Trichinella-induced immunomodulation: Another tale of helminth success

Food and Waterborne Parasitology - Tập 27 - Trang e00164 - 2022
F. Bruschi1, D.S. Ashour2, A.A. Othman2
1School of Medicine, Department of Translational Research, N.T.M.S., Università di Pisa, Pisa, Italy
2Department of Medical Parasitology, Faculty of Medicine, Tanta University, Tanta, Egypt

Tài liệu tham khảo

Ahn, 2016, Activation and recruitment of regulatory T cells via chemokine receptor activation in Trichinella spiralis-infected mice, Korean J. Parasitol., 54, 163, 10.3347/kjp.2016.54.2.163 Alkarmi, 1995, Suppression of transplant immunity in experimental trichinellosis, Comp. Immunol. Microbiol. Infect. Dis., 18, 171, 10.1016/0147-9571(95)00005-S Aranzamendi, 2012, Trichinella spiralis-secreted products modulate DC func-tionality and expand regulatory T cells in vitro, Parasite Immunol., 34, 210, 10.1111/j.1365-3024.2012.01353.x Aranzamendi, 2013, Protection against allergic airway inflammation during the chronic and acute phases of Trichinella spiralis infection, Clin. Exp. Allergy, 43, 103, 10.1111/cea.12042 Ashour, 2013, Trichinella spiralis immunomodulation: an interactive multifactorial process, Expert. Rev. Clin. Immunol., 9, 669, 10.1586/1744666X.2013.811187 Ashour, 2014, Interactions between Trichinella spiralis infection and induced colitis in mice, J. Helminthol., 88, 210, 10.1017/S0022149X13000059 Bany, 1992, Activity of natural killer (NK) cells in the course of experimental trichinellosis in mice, Wiad. Parazytol., 38, 117 Beiting, 2007, Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta, J. Immunol., 178, 1039, 10.4049/jimmunol.178.2.1039 Belkaid, 2006, Parasites and immunoregulatory T cells, Curr. Opin. Immunol., 18, 406, 10.1016/j.coi.2006.05.014 Bendele, 2001, Animal models of rheumatoid arthritis, J. Musculoskelet. Neuronal Interact., 1, 377 Bevaart, 2010, Evaluation of therapeutic targets in animal models of arthritis: how does it relate to rheumatoid arthritis, Arthritis Rheum., 62, 2192, 10.1002/art.27503 Bian, 2001, Down-regulation of inducible nitric-oxide synthase (NOS-2) during parasite-induced gut inflammation: a path to identify a selective NOS-2 inhibitor, Mol. Pharmacol., 59, 939, 10.1124/mol.59.4.939 Bian, 2005, Helminth regulation of host IL-4Ra / Stat6 signaling: mechanism underlying NOS-2 inhibition by Trichinella spiralis, Proc. Natl. Acad. Sci., 102, 3936, 10.1073/pnas.0409461102 Bisht, 2019, Cystatin from filarial parasites suppress the clinical symptoms and pathology of experimentally induced colitis in mice by inducing T-regulatory cells, B1- cells, and alternatively activated macrophages, Biomedicines, 7, 85, 10.3390/biomedicines7040085 Blumberg, 2001, Prospects for research in inflammatory bowel disease, JAMA, 285, 643, 10.1001/jama.285.5.643 Boonmars, 2005, What is the role of p53 during the cyst formation of Trichinella spiralis? A comparable study between knockout mice and wild type mice, Parasitology., 131, 705, 10.1017/S0031182005008036 Bruschi, 2002, The immune response to the parasitic nematode Trichinella and the ways to escape it. From experimental studies to implications for human infection, Curr. Drug Targets Immun. Endocr. Metabol. Disord., 2, 269, 10.2174/1568008023340523 Bruschi, 2004, Focus on immunology of trichinellosis, Med. Chem. Rev., 1, 179 Bruschi, 2012, Immunomodulation in trichinellosis: does Trichinella really escape the host immune system?, Endocr. Metabol. Immune Dis. Drug Target, 12, 4, 10.2174/187153012799279081 Bruschi, 2000, Inhibitory effects of human neutrophil functions by the 45-kD glycoprotein derived from the parasitic nematode Trichinella spiralis, Int. Arch. Allerg. Appl. Immunol., 122, 58, 10.1159/000024359 Bruschi, 2008, Eosinophils and Trichinella infection: toxic for the parasite and the host?, Trends Parasitol., 24, 462, 10.1016/j.pt.2008.07.001 Bruschi, 2014, Trichinellosis Bruschi, 2021, Trichinella spiralis excretory-secretory products downregulate MMP-9 in Dark Agouti rats affected by experimental autoimmune encephalomyelitis, Exp. Parasitol., 225, 108, 10.1016/j.exppara.2021.108112 Camoglio, 2000, Hapten-induced colitis associated with maintained Th1 and inflammatory responses in IFN-gamma receptor-deficient mice, Eur. J. Immunol., 30, 1486, 10.1002/(SICI)1521-4141(200005)30:5<1486::AID-IMMU1486>3.0.CO;2-8 Cao, 2018, Protective effect of Naringin on DSS-induced ulcerative colitis in mice, J. Agric. Food Chem., 66, 13133, 10.1021/acs.jafc.8b03942 Chapman, 2014, Animal models of allergic airways disease: where are we and where to next?, J. Cell. Biochem., 115, 2055, 10.1002/jcb.24881 Chatila, 2005, Role of regulatory T cells in human diseases, J. Allergy Clin. Immunol., 116, 949, 10.1016/j.jaci.2005.08.047 Chen, 2015, Effect of rTsP53 on the M1/M2 activation of bone-marrow derived macrophage in vitro, Int. J. Clin. Exp. Pathol., 8, 13661 Chen, 2016, Recombinant Trichinella spiralis 53-kDa protein activates M2 macrophages and attenuates the LPS-induced damage of endotoxemia, Innate Immun., 22, 419, 10.1177/1753425916651984 Chen, 2018, Targeted delivery of antigen to intestinal dendritic cells induces oral tolerance and prevents autoimmune diabetes in NOD mice, Diabetologia, 61, 1384, 10.1007/s00125-018-4593-3 Chen, 2020, Therapeutic efficacy of a Trichinella spiralis paramyosin-derived peptide modified with a membrane-targeting signal in mice with antigen-induced arthritis, Front. Microbiol., 11, 10.3389/fmicb.2020.608380 Chen, 2021, Higher mucosal type II immunity is associated with increased gut microbiota diversity in BALB/c mice after Trichinella spiralis infection, Mol. Immunol., 138, 87, 10.1016/j.molimm.2021.07.014 Cheng, 2018, Trichinella spiralis infection mitigates collagen-induced arthritis via programmed death 1-mediated immunomodulation, Front. Immunol., 9, 1566, 10.3389/fimmu.2018.01566 Chimyshkyan, 1976, The effect of Trichinella spiralis on graft-versus-host reaction, transplantation immunity and antibody formation, Biomedicine, 25, 176 Cho, 2012, Trichinella spiralis infection suppressed gut inflammation with CD4(+)CD25(+)Foxp3(+) T cell recruitment, Korean J. Parasitol., 50, 385, 10.3347/kjp.2012.50.4.385 Chu, 2019, The resistance against Trichinella spiralis infection induced by primary infection with respiratory syncytial virus, Parasitology, 146, 634, 10.1017/S0031182018001889 Chu, 2020, Preliminary Trichinella spiralis infection ameliorates subsequent RSV infection-induced inflammatory response, Cells, 9, 1314, 10.3390/cells9051314 Coakley, 2015, Exosomes and other extracellular vesicles: the new communicators in parasite infections, Trends Parasitol., 31, 477, 10.1016/j.pt.2015.06.009 Cope, 2007, The central role of T cells in rheumatoid arthritis, Clin. Exp. Rheumatol., 25, S4 Cvetkovic, 2016, Immunomodulatory potential of particular Trichinella spiralis muscle larvae excretory-secretory components, Int. J. Parasitol., 46, 833, 10.1016/j.ijpara.2016.07.008 Cvetkovic, 2020, DC-SIGN signaling by Trichinella spiralis antigens is required for tolerogenic signatures of human DCs, Sci. Rep., 10, 20283, 10.1038/s41598-020-77497-x Cypess, 1974, Decreased susceptibility to Listeria monocytogenes in mice after infection with Trichinella spiralis, Infect. Immun., 9, 477, 10.1128/iai.9.2.477-479.1974 Date, 2014, Kruppel-like transcription factor 6 regulates inflammatory macrophage polarization, J. Biol. Chem., 289, 10318, 10.1074/jbc.M113.526749 Deng, 2013, Identification of the differentially expressed genes in SP2/0 myeloma cells from Balb/c mice infected with Trichinella spiralis, Vet. Parasitol., 194, 179, 10.1016/j.vetpar.2013.01.050 Deng, 2016, Trichinella spiralis infection changes immune response in mice performed abdominal heterotopic cardiac transplantation and prolongs cardiac allograft survival time, Parasitol. Res., 115, 407, 10.1007/s00436-015-4762-y Ding, 2016, Developmental profile of select immune cells in mice infected with Trichinella spiralis during the intestinal phase, Vet. Parasitol., 231, 77, 10.1016/j.vetpar.2016.07.019 Du, 2011, The protective effect of the recombinant 53-kDa protein of Trichinella spiralis on experimental colitis in mice, Dig. Dis. Sci., 56, 2810, 10.1007/s10620-011-1689-8 Du, 2014, Trichinella spiralis excretory-secretory products protect against polymicrobial sepsis by suppressing MyD88 via mannose receptor, Biomed. Res. Int., 2014, 10.1155/2014/898646 Dutta, 2010, Lacto-N-fucopentaose III, a pentasaccharide, prolongs heart transplant survival, Transplantation, 90, 1071, 10.1097/TP.0b013e3181f8f296 Eissa, 2016, Anti-arthritic activity of Schistosoma mansoni and Trichinella spiralis derived-antigens in adjuvant arthritis in rats: role of FOXP3+ treg cells, PLoS One, 11, 10.1371/journal.pone.0165916 Elhasawy, 2021, The apoptotic effect of Trichinella spiralis infection against experimentally induced hepatocellular carcinoma, Asian Pac. J. Cancer Prev., 22, 935, 10.31557/APJCP.2021.22.3.935 Fabre, 2009, Immunity to Trichinella spiralis muscle infection, Vet. Parasitol., 159, 245, 10.1016/j.vetpar.2008.10.051 Fang, 2014, Heat shock protein 70 from Trichinella spiralis induces protective immunity in BALB/c mice by activating dendritic cells, Vaccine, 32, 4412, 10.1016/j.vaccine.2014.06.055 Faz-López, 2016, Role of macrophages in the repair process during the tissue migrating and resident helminth infections, Biomed. Res. Int., 2016, 8634603, 10.1155/2016/8634603 Fehérvari, 2004, Development and function of CD25+CD4+ regulatory T cells, Curr. Opin. Immunol., 16, 203, 10.1016/j.coi.2004.01.004 Ferreira, 2004, Role of calreticulin from parasites in its interaction with vertebrate hosts, Mol. Immunol., 40, 1279, 10.1016/j.molimm.2003.11.018 Fillatreau, 2002, B cells regulate autoimmunity by provision of IL-10, Nat. Immunol., 3, 944, 10.1038/ni833 Fletcher, 2010, T cells in multiple sclerosis and experimental autoimmune encephalomyelitis, Clin. Exp. Immunol., 162, 1, 10.1111/j.1365-2249.2010.04143.x Fontenot, 2003, Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells, Nat. Immunol., 4, 330, 10.1038/ni904 Furze, 2006, Differential roles of the co-stimulatory molecules GITR and CTLA-4 in the immune response to Trichinella spiralis, Microbes Infect., 8, 2803, 10.1016/j.micinf.2006.08.013 Furze, 2006, Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis, Infect. Immun., 74, 1924, 10.1128/IAI.74.3.1924-1932.2006 Fuss, 2004, Non classical CD1d-restricted NKTcells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis, J. Clin. Investig., 113, 1490, 10.1172/JCI19836 Gansmüller, 1987, Antibody-dependent in- vitro cytotoxicity of newborn Trichinella spiralis larvae: nature of the cells involved, Parasite Immunol., 9, 281, 10.1111/j.1365-3024.1987.tb00508.x Gao, 2021, Extracellular vesicles derived from Trichinella spiralis prevent colitis by inhibiting M1 macrophage polarization, Acta Trop., 213, 10.1016/j.actatropica.2020.105761 García-Manrique, 2018, Therapeutic biomaterials based on extracellular vesicles: classification of bio-engineering and mimetic preparation routes, J. Extracell. Vesicles, 7, 1422676, 10.1080/20013078.2017.1422676 Gause, 2016, Macrobiota- helminths as active participants and partners of the microbiota in host intestinal homeostasis, Curr. Opin. Microbiol., 32, 14, 10.1016/j.mib.2016.04.004 Gazzinelli-Guimaraes, 2018, Helminth parasites and immune regulation, F1000Res., 7(F1000 Faculty Rev) Goetz, 2008, Caveolin-1 in tumor progression: the good, the bad and the ugly, Cancer Metastasis Rev., 27, 715, 10.1007/s10555-008-9160-9 Gong, 2011, Identification and characterization of myeloma-associated antigens in Trichinella spiralis, Exp. Parasitol., 127, 784, 10.1016/j.exppara.2010.12.001 Gordon, 2003, Alternative activation of macrophages, Nat. Rev. Immunol., 3, 23, 10.1038/nri978 Grencis, 2021, Immunity to Trichinella, 267 Grencis, 2014, Immunity to gastrointestinal nematodes: mechanisms and myths, Immunol. Rev., 260, 183, 10.1111/imr.12188 Gruden-Movsesijan, 2008, Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats, Exp. Parasitol., 118, 641, 10.1016/j.exppara.2007.12.003 Gruden-Movsesijan, 2010, Mechanisms of modulation of experimental autoimmune encephalomyelitis by chronic Trichinella spiralis infection in Dark Agouti rats, Parasite Immunol., 32, 450, 10.1111/j.1365-3024.2010.01207.x Gruden-Movsesijan, 2011, The impact of Trichinella spiralis excretory-secretory products on dendritic cells, Comp. Immunol. Microbiol. Infect. Dis., 34, 429, 10.1016/j.cimid.2011.08.004 Gruden-Movsesijan, 2020, Antibodies in sera from multiple sclerosis patients recognize Trichinella spiralis muscle larvae excretory-secretory antigens, Immunobiology, 225, 10.1016/j.imbio.2020.151954 Guo, 2016, Trichinella spiralis paramyosin activates mouse bone marrow-derived dendritic cells and induces regulatory T cells, Parasit. Vectors, 9, 569, 10.1186/s13071-016-1857-y Hao, 2021, Trichinella spiralis paramyosin induces colonic regulatory T cells to mitigate inflammatory bowel disease, Front. Cell. Dev. Biol., 9, 10.3389/fcell.2021.695015 Harnett, 2006, Molecular basis of worm-induced immunomodulation, Parasite Immunol., 28, 535, 10.1111/j.1365-3024.2006.00893.x Hartgers, 2006, Co-infection of helminths and malaria: modulation of the immune responses to malaria, Parasite Immunol., 28, 497, 10.1111/j.1365-3024.2006.00901.x He, 2020, A daf-7-related TGF-β ligand (Hc-tgh-2) shows important regulations on the development of Haemonchus contortus, Parasit. Vectors, 13, 326, 10.1186/s13071-020-04196-x Hernandez-Bello, 2008, Identification, molecular characterization and differential expression of caveolin-1 in Trichinella spiralis maturing oocytes and embryos, Int. J. Parasitol., 38, 191, 10.1016/j.ijpara.2007.07.009 Herpin, 2004, Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans, Dev. Comp. Immunol., 28, 461, 10.1016/j.dci.2003.09.007 Hori, 2003, Control of regulatory T cell development by the transcription factor Foxp3, Science, 299, 1057, 10.1126/science.1079490 Hu, 2021, Characterization of a novel cysteine protease in Trichinella spiralis and its role in larval intrusion, development and fecundity, Vet. Res., 52, 113, 10.1186/s13567-021-00983-1 Huang, 2016, Eosinophils in helminth infection: defenders and dupes, Trends Parasitol., 32, 798, 10.1016/j.pt.2016.05.004 Ilic, 2008, Characterization of rat bone marrow dendritic cells initially primed by Trichinella spiralis antigens, Parasite Immunol., 30, 491, 10.1111/j.1365-3024.2008.01049.x Ilic, 2012, Trichinella spiralis: shaping the immune response, Immunol. Res., 52, 111, 10.1007/s12026-012-8287-5 Ilic, 2018, Trichinella spiralis excretory secretory products induce tolerogenic properties in human dendritic cells via toll-like receptors 2 and 4, Front. Immunol., 9, 11, 10.3389/fimmu.2018.00011 Ilic, 2021, Harnessing immunomodulatory mechanisms of Trichinella spiralis to design novel nanomedical approaches for restoring self-tolerance in autoimmunity, Immunol. Lett., 238, 57, 10.1016/j.imlet.2021.04.012 Ingulli, 2010, Mechanism of cellular rejection in transplantation, Pediatr. Nephrol., 25, 61, 10.1007/s00467-008-1020-x Intapan, 2006, Potential use of Trichinella spiralis antigen for serodiagnosis of human capillariasis philippinensis by immunoblot analysis, Parasitol. Res., 98, 227, 10.1007/s00436-005-0070-2 Jankovic, 1998, CD4+ T cell mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling, J. Exp. Med., 187, 619, 10.1084/jem.187.4.619 Jiang, 2016, Intestinal microbes influence the survival, reproduction and protein profile of Trichinella spiralis in vitro, Int. J. Parasitol., 46, 51, 10.1016/j.ijpara.2015.08.007 Jin, 2019, Glutathione- S transferase of Trichinella spiralis regulates maturation and function of dendritic cells, Parasitology, 146, 1725, 10.1017/S003118201900115X Jin, 2020, NLRP3 played a role in Trichinella spiralis-triggered Th2 and regulatory T cells response, Vet. Res., 51, 107, 10.1186/s13567-020-00829-2 Jin, 2020, Trichinella spiralis thioredoxin peroxidase 2 regulates protective Th2 immune response in mice by directly inducing alternatively activated macrophages, Front. Immunol., 11, 2015, 10.3389/fimmu.2020.02015 Johansson, 2004, Revised nomenclature for allergy for global use: report of the nomenclature review committee of the World Allergy Organization, October 2003, J. Allergy Clin. Immunol., 113, 832, 10.1016/j.jaci.2003.12.591 Jungery, 1983, A major change in surface antigens during the maturation of newborn larvae of Trichinella spiralis, Mol. Biochem. Parasitol., 7, 101, 10.1016/0166-6851(83)90038-5 Kamińska, 2017, Multiple sclerosis - etiology and diagnostic potential, Postepy Hig. Med. Dosw., 71, 551, 10.5604/01.3001.0010.3836 Kang, 2013, Trichinella spiralis infection reduces tumor growth and metastasis of B16-F10 melanoma cells, Vet. Parasitol., 196, 106, 10.1016/j.vetpar.2013.02.021 Kang, 2019, Adoptive transfer of Trichinella spiralis-activated macrophages can ameliorate both Th1- and Th2- activated inflammation in murine models, Sci. Rep., 9, 6547, 10.1038/s41598-019-43057-1 Kang, 2021, Trichinella spiralis infection ameliorated diet-induced obesity model in mice, Int. J. Parasitol., 51, 63, 10.1016/j.ijpara.2020.07.012 Khan, 2002, Intestinal nematode infection ameliorates experimental colitis in mice, Infect. Immun., 70, 5931, 10.1128/IAI.70.11.5931-5937.2002 King, 2012, The use of animal models in diabetes research, Br. J. Pharmacol., 166, 877, 10.1111/j.1476-5381.2012.01911.x Kiss, 2020, Effectiveness of helminth therapy in the prevention of allograft rejection: a systematic review of allogeneic transplantation, Front. Immunol., 11, 1604, 10.3389/fimmu.2020.01604 Kobpornchai, 2020, A novel cystatin derived from Trichinella spiralis suppresses macrophage-mediated inflammatory responses, PLoS Negl. Trop. Dis., 14, 10.1371/journal.pntd.0008192 Kobpornchai, 2021, Trichinella spiralis cystatin, TsCstN, modulates STAT4/IL-12 to specifically suppress IFN-γ production, Cell. Immunol., 362, 10.1016/j.cellimm.2021.104303 Kosanović, 2019, Trichinella spiralis muscle larvae release extracellular vesicles with immunomodulatory properties, Parasite Immunol., 41, 10.1111/pim.12665 Krakowski, 1996, Interferon-g confers resistance to experimental allergic encephalomyelitis, Eur. J. Immunol., 26, 1641, 10.1002/eji.1830260735 Leiro, 1988, Immunomodulation by Trichinella spiralis: primary versus secondary response to phosphorylcholine-containing antigens, Med. Microbiol. Immunol., 177, 161, 10.1007/BF00232895 Li, 2015, Trichinella spiralis: low vaccine potential of glutathione S-transferase against infections in mice, Acta Trop., 146, 25, 10.1016/j.actatropica.2015.02.020 Li, 2021, Therapeutic efficacy of excretory-secretory products of Trichinella spiralis adult worms on sepsis-induced acute lung injury in a mouse model, Front. Cell. Infect. Microbiol., 11 Liao, 2018, Trichinella spiralis and tumors: cause, coincidence or treatment?, Anti Cancer Agents Med. Chem., 18, 1091, 10.2174/1871520617666171121115847 Liu, 2015, Treatment with recombinant Trichinella spiralis cathepsin B–like protein ameliorates intestinal ischemia/reperfusion injury in mice by promoting a switch from M1 to M2 macrophages, J. Immunol., 1401864 Liu, 2015, Mammalian models of chemically induced primary malignancies exploitable for imaging-based preclinical theragnostic research, Quant Imaging Med. Surg., 5, 708 Liu, 2016, Vaccination with a co-expression DNA plasmid containing GAD65 fragment gene and IL-10 gene induces regulatory CD4(+) T cells that prevent experimental autoimmune diabetes, Diabetes Metab. Res. Rev., 32, 522, 10.1002/dmrr.2780 Liu, 2017, Cloning and expression of a Trichinella spiralis putative glutathione S-transferase and its elicited protective immunity against challenge infections, Parasit. Vectors, 10, 448, 10.1186/s13071-017-2384-1 Liu, 2021, Evaluation of a cystatin-like protein of Trichinella spiralis for serodiagnosis and identification of immunodominant epitopes using monoclonal antibodies, Vet. Parasitol., 297, 10.1016/j.vetpar.2020.109127 Liu, 2021, Trichinella spiralis infection decreases the diversity of the intestinal flora in the infected mouse, J. Microbiol. Immunol. Infect., 54, 10.1016/j.jmii.2019.09.009 Lubiniecki, 1974, Synergistic interaction of two agents in mice: Japanese B encephalitis virus and Trichinella spiralis, Am. J. Trop Med. Hyg., 23, 235, 10.4269/ajtmh.1974.23.235 Luo, 2016, LC-MS/MS analysis on the components of excretory-secretory protein of Trichinella spiralis muscle larvae, Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi, 34, 53 Luo, 2017, Study on the mitochondrial apoptosis pathways of small cell lung cancer H446 cells induced by Trichinella spiralis muscle larvae ESPs, Parasitology, 144, 793, 10.1017/S0031182016002535 Maizels, 2016, Regulation of the host immune system by helminth parasites, J. Allergy Clin. Immunol., 138, 666, 10.1016/j.jaci.2016.07.007 Maizels, 2003, Immune regulation by helminth parasites: cellular and molecular mechanisms, Nat. Rev. Immunol., 3, 733, 10.1038/nri1183 Maizels, 2004, Helminth parasites--masters of regulation, Immunol. Rev., 201, 89, 10.1111/j.0105-2896.2004.00191.x Malpica, 2019, Regulatory T cells and IgE expression in duodenal mucosa of Strongyloides stercoralis and human T lymphotropic virus type 1 co-infected patients, PLoS Negl. Trop. Dis., 13, 10.1371/journal.pntd.0007415 McCarthy, 2017, An antigen-encapsulating nanoparticle platform for TH 1/17 immune tolerance therapy, Nanomedicine, 13, 191, 10.1016/j.nano.2016.09.007 McDermott, 2005, Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection, J. Immunol., 175, 3207, 10.4049/jimmunol.175.5.3207 Mei, 2020, Trichinella spiralis co-infection exacerbates plasmodium berghei malaria-induced hepatopathy, Parasit. Vectors, 13, 440, 10.1186/s13071-020-04309-6 Mendlovic, 2015, Cytokine, antibody and proliferative cellular responses elicited by Taenia solium calreticulin upon experimental infection in hamsters, PLoS One, 10, 10.1371/journal.pone.0121321 Miyazaki, 2021, NKTR-255, a novel polymer-conjugated rhIL-15 with potent antitumor efficacy, J. Immunother. Cancer., 9, 10.1136/jitc-2020-002024 Molehin, 2012, Serine protease inhibitors of parasitic helminths, Parasitology, 139, 681, 10.1017/S0031182011002435 Morikawa, 2016, TGF-beta and the TGF-beta family: context-dependent roles in cell and tissue physiology, Cold Spring Harb. Perspect. Biol., 8, 10.1101/cshperspect.a021873 Moser, 2020, The role of TH17 cells in multiple sclerosis: therapeutic implications, Autoimmun. Rev., 19, 10.1016/j.autrev.2020.102647 Mukherjee, 2019, Wuchereria bancrofti filaria activates human dendritic cells and polarizes T helper 1 and regulatory T cells via toll-like receptor 4, Commun. Biol., 7, 169, 10.1038/s42003-019-0392-8 Murambiwa, 2020, Chemokine, cytokine and haematological profiles in Sprague-Dawley rats co-infected with plasmodium berghei ANKA and Trichinella zimbabwensis-a laboratory animal model for malaria and tissue-dwelling nematodes co-infection, Heliyon, 6, 10.1016/j.heliyon.2020.e03475 Nagano, 2009, Functional genes and proteins of Trichinella spp, Parasitol. Res., 104, 197, 10.1007/s00436-008-1248-1 Näreaho, 2009, Complement membrane attack complex formation and infectivity of Trichinella spiralis and T. nativa in rats, Vet. Parasitol., 23, 263, 10.1016/j.vetpar.2008.10.037 Ndlovu, 2018, Interleukin-4 receptor alpha expressing B cells are essential to Down-modulate host granulomatous inflammation during schistosomasis, Front. Immunol., 18, 2928, 10.3389/fimmu.2018.02928 Noël, 2004, Alternatively activated macrophages during parasite infections, Trends Parasitol., 3, 126, 10.1016/j.pt.2004.01.004 Ochieng, 2010, Cystatin superfamily, J. Health Care Poor Underserved, 21, 51, 10.1353/hpu.0.0257 Okada, 2013, Effect of nematode Trichinella infection on glucose tolerance and status of macrophage in obese mice, Endocr. J., 60, 1241, 10.1507/endocrj.EJ13-0312 Othman, 2011, Kinetics of Foxp3-expressing regulatory cells in experimental Toxocara canis infection, Exp. Parasitol., 127, 454, 10.1016/j.exppara.2010.10.005 Ouyang, 2019, IL-10 family cytokines IL-10 and IL-22: from basic science to clinical translation, Immunity, 50, 871, 10.1016/j.immuni.2019.03.020 Pang, 2020, Effect of recombinant serine protease from adult stage of Trichinella spiralis on TNBS-induced experimental colitis in mice, Int. Immunopharmacol., 86, 10.1016/j.intimp.2020.106699 Park, 2011, Trichinella spiralis: infection reduces airway allergic inflammation in mice, Exp. Parasitol., 127, 539, 10.1016/j.exppara.2010.10.004 Pawlak, 2004, Alterations in tropomyosin isoform expression in human transitional cell carcinoma of the urinary bladder, Int. J. Cancer, 110, 368, 10.1002/ijc.20151 Pennock, 1998, Rapid purification and characterization of L-dopachrome-methyl ester tautomerase (macrophage-migration-inhibitory factor) from Trichinella spiralis, Trichuris muris and Brugia pahangi, Biochem. J., 335, 495, 10.1042/bj3350495 Piaggi, 2021, Glutathione-S-transferase omega 1 and nurse cell formation during experimental Trichinella infection, Vet. Parasitol., 297, 10.1016/j.vetpar.2020.109114 Piccirillo, 2004, Naturally-occurring CD4+CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance, Semin. Immunol., 16, 81, 10.1016/j.smim.2003.12.003 Pontes-de-Carvalho, 2013, Antigen mimicry between infectious agents and self or environmental antigens may lead to long-term regulation of inflammation, Front. Immunol., 4, 314, 10.3389/fimmu.2013.00314 Pozio, 2021, Epidemiology, 185 Prasad, 2015, Nanomedicine delivers promising treatments for rheumatoid arthritis, Nanomedicine, 10, 2063, 10.2217/nnm.15.45 Radovic, 2015, Immunomodulatory effects of Trichinella spiralis-derived excretory–secretory antigens, Immunol. Res., 61, 312, 10.1007/s12026-015-8626-4 Rittirsch, 2009, Immunodesign of experimental sepsis by cecal ligation and puncture, Nat. Protoc., 4, 31, 10.1038/nprot.2008.214 Robinson, 2005, Proteomic analysis of the excretory-secretory proteins of the Trichinella spiralis L1 larva, a nematode parasite of skeletal muscle, Proteomics, 5, 4525, 10.1002/pmic.200402057 Rouse, 2004, Regulatory cells and infectious agents: détentes cordiale and contraire, J. Immunol., 173, 2211, 10.4049/jimmunol.173.4.2211 Rzepecka, 2022, Can the study of parasitic helminths be fruitful for human diseases? Sakaguchi, 2005, Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self, Nat. Immunol., 6, 345, 10.1038/ni1178 Samanta, 2012, Alterations in the Smad pathway in human cancers, Front. Biosci., 17, 1281, 10.2741/3986 Saunders, 2007, Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection, Infect. Immun., 75, 397, 10.1128/IAI.00664-06 Shao, 2020, Trichinella spiralis calreticulin S-domain binds to human complement C1q to interfere with C1q-mediated immune functions, Front. Immunol., 11, 10.3389/fimmu.2020.572326 Sharma, 2020, Hiding in plain sight: discovery and phylogeography of a cryptic species of Trichinella (Nematoda: Trichinellidae) in wolverine (Gulo gulo), Int. J. Parasitol., 50, 277, 10.1016/j.ijpara.2020.01.003 Shevach, 2002, CD4+ 25+ suppressor T cells: more questions than answers, Nat. Rev. Immunol., 2, 389, 10.1038/nri821 Singh, 2005, Retroviral Foxp3 gene transfer ameliorates liver granuloma pathology in Schistosoma mansoni infected mice, Immunology, 114, 410, 10.1111/j.1365-2567.2004.02083.x Smallwood, 2017, Helminth immunomodulation in autoimmune disease, Front. Immunol., 8, 453, 10.3389/fimmu.2017.00453 Sofronic-Milosavljevic, 2013, Application of dendritic cells stimulated with Trichinella spiralis excretory-secretory antigens alleviates experimental auto-immune encephalomyelitis, Med. Microbiol. Immunol., 202, 239, 10.1007/s00430-012-0286-6 Somboonpatarakun, 2018, Immuno-proteomic analysis of Trichinella spiralis, T. pseudospiralis, and T. papuae extracts recognized by human T. spiralis-infected sera, Parasitol. Res., 117, 201, 10.1007/s00436-017-5694-5 Sorobetea, 2018, Immunity to gastrointestinal nematode infections, Mucosal Immunol., 11, 304, 10.1038/mi.2017.113 Stewart, 1995, Myopathogenesis and myoredifferentiation in trichinosis, Bas. Appl. Myol., 5, 213 Strober, 2011, Pro-inflammatory cytokines in the pathogenesis of inflammatory bowel diseases, Gastroenterology, 40, 1756, 10.1053/j.gastro.2011.02.016 Sun, 2015, Trichinella spiralis paramyosin binds human complement C1q and inhibits classical complement activation, Plos NTD, 1 Sun, 2019, Trichinella spiralis excretory secretory products stimulate host regulatory t cell differentiation through activating dendritic cells, Cells, 8, 1404, 10.3390/cells8111404 Sun, 2019, Preventive and therapeutic effects of Trichinella spiralis adult extracts on allergic inflammation in an experimental asthma mouse model, Parasit. Vectors, 12, 326, 10.1186/s13071-019-3561-1 Svet-Moldavsky, 1969, Mouse transplantation immunity depressed by Trichinella spiralis, Lancet, 2, 320, 10.1016/S0140-6736(69)90078-6 Tang, 2015, Characterisation of a high-frequency gene encoding a strongly antigenic cystatin-like protein from Trichinella spiralis at its early invasion stage, Parasit. Vectors, 8, 78, 10.1186/s13071-015-0689-5 Tong, 2009, RUNX3 inhibits cell proliferation and induces apoptosis by TGFbeta-dependent and -independent mechanisms in human colon carcinoma cells, Pathobiology, 76, 163, 10.1159/000218332 Torre, 2015, Global cancer statistics, 2012, CA Cancer J. Clin., 65, 87, 10.3322/caac.21262 Tran, 2012, TGF-β: the sword, the wand, and the shield of FOXP3+ regulatory T cells, J. Mol. Cell Biol., 4, 29, 10.1093/jmcb/mjr033 van Belle, 2011, Type 1 diabetes: etiology, immunology, and therapeutic strategies, Physiol. Rev., 91, 79, 10.1152/physrev.00003.2010 Vasilev, 2015, Necrosis and apoptosis in Trichinella spiralis-mediated tumour reduction, Centr. Eur. J. Immunol., 40, 42, 10.5114/ceji.2015.50832 Venturiello, 1993, Immune killing of newborn Trichinella larvae by human leucocytes, Parasite Immunol., 15, 559, 10.1111/pim.1993.15.10.559 Wagner, 1976, Concurrent infections in mice with Trypanosoma equiperdum and Trichinella spiralis, Jpn. J. Parasitol., 25, 1 Wang, 2009, Molecular cloning and characterization of heat shock protein 70 from Trichinella spiralis, Acta Trop., 110, 46, 10.1016/j.actatropica.2009.01.003 Wang, 2009, Trichinella spiralis – a potential anti-tumor agent, Vet. Parasitol., 159, 249, 10.1016/j.vetpar.2008.10.052 Wang, 2012, Specific antitumor immunity induced by cross-linking complex heat shock protein 72 and alpha-fetoprotein, Cancer Biother. Radiopharm., 27, 189, 10.1089/cbr.2011.1135 Wang, 2013, An anti-tumor protein produced by Trichinella spiralis induces apoptosis in human hepatoma H7402 cells, Vet. Parasitol., 194, 186, 10.1016/j.vetpar.2013.01.052 Wang, 2017, Heterologous prime-boost vaccination enhances TsPmy’s protective immunity against Trichinella spiralis infection in a murine model, Front. Microbiol., 8, 1394, 10.3389/fmicb.2017.01394 Wang, 2020, Primary characterization othe immune response in pigs infected with Trichinella spiralis, Vet. Res., 51, 17, 10.1186/s13567-020-0741-0 Wang, 2020, Excretory/secretory products from Trichinella spiralis adult worms attenuated DSS-induced colitis in mice by driving PD-1-mediated m2 macrophage polarization, Front. Immunol., 11 Watanabe, 2005, IgE: a question of protective immunity in Trichinella spiralis infection, Trends Parasitol., 21, 175, 10.1016/j.pt.2005.02.010 Wei, 2021, Protective effects of recombinant 53-kDa protein of Trichinella spiralis on acute lung injury in mice via alleviating lung pyroptosis by promoting M2 macrophage polarization, Innate Immun., 27, 313, 10.1177/17534259211013397 Witkiewicz, 2014, Retinoblastoma tumor suppressor pathway in breast cancer: prognosis, precision medicine, and therapeutic interventions, Breast Cancer Res., 16, 207 Wu, 2008, Candidate genes responsible for common and different pathology of infected muscle tissues between Trichinella spiralis and T. pseudospiralis infection, Parasitol. Int., 57, 368, 10.1016/j.parint.2008.03.005 Wu, 2008, Trichinella spiralis: nurse cell formation with emphasis on analogy to muscle cell repair, Parasit. Vectors, 1, 27, 10.1186/1756-3305-1-27 Wu, 2009, Identification of antigenic genes in Trichinella spiralis by immunoscreening of cDNA libraries, Vet. Parasitol., 159, 272, 10.1016/j.vetpar.2008.10.035 Xie, 2021, Induction of the IL-10-producing regulatory B cell phenotype following Trichinella spiralis infection, Mol. Immunol., 133, 86, 10.1016/j.molimm.2021.02.012 Xu, 2020, Effect of T. spiralis serine protease inhibitors on TNBS-induced experimental colitis mediated by macrophages, Sci. Rep., 10, 3147, 10.1038/s41598-020-60155-7 Yang, 2014, Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice, PLoS One, 9 Yang, 2015, Immunoproteomic profile of Trichinella spiralis adult worm proteins recognized by early infection sera, Parasit. Vectors, 8, 20, 10.1186/s13071-015-0641-8 Yang, 2017, Component analysis of excretory/secretory protein from Trichinella spiralis adult worm, Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi, 35, 24 Yang, 2020, Extracellular vesicles derived from Trichinella spiralis muscle larvae ameliorate TNBS-induced colitis in mice, Front. Immunol., 11, 1174, 10.3389/fimmu.2020.01174 Yuan, 2019, Protective effect of excretory-secretory protein from adult Trichinella spiralis on ovalbumin-induced allergic rhinitis in mice, Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi, 31, 504 Yusuf, 1980, Concurrent infections of Trichinella spiralis and toxoplasma gondii in mice, Z Parasitenkd, 62, 231, 10.1007/BF00926564 Zhan, 2013, Analysis of a novel cathepsin B circulating antigen and its response to drug treatment in Trichinella-infected mice, Parasitol. Res., 112, 3213, 10.1007/s00436-013-3497-x Zhang, 2001, Activation of CD25+ CD4+ regulatory T cells control Leishmania major persistence and immunity, Nature, 420, 502 Zhang, 2009, Anti-tumor effect of Trichinella spiralis on Hepal-6 hepatoma carcinoma cell in the C57BL/6 mice, J. Pathog. Biol., 4, 24 Zhang, 2018, Ts-Hsp70 induces protective immunity against Trichinella spiralis infection in mouse by activating dendritic cells through TLR2 and TLR4, PLoS Negl. Trop. Dis., 12, 10.1371/journal.pntd.0006502 Zhao, 2017, Trichinella spiralis calreticulin binds human complement C1q as an immune evasion strategy, Front. Immunol., 8, 636, 10.3389/fimmu.2017.00636