Abstract
Schistosoma mansoni infection modulates the immunity to unrelated antigens in the host. In this study, we have investigated the effect of pregnancy and nursing from schistosomotic mother mice on the immune response to ovalbumin (OA), in adult offspring. Then, newborn mice were divided into four groups: animals born from infected mothers (BIM) suckled by non-infected mothers; animals from non-infected mothers suckled by infected mothers (SIM); and two other groups that were mice born and suckled in infected mothers (BSIM) or non-infected (control) mothers. The adult offspring were immunized with OA plus adjuvant. We compared the OA-specific hypersensitivity reactions (HR), antibodies levels (IgG, IgG2a) and the cytokine production in splenocyte cultures. Remarkable interleukin (IL)-10 synthesis was observed in mice BIM; while the anti-OA antibodies levels and immediate HR were impaired. IL-10 neutralization recovered this suppression. Differently, in mice SIM and BSIM there was an enhancement in the anti-OA humoral response and high IL-2 production, however low level of the IL-10 was detected in mice BSIM. In conclusion, schistosomotic pregnancy provides an immunosuppressive potential, IL-10 dependent, which was sustained throughout adult life. Regardless, suckling by infected mothers induces great responsiveness to an unrelated antigen and repairs the inhibitory potential acquired during prenatal stage.
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Actor JK, Marshall MA, Eltoum IA, Buller RM, Berzofsky JA, Sher A (1994) Increased susceptibility of mice infected with Schistosoma mansoni to recombinant vaccinia virus: association of viral persistence with egg granuloma formation. Eur J Immunol 24:3050–3056
Attallah AM, Ghanem GE, Ismail H, El Waseef AM (2003) Placental and oral delivery of Schistosoma mansoni antigen from infected mothers to their newborns and children. Am J Trop Med Hyg 68:647–651
Attallah AM, Abbas AT, Dessouky MI, El-emshaty HM, Elsheikha HM (2006) Susceptibility of neonate mice born to Schistosoma mansoni-infected and noninfected mothers to subsequent S. mansoni infection. Parasitol Res 99:137–145
Barbosa CS, Favre TC, Wanderley TN, Callou AC, Pieri OS (2006) Assessment of schistosomiasis, through school surveys, in the Forest Zone of Pernambuco, Brazil. Mem Inst Oswaldo Cruz 101(suppl I):55–62
Barriga OO (1984) Immunomodulation by nematodes: a review. Vet Parasitol 14:299–320
Barriga OO, Ingalls WL (1984) Potentiation of IgE-like response to Bordetella bronchiseptica in pigs following Ascaris suum infection. Vet Parasitol 16:343–345
Blois SM, Soto CDA, Tometten M, Klapp BF, Margni RA, Arck PC (2004) Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol Reprod 70:1018–1023
Brustoski K, Moüller U, Kramer M, Petelski A, Brenner S, Palmer DR, Bongartz M, Kremsner PG, Luty AJF, Krzych U (2005) IFN-γ and IL-10 mediate parasite-specific immune responses of cord blood cells induced by pregnancy-associated plasmodium falciparum malaria. J Immunol 174:1738–1745
Carvalho CR, Verdolin BA, Vaz NM (1997) Indirect effects of oral tolerance cannot be ascribed to bystander suppression. Scand J Immunol 45:276–281
Ferreira AP, Faquim ES, Abrahamsohn IA, Macedo MS (1995) Immunization with Ascaris suum extract impairs T cell functions in mice. Cell Immunol 162:202–210
Fowler RE, Edwards RG (1957) Induction of superovulation and pregnancy in mature mice by gonadotrophins. J Endocrinol 15:374–384
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD (2007) Schistosomiasis and pregnancy. Trends Parasitol 23:159–164
Hang LM, Boros DL, Warren KS (1974) Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. J Infect Dis 130:515–522
Heikkinen J, Möttönen M, Komi J, Alanen A, Lassila O (2003) Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 131:498–505
Herz U, Joachim R, Ahrens B, Scheffold A, Radbruch A, Henz H (2000) Prenatal sensitization in a mouse model. Am J Respir Crit Care Med 162:S62–S65
Katz N, Chaves A, Pellegrino J (1972) A simple device for quantitative stool thick smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14:397–400
La Flamme AC, Ruddenklau K, Backstrom BT (2003) Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun 71:4996–5004
Leme AS, Hubeau C, Xiang Y, Goldman A, Hamada K, Suzaki Y, Kobzik L (2006) Role of breast milk in a mouse model of maternal transmission of asthma susceptibility. J Immunol 176:762–769
Lenzi JA, Sobral AC, Jr A, Grimaldi FG, Lenzi HL (1987) Congenital and nursing effects on the evolution of Schistosoma mansoni infection in mice. Mem Inst Oswaldo Cruz 82:257–267
Malanchère E, Huetz F, Coutinho A (1997) Maternal IgG stimulates B lineage cell development in the progeny. Eur J Immunol 27:788–793
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
Medeiros M Jr, Figueiredo JP, Almeida MC, Matos MA, Araújo MI, Cruz AA, Atta AM, Rego MA, De Jesus AR, Taketomi EA, Carvalho EM (2003) Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 111:947–951
Noureldin MS, Shaltout AA (1998) Anti-schistosomal IgE and its relation to gastrointestinal allergy in breast-fed infants of Schistosoma mansoni infected mothers. J Egypt Soc Parasitol 28:539–550
Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A (1991) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 173:159–166
Sabin EA, Araújo MI, Carvalho EM, Pearce EJ (1996) Impairment of tetanus toxoid-specific Th1-like immune responses in humans infected with Schistosoma mansoni. J Infect Dis 173:269–272
Sakaguchi S (2003) Regulatory T cells: mediating compromises between host and parasite. Nature Immunol 4:10–11
Smits HH, Hammad H, van Nimwegen M, Soullie T, Willart MA, Lievers E, Kadouch J, Kool M, Kos-van Oosterhoud J, Deelder AM, Lambrecht BN, Yazdanbakhsh M (2007) Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120:932–940
Souza VM, Faquim-Mauro EL, Macedo MS (2002) Extracts of Ascaris suum egg and adult worm share similar immunosuppressive properties. Braz J Med Biol Res 35:81–89
Srivatsa B, Srivatsa S, Johnson KL, Bianchi DW (2003) Maternal cell microchimerism in newborn tissues. J Pediatr 142:31–35
Tanabe M, Gonçalves JF, Gonçalves FJ, Tateno S, Takeuchi T (1997) Occurrence of a community with high morbidity associated with Schistosoma mansoni infection regardless of low infection intensity in north-east Brazil. Trans R Soc Trop Med Hyg 91:144–149
Tasker L, Marshall-Clarke S (1997) Immature B cells from neonatal mice show a selective inability to up-regulate MHC class II expression in response to antigen receptor ligation. Int Immunol 9:475–484
Taylor S, Bryson YJ (1985) Impaired production of γ-interferon by newborn cells in vitro is due to a functionally immature macrophage. J Immunol 134:1493–1497
Taylor JJ, Mohrs M, Pearce EJ (2006) Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J Immunol 176:5839–5847
Thomas PG, Harn DAJ (2004) Immune biasing by helminth glycans. Cell Microbiol 6:13–22
Wan W, Shimizu S, Ikawa H, Sugiyama K, Yamaguchi N (2002) Maternal cell traffic bounds for immune modulation: tracking maternal H-2 alleles in spleens of baby mice by DNA fingerprinting. Immunol 107:261–267
Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85:148–154
Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM (2004) Immunopathogenesis of schistosomiasis. Immunol Rev 201:156–167
Acknowledgements
The authors would like to thank Dr. Carla Lima from the Special Laboratory of Applied Toxinology (CAT/CEPID), Butantan Institute, São Paulo-Brazil for her helpful comments and suggestions. We also thank Maria da Conceição Batista for competent technical assistance. This work was conducted in compliance with Brazilian laws.
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This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and P.E.A. Santos was in receipt of a Master's Fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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Santos, P.d.A., Sales, I.R.F., Schirato, G.V. et al. Influence of maternal schistosomiasis on the immunity of adult offspring mice. Parasitol Res 107, 95–102 (2010). https://doi.org/10.1007/s00436-010-1839-5
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DOI: https://doi.org/10.1007/s00436-010-1839-5