Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T11:52:18.917Z Has data issue: false hasContentIssue false
  • English
  • Français

B-1 cells contribute to susceptibility in experimental infection with Leishmania (Leishmania) chagasi

Published online by Cambridge University Press:  18 August 2015

WAGNER FRANCISCO KENNERLY MARCONDES GONZAGA ,
VANESSA XAVIER ,
BRUNO CAMOLESE VIVANCO ,
JOSÉ DANIEL LOPES  and
PATRICIA XANDER
WAGNER FRANCISCO KENNERLY MARCONDES GONZAGA
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, Brazil
VANESSA XAVIER
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo – Campus Diadema, Brazil
BRUNO CAMOLESE VIVANCO
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, Brazil
JOSÉ DANIEL LOPES
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, Brazil Universidade Federal de São Paulo – Campus Diadema
PATRICIA XANDER*
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo – Campus Diadema, Brazil
*
*Corresponding author. Departamento de Ciências Biológicas, Universidade Federal de São Paulo – Campus Diadema, Rua São Nicolau, 210, 4° andar, 04023-900, Diadema, Brasil. E-mail: patricia.xander@unifesp.com.
Get access Rights & Permissions [Opens in a new window]

Summary

The immune response to leishmaniasis is complex, and the result of infection depends on both the genetic composition of the Leishmania species and the immunity of the host. Clinical and experimental evidence suggest that the activation of B cells leads to exacerbation of visceral leishmaniasis. However, the role of B-1 cells (a subtype of B lymphocytes) in the pathogenesis of experimental visceral leishmaniasis has not yet been elucidated. In this study, we investigated the importance of B-1 cells in experimental infection with Leishmania. (L.) chagasi. Our results showed that BALB/XID mice (X-linked immunodeficient mice which are genetically deficient in B-1 cells) infected with L. (L.) chagasi for 45 days had a significant reduction in parasite load in the spleen when compared with control mice. Cytokine analysis showed that the BALB/XID mice had lower amounts of IL-10 in their sera compared with control group. In addition, the transfer of B-1 cells from wild type mice into IL-10KO animals led to an increase in susceptibility to L. (L.) chagasi infection in the IL-10KO mice, suggesting that the IL-10 produced by these cells is important in experimental infection. Our results suggest that B-1 cells may play an important role in susceptibility to L. (L.) chagasi.

Keywords

visceral leishmaniasisB-1 cellsIL-10
Type
Research Article
Information
Parasitology , Volume 142 , Issue 12 , October 2015 , pp. 1506 - 1515
Copyright
Copyright © Cambridge University Press 2015 

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

Almeida, S. R., Aroeira, L. S., Frymuller, E., Dias, M. A., Bogsan, C. S., Lopes, J. D. and Mariano, M. (2001). Mouse B-1 cell-derived mononuclear phagocyte, a novel cellular component of acute non-specific inflammatory exudate. International Immunology 13, 1193–1201.Google Scholar
Ansari, N. A., Kumar, R., Gautam, S., Nylén, S., Singh, O. P., Sundar, S. and Sacks, D. (2011). IL-27 and IL-21 are associated with T cell IL-10 responses in human visceral leishmaniasis. Journal of Immunology 186, 3977–3985.Google Scholar
Ansel, K. M., Harris, R. B. and Cyster, J. G. (2002). CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16, 67–76.CrossRefGoogle ScholarPubMed
Babai, B., Louzir, H., Cazenave, P. A. and Dellagi, K. (1999). Depletion of peritoneal CD5+ B cells has no effect on the course of Leishmania major infection in susceptible and resistant mice. Clinical and Experimental Immunology 117, 123–129.CrossRefGoogle ScholarPubMed
Barbiéri, C. L., Doine, A. I. and Freymuller, E. (1990). Lysosomal depletion in macrophages from spleen and foot lesions of Leishmania-infected hamster. Experimental Parasitology 71, 218–228.Google Scholar
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J. and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Casato, M., de Rosa, F. G., Pucillo, L. P., Ilardi, I., di Vico, B., Zorzin, L. R., Sorgi, M. L., Fiaschetti, P., Coviello, R., Laganà, B., Fiorilli, M. (1999). Mixed cryoglobulinemia secondary to visceral Leishmaniasis. Arthritis and Rheumatism 42, 2007–2011.Google Scholar
Crane, D. D., Griffin, A. J., Wehrly, T. D. and Bosio, C. M. (2013). B1a cells enhance susceptibility to infection with virulent Francisella tularensis via modulation of NK/NKT cell responses. Journal of Immunology 190, 2756–2766.CrossRefGoogle ScholarPubMed
Engwerda, C. R., Ato, M. and Kaye, P. M. (2004). Macrophages, pathology and parasite persistence in experimental visceral leishmaniasis. Trends in Parasitology 20, 524–530.CrossRefGoogle ScholarPubMed
Ferreira, J. H., Gentil, L. G., Dias, S. S., Fedeli, C. E., Katz, S and Barbiéri, C. L. (2008). Immunization with the cysteine proteinase Ldccys1 gene from Leishmania (Leishmania) chagasi and the recombinant Ldccys1 protein elicits protective immune responses in a murine model of visceral leishmaniasis. Vaccine 26, 677–685.Google Scholar
Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D. and Anderton, S. M. (2002). B cells regulate autoimmunity by provision of IL-10. Nature Immunology 3, 944–950.Google Scholar
Gaubert, S., Viana da Costa, A., Maurage, C. A., Lima, E. C., Fontaine, J., Lafitte, S., Minoprio, P., Capron, A. and Grzych, J. M. (1999). X-linked immunodeficiency affects the outcome of Schistosoma mansoni infection in the murine model. Parasite Immunology 21, 89–101.Google Scholar
González, A., Yáñez, A., Gozalbo, D. and Gil, M. L. (2008). MyD88 is dispensable for resistance to Paracoccidioides brasiliensis in a murine model of blood-borne disseminated infection. FEMS Immunology and Medical Microbiology 54, 365–374.Google Scholar
Goto, H. and Prianti, M. D. (2009). Immunoactivation and immunopathogeny during active visceral leishmaniasis. Revista do Instituto de Medicina Tropical de São Paulo 51, 241–246.Google Scholar
Griffin, D. O. and Rothstein, T. L. (2012). Human “orchestrator” CD11b(+) B1 cells spontaneously secrete interleukin-10 and regulate T-cell activity. Molecular Medicine 18, 1003–1008.Google Scholar
Hayakawa, K., Hardy, R. R., Parks, D. R. and Herzenberg, L. A. (1983). The “Ly-1 B” cell subpopulation in normal immunodefective, and autoimmune mice. Journal of Experimental Medicine 157, 202–218.CrossRefGoogle Scholar
Hayakawa, K., Hardy, R. R., Herzenberg, L. A. and Herzenberg, L. A. (1985). Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. Journal of Experimental Medicine 161, 1554–1568.Google Scholar
Herbert, D. R., Nolan, T. J., Schad, G. A. and Abraham, D. (2002). The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunology 24, 95–101.Google Scholar
Herzenberg, L. A., Stall, A. M., Lalor, P. A., Sidman, C., Moore, W. A., Parks, D. R. and Herzenberg, L. A. (1986). The Ly-1 B cell lineage. Immunological Review 93, 81–102.Google Scholar
Hoerauf, A., Solbach, W., Lohoff, M. and Röllinghoff, M. (1994). The Xid defect determines an improved clinical course of murine leishmaniasis in susceptible mice. International Immunology 6, 1117–1124.Google Scholar
Junqueira-Kipnis, A. P., Kipnis, A., Henao Tamayo, M., Harton, M., Gonzalez Juarrero, M., Basaraba, R. J. and Orme, I. M. (2005). Interleukin-10 production by lung macrophages in CBA xid mutant mice infected with Mycobacterium tuberculosis . Immunology 115, 246–252.Google Scholar
Kantor, A. B. and Herzenberg, L. A. (1993). Origin of murine B cell lineages. Annual Review of Immunology 11, 501–538.Google Scholar
Kumar, R. and Nylén, S. (2012). Immunobiology of visceral leishmaniasis. Frontiers in Immunology 3, 251.Google Scholar
Lima, H. C., Bleyenberg, J. A. and Titus, R. G. (1997). A simple method for quantifying Leishmania in tissues of infected animals. Parasitology Today 13, 80–82.Google Scholar
Liu, Y., Chen, Y., Li, Z., Han, Y., Sun, Y., Wang, Q., Liu, B. and Su, Z. (2013). Role of IL-10-producing regulatory B cells in control of cerebral malaria in Plasmodium berghei infected mice. European Journal of Immunology 43, 2907–2918. doi: 10.1002/eji.201343512.Google Scholar
Louzir, H., Belal-Kacemi, L., Sassi, A., Laouini, D., Ben Ismail, R. and Dellagi, K. (1994). Natural autoantibodies, IgG antibodies to tetanus toxoid and CD5+ B cells in patients with Mediterranean visceral leishmaniasis. The Leishmania Study Group. Clinical and Experimental Immunology 95, 479–484.Google Scholar
Maroof, A., Beattie, L., Zubairi, S., Svensson, M., Stager, S. and Kaye, P. M. (2008). Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29, 295–305.CrossRefGoogle ScholarPubMed
McCall, L. I., Zhang, W. W. and Matlashewski, G. (2013). Determinants for the Development of Visceral Leishmaniasis Disease. PLoS Pathogens 9, e1003053.Google Scholar
Merino, M. C., Montes, C. L., Acosta-Rodriguez, E. V., Bermejo, D. A., Amezcua-Vesely, M. C . and Gruppi, A. (2010). Peritoneum from Trypanosoma cruzi-infected mice is a homing site of Syndecan-1 neg plasma cells which mainly provide non-parasite-specific antibodies. International Immunology 22, 399–410.Google Scholar
Minoprio, P., el Cheikh, M. C., Murphy, E., Hontebeyrie-Joskowicz, M., Coffman, R., Coutinho, A. and O'Garra, A. (1993). Xid-associated resistance to experimental Chagas’ disease is IFN-gamma dependent. Journal of Immunology 151, 4200–4208.Google Scholar
Mussalem, J. S., Squaiella-Baptistão, C. C., Teixeira, D., Yendo, T. M., Thies, F. G., Popi, A. F., Mariano, M. and Longo-Maugéri, I. (2012). Adjuvant effect of killed Propionibacterium acnes on mouse peritoneal B-1 lymphocytes and their early phagocyte differentiation. PLoS ONE 7, e33955.Google Scholar
Nylén, S. and Sacks, D. (2007). Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends in Immunology 28, 378–384.Google Scholar
Nylén, S., Khamesipour, A., Mohammadi, A., Jafari-Shakib, R., Eidsmo, L., Noazin, S., Modabber, F. and Akuffo, H. (2006). Surrogate markers of immunity to Leishmania major in leishmanin skin test negative individuals from an endemic area re-visited. Vaccine 24, 6944–6954.CrossRefGoogle ScholarPubMed
O'Garra, A., Chang, R., Go, N., Hastings, R., Haughton, G. and Howard, M. (1992). Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. European Journal of Immunology 22, 711–717.Google Scholar
Peruhype-Magalhães, V., Martins-Filho, O. A., Prata, A., Silva Lde, A., Rabello, A., Teixeira-Carvalho, A., Figueiredo, R. M., Guimarães-Carvalho, S. F., Ferrari, T. C., Van Weyenbergh, J. and Correa-Oliveira, R. (2006). Mixed inflammatory/regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral Leishmaniasis due to Leishmania chagasi infection. Clinical and Experimental Immunology 146, 124–132.Google Scholar
Popi, A. F., Godoy, L. C., Xander, P., Lopes, J. D. and Mariano, M. (2008). B-1 cells facilitate Paracoccidioides brasiliensis infection in mice via IL-10 secretion. Microbes and Infection 10, 817–824.CrossRefGoogle ScholarPubMed
Popi, A. F., Osugui, L., Perez, K. R., Longo-Maugéri, I. M. and Mariano, M. (2012). Could a B-1 cell derived phagocyte “be one” of the peritoneal macrophages during LPS-driven inflammation? PLoS ONE 7, e34570.Google Scholar
Ranatunga, D., Hedrich, C. M., Wang, F., McVicar, D. W., Nowak, N., Joshi, T., Feigenbaum, L., Grant, L. R., Stäger, S., Bream, J. H. (2009). A human IL10 BAC transgene reveals tissue-specific control of IL-10 expression and alters disease outcome. Proceedings of the National Academy of Sciences USA 106, 17123–17128.Google Scholar
Reimão, J. Q., Colombo, F. A., Pereira-Chioccola, V. L. and Tempone, A. G. (2011). In vitro and experimental therapeutic studies of the calcium channel blocker bepridil: detection of viable Leishmania (L.) chagasi by real-time PCR. Experimental Parasitology 128, 111–115.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, 886–894.Google Scholar
Russo, R. T. and Mariano, M. (2010). B-1 cell protective role in murine primary Mycobacterium bovis bacillus Calmette-Guerin infection. Immunobiology 215, 1005–1014.CrossRefGoogle ScholarPubMed
Singh, O. P., Gidwani, K., Kumar, R., Nylen, S., Jones, S. L., Boelaert, M., Sacks, D. and Sundar, S. (2012). Reassessment of immune correlates in human visceral leishmaniasis as defined by cytokine release in whole blood. Clinical Vaccine Immunology 19, 961–966.CrossRefGoogle ScholarPubMed
Stanley, A. C. and Engwerda, C. R. (2007). Balancing immunity and pathology in visceral leishmaniasis. Cellular Immunology 85, 138–147.Google Scholar
Stockdale, L. and Newton, R. (2013). A review of preventative methods against human leishmaniasis infection. PLOS Neglected Tropical Diseases 7, e2278.Google Scholar
Szymczak, W. A., Davis, M. J., Lundy, S. K., Dufaud, C., Olszewski, M. and Pirofski, L. A. (2013). X-linked immunodeficient mice exhibit enhanced susceptibility to Cryptococcus neoformans Infection. MBio Journal 4, e00265-13. doi: 10.1128/mBio.00265-13.Google Scholar
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, RESEARCH0034.Google Scholar
World Health Organization (2010). Control of the Leishmaniases. WHO Technical Report Series. No. 949. World Health Organization, Geneva, Switzerland.Google Scholar
Supplementary material: Image

Gonzaga supplementary material S1

Supplementary Figure

Download Gonzaga supplementary material S1(Image)
Image 28.8 MB