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Trichinella spiralis: inflammation modulator

Published online by Cambridge University Press:  21 September 2020

Jing Ding
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Xiaolei Liu
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Xue Bai
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Yang Wang
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Jian Li
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Chun Wang
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Shicun Li
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Mingyuan Liu
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
Xuelin Wang*
Affiliation:
Key Laboratory for Zoonoses Research, Ministry of Education, Institute of Zoonoses, College of Veterinary Medicine, Jilin University, OIE Collaborating Center on Foodborne Parasites in Asian-Pacific Region, Changchun130062, P.R. China
*
Author for correspondence: X. Wang, E-mail: xuelin@jlu.edu.cn

Abstract

The hygiene hypothesis posits that the decreased incidence of parasitic infection in developed countries may underlie an increased prevalence of allergic and autoimmune diseases in these countries. As unique inflammation modulator of intracellular parasitism, Trichinella spiralis, or its excretory–secretory (ES) product, shows improved responses to allergies, autoimmune diseases, inflammatory bowel disease, type 1 diabetes, rheumatic arthritis and autoimmune encephalomyelitis by exerting immunomodulatory effects on both innate and adaptive immune cells in animal models. Research has shown that T. spiralis differs from other helminths in manipulation of the host immune response not only by well-known characteristics of its life cycle, but also by its inflammation modulation pathway. How the parasite achieves inflammation modulation has not been fully elucidated yet. This review will generalize the mechanism and focuses on ES immunomodulatory molecules of T. spiralis that may be important for developing new therapeutics for inflammatory disorders.

Type
Review Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abdoli, A (2019) Therapeutic potential of helminths and helminth-derived antigens for resolution of inflammation in inflammatory bowel disease. Archives of Medical Research 50, 5859.CrossRefGoogle ScholarPubMed
Ahn, JB, Kang, SA, Kim, DH and Yu, HS (2016) Activation and recruitment of regulatory t cells via chemokine receptor activation in Trichinella spiralis-infected mice. Korean Journal of Parasitology 54, 163171.CrossRefGoogle ScholarPubMed
Akiho, H, Blennerhassett, P, Deng, Y and Collins, SM (2002) Role of IL-4, IL-13, and STAT6 in inflammation-induced hypercontractility of murine smooth muscle cells. American Journal of Physiology: Gastrointestinal and Liver Physiology 282, G226G232.Google ScholarPubMed
Aranzamendi, C, Fransen, F, Langelaar, M, Franssen, F, van der Ley, P, van Putten, JP, Rutten, V and Pinelli, E (2012) Trichinella spiralis-secreted products modulate DC functionality and expand regulatory T cells in vitro. Parasite Immunology 34, 210223.CrossRefGoogle ScholarPubMed
Aranzamendi, C, de Bruin, A, Kuiper, R, Boog, CJ, van Eden, W, Rutten, V and Pinelli, E (2013a) Protection against allergic airway inflammation during the chronic and acute phases of Trichinella spiralis infection. Clinical & Experimental Allergy 43, 103115.CrossRefGoogle Scholar
Aranzamendi, C, Sofronic-Milosavljevic, L and Pinelli, E (2013b) Helminths: immunoregulation and inflammatory diseases—which side are Trichinella spp. and Toxocara spp. on? Journal of Parasitology Research 2013, 329438.CrossRefGoogle Scholar
Bach, JF (2018) The hygiene hypothesis in autoimmunity: the role of pathogens and commensals. Nature Reviews Immunology 18, 105120.CrossRefGoogle ScholarPubMed
Bai, X, Wu, X, Wang, X, et al. (2012) Regulation of cytokine expression in murine macrophages stimulated by excretory/secretory products from Trichinella spiralis in vitro. Molecular and Cellular Biochemistry 360, 7988.CrossRefGoogle ScholarPubMed
Bedoya, SK, Lam, B, Lau, K and Larkin, J 3rd (2013) Th17 cells in immunity and autoimmunity. Clinical & Developmental Immunology 2013, 986789.CrossRefGoogle ScholarPubMed
Beiting, DP, Bliss, SK, Schlafer, DH, Roberts, VL and Appleton, JA (2004) Interleukin-10 limits local and body cavity inflammation during infection with muscle-stage Trichinella spiralis. Infection and Immunity 72, 31293137.CrossRefGoogle ScholarPubMed
Beiting, DP, Gagliardo, LF, Hesse, M, Bliss, SK, Meskill, D and Appleton, JA (2007) Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. Journal of Immunology 178, 10391047.CrossRefGoogle ScholarPubMed
Broide, DH (2009) Immunomodulation of allergic disease. Annual Review of Medicine 60, 279291.CrossRefGoogle ScholarPubMed
Bruschi, F, Korenaga, M and Watanabe, N (2008) Eosinophils and Trichinella infection: toxic for the parasite and the host? Trends in Parasitology 24, 462467.CrossRefGoogle ScholarPubMed
Caraballo, L (2018) The tropics, helminth infections and hygiene hypotheses. Expert Review of Clinical Immunology 14, 99102.CrossRefGoogle ScholarPubMed
Carvalho, L, Sun, J, Kane, C, Marshall, F, Krawczyk, C and Pearce, EJ (2009) Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126, 2834.CrossRefGoogle ScholarPubMed
Charabati, M, Donkers, SJ, Kirkland, MC and Osborne, LC (2020) A critical analysis of helminth immunotherapy in multiple sclerosis. Multiple Sclerosis, 1352458519899040.CrossRefGoogle ScholarPubMed
Chen, JQ, Szodoray, P and Zeher, M (2016a) Toll-like receptor pathways in autoimmune diseases. Clinical Reviews in Allergy & Immunology 50, 117.CrossRefGoogle Scholar
Chen, ZB, Tang, H, Liang, YB, Yang, W, Wu, JG, Hu, XC, Li, ZY, Zeng, LJ and Ma, ZF (2016b) Recombinant Trichinella spiralis 53-kDa protein activates M2 macrophages and attenuates the LPS-induced damage of endotoxemia. Innate Immunity 22, 419432.CrossRefGoogle Scholar
Cheng, Y, Zhu, X, Wang, X, Zhuang, Q, Huyan, X, Sun, X, Huang, J, Zhan, B and Zhu, X (2018) Trichinella spiralis infection mitigates collagen-induced arthritis via programmed death 1-mediated immunomodulation. Frontiers in Immunology 9, 1566.CrossRefGoogle ScholarPubMed
Cho, MK, Park, MK, Kang, SA, Choi, SH, Ahn, SC and Yu, HS (2012) Trichinella spiralis infection suppressed gut inflammation with CD4(+)CD25(+)Foxp3(+) T cell recruitment. The Korean Journal of Parasitology 50, 385390.CrossRefGoogle ScholarPubMed
Conroy, DM and Williams, TJ (2001) Eotaxin and the attraction of eosinophils to the asthmatic lung. Respiratory Research 2, 150156.CrossRefGoogle ScholarPubMed
Cvetkovic, J, Ilic, N, Sofronic-Milosavljevic, L and Gruden-Movsesijan, A (2014) Glycans expressed on Trichinella spiralis excretory-secretory antigens are important for anti-inflammatory immune response polarization. Comparative Immunology, Microbiology and Infectious Diseases 37, 355367.CrossRefGoogle ScholarPubMed
Cvetkovic, J, Sofronic-Milosavljevic, L, Ilic, N, Gnjatovic, M, Nagano, I and Gruden-Movsesijan, A (2016) Immunomodulatory potential of particular Trichinella spiralis muscle larvae excretory-secretory components. International Journal for Parasitology 46, 833842.CrossRefGoogle ScholarPubMed
Danilowicz-Luebert, E, O'Regan, NL, Steinfelder, S and Hartmann, S (2011) Modulation of specific and allergy-related immune responses by helminths. Journal of Biomedicine and Biotechnology 2011, 821578.CrossRefGoogle ScholarPubMed
Ding, J, Bai, X, Wang, X, Shi, H, Cai, X, Luo, X, Liu, M and Liu, X (2017) Immune Cell Responses and Cytokine Profile in Intestines of Mice Infected with Trichinella spiralis. Frontiers in Microbiology 8, 2069.CrossRefGoogle ScholarPubMed
Du, L, Tang, H, Ma, Z, et al. (2011) The protective effect of the recombinant 53-kDa protein of Trichinella spiralis on experimental colitis in mice. Digestive Diseases and Sciences 56, 28102817.CrossRefGoogle ScholarPubMed
Dzik, JM, Zieliński, Z, Cieśla, J and Wałajtys-Rode, E (2010) Trichinella spiralis infection enhances protein kinase C phosphorylation in guinea pig alveolar macrophages. Parasite Immunology 32, 209220.CrossRefGoogle ScholarPubMed
Eissa, MM, Mostafa, DK, Ghazy, AA, El Azzouni, MZ, Boulos, LM and Younis, LK (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, e0165916.CrossRefGoogle ScholarPubMed
Elliott, DE and Weinstock, JV (2012) Where are we on worms? Current Opinion in Gastroenterology 28, 551556.CrossRefGoogle ScholarPubMed
Erb, KJ (2007) Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? European Journal of Immunology 37, 11701173.CrossRefGoogle ScholarPubMed
Everts, B, Smits, HH, Hokke, CH and Yazdanbakhsh, M (2010) Helminths and dendritic cells: sensing and regulating via pattern recognition receptors, Th2 and Treg responses. European Journal of Immunology 40, 15251537.CrossRefGoogle ScholarPubMed
Fabre, MV, Beiting, DP, Bliss, SK and Appleton, JA (2009) Immunity to Trichinella spiralis muscle infection. Veterinary Parasitology 159, 245248.CrossRefGoogle ScholarPubMed
Fasching, P, Stradner, M, Graninger, W, Dejaco, C and Fessler, J (2017) Therapeutic potential of targeting the Th17/Treg axis in autoimmune disorders. Molecules. doi:10.3390/molecules22010134CrossRefGoogle ScholarPubMed
Finkelman, FD, Shea-Donohue, T, Morris, SC, Gildea, L, Strait, R, Madden, KB, Schopf, L and Urban, JF Jr (2004) Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139155.CrossRefGoogle ScholarPubMed
Gruden-Movsesijan, A, Ilic, N, Mostarica-Stojkovic, M, Stosic-Grujicic, S, Milic, M and Sofronic-Milosavljevic, L (2010) Mechanisms of modulation of experimental autoimmune encephalomyelitis by chronic Trichinella spiralis infection in Dark Agouti rats. Parasite Immunology 32, 450459.CrossRefGoogle ScholarPubMed
Gruden-Movsesijan, A, Ilic, N, Colic, M, Majstorovic, I, Vasilev, S, Radovic, I and Sofronic-Milosavljevic, L (2011) The impact of Trichinella spiralis excretory-secretory products on dendritic cells. Comparative Immunology, Microbiology and Infectious Diseases 34, 429439.CrossRefGoogle ScholarPubMed
Guo, K, Sun, X, Gu, Y, Wang, Z, Huang, J and Zhu, X (2016) Trichinella spiralis paramyosin activates mouse bone marrow-derived dendritic cells and induces regulatory T cells. Parasites & Vectors 9, 569.CrossRefGoogle ScholarPubMed
Gurish, MF, Bryce, PJ, Tao, H, Kisselgof, AB, Thornton, EM, Miller, HR, Friend, DS and Oettgen, HC (2004) IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology 172, 11391145.CrossRefGoogle ScholarPubMed
Han, C, Yu, J, Zhang, Z, Zhai, P, Zhang, Y, Meng, S, Yu, Y, Li, X and Song, M (2019) Immunomodulatory effects of Trichinella spiralis excretory-secretory antigens on macrophages. Experimental Parasitology 196, 6872.CrossRefGoogle ScholarPubMed
Harnett, MM and Harnett, W (2017) Can parasitic worms cure the modern world's ills? Trends in Parasitology 33, 694705.CrossRefGoogle ScholarPubMed
Harris, DP, Haynes, L, Sayles, PC, Duso, DK, Eaton, SM, Lepak, NM, Johnson, LL, Swain, SL and Lund, FE (2000) Reciprocal regulation of polarized cytokine production by effector B and T cells. Nature Immunologyl 1, 475482.CrossRefGoogle ScholarPubMed
Helmby, H and Grencis, RK (2003) IFN-gamma-independent effects of IL-12 during intestinal nematode infection. Journal of Immunology 171, 36913696.CrossRefGoogle ScholarPubMed
Hernandez-Ancheyta, L, Salinas-Tobon, MDR, Cifuentes-Goches, JC and Hernandez-Sanchez, J (2018) Trichinella spiralis muscle larvae excretory-secretory products induce changes in cytoskeletal and myogenic transcription factors in primary myoblast cultures. International Journal for Parasitology 48, 275285.CrossRefGoogle ScholarPubMed
Hubner, MP, Shi, Y, Torrero, MN, et al. (2012) Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-beta. Journal of Immunology 188, 559568.CrossRefGoogle ScholarPubMed
Ilic, N, Worthington, JJ, Gruden-Movsesijan, A, Travis, MA, Sofronic-Milosavljevic, L and Grencis, RK (2011) Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro. Parasite Immunology 33, 572582.CrossRefGoogle Scholar
Ilic, N, Gruden-Movsesijan, A and Sofronic-Milosavljevic, L (2012) Trichinella spiralis: shaping the immune response. Immunologic Research 52, 111119.CrossRefGoogle ScholarPubMed
Ilic, N, Gruden-Movsesijan, A, Cvetkovic, J, Tomic, S, Vucevic, DB, Aranzamendi, C, Colic, M, Pinelli, E and Sofronic-Milosavljevic, L (2018) Trichinella spiralis excretory-secretory products induce tolerogenic properties in human dendritic cells via toll-like receptors 2 and 4. Frontiers in Immunology 9, 11.CrossRefGoogle ScholarPubMed
Inclan-Rico, JM and Siracusa, MC (2018) First responders: innate immunity to helminths. Trends in Parasitology 34, 861880.CrossRefGoogle ScholarPubMed
Jin, X, Yang, Y, Liu, X, Shi, H, Cai, X, Luo, X, Liu, M and Bai, X (2019) Glutathione-S-transferase of Trichinella spiralis regulates maturation and function of dendritic cells. Parasitology 146, 17251732.CrossRefGoogle ScholarPubMed
Kahl, J, Brattig, N and Liebau, E (2018) The untapped pharmacopeic potential of helminths. Trends in Parasitology 34, 828842.CrossRefGoogle ScholarPubMed
Kamal, M, Wakelin, D, Ouellette, AJ, Smith, A, Podolsky, DK and Mahida, YR (2001) Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clinical and Experimental Immunology 126, 117125. xCrossRefGoogle ScholarPubMed
Kang, SA, Cho, MK, Park, MK, Kim, DH, Hong, YC, Lee, YS, Cha, HJ, Ock, MS and Yu, HS (2012) Alteration of helper T-cell related cytokine production in splenocytes during Trichinella spiralis infection. Veterinary Parasitology 186, 319327.CrossRefGoogle ScholarPubMed
Kang, YJ, Jo, JO, Cho, MK, Yu, HS, Leem, SH, Song, KS, Ock, MS and Cha, HJ (2013) Trichinella spiralis infection reduces tumor growth and metastasis of B16-F10 melanoma cells. Veterinary Parasitology 196, 106113.CrossRefGoogle ScholarPubMed
Kang, SA, Park, MK, Cho, MK, Park, SK, Jang, MS, Yang, BG, Jang, MH, Kim, DH and Yu, HS (2014) Parasitic nematode-induced CD4+Foxp3+T cells can ameliorate allergic airway inflammation. PLoS Neglected Tropical Diseases 8, e3410.CrossRefGoogle ScholarPubMed
Kang, SA, Park, MK, Park, SK, Choi, JH, Lee, DI, Song, SM and Yu, HS (2019) Adoptive transfer of Trichinella spiralis-activated macrophages can ameliorate both Th1- and Th2-activated inflammation in murine models. Scientific Reports 9, 6547.CrossRefGoogle ScholarPubMed
Kim, S, Park, MK and Yu, HS (2015) Toll-Like Receptor Gene Expression during Trichinella spiralis Infection. Korean Journal of Parasitology 53, 431438.CrossRefGoogle ScholarPubMed
Knight, PA, Pemberton, AD, Robertson, KA, Roy, DJ, Wright, SH and Miller, HR (2004) Expression profiling reveals novel innate and inflammatory responses in the jejunal epithelial compartment during infection with Trichinella spiralis. Infection and Immunity 72, 60766086.CrossRefGoogle ScholarPubMed
Kobpornchai, P, Flynn, RJ, Reamtong, O, et al. (2020) A novel cystatin derived from Trichinella spiralis suppresses macrophage-mediated inflammatory responses. PLoS Neglected Tropical Diseases 14, e0008192.CrossRefGoogle ScholarPubMed
Kosanović, M, Cvetković, J, Gruden-Movsesijan, A, Vasilev, S, Svetlana, M, Ilić, N and Sofronić-Milosavljević, L (2019) Trichinella spiralis muscle larvae release extracellular vesicles with immunomodulatory properties. Parasite Immunology 41, e12665.CrossRefGoogle ScholarPubMed
Kotake, S, Yago, T, Kobashigawa, T and Nanke, Y (2017) The plasticity of Th17 cells in the pathogenesis of rheumatoid arthritis. Journal of Clinical Medicine 6.CrossRefGoogle ScholarPubMed
Kuijk, LM, Klaver, EJ, Kooij, G, et al. (2012) Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation. Molecular Immunology 51, 210218.CrossRefGoogle ScholarPubMed
Langelaar, M, Aranzamendi, C, Franssen, F, Van Der Giessen, J, Rutten, V, van der Ley, P and Pinelli, E (2009) Suppression of dendritic cell maturation by Trichinella spiralis excretory/secretory products. Parasite Immunology 31, 641645.CrossRefGoogle ScholarPubMed
Li, CK, Seth, R, Gray, T, Bayston, R, Mahida, YR and Wakelin, D (1998) Production of proinflammatory cytokines and inflammatory mediators in human intestinal epithelial cells after invasion by Trichinella spiralis. Infection and immunity 66, 22002206.CrossRefGoogle ScholarPubMed
Liu, XD, Wang, XL, Bai, X, et al. (2014) Oral administration with attenuated Salmonella encoding a Trichinella cystatin-like protein elicited host immunity. Experimental Parasitology 141, 111.CrossRefGoogle ScholarPubMed
Luo, J, Yu, L, Xie, G, Li, D, Su, M, Zhao, X and Du, L (2017) Study on the mitochondrial apoptosis pathways of small cell lung cancer H446 cells induced by Trichinella spiralis muscle larvae ESPs. Parasitology 144, 793800.CrossRefGoogle Scholar
Luo, XC, Chen, ZH, Xue, JB, et al. (2019) Infection by the parasitic helminth Trichinella spiralis activates a Tas2r-mediated signaling pathway in intestinal tuft cells. Proceedings of the National Academy of Sciences of the United States of America 116, 55645569.CrossRefGoogle ScholarPubMed
Maizels, RM (2016) Parasitic helminth infections and the control of human allergic and autoimmune disorders. Clinical Microbiology and Infection 22, 481486.CrossRefGoogle ScholarPubMed
Maizels, RM (2020) Regulation of immunity and allergy by helminth parasites. Allergy 75, 524534.CrossRefGoogle ScholarPubMed
Maizels, RM, Balic, A, Gomez-Escobar, N, Nair, M, Taylor, MD and Allen, JE (2004) Helminth parasites–masters of regulation. Immunological Reviews 201, 89116.CrossRefGoogle Scholar
McKay, DM (2009) The therapeutic helminth? Trends in Parasitology 25, 109114.CrossRefGoogle ScholarPubMed
McSorley, HJ, Chaye, MAM and Smits, HH (2019) Worms: Pernicious parasites or allies against allergies? Parasite Immunology 41, e12574.CrossRefGoogle ScholarPubMed
Milcheva, R, Petkova, S, Hurnikova, Z, Janega, P and Babal, P (2013) The occupation of intestinal epithelium by Trichinella spiralis in BALB/C mice is not associated with local manifestation of apoptosis related factors. Parasitology Research 112, 39173924.CrossRefGoogle Scholar
Ming, L, Peng, RY, Zhang, L, Zhang, CL, Lv, P, Wang, ZQ, Cui, J and Ren, HJ (2016) Invasion by Trichinella spiralis infective larvae affects the levels of inflammatory cytokines in intestinal epithelial cells in vitro. Experimental Parasitology 170, 220226.CrossRefGoogle ScholarPubMed
Moon, E-K, Lee, S-H, Soh, Y, Guo, Y-R, Piao, Y and Quan, F-S (2018) Correlates of Immune Response in Trichinella spiralis Infection. Immunological Investigations 47, 605614.CrossRefGoogle ScholarPubMed
Motomura, Y, Wang, H, Deng, Y, El-Sharkawy, RT, Verdu, EF and Khan, WI (2009) Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clinical and Experimental Immunology 155, 8895.CrossRefGoogle Scholar
Mucida, D and Cheroutre, H (2010) The many face-lifts of CD4 T helper cells. Advances in Immunology 107, 139152.CrossRefGoogle ScholarPubMed
Nascimento Santos, L, Carvalho Pacheco, LG, Silva Pinheiro, C and Alcantara-Neves, NM (2017) Recombinant proteins of helminths with immunoregulatory properties and their possible therapeutic use. Acta Tropica 166, 202211.CrossRefGoogle ScholarPubMed
Park, HK, Cho, MK, Choi, SH, Kim, YS and Yu, HS (2011) Trichinella spiralis: infection reduces airway allergic inflammation in mice. Experimental Parasitology 127, 539544.CrossRefGoogle ScholarPubMed
Piras, V and Selvarajoo, K (2014) Beyond MyD88 and TRIF pathways in toll-like receptor signaling. Frontiers in Immunology 5, 70.CrossRefGoogle ScholarPubMed
Qian, C and Cao, X (2018) Dendritic cells in the regulation of immunity and inflammation. Seminars in Immunology 35, 311.CrossRefGoogle ScholarPubMed
Ronet, C, Hauyon-La Torre, Y, Revaz-Breton, M, Mastelic, B, Tacchini-Cottier, F, Louis, J and Launois, P (2010) Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. Journal of Immunology 184, 886894.CrossRefGoogle ScholarPubMed
Saunders, KA, Raine, T, Cooke, A and Lawrence, CE (2007) Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infection and Immunity 75, 397407.CrossRefGoogle ScholarPubMed
Serna, H, Porras, M and Vergara, P (2006) Mast cell stabilizer ketotifen [4-(1-methyl-4-piperidylidene)-4h-benzo[4,5]cyclohepta[1,2-b]thiophen-10(9H)-one fumarate] prevents mucosal mast cell hyperplasia and intestinal dysmotility in experimental Trichinella spiralis inflammation in the rat. Journal of Pharmacology and Experimental Therapeutics 319, 11041111.CrossRefGoogle ScholarPubMed
Smallwood, TB, Giacomin, PR, Loukas, A, Mulvenna, JP, Clark, RJ and Miles, JJ (2017) Helminth immunomodulation in autoimmune disease. Frontiers in Immunology 8, 453.CrossRefGoogle ScholarPubMed
Sofronic-Milosavljevic, LJ, Radovic, I, Ilic, N, Majstorovic, I, Cvetkovic, J and Gruden-Movsesijan, A (2013) Application of dendritic cells stimulated with Trichinella spiralis excretory-secretory antigens alleviates experimental autoimmune encephalomyelitis. Medical Microbiology and Immunology 202, 239249.CrossRefGoogle ScholarPubMed
Sofronic-Milosavljevic, L, Ilic, N, Pinelli, E and Gruden-Movsesijan, A (2015) Secretory products of Trichinella spiralis muscle larvae and immunomodulation: implication for autoimmune diseases, allergies, and malignancies. The Journal of Immunology 2015, 523875.Google ScholarPubMed
Stadnyk, AW, Dollard, CD and Issekutz, AC (2000) Neutrophil migration stimulates rat intestinal epithelial cell cytokine expression during helminth infection. Journal of Leukocyte Biology 68, 821827.Google ScholarPubMed
Steel, N, Faniyi, AA, Rahman, S, et al. (2019) TGFbeta-activation by dendritic cells drives Th17 induction and intestinal contractility and augments the expulsion of the parasite Trichinella spiralis in mice. PLoS Pathogens 15, e1007657.CrossRefGoogle ScholarPubMed
Strachan, DP (1989) Hay fever, hygiene, and household size. BMJ 299, 12591260.CrossRefGoogle ScholarPubMed
Strachan, DP (2000) Family size, infection and atopy: the first decade of the “hygiene hypothesis”. Thorax 55(Suppl 1), S2S10.CrossRefGoogle ScholarPubMed
Sun, S, Wang, X, Wu, X, Zhao, Y, Wang, F, Liu, X, Song, Y, Wu, Z and Liu, M (2011) Toll-like receptor activation by helminths or helminth products to alleviate inflammatory bowel disease. Parasites & Vectors 4, 186.CrossRefGoogle ScholarPubMed
Sun, R, Zhao, X, Wang, Z, Yang, J, Zhao, L, Zhan, B and Zhu, X (2015) Trichinella spiralis paramyosin binds human complement c1q and inhibits classical complement activation. PLoS Neglected Tropical Diseases 9, e0004310.CrossRefGoogle ScholarPubMed
Sun, S, Li, H, Yuan, Y, et al. (2019) Preventive and therapeutic effects of Trichinella spiralis adult extracts on allergic inflammation in an experimental asthma mouse model. Parasites & Vectors 12, 326.CrossRefGoogle Scholar
Szkudlapski, D, Labuzek, K, Pokora, Z, Smyla, N, Gonciarz, M, Mularczyk, A, Maluch, P and Okopien, B (2014) The emerging role of helminths in treatment of the inflammatory bowel disorders. Journal of Physiology and Pharmacology 65, 741751.Google Scholar
Tahapary, DL, de Ruiter, K, Martin, I, et al. (2015) Helminth infections and type 2 diabetes: a cluster-randomized placebo controlled SUGARSPIN trial in Nangapanda, Flores, Indonesia. BMC Infectious Diseases 15, 133.CrossRefGoogle ScholarPubMed
Tahmasebinia, F and Pourgholaminejad, A (2017) The role of Th17 cells in auto-inflammatory neurological disorders. Progress in Neuro-Psychopharmacology & Biological Psychiatry 79, 408416.CrossRefGoogle ScholarPubMed
Tang, B, Liu, M, Wang, L, Yu, S, Shi, H, Boireau, P, Cozma, V, Wu, X and Liu, X (2015) Characterisation of a high-frequency gene encoding a strongly antigenic cystatin-like protein from Trichinella spiralis at its early invasion stage. Parasites & Vectors 8, 78.CrossRefGoogle ScholarPubMed
Valenta, R, Campana, R and Niederberger, V (2017) Recombinant allergy vaccines based on allergen-derived B cell epitopes. Immunology Letters 189, 1926.CrossRefGoogle ScholarPubMed
Varyani, F, Fleming, JO and Maizels, RM (2017) Helminths in the gastrointestinal tract as modulators of immunity and pathology. American Journal of Physiology: Gastrointestinal and Liver Physiology 312, G537G549.Google ScholarPubMed
Wang, M, Wu, L, Weng, R, Zheng, W, Wu, Z and Lv, Z (2017) Therapeutic potential of helminths in autoimmune diseases: helminth-derived immune-regulators and immune balance. Parasitology Research 116, 20652074. 5CrossRefGoogle ScholarPubMed
Wang, XL, Liu, MY, Sun, SM, et al. (2013) An anti-tumor protein produced by Trichinella spiralis induces apoptosis in human hepatoma H7402 cells. Veterinary Parasitology 194, 186188.CrossRefGoogle ScholarPubMed
Watanabe, N (2014) Impaired protection against Trichinella spiralis in mice with high levels of IgE. Parasitology International 63, 332336.CrossRefGoogle ScholarPubMed
Weinstock, JV, Summers, RW, Elliott, DE, Qadir, K, Urban, JF Jr and Thompson, R (2002) The possible link between de-worming and the emergence of immunological disease. Journal of Laboratory and Clinical Medicine 139, 334338.CrossRefGoogle ScholarPubMed
Wojtkowiak-Giera, A, Wandurska-Nowak, E, Derda, M, Jankowska, W, Jagodzinski, PP and Hadas, E (2018) Trichinella Spiralis: impact on the expression of toll-like receptor 4 (TLR4) gene during the intestinal phase of experimental trichinellosis. Veterinary Research 62, 493496.CrossRefGoogle ScholarPubMed
Wolf, SD, Dittel, BN, Hardardottir, F and Janeway, CA Jr (1996) Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. Journal of Experimental Medicine 184, 22712278.CrossRefGoogle ScholarPubMed
Wu, Z, Wang, L, Tang, Y and Sun, X (2017) Parasite-derived proteins for the treatment of allergies and autoimmune diseases. Frontiers in Microbiology 8, 2164.CrossRefGoogle ScholarPubMed
Xu, D, Liu, H and Komai-Koma, M (2004) Direct and indirect role of Toll-like receptors in T cell mediated immunity. Cellular & Molecular Immunology 1, 239246.Google ScholarPubMed
Xu, J, Liu, M, Yu, P, Wu, L and Lu, Y (2019a) Effect of recombinant Trichinella spiralis cysteine proteinase inhibitor on TNBS-induced experimental inflammatory bowel disease in mice. International Immunopharmacology 66, 2840.CrossRefGoogle Scholar
Xu, J, Yu, P, Wu, L, Liu, M and Lu, Y (2019b) Effect of Trichinella spiralis intervention on TNBS-induced experimental colitis in mice. Immunobiology 224, 147153.CrossRefGoogle Scholar
Yang, Y, Yang, X, Gu, Y, Wang, Y, Zhao, X and Zhu, X (2013) Protective immune response induced by co-immunization with the Trichinella spiralis recombinant Ts87 protein and a Ts87 DNA vaccine. Veterinary Parasitology 194, 207210.CrossRefGoogle Scholar
Yang, X, Yang, Y, Wang, Y, Zhan, B, Gu, Y, Cheng, Y and Zhu, X (2014) Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice. PLoS One 9, e96454.CrossRefGoogle ScholarPubMed
Yang, DQ, Liu, F, Bai, Y, et al. (2020a) Functional characterization of a glutathione S-transferase in Trichinella spiralis invasion, development and reproduction. Veterinary Parasitology, 109128.CrossRefGoogle Scholar
Yang, Y, Liu, L, Liu, X, et al. (2020b) Extracellular vesicles derived from trichinella spiralis muscle larvae ameliorate TNBS-induced colitis in mice. Frontiers in Immunology 11, 1174.CrossRefGoogle Scholar
Yazdanbakhsh, M and Matricardi, PM (2004) Parasites and the hygiene hypothesis: regulating the immune system? Clinical Reviews in Allergy & Immunology 26, 1524.CrossRefGoogle ScholarPubMed
Yu, YR, Deng, MJ, Lu, WW, Jia, MZ, Wu, W and Qi, YF (2013) Systemic cytokine profiles and splenic toll-like receptor expression during Trichinella spiralis infection. Experimental Parasitology 134, 92101.CrossRefGoogle ScholarPubMed
Zhao, L, Shao, S, Chen, Y, Sun, X, Sun, R, Huang, J, Zhan, B and Zhu, X (2017) Trichinella spiralis calreticulin binds human complement C1q as an immune evasion strategy. Frontiers in Immunology 8, 636.CrossRefGoogle ScholarPubMed
Zhao, Y, Liu, MY, Wang, XL, et al. (2013) Modulation of inflammatory bowel disease in a mouse model following infection with Trichinella spiralis. Veterinary Parasitology 194, 211216.CrossRefGoogle Scholar