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Glutathione-S-transferase of Trichinella spiralis regulates maturation and function of dendritic cells

Published online by Cambridge University Press:  30 August 2019

Xuemin Jin ,
Yong Yang ,
Xiaolei Liu ,
Haining Shi ,
Xuepeng Cai ,
Xuenong Luo ,
Mingyuan Liu  and
Xue Bai Open the ORCID record for Xue Bai [Opens in a new window]
Xuemin Jin
Affiliation:
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun 130062, China
Yong Yang
Affiliation:
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun 130062, China
Xiaolei Liu
Affiliation:
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun 130062, China
Haining Shi
Affiliation:
Mucosal Immunology Laboratory, Pediatric Gastroenterology Unit, Massachusetts General Hospital, Boston, MA, USA
Xuepeng Cai
Affiliation:
China Institute of Veterinary Drugs Control, Beijing 100000, China State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, China
Xuenong Luo
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, China
Mingyuan Liu*
Affiliation:
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun 130062, China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225000, China.
Xue Bai*
Affiliation:
Key Laboratory of Zoonosis Research, Ministry of Education, Institute of Zoonosis, College of Veterinary Medicine, Jilin University, Changchun 130062, China
*
Author for correspondence: Xue Bai, E-mail: [email protected]; Mingyuan Liu, E-mail: [email protected]
Author for correspondence: Xue Bai, E-mail: [email protected]; Mingyuan Liu, E-mail: [email protected]
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Abstract

Immunomodulation by molecules from Trichinella spiralis (T. spiralis) has been widely reported. Glutathione-S-transferase (GST) is a major immune-modulator of the family of detoxification enzymes. Dendritic cells (DCs) are an important target for the regulation of the immune response by T. spiralis. In this study, the recombinant GST of T. spiralis (rTs-GST) was expressed and purified. rTs-GST induced low CD40 expression and moderate CD80, CD86 and MHC-II expressions and inhibited the increase of CD40, CD80 and CD86 on DCs induced by LPS. We showed that rTs-GST decreased the LPS-induced elevated level of pro-inflammatory cytokines of DCs and enhanced the level of regulatory cytokines IL-10 and TGF-β. Furthermore, co-culture of DCs and CD4+ T cells demonstrated that rTs-GST-treated DCs suppressed the proliferation of OVA-specific CD4+ T cells and increased the population of regulatory T cells (Tregs). rTs-GST-treated DCs induced a higher level of IL-4, IL-10 and TGF-β, but inhibited the level of IFN-γ. This indicates that rTs-GST-pulsed DCs induce both Th2-type responses and Tregs. These findings contribute to the current understanding of the immunomodulation of Ts-GST on cellular response and immunomodulation of T. spiralis.

Keywords

Dendritic cellsglutathione-S-transferasesemi-maturationTh2 immune responseTregsTrichinella spiralis
Type
Research Article
Information
Parasitology , Volume 146 , Special Issue 14: BSP 2018 Autumn Symposium , December 2019 , pp. 1725 - 1732
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Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

These authors contributed equally to this study

References

Bai, X, Wu, X, Wang, X, Guan, Z, Gao, F, Yu, J, Yu, L, Tang, B, Liu, X, Song, Y, Wang, X, Radu, B, Boireau, P, Wang, F and Liu, M (2012) Regulation of cytokine expression in murine macrophages stimulated by excretory/secretory products from Trichinella spiralis in vitro. Molecular and Cellular Biochemistry 360, 79–88.Google Scholar
Blum, A M., Hang, L, Setiawan, T, Urban, JP Jr., Stoyanoff, KM, Leung, J and Weinstock, JV (2012) Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. Journal of Immunology 189, 2512–2520.Google Scholar
Chen, ZB, Tang, H, Liang, YB, Yang, W, Wu, JG, Hu, XC, Li, ZY, Zeng, LJ and Ma, ZF (2016) Recombinant Trichinella spiralis 53-kDa protein activates M2 macrophages and attenuates the LPS-induced damage of endotoxemia. Innate Immunity 22, 419–432.Google Scholar
Cui, J, Li, LG, Jiang, P, Liu, RD, Yang, X, Liu, LN, Liu, P, Zhang, SB and Wang, ZQ (2015) Biochemical and functional characterization of the glutathione S-transferase from Trichinella spiralis. Parasitology Research 114, 2007–2013.Google Scholar
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, 833–842.Google Scholar
Della Bella, C, Benagiano, M, De Gennaro, M, Gomez-Morales, MA, Ludovisi, A, D'Elios, S, Luchi, S, Pozio, E, D'Elios, MM and Bruschi, F (2017) T-cell clones in human trichinellosis: evidence for a mixed Th1/Th2 response. Parasite Immunology 39, e12412.Google Scholar
Ding, J, Bai, X, Wang, XL, Wang, YF, Shi, HN, Rosenthal, B, Boireau, P, Wu, XP, Liu, MY and Liu, XL (2016) Developmental profile of select immune cells in mice infected with Trichinella spiralis during the intestinal phase. Veterinary Parasitology 231, 77–82.Google Scholar
Dowling, DJ, Hamilton, CM, Donnelly, S, La Course, J, Brophy, PM, Dalton, J and O'Neill, SM (2010) Major secretory antigens of the helminth Fasciola hepatica activate a suppressive dendritic cell phenotype that attenuates Th17 cells but fails to activate Th2 immune responses. Infection and Immunity 78, 793–801.Google Scholar
Driss, V, El Nady, M, Delbeke, M, Rousseaux, C, Dubuquoy, C, Sarazin, A, Gatault, S, Dendooven, A, Riveau, G, Colombel, JF, Desreumaux, P, Dubuquoy, L and Capron, M (2016) The schistosome glutathione S-transferase P28GST, a unique helminth protein, prevents intestinal inflammation in experimental colitis through a Th2-type response with mucosal eosinophils. Mucosal Immunology 9, 322–335.Google Scholar
Grezel, D, Capron, M, Grzych, JM, Fontaine, J, Lecocq, JP and Capron, A (1993) Protective immunity induced in rat schistosomiasis by a single dose of the Sm28GST recombinant antigen: effector mechanisms involving IgE and IgA antibodies. European Journal of Immunology 23, 454–460.Google Scholar
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.Google Scholar
Gupta, S, Bhandari, YP, Reddy, MV, Harinath, BC and Rathaur, S (2005) Setaria cervi: immunoprophylactic potential of glutathione-S-transferase against filarial parasite Brugia malayi. Experimental Parasitology 109, 252–255.Google Scholar
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.Google Scholar
Kapsenberg, ML (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nature Reviews Immunology 3, 984.Google Scholar
Li, LG, Wang, ZQ, Liu, RD, Yang, X, Liu, LN, Sun, GG, Jiang, P, Zhang, X, Zhang, GY and Cui, J (2015) Trichinella spiralis: low vaccine potential of glutathione S-transferase against infections in mice. Acta Tropica 146, 25–32.Google Scholar
Lutz, MB, Kukutsch, N, Ogilvie, AL, Rossner, S, Koch, F, Romani, N and Schuler, G (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223, 77–92.Google Scholar
Maizels, RM and McSorley, HJ (2016) Regulation of the host immune system by helminth parasites. Journal of Allergy and Clinical Immunology 138, 666–675.Google Scholar
Mannervik, B, Alin, P, Guthenberg, C, Jensson, H, Tahir, MK, Warholm, M and Jornvall, H (1985) Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proceedings of the National Academy of Sciences of the United States of America 82, 7202–7206.Google Scholar
Matisz, CE, Faz-Lopez, B, Thomson, E, Al Rajabi, A, Lopes, F, Terrazas, LI, Wang, A, Sharkey, KA and McKay, DM (2017) Suppression of colitis by adoptive transfer of helminth antigen-treated dendritic cells requires interleukin-4 receptor-alpha signaling. Scientific Reports 7, 40631.Google Scholar
Morrison, CA, Colin, T, Sexton, JL, Bowen, F, Wicker, J, Friedel, T and Spithill, TW (1996) Protection of cattle against Fasciola hepatica infection by vaccination with glutathione S-transferase. Vaccine 14, 1603–1612.Google Scholar
Ren, HJ, Cui, J, Yang, W, Liu, RD and Wang, ZQ (2013) Identification of differentially expressed genes of Trichinella spiralis larvae after exposure to host intestine milieu. PLoS One 8, e67570.Google Scholar
Rojas, J, Rodriguez-Osorio, M and Gomez-Garcia, V (1997) Immunological characteristics and localization of the Trichinella spiralis glutathione S-transferase. Journal of Parasitology 83, 630–635.Google Scholar
Rutella, S, Bonanno, G, Procoli, A, Mariotti, A, de Ritis, DG, Curti, A, Danese, S, Pessina, G, Pandolfi, S, Natoni, F, Di Febo, A, Scambia, G, Manfredini, R, Salati, S, Ferrari, S, Pierelli, L, Leone, G and Lemoli, RM (2006) Hepatocyte growth factor favors monocyte differentiation into regulatory interleukin (IL)-10++IL-12low/neg accessory cells with dendritic-cell features. Blood 108, 218–227.Google Scholar
Schwarz, H, Schmittner, M, Duschl, A and Horejs-Hoeck, J (2014) Residual endotoxin contaminations in recombinant proteins are sufficient to activate human CD1c+ dendritic cells. PLoS One 9, e113840.Google Scholar
Shevach, EM (2018) Foxp3(+) T regulatory cells: still many unanswered questions-A perspective after 20 years of study. Frontiers in Immunology 9, 1048.Google Scholar
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, 239–249.Google Scholar
Sun, Y, Liu, G, Li, Z, Chen, Y, Liu, Y, Liu, B and Su, Z (2013) Modulation of dendritic cell function and immune response by cysteine protease inhibitor from murine nematode parasite Heligmosomoides polygyrus. Immunology 138, 370–381.Google Scholar
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.Google Scholar
Tang, B, Liu, MY, Wang, LB, Yu, SY, Shi, HN, Boireau, P, Cozma, V, Wu, XP and Liu, XL (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.Google Scholar
Torres-Aguilar, H, Aguilar-Ruiz, SR, Gonzalez-Perez, G, Munguia, R, Bajana, S, Meraz-Rios, MA and Sanchez-Torres, C (2010) Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific energy and regulatory properties in memory CD4+ T cells. Journal of Immunology 184, 1765–1775.Google Scholar
Villablanca, EJ, Russo, V and Mora, JR (2008) Dendritic cell migration and lymphocyte homing imprinting. Histology and Histopathology 23, 897–910.Google Scholar
Williams, JW, Tjota, MY, Clay, BS, Vander Lugt, B, Bandukwala, HS, Hrusch, CL, Decker, DC, Blaine, KM, Fixsen, BR, Singh, H, Sciammas, R and Sperling, AI (2013) Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nature Communications 4, 2990.Google Scholar
Xiao, YJ, Shi, MH, Qiu, Q, Huang, MC, Zeng, S, Zou, YY, Zhan, ZP, Liang, LQ, Yang, XY and Xu, HS (2016) Piperlongumine suppresses dendritic cell maturation by reducing production of reactive oxygen species and has therapeutic potential for rheumatoid arthritis. Journal of Immunology 196, 4925–4934.Google Scholar
Xu, N, Liu, X, Tang, B, Wang, L, Shi, HN, Boireau, P, Liu, M and Bai, X (2017) Recombinant Trichinella pseudospiralis serine protease inhibitors alter macrophage polarization in vitro. Frontiers in Microbiology 8, 1834.Google Scholar
Zhan, B, Liu, S, Perally, S, Xue, J, Fujiwara, R, Brophy, P, Xiao, S, Liu, Y, Feng, J, Williamson, A, Wang, Y, Bueno, LL, Mendez, S, Goud, G, Bethony, JM, Hawdon, JM, Loukas, A, Jones, K and Hotez, PJ (2005) Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infection and Immunity 73, 6903–6911.Google Scholar
Zhan, B, Perally, S, Brophy, PM, Xue, J, Goud, G, Liu, S, Deumic, V, de Oliveira, LM, Bethony, J, Bottazzi, ME, Jiang, D, Gillespie, P, Xiao, SH, Gupta, R, Loukas, A, Ranjit, N, Lustigman, S, Oksov, Y and Hotez, P (2010) Molecular cloning, biochemical characterization, and partial protective immunity of the heme-binding glutathione S-transferases from the human hookworm Necator americanus. Infection and Immunity 78, 1552–1563.Google Scholar
Zhu, J, Yamane, H and Paul, WE (2010) Differentiation of effector CD4 T cell populations (*). Annual Review of Immunology 28, 445–489.Google Scholar