Skip to main content

Advertisement

Log in

Schistosoma japonicum infection modulates the development of allergen-induced airway inflammation in mice

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Asthma, a chronic inflammatory disorder of the airways, is coordinated by Th2 cells in both human asthmatics and animal models of allergic asthma. It has been shown that helminth infections including Schistosoma mansoni may modulate atopic diseases including asthma. In the present study, BALB/c mice were infected with bisexual and unisexual (male) S. japonicum, respectively, prior to ovalbumin (OVA) sensitization and challenge. Compared to mice with OVA sensitization/challenge alone, S. japonicum infection led to a significant decrease of eosinophil accumulation in bronchoalveolar lavage fluid (BALF) collected 48 h postchallenge, as well as to a marked reduction in inflammatory cell infiltration around the airways and pulmonary blood vessels. Compared to OVA-immunized uninfected mice, the level of OVA-specific serum IgE as well as interleukin (IL)-4 and IL-5 in BALF were reduced, but IL-10 was strongly elevated in mice with preexisting S. japonicum infection prior to OVA immunization. These results suggest that both bisexual and male S. japonicum infections may modulate the development of allergic asthma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Araújo MI, Hoppe BS, Medeiros M Jr (2004a) Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 190:1797–1803

    Article  PubMed  Google Scholar 

  • Araújo MI, Hoppe BS, Manoel M Jr, Edgar MC (2004b) Schistosoma mansoni infection modulates the immune response against allergic and auto-immune diseases. Mem Inst Oswaldo Cruz 99:27–32

    PubMed  Google Scholar 

  • Baxter AG, Healey D, Cooke A (1994) Mycobacteria precipitate auto-immune rheumatic disease in NOD mice via an adjuvant-like activity. Scand J Immunol 39:602–606

    Article  PubMed  CAS  Google Scholar 

  • Chung CD, Kuo F, Kumer J, Motani AS, Lawrence CE, Henderson WR Jr, Venkataraman C (2003) CCR8 is not essential for the development of inflammation in a mouse model of allergic airway disease. J Immunol 170:581–587

    PubMed  CAS  Google Scholar 

  • Corrigan CJ, Kay AB (1996) T-cell/eosinophil interactions in the induction of asthma. Eur Respir J Suppl 22:72s–8s

    PubMed  CAS  Google Scholar 

  • Deborah NC, Micheline RS, Cynthia MB, Danielle GS, Mauro MT (2003) Changes in pulmonary function and parasite burden in rats infected with Strongyloides enezuelensis concomitant with induction of allergic airway inflammation. Infect Immun 71:2607–2614

    Article  CAS  Google Scholar 

  • Dittrich AM, Erbacher A, Specht S, Diesner F, Krokowski M, Avagyan A, Stock P, Ahrens B, Hoffmann WH, Hoerauf A, Hamelmann E (2008) Helminth infection with Litomosoides sigmodontis induces regulatory T cells and inhibits allergic sensitization, airway inflammation, and hyperreactivity in a murine asthma model. J Immunol 180:1792–1799

    PubMed  CAS  Google Scholar 

  • de Vries JE, Carballido JM, Aversa G (1999) Receptors and cytokines involved in allergic TH2 cell responses. J Allergy Clin Immunol 103:S492–496

    Article  PubMed  Google Scholar 

  • Eduardo VP, Jose AR, Alvaro AC (2007) Interrelationship among asthma, atopy, and helminth infections. J Bras Pneumol 33:335–342

    Google Scholar 

  • Gale EA (2002) A missing link in the hygiene hypothesis? Diabetologia 45:588–594

    Article  PubMed  CAS  Google Scholar 

  • Grunig G, Corry DB, Leach MW (1997) Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J Exp Med 185:1089–1099

    Article  PubMed  CAS  Google Scholar 

  • Grzych JM, Pearce E, Cheever A (1991) Egg deposition is the major stimulus for the production of Th2 cytokines in murine Schistosomiasis mansoni. J Immunol 146:1332–1327

    Google Scholar 

  • Hopfenspirger MT, Agrawal DK (2002) Airway hyperresponsiveness, late allergic response, and eosinophilia are reversed with mycobacterial antigens in ovalbumin presensitized mice. J Immunol 168:2516–2522

    PubMed  CAS  Google Scholar 

  • Humbert M, Corrigan CJ, Kimmitt (1997) Relationship between IL-4 and IL-5 mRNA expression and disease severity in atopic asthma. Am J Respir Crit Care Med 156:704–708

    PubMed  CAS  Google Scholar 

  • Kay AB, Ying S, Durham SR (1995) Phenotype of cells positive for interleukin-4 and interleukin-5 mRNA in allergic tissue reactions. Int Arch Allergy Immunol 107:208–10

    Article  PubMed  CAS  Google Scholar 

  • Mangan NE, van Rooijen N, McKenzie AN, Fallon PG (2006) Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 176:138–147

    PubMed  CAS  Google Scholar 

  • McKee AS, Pearce EJ (2004) CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J Immunol 173:1224–1231

    PubMed  CAS  Google Scholar 

  • Mo HM, Liu WQ, Lei JH, Cheng YL, Wang CZ, Li YL (2007) Schistosoma japonicum eggs modulate the activity of CD4+CD25+ Tregs and prevent development of colitis in mice. Exp Parasitol 116:385–389

    Article  PubMed  CAS  Google Scholar 

  • Moore KW, Waal MR, Coffman RL (2001) Interleukin-10 and the interleukin-10 receptor. Ann Rev Immunol 19:683–765

    Article  CAS  Google Scholar 

  • Naura AS, Hans CP, Zerfaoui M, You D, Cormier SA, Oumouna M, Boulares AH (2008) Post-allergen challenge inhibition of poly(ADP-ribose) polymerase harbors therapeutic potential for treatment of allergic airway inflammation. Clin Exp Allergy 38:839–846

    Article  PubMed  CAS  Google Scholar 

  • Okano M, Satoskar AR, Nishizaki K, Harn DA Jr (2001) Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J Immunol 167:442–50

    PubMed  CAS  Google Scholar 

  • Roberts M, Butterworth AE, Kimani G (1993) Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect Immun 61:4984–4993

    PubMed  CAS  Google Scholar 

  • Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259–1260

    PubMed  CAS  Google Scholar 

  • Tavernier J, Plaetinck G, Guisez Y (1996) The role of interleukin-5 in the production and function of eosinophils. In: Whetton AD, Gordon J (eds) Cell biochemistry, vol. 7. Hematopoietic cell growth factors and their receptors. Plenum, New York, pp 321–361

    Google Scholar 

  • Taylor MD, LeGoff L, Harris A, Malone E, Allen JE, Maizels RM (2005) Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol 174:4924–4933

    PubMed  CAS  Google Scholar 

  • Terrazas LI, Walsh KL, Piskorska D, McGuire E, Harn DA Jr (2001) The schistosome oligosaccharide lacto-N-neotetraose expands Gr1(+) cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4(+) cells: a potential mechanism for immune polarization in helminth infections. J Immunol 167:5294–5303

    PubMed  CAS  Google Scholar 

  • Walker JK, Fong AM, Lawson BL, Savov JD, Patel DD, Schwartz DA, Lefkowitz RJ (2003) Beta-arrestin-2 regulates the development of allergic asthma. J Clin Invest 112:566–574

    PubMed  CAS  Google Scholar 

  • Wang CC, Nolan TJ, Schad GA, Abraham D (2001) Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic response to ovalbumin. Clin Exp Allergy 31:495–503

    Article  PubMed  CAS  Google Scholar 

  • Wohlleben G, Trujillo C, Muller J (2004) Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 16:585–596

    Article  PubMed  CAS  Google Scholar 

  • Wynn TA, Morawetz R, Scharton-Kersten T (1997) Analysis of granuloma formation in double cytokine-deficient mice reveals a central role for IL-10 in polarizing both T helper cell 1- and T helper cell 2-type cytokine responses in vivo. J Immunol 159:5014–5023

    PubMed  CAS  Google Scholar 

  • Yang JH, Zhao JQ, Yang YF, Zhang L, Yang X, Zhu X, Ji MJ, Sun NX, Su C (2006) Schistosoma japonicum egg antigens stimulate CD4+CD25+ T cells and modulate airway inflammation in a murine model of asthma. Immunology 120:8–18

    PubMed  Google Scholar 

  • Yazdanbakhsh M, Matricardi PM (2004) Parasites and the hygiene hypothesis: regulating the immune system? Clin Rev Allergy Immunol 26:15–24

    Article  PubMed  CAS  Google Scholar 

  • Yazdanbakhsh M, Matricardi PM, van Ree R (2002) Allergy, parasites, and the hygiene hypothesis. Science 296:490–494

    Article  PubMed  CAS  Google Scholar 

  • Zosky GR, Larcombe AN, White OJ, Burchell JT, Janosi TZ, Hantos Z, Holt PG, Sly PD, Turner DJ (2007) Ovalbumin-sensitized mice are good models for airway hyperresponsiveness but not acute physiological responses to allergen inhalation. Clin Exp Allergy 38:829–838

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful for the valuable discussion and critical revision of Prof. Andreas Ruppel from Heidelberg University, Heidelberg, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wen-qi Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mo, Hm., Lei, Jh., Jiang, Zw. et al. Schistosoma japonicum infection modulates the development of allergen-induced airway inflammation in mice. Parasitol Res 103, 1183–1189 (2008). https://doi.org/10.1007/s00436-008-1114-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-008-1114-1

Keywords

Navigation