1921
Volume 77, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

and helminth infections coincide geographically and are classically described as TH1 and TH2 pathologies. There is much interest in exploring how concurrent worm infections might alter immune responses to mycobacterial infection. To explore this issue, mice were infected with and co-infected with . Mice infected with had high numbers of neutrophils and mononuclear cells within the alveolar spaces, with increased parenchymal interferon (IFN)-γ levels. However, in -infected mice we detected increased eosinophil numbers in bronchoalveolar lavage fluid (BALF) and increased parenchymal levels of interleukin (IL)-5. In co-infected mice the BALF demonstrated enhanced eosinophil influx with decreased neutrophil and mononuclear cell accumulation. However, co-infected mice had similar mycobacterial proliferation in their lungs accompanied by similar histopathological changes and similar cytokine/nitric oxide production compared with -only–infected mice. Our results suggest that infection does not necessarily lead to increased susceptibility to pulmonary tuberculosis.

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References

  1. Colley DG, LoVerde PT, Savioli L, 2001. Infectious disease. Medical helminthology in the 21st century. Science 293 : 1437–1438. [Google Scholar]
  2. Loukas A, Constant SL, Bethony JM, 2005. Immunobiology of hookworm infection. FEMS Immunol Med Microbiol 43 : 115–124. [Google Scholar]
  3. Maizels RM, Yazdanbakhsh M, 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3 : 733–744. [Google Scholar]
  4. Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, Berzofsky JA, 1993. Helminth infection results in decreased virus-specific CD8-cytotoxic T-cell and TH1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci USA 90 : 948–952. [Google Scholar]
  5. Araujo MI, Bliss SK, Suzuki Y, Alcaraz A, Denkers EY, Pearce EJ, 2001. Interleukin-12 promotes pathologic liver changes and death in mice coinfected with Schistosoma mansoni and Toxoplasma gondii. Infect Immun 69 : 1454–1462. [Google Scholar]
  6. Mansfield LS, Gauthier DT, Abner SR, Jones KM, Wilder SR, Urban JF Jr, 2003. Enhancement of disease and pathology by synergy of Trichuris suis and Campylobacter jejuni in the colon of immunologically naïve swine. Am J Trop Med Hyg 68 : 70–80. [Google Scholar]
  7. Chen CC, Louie S, McCormick B, Walker WA, Shi HN, 2005. Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infect Immun 73 : 5468–5481. [Google Scholar]
  8. Elias D, Akuffo H, Thors C, Pawlowski A, Britton S, 2005a. Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol 139 : 398–404. [Google Scholar]
  9. Rook GA, Dheda K, Zumla A, 2006. Immune systems in developed and developing countries; implications for the design of vaccines that will work where BCG does not. Tuberculosis (Edinb) 86 : 152–162. [Google Scholar]
  10. Figueiredo SD, Taddei JA, Menezes JJ, Novo NF, Silva EO, Cristovao HL, Cury MC, 2005. Clinical-epidemiological study of toxocariasis in a pediatric population. J Pediatr 81 : 126–132. [Google Scholar]
  11. Pinelli E, Brandes S, Dormans J, Fonville M, Hamilton CM, der Giessen JV, 2006. Toxocara canis: effect of inoculum size on pulmonary pathology and cytokine expression in BALB/c mice. Exp Parasitol 115 : 76–82. [Google Scholar]
  12. Olson LJ, Schulz CW, 1963. Nematode induced hypersensibility reactions in guinea pig: onset of eosinophilia and positive Schultz–Dale reactions following graded infection with Toxocara canis. Ann NY Acad Sci 113 : 440–455. [Google Scholar]
  13. Faccioli LH, Mokwa VF, Silva CL, Rocha GM, Araujo JI, Nahori MA, Vargaftig BB, 1996. IL-5 drives eosinophils from bone marrow to blood and tissues in a guinea-pigs model of visceral larva migrans syndrome. Med Inflamm 5 : 24–31. [Google Scholar]
  14. Bonato VL, Goncalves ED, Soares EG, Santos Junior RR, Sartori A, Coelho-Castelo AA, Silva CL, 2004. Immune regulatory effect of pHSP65 DNA therapy in pulmonary tuberculosis: activation of CD8+ cells, interferon-γ recovery and reduction of lung injury. Immunology 113 : 130–138. [Google Scholar]
  15. Rogerio AP, Sa-Nunes A, Albuquerque DA, Anibal FF, Medeiros AI, Machado ER, Souza AO, Prado JC Jr, Faccioli LH, 2003. Lafoensia pacari extract inhibits IL-5 production in toxocariasis. Parasite Immunol 25 : 393–400. [Google Scholar]
  16. Faccioli LH, Souza GE, Cunha FQ, Poole S, Ferreira SH, 1990. Recombinant interleukin-1 and tumor necrosis factor induce neutrophil migration “in vivo” by indirect mechanisms. Agents Actions 30 : 344–349. [Google Scholar]
  17. Lowrie DB, Tascon RE, Bonato VL, Lima VM, Faccioli LH, Stavropoulos E, Colston MJ, Hewinson RG, Moelling K, Silva CL, 1999. Therapy of tuberculosis in mice by DNA vaccination. Nature 400 : 269–271. [Google Scholar]
  18. Stuehr DJ, Gross SS, Sakuma I, Levi R, Nathan CF, 1989. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J Exp Med 169 : 1011–1020. [Google Scholar]
  19. Carlos D, Sa-Nunes A, de Paula L, Matias-Peres C, Jamur MC, Oliver C, Serra MF, Martins MA, Faccioli LH, 2006. Histamine modulates mast cell degranulation through an indirect mechanism in a model IgE-mediated reaction. Eur J Immunol 36 : 1494–1503. [Google Scholar]
  20. Fan CK, Liao CW, Kao TC, Li MH, Du WY, Su KE, 2005. Sero-epidemiology of Toxocara canis infection among aboriginal schoolchildren in the mountainous areas of north-eastern Taiwan. Ann Trop Med Parasitol 99 : 593–600. [Google Scholar]
  21. Traub RJ, Robertson ID, Irwin PJ, Mencke N, Thompson RC, 2005. Canine gastrointestinal parasitic zoonoses in India. Trends Parasitol 21 : 42–48. [Google Scholar]
  22. Virginia P, Nagakura K, Ferreira O, Tateno S, 1991. Serologic evidence of toxocariasis in northeast Brazil. Jpn J Med Sci Biol 44 : 1–6. [Google Scholar]
  23. Iwanaga Y, Goncalves JF, Tanabe M, Tateno S, Tsuji M, Takeuchi T, 1993. Sero-epidemiological study on human toxocariasis in the rural sector around Recife, northeast Brazil. Jpn J Trop Med Hyg 21 : 255–258. [Google Scholar]
  24. World Health Organization, 2006. Global Tuberculosis Control: Surveillance, Planning, Financing. WHO Report. Geneva: World Health Organization.
  25. Medina E, North RJ, 1998. Resistance ranking of some common inbred mouse strains to Mycobacterium tuberculosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype. Immunology 93 : 270–274. [Google Scholar]
  26. Medina E, North RJ, 1999. Genetically susceptible mice remain proportionally more susceptible to tuberculosis after vaccination. Immunology 96 : 16–21. [Google Scholar]
  27. Hsieh CS, Macatonia SE, O’Garra A, Murphy KM, 1995. T cell genetic background determines default T helper phenotype development in vitro. J Exp Med 181 : 713–721. [Google Scholar]
  28. Peres CM, de Paula L, Medeiros AI, Sorgi CA, Soares EG, Carlos D, Peters-Golden M, Silva CL, Faccioli LH, 2007. Inhibition of leukotriene biosynthesis abrogates the host control of Mycobacterium tuberculosis. Microbes Infect 9 : 483–489. [Google Scholar]
  29. Erb KJ, Trujillo C, Fugate M, Moll H, 2002. Infection with the helminth Nippostrongylus brasiliensis does not interfere with efficient elimination of Mycobacterium bovis BCG from the lungs of mice. Clin Diagn Lab Immunol 9 : 727–730. [Google Scholar]
  30. Elias D, Wolday D, Akuffo H, Petros B, Bronner U, Britton S, 2001. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guérin (BCG) vaccination. Clin Exp Immunol 123 : 219–225. [Google Scholar]
  31. Lima VM, Bonato VL, Lima KM, Dos Santos SA, Dos Santos RR, Goncalves ED, Faccioli LH, Brandao IT, Rodrigues-Junior JM, Silva CL, 2001. Role of trehalose dimycolate in recruitment of cells and modulation of production of cytokines and NO in tuberculosis. Infect Immun 69 : 5305–5312. [Google Scholar]
  32. Kaufmann SH, 2001. How can immunology contribute to the control of tuberculosis? Nat Rev Immunol 1 : 20–30. [Google Scholar]
  33. Cooper AM, Magram J, Ferrante J, Orme IM, 1997. Interleukin-12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with Mycobacterium tuberculosis. J Exp Med 186 : 39–45. [Google Scholar]
  34. Silva CL, Bonato VLD, Lima KM, Coelho-Castelo AAM, Faccioli LH, Sartori A, de Souza AO, Leão SC, 2001. Cytotoxic T cells and mycobacteria. FEMS Microbiol Lett 197 : 11–18. [Google Scholar]
  35. Salgame P, 2005. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol 17 : 374–380. [Google Scholar]
  36. Flynn JL, Chan J, 2001. Immunology of tuberculosis. Annu Rev Immun 19 : 93–129. [Google Scholar]
  37. Kawakami K, Kinjo Y, Uezu K, Miyagi K, Kinjo T, Yara S, Koguchi Y, Miyazato A, Shibuya K, Iwakura Y, Takeda K, Akira S, Saito A, 2004. Interferon-γ production and host protective response against Mycobacterium tuberculosis in mice lacking both IL-12p40 and IL-18. Microbes Infect 6 : 339–349. [Google Scholar]
  38. Franke-Ullmann G, Pfortner C, Walter P, Steinmuller C, Lohmann-Matthes ML, Kobzik L, 1996. Characterization of murine lung interstitial macrophages in comparison with alveolar macrophages in vitro. J Immunol 157 : 3097–3104. [Google Scholar]
  39. Delbridge LM, O’Riordan MX, 2007. Innate recognition of intracellular bacteria. Curr Opin Immunol 19 : 10–16. [Google Scholar]
  40. Briken V, Porcelli SA, Besra GS, Kremer L, 2004. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol Microbiol 53 : 391–403. [Google Scholar]
  41. van Die I, Cummings RD, 2006. Glycans modulate immune responses in helminth infections and allergy. Chem Immunol Allergy 90 : 91–112. [Google Scholar]
  42. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A, 1991. Down-regulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 173 : 159–166. [Google Scholar]
  43. Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma JH, Kazura JW, King CL, 1999. Helminth- and Bacillus Calmette-Guérin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162 : 6843–6848. [Google Scholar]
  44. Kullberg MC, Pearce EJ, Hieny SE, Sher A, Berzofsky JA, 1992. Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J Immunol 148 : 3264–3270. [Google Scholar]
  45. Elias D, Akuffo H, Pawlowski A, Haile M, Schon T, Britton S, 2005b. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine 23 : 1326–1334. [Google Scholar]
  46. Elias D, Akuffo H, Britton S, 2006a. Helminths could influence the outcome of vaccines against TB in the tropics. Parasite Immunol 28 : 507–513. [Google Scholar]
  47. Elias D, Mengistu G, Akuffo H, Britton S, 2006b. Are intestinal helminths risk factors for developing active tuberculosis? Trop Med Int Health 11 : 551–558. [Google Scholar]
  48. Kullberg MC, Jankovic D, Gorelick PL, Caspar P, Letterio JJ, Cheever AW, Sher A, 2002. Bacteria triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J Exp Med 196 : 505–515. [Google Scholar]
  49. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE, 2004. Helminth parasites—masters of regulation. Immunol Rev 201 : 89–116. [Google Scholar]
  50. Oldenhove G, de Heusch M, Urbain-Vansanten G, Urbain J, Maliszewski C, Leo O, Moser M, 2003. CD4+CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J Exp Med 198 : 259–266. [Google Scholar]
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  • Received : 19 Jan 2007
  • Accepted : 22 May 2007

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