IgG responses to Anopheles gambiae salivary antigen gSG6 detect variation in exposure to malaria vectors and disease risk

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Stone, Will ^a,b   Bousema, Teun ^a,b   Jones, Sophie ^a   Gesase, Samwel ^c   Hashim, Rhamadhan ^c   Gosling, Roly ^d   Carneiro, Ilona ^a   Chandramohan, Daniel ^a   Theander, Thor ^e   Ronca, Raffaele ^f   Modiano, David ^g   Arcà, Bruno ^f,g   Drakeley, Chris ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; IMMUNOGLOBULIN G; PARASITE ANTIGEN; PROTEIN AMA 1; PROTEIN GLURP R1; PROTEIN GLURP R2; PROTEIN GSG6; PROTEIN MSP 1; PROTEIN MSP 3; SALIVA PROTEIN; UNCLASSIFIED DRUG;

ANOPHELES GAMBIAE; ANTIGEN DETECTION; ANTIGENIC VARIATION; ARTICLE; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GEOGRAPHIC DISTRIBUTION; HUMAN; IMMUNE RESPONSE; IMMUNOASSAY; INCIDENCE; INFANT; INFECTION RISK; MAJOR CLINICAL STUDY; MALARIA; MORBIDITY; NONHUMAN; SEROPREVALENCE; TANZANIA;

ANIMALS; ANOPHELES GAMBIAE; DISEASE VECTORS; FAMILY CHARACTERISTICS; FEMALE; HUMANS; IMMUNOGLOBULIN G; INCIDENCE; INFANT; INSECT PROTEINS; MALARIA; PLASMODIUM FALCIPARUM; RISK FACTORS; SALIVARY PROTEINS AND PEPTIDES; SEROEPIDEMIOLOGIC STUDIES; TANZANIA;

ANOPHELES (GENUS); ANOPHELES GAMBIAE;

EID: 84863084935     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040170     Document Type: Article

References (70)

1. Kreuels B, Kobbe R, Adjei S, Kreuzberg C, von Reden C, et al. (2008) Spatial Variation of Malaria Incidence in Young Children from a Geographically Homogeneous Area with High Endemicity. Journal of Infectious Diseases 197: 85-93.
2. Bhattarai A, Ali AS, Kachur SP, Mårtensson A, Abbas AK, et al. (2007) Impact of Artemisinin-Based Combination Therapy and Insecticide-Treated Nets on Malaria Burden in Zanzibar. PLoS Med 4: e309.
3. Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, et al. (2008) Factors Determining the Heterogeneity of Malaria Incidence in Children in Kampala, Uganda. Journal of Infectious Diseases 198: 393-400.
4. Okiro E, Hay S, Gikandi P, Sharif S, Noor A, et al. (2007) The decline in paediatric malaria admissions on the coast of Kenya. Malaria Journal 6: 151.
5. Hommel M, (2008) Towards a research agenda for global malaria elimination. Malaria Journal 7: S1.
6. Das P, Horton R, (2010) Malaria elimination: worthy, challenging, and just possible. The Lancet 376: 1515-1517.
7. O'Meara WP, Mangeni JN, Steketee R, Greenwood B, (2010) Changes in the burden of malaria in sub-Saharan Africa. The Lancet Infectious Diseases 10: 545-555.
8. Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, et al. (2010) Operational strategies to achieve and maintain malaria elimination. The Lancet 376: 1592-1603.
9. World Health Organisation (2007) Malaria elimination: a field manual for low and moderate endemic countries.
10. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, et al. (2012) Hitting Hotspots: Spatial Targeting of Malaria for Control and Elimination. PLoS Med 9: e1001165.
11. Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, et al. (2010) Identification of Hot Spots of Malaria Transmission for Targeted Malaria Control. Journal of Infectious Diseases 201: 1764-1774.
12. Smith DL, Drakeley CJ, Chiyaka C, Hay SI, (2010) A quantitative analysis of transmission efficiency versus intensity for malaria. Nat Commun 1: 108.
13. Oesterholt M, Bousema JT, Mwerinde OK, Harris C, Lushino P, et al. (2006) Spatial and temporal variation in malaria transmission in a low endemicity area in northern Tanzania. Malaria Journal 5: 1-7.
14. World Health Organisation (2010) World Malaria Report.
15. Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, et al. (2003) An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Tropical Medicine & International Health 8: 767-774.
16. Hay SI, Rogers DJ, Toomer JF, Snow RW, (2000) Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, internet access and review. Transactions of the Royal Society of Tropical Medicine and Hygiene 94: 113-127.
17. Hii JLK, Smith T, Mai A, Ibam E, Alpers MP, (2000) Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bulletin of Entomological Research 90: 211-219.
18. Corran P, Coleman P, Riley E, Drakeley C, (2007) Serology: a robust indicator of malaria transmission intensity? Trends in Parasitology 23: 575-582.
19. Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, et al. (1993) Evaluation of light traps for sampling anopheline mosquitoes in Kilifi, Kenya. Journal Of The American Mosquito Control Association 9: 260-263.
20. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SLR, et al. (2005) Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proceedings of the National Academy of Sciences of the United States of America 102: 5108-5113.
21. Stewart L, Gosling R, Griffin J, Gesase S, Campo J, et al. (2009) Rapid Assessment of Malaria Transmission Using Age-Specific Sero-Conversion Rates. PLoS ONE 4: e6083.
22. Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, et al. (2010) Stable and Unstable Malaria Hotspots in Longitudinal Cohort Studies in Kenya. PLoS Med 7: e1000304.
23. Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, et al. (2010) Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerging infectious diseases 16: 392-399.
24. Cook J, Kleinschmidt I, Schwabe C, Nseng G, Bousema T, et al. (2011) Serological Markers Suggest Heterogeneity of Effectiveness of Malaria Control Interventions on Bioko Island, Equatorial Guinea. PLoS ONE 6: e25137.
25. Drakeley C, Cook J, (2009) Chapter 5 Potential Contribution of Sero-Epidemiological Analysis for Monitoring Malaria Control and Elimination: Historical and Current Perspectives. In: Rollinson D, Hay SI, editors. pp. 299-352 editors. Advances in Parasitology: Academic Press.
26. Mendis C, Del Giudice G, Gamage-Mendis AC, Tougne C, Pessi A, et al. (1992) Anti-circumsporozoite protein antibodies measure age related exposure to malaria in Kataragama, Sri Lanka. Parasite Immunology 14: 75-86.
27. Proietti C, Pettinato DD, Kanoi BN, Ntege E, Crisanti A, et al. (2011) Continuing Intense Malaria Transmission in Northern Uganda. The American Journal of Tropical Medicine and Hygiene 84: 830-837.
28. Satoguina J, Walther B, Drakeley C, Nwakanma D, Oriero E, et al. (2009) Comparison of surveillance methods applied to a situation of low malaria prevalence at rural sites in The Gambia and Guinea Bissau. Malaria Journal 8: 274.
29. Smith DL, McKenzie FE, Snow RW, Hay SI, (2007) Revisiting the Basic Reproductive Number for Malaria and Its Implications for Malaria Control. PLoS Biol 5: e42.
30. Brummer-Korvenkontio H, Lappalainen P, Reunala T, Palosuo T, (1994) Detection of mosquito saliva-specific IgE and IgG4 antibodies by immunoblotting. Journal of Allergy and Clinical Immunology 93: 551-555.
31. Palosuo K, Brummer-Korvenkontio H, Mikkola J, Sahi T, Reunala T, (1997) Seasonal Increase in Human IgE and lgG4 Antisaliva Antibodies to Aedes Mosquito Bites. International Archives of Allergy and Immunology 114: 367-372.
32. Peng Z, Simons FER, (2007) Advances in mosquito allergy. Current Opinion in Allergy and Clinical Immunology 7: 350-354.
33. Schwartz BS, Ribeiro JMC, Goldstein MD, (1990) Anti-Tick Antibodies: An Epidemiologic Tool in Lyme Disease Research. American Journal of Epidemiology 132: 58-66.
34. Schwartz BS, Ford DP, Childs JE, Rothman N, Thomas RJ, (1991) Anti-tick Saliva Antibody: A Biologic Marker of Tick Exposure That Is a Risk Factor for Lime Disease Seropositivity. American Journal of Epidemiology 134: 86-95.
35. Schwarz A, Sternberg JM, Johnston V, Medrano-Mercado N, Anderson JM, et al. (2009) Antibody responses of domestic animals to salivary antigens of Triatoma infestans as biomarkers for low-level infestation of triatomines. International Journal for Parasitology 39: 1021-1029.
36. Poinsignon A, Remoue F, Rossignol M, Cornelie S, Courtin D, et al. (2008) Human IgG Antibody Response to Glossina Saliva: An Epidemiologic Marker of Exposure to Glossina Bites. The American Journal of Tropical Medicine and Hygiene 78: 750-753.
37. Barral A, Honda E, Caldas A, Costa J, Vinhas V, et al. (2000) Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? The American Journal of Tropical Medicine and Hygiene 62: 740-745.
38. Marzouki S, Ahmed MB, Boussoffara T, Abdeladhim M, Aleya-Bouafif NB, et al. (2011) Characterization of the Antibody Response to the Saliva of Phlebotomus papatasi in People Living in Endemic Areas of Cutaneous Leishmaniasis. The American Journal of Tropical Medicine and Hygiene 84: 653-661.
39. Cornelie S, Remoue F, Doucoure S, NDiaye T, Sauvage F-X, et al. (2007) An insight into immunogenic salivary proteins of Anopheles gambiae in African children. Malaria Journal 6: 75.
40. Arcà B, Lombardo F, Valenzuela JG, Francischetti IMB, Marinotti O, et al. (2005) An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. Journal of Experimental Biology 208: 3971-3986.
41. Lanfrancotti A, Lombardo F, Santolamazza F, Veneri M, Castrignanò T, et al. (2002) Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. FEBS Letters 517: 67-71.
42. Ribeiro JMC, Mans BJ, Arcà B, (2010) An insight into the sialome of blood-feeding Nematocera. Insect Biochemistry and Molecular Biology 40: 767-784.
43. Rizzo C, Ronca R, Fiorentino G, Mangano V, Sirima S, et al. (2011) Wide cross-reactivity between Anopheles gambiae and Anopheles funestus SG6 salivary proteins supports exploitation of gSG6 as a marker of human exposure to major malaria vectors in tropical Africa. Malaria Journal 10: 206.
44. Orlandi-Pradines E, Almeras L, Denis de Senneville L, Barbe S, Remoué F, et al. (2007) Antibody response against saliva antigens of Anopheles gambiae and Aedes aegypti in travellers in tropical Africa. Microbes and Infection 9: 1454-1462.
45. Poinsignon A, Cornelie S, Ba F, Boulanger D, Sow C, et al. (2009) Human IgG response to a salivary peptide, gSG6-P1, as a new immuno-epidemiological tool for evaluating low-level exposure to Anopheles bites. Malaria Journal 8: 198.
46. Drame PM, Poinsignon A, Besnard P, Cornelie S, Le Mire J, et al. (2010) Human Antibody Responses to the Anopheles Salivary gSG6-P1 Peptide: A Novel Tool for Evaluating the Efficacy of ITNs in Malaria Vector Control. PLoS ONE 5: e15596.
47. Drame P, Machault V, Diallo A, Cornelie S, Poinsignon A, et al. (2012) IgG responses to the gSG6-P1 salivary peptide for evaluating human exposure to Anopheles bites in urban areas of Dakar region, Senegal. Malaria Journal 11: 72.
48. Rizzo C, Ronca R, Fiorentino G, Verra F, Mangano V, et al. (2011) Humoral Response to the Anopheles gambiae Salivary Protein gSG6: A Serological Indicator of Exposure to Afrotropical Malaria Vectors. PLoS ONE 6: e17980.
49. Remoue F, Cisse B, Ba F, Sokhna C, Herve J-P, et al. (2006) Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 100: 363-370.
50. Gosling RD, Gesase S, Mosha JF, Carneiro I, Hashim R, et al. (2009) Protective efficacy and safety of three antimalarial regimens for intermittent preventive treatment for malaria in infants: a randomised, double-blind, placebo-controlled trial. The Lancet 374: 1521-1532.
51. Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, et al. (2010) A progressive declining in the burden of malaria in north-eastern Tanzania. Malaria Journal 9: 216.
52. Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, et al. (2008) Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malaria Journal 7: 195.
53. Theisen M, Soe S, Brunstedt K, Follmann F, Bredmose L, et al. (2004) A Plasmodium falciparum GLURP-MSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine 22: 1188-1198.
54. Cham GK, Kurtis J, Lusingu J, Theander TG, Jensen AT, et al. (2008) A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malaria Journal 7: 108.
55. Poinsignon A, Cornelie S, Mestres-Simon M, Lanfrancotti A, Rossignol M, et al. (2008) Novel Peptide Marker Corresponding to Salivary Protein gSG6 Potentially Identifies Exposure to Anopheles Bites. PLoS ONE 3: e2472.
56. Woolhouse MEJ, Dye C, Etard J-F, Smith T, Charlwood JD, et al. (1997) Heterogeneities in the transmission of infectious agents: Implications for the design of control programs. Proceedings of the National Academy of Sciences 94: 338-342.
57. Smith DL, Dushoff J, McKenzie FE, (2004) The Risk of a Mosquito-Borne Infectionin a Heterogeneous Environment. PLoS Biol 2: e368.
58. Bousema T, Kreuels B, Gosling R, (2011) Adjusting for Heterogeneity of Malaria Transmission in Longitudinal Studies. Journal of Infectious Diseases 204: 1-3.
59. Clarke SE, Bøgh C, Brown RC, Walraven GEL, Thomas CJ, et al. (2002) Risk of malaria attacks in Gambian children is greater away from malaria vector breeding sites. Transactions of the Royal Society of Tropical Medicine and Hygiene 96: 499-506.
60. Greenhouse B, Ho B, Hubbard A, Njama-Meya D, Narum DL, et al. (2011) Antibodies to Plasmodium falciparum Antigens Predict a Higher Risk of Malaria But Protection From Symptoms Once Parasitemic. Journal of Infectious Diseases 204: 19-26.
61. Bejon P, Cook J, Bergmann-Leitner E, Olotu A, Lusingu J, et al. (2011) Effect of the pre-erythrocytic candidate malaria vaccine RTS,S/AS01E on blood stage immunity in young children. The Journal of infectious diseases 204: 9-18.
62. Bejon P, Warimwe G, Mackintosh CL, Mackinnon MJ, Kinyanjui SM, et al. (2009) Analysis of Immunity to Febrile Malaria in Children That Distinguishes Immunity from Lack of Exposure. Infect Immun 77: 1917-1923.
63. Kinyanjui SM, Bejon P, Osier FH, Bull PC, Marsh K, (2009) What you see is not what you get: implications of the brevity of antibody responses to malaria antigens and transmission heterogeneity in longitudinal studies of malaria immunity. Malaria Journal 8: 242.
64. Beier JC, Killeen GF, Githure JI, (1999) Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. The American Journal of Tropical Medicine and Hygiene 61: 109-113.
65. Greenwood BM, (1990) Immune responses to sporozoite antigens and their relationship to naturally acquired immunity to malaria. Bulletin of the World Health Organization 68.
66. Fowkes FJI, Richards JS, Simpson JA, Beeson JG, (2010) The Relationship between Anti-merozoite Antibodies and Incidence of Plasmodium falciparum Malaria: A Systematic Review and Meta-analysis. PLoS Med 7: e1000218.
67. Matsuoka H, Yoshida S, Hirai M, Ishii A, (2002) A rodent malaria, Plasmodium berghei, is experimentally transmitted to mice by merely probing of infective mosquito, Anopheles stephensi. Parasitology International 51: 17-23.
68. Rosenberg R, Wirtz RA, Schneider I, Burge R, (1990) An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Transactions of the Royal Society of Tropical Medicine and Hygiene 84: 209-212.
69. Medica DL, Sinnis P, (2005) Quantitative Dynamics of Plasmodium yoelii Sporozoite Transmission by Infected Anopheline Mosquitoes. Infect Immun 73: 4363-4369.
70. King JG, Vernick KD, Hillyer JF, (2011) Members of the Salivary Gland Surface Protein (SGS) Family Are Major Immunogenic Components of Mosquito Saliva. Journal of Biological Chemistry 286: 40824-40834.