glycyl-aspartic acid (RGD) containing nanostructured lipid carrier co-loaded with doxorubicin and sildenafil citrate enhanced anti-cancer effects and overcomes drug resistance. Process Biochem. 84:172–179. doi: 10.1016/j.procbio.2019.06.013.
   Web of Science ®Google Scholar
• Hajipour H, Farzadi L, Roshangar L, Latifi Z, Kahroba H, Shahnazi V, Hamdi K, Ghasemzadeh A, Fattahi A, Nouri M, et al. 2021. Human chorionic gonadotropin (hcg) delivery platform using engineered uterine exosomes to improve endometrial receptivity. Life Sci. 275:119351. doi: 10.1016/j.lfs.2021.119351.
   PubMed Web of Science ®Google Scholar
• Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, Patel T, Piroyan A, Sokolsky M, Kabanov AV, et al. 2015. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 207:18–30. doi: 10.1016/j.jconrel.2015.03.033.
   PubMed Web of Science ®Google Scholar
• Hanna N, Hanna I, Hleb M, Wagner E, Dougherty J, Balkundi D, Padbury J, Sharma S. 2000. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol. 164(11):5721–5728. doi: 10.4049/jimmunol.164.11.5721.
   PubMed Web of Science ®Google Scholar
• Hitl M, Kladar N, Gavarić N, Božin B. 2021. Rosmarinic acid–human pharmacokinetics and health benefits. Planta Med. 87(4):273–282. doi: 10.1055/a-1301-8648.
   PubMedGoogle Scholar
• Hu X, Li D, Wang J, Guo J, Li Y, Cao Y, Zhang N, Fu Y. 2018. Melatonin inhibits endoplasmic reticulum stress-associated TXNIP/NLRP3 inflammasome activation in lipopolysaccharide-induced endometritis in mice. Int Immunopharmacol. 64:101–109. doi: 10.1016/j.intimp.2018.08.028.
   PubMed Web of Science ®Google Scholar
• Lamichhane TN, Jeyaram A, Patel DB, Parajuli B, Livingston NK, Arumugasaamy N, Schardt JS, Jay SM. 2016. Oncogene knockdown via active loading of small RNAs into extracellular vesicles by sonication. Cell Mol Bioeng. 9(3):315–324. doi: 10.1007/s12195-016-0457-4.
   PubMed Web of Science ®Google Scholar
• Lamprecht A. 2015. Nanomedicines in gastroenterology and hepatology. Nat Rev Gastroenterol Hepatol. 12(4):195–204. doi: 10.1038/nrgastro.2015.37.
   PubMed Web of Science ®Google Scholar
• Lédée N, Dubanchet S, Oger P, Meynant C, Lombroso R, Ville Y, Chaouat G. 2007. Uterine receptivity and cytokines: new concepts and new applications. Gynecol Obstet Invest. 64(3):138–143. doi: 10.1159/000101737.
   PubMed Web of Science ®Google Scholar
• Lee D, Lee YG, Won J, Hong SH, Kim JH, Kang YJ. 2022. Effects of intrauterine human chorionic gonadotropin administration on endometrial receptivity and embryo implantation. Life Sci. 311(Pt A):121154. doi: 10.1016/j.lfs.2022.121154.
   PubMedGoogle Scholar
• Li H, Huang X, Chang X, Yao J, He Q, Shen Z, Ji Y, Wang K. 2020. S100‐A9 protein in exosomes derived from follicular fluid promotes inflammation via activation of NF‐κb pathway in polycystic ovary syndrome. J Cell Mol Med. 24(1):114–125. doi: 10.1111/jcmm.14642.
   PubMed Web of Science ®Google Scholar
• Li X, Qi M, Sun X, Weir MD, Tay FR, Oates TW, Dong B, Zhou Y, Wang L, Xu HHK, et al. 2019. Surface treatments on titanium implants via nanostructured ceria for antibacterial and anti-inflammatory capabilities. Acta Biomater. 94:627–643. doi: 10.1016/j.actbio.2019.06.023.
   PubMed Web of Science ®Google Scholar
• Liu L, Wang Y, Chen X, Tian Y, Li TC, Zhao L, Chen Q, Wei M, Zhang S. 2020. Evidence from three cohort studies on the expression of MUC16 around the time of implantation suggests it is an inhibitor of implantation. J Assist Reprod Genet. 37(5):1105–1115. doi: 10.1007/s10815-020-01764-z.
   PubMed Web of Science ®Google Scholar
• Matteo M, Cicinelli E, Greco P, Massenzio F, Baldini D, Falagario T, Rosenberg P, Castellana L, Specchia G, Liso A, et al. 2009. Abnormal pattern of lymphocyte subpopulations in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 61(5):322–329. doi: 10.1111/j.1600-0897.2009.00698.x.
   PubMed Web of Science ®Google Scholar
• Nadeem M, Imran M, Aslam Gondal T, Imran A, Shahbaz M, Muhammad Amir R, Wasim Sajid M, Batool Qaisrani T, Atif M, Hussain G, et al. 2019. Therapeutic potential of rosmarinic acid: A comprehensive review. Appl Sci. 9(15):3139. doi: 10.3390/app9153139.
   Google Scholar
• Nakamura K, Kusama K, Bai R, Sakurai T, Isuzugawa K, Godkin JD, Suda Y, Imakawa K. 2016. Induction of IFNT-stimulated genes by conceptus-derived exosomes during the attachment period. Plos One. 11(6):e0158278. doi: 10.1371/journal.pone.0158278.
   PubMed Web of Science ®Google Scholar
• Nguyen HP, Simpson RJ, Salamonsen LA, Greening DW. 2016. Extracellular vesicles in the intrauterine environment: challenges and potential functions. Biol Reprod. 95(5):109–109. doi: 10.1095/biolreprod.116.143503.
   PubMedGoogle Scholar
• Ni H, Ding NZ, Harper MJ, Yang ZM. 2002. Expression of leukemia inhibitory factor receptor and gp130 in mouse uterus during early pregnancy. Mol Reprod Dev. 63(2):143–150. doi: 10.1002/mrd.10168.
   PubMed Web of Science ®Google Scholar
• Noonin C, Thongboonkerd V. 2021. Exosome-inflammasome crosstalk and their roles in inflammatory responses. Theranostics. 11(9):4436–4451. doi: 10.7150/thno.54004.
   PubMed Web of Science ®Google Scholar
• Ostojic S, Dubanchet S, Chaouat G, Abdelkarim M, Truyens C, Capron F. 2003. Demonstration of the presence of IL‐16, IL‐17 and IL‐18 at the murine fetomaternal interface during murine pregnancy. Am J Reprod Immunol. 49(2):101–112. doi: 10.1034/j.1600-0897.2003.01150.x.
   PubMed Web of Science ®Google Scholar
• Pethő A, Chen Y, George A. 2018. Exosomes in extracellular matrix bone biology. Curr Osteoporos Rep. 16(1):58–64. doi: 10.1007/s11914-018-0419-y.
   PubMed Web of Science ®Google Scholar
• Pizzicannella J, Gugliandolo A, Orsini T, Fontana A, Ventrella A, Mazzon E, Bramanti P, Diomede F, Trubiani O. 2019. Engineered extracellular vesicles from human periodontal-ligament stem cells increase VEGF/VEGFR2 expression during bone regeneration. Front Physiol. 10:512. doi: 10.3389/fphys.2019.00512.
   PubMed Web of Science ®Google Scholar
• Poole JA, Claman HN. 2004. Immunology of pregnancy: implications for the mother. Clin Rev Allergy Immunol. 26(3):161–170. doi: 10.1385/CRIAI:26:3:161.
   PubMed Web of Science ®Google Scholar
• PrabhuDas M, Bonney E, Caron K, Dey S, Erlebacher A, Fazleabas A, Fisher S, Golos T, Matzuk M, McCune JM, et al. 2015. Immune mechanisms at the maternal-fetal interface: perspectives and challenges. Nat Immunol. 16(4):328–334. doi: 10.1038/ni.3131.
   PubMed Web of Science ®Google Scholar
• Price JC, Bromfield JJ, Sheldon IM. 2013. Pathogen-associated molecular patterns initiate inflammation and perturb the endocrine function of bovine granulosa cells from ovarian dominant follicles via TLR2 and TLR4 pathways. Endocrinol. 154(9):3377–3386. doi: 10.1210/en.2013-1102.
   PubMed Web of Science ®Google Scholar
• Ren J, He W, Zheng L, Duan H. 2016. From structures to functions: insights into exosomes as promising drug delivery vehicles. Biomater Sci. 4(6):910–921. doi: 10.1039/C5BM00583C.
   PubMed Web of Science ®Google Scholar
• Robertson SA, Petroff MG, Hunt JS. 2015. Immunology of pregnancy. Knobil and Neill’s Physiol Reprod. 4th ed. Oxford, UK: Elsevier; p. 1835–1874.
   Google Scholar
• rodríguez-Luna A, Talero E, Ávila-Román J, Romero AMF, Rabasco AM, Motilva V, González-Rodríguez ML. 2021. Preparation and in vivo evaluation of rosmarinic acid-loaded transethosomes after percutaneous application on a psoriasis animal model. AAPS Pharmscitech. 22(3):103. doi: 10.1208/s12249-021-01966-3.
   PubMed Web of Science ®Google Scholar
• Simón C, Martín JC, Pellicer A. 2000. Paracrine regulators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol. 14(5):815–826. doi: 10.1053/beog.2000.0121.
   PubMed Web of Science ®Google Scholar
• Singh M, Chaudhry P, Asselin E. 2011. Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J Endocrinol. 210(1):5–14. doi: 10.1530/JOE-10-0461.
   PubMed Web of Science ®Google Scholar
• Taravat M, Asadpour R, Jozani RJ, Fattahi A, Khordadmehr M. 2023. Enhanced anti-inflammatory effect of Rosmarinic acid by encapsulation and combination with the exosome in mice with LPS-induced endometritis through suppressing the TLR4-NLRP3 signaling pathway. J Reprod Immunol. 159:103992. 1 doi: 10.1016/j.jri.2023.103992.
   PubMed Web of Science ®Google Scholar
• Tremellen K, Syedi N, Tan S, Pearce K. 2015. Metabolic endotoxaemia–a potential novel link between ovarian inflammation and impaired progesterone production. Gynecol Endocrinol. 31(4):309–312. doi: 10.3109/09513590.2014.994602.
   PubMed Web of Science ®Google Scholar
• Van Mourik MS, Macklon NS, Heijnen CJ. 2009. Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment. J Leukoc Biol. 85(1):4–19. doi: 10.1189/jlb.0708395.
   PubMed Web of Science ®Google Scholar
• Vitagliano A, Saccardi C, Noventa M, Di Spiezio Sardo A, Saccone G, Cicinelli E, Pizzi S, Andrisani A, Litta PS. 2018. Effects of chronic endometritis therapy on in vitro fertilization outcome in women with repeated implantation failure: a systematic review and meta-analysis. Fertil Steril. 110(1):103–112.e1. doi: 10.1016/j.fertnstert.2018.03.017.
   PubMed Web of Science ®Google Scholar
• Zhang D, Lee H, Wang X, Rai A, Groot M, Jin Y. 2018. Exosome-mediated small RNA delivery: a novel therapeutic approach for inflammatory lung responses. Mol Ther. 26(9):2119–2130. doi: 10.1016/j.ymthe.2018.06.007.
   PubMed Web of Science ®Google Scholar
• Zhang W, Wang Y, Kong Y. 2019. Exosomes derived from mesenchymal stem cells modulate mir-126 to ameliorate hyperglycemia-induced retinal inflammation via targeting HMGB1. Invest Ophthalmol Vis Sci. 60(1):294–303. doi: 10.1167/iovs.18-25617.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhang T, Guo X, Wong CK, Chen X, Chan YL, Wang CC, Laird S, Li TC. 2021. Successful implantation is associated with a transient increase in serum pro-inflammatory cytokine profile followed by a switch to anti-inflammatory cytokine profile prior to confirmation of pregnancy. Fertil Steril. 115(4):1044–1053. doi: 10.1016/j.fertnstert.2020.10.031.
   PubMed Web of Science ®Google Scholar
• Zhou W-J, Yang H-L, Shao J, Mei J, Chang K-K, Zhu R, Li M-Q. 2019. Anti-inflammatory cytokines in endometriosis. Cell Mol Life Sci. 76(11):2111–2132. doi: 10.1007/s00018-019-03056-x.
   PubMed Web of Science ®Google Scholar