Malaria resistance genes are associated with the levels of IgG subclasses directed against Plasmodium falciparum blood-stage antigens in Burkina Faso

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Afridi, Sarwat ^a,b   Atkinson, Alexandre ^a,b   Garnier, Séverine ^a,b   Fumoux, Francis ^b,c   Rihet, Pascal ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c UMR MD3   (France)

Author keywords

Family based association; HBB; IgG subclass; Immune genes; Malaria; Plasmodium falciparum

Indexed keywords

FC RECEPTOR IIA; HEMOGLOBIN BETA CHAIN; HEMOGLOBIN C; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G3 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 4; LYMPHOTOXIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; TUMOR NECROSIS FACTOR;

ADOLESCENT; ADULT; ARTICLE; BURKINA FASO; CHILD; DNA POLYMORPHISM; FEMALE; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; PARASITEMIA; PRESCHOOL CHILD; SCHOOL CHILD;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; BURKINA FASO; CHILD; CHILD, PRESCHOOL; HEMOGLOBINS; HUMANS; IMMUNOGLOBULIN G; INFANT; INTERLEUKIN-12; INTERLEUKIN-4; LEUKOTRIENE A4; MALARIA, FALCIPARUM; PARASITEMIA; PLASMODIUM FALCIPARUM; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, IGG; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84865659015     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-308     Document Type: Article

References (52)

1. How malaria has affected the human genome and what human genetics can teach us about malaria. Kwiatkowski DP, Am J Hum Genet 2005 77 171 192 10.1086/432519 16001361 (Pubitemid 41022702)
2. Linkage and association between Plasmodium falciparum blood infection levels and chromosome 5q31-q33. Flori L, Kumulungui B, Aucan C, Esnault C, Traoré AS, Fumoux F, Rihet P, Genes Immun 2003 4 265 268 10.1038/sj.gene.6363960 12761562 (Pubitemid 39562125)
3. Linkage of mild malaria to the major histocompatibility complex in families living in Burkina Faso. Flori L, Sawadogo S, Esnault C, Delahaye NF, Fumoux F, Rihet P, Hum Molec Genet 2003 12 375 378 10.1093/hmg/ddg033 12566384 (Pubitemid 36285129)
4. Allelic polymorphisms in the repeat and promoter regions of the interleukin-4 gene and malaria severity in Ghanaian children. Gyan BA, Goka B, Cvetkovic JT, Kurtzhals JL, Adabayeri V, Perlmann H, Lefvert AK, Akanmori BD, Troye-Blomberg M, Clin Exp Immunol 2004 138 145 150 10.1111/j.1365-2249.2004. 02590.x 15373917 (Pubitemid 39279977)
5. Haplotypes of IL12B promoter polymorphisms condition susceptibility to severe malaria and functional changes in cytokine levels in Thai adults. Phawong C, Ouma C, Tangteerawatana P, Thongshoob J, Were T, Mahakunkijcharoen Y, Wattanasirichaigoon D, Perkins DJ, Khusmith S, Immunogenetics 2010 62 345 356 10.1007/s00251-010-0439-y 20387064
6. Family-based association of a low producing lymphotoxin-alpha allele with reduced Plasmodium falciparum parasitemia. Barbier M, Delahaye NF, Fumoux F, Rihet P, Microbes Infect 2008 10 673 679 10.1016/j.micinf.2008.03.001 18457972
7. Significant association between TNF-alpha (TNF) promoter allele (-1031C, -863C, and -857C) and cerebral malaria in Thailand. Hananantachai H, Patarapotikul J, Ohashi J, Naka I, Krudsood S, Looareesuwan S, Tokunaga K, Tissue Antigens 2007 69 277 280 10.1111/j.1399-0039.2006.00756.x 17493155 (Pubitemid 46696936)
8. Severe malarial anemia and cerebral malaria are associated with different tumor necrosis factor promoter alleles. McGuire W, Knight JC, Hill AV, Allsopp CE, Greenwood BM, Kwiatkowski D, J Infect Dis 1999 179 287 290 10.1086/314533 9841857 (Pubitemid 29028373)
9. Association analyses of NCR3 polymorphisms with P. falciparum mild malaria. Delahaye NF, Barbier M, Fumoux F, Rihet P, Microbes Infect 2007 9 160 166 10.1016/j.micinf.2006.11.002 17208487 (Pubitemid 46228001)
10. TNF as a malaria candidate gene: polymorphism-screening and family-based association analysis of mild malaria attack and parasitemia in Burkina Faso. Flori L, Delahaye NF, Iraqi FA, Hernandez-Valladares M, Fumoux F, Rihet P, Genes Immun 2005 6 472 480 10.1038/sj.gene.6364231 15931230 (Pubitemid 43090505)
11. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. Bouharoun-Tayoun H, Oeuvray C, Lunel F, Druilhe P, J Exp Med 1995 182 409 418 10.1084/jem.182.2.409 7629503
12. Age-dependent association between IgG2 and IgG3 subclasses to Pf332-C231 antigen and protection from malaria, and induction of protective antibodies by sub-patent malaria infections, in Daraweesh. Giha HA, Nasr A, Iriemenam NC, Balogun HA, Arnot D, Theander TG, Troye-Blomberg M, Berzins K, ElGhazali G, Vaccine 2010 28 1732 1739 10.1016/j.vaccine.2009.12.018 20036751
13. Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. Roussilhon C, Oeuvray C, Müller-Graf C, Tall A, Rogier C, Trape J-F, Theisen M, Balde A, Pérignon J-L, Druilhe P, PLoS Med 2007 4 320 10.1371/journal.pmed.0040320 18001147 (Pubitemid 350220532)
14. High immunoglobulin G2 (IgG2) and low IgG4 levels are associated with human resistance to Plasmodium falciparum malaria. Aucan C, Traore Y, Tall F, Nacro B, Traore-Leroux T, Fumoux F, Rihet P, Infect Immun 2000 68 1252 1258 10.1128/IAI.68.3.1252-1258.2000 10678934 (Pubitemid 30108518)
15. Genetic regulation of human anti-malarial antibodies in twins. Sjöberg K, Lepers JP, Raharimalala L, Larsson A, Olerup O, Marbiah NT, Troye-Blomberg M, Perlmann P, Proc Natl Acad Sci USA 1992 89 2101 2104 10.1073/pnas.89.6.2101 1549568
16. Familial correlation of immunoglobulin G subclass responses to Plasmodium falciparum antigens in Burkina Faso. Aucan C, Traoré Y, Fumoux F, Rihet P, Infect Immun 2001 69 996 1001 10.1128/IAI.69.2.996-1001.2001 11159995 (Pubitemid 32109566)
17. Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Jepson A, Infect Immun 1997 65 872 876 9038290 (Pubitemid 27087984)
18. Heritability and segregation analysis of immune responses to specific malaria antigens in Papua New Guinea. Stirnadel HA, Beck HP, Alpers MP, Smith TA, Genet Epidemiol 1999 17 16 34 10.1002/(SICI)1098-2272(1999)17:1<16::AID- GEPI2>3.0.CO;2-7 10323182 (Pubitemid 29481855)
19. Humoral response to Plasmodium falciparum Pf155/ring-infected erythrocyte surface antigen and Pf332 in three sympatric ethnic groups of Burkina Faso. Modiano D, Chiucchiuini A, Petrarca V, Sirima BS, Luoni G, Perlmann H, Esposito F, Coluzzi M, Am J Trop Med Hyg 1998 58 220 224 9502607 (Pubitemid 28096230)
20. IL4 gene polymorphism and previous malaria experiences manipulate anti-Plasmodium falciparum antibody isotype profiles in complicated and uncomplicated malaria. Tangteerawatana P, Perlmann H, Hayano M, Kalambaheti T, Troye-Blomberg M, Khusmith S, Malar J 2009 8 286 10.1186/1475-2875-8-286 20003246
21. The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, Luty AJF, J Infect Dis 2005 191 1631 1638 10.1086/429832 15838789 (Pubitemid 40656750)
22. Influence of carriage of hemoglobin AS and the Fc gamma receptor IIa-R131 allele on levels of immunoglobulin G2 antibodies to Plasmodium falciparum merozoite antigens in Gabonese children. Ntoumi F, Flori L, Mayengue PI, Matondo Maya DW, Issifou S, Deloron P, Lell B, Kremsner PG, Rihet P, J Infect Dis 2005 192 1975 1980 10.1086/497611 16267770 (Pubitemid 41681896)
23. Differences in Fcgamma receptor IIa genotypes and IgG subclass pattern of anti-malarial antibodies between sympatric ethnic groups in Mali. Israelsson E, Vafa M, Maiga B, Lysén A, Iriemenam NC, Dolo A, Doumbo OK, Troye-Blomberg M, Berzins K, Malar J 2008 7 175 10.1186/1475-2875-7-175 18793404
24. Human genetic factors related to susceptibility to mild malaria in Gabon. Migot-Nabias F, Mombo LE, Luty AJ, Dubois B, Nabias R, Bisseye C, Millet P, Lu CY, Deloron P, Genes Immun 2000 1 435 441 10.1038/sj.gene.6363703 11196674
25. Genetics of susceptibility to malaria related phenotypes. Carpenter D, Rooth I, Färnert A, Abushama H, Quinnell RJ, Shaw M-A, Infect Genet Evol 2009 9 97 103 10.1016/j.meegid.2008.10.008 19022401
26. Hemoglobin C is associated with reduced Plasmodium falciparum parasitemia and low risk of mild malaria attack. Rihet P, Flori L, Tall F, Traore AS, Fumoux F, Hum Molec Genet 2004 13 1 6 10.1093/hmg/ddh084 14613965 (Pubitemid 38072129)
27. Malaria in humans: Plasmodium falciparum blood infection levels are linked to chromosome 5q31-q33. Rihet P, Traoré Y, Abel L, Aucan C, Traoré-Leroux T, Fumoux F, Am J Hum Genet 1998 63 498 505 10.1086/301967 9683598 (Pubitemid 30418631)
28. Whole genome amplification from a single cell: implications for genetic analysis. Zhang L, Cui X, Schmitt K, Hubert R, Navidi W, Arnheim N, Proc Natl Acad Sci USA 1992 89 5847 5851 10.1073/pnas.89.13.5847 1631067
29. Evidence for epistasis between hemoglobin C and immune genes in human P. falciparum malaria: a family study in Burkina Faso. Atkinson A, Barbier M, Afridi S, Fumoux F, Rihet P, Genes Immun 2011 12 481 489 10.1038/gene.2011.19 21451558
30. IL12B polymorphisms are linked but not associated with Plasmodium falciparum parasitemia: a familial study in Burkina Faso. Barbier M, Atkinson A, Fumoux F, Rihet P, Genes Immun 2008 9 405 411 10.1038/gene.2008.31 18449199
31. Rapid detection of the Fc gamma RIIA-H/R 131 ligand-binding polymorphism using an allele-specific restriction enzyme digestion (ASRED). Jiang XM, Arepally G, Poncz M, McKenzie SE, J Immunol Meth 1996 199 55 59 10.1016/S0022-1759(96)00164-0 (Pubitemid 26392327)
32. Implementing a unified approach to family-based tests of association. Laird NM, Horvath S, Xu X, Genet Epidemiol 2000 19 Suppl 1 36 S42 11055368
33. Statistical significance for genomewide studies. Storey JD, Tibshirani R, Proc Natl Acad Sci USA 2003 100 9440 9445 10.1073/pnas.1530509100 12883005 (Pubitemid 37033947)
34. Differential regulation of IgG subclasses and IgE antimalarial antibody responses in complicated and uncomplicated Plasmodium falciparum malaria. Tangteerawatana P, Montgomery SM, Perlmann H, Looareesuwan S, Troye-Blomberg M, Khusmith S, Parasite Immunol 2007 29 475 483 10.1111/j.1365-3024.2007.00965.x 17727571 (Pubitemid 47313231)
35. Cohort study of the association of antibody levels to AMA1, MSP119, MSP3 and GLURP with protection from clinical malaria in Ghanaian children. Dodoo D, Aikins A, Kusi KA, Lamptey H, Remarque E, Milligan P, Bosomprah S, Chilengi R, Osei YD, Akanmori BD, Theisen M, Malar J 2008 7 142 10.1186/1475-2875-7-142 18664257
36. IL-4 plus CD40 monoclonal antibody induces human B cells gamma subclass-specific isotype switch: switching to gamma 1, gamma 3, and gamma 4, but not gamma 2. Fujieda S, Zhang K, Saxon A, J Immunol 1995 155 2318 2328 7544371
37. Regulation of human IgG subclass production by cytokines: human IgG subclass production enhanced differentially by interleukin-6. Kawano Y, Noma T, Kou K, Yoshizawa I, Yata J, Immunology 1995 84 278 284 7751005
38. Regulation of antigen-specific immunoglobulin G subclasses in response to conserved and polymorphic Plasmodium falciparum antigens in an in vitro model. Garraud O, Perraut R, Diouf A, Nambei WS, Tall A, Spiegel A, Longacre S, Kaslow DC, Jouin H, Mattei D, Engler GM, Nutman TB, Riley EM, Mercereau-Puijalon O, Infect Immun 2002 70 2820 2827 10.1128/IAI.70.6.2820-2827.2002 12010968 (Pubitemid 34564137)
39. Interleukin-10 induces immunoglobulin G isotype switch recombination in human CD40-activated naive B lymphocytes. Malisan F, Brière F, Bridon JM, Harindranath N, Mills FC, Max EE, Banchereau J, Martinez-Valdez H, J Exp Med 1996 183 937 947 10.1084/jem.183.3.937 8642297 (Pubitemid 26113963)
40. Regulation of human IgG subclass production by cytokines. IFN-gamma and IL-6 act antagonistically in the induction of human IgG1 but additively in the induction of IgG2. Kawano Y, Noma T, Yata J, J Immunol 1994 153 4948 4958 7963558 (Pubitemid 24356126)
41. Delayed IgG2 humoral response in infants is not due to intrinsic T or B cell defects. Servet-Delprat C, Bridon JM, Djossou O, Yahia SA, Banchereau J, Briere F, Int Immunol 1996 8 1495 1502 10.1093/intimm/8.10.1495 8921428 (Pubitemid 26341089)
42. An immune basis for malaria protection by the sickle cell trait. Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K, PLoS Med 2005 2 128 10.1371/journal.pmed.0020128 15916466 (Pubitemid 40973531)
43. Abnormal haemoglobins in the Sudan savanna of Nigeria. IV. Malaria, immunoglobulins and antimalarial antibodies in haemoglobin AC individuals. Storey J, Fleming AF, Cornille-Brøgger R, Molineaux L, Matsushima T, Kagan I, Ann Trop Med Parasitol 1979 73 311 315 496483 (Pubitemid 10230849)
44. Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. Verra F, Simpore J, Warimwe GM, Tetteh KK, Howard T, Osier FHA, Bancone G, Avellino P, Blot I, Fegan G, Bull PC, Williams TN, Conway DJ, Marsh K, Modiano D, PLoS One 2007 2 978 10.1371/journal.pone.0000978 17912355 (Pubitemid 351472371)
45. Isotypic analysis of maternally transmitted Plasmodium falciparum-specific antibodies in Cameroon, and relationship with risk of P. falciparum infection. Deloron P, Dubois B, Le Hesran JY, Riche D, Fievet N, Cornet M, Ringwald P, Cot M, Clin Exp Immunol 1997 110 212 218 9367404 (Pubitemid 27469593)
46. Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Oeuvray C, Theisen M, Rogier C, Trape JF, Jepsen S, Druilhe P, Infect Immun 2000 68 2617 2620 10.1128/IAI.68.5.2617-2620.2000 10768952 (Pubitemid 30253834)
47. FcγRIIa (CD32) polymorphism and anti-malarial IgG subclass pattern among Fulani and sympatric ethnic groups living in eastern Sudan. Nasr A, Iriemenam NC, Giha HA, Balogun HA, Anders RF, Troye-Blomberg M, ElGhazali G, Berzins K, Malar J 2009 8 43 10.1186/1475-2875-8-43 19284648
48. Dynamics of the interaction of human IgG subtype immune complexes with cells expressing R and H allelic forms of a low-affinity Fc gamma receptor CD32A. Shashidharamurthy R, Zhang F, Amano A, Kamat A, Panchanathan R, Ezekwudo D, Zhu C, Selvaraj P, J Immunol 2009 183 8216 8224 10.4049/jimmunol.0902550 20007585
49. Fc gamma receptor IIa (CD32) polymorphism and antibody responses to asexual blood-stage antigens of Plasmodium falciparum malaria in Sudanese patients. Nasr A, Iriemenam NC, Troye-Blomberg M, Giha HA, Balogun HA, Osman OF, Montgomery SM, ElGhazali G, Berzins K, Scand J Immunol 2007 66 87 96 10.1111/j.1365-3083.2007.01947.x 17587350 (Pubitemid 46991978)
50. Polymorphism of the 5'-flanking region of the human tumor necrosis factor (TNF)-alpha gene in Japanese. Higuchi T, Seki N, Kamizono S, Yamada A, Kimura A, Kato H, Itoh K, Tissue Antigens 1998 51 605 612 10.1111/j.1399-0039.1998. tb03002.x 9694352 (Pubitemid 28306464)
51. Allele-specific binding of the ubiquitous transcription factor OCT-1 to the functional single nucleotide polymorphism (SNP) sites in the tumor necrosis factor-alpha gene (TNFA) promoter. Hohjoh H, Tokunaga K, Genes Immun 2001 2 105 109 10.1038/sj.gene.6363721 11393654 (Pubitemid 33674236)
52. Tumor necrosis factor alpha is an autocrine growth factor for normal human B cells. Boussiotis VA, Nadler LM, Strominger JL, Goldfeld AE, Proc Natl Acad Sci USA 1994 91 7007 7011 10.1073/pnas.91.15.7007 7518925 (Pubitemid 24226791)