Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation

Clinical and Experimental Immunology

Volumn 160, Issue 2, 2010, Pages 266-274

  Cardoso, L S ^a   Oliveira, S C ^b   Goes A M ^b   Oliveira, R R ^a   Pacifico L G ^b   Marinho, F V ^b   Fonseca, C T ^b   Cardoso, F C ^b   Carvalho, E M ^a,c,d   Araujo, M I ^a,c,d  

^a FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c ESCOLA BAHIANA DE MEDICINA E SAÚDE PÚBLICA   (Brazil)

^d Instituto de Ciências da Saúde   (Brazil)

Author keywords

Allergy; Asthma; Vaccines

Indexed keywords

EOSINOPHIL PEROXIDASE; GAMMA INTERFERON; GLYCOPROTEIN; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; IPSE PROTEIN; OVALBUMIN; PARASITE ANTIGEN; PIII ANTIGEN; SM22.6 ANTIGEN; SM29 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNOGLOBULIN PRODUCTION; IMMUNOMODULATION; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; SCHISTOSOMA MANSONI;

ALVEOLITIS, EXTRINSIC ALLERGIC; ANIMALS; ANTIGENS, HELMINTH; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNIZATION; INTERLEUKINS; LUNG; MICE; MICE, INBRED BALB C; OVALBUMIN; PULMONARY EOSINOPHILIA; SCHISTOSOMA MANSONI; T-LYMPHOCYTE SUBSETS;

EID: 77950633930     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.04084.x     Document Type: Article

References (53)

1. Pearce N, Douwes J, Beasley R. The rise and rise of asthma: a new paradigm for the new millennium? J Epidemiol Biostat 2000 5 : 5 16.
2. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000 161 : 1720 1745.
3. Masoli M, Fabian D, Holt S, Beasley R. The global burden of asthma: executive summary of the GINA dissemination committee report. Allergy 2004 59 : 469 478.
4. Lynch NR, Hagel IA, Palenque ME et al. Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. J Allergy Clin Immunol 1998 101 : 217 221.
5. Hagel I, Lynch NR, Perez M, Di Prisco MC, Lopez R, Rojas E. Modulation of the allergic reactivity of slum children by helminthic infection. Parasite Immunol 1993 15 : 311 315. (Pubitemid 23202083)
6. Araujo MI, Lopes AA, Medeiros M et al. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 2000 123 : 145 148.
7. Cooper PJ, Chico ME, Rodrigues LC et al. Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol 2003 111 : 995 1000.
8. Lynch NR, Hagel I, Perez M, Di Prisco MC, Lopez R, Alvarez N. Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J Allergy Clin Immunol 1993 92 : 404 411. (Pubitemid 24088692)
9. Cooper PJ, Chico ME, Bland M, Griffin GE, Nutman TB. Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med 2003 168 : 313 317.
10. Araujo MI, de Carvalho EM. Human schistosomiasis decreases immune responses to allergens and clinical manifestations of asthma. Chem Immunol Allergy 2006 90 : 29 44.
11. Medeiros M Jr., Figueiredo JP, Almeida MC et al. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 2003 111 : 947 951.
12. Araujo MI, Hoppe B, Medeiros M et al. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 2004 190 : 1797 1803.
13. Araujo MI, de Jesus AR, Bacellar O, Sabin E, Pearce E, Carvalho EM. Evidence of a T helper type 2 activation in human schistosomiasis. Eur J Immunol 1996 26 : 1399 1403.
14. Correa-Oliveira R, Malaquias LC, Falcao PL et al. Cytokines as determinants of resistance and pathology in human Schistosoma mansoni infection. Braz J Med Biol Res 1998 31 : 171 177.
15. Borish L, Aarons A, Rumbyrt J, Cvietusa P, Negri J, Wenzel S. Interleukin-10 regulation in normal subjects and patients with asthma. J Allergy Clin Immunol 1996 97 : 1288 1296.
16. Adachi M, Oda N, Kokubu F, Minoguchi K. IL-10 induces a Th2 cell tolerance in allergic asthma. Int Arch Allergy Immunol 1999 118 : 391 394.
17. Akdis CA, Joss A, Akdis M, Blaser K. Mechanism of IL-10-induced T cell inactivation in allergic inflammation and normal response to allergens. Int Arch Allergy Immunol 2001 124 : 180 182.
18. van den Biggelaar AH, van Ree R, Rodrigues LC et al. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000 356 : 1723 1727.
19. Kitagaki K, Businga TR, Racila D, Elliott DE, Weinstock JV, Kline JN. Intestinal helminths protect in a murine model of asthma. J Immunol 2006 177 : 1628 1635.
20. Akdis CA, Blesken T, Akdis M, Wuthrich B, Blaser K. Role of interleukin 10 in specific immunotherapy. J Clin Invest 1998 102 : 98 106.
21. Akdis CA, Blaser K. [Principles of specific immunotherapy of IgE-induced allergic reactions]. Ther Umsch 2001 58 : 274 277.
22. Elliott DE, Li J, Blum A et al. Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 2003 284 : G385 91.
23. Itami DM, Oshiro TM, Araujo CA et al. Modulation of murine experimental asthma by Ascaris suum components. Clin Exp Allergy 2005 35 : 873 879.
24. Vissers JL, van Esch BC, Hofman GA, Kapsenberg ML, Weller FR, van Oosterhout AJ. Allergen immunotherapy induces a suppressive memory response mediated by IL-10 in a mouse asthma model. J Allergy Clin Immunol 2004 113 : 1204 1210.
25. Oliveira DM, Gustavson S, Silva-Teixeira DN, Goes AM. Nitric oxide and IL-10 production induced by PIII - a fraction of Schistosoma mansoni adult worm antigenic preparation - associated with downregulation of in vitro granuloma formation. Hum Immunol 1999 60 : 305 311.
26. Oliveira DM, Silva-Teixeira DN, Gustavson S, Oliveira SM, Goes AM. Nitric oxide interaction with IL-10, MIP-1alpha, MCP-1 and RANTES over the in vitro granuloma formation against different Schistosoma mansoni antigenic preparations on human schistosomiasis. Parasitology 2000 120 : 391 398.
27. Jeffs SA, Hagan P, Allen R, Correa-Oliveira R, Smithers SR, Simpson AJ. Molecular cloning and characterisation of the 22-kilodalton adult Schistosoma mansoni antigen recognised by antibodies from mice protectively vaccinated with isolated tegumental surface membranes. Mol Biochem Parasitol 1991 46 : 159 167.
28. Pacifico LG, Fonseca CT, Chiari L, Oliveira SC. Immunization with Schistosoma mansoni 22·6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine. Immunobiology 2006 211 : 97 104.
29. Hirsch C, Goes AM. Characterization of fractionated Schistosoma mansoni soluble adult worm antigens that elicit human cell proliferation and granuloma formation in vitro. Parasitology 1996 112 : 529 535.
30. Hirsch C, Zouain CS, Alves JB, Goes AM. Induction of protective immunity and modulation of granulomatous hypersensitivity in mice using PIII, an anionic fraction of Schistosoma mansoni adult worm. Parasitology 1997 115 : 21 8.
31. Cardoso FC, Pacifico RN, Mortara RA, Oliveira SC. Human antibody responses of patients living in endemic areas for schistosomiasis to the tegumental protein Sm29 identified through genomic studies. Clin Exp Immunol 2006 144 : 382 391.
32. Cardoso FC, Macedo GC, Gava E et al. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2008 2 : e308.
33. Cardoso LS, Oliveira SC, Pacifico LG et al. Schistosoma mansoni antigen-driven interleukin-10 production in infected asthmatic individuals. Mem Inst Oswaldo Cruz 2006 101 (Suppl. 1 339 343.
34. Schramm G, Falcone FH, Gronow A et al. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J Biol Chem 2003 278 : 18384 18392.
35. Siddiqui S, Morris J, Avery N, Wyand S, Rood D, Silbart LK. Pulmonary eosinophilia correlates with allergen deposition to the lower respiratory tract in a mouse model of asthma. Clin Exp Allergy 2008 38 : 1381 1390.
36. Mo HM, Lei JH, Jiang ZW et al. Schistosoma japonicum infection modulates the development of allergen-induced airway inflammation in mice. Parasitol Res 2008 103 : 1183 1189.
37. Strath M, Warren DJ, Sanderson CJ. Detection of eosinophils using an eosinophil peroxidase assay. Its use as an assay for eosinophil differentiation factors. J Immunol Meth 1985 83 : 209 215.
38. Pacifico LG, Marinho FA, Fonseca CT et al. Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+CD25+Foxp3+ T cells independent of IL-10. Infect Immun 2009 77 : 98 107.
39. Fallon PG, Dunne DW. Tolerization of mice to Schistosoma mansoni egg antigens causes elevated type 1 and diminished type 2 cytokine responses and increased mortality in acute infection. J Immunol 1999 162 : 4122 4132.
40. Mangan NE, van Rooijen N, McKenzie AN, Fallon PG. Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 2006 176 : 138 147.
41. Gavett SH, Chen X, Finkelman F, Wills-Karp M. Depletion of murine CD4+ T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am J Respir Cell Mol Biol 1994 10 : 587 593.
42. Gleich GJ. The eosinophil and bronchial asthma: current understanding. J Allergy Clin Immunol 1990 85 : 422 436.
43. Gleich GJ, Flavahan NA, Fujisawa T, Vanhoutte PM. The eosinophil as a mediator of damage to respiratory epithelium: a model for bronchial hyperreactivity. J Allergy Clin Immunol 1988 81 : 776 781.
44. Gonzalo JA, Lloyd CM, Wen D et al. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J Exp Med 1998 188 : 157 167.
45. Negrao-Correa D, Silveira MR, Borges CM, Souza DG, Teixeira MM. Changes in pulmonary function and parasite burden in rats infected with Strongyloides venezuelensis concomitant with induction of allergic airway inflammation. Infect Immun 2003 71 : 2607 2614.
46. Epstein MM. Do mouse models of allergic asthma mimic clinical disease? Int Arch Allergy Immunol 2004 133 : 84 100.
47. Whitehead GS, Walker JK, Berman KG, Foster WM, Schwartz DA. Allergen-induced airway disease is mouse strain dependent. Am J Physiol Lung Cell Mol Physiol 2003 285 : L32 42.
48. Takeda K, Haczku A, Lee JJ, Irvin CG, Gelfand EW. Strain dependence of airway hyperresponsiveness reflects differences in eosinophil localization in the lung. Am J Physiol Lung Cell Mol Physiol 2001 281 : L394 402.
49. Brewer JP, Kisselgof AB, Martin TR. Genetic variability in pulmonary physiological, cellular, and antibody responses to antigen in mice. Am J Respir Crit Care Med 1999 160 : 1150 1156.
50. Renz H, Smith HR, Henson JE, Ray BS, Irvin CG, Gelfand EW. Aerosolized antigen exposure without adjuvant causes increased IgE production and increased airway responsiveness in the mouse. J Allergy Clin Immunol 1992 89 : 1127 1138.
51. Wohlleben G, Trujillo C, Muller J et al. Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 2004 16 : 585 596.
52. Trujillo-Vargas CM, Werner-Klein M, Wohlleben G et al. Helminth-derived products inhibit the development of allergic responses in mice. Am J Respir Crit Care Med 2007 175 : 336 344.
53. Stephens R, Randolph DA, Huang G, Holtzman MJ, Chaplin DD. Antigen-nonspecific recruitment of Th2 cells to the lung as a mechanism for viral infection-induced allergic asthma. J Immunol 2002 169 : 5458 5467.