Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-19T07:15:16.545Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased susceptibility to Strongyloides venezuelensis in mice due to Mycobacterium bovis co-infection which modulates production of Th2 cytokines

Published online by Cambridge University Press:  07 August 2009

A. M. CARMO ,
M. A. VICENTINI ,
A. T. DIAS ,
L. L. ALVES ,
C. C. S. ALVES ,
J. S. BRANDI ,
M. L. DE PAULA ,
A. FERNANDES ,
M. M. BARSANTE  and
M. A. SOUZA
...Show all authors
A. M. CARMO
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
M. A. VICENTINI
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
A. T. DIAS
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
L. L. ALVES
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
C. C. S. ALVES
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
J. S. BRANDI
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
M. L. DE PAULA
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
A. FERNANDES
Affiliation:
Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-901, Minas Gerais, Brazil
M. M. BARSANTE
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
M. A. SOUZA
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
H. C. TEIXEIRA
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
D. NEGRÃO-CORRÊA
Affiliation:
Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-901, Minas Gerais, Brazil
A. P. FERREIRA*
Affiliation:
Departamento de Parasitologia, Microbiologia e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, 36036-330, Minas Gerais, Brazil
*
*Corresponding author: Laboratório de Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Campus Martelos, 36036-330 Juiz de Fora, MG, Brazil. Tel: +55 32 32293214. Fax: +55 32 32293214. E-mail address: ana.paula@ufjf.edu.br.
Get access Rights & Permissions [Opens in a new window]

Summary

An estimated quarter of the world's population possesses an infection caused by gastrointestinal nematodes, which induce a Th2 type immune response. Concomitant infection of nematodes with Mycobacterium tuberculosis, which induces a predominantly Th1 type response, is very frequent in tropical and subtropical regions. This study examined immune responses of BALB/c mice infected with Strongyloides venezuelensis and then co-infected with Mycobacterium bovis. The number of worms in the intestine, eggs in feces, cytokine production in lungs and intestine and the expression of CD80, CD86, CTLA-4 and CD28 cell markers on pulmonary cells were analysed. Our results indicate that co-infected mice had an increased parasite burden, which correlates with elevated IFN-γ and IL-10 cytokine production and decreased IL-4 and IL-13. Moreover, decreased expression of CD80 and increased expression of CTLA-4 were observed in co-infected mice. Our data point out that susceptibility to Strongyloides venezuelensis infection is increased by Mycobacterium bovis co-infection, resulting in higher parasite survival.

Keywords

Mycobacterium bovisStrongyloides venezuelensisco-infectionBALB/c micecytokine productionparasite susceptibility
Type
Research Article
Information
Parasitology , Volume 136 , Issue 11 , September 2009 , pp. 1357 - 1365
Copyright
Copyright © Cambridge University Press 2009

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

Baek, B. K., Islam, M. K., Kim, B. S., Lim, C. W., Oluoch, A. O., Kim, C. H. and Kakoma, I. (2003). Characterization of the protective response against a homologous challenge infection with Strongyloides venezuelensis in rats. Veterinary Parasitology 113, 217–227.CrossRefGoogle ScholarPubMed
Carvalho, E. M. and Porto, A. F. (2004). Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunology 6, 487–497.CrossRefGoogle Scholar
Couper, K. N., Blount, D. G. and Riley, E. M. (2008). IL-10: The master regulator of immunity to infection. Journal of Immunology 180, 5771–5777.CrossRefGoogle ScholarPubMed
Demangel, C., Bertolino, P. and Britton, W. J. (2002). Autocrine IL-10 impairs dendritic cell (DC)-derived immune response to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. European Journal of Immunology 32, 994–1002.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Elias, D., Akuffo, H., Pawlowski, A., Haile, M., Schön, T. and Britton, S. (2005). Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent M. tuberculosis. Vaccine 23, 1326–1334.CrossRefGoogle Scholar
Fernandes, A., Pereira, A. T. M., Eschenazi, P. D., Schilter, H. C., Sousa, A. L. S., Teixeira, M. M. and Negrão-Corrêa, D. (2008). Evaluation of the immune response against Strongyloides venezuelensis in antigen-immunized or previously infected mice. Parasite Immunology 30, 139–149.CrossRefGoogle ScholarPubMed
Ferreira, A. P., Aguiar, A. S., Fava, M. W. B., Corrêa, J. O., Teixeira, F. M. and Teixeira, H. C. (2002). Can the efficacy of Bacille Calmette-Guérin tuberculosis vaccine be affected by intestinal parasitic infections. Journal of Infectious Diseases 186, 441–442.CrossRefGoogle ScholarPubMed
Ferreira, C. M., Pereira, A. T., Souza, R. S., Cassali, G. D., Souza, D. G., Lemos, V. S., Teixeira, M. M. and Negrão-Corrêa, D. (2007). Prevention of changes in airway function facilities Strongyloides venezuelensis infection in rats. Microbes and Infection 9, 813–820.CrossRefGoogle Scholar
Flynn, J. L. and Chan, J. (2001). Immunology of tuberculosis. Annual Review of Immunology 19, 93–129.CrossRefGoogle ScholarPubMed
Genta, R. M. (1989). Global prevalence of strongyloidiasis: critical review with epidemiologic insights into the prevention of disseminated disease. Reviews of Infectious Diseases 11, 755–767.CrossRefGoogle ScholarPubMed
Jung, Y. J., LaCourse, R., Ryan, L. and North, R. J. (2008). ‘Immunization’ against airborne tuberculosis by an earlier primary response to a concurrent intravenous infection. Immunology 124, 514–521.CrossRefGoogle ScholarPubMed
Kursar, M., Koch, M., Mittruker, H. W., Nouailles, G., Bonhagen, K., Kamradt, T. and Kaufmann, S. H. (2007). Cutting edge: regulatory T cells prevent efficient clearance of Mycobacterium tuberculosis. Journal of Immunology 178, 2661–2665.CrossRefGoogle ScholarPubMed
Lenschow, D. J., Su, G. H., Zuckerman, L. A., Nabavi, N., Jellis, C. L., Gray, G. S., Miller, J. and Bluestone, J. A. (1993). Expression and functional significance of an additional ligand for CTLA-4. Proceedings of the National Academy of Sciences, USA 90, 11054–11058.CrossRefGoogle ScholarPubMed
Linsley, P. S., Bradshaw, J., Urnes, M., Grosmaire, L. and Ledbetter, J. A. (1993). CD28 engagement by B7/BB-1 induces transient down-regulation of CD28 synthesis and prolonged unresponsiveness to CD28 signaling. Journal of Immunology 150, 3161–3169.CrossRefGoogle ScholarPubMed
Liu, Z., Liu, Q., Pesce, J., Whitmire, J., Ekkens, M. J., Foster, A., VanNoy, J., Sharpe, A. H., Urban, J. F. Jr, and Gause, W. C. (2002). Nippostrongylus brasiliensis can induce B7-independent antigen-specific development of IL-4-producing T cells from Naïve CD4 T cells in vivo. Journal of Immunology 169, 6959–6968.CrossRefGoogle ScholarPubMed
Lu, P., Zhou, X., Chen, S. J., Moorman, M., Morris, S. C., Finkelman, F. D., Linsley, P., Urban, J. F. and Gause, W. C. (1994). CTLA-4 ligands are required to induce an in vivo intreleukin 4 response to a gastrointestinal nematode parasite. The Journal of Experimental Medicine 180, 693–698.CrossRefGoogle Scholar
Machado, E. R., Ueta, M. T., Lourenço, E. V., Aníbal, F. F., Roque-Barreira, M. C. and Faccioli, L. H. (2007). Comparison of immune responses in mice infected with different strains of Strongyloides venezuelensis. Parasite Immunology 29, 549–557.CrossRefGoogle ScholarPubMed
Manzotti, C. N., Tipping, H., Perry, L. C., Mead, K. I., Blair, P. J., Zheng, Y. and Sansom, D. M. (2002). Inhibition of human T cell proliferation by CTLA-4 utilizes CD80 and requires CD25+ regulatory T cells. European Journal of Immunology 32, 2888–2896.3.0.CO;2-F>CrossRefGoogle Scholar
Mueller, D. L. (2000). T cells: A proliferation of costimulatory molecules. Current Biology 10, 227–230.CrossRefGoogle ScholarPubMed
Nakajima, A., Watanabe, N., Yoshino, S., Yagita, H., Okumura, K. and Azuma, M. (1997). Requirement of CD28 – CD86 co-stimulation in the interaction between antigen – primed T helper type 2 and B cells. International Immunology 9, 637–644.CrossRefGoogle ScholarPubMed
Negrão-Corrêa, D. and Teixeira, M. M. (2006). The mutual influence of nematode infection and allergy. Chemical Immunology and Allergy 90, 14–28.Google ScholarPubMed
Negrão-Corrêa, D., Pinho, V., Souza, D. G., Pereira, A. T., Fernandes, A., Scheuermann, K., Souza, A. L. and Teixeira, M. M. (2006). Expression of IL-4 receptor on non-bone marrow-derived cells is necessary for the timely elimination of Strongyloides venezuelensis in mice, but not for intestinal IL-4 production. International Journal for Parasitology 36, 1185–1195.CrossRefGoogle Scholar
Porto, A. F., Neva, F. A., Bittencourt, H., Lisboa, W., Thompson, R., Alcântara, L. and Carvalho, E. M. (2001). HTLV-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunology 23, 503–507.CrossRefGoogle ScholarPubMed
Sato, Y. and Toma, H. (1990). Strongyloides venezuelensis infections in mice. International Journal for Parasitology 20, 57–62.CrossRefGoogle ScholarPubMed
Siddiqui, A. A. and Berk, S. L. (2001). Diagnosis of Strongyloides stercoralis infection. Current Treatment Options in Infectious Diseases 33, 1040–1047.Google ScholarPubMed
Siddiqui, A. A. and Berk, S. L. (2003). Strongyloidiasis. Current Treatment Option 5, 283–289.Google Scholar
Takamure, A. (1995). Migration route of Strongyloides venezuelensis in rodents. International Journal for Parasitology 25, 907–911.CrossRefGoogle ScholarPubMed
Talaat, K. R., Bonawitz, R. E., Domenech, P. and Nutman, T. B. (2006). Preexposure to live Brugia malayi microfilariae alters the innate response of human dendritic cells to Mycobacterium tuberculosis. Journal of Infectious Diseases 193, 196–204.CrossRefGoogle ScholarPubMed
Yazdanbakhsh, M., Kremsner, P. G. and Ree, VAN R. (2002). Allergy, parasites, and the hygiene hypothesis. Science 296, 490–494.CrossRefGoogle ScholarPubMed