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Published in: Malaria Journal 1/2009

Open Access 01-12-2009 | Research

Human IgG response to a salivary peptide, gSG6-P1, as a new immuno-epidemiological tool for evaluating low-level exposure to Anopheles bites

Authors: Anne Poinsignon, Sylvie Cornelie, Fatou Ba, Denis Boulanger, Cheikh Sow, Marie Rossignol, Cheikh Sokhna, Badara Cisse, François Simondon, Franck Remoue

Published in: Malaria Journal | Issue 1/2009

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Abstract

Background

Human populations exposed to low malaria transmission present particular severe risks of malaria morbidity and mortality. In addition, in a context of low-level exposure to Anopheles vector, conventional entomological methods used for sampling Anopheles populations are insufficiently sensitive and probably under-estimate the real risk of malaria transmission. The evaluation of antibody (Ab) responses to arthropod salivary proteins constitutes a novel tool for estimating exposure level to insect bites. In the case of malaria, a recent study has shown that human IgG responses to the gSG6-P1 peptide represented a specific biomarker of exposure to Anopheles gambiae bites. The objective of this study was to investigate if this biomarker can be used to estimate low-level exposure of individuals to Anopheles vector.

Methods

The IgG Ab level to gSG6-P1 was evaluated at the peak and at the end of the An. gambiae exposure season in children living in Senegalese villages, where the Anophele s density was estimated to be very low by classical entomological trapping but where malaria transmission occurred during the studied season.

Results

Specific IgG responses to gSG6-P1 were observed in children exposed to very low-level of Anopheles bites. In addition, a significant increase in the specific IgG Ab level was observed during the Anopheles exposure season whereas classical entomological data have reported very few or no Anopheles during the studied period. Furthermore, this biomarker may also be applicable to evaluate the heterogeneity of individual exposure.

Conclusion

The results strengthen the hypothesis that the evaluation of IgG responses to gSG6-P1 during the season of exposure could reflect the real human contact with anthropophilic Anopheles and suggest that this biomarker of low exposure could be used at the individual level. This promising immuno-epidemiological marker could represent a useful tool to assess the risk to very low exposure to malaria vectors as observed in seasonal, urban, altitude or travellers contexts. In addition, this biomarker could be used for the surveillance survey after applying anti-vector strategy.
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Literature
1.
go back to reference WHO: Weekly epidemiological record. 1996, 71 (3): 17-22. WHO: Weekly epidemiological record. 1996, 71 (3): 17-22.
2.
go back to reference Baudon D, Louis FJ, Martet G: In Africa, urban malaria is the malaria of tomorrow. Med Trop. 1996, 56 (4): 323-325. Baudon D, Louis FJ, Martet G: In Africa, urban malaria is the malaria of tomorrow. Med Trop. 1996, 56 (4): 323-325.
3.
go back to reference Remoue F, Cornelie S, NGom A, Boulanger D, Simondon F: Immune responses to arthropod bites during vector-borne diseases. Update in tropical immunology. Edited by: Garraud O. 2005, Fort P.O. Trivandrum, Herala, India: Transworld research Network, 377-400. Remoue F, Cornelie S, NGom A, Boulanger D, Simondon F: Immune responses to arthropod bites during vector-borne diseases. Update in tropical immunology. Edited by: Garraud O. 2005, Fort P.O. Trivandrum, Herala, India: Transworld research Network, 377-400.
4.
go back to reference Billingsley PF, Baird J, Mitchell JA, Drakeley C: Immune interactions between mosquitoes and their hosts. Parasite Immunol. 2006, 28 (4): 143-153.CrossRefPubMed Billingsley PF, Baird J, Mitchell JA, Drakeley C: Immune interactions between mosquitoes and their hosts. Parasite Immunol. 2006, 28 (4): 143-153.CrossRefPubMed
5.
go back to reference Ribeiro JM: Blood-feeding arthropods: live syringes or invertebrate pharmacologists?. Infect Agents Dis. 1995, 4 (3): 143-152.PubMed Ribeiro JM: Blood-feeding arthropods: live syringes or invertebrate pharmacologists?. Infect Agents Dis. 1995, 4 (3): 143-152.PubMed
6.
go back to reference Champagne DE: Antihemostatic strategies of blood-feeding arthropods. Curr Drug Targets Cardiovasc Haematol Disord. 2004, 4 (4): 375-396. 10.2174/1568006043335862.CrossRefPubMed Champagne DE: Antihemostatic strategies of blood-feeding arthropods. Curr Drug Targets Cardiovasc Haematol Disord. 2004, 4 (4): 375-396. 10.2174/1568006043335862.CrossRefPubMed
7.
go back to reference Penneys NS, Nayar JK, Bernstein H, Knight JW, Leonardi C: Mosquito salivary gland antigens identified by circulating human antibodies. Arch Dermatol. 1989, 125 (2): 219-222. 10.1001/archderm.125.2.219.CrossRefPubMed Penneys NS, Nayar JK, Bernstein H, Knight JW, Leonardi C: Mosquito salivary gland antigens identified by circulating human antibodies. Arch Dermatol. 1989, 125 (2): 219-222. 10.1001/archderm.125.2.219.CrossRefPubMed
8.
go back to reference Brummer-Korvenkontio H, Palosuo T, Francois G, Reunala T: Characterization of Aedes communis, Aedes aegypti and Anopheles stephensi mosquito saliva antigens by immunoblotting. Int Arch Allergy Immunol. 1997, 112 (2): 169-174.CrossRefPubMed Brummer-Korvenkontio H, Palosuo T, Francois G, Reunala T: Characterization of Aedes communis, Aedes aegypti and Anopheles stephensi mosquito saliva antigens by immunoblotting. Int Arch Allergy Immunol. 1997, 112 (2): 169-174.CrossRefPubMed
9.
go back to reference Lane RS, Moss RB, Hsu YP, Wei T, Mesirow ML, Kuo MM: Anti-arthropod saliva antibodies among residents of a community at high risk for Lyme disease in California. Am J Trop Med Hyg. 1999, 61 (5): 850-859.PubMed Lane RS, Moss RB, Hsu YP, Wei T, Mesirow ML, Kuo MM: Anti-arthropod saliva antibodies among residents of a community at high risk for Lyme disease in California. Am J Trop Med Hyg. 1999, 61 (5): 850-859.PubMed
10.
go back to reference Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, Valenzuela JG, Charlab R, Barral-Netto M, Ribeiro JM: Human immune response to sand fly salivary gland antigens: a useful epidemiological marker?. Am J Trop Med Hyg. 2000, 62 (6): 740-745.PubMed Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, Valenzuela JG, Charlab R, Barral-Netto M, Ribeiro JM: Human immune response to sand fly salivary gland antigens: a useful epidemiological marker?. Am J Trop Med Hyg. 2000, 62 (6): 740-745.PubMed
11.
go back to reference Nascimento RJ, Santana JM, Lozzi SP, Araujo CN, Teixeira AR: Human IgG1 and IgG4: the main antibodies against Triatoma infestans (Hemiptera: Reduviidae) salivary gland proteins. Am J Trop Med Hyg. 2001, 65 (3): 219-226.PubMed Nascimento RJ, Santana JM, Lozzi SP, Araujo CN, Teixeira AR: Human IgG1 and IgG4: the main antibodies against Triatoma infestans (Hemiptera: Reduviidae) salivary gland proteins. Am J Trop Med Hyg. 2001, 65 (3): 219-226.PubMed
12.
go back to reference Poinsignon A, Remoue F, Rossignol M, Cornelie S, Courtin D, Grebaut P, Garcia A, Simondon F: Human IgG antibody response to Glossina saliva: an epidemiologic marker of exposure to Glossina bites. Am J Trop Med Hyg. 2008, 78 (5): 750-753.PubMed Poinsignon A, Remoue F, Rossignol M, Cornelie S, Courtin D, Grebaut P, Garcia A, Simondon F: Human IgG antibody response to Glossina saliva: an epidemiologic marker of exposure to Glossina bites. Am J Trop Med Hyg. 2008, 78 (5): 750-753.PubMed
13.
go back to reference Palosuo K, Brummer-Korvenkontio H, Mikkola J, Sahi T, Reunala T: Seasonal increase in human IgE and IgG4 antisaliva antibodies to Aedes mosquito bites. Int Arch Allergy Immunol. 1997, 114 (4): 367-372.CrossRefPubMed Palosuo K, Brummer-Korvenkontio H, Mikkola J, Sahi T, Reunala T: Seasonal increase in human IgE and IgG4 antisaliva antibodies to Aedes mosquito bites. Int Arch Allergy Immunol. 1997, 114 (4): 367-372.CrossRefPubMed
14.
go back to reference Remoue F, Alix E, Cornelie S, Sokhna C, Cisse B, Doucoure S, Mouchet F, Boulanger D, Simondon F: IgE and IgG4 antibody responses to Aedes saliva in African children. Acta Trop. 2007, 104 (2-3): 108-115. 10.1016/j.actatropica.2007.07.011.CrossRefPubMed Remoue F, Alix E, Cornelie S, Sokhna C, Cisse B, Doucoure S, Mouchet F, Boulanger D, Simondon F: IgE and IgG4 antibody responses to Aedes saliva in African children. Acta Trop. 2007, 104 (2-3): 108-115. 10.1016/j.actatropica.2007.07.011.CrossRefPubMed
15.
go back to reference Remoue F, Cisse B, Ba F, Sokhna C, Herve J-P, Boulanger D, Simondon F: Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Trans R Soc Trop Med Hyg. 2006, 100 (4): 363-370. 10.1016/j.trstmh.2005.06.032.CrossRefPubMed Remoue F, Cisse B, Ba F, Sokhna C, Herve J-P, Boulanger D, Simondon F: Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Trans R Soc Trop Med Hyg. 2006, 100 (4): 363-370. 10.1016/j.trstmh.2005.06.032.CrossRefPubMed
16.
go back to reference Waitayakul A, Somsri S, Sattabongkot J, Looareesuwan S, Cui L, Udomsangpetch R: Natural human humoral response to salivary gland proteins of Anopheles mosquitoes in Thailand. Acta Trop. 2006, 98 (1): 66-73. 10.1016/j.actatropica.2006.02.004.CrossRefPubMed Waitayakul A, Somsri S, Sattabongkot J, Looareesuwan S, Cui L, Udomsangpetch R: Natural human humoral response to salivary gland proteins of Anopheles mosquitoes in Thailand. Acta Trop. 2006, 98 (1): 66-73. 10.1016/j.actatropica.2006.02.004.CrossRefPubMed
17.
go back to reference Valenzuela JG, Francischetti IM, Pham VM, Garfield MK, Ribeiro JM: Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol. 2003, 33 (7): 717-732. 10.1016/S0965-1748(03)00067-5.CrossRefPubMed Valenzuela JG, Francischetti IM, Pham VM, Garfield MK, Ribeiro JM: Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol. 2003, 33 (7): 717-732. 10.1016/S0965-1748(03)00067-5.CrossRefPubMed
18.
go back to reference Lombardo F, Ronca R, Rizzo C, Mestres-Simon M, Lanfrancotti A, Curra C, Fiorentino G, Bourgouin C, Ribeiro JM, Petrarca V: The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem Mol Biol. 2009, 39 (7): 457-466. 10.1016/j.ibmb.2009.04.006.PubMedCentralCrossRefPubMed Lombardo F, Ronca R, Rizzo C, Mestres-Simon M, Lanfrancotti A, Curra C, Fiorentino G, Bourgouin C, Ribeiro JM, Petrarca V: The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem Mol Biol. 2009, 39 (7): 457-466. 10.1016/j.ibmb.2009.04.006.PubMedCentralCrossRefPubMed
19.
go back to reference Orlandi-Pradines E, Almeras L, Denis de Senneville L, Barbe S, Remoue F, Villard C, Cornelie S, Penhoat K, Pascual A, Bourgouin C: Antibody response against saliva antigens of Anopheles gambiae and Aedes aegypti in travellers in tropical Africa. Microbes Infect. 2007, 9 (12-13): 1454-1462. 10.1016/j.micinf.2007.07.012.CrossRefPubMed Orlandi-Pradines E, Almeras L, Denis de Senneville L, Barbe S, Remoue F, Villard C, Cornelie S, Penhoat K, Pascual A, Bourgouin C: Antibody response against saliva antigens of Anopheles gambiae and Aedes aegypti in travellers in tropical Africa. Microbes Infect. 2007, 9 (12-13): 1454-1462. 10.1016/j.micinf.2007.07.012.CrossRefPubMed
20.
go back to reference Poinsignon A, Cornelie S, Mestres-Simon M, Lanfrancotti A, Rossignol M, Boulanger D, Cisse B, Sokhna C, Arca B, Simondon F: Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS ONE. 2008, 3 (6): e2472-10.1371/journal.pone.0002472.PubMedCentralCrossRefPubMed Poinsignon A, Cornelie S, Mestres-Simon M, Lanfrancotti A, Rossignol M, Boulanger D, Cisse B, Sokhna C, Arca B, Simondon F: Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS ONE. 2008, 3 (6): e2472-10.1371/journal.pone.0002472.PubMedCentralCrossRefPubMed
21.
go back to reference Robert V, Dieng H, Lochouran L, Traore SF, Trape JF, Simondon F, Fontenille D: Malaria transmission in the rural zone of Niakhar, Senegal. Trop Med Int Health. 1998, 3 (8): 667-677. 10.1046/j.1365-3156.1998.00288.x.CrossRefPubMed Robert V, Dieng H, Lochouran L, Traore SF, Trape JF, Simondon F, Fontenille D: Malaria transmission in the rural zone of Niakhar, Senegal. Trop Med Int Health. 1998, 3 (8): 667-677. 10.1046/j.1365-3156.1998.00288.x.CrossRefPubMed
22.
go back to reference Cisse B, Sokhna C, Boulanger D, Milet J, Ba el H, Richardson K, Hallett R, Sutherland C, Simondon K, Simondon F: Seasonal intermittent preventive treatment with artesunate and sulfadoxine-pyrimethamine for prevention of malaria in Senegalese children: a randomised, placebo-controlled, double-blind trial. Lancet. 2006, 367 (9511): 659-667. 10.1016/S0140-6736(06)68264-0.CrossRefPubMed Cisse B, Sokhna C, Boulanger D, Milet J, Ba el H, Richardson K, Hallett R, Sutherland C, Simondon K, Simondon F: Seasonal intermittent preventive treatment with artesunate and sulfadoxine-pyrimethamine for prevention of malaria in Senegalese children: a randomised, placebo-controlled, double-blind trial. Lancet. 2006, 367 (9511): 659-667. 10.1016/S0140-6736(06)68264-0.CrossRefPubMed
23.
go back to reference Cornelie S, Remoue F, Doucoure S, Ndiaye T, Sauvage FX, Boulanger D, Simondon F: An insight into immunogenic salivary proteins of Anopheles gambiae in African children. Malar J. 2007, 6: 75-10.1186/1475-2875-6-75.PubMedCentralCrossRefPubMed Cornelie S, Remoue F, Doucoure S, Ndiaye T, Sauvage FX, Boulanger D, Simondon F: An insight into immunogenic salivary proteins of Anopheles gambiae in African children. Malar J. 2007, 6: 75-10.1186/1475-2875-6-75.PubMedCentralCrossRefPubMed
24.
go back to reference Grindstaff JL, Brodie ED, Ketterson ED: Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc Biol Sci. 2003, 270 (1531): 2309-2319. 10.1098/rspb.2003.2485.PubMedCentralCrossRefPubMed Grindstaff JL, Brodie ED, Ketterson ED: Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc Biol Sci. 2003, 270 (1531): 2309-2319. 10.1098/rspb.2003.2485.PubMedCentralCrossRefPubMed
25.
go back to reference Simister NE: Placental transport of immunoglobulin G. Vaccine. 2003, 21 (24): 3365-3369. 10.1016/S0264-410X(03)00334-7.CrossRefPubMed Simister NE: Placental transport of immunoglobulin G. Vaccine. 2003, 21 (24): 3365-3369. 10.1016/S0264-410X(03)00334-7.CrossRefPubMed
26.
go back to reference McCall PJ, Mosha FW, Njunwa KJ, Sherlock K: Evidence for memorized site-fidelity in Anopheles arabiensis. Trans R Soc Trop Med Hyg. 2001, 95 (6): 587-590. 10.1016/S0035-9203(01)90087-2.CrossRefPubMed McCall PJ, Mosha FW, Njunwa KJ, Sherlock K: Evidence for memorized site-fidelity in Anopheles arabiensis. Trans R Soc Trop Med Hyg. 2001, 95 (6): 587-590. 10.1016/S0035-9203(01)90087-2.CrossRefPubMed
Metadata
Title
Human IgG response to a salivary peptide, gSG6-P1, as a new immuno-epidemiological tool for evaluating low-level exposure to Anopheles bites
Authors
Anne Poinsignon
Sylvie Cornelie
Fatou Ba
Denis Boulanger
Cheikh Sow
Marie Rossignol
Cheikh Sokhna
Badara Cisse
François Simondon
Franck Remoue
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2009
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-8-198

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