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      Schistosomiasis Coinfection in Children Influences Acquired Immune Response against Plasmodium falciparum Malaria Antigens

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          Abstract

          Background

          Malaria and schistosomiasis coinfection frequently occurs in tropical countries. This study evaluates the influence of Schistosoma haematobium infection on specific antibody responses and cytokine production to recombinant merozoite surface protein-1-19 (MSP1- 19) and schizont extract of Plasmodium falciparum in malaria-infected children.

          Methodology

          Specific IgG1 to MSP1- 19, as well as IgG1 and IgG3 to schizont extract were significantly increased in coinfected children compared to P. falciparum mono-infected children. Stimulation with MSP1- 19 lead to a specific production of both interleukin-10 (IL-10) and interferon-γ (IFN-γ), whereas the stimulation with schizont extract produced an IL-10 response only in the coinfected group.

          Conclusions

          Our study suggests that schistosomiasis coinfection favours anti-malarial protective antibody responses, which could be associated with the regulation of IL-10 and IFN-γ production and seems to be antigen-dependent. This study demonstrates the importance of infectious status of the population in the evaluation of acquired immunity against malaria and highlights the consequences of a multiple infection environment during clinical trials of anti-malaria vaccine candidates.

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          Most cited references32

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          Human malaria parasites in continuous culture.

          W Trager, Jens-Erik B Jensen, Louise Jensen (1976)
          Plasmodium falciparum can now be maintained in continuous culture in human erythrocytes incubated at 38 degrees C in RPMI 1640 medium with human serum under an atmosphere with 7 percent carbon dioxide and low oxygen (1 or 5 percent). The original parasite material, derived from an infected Aotus trivirgatus monkey, was diluted more than 100 million times by the addition of human erythrocytes at 3- or 4-day intervals. The parasites continued to reproduce in their normal asexual cycle of approximately 48 hours but were no longer highly synchronous. The have remained infective to Aotus.
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            Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10.

            B Lell, Rita C. L. B. Rodrigues, Herman Tilbeurgh … (2000)
            Most of the effort directed at understanding the role infections have in preventing allergy has focused on bacteria and viruses and their ability to divert the immune system towards T-helper-1 responses and away from proallergic T-helper-2 responses. However, helminth infections, highly prevalent in large parts of the developing world, where allergy is uncommon, stimulate strong T-helper-2 responses. We investigated the influence of chronic helminth infections on the prevalence of atopy and aimed to understand the relation at a detailed immunological level. 520 Gabonese schoolchildren were tested for skin reaction to house-dust mite and other allergens, for Schistosoma haematobium eggs in urine, and for microfilariae in blood samples. Total and mite-specific IgE antibodies were measured. A subsample selected on the basis of their skin test to house-dust mite received detailed immunological investigations. Children with urinary schistosomiasis had a lower prevalence of a positive skin reaction to house-dust mite than those free of this infection (odds ratio 0.32 [95% CI 0.16-0.63]). The degree of sensitisation to house-dust mite could not explain this difference in skin-prick positivity. Schistosome-antigen-specific concentrations of interleukin-10 were significantly higher in infected children, and higher specific concentrations of this anti-inflammatory cytokine were negatively associated with the outcome of skin-test reactivity to mite (0.53 [0.30-0.96]). No association between polyclonal IgE antibodies and skin-test results was found. The anti-inflammatory cytokine, interleukin-10, induced in chronic schistosomiasis, appears central to suppressing atopy in African children.
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              Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages

              Hasnaa Bouharoun-Tayoun, Claude Oeuvray, Françoise Lunel … (1995)
              The relevance of the antibody-dependent cellular inhibition (ADCI) of Plasmodium falciparum to clinical protection has been previously established by in vitro studies of material obtained during passive transfer of protection by immunoglobulin G in humans. We here report further in vitro investigations aimed at elucidating the mechanisms underlying this ADCI effect. Results obtained so far suggest that (a) merozoite uptake by monocytes (MN) as well as by polymorphonuclear cells has little influence on the course of parasitemia; (b) the ADCI effect is mediated by a soluble factor released by MN; (c) this or these factors are able to block the division of surrounding intraerythrocytic parasites at the one nucleus stage; (d) the critical triggering antigen(s) targeted by effective Abs would appear to be associated with the surface of merozoites, as opposed to that of infected red blood cells; (e) the MN receptor for Abs effective in ADCI is apparently Fc gamma RII, and not RI; (f) MN function is up- and down- regulated by interferon-gamma and interleukin 4, respectively; and (g) of several potential mediators released by MN, only tumor necrosis factor (TNF) proved of relevance. The involvement of TNF in defense may explain the recently described increased frequency of the TNF-2 high- expression promoter in individuals living in endemic regions despite its compromising role in severe malaria.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2010
                Publication date (Electronic): 15 September 2010
                Volume: 5
                Issue: 9
                Electronic Location Identifier: e12764
                Affiliations
                [1 ]Inserm Unité 547, Institut Pasteur de Lille, Lille, France
                [2 ]ONG ESPOIR Pour La Santé, Laboratoire de Recherches Médicales, B.P. 226, Saint-Louis, Sénégal
                [3 ]Institut de Recherche pour le Développement (IRD) - UR 016 “Caractérisation et Contrôle des Populations de Vecteurs” - BP 64501 - 34394, Montpellier, France
                [4 ]GIMAP, EA3064, Université Jean Monnet, Saint Etienne, France
                Karolinska Institutet, Sweden
                Author notes

                Conceived and designed the experiments: TOD FR NC DDC JPD OG AAN GR. Performed the experiments: TOD FR SP. Analyzed the data: TOD FR LG AMS OG GR. Contributed reagents/materials/analysis tools: TOD FR AMS NC SP. Wrote the paper: TOD FR LG AMS OG AAN GR.

                [¤]

                Current address: Centre IRD, UR 16 Caractérisation et Contrôle des Populations de Vecteurs, Montpellier, France

                Article
                Publisher ID: 10-PONE-RA-16409R1
                DOI: 10.1371/journal.pone.0012764
                PMC ID: 2939900
                PubMed ID: 20856680
                SO-VID: 8320ce3a-5912-41be-8f99-001b7f23d711
                Copyright © Diallo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                Date received : 5 February 2010
                Date accepted : 3 August 2010
                Page count
                Pages: 7
                Categories
                Subject: Research Article
                Subject: Infectious Diseases
                Subject: Immunology/Immune Response
                Subject: Immunology/Immunity to Infections

                ScienceOpen disciplines: Uncategorized
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                ScienceOpen disciplines: Uncategorized

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