Research progress on the role of schistosome and its derivatives on modulation of immune dysregulatory diseases

doi:10.12140/j.issn.1000-7423.2023.01.013

Abstract

Abstract:

Schistosoma sp. is a parasite infect in mammals including humans. During co-evolution of host and schistosomes, the parasite have developed mechanisms that manipulate the host innate and adaptive immunity to create a microenviroments that benefi its survival. Recently, the pharmacological effects of schistosome infection and relevant molecules in the management of allergy, autoimmune and metabolic diseases has attracted great attention. This article reviews the modulatory role and underlying mechanisms of schistosomes and their derivatives in immune dysregulatory diseases, to provide a basis for subsequent laboratory and clinical investigations.

Key words: Schistosome, Derivatives, Immunoregulation, Immune dysregulatory diseases

CLC Number:

R383.24

LI Gen, SUN Tongjun, QIAN Yayun, LI Qianqian, YANG Xiaodi. Research progress on the role of schistosome and its derivatives on modulation of immune dysregulatory diseases[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2023, 41(1): 85-91.

Figures/Tables 1

References 67

[1]	Bach JF. The hygiene hypothesis in autoimmunity: the role of pathogens and commensals[J]. Nat Rev Immunol, 2018, 18(2): 105-120. doi: 10.1038/nri.2017.111
[2]	Mu SS, Yang JQ. Relationship between parasitic infections and hygiene hypothesis: a review[J]. Chin J Schisto Control, 2020, 32(2): 203-207. (in Chinese)
	(穆莎莎, 杨俊齐. 寄生虫感染与“卫生假说”关系研究进展[J]. 中国血吸虫病防治杂志, 2020, 32(2): 203-207.)
[3]	Xu ZP, Ji MJ, Wu GL. The toxicological and pharmacological effects of parasite derived components on the host[J]. Chin J Parasitol Parasit Dis, 2022, 40(4): 1-11. (in Chinese)
	(徐志鹏, 季旻珺, 吴观陵. 寄生虫虫源性成分对宿主的毒理与药理效应[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(4): 1-11.)
[4]	Mu Y, McManus DP, Hou N, et al. Schistosome infection and schistosome-derived products as modulators for the prevention and alleviation of immunological disorders[J]. Front Immunol, 2021, 12: 619776. doi: 10.3389/fimmu.2021.619776
[5]	Cai ZS, Deng X, Zhao L, et al. The relationship between Schistosoma and glycolipid metabolism[J]. Microb Pathog, 2021, 159: 105120. doi: 10.1016/j.micpath.2021.105120
[6]	Li JH, Liu H, Jiang J, et al. The potential role of schistosome-associated factors as therapeutic modulators of the immune system[J]. Infect Immun, 2020, 88(8): e00754-e00719.
[7]	Souza COS, Gardinassi LG, Rodrigues V, et al. Monocyte and macrophage-mediated pathology and protective immunity during schistosomiasis[J]. Front Microbiol, 2020, 11: 1973. doi: 10.3389/fmicb.2020.01973 pmid: 32922381
[8]	Ho CH, Cheng CH, Huang TW, et al. Switched phenotypes of macrophages during the different stages of Schistosoma japonicum infection influenced the subsequent trends of immune responses[J]. J Microbiol Immunol Infect, 2022, 55(3): 503-526. doi: 10.1016/j.jmii.2021.06.005
[9]	Chen Y, Wei BG, Xu PP, et al. Schistosoma japonicum cystatin suppresses osteoclastogenesis via manipulating the NF-κB signaling pathway[J]. Mol Med Rep, 2021, 23(4): 273. doi: 10.3892/mmr
[10]	Sun X, Lv ZY, Peng H, et al. Effects of a recombinant schistosomal-derived anti-inflammatory molecular (rSj16) on the lipopolysaccharide (LPS)-induced activated RAW_264.7[J]. Parasitol Res, 2012, 110(6): 2429-2437. doi: 10.1007/s00436-011-2782-9 pmid: 22281546
[11]	Liu J, Pan T, You X, et al. SjCa8, a calcium-binding protein from Schistosoma japonicum, inhibits cell migration and suppresses nitric oxide release of RAW_264.7 macrophages[J]. Parasit Vectors, 2015, 8: 513. doi: 10.1186/s13071-015-1119-4 pmid: 26445908
[12]	Shen P, Zhang TY, Chen G, et al. Recombinant P40 protein of Schistosoma japonicum inhibits TREM-1 expression in RAW_264.7 cells via FOXO3a[J]. Biomed Pharmacother, 2022, 149: 112826. doi: 10.1016/j.biopha.2022.112826
[13]	Winkel BMF, Dalenberg MR, de Korne CM, et al. Early induction of human regulatory dermal antigen presenting cells by skin-penetrating Schistosoma mansoni cercariae[J]. Front Immunol, 2018, 9: 2510. doi: 10.3389/fimmu.2018.02510
[14]	Sun X, Yang F, Shen J, et al. Recombinant Sj16 from Schistosoma japonicum contains a functional N-terminal nuclear localization signal necessary for nuclear translocation in dendritic cells and interleukin-10 production[J]. Parasitol Res, 2016, 115(12): 4559-4571. pmid: 27640151
[15]	Lopes DM, Oliveira SC, Page B, et al. Schistosoma mansoni rSm29 antigen induces a regulatory phenotype on dendritic cells and lymphocytes from patients with cutaneous leishmaniasis[J]. Front Immunol, 2019, 9: 3122. doi: 10.3389/fimmu.2018.03122
[16]	Kaisar MMM, Ritter M, Del Fresno C, et al. Dectin-1/2-induced autocrine PGE2 signaling licenses dendritic cells to prime Th2 responses[J]. PLoS Biol, 2018, 16(4): e2005504. doi: 10.1371/journal.pbio.2005504
[17]	Klaver EJ, Kuijk LM, Lindhorst TK, et al. Schistosoma mansoni soluble egg antigens induce expression of the negative regulators SOCS₁ and SHP₁ in human dendritic cells via interaction with the mannose receptor[J]. PLoS One, 2015, 10(4): e0124089. doi: 10.1371/journal.pone.0124089
[18]	Webb LM, Phythian-Adams AT, Costain AH, et al. Plasmacytoid dendritic cells facilitate Th cell cytokine responses throughout Schistosoma mansoni infection[J]. ImmunoHorizons, 2021, 5(8): 721-732. doi: 10.4049/immunohorizons.2100071
[19]	Zhao Y, Yang Q, Jin CX, et al. Changes of CD103-expressing pulmonary CD4⁺ and CD8⁺ T cells in S. japonicum infected C57BL/6 mice[J]. BMC Infect Dis, 2019, 19(1): 999. doi: 10.1186/s12879-019-4633-8 pmid: 31775660
[20]	Meningher T, Barsheshet Y, Ofir-Birin Y, et al. Schistosomal extracellular vesicle-enclosed miRNAs modulate host T helper cell differentiation[J]. EMBO Rep, 2020, 21(1): e47882.
[21]	Qi QQ, Wang XF, Zhang LN, et al. Schistosoma japonicum heat shock protein 60 enhances regulatory T cell immunosuppressive function by promoting the expressions of IL-10 and TGF-β[J]. Chin J Schisto Control, 2018, (01): 42-46. (in Chinese)
	(齐倩倩, 王小番, 张丽娜, 等. 日本血吸虫热休克蛋白60通过诱导细胞表达IL-10和TGF-β增强其免疫抑制功能[J]. 中国血吸虫病防治杂志, 2018, (1): 42-46.)
[22]	Gao YR, Chen WW, Li JW, et al. Treg/Th17 balance and immunology of schistosome infection: a review[J]. Chin J Schisto Control, 2018, 30(5): 588-591. (in Chinese)
	(高彦茹, 陈尉文, 李佳望, 等. Treg/Th17平衡与血吸虫感染免疫[J]. 中国血吸虫病防治杂志, 2018, 30(5): 588-591.)
[23]	Du JW, Wang XF. Research progress on the role of schistosomiasis in regulating autoimmune and allergic diseases[J]. Chin J Parasitol Parasit Dis, 2011, 29(6): 473-476. (in Chinese)
	(杜久伟, 汪雪峰. 血吸虫感染调节自身免疫性疾病和过敏性疾病的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2011, 29(6): 473-476.)
[24]	Schramm G, Suwandi A, Galeev A, et al. Schistosome eggs impair protective Th1/Th17 immune responses against Salmonella infection[J]. Front Immunol, 2018, 9: 2614. doi: 10.3389/fimmu.2018.02614
[25]	Li L, Shan WQ, Zhu HJ, et al. SJMHE1 peptide from Schistosoma japonicum inhibits asthma in mice by regulating Th17/treg cell balance via miR-155[J]. J Inflamm Res, 2021, 14: 5305-5318. doi: 10.2147/JIR.S334636 pmid: 34703270
[26]	Xiao JL, Guan F, Sun L, et al. B cells induced by Schistosoma japonicum infection display diverse regulatory phenotypes and modulate CD4⁺ T cell response[J]. Parasit Vectors, 2020, 13(1): 147. doi: 10.1186/s13071-020-04015-3
[27]	van der Vlugt LEPM, Zinsou JF, Ozir-Fazalalikhan A, et al. Interleukin 10 (IL-10)-producing CD1d^hi regulatory B cells from Schistosoma haematobium-infected individuals induce IL-10-positive T cells and suppress effector T-cell cytokines[J]. J Infect Dis, 2014, 210(8): 1207-1216. doi: 10.1093/infdis/jiu257
[28]	Haeberlein S, Obieglo K, Ozir-Fazalalikhan A, et al. Schistosome egg antigens, including the glycoprotein IPSE/alpha-1, trigger the development of regulatory B cells[J]. PLoS Pathog, 2017, 13(7): e1006539. doi: 10.1371/journal.ppat.1006539
[29]	Fernandes JS, Cardoso LS, Pitrez PM, et al. Helminths and asthma: risk and protection[J]. Immunol Allergy Clin North Am, 2019, 39(3): 417-427. doi: 10.1016/j.iac.2019.03.009
[30]	Li ZD, Zhang W, Luo F, et al. Allergen-specific treg cells upregulated by lung-stage S. japonicum infection alleviates allergic airway inflammation[J]. Front Cell Dev Biol, 2021, 9: 678377. doi: 10.3389/fcell.2021.678377
[31]	van der Vlugt LEPM, Obieglo K, Ozir-Fazalalikhan A, et al. Schistosome-induced pulmonary B cells inhibit allergic airway inflammation and display a reduced Th2-driving function[J]. Int J Parasitol, 2017, 47(9): 545-554. doi: S0020-7519(17)30098-X pmid: 28385494
[32]	Wang T, Shan WQ, Xue F, et al. Schistosoma japonicum polypeptide SJMHE1 attenuates airway inflammation by inhibiting Th2 cells and ILC2 responses in lung tissues of asthmatic mice[J]. Chin J Cell Mol Immunol, 2021, 37(12): 1106-1110. (in Chinese)
	(王婷, 单文琪, 薛菲, 等. 日本血吸虫多肽SJMHE1通过抑制哮喘小鼠肺组织中Th2细胞和ILC2反应减轻小鼠气道炎症[J]. 细胞与分子免疫学杂志, 2021, 37(12): 1106-1110.)
[33]	Zhang WZ, Li L, Zheng Y, et al. Schistosoma japonicum peptide SJMHE1 suppresses airway inflammation of allergic asthma in mice[J]. J Cell Mol Med, 2019, 23(11): 7819-7829. doi: 10.1111/jcmm.v23.11
[34]	Marinho FV, Alves CC, de Souza SC, et al. Schistosoma mansoni tegument (smteg) induces IL-10 and modulates experimental airway inflammation[J]. PLoS One, 2016, 11(7): e0160118. doi: 10.1371/journal.pone.0160118
[35]	He L, Zhou S, Qi QQ, et al. The regulation of regulation: Interleukin-10 increases CD4⁺ CD25⁺ regulatory T cells but impairs their immunosuppressive activity in murine models with schistosomiasis japonica or asthma[J]. Immunology, 2018, 153(1): 84-96. doi: 10.1111/imm.12813
[36]	Kaplan GG. The global burden of IBD: from 2015 to 2025[J]. Nat Rev Gastroenterol Hepatol, 2015, 12(12): 720-727. doi: 10.1038/nrgastro.2015.150 pmid: 26323879
[37]	Pêgo B, Martinusso CA, Bernardazzi C, et al. Schistosoma mansoni coinfection attenuates murine Toxoplasma gondii-induced Crohn’s-like ileitis by preserving the epithelial barrier and downregulating the inflammatory response[J]. Front Immunol, 2019, 10: 442. doi: 10.3389/fimmu.2019.00442
[38]	Zhou HL, Zeng XJ, Sun DC, et al. Monosexual cercariae of Schistosoma japonicum infection protects against DSS-induced colitis by shifting the Th1/Th2 balance and modulating the gut Microbiota[J]. Front Microbiol, 2021, 11: 606605. doi: 10.3389/fmicb.2020.606605
[39]	Driss V, El Nady M, Delbeke M, et al. The schistosome glutathione S-transferase P28GST, a unique helminth protein, prevents intestinal inflammation in experimental colitis through a Th2-type response with mucosal eosinophils[J]. Mucosal Immunol, 2016, 9(2): 322-335. doi: 10.1038/mi.2015.62 pmid: 26174763
[40]	Sarazin A, Dendooven A, Delbeke M, et al. Treatment with P28GST, a schistosome-derived enzyme, after acute colitis induction in mice: decrease of intestinal inflammation associated with a down regulation of Th1/Th17 responses[J]. PLoS One, 2018, 13(12): e0209681. doi: 10.1371/journal.pone.0209681
[41]	Capron M, Béghin L, Leclercq C, et al. Safety of P28GST, a protein derived from a schistosome helminth parasite, in patients with Crohn’s disease: a pilot study (ACROHNEM)[J]. J Clin Med, 2019, 9(1): 41. doi: 10.3390/jcm9010041
[42]	Floudas A, Aviello G, Schwartz C, et al. Schistosoma mansoni worm infection regulates the intestinal Microbiota and susceptibility to colitis[J]. Infect Immun, 2019, 87(8): e00275-e00219.
[43]	Zhang BB, Wu XY, Song QY, et al. Gut Microbiota modulates intestinal pathological injury in Schistosoma japonicum-infected mice[J]. Front Med (Lausanne), 2020, 7: 588928.
[44]	Zhu TY, Xue QK, Liu YY, et al. Analysis of intestinal microflora and metabolites from mice with DSS-induced IBD treated with Schistosoma soluble egg antigen[J]. Front Cell Dev Biol, 2021, 9: 777218. doi: 10.3389/fcell.2021.777218
[45]	Zhu YJ, Xu ZP, Ji MJ. Advances in the research on the interaction between human parasites and gut microbiota[J]. Chin J Schisto Control, 2020, 32(6): 649-653. (in Chinese)
	(朱元杰, 徐志鹏, 季旻珺. 人体寄生虫与肠道菌群相互作用的研究进展[J]. 中国血吸虫病防治杂志, 2020, 32(6): 649-653.)
[46]	Weng JP. The epidemic study and burden of type 1 diabetes in China[J]. Sci Sin Vitae, 2018, 48(8): 834-839. (in Chinese) doi: 10.1360/N052018-00016
	(翁建平. 我国1型糖尿病的流行病学研究与疾病负担[J]. 中国科学: 生命科学, 2018, 48(8): 834-839.)
[47]	Mughal MAS, Khan MK, Abbas Z, et al. Helminth protection against type-1 diabetes: an insight into immunomodulatory effect of helminth-induced infection[J]. Mol Biol Rep, 2021, 48(9): 6581-6588. doi: 10.1007/s11033-021-06663-9 pmid: 34432219
[48]	Zaccone P, Burton OT, Gibbs S, et al. Immune modulation by Schistosoma mansoni antigens in NOD mice: effects on both innate and adaptive immune systems[J]. J Biomed Biotechnol, 2010, 2010: 795210.
[49]	Yan K, Wang B, Zhou HB, et al. Amelioration of type 1 diabetes by recombinant fructose-1, 6-bisphosphate aldolase and cystatin derived from Schistosoma japonicum in a murine model[J]. Parasitol Res, 2020, 119(1): 203-214. doi: 10.1007/s00436-019-06511-7 pmid: 31845020
[50]	Osada Y, Fujiyama T, Kamimura N, et al. Dual genetic absence of STAT6 and IL-10 does not abrogate anti-hyperglycemic effects of Schistosoma mansoni in streptozotocin-treated diabetic mice[J]. Exp Parasitol, 2017, 177: 1-12. doi: 10.1016/j.exppara.2017.03.008
[51]	Rudd KE, Johnson SC, Agesa KM, et al. Global, regional, and national sepsis incidence and mortality, 1990—2017: analysis for the global burden of disease study[J]. Lancet, 2020, 395(10219): 200-211. doi: 10.1016/S0140-6736(19)32989-7
[52]	Tang H, Liang YB, Chen ZB, et al. Soluble egg antigen activates M2 macrophages via the STAT6 and PI3K pathways, and Schistosoma japonicum alternatively activates macrophage polarization to improve the survival rate of septic mice[J]. J Cell Biochem, 2017, 118(12): 4230-4239. doi: 10.1002/jcb.26073 pmid: 28419526
[53]	Li HH, Wang SS, Zhan B, et al. Therapeutic effect of Schistosoma japonicum cystatin on bacterial sepsis in mice[J]. Parasites Vectors, 2017, 10(1): 222. doi: 10.1186/s13071-017-2162-0
[54]	Gao SF, Li HH, Xie H, et al. Therapeutic efficacy of Schistosoma japonicum cystatin on sepsis-induced cardiomyopathy in a mouse model[J]. Parasit Vectors, 2020, 13(1): 260. doi: 10.1186/s13071-020-04104-3
[55]	Xie H, Wu LQ, Chen XZ, et al. Schistosoma japonicum cystatin alleviates sepsis through activating regulatory macrophages[J]. Front Cell Infect Microbiol, 2021, 11: 617461. doi: 10.3389/fcimb.2021.617461
[56]	Collaborators GBD2O, Afshin A, Forouzanfar MH, et al. Health effects of overweight and obesity in 195 countries over 25 years[J]. N Engl J Med, 2017, 377(1): 13-27. doi: 10.1056/NEJMoa1614362
[57]	Zinsou JF, Janse JJ, Honpkehedji YY, et al. Schistosoma haematobium infection is associated with lower serum cholesterol levels and improved lipid profile in overweight/obese individuals[J]. PLoS Negl Trop Dis, 2020, 14(7): e0008464. doi: 10.1371/journal.pntd.0008464
[58]	Hussaarts L, García-Tardón N, van Beek L, et al. Chronic helminth infection and helminth-derived egg antigens promote adipose tissue M2 macrophages and improve insulin sensitivity in obese mice[J]. FASEB J, 2015, 29(7): 3027-3039. doi: 10.1096/fj.14-266239 pmid: 25852044
[59]	van den Berg SM, Dam ADV, Kusters PJH, et al. Helminth antigens counteract a rapid high-fat diet-induced decrease in adipose tissue eosinophils[J]. J Mol Endocrinol, 2017, 59(3): 245-255. doi: 10.1530/JME-17-0112 pmid: 28694301
[60]	van der Zande HJP, Gonzalez MA, de Ruiter K, et al. The helminth glycoprotein omega-1 improves metabolic homeostasis in obese mice through type 2 immunity-independent inhibition of food intake[J]. FASEB J, 2021, 35(2): e21331.
[61]	Li MN, Wang HQ, Ni YY, et al. Helminth-induced CD9⁺ B-cell subset alleviates obesity-associated inflammation via IL-10 production[J]. Int J Parasitol, 2022, 52(2/3): 111-123. doi: 10.1016/j.ijpara.2021.08.009
[62]	Cortes-Selva D, Elvington AF, Ready A, et al. Schistosoma mansoni infection-induced transcriptional changes in hepatic macrophage metabolism correlate with an athero-protective phenotype[J]. Front Immunol, 2018, 9: 2580. doi: 10.3389/fimmu.2018.02580 pmid: 30483256
[63]	Yang HJ, Li HQ, Chen WD, et al. Therapeutic effect of Schistosoma japonicum cystatin on atherosclerotic renal damage[J]. Front Cell Dev Biol, 2021, 9: 760980. doi: 10.3389/fcell.2021.760980
[64]	Li YN, Yang XD, Chen SY, et al. Effect of recombinant cysteine protease inhibitor of Schistosoma japonicum on prognosis of myocardial infarction in mice and its immuno-regulation mechanism[J]. Chin J Biol, 2022, 35(1): 55-62. (in Chinese)
	(李燕楠, 杨小迪, 陈思宇, 等. 日本血吸虫重组半胱氨酸蛋白酶抑制剂对小鼠心肌梗死预后的影响及其免疫调节机制[J]. 中国生物制品学杂志, 2022, 35(1): 55-62.)
[65]	Peng B, She XG, Cheng K, et al. Orthotopic liver transplantation from a donor with Schistosoma japonicum[J]. Hepatobiliary Pancreat Dis Int, 2017, 16(3): 326-328. doi: 10.1016/S1499-3872(17)60023-7
[66]	Mahmoud KM, Sobh MA, El-Agroudy AE, et al. Impact of schistosomiasis on patient and graft outcome after renal transplantation: 10 years’ follow-up[J]. Nephrol Dial Transplant, 2001, 16(11): 2214-2221. doi: 10.1093/ndt/16.11.2214
[67]	Arroyo-López C. Helminth therapy for autism under gut-brain axis-hypothesis[J]. Med Hypotheses, 2019, 125: 110-118. doi: S0306-9877(18)31248-9 pmid: 30902137