Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T00:25:56.310Z Has data issue: false hasContentIssue false

Galectin-3 is essential for reactive oxygen species production by peritoneal neutrophils from mice infected with a virulent strain of Toxoplasma gondii

Published online by Cambridge University Press:  14 September 2012

C. M. O. S. ALVES
Affiliation:
Laboratory of Immunoparasitology, Institute of Biomedical Sciences, Universidade Federal de Uberlândia, Av. Pará 1720, 38400-902, Uberlândia, MG, Brazil
D. A. O. SILVA
Affiliation:
Laboratory of Immunoparasitology, Institute of Biomedical Sciences, Universidade Federal de Uberlândia, Av. Pará 1720, 38400-902, Uberlândia, MG, Brazil
A. E. C. S. AZZOLINI
Affiliation:
Laboratory of Immunochemistry, Department of Physics and Chemistry, Universidade de São Paulo, Av. do Café s/no, 14040-903, Ribeirão Preto, SP, Brazil
C. M. MARZOCCHI-MACHADO
Affiliation:
Department of Clinical, Toxicological and Bromatological Analyses, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av. do Café s/no, 14040-903, Ribeirão Preto, SP, Brazil
Y. M. LUCISANO-VALIM
Affiliation:
Laboratory of Immunochemistry, Department of Physics and Chemistry, Universidade de São Paulo, Av. do Café s/no, 14040-903, Ribeirão Preto, SP, Brazil
M. C. ROQUE-BARREIRA
Affiliation:
Laboratory of Glycobiology, Department of Molecular and Cellular Biology and Pathogenic Bioagents, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Av. dos Bandeirantes 3900, 14049-900, Ribeirão Preto, SP, Brazil
J. R. MINEO*
Affiliation:
Laboratory of Immunoparasitology, Institute of Biomedical Sciences, Universidade Federal de Uberlândia, Av. Pará 1720, 38400-902, Uberlândia, MG, Brazil
*
*Corresponding author: Laboratório de Imunoparasitologia, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Pará 1720, Campus Umuarama, 38400-902, Uberlândia, MG, Brazil. Tel: +55 34 3218 2058. Fax: +55 34 3218 2333. E-mail: [email protected]

Summary

Toxoplasma gondii stimulates a potent pro-inflammatory response and neutrophils are involved in early infection. Galectin-3 (Gal-3) is an endogenous modulator of inflammatory processes and anti-infective agents, but its interaction with neutrophils in T. gondii infection is still unclear. Here, we evaluated the role of Gal-3 in peritoneal inflammation, reactive oxygen species (ROS) production by neutrophils and survival, after in vivo T. gondii infection with virulent RH strain, using Gal-3 deficient and wild type mice. Animals were inoculated with thioglycollate or tachyzoites, and peritoneal cells were harvested for analysis of the influx of leukocytes. Neutrophils were isolated from peritoneal exudates from infected mice and stimulated with phorbol myristate acetate (PMA) to evaluate ROS production by luminol-dependent chemiluminescence assay. Our results showed that: (1) Gal-3 upregulates peritoneal inflammation, with enhanced recruitment of neutrophils and lymphocytes after thioglycollate stimulation, but does not influence the enhanced neutrophil influx after early T. gondii infection; (2) Gal-3 upregulates ROS generation by inflammatory peritoneal neutrophils from infected mice, but downregulates its production in non-infected mice and (3) Gal-3 does not influence the survival of mice after infection with the virulent T. gondii strain. In conclusion, Gal-3 is essential for ROS generation by neutrophils in the initial acute phase of T. gondii infection and this phenomenon may constitute an attempt to control parasite growth during in vivo infection with the T. gondii virulent strain.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alves, C. M. O. S., Marzocchi-Machado, C. M., Carvalho, I. F. and Lucisano-Valim, Y. M. (2003). Application of the chemiluminescence systems to evaluated the role of Fcγ and complement receptors in stimulating the oxidative burst in neutrophils. Talanta 60, 601608. doi: 10.1016/S0039-9140(03)00188-7.CrossRefGoogle ScholarPubMed
Alves, C. M. O. S., Silva, D. A. O., Azzolini, A. E. C. S., Marzocchi-Machado, C. M., Carvalho, J. V., Pajuaba, A. C., Lucisano-Valim, Y. M., Chammas, R., Liu, F. T, Roque-Barreira, M. C. and Mineo, J. R. (2010). Galectin-3 plays a modulatory role in the life span and activation of murine neutrophils during early Toxoplasma gondii infection. Immunobiology 215, 475485. doi: 10.1016/j.imbio.2009.08.001.CrossRefGoogle Scholar
Baron, E. J. and Proctor, R. A. (1982). Elicitation of peritoneal polymorphonuclear neutrophils from mice. Journal of Immunological Methods 49, 305313.CrossRefGoogle ScholarPubMed
Barondes, S. H., Cooper, D. N. W., Gitt, S. M. A. and Leffler, H. (1994). Galectins. Structure and function of a large family of animal lectins. The Journal of Biological Chemistry 269, 2080720810.CrossRefGoogle ScholarPubMed
Bartley, P. M., Wright, S., Sales, J., Chianini, F., Buxton, D. and Innes, E. A. (2006). Long-term passage of tachyzoites in tissue culture can attenuate virulence of Neospora caninum in vivo. Parasitology 133, 421432. doi: 10.1017/S0031182006000539.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. The American Journal of Pathology 168, 19101920. doi: 10.2353/ajpath.2006.050636.CrossRefGoogle ScholarPubMed
Bliss, S. K., Butcher, B. A. and Denkers, E. Y. (2000). Rapid recruitment of neutrophils containing prestored IL-12 during microbial infection. The Journal of Immunology 165, 45154521.CrossRefGoogle ScholarPubMed
Bliss, S. K., Gavrilescu, L. C., Alcaraz, A. and Denkers, E. Y. (2001). Neutrophil depletion during Toxoplasma gondii infection leads to impaired immunity and lethal systemic pathology. Infection and Immunity 69, 48984905. doi: 10.1128/IAI.69.8.4898-4905.2001.CrossRefGoogle ScholarPubMed
Breuilh, L., Vanhoutte, F., Fontaine, J., van Stijn, C. M., Tillie-Leblond, I., Capron, M., Faveeuw, C., Jouault, T., van Die, I., Gosset, P. and Trottein, F. (2007). Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells. Infection and Immunity 75, 51485157. doi: 10.1128/IAI.02006-06.CrossRefGoogle ScholarPubMed
Buzoni-Gatel, D., Schulthess, J., Menard, L. C. and Kasper, L. H. (2006). Mucosal defences against orally acquired protozoan parasites, emphasis on Toxoplasma gondii infections. Cellular Microbiology 8, 535544. doi: 10.1111/j.1462-5822.2006.00692.x.CrossRefGoogle ScholarPubMed
Cheung, K., Archibald, A. C. and Robinson, M. F. (1983). The origin of chemiluminescence produced by neutrophils stimulated by opsonized zymosan. The Journal of Immunology 130, 23242329.CrossRefGoogle ScholarPubMed
Colnot, C., Ripoche, M. A., Milon, G., Montagutelli, X., Crocker, P. R. and Poirier, F. (1998). Maintenance of granulocyte numbers during acute peritonitis is defective in galectin-3-null mutant mice. Immunology 94, 290296.CrossRefGoogle ScholarPubMed
Debierre-Grockiego, F., Niehus, S., Coddeville, B., Elass, E., Poirier, F., Weingart, R., Schmidt, R. R, Mazurier, J., Guérardel, Y. and Schwarz, R. T. (2010). Binding of Toxoplasma gondii glycosylphosphatidylinositols to galectin-3 is required for their recognition by macrophages. The Journal of Biological Chemistry 285, 3274432750. doi: 10.1074/jbc.M110.137588.CrossRefGoogle ScholarPubMed
Del Rio, L., Bennouna, S., Salinas, J. and Denkers, E. Y. (2001). CXXR2 deficiency confers impaired neutrophil recruitment and increased susceptibility during Toxoplasma gondii infection. The Journal of Immunology 167, 65036509.CrossRefGoogle ScholarPubMed
Hsu, D. K., Yang, R., Pan, Z., Yu, L., Salomon, D. R., Fung-Leung, W. P. and Liu, F. T. (2000). Targeted disruption of the Galectin-3 gene results in attenuated peritoneal inflammatory responses. The American Journal of Pathology 156, 10731083.CrossRefGoogle ScholarPubMed
Iwasaki, A. and Medzhitov, R. (2004). Toll-like receptor control of the adaptive immune responses. Nature Immunology 5, 987995. doi:10.1038/ni1112.CrossRefGoogle ScholarPubMed
Kim, H., Lee, J., Hyun, J. W., Park, J. W., Joo, H. G. and Shin, T. (2007). Expression and immunohistochemical localization of galectin-3 in various mouse tissues. Cell Biology International 31, 655662.CrossRefGoogle ScholarPubMed
Liu, F. T. (2005). Regulatory roles of galectins in the immune response. International Archives of Allergy and Immunology 136, 385400. doi: 10.1159/000084545.CrossRefGoogle ScholarPubMed
Mineo, J. R., Camargo, M. E. and Ferreira, A. W. (1980). Enzyme-linked immunosorbent assay for antibodies to Toxoplasma gondii polysaccharides in human toxoplasmosis. Infection and Immunity 27, 283287.CrossRefGoogle ScholarPubMed
Munoz, M., Liesenfeld, O. and Heimesaat, M. M. (2011). Immunology to Toxoplasma gondii. Immunological Reviews 240, 269285. doi: 10.1111/j.1600-065X.2010.00992.x.CrossRefGoogle ScholarPubMed
Ruas, L. P., Bernardes, E. S., Fermino, M. L., de Oliveira, L. L., Hsu, D. K., Liu, F. T., Chammas, R. and Roque-Barreira, M. C. (2009). Lack of galectin-3 drives response to Paracoccidioides brasiliensis toward a Th2-biased immunity. PLoS One 4, e4519. doi: 10.1371/journal.pone.0004519.CrossRefGoogle Scholar
Sayles, P. C. and Johnson, L. L. (1996). Exacerbation of toxoplasmosis in neutrophil-depleted mice. Natural Immunity 15, 249258.Google ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258. doi: 10.1016/S0020-7519(00)00124-7.CrossRefGoogle ScholarPubMed
van den Berg, T. K., Honing, H., Franke, N., van Remoortere, A., Schiphorst, W. E., Liu, F. T., Deelder, A. M., Cummings, R. D., Hokke, C. H. and van Die, I. (2004). LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition. The Journal of Immunology 173, 19021907.CrossRefGoogle ScholarPubMed
van Gisbergen, K. P., Geijtenbeek, T. B. and van Kooyk, Y. (2005). Close encounters of neutrophils and DCs. Trends in Immunology 26, 626631. doi: 10.1016/j.it.2005.09.007.CrossRefGoogle ScholarPubMed
Wilkie, R. P., Vissers, M. C. M., Dragunow, M. and Hampton, M. B. (2007). A functional NADPH-oxidase prevents caspase involvement in the clearance of phagocytic neutrophils. Infection and Immunity 75, 32563263. doi: 10.1128/IAI.01984-06.CrossRefGoogle ScholarPubMed