Polymorphisms in the fc gamma receptor iiia and toll-like receptor 9 are associated with protection against severe malarial anemia and changes in circulating gamma interferon levels

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4435-4443

  Munde, Elly O ^a   Okeyo, Winnie A ^a   Anyona, Samwel B ^a   Raballah, Evans ^b   Konah, Stephen ^a   Okumu, Wilson ^a   Ogonda, Lilian ^a   Vulule, John ^c   Ouma, Collins ^a  

^a MASENO UNIVERSITY   (Kenya)

^b MASINDE MULIRO UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Kenya)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

FC GAMMA RECEPTOR IIIA; FC RECEPTOR; GAMMA INTERFERON; HEMOGLOBIN; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANEMIA; ARTICLE; CHILD; DISEASE PREDISPOSITION; DISEASE SEVERITY; DNA POLYMORPHISM; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALARIA; MALE; MULTIVARIATE LOGISTIC REGRESSION ANALYSIS; PATHOGENESIS; PRIORITY JOURNAL; SEVERE MALARIAL ANEMIA;

ANEMIA; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; INFANT; INTERFERON-GAMMA; KENYA; MALARIA, FALCIPARUM; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; RECEPTORS, IGG; SEVERITY OF ILLNESS INDEX; TOLL-LIKE RECEPTOR 9;

EID: 84870802553     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00945-12     Document Type: Article

References (65)

1. Abdalla S, Weatherall DJ, Wickramasinghe SN, Hughes M. 1980. The anaemia of P. falciparum malaria. Br. J. Haematol. 46:171-183.
2. Adler AJ, Scheller A, Robins DM. 1993. The stringency and magnitude of androgen-specific gene activation are combinatorial functions of receptor and nonreceptor binding site sequences. Mol. Cell. Biol. 13:6326-6335.
3. Aidoo M, et al. 2002. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 359:1311-1312.
4. Akira S. 2003. Mammalian Toll-like receptors. Curr. Opin. Immunol. 15:5-11.
5. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
6. Aribot G, et al. 1996. Pattern of immunoglobulin isotype response to Plasmodiumfalciparum blood-stage antigens in individuals living in a holoendemic area of Senegal (Dielmo, west Africa). Am. J. Trop. Med. Hyg. 54:449-457.
7. Balaresque PL, Ballereau SJ, Jobling MA. 2007. Challenges in human genetic diversity: demographic history and adaptation. Hum. Mol. Genet. 16(special issue 2):R134 -R139.
8. Bauer S, et al. 2001. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U. S. A. 98:9237-9242.
9. Bloland PB, et al. 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children. Am. J. Trop. Med. Hyg. 60:641-648.
10. Brattig NW, et al. 2008. Plasmodium falciparum glycosylphosphatidylinositol toxin interacts with the membrane of non-parasitized red blood cells: a putative mechanism contributing to malaria anemia. Microbes Infect. 10:885-891.
11. Breman JG, Alilio MS, Mills A. 2004. Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am. J. Trop. Med. Hyg. 71:1-15.
12. Buffet PA, Safeukui I, Milon G, Mercereau-Puijalon O, David PH. 2009. Retention of erythrocytes in the spleen: a double-edged process in human malaria. Curr. Opin. Hematol. 16:157-164.
13. Campino S, et al. 2009. TLR9 polymorphisms in African populations: no association with severe malaria, but evidence of cis-variants acting on gene expression. Malar. J. 8:44. doi:10.1186/1475-2875-8-44.
14. Clark IA, Cowden WB. 2003. The pathophysiology of falciparum malaria. Pharmacol. Ther. 99:221-260.
15. Clarkson SB, et al. 1986. Blockade of clearance of immune complexes by an anti-Fc gamma receptor monoclonal antibody. J. Exp. Med. 164:474-489.
16. Coban C, et al. 2005. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J. Exp. Med. 201:19-25.
17. Daeron M. 1997. Fc receptor biology. Annu. Rev. Immunol. 15:203-234.
18. Dodoo D, et al. 2002. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J. Infect. Dis. 185:971-979.
19. D'Ombrain MC, et al. 2008. Association of early interferon-gamma production with immunity to clinical malaria: a longitudinal study among Papua New Guinean children. Clin. Infect. Dis. 47:1380-1387.
20. Dondorp AM, et al. 1999. Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am. J. Trop. Med. Hyg. 60:733-737.
21. Dondorp AM, et al. 1999. Red cell deformability, splenic function and anaemia in thalassaemia. Br. J. Haematol. 105:505-508.
22. Du X, Poltorak A, Wei Y, Beutler B. 2000. Three novel mammalian Toll-like receptors: gene structure, expression, and evolution. Eur. Cytokine Netw. 11:362-371.
23. Fanger MW, Shen L, Graziano RF, Guyre PM. 1989. Cytotoxicity mediated by human Fc receptors for IgG. Immunol. Today 10:92-99.
24. Franklin BS, et al. 2009. Malaria primes the innate immune response due to interferon-gamma induced enhancement of Toll-like receptor expression and function. Proc. Natl. Acad. Sci. U. S. A. 106:5789-5794.
25. Gajewski TF, Joyce J, Fitch FW. 1989. Antiproliferative effect of IFNgamma in immune regulation. III. Differential selection of TH1 and TH2 murine helper T lymphocyte clones using recombinant IL-2 and recombinant IFN-gamma. J. Immunol. 143:15-22.
26. Helleberg M, et al. 2005. Bone marrow suppression and severe anaemia associated with persistent Plasmodium falciparum infection in African children with microscopically undetectable parasitaemia. Malar. J. 4:56. doi:10.1186/1475-2875-4-56.
27. Indik ZK, Park JG, Hunter S, Schreiber AD. 1995. The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood 86:4389-4399.
28. Janeway CA, Jr, Medzhitov R. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197-216.
29. Koene HR, et al. 1997. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood 90:1109-1114.
30. Leoratti FM, et al. 2008. Variants in the Toll-like receptor signaling pathway and clinical outcomes of malaria. J. Infect. Dis. 198:772-780.
31. Li X, Ptacek TS, Brown EE, Edberg JC. 2009. Fcgamma receptors:structure, function and role as genetic risk factors in SLE. Genes Immun. 10:380-389.
32. Marsh K, et al. 1995. Indicators of life-threatening malaria in African children. N. Engl. J. Med. 332:1399-1404.
33. McElroy PD, et al. 1999. Analysis of repeated hemoglobin measures in full-term, normal birth weight Kenyan children between birth and four years of age. III. The Asemobo Bay Cohort Project. Am. J. Trop. Med. Hyg. 61:932-940.
34. Mirghani HA, Eltahir HGAETM, Mirghani YA, Elbashir MI, Adam I. 2011. Cytokine profiles in children with severe Plasmodium falciparum malaria in an area of unstable malaria transmission in central Sudan. J. Trop. Pediatr. 57:392-395.
35. Mockenhaupt FP, et al. 2006. Common polymorphisms of Toll-like receptors 4 and 9 are associated with the clinical manifestation of malaria during pregnancy. J. Infect. Dis. 194:184-188.
36. Naotunne TS, et al. 1991. Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. J. Exp. Med. 173:523-529.
37. Ng MT, et al. 2010. Increase in NF-kappaB binding affinity of the variant C allele of the Toll-like receptor 9-1237T/C polymorphism is associated with Helicobacter pylori-induced gastric disease. Infect. Immun. 78:1345-1352.
38. Nussler AK, et al. 1993. In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants. Eur. J. Immunol. 23:882-887.
39. Obonyo CO, Vulule J, Akhwale WS, Grobbee DE. 2007. In-hospital morbidity and mortality due to severe malarial anemia in western Kenya. Am. J. Trop. Med. Hyg. 77:23-28.
40. Omar AH, et al. 2012. Toll-like receptor 9 (TLR9) polymorphism associated with symptomatic malaria: a cohort study. Malar. J. 11:168. doi:10.1186/1475-2875-11-168.
41. Omi K, et al. 2002. Absence of association between the Fc gamma receptor IIIA-176F/V polymorphism and the severity of malaria in Thai. Jpn. J. Infect. Dis. 55:167-169.
42. Ong'echa JM, Davenport GC, Vulule JM, Hittner JB, Perkins DJ. 2011. Identification of inflammatory biomarkers for pediatric malarial anemia severity using novel statistical methods. Infect. Immun. 79:4674-4680.
43. Ong'echa JM, et al. 2006. Parasitemia, anemia, and malarial anemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. Am. J. Trop. Med. Hyg. 74:376-385.
44. Oswald IP, Wynn TA, Sher A, James SL. 1992. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc. Natl. Acad. Sci. U. S. A. 89:8676-8680.
45. Otieno RO, et al. 2006. Increased severe anemia in HIV-1-exposed and HIV-1-positive infants and children during acute malaria. AIDS 20:275-280.
46. Ouma C, et al. 2012. Functional haplotypes of Fc gamma (Fcgamma) receptor (FcgammaRIIA and FcgammaRIIIB) predict risk to repeated episodes of severe malarial anemia and mortality in Kenyan children. Hum. Genet. 131:289-299.
47. Ouma C, et al. 2006. Association of FCgamma receptor IIA (CD32) polymorphism with malarial anemia and high-density parasitemia in infants and young children. Am. J. Trop. Med. Hyg. 74:573-577.
48. Parroche P, et al. 2007. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Tolllike receptor 9. Proc. Natl. Acad. Sci. U. S. A. 104:1919-1924.
49. Phillips RE, et al. 1986. The importance of anaemia in cerebral and uncomplicated falciparum malaria: role of complications, dyserythropoiesis and iron sequestration. Q. J. Med. 58:305-323.
50. Pichyangkul S, et al. 2004. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J. Immunol. 172:4926-4933.
51. Price RN, et al. 2001. Factors contributing to anemia after uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 65:614-622.
52. Ravetch JV, Kinet JP. 1991. Fc receptors. Annu. Rev. Immunol. 9:457-492.
53. Sam-Agudu NA, et al. 2010. TLR9 polymorphisms are associated with altered IFN-gamma levels in children with cerebral malaria. Am. J. Trop. Med. Hyg. 82:548-555.
54. Stevenson MM, Tam MF, Wolf SF, Sher A. 1995. IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFNgamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J. Immunol. 155:2545-2556.
55. Su Z, Stevenson MM. 2000. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immun. 68:4399-4406.
56. Tangteerawatana P, et al. 2007. Relative levels of IL4 and IFN-gamma in complicated malaria: association with IL4 polymorphism and peripheral parasitemia. Acta Trop. 101:258-265.
57. Taylor RR, Allen SJ, Greenwood BM, Riley EM. 1998. IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. Am. J. Trop. Med. Hyg. 58:406-413.
58. Tishkoff SA, Williams SM. 2002. Genetic analysis of African populations:human evolution and complex disease. Nat. Rev. Genet. 3:611-621.
59. Torre D, et al. 2002. Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria. Clin. Diagn. Lab. Immunol. 9:348-351.
60. Tsuji M, et al. 1995. Development of antimalaria immunity in mice lacking IFN-gamma receptor. J. Immunol. 154:5338-5344.
61. van Sorge NM, van der Pol WL, van de Winkel JG. 2003. FcgammaR polymorphisms: implications for function, disease susceptibility and immunotherapy. Tissue Antigens 61:189-202.
62. Were T, et al. 2011. Bacteremia in Kenyan children presenting with malaria. J. Clin. Microbiol. 49:671-676.
63. WHO. 2010. World malaria report. WHO Press, Geneva Switzerland.
64. Xu H, et al. 2002. The mechanism and significance of deletion of parasitespecific CD4(+) T cells in malaria infection. J. Exp. Med. 195:881-892.
65. Zakeri S, Pirahmadi S, Mehrizi AA, Djadid ND. 2011. Genetic variation of TLR-4, TLR-9 and TIRAP genes in Iranian malaria patients. Malar. J. 10:77. doi:10.1186/1475-2875-10-77.