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Research article

Sja-miR-71a in Schistosome egg-derived extracellular vesicles suppresses liver fibrosis caused by schistosomiasis via targeting semaphorin 4D

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Article: 1785738 | Received 24 Feb 2020, Accepted 12 Jun 2020, Published online: 09 Jul 2020

References

  • Shen J, Lai DH, Wilson RA, et al. Nitric oxide blocks the development of the human parasite Schistosoma japonicum. Proc Natl Acad Sci USA. 2017;114:10214–17.
  • Anthony BJ, James KR, Gobert GN, et al. Schistosoma japonicum eggs induce a proinflammatory, anti-fibrogenic phenotype in hepatic stellate cells. PloS One. 2013;8:e68479.
  • Anthony B, Mathieson W, de Castro-borges W, et al. Schistosoma mansoni: egg-induced downregulation of hepatic stellate cell activation and fibrogenesis. Exp Parasitol. 2010;124:409–420.
  • Duan Y, Pan J, Chen J, et al. Soluble egg antigens of Schistosoma japonicum induce senescence of activated hepatic stellate cells by activation of the FoxO3a/SKP2/P27 pathway. PLoS Negl Trop Dis. 2016;10:e0005268.
  • Chen J, Pan J, Wang J, et al. Soluble egg antigens of Schistosoma japonicum induce senescence in activated hepatic stellate cells by activation of the STAT3/p53/p21 pathway. Sci Rep. 2016;6:30957.
  • Wang J, Xu F, Zhu D, et al. Schistosoma japonicum soluble egg antigens facilitate hepatic stellate cell apoptosis by downregulating Akt expression and upregulating p53 and DR5 expression. PLoS Negl Trop Dis. 2014;8:e3106.
  • Lőrincz ÁM, Bartos B, Szombath D, et al. Role of Mac-1 integrin in generation of extracellular vesicles with antibacterial capacity from neutrophilic granulocytes. J Extracell Vesicles. 2020;9:1698889.
  • Jiang F, Chen Q, Wang W, et al. Hepatocyte-derived extracellular vesicles promote endothelial inflammation and atherogenesis via microRNA-1. J Hepatol. 2020;72:156–166.
  • Bernal D, Trelis M, Montaner S, et al. Surface analysis of Dicrocoelium dendriticum The molecular characterization of exosomes reveals the presence of miRNAs. J Proteomics. 2014;105:232–241.
  • Eichenberger RM, Ryan S, Jones L, et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front Immunol. 2018;9:850.
  • Ding J, He G, Je W, et al. miRNA-seq of Echinococcus multilocularis extracellular vesicles and immunomodulatory effects of miR-4989. Front Microbiol. 2019;10:2707.
  • Hansen EP, Fromm B, Andersen SD, et al. Exploration of extracellular vesicles from Ascaris suum provides evidence of parasite–host cross talk. J Extracell Vesicles. 2019;8:1578116.
  • Buck AH, Coakley G, Simbari F, et al. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat Commun. 2014;5:5488.
  • Wang L, Li Z, Shen J, et al. Exosome-like vesicles derived by Schistosoma japonicum adult worms mediates M1 type immune-activity of macrophage. Parasitol Res. 2015;114:1865–1873.
  • Meningher T, Lerman G, Regev-Rudzki N, et al. Schistosomal MicroRNAs isolated from extracellular vesicles in sera of infected patients: a new tool for diagnosis and follow-up of human schistosomiasis. J Infect Dis. 2016;215:378–386.
  • Zhu L, Liu J, Dao J, et al. Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions. Sci Rep. 2016;6:25885.
  • Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni. J Extracell Vesicles. 2015;4:28665.
  • Samoil V, Dagenais M, Ganapathy V, et al. Vesicle-based secretion in schistosomes: analysis of protein and microRNA (miRNA) content of exosome-like vesicles derived from Schistosoma mansoni. Sci Rep. 2018;8:3286.
  • Liu J, Zhu L, Wang J, et al. Schistosoma japonicum extracellular vesicle miRNA cargo regulates host macrophage functions facilitating parasitism. PLoS Pathog. 2019;15:e1007817.
  • Zhu S, Wang S, Lin Y, et al. Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum. Parasit Vectors. 2016;9:574.
  • Meningher T, Barsheshet Y, Ofir‐Birin Y, et al. Schistosomal extracellular vesicle‐enclosed miRNAs modulate host T helper cell differentiation. EMBO Rep. 2020;21:e47882.
  • Mathieu M, Martin-Jaular L, Lavieu G, et al. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol. 2019;21:9–17.
  • Ren X-S, Tong Y, Qiu Y, et al. MiR155-5p in adventitial fibroblasts-derived extracellular vesicles inhibits vascular smooth muscle cell proliferation via suppressing angiotensin-converting enzyme expression. J Extracell Vesicles. 2020;9:1698795.
  • Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–233.
  • Benmoussa A, Ly S, Shan ST, et al. A subset of extracellular vesicles carries the bulk of microRNAs in commercial dairy cow’s milk. J Extracell Vesicles. 2017;6:1401897.
  • Min L, Zhu S, Chen L, et al. Evaluation of circulating small extracellular vesicles derived miRNAs as biomarkers of early colon cancer: a comparison with plasma total miRNAs. J Extracell Vesicles. 2019;8:1643670.
  • He X, Xie J, Zhang D, et al. rAAV8-mediated inhibition of miRNA-21 protects mice against the lethal schistosome infection by repressing both IL-13 and TGF-β1 pathways. Hepatology. 2015;61:2008–2017.
  • Cabantous S, Hou X, Louis L, et al. Evidence for an important role of host microRNAs in regulating hepatic fibrosis in humans infected with Schistosoma japonicum. Int J Parasitol. 2017;47:823–830.
  • Zhao Y, Dang Z, Chong S. Mmu-miR-92a-2-5p targets TLR2 to relieve Schistosoma japonicum-induced liver fibrosis. Int Immunopharmacol. 2019;69:126–135.
  • Chapoval SP, Vadasz Z, Chapoval AI, et al. Semaphorins 4A and 4D in chronic inflammatory diseases. Inflamm Res. 2017;66:111–117.
  • Derakhshandeh R, Sanadhya S, Han KL, et al. Semaphorin 4D in human head and neck cancer tissue and peripheral blood: a dense fibrotic peri-tumoral stromal phenotype. Oncotarget. 2018;9:11126–11144.
  • Shanks K, Nkyimbeng-Takwi E, Smith E, et al. Neuroimmune semaphorin 4D is necessary for optimal lung allergic inflammation. Mol Immunol. 2013;56:480–487.
  • Du P, Ma Q, Zhu Z-D, et al. Mechanism of Corilagin interference with IL-13/STAT6 signaling pathways in hepatic alternative activation macrophages in schistosomiasis-induced liver fibrosis in mouse model. Eur J Pharmacol. 2016;793:119–126.
  • Chen B-L, Peng J, Li Q-F, et al. Exogenous bone morphogenetic protein-7 reduces hepatic fibrosis in Schistosoma japonicum-infected mice via transforming growth factor-β/Smad signaling. World J Gastroenterol. 2013;19:1405–1415.
  • Kumanogoh A, Kikutani H. Immunological functions of the neuropilins and plexins as receptors for semaphorins. Nat Rev Immunol. 2013;13:802–814.
  • Koch MA, Perdue NR, Killebrew JR, et al. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol. 2009;10:595–602.
  • Coutinho H, Acosta L, Wu H, et al. Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. J Infect Dis. 2007;195:288–295.
  • Li J, Qiu S-J, She W-M, et al. Significance of the balance between regulatory T (Treg) and T helper 17 (Th17) cells during hepatitis B virus related liver fibrosis. PloS One. 2012;7:e39307.
  • Barbi J, Pardoll D, Pan F. Metabolic control of the Treg/Th17 axis. Immunol Rev. 2013;252:52–77.
  • Duan Y, Gu X, Zhu D, et al. Schistosoma japonicum soluble egg antigens induce apoptosis and inhibit activation of hepatic stellate cells: a possible molecular mechanism. Int J Parasitol. 2014;44:217–224.
  • Nawaz M, Malik MI, Hameed M, et al. Research progress on the composition and function of parasite-derived exosomes. Acta Trop. 2019;196:30–36.
  • He X, Wang Y, Fan X, et al. A schistosome miRNA promotes host hepatic fibrosis by targeting transforming growth factor beta receptor III. J Hepatol. 2020;72:519–527.
  • Patel GK, Khan MA, Zubair H, et al. Comparative analysis of exosome isolation methods using culture supernatant for optimum yield, purity and downstream applications. Sci Rep. 2019;9:5335.
  • Paolini L, Zendrini A, Di Noto G, et al. Residual matrix from different separation techniques impacts exosome biological activity. Sci Rep. 2016;6:23550.
  • Kulkarni B, Kirave P, Gondaliya P, et al. Exosomal miRNA in chemoresistance, immune evasion, metastasis and progression of cancer. Drug Discov Today. 2019;24:2058–2067.
  • Samoil V, Dagenais M, Ganapathy V, et al. Vesicle-based secretion in schistosomes: analysis of protein and microRNA (miRNA) content of exosome-like vesicles derived from Schistosoma mansoni. Sci Rep. 2018;8:1–16.
  • Fromm B, Trelis M, Hackenberg M, et al. The revised microRNA complement of Fasciola hepatica reveals a plethora of overlooked microRNAs and evidence for enrichment of immuno-regulatory microRNAs in extracellular vesicles. Int J Parasitol. 2015;45:697–702.
  • Zheng Y, Cai X, Bradley JE. microRNAs in parasites and parasite infection. RNA Biol. 2013;10:371–379.
  • Lei X-F, Fu W, Kim-Kaneyama J-R, et al. Hic-5 deficiency attenuates the activation of hepatic stellate cells and liver fibrosis through upregulation of Smad7 in mice. J Hepatol. 2016;64:110–117.
  • Attisano L, Wrana JL. Signal transduction by the TGF-β superfamily. Science. 2002;296: 1646–1467.
  • Yoshida K, Matsuzaki K, Mori S, et al. Transforming growth factor-β and platelet-derived growth factor signal via c-Jun N-terminal kinase-dependent Smad2/3 phosphorylation in rat hepatic stellate cells after acute liver injury. Am J Pathol. 2005;166:1029–1039.
  • Xu F, Liu C, Zhou D, et al. TGF-β/SMAD pathway and its regulation in hepatic fibrosis. J Histochem Cytochem. 2016;64:157–167.
  • Lee CG, Cho SJ, Kang MJ, et al. Early growth response gene 1–mediated apoptosis is essential for transforming growth factor β1–induced pulmonary fibrosis. J Exp Med. 2004;200:377–389.
  • Oh C, Geba G, Molfino N. Investigational therapeutics targeting the IL-4/IL-13/STAT-6 pathway for the treatment of asthma. Eur Respir Rev. 2010;19:46–54.
  • Witherden DA, Watanabe M, Garijo O, et al. The CD100 receptor interacts with its plexin B2 ligand to regulate epidermal γδ T cell function. Immunity. 2012;37:314–325.
  • Wynn TA, Thompson RW, Cheever AW, et al. Immunopathogenesis of schistosomiasis. Immunol Rev. 2004;201:156–167.
  • Chen D, Luo X, Xie H, et al. Characteristics of IL‐17 induction by Schistosoma japonicum infection in C57 BL/6 mouse liver. Immunology. 2013;139:523–532.
  • Fichtner-Feigl S, Strober W, Kawakami K, et al. IL-13 signaling through the IL-13α 2 receptor is involved in induction of TGF-β 1 production and fibrosis. Nat Med. 2006;12:99–106.