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Galectins expressed differently in genetically susceptible C57BL/6 and resistant BALB/c mice during acute ocular Toxoplasma gondii infection

Published online by Cambridge University Press:  09 March 2017

S.-J. CHEN
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of Education, Guangzhou 510080, Guangdong, China
Y.-X. ZHANG
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of Education, Guangzhou 510080, Guangdong, China
S.-G. HUANG*
Affiliation:
School of Stomatology, Jinan University, Guangzhou 510632, Guangdong, China
F.-L. LU*
Affiliation:
Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of Education, Guangzhou 510080, Guangdong, China
*
*Corresponding author: Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China, Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of Education, Guangzhou 510080, Guangdong, China and School of Stomatology, Jinan University, Guangzhou 510632, Guangdong, China. E-mail: [email protected]; [email protected]
*Corresponding author: Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, Guangdong, China, Key Laboratory of Tropical Disease Control (Sun Yat-sen University), Ministry of Education, Guangzhou 510080, Guangdong, China and School of Stomatology, Jinan University, Guangzhou 510632, Guangdong, China. E-mail: [email protected]; [email protected]

Summary

Ocular toxoplasmosis (OT) caused by Toxoplasma gondii is a major cause of infectious uveitis, however little is known about its immunopathological mechanism. Susceptible C57BL/6 (B6) and resistant BALB/c mice were intravitreally infected with 500 tachyzoites of the RH strain of T. gondii. B6 mice showed more severe ocular pathology and higher parasite loads in the eyes. The levels of galectin (Gal)-9 and its receptors (Tim-3 and CD137), interferon (IFN)-γ, IL-6 and IL-10 were significantly higher in the eyes of B6 mice than those of BALB/c mice; however, the levels of IFN-α and -β were significantly decreased in the eyes and CLNs of B6 mice but significantly increased in BALB/c mice after infection. After blockage of galectin–receptor interactions by α-lactose, neither ocular immunopathology nor parasite loads were different from those of infected BALB/c mice without α-lactose treatment. Although the expressions of Gal-9/receptor were significantly increased in B6 mice and Gal-1 and -3 were upregulated in both strains of mice upon ocular T. gondii infection, blockage of galectins did not change the ocular pathogenesis of genetic resistant BALB/c mice. However, IFN-α and -β were differently expressed in B6 and BALB/c mice, suggesting that type I IFNs may play a protective role in experimental OT.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Anderson, A. C., Anderson, D. E., Bregoli, L., Hastings, W. D., Kassam, N., Lei, C., Chandwaskar, R., Karman, J., Su, E. W., Hirashima, M., Bruce, J. N., Kane, L. P., Kuchroo, V. K. and Hafler, D. A. (2007). Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318, 11411143.CrossRefGoogle ScholarPubMed
Argüeso, P., Guzman-Aranguez, A., Mantelli, F., Cao, Z., Ricciuto, J. and Panjwani, N. (2009). Association of cell surface mucins with galectin-3 contributes to the ocular surface epithelial barrier. Journal of Biological Chemistry 284, 2303723045.CrossRefGoogle Scholar
Baum, L. G., Garner, O. B., Schaefer, K. and Lee, B. (2014). Microbe-host interactions are positively and negatively regulated by galectin-glycan interactions. Frontiers in Immunology 5, 284.CrossRefGoogle ScholarPubMed
Bernardes, E. S., Silva, N. M., Ruas, L. P., Mineo, J. R., Loyola, A. M., Hsu, D. K., Liu, F. T., Chammas, R. and Roque-Barreira, M. C. (2006). Toxoplasma gondii infection reveals a novel regulatory role for galectin-3 in the interface of innate and adaptive immunity. American Journal of Pathology 168, 19101920.CrossRefGoogle ScholarPubMed
Buzoni–Gatel, D., Debbabi, H., Mennechet, F. J., Martin, V., Lepage, A. C., Schwartzman, J. D. and Kasper, L. H. (2001). Murine ileitis after intracellular parasite infection is controlled by TGF-β–producing intraepithelial lymphocytes. Gastroenterology 120, 914924.CrossRefGoogle ScholarPubMed
Charles, E., Callegan, M. C. and Blader, I. J. (2007). The SAG1 Toxoplasma gondii surface protein is not required for acute ocular toxoplasmosis in mice. Infection and Immunity 75, 20792083.CrossRefGoogle Scholar
Chiba, S., Baghdadi, M., Akiba, H., Yoshiyama, H., Kinoshita, I., Dosaka-Akita, H., Fujioka, Y., Ohba, Y., Gorman, J. V., Colgan, J. D., Hirashima, M., Uede, T., Takaoka, A., Yagita, H. and Jinushi, M. (2012). Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nature Immunology 13, 832842.CrossRefGoogle ScholarPubMed
Deckert-Schlüter, M., Rang, A., Weiner, D., Huang, S., Wiestler, O. D., Hof, H. and Schlüter, D. (1996). Interferon-gamma receptor-deficiency renders mice highly susceptible to toxoplasmosis by decreased macrophage activation. Laboratory Investigation: a Journal of Technical Methods and Pathology 75, 827841.Google ScholarPubMed
Diez, B., Galdeano, A., Nicolas, R. and Cisterna, R. (1989). Relationship between the production of interferon-α/β and interferon-γ during acute toxoplasmosis. Parasitology 99, 1115.CrossRefGoogle ScholarPubMed
Dukaczewska, A., Tedesco, R. and Liesenfeld, O. (2015). Experimental Models of Ocular Infection with Toxoplasma Gondii . European Journal of Microbiology & Immunology (Bp) 5, 293305.CrossRefGoogle ScholarPubMed
Freshman, M. M., Merigan, T. C., Remington, J. S. and Brownlee, I. E. (1966). In vitro and in vivo antiviral action of an interferon-like substance induced by Toxoplasma gondii . Proceedings of the Society for Experimental Biology and Medicine 123, 862866.CrossRefGoogle ScholarPubMed
Gazzinelli, R. T., Hakim, F. T., Hieny, S., Shearer, G. M. and Sher, A. (1991). Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. Journal of Immunology 146, 286292.CrossRefGoogle ScholarPubMed
Gazzinelli, R., Xu, Y., Hieny, S., Cheever, A. and Sher, A. (1992). Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii . The Journal of Immunology 149, 175180.CrossRefGoogle ScholarPubMed
Han, S. J., Melichar, H. J., Coombes, J. L., Chan, S. W., Koshy, A. A., Boothroyd, J. C., Barton, G. M. and Robey, E. A. (2014). Internalization and TLR-dependent type I interferon production by monocytes in response to Toxoplasma gondii . Immunology and Cell Biology 92, 872881.CrossRefGoogle ScholarPubMed
Holland, G. N. (2003). Ocular toxoplasmosis: a global reassessment. Part I: epidemiology and course of disease. American Journal of Ophthalmology 136, 973988.CrossRefGoogle ScholarPubMed
Holland, G. N. (2004). Ocular toxoplasmosis: a global reassessment. Part II: disease manifestations and management. American Journal of Ophthalmology 137, 117.Google Scholar
Hu, X. H, Tang, M. X., Mor, G. and Liao, A. H. (2016). Tim-3: expression on immune cells and roles at the maternal-fetal interface. Journal of Reproductive Immunology 118, 9299.CrossRefGoogle ScholarPubMed
Kojima, K., Arikawa, T., Saita, N., Goto, E., Tsumura, S., Tanaka, R., Masunaga, A., Niki, T., Oomizu, S. and Hirashima, M. (2011). Galectin-9 attenuates acute lung injury by expanding CD14–plasmacytoid dendritic cell-like macrophages. American Journal of Respiratory and Critical Care Medicine 184, 328339.CrossRefGoogle ScholarPubMed
Kwon, B. S. and Weissman, S. M. (1989). cDNA sequences of two inducible T-cell genes. Proceedings of the National Academy of Sciences of the United States of America 86, 19631967.CrossRefGoogle ScholarPubMed
Liang, S. and Qin, X. (2013). Critical role of type I interferon-induced macrophage necroptosis during infection with Salmonella enterica serovar Typhimurium. Cellular & Molecular Immunology 10, 99100.CrossRefGoogle ScholarPubMed
Liesenfeld, O. (2002). Oral infection of C57BL/6 mice with Toxoplasma gondii: a new model of inflammatory bowel disease? Journal of Infectious Diseases 185 (Suppl. 1), S96101.CrossRefGoogle ScholarPubMed
Liesenfeld, O., Kosek, J., Remington, J. S. and Suzuki, Y. (1996). Association of CD4+ T cell-dependent, interferon-gamma-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii . Journal of Experimental Medicine 184, 597607.CrossRefGoogle ScholarPubMed
Liu, F. T. and Rabinovich, G. A. (2010). Galectins: regulators of acute and chronic inflammation. Annals of the New York Academy of Sciences 1183, 158182.CrossRefGoogle ScholarPubMed
Lu, F., Huang, S. and Kasper, L. H. (2003). Interleukin-10 and pathogenesis of murine ocular toxoplasmosis. Infection and Immunity 71, 71597163.CrossRefGoogle ScholarPubMed
Lu, F., Huang, S., Hu, M. S. and Kasper, L. H. (2005). Experimental ocular toxoplasmosis in genetically susceptible and resistant mice. Infection and Immunity 73, 51605165.CrossRefGoogle ScholarPubMed
Lu, X. X., McCoy, K. S., Xu, J. L., Hu, W. K., Chen, H. B., Jiang, K., Han, F., Chen, P. and Wang, Y. L. (2015). Galectin-9 ameliorates respiratory syncytial virus-induced pulmonary immunopathology through regulating the balance between Th17 and regulatory T cells. Virus Research 195, 162171.CrossRefGoogle ScholarPubMed
Lückoff, A., Caramoy, A., Scholz, R., Prinz, M., Kalinke, U. and Langmann, T. (2016). Interferon-beta signaling in retinal mononuclear phagocytes attenuates pathological neovascularization. EMBO Molecular Medicine 8, 670678.CrossRefGoogle ScholarPubMed
Maenz, M., Schluter, D., Liesenfeld, O., Schares, G., Gross, U. and Pleyer, U. (2014). Ocular toxoplasmosis past, present and new aspects of an old disease. Progress in Retinal and Eye Research 39, 77106.CrossRefGoogle ScholarPubMed
Nagineni, C. N., Pardhasaradhi, K., Martins, M. C., Detrick, B. and Hooks, J. J. (1996). Mechanisms of interferon-induced inhibition of Toxoplasma gondii replication in human retinal pigment epithelial cells. Infection and Immunity 64, 41884196.CrossRefGoogle ScholarPubMed
Orellana, M. A., Suzuki, Y., Araujo, F. and Remington, J. S. (1991). Role of beta interferon in resistance to Toxoplasma gondii infection. Infection and Immunity 59, 32873290.CrossRefGoogle ScholarPubMed
Panjwani, N. (2014). Role of galectins in re-epithelialization of wounds. Annals of Translational Medicine 2, 89.Google ScholarPubMed
Rochet, É., Brunet, J., Sabou, M., Marcellin, L., Bourcier, T., Candolfi, E. and Pfaff, A. W. (2015). Interleukin-6-driven inflammatory response induces retinal pathology in a model of ocular toxoplasmosis reactivation. Infection and Immunity 83 , 21092117.CrossRefGoogle Scholar
Sadler, A. J. and Williams, B. R. (2008). Interferon-inducible antiviral effectors. Nature Reviews. Immunology 8, 559568.CrossRefGoogle ScholarPubMed
Sampson, J. F., Hasegawa, E., Mulki, L., Suryawanshi, A., Jiang, S., Chen, W. S., Rabinovich, G. A., Connor, K. M. and Panjwani, N. (2015). Galectin-8 ameliorates murine autoimmune ocular pathology and promotes a regulatory T cell response. PLoS ONE 10, e0130772.CrossRefGoogle ScholarPubMed
Sampson, J. F., Suryawanshi, A., Chen, W.-S., Rabinovich, G. A. and Panjwani, N. (2016). Galectin-8 promotes regulatory T-cell differentiation by modulating IL-2 and TGFβ signaling. Immunology and Cell Biology 94, 213219.CrossRefGoogle ScholarPubMed
Sehrawat, S., Suryawanshi, A., Hirashima, M. and Rouse, B. T. (2009). Role of Tim-3/galectin-9 inhibitory interaction in viral-induced immunopathology: shifting the balance toward regulators. Journal of Immunology 182, 31913201.CrossRefGoogle ScholarPubMed
Sehrawat, S., Reddy, P. B., Rajasagi, N., Suryawanshi, A., Hirashima, M. and Rouse, B. T. (2010). Galectin-9/TIM-3 interaction regulates virus-specific primary and memory CD8 T cell response. PLoS Pathogens 6, e1000882.CrossRefGoogle ScholarPubMed
Sunil, V. R., Francis, M., Vayas, K. N., Cervelli, J. A., Choi, H., Laskin, J. D. and Laskin, D. L. (2015). Regulation of ozone-induced lung inflammation and injury by the beta-galactoside-binding lectin galectin-3. Toxicology and Applied Pharmacology 284, 236245.CrossRefGoogle ScholarPubMed
Suryawanshi, A., Cao, Z., Thitiprasert, T., Zaidi, T. S. and Panjwani, N. (2013). Galectin-1-mediated suppression of Pseudomonas aeruginosa–induced corneal immunopathology. The Journal of Immunology 190, 63976409.CrossRefGoogle ScholarPubMed
Suzuki, Y., Orellana, M. A., Schreiber, R. D. and Remington, J. S. (1988). Interferon-gamma: the major mediator of resistance against Toxoplasma gondii . Science 240, 516518.CrossRefGoogle ScholarPubMed
Suzuki, Y., Yang, Q. and Remington, J. S. (1995). Genetic resistance against acute toxoplasmosis depends on the strain of Toxoplasma gondii . Journal of Parasitology 81, 10321034.CrossRefGoogle ScholarPubMed
Vasta, G. R. (2009). Roles of galectins in infection. Nature Reviews Microbiology 7, 424438.CrossRefGoogle ScholarPubMed
Viguier, M., Advedissian, T., Delacour, D., Poirier, F. and Deshayes, F. (2014). Galectins in epithelial functions. Tissue Barriers 2, e29103.CrossRefGoogle ScholarPubMed
Wu, C., Thalhamer, T., Franca, R. F., Xiao, S., Wang, C., Hotta, C., Zhu, C., Hirashima, M., Anderson, A. C. and Kuchroo, V. K. (2014). Galectin-9-CD44 interaction enhances stability and function of adaptive regulatory T cells. Immunity 41, 270282.CrossRefGoogle ScholarPubMed