SJMHE1 Peptide from Schistosoma japonicum Inhibits Asthma in Mice by Regulating Th17/Treg Cell Balance via miR-155

References

• Xue F, Yu M, Li L, et al. Elevated granulocytic myeloid-derived suppressor cells are closely related with elevation of Th17 cells in mice with experimental asthma. Int J Biol Sci. 2020;16(12):2072–2083. doi:10.7150/ijbs.43596
   PubMed Web of Science ®Google Scholar
• Muehling LM, Lawrence MG, Woodfolk JA. Pathogenic CD4(+) T cells in patients with asthma. J Allergy Clin Immunol. 2017;140(6):1523–1540. doi:10.1016/j.jaci.2017.02.025
   PubMed Web of Science ®Google Scholar
• Shi YH, Shi GC, Wan HY, et al. Coexistence of Th1/Th2 and Th17/Treg imbalances in patients with allergic asthma. Chin Med J (Engl). 2011;124(13):1951–1956.
   PubMed Web of Science ®Google Scholar
• Corren J, Lemanske RF, Hanania NA, et al. Lebrikizumab treatment in adults with asthma. N Engl J Med. 2011;365(12):1088–1098. doi:10.1056/NEJMoa1106469
   PubMed Web of Science ®Google Scholar
• Just J, Deschildre A, Lejeune S, Amat F. New perspectives of childhood asthma treatment with biologics. Pediatr Allergy Immunol. 2019;30(2):159–171.
   PubMed Web of Science ®Google Scholar
• Maizels RM, McSorley HJ. Regulation of the host immune system by helminth parasites. J Allergy Clin Immunol. 2016;138(3):666–675. doi:10.1016/j.jaci.2016.07.007
   PubMed Web of Science ®Google Scholar
• Gazzinelli-Guimaraes PH, Nutman TB. Helminth parasites and immune regulation. F1000Res. 2018;7:F1000 Faculty Rev–1685. doi:10.12688/f1000research.15596.1
   PubMedGoogle Scholar
• Maizels RM. Regulation of immunity and allergy by helminth parasites. Allergy. 2020;75(3):524–534. doi:10.1111/all.13944
   PubMed Web of Science ®Google Scholar
• Fernandes JS, Cardoso LS, Pitrez PM, Cruz AA. Helminths and asthma: risk and protection. Immunol Allergy Clin North Am. 2019;39(3):417–427. doi:10.1016/j.iac.2019.03.009
   PubMed Web of Science ®Google Scholar
• Bohnacker S, Troisi F, de Los Reyes Jimenez M, Esser-von Bieren J. What can parasites tell us about the pathogenesis and treatment of asthma and allergic diseases. Front Immunol. 2020;11:2106. doi:10.3389/fimmu.2020.02106
   PubMed Web of Science ®Google Scholar
• Pacifico LG, Marinho FA, Fonseca CT, et al. Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3+ T cells independent of interleukin-10. Infect Immun. 2009;77(1):98–107. doi:10.1128/IAI.00783-07
   PubMed Web of Science ®Google Scholar
• Navarro S, Pickering DA, Ferreira IB, et al. Hookworm recombinant protein promotes regulatory T cell responses that suppress experimental asthma. Sci Transl Med. 2016;8(362):362ra143. doi:10.1126/scitranslmed.aaf8807
   PubMed Web of Science ®Google Scholar
• Logan J, Navarro S, Loukas A, Giacomin P. Helminth-induced regulatory T cells and suppression of allergic responses. Curr Opin Immunol. 2018;54:1–6. doi:10.1016/j.coi.2018.05.007
   PubMed Web of Science ®Google Scholar
• Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol. 2010;125(5):1114–1124e1118. doi:10.1016/j.jaci.2010.01.018
   PubMed Web of Science ®Google Scholar
• Coltherd JC, Rodgers DT, Lawrie RE, et al. The parasitic worm-derived immunomodulator, ES-62 and its drug-like small molecule analogues exhibit therapeutic potential in a model of chronic asthma. Sci Rep. 2016;6(1):19224. doi:10.1038/srep19224
   PubMedGoogle Scholar
• Obieglo K, Schuijs MJ, Ozir-Fazalalikhan A, et al. Isolated Schistosoma mansoni eggs prevent allergic airway inflammation. Parasite Immunol. 2018;40(10):e12579. doi:10.1111/pim.12579
   PubMed Web of Science ®Google Scholar
• Reece JJ, Siracusa MC, Southard TL, Brayton CF, Urban JF Jr., Scott AL. Hookworm-induced persistent changes to the immunological environment of the lung. Infect Immun. 2008;76(8):3511–3524. doi:10.1128/IAI.00192-08
   PubMed Web of Science ®Google Scholar
• Wang X, Zhou S, Chi Y, et al. CD4+CD25+ Treg induction by an HSP60-derived peptide SJMHE1 from Schistosoma japonicum is TLR2 dependent. Eur J Immunol. 2009;39(11):3052–3065. doi:10.1002/eji.200939335
   PubMed Web of Science ®Google Scholar
• Wang X, Wang J, Liang Y, et al. Schistosoma japonicum HSP60-derived peptide SJMHE1 suppresses delayed-type hypersensitivity in a murine model. Parasit Vectors. 2016;9(1):147. doi:10.1186/s13071-016-1434-4
   PubMedGoogle Scholar
• Wang X, Li L, Wang J, et al. Inhibition of cytokine response to TLR stimulation and alleviation of collagen-induced arthritis in mice by Schistosoma japonicum peptide SJMHE1. J Cell Mol Med. 2017;21(3):475–486. doi:10.1111/jcmm.12991
   PubMed Web of Science ®Google Scholar
• Zhang W, Li L, Zheng Y, et al. Schistosoma japonicum peptide SJMHE1 suppresses airway inflammation of allergic asthma in mice. J Cell Mol Med. 2019;23(11):7819–7829. doi:10.1111/jcmm.14661
   PubMed Web of Science ®Google Scholar
• Chen Y, Mao ZD, Shi YJ, et al. Comprehensive analysis of miRNA-mRNA-lncRNA networks in severe asthma. Epigenomics. 2019;11(2):115–131. doi:10.2217/epi-2018-0132
   PubMed Web of Science ®Google Scholar
• Specjalski K, Jassem E. MicroRNAs: potential biomarkers and targets of therapy in allergic diseases? Arch Immunol Ther Exp (Warsz). 2019;67(4):213–223. doi:10.1007/s00005-019-00547-4
   PubMed Web of Science ®Google Scholar
• Suojalehto H, Lindstrom I, Majuri ML, et al. Altered microRNA expression of nasal mucosa in long-term asthma and allergic rhinitis. Int Arch Allergy Immunol. 2014;163(3):168–178. doi:10.1159/000358486
   PubMed Web of Science ®Google Scholar
• Xiao R, Noel A, Perveen Z, Penn AL. In utero exposure to second-hand smoke activates pro-asthmatic and oncogenic miRNAs in adult asthmatic mice. Environ Mol Mutagen. 2016;57(3):190–199. doi:10.1002/em.21998
   PubMed Web of Science ®Google Scholar
• Zhou H, Li J, Gao P, Wang Q, Zhang J. miR-155: a novel target in allergic asthma. Int J Mol Sci. 2016;17(10):10. doi:10.3390/ijms17101773
   Web of Science ®Google Scholar
• Banerjee A, Schambach F, DeJong CS, Hammond SM, Reiner SL. Micro-RNA-155 inhibits IFN-gamma signaling in CD4+ T cells. Eur J Immunol. 2010;40(1):225–231. doi:10.1002/eji.200939381
   PubMed Web of Science ®Google Scholar
• Kohlhaas S, Garden OA, Scudamore C, Turner M, Okkenhaug K, Vigorito E. Cutting edge: the Foxp3 target miR-155 contributes to the development of regulatory T cells. J Immunol. 2009;182(5):2578–2582. doi:10.4049/jimmunol.0803162
   PubMed Web of Science ®Google Scholar
• Wang D, Tang M, Zong P, et al. MiRNA-155 regulates the Th17/Treg ratio by targeting SOCS1 in severe acute pancreatitis. Front Physiol. 2018;9:686. doi:10.3389/fphys.2018.00686
   PubMed Web of Science ®Google Scholar
• Malmhall C, Alawieh S, Lu Y, et al. MicroRNA-155 is essential for T(H)2-mediated allergen-induced eosinophilic inflammation in the lung. J Allergy Clin Immunol. 2014;133(5):1429–1438. doi:10.1016/j.jaci.2013.11.008
   PubMed Web of Science ®Google Scholar
• Bergallo M, Accorinti M, Galliano I, et al. Expression of miRNA 155, FOXP3 and ROR gamma, in children with moderate and severe atopic dermatitis. G Ital Dermatol Venereol. 2020;155(2):168–172. doi:10.23736/S0392-0488.17.05707-8
   PubMed Web of Science ®Google Scholar
• Xia G, Wu S, Wang X, Fu M. Inhibition of microRNA-155 attenuates concanavalin-A-induced autoimmune hepatitis by regulating Treg/Th17 cell differentiation. Can J Physiol Pharmacol. 2018;96(12):1293–1300. doi:10.1139/cjpp-2018-0467
   PubMed Web of Science ®Google Scholar
• Wang L, Wan H, Tang W, et al. Critical roles of adenosine A2A receptor in regulating the balance of Treg/Th17 cells in allergic asthma. Clin Respir J. 2018;12(1):149–157. doi:10.1111/crj.12503
   PubMed Web of Science ®Google Scholar
• Escobar T, Yu CR, Muljo SA, Egwuagu CE. STAT3 activates miR-155 in Th17 cells and acts in concert to promote experimental autoimmune uveitis. Invest Ophthalmol Vis Sci. 2013;54(6):4017–4025. doi:10.1167/iovs.13-11937
   PubMed Web of Science ®Google Scholar
• Lu LF, Thai TH, Calado DP, et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity. 2009;30(1):80–91. doi:10.1016/j.immuni.2008.11.010
   PubMed Web of Science ®Google Scholar
• Wei L, Laurence A, O’Shea JJ. New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation. Semin Cell Dev Biol. 2008;19(4):394–400. doi:10.1016/j.semcdb.2008.07.011
   PubMed Web of Science ®Google Scholar
• Escobar TM, Kanellopoulou C, Kugler DG, et al. miR-155 activates cytokine gene expression in Th17 cells by regulating the DNA-binding protein Jarid2 to relieve polycomb-mediated repression. Immunity. 2014;40(6):865–879. doi:10.1016/j.immuni.2014.03.014
   PubMed Web of Science ®Google Scholar
• Qiu L, Zhang Y, Do DC, et al. miR-155 modulates cockroach allergen- and oxidative stress-induced cyclooxygenase-2 in asthma. J Immunol. 2018;201(3):916–929. doi:10.4049/jimmunol.1701167
   PubMed Web of Science ®Google Scholar
• Ding F, Fu Z, Liu B. Lipopolysaccharide exposure alleviates asthma in mice by regulating Th1/Th2 and Treg/Th17 balance. Med Sci Monit. 2018;24:3220–3229. doi:10.12659/MSM.905202
   PubMed Web of Science ®Google Scholar
• Liang P, Peng S, Zhang M, Ma Y, Zhen X, Huai LH. Qi Huang corrects the balance of Th1/Th2 and Treg/Th17 in an ovalbumin-induced asthma mouse model. Biosci Rep. 2017;37(6):BSR20171071. doi:10.1042/BSR20171071
   PubMedGoogle Scholar
• Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16(1):45–56. doi:10.1038/ni.3049
   PubMed Web of Science ®Google Scholar
• Allen JE, Sutherland TE, Ruckerl D. IL-17 and neutrophils: unexpected players in the type 2 immune response. Curr Opin Immunol. 2015;34:99–106. doi:10.1016/j.coi.2015.03.001
   PubMed Web of Science ®Google Scholar
• Nanzer AM, Chambers ES, Ryanna K, et al. Enhanced production of IL-17A in patients with severe asthma is inhibited by 1alpha,25-dihydroxyvitamin D3 in a glucocorticoid-independent fashion. J Allergy Clin Immunol. 2013;132(2):297–304. doi:10.1016/j.jaci.2013.03.037
   PubMed Web of Science ®Google Scholar
• McKinley L, Alcorn JF, Peterson A, et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol. 2008;181(6):4089–4097. doi:10.4049/jimmunol.181.6.4089
   PubMed Web of Science ®Google Scholar
• Entwistle LJ, Wilson MS. MicroRNA-mediated regulation of immune responses to intestinal helminth infections. Parasite Immunol. 2017;39(2):e12406. doi:10.1111/pim.12406
   Web of Science ®Google Scholar
• Terrazas LI, Sanchez-Munoz F, Perez-Miranda M, et al. Helminth excreted/secreted antigens repress expression of LPS-induced Let-7i but not miR-146a and miR-155 in human dendritic cells. Biomed Res Int. 2013;2013:972506. doi:10.1155/2013/972506
   PubMed Web of Science ®Google Scholar
• Okoye IS, Czieso S, Ktistaki E, et al. Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity. Proc Natl Acad Sci U S A. 2014;111(30):E3081–3090. doi:10.1073/pnas.1406322111
   PubMed Web of Science ®Google Scholar
• Yao R, Ma YL, Liang W, et al. MicroRNA-155 modulates Treg and Th17 cells differentiation and Th17 cell function by targeting SOCS1. PLoS One. 2012;7(10):e46082. doi:10.1371/journal.pone.0046082
   PubMed Web of Science ®Google Scholar
• Wan CK, Andraski AB, Spolski R, et al. Opposing roles of STAT1 and STAT3 in IL-21 function in CD4+ T cells. Proc Natl Acad Sci U S A. 2015;112(30):9394–9399. doi:10.1073/pnas.1511711112
   PubMed Web of Science ®Google Scholar
• Zorn E, Nelson EA, Mohseni M, et al. IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STAT-dependent mechanism and induces the expansion of these cells in vivo. Blood. 2006;108(5):1571–1579. doi:10.1182/blood-2006-02-004747
   PubMed Web of Science ®Google Scholar
• Yu CR, Mahdi RR, Oh HM, et al. Suppressor of cytokine signaling-1 (SOCS1) inhibits lymphocyte recruitment into the retina and protects SOCS1 transgenic rats and mice from ocular inflammation. Invest Ophthalmol Vis Sci. 2011;52(9):6978–6986.
   PubMed Web of Science ®Google Scholar
• Jager LD, Dabelic R, Waiboci LW, et al. The kinase inhibitory region of SOCS-1 is sufficient to inhibit T-helper 17 and other immune functions in experimental allergic encephalomyelitis. J Neuroimmunol. 2011;232(1–2):108–118. doi:10.1016/j.jneuroim.2010.10.018
   PubMed Web of Science ®Google Scholar
• Park JS, Lee J, Lim MA, et al. JAK2-STAT3 blockade by AG490 suppresses autoimmune arthritis in mice via reciprocal regulation of regulatory T cells and Th17 cells. J Immunol. 2014;192(9):4417–4424. doi:10.4049/jimmunol.1300514
   PubMed Web of Science ®Google Scholar
• Ju JH, Heo YJ, Cho ML, et al. Modulation of STAT-3 in rheumatoid synovial T cells suppresses Th17 differentiation and increases the proportion of Treg cells. Arthritis Rheum. 2012;64(11):3543–3552. doi:10.1002/art.34601
   PubMedGoogle Scholar
• Dong L, Wang X, Tan J, et al. Decreased expression of microRNA-21 correlates with the imbalance of Th17 and Treg cells in patients with rheumatoid arthritis. J Cell Mol Med. 2014;18(11):2213–2224. doi:10.1111/jcmm.12353
   PubMed Web of Science ®Google Scholar
• Park JS, Kwok SK, Lim MA, et al. STA-21, a promising STAT-3 inhibitor that reciprocally regulates Th17 and Treg cells, inhibits osteoclastogenesis in mice and humans and alleviates autoimmune inflammation in an experimental model of rheumatoid arthritis. Arthritis Rheumatol. 2014;66(4):918–929. doi:10.1002/art.38305
   PubMed Web of Science ®Google Scholar
• Jhun JY, Moon SJ, Yoon BY, et al. Grape seed proanthocyanidin extract-mediated regulation of STAT3 proteins contributes to Treg differentiation and attenuates inflammation in a murine model of obesity-associated arthritis. PLoS One. 2013;8(11):e78843. doi:10.1371/journal.pone.0078843
   PubMed Web of Science ®Google Scholar