Carriage of DRB1*13 is associated with increased posttreatment IgE levels against Schistosoma mansoni antigens and lower long-term reinfection levels

Journal of Immunology

Volumn 176, Issue 11, 2006, Pages 7112-7118

  Booth, Mark ^a   Shaw, Marie A ^b   Carpenter, Danielle ^b   Joseph, Sarah ^a   Kabatereine, Narcis B ^c   Kariuki, Henry C ^d   Mwatha, Joseph K ^e   Jones, Frances M ^a   Vennervald, Brigitte J ^f   Ouma, John H ^g   Dunne, David W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c MINISTRY OF HEALTH   (Uganda)

^d MINISTRY OF HEALTH   (Kenya)

^e KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^f DANISH BILHARZIASIS LABORATORY   (Denmark)

^g MASENO UNIVERSITY   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DR ANTIGEN; HLA DRB1 13 ANTIGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G4; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; PARASITE ANTIGEN; PRAZIQUANTEL; SOLUBLE EGG ANTIGEN; SOLUBLE WORM ANTIGEN; TEGUMENT ANTIGEN; UNCLASSIFIED DRUG; ANTHELMINTIC AGENT; HELMINTH ANTIBODY; HLA DQ ANTIGEN; HLA DRB1*13 ANTIGEN, HUMAN; HLA-DRB1 ANTIGEN; HLA-DRB1*13 ANTIGEN, HUMAN;

ADOLESCENT; ADULT; ANALYSIS OF COVARIANCE; ANTIGEN DETECTION; ARTICLE; BLOOD SAMPLING; CORRELATION ANALYSIS; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; HUMAN; IMMUNE RESPONSE; LONG TERM CARE; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; REINFECTION; SCHISTOSOMA MANSONI; SCHOOL CHILD; SCORING SYSTEM; TH2 CELL; UGANDA; AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMAL; BIOSYNTHESIS; BLOOD; CHILD; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; MALE; MIDDLE AGED; MOLECULAR GENETICS; PARASITE IDENTIFICATION; PARASITOLOGY; RECURRENT DISEASE; SCHISTOSOMIASIS; STATISTICS;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; ANTHELMINTICS; ANTIBODIES, HELMINTH; ANTIGENS, HELMINTH; CHILD; FEMALE; HLA-DQ ANTIGENS; HLA-DR ANTIGENS; HUMANS; IMMUNOGLOBULIN E; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PARASITE EGG COUNT; PRAZIQUANTEL; RECURRENCE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

EID: 33646878158     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.11.7112     Document Type: Article

References (52)

1. Kabatereine, N. B., B. J. Vennervald, J. H. Ouma, J. Kemijumbi, A. E. Butterworth, D. W. Dunne, and A. J. Fulford. 1999. Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118: 101-105.
2. Naus, C. W., M. Booth, F. M. Jones, J. Kemijumbi, B. J. Vennervald, C. H. Kariuki, J. H. Ouma, N. B. Kabatereine, and D. W. Dunne. 2003. The relationship between age, sex, egg-count and specific antibody responses against Schistosoma mansoni antigens in a Ugandan fishing community. Trop. Med. Int. Health 8: 561-568.
3. Dunne, D. W., A. E. Butterworth, A. J. Fulford, H. C. Kariuki, J. G. Langley, J. H. Ouma, A. Capron, R. J. Pierce, and R. F. Sturrock. 1992. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Ear. J. Immunol. 22: 1483-1494.
4. Webster, M., P. G. Fallon, A. J. Fulford, A. E. Butterworth, J. H. Ouma, G. Kimani, and D. W. Dunne. 1997. Effect of praziquantel and oxamniquine treatment on human isotype responses to Schistosoma mansoni: elevated IgE to adult worm. Parasite Immunol. 19: 333-335.
5. Joseph, S., F. M. Jones, K. Walter, A. J. Fulford, G. Kimani, J. K. Mwatha, T. Kamau, H. C. Kariuki, F. Kazibwe, E. Tukahebwa, et al. 2004. Increases in human T helper 2 cytokine responses to Schistosoma mansoni worm and worm-tegument antigens are induced by treatment with praziquantel. J. Infect. Dis. 190: 835-842.
6. Geha, R. S., H. H. Jabara, and S. R. Brodeur. 2003. The regulation of immunoglobulin E class-switch recombination. Nat. Rev. Immunol. 3: 721-732.
7. Blumenthal, M. N., K. Namboodiri, N. Mendell, G. Gleich, R. C. Elston, and E. Yunis. 1981. Genetic transmission of serum IgE Levels. Am. J. Med. Genet. 10: 219-228.
8. Marsh, D. G., J. D. Neely, D. R. Breazeale, B. Ghosh, L. R. Freidhoff, E. Ehrlich-Kautzky, C. Schou, G. Krishnaswamy, and T. H. Beaty. 1994. Linkage analysis of IL4 and other chromosome 5q31.1 markers and total serum immunoglobulin E concentrations. Science 264: 1152-1156.
9. Marquet, S., L. Abel, D. Hillaire, H. Dessein, J. Kalil, J. Feingold, J. Weissenbach, and A. J. Dessein. 1996. Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Nat. Genet. 14: 181-184.
10. Xu, J., D. S. Postma, T. D. Howard, G. H. Koppelman, S. L. Zheng, O. C. Stine, E. R. Bleecker, and D. A. Meyers. 2000. Major genes regulating total serum immunoglobulin E levels in families with asthma. Am. J. Hum. Genet. 67: 1163-1173.
11. Mansur, A. H., G. A. Williams, D. T. Bishop, A. F. Markham, S. Lewis, J. Britton, and J. F. Morrison. 2000. Evidence for a role of HLA DKBI alleles in the control of IgE levels, strengthened by interacting TCR A/D marker alleles. Clin. Exp. Allergy 30: 1371-1378.
12. Hirayama, K. 2004. Immunogenetic analysis of post-schistosomal liver fibrosis. Parasitol. Int. 53: 193-196.
13. Ohta, N., Y. K. Nishimura, M. Iuchi, and T. Sasazuki. 1982. Immunogenetic analysis of patients with post-schistosomal liver cirrhosis in man. Clin. Exp. Immunol. 49: 493-499.
14. Ohta, N., M. Hayashi, L. C. Tormis, B. L. Bias, J. S. Nosenas, and T. Sasazuki. 1987. Immunogenetic factors involved in the pathogenesis of distinct clinical manifestations of schistosomiasis japonica in the Philippine population. Trans. R. Soc. Trop. Med. Hyg. 81: 292-296.
15. Hirayama, K., H. Chen, M. Kikuchi, T. Yin, M. Itoh, X. Gu, S. Zhang, and H. Yuan. 1998. Glycine-valine dimorphism at the 86th amino acid of HLA-DRB1 influenced the prognosis of postschistosomal hepatic fibrosis. J. Infect. Dis. 177: 1682-1686.
16. Hirayama, K., H. Chen, M. Kikuchi, T. Yin, X. Gu, J. Liu, S. Zhang, and H. Yuan. 1999. HLA-DR-DQ alleles and HLA-DP alleles are independently associated with susceptibility to different stages of post-schistosomal hepatic fibrosis in the Chinese population. Tissue Antigens 53: 269-274.
17. Waine, G. J., A. G. Ross, G. M. Williams, A. C. Sleigh, and D. P. McManus. 1998. HLA class II antigens are associated with resistance or susceptibility to hepatosplenic disease in a Chinese population infected with Schistosoma japonicum. Int. J. Parasitol. 28: 537-542.
18. McManus, D. P., A. G. Ross, G. M. Williams, A. C. Sleigh, P. Wiest, H. Erlich, E. Trachtenberg, W. Guanling, S. T. McGarvey, Y. S. Li, and G. J. Waine. 2001. HLA class II antigens positively and negatively associated with hepatosplenic schistosomiasis in a Chinese population. Int. J. Parasitol. 31: 674-680.
19. Secor, W. E., H. del Corral, M. G. dos Reis, E. A. Ramos, A. E. Zimon, E. P. Matos, E. A. Reis, T. M. do Carmo, K. Hirayama, R. A. David, et al. 1996. Association of hepatosplenic schistosomiasis with HLA-DQB1*0201. J. Infect. Dis. 174: 1131-1135.
20. May, J., P. G. Kremsner, D. Milovanovic, L. Schnittger, C. C. Loliger, U. Bienzle, and C. G. Meyer. 1998. HLA-DP control of human Schistosoma haematobium infection. Am. J. Trop. Med. Hyg. 59: 302-306.
21. Webster, M., A. J. Fulford, G. Braun, J. H. Ouma, H. C. Kariuki, J. C. Havercroft, K. Gachuhi, R. F. Sturrock, A. E. Butterworth, and D. W. Dunne. 1996. Human immunoglobulin E responses to a recombinant 22.6-kilodalton antigen from Schistosoma mansoni adult worms are associated with low intensities of reinfection after treatment. Infect. Immun. 64: 4042-4046.
22. Kabatereine, N. B., J. Kemijumbi, J. H. Ouma, H. C. Kariuki, J. Richter, H. Kadzo, H. Madsen, A. E. Butterworth, N. Ornbjerg, and B. J. Vennervald. 2004. Epidemiology and morbidity of Schistosoma mansoni infection in a fishing community along Lake Albert in Uganda. Trans. K. Soc. Trop. Med. Hyg. 98: 711-718.
23. Booth, M., B. J. Vennervald, H. Kadzo, F. Kazibwe, J. H. Ouma, K. Gachuhi, N. B. Kabatereine, and D. W. Dunne. 2004. Hepatosplenic morbidity in two neighbouring communities in Uganda with high levels of Schistosoma mansoni infection but very different durations of residence. Trans. K. Soc. Trop. Med. Hyg. 98: 125-136.
24. Katz, N., A. Chaves, and J. Pellegrino. 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev. Inst. Med. Trop. Sao Paulo 14: 397-400.
25. Erlich, H. A. 1989. HLA class II gene polymorphisms: DNA typing, evolution and relationship to disease susceptibility. In PCR Technology: Principles and Applications for DNA Amplifications. H. A. Erlich, ed. Stockton Press, New York, pp. 193-208.
26. Lundin, K. E., K. S. Ronningen, S. Aono, A. Spurkland, G. Gaudernack, G. Isshiki, and E. Thorsby. 1989. HLA-DQ antigens and DQ β amino acid 57 of Japanese patients with insulin-dependent diabetes mellitus: detection of a DRw8DQw8 haplotype. Tissue Antigens 34: 233-241.
27. Ronningen, K. S., T. Iwe, T. S. Halstensen, A. Spurkland, and E. Thorsby. 1989. The amino acid at position 57 of the HLA-DQ β chain and susceptibility to develop insulin-dependent diabetes mellitus. Hum. Immunol. 26: 215-225.
28. Kimura, A., and T. Sasazuki. 1993. Eleventh International Histocompatibility Workshop reference protocol for the HLA DNA-typing technique. In HLA. K. Tsuji, ed. Oxford University Press, Oxford, pp. 397-419.
29. Booth, M., J. K. Mwatha, S. Joseph, F. M. Jones, H. Kadzo, E. Ireri, F. Kazibwe, J. Kemijumbi, C. H. Kariuki, K. Gachuhi, et al. 2004. Peri-portal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFNγ, high TNFα or low RANTES, depending on age and gender. J. Immunol. 172: 1295-1303.
30. Singh, H., and G. P. Raghava. 2001. ProPred: prediction of HLA-DR binding sites. Bioinformatics 17: 1236-1237.
31. Butterworth, A. E., M. Capron, J. S. Cordingley, P. R. Dalton, D. W. Dunne, H. C. Kariuki, G. Kimani, D. Koech, M. Mugambi, J. H. Ouma, et al. 1985. Immunity after treatment of human schistosomiasis mansoni. II. Identification of resistant individuals, and analysis of their immune responses. Trans. R. Soc. Trop. Med. Hyg. 79: 393-408.
32. Roberts, M., A. E. Butterworth, G. Kimani, T. Kamau, A. J. Fulford, D. W. Dunne, J. H. Ouma, and R. F. Sturrock. 1993. Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect. Immun. 61: 4984-4993.
33. Joseph, S., F. M. Jones, G. Kimani, J. K. Mwatha, T. Kamau, F. Kazibwe, J. Kemijumbi, N. B. Kabatereine, M. Booth, H. C. Kariuki, et al. 2004. Cytokine production in whole blood cultures from a fishing community in an area of high endemicity for Schistosoma mansoni in Uganda: the differential effect of parasite worm and egg antigens. Infect. Immun. 72: 728-734.
34. Fitzsimmons, C. M., S. Joseph, F. M. Jones, C. M. Reimen, K. F. Hoffmann, F. Kazibwe, G. Kimani, J. K. Mwatha, J. H. Ouma, E. M. Tukahebwa, et al. 2004. Chemotherapy for schistosomiasis in Ugandan fishermen: treatment can cause a rapid increase in interleukin-5 levels in plasma but decreased levels of eosinophilia and worm-specific immunoglobulin E. Infect. Immun. 72: 4023-4030.
35. Khalife, J., D. W. Dunne, B. A. Richardson, G. Mazza, K. J. Thorne, A. Capron, and A. E. Butterworth. 1989. Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. J. Immunol. 142: 4422-4427.
36. Demeure, C. E., P. Rihet, L. Abel, M. Ouattara, A. Bourgois, and A. J. Dessein. 1993. Resistance to Schistosoma mansoni in humans: influence of the IgE/IgG4 balance and IgG2 in immunity to reinfection after chemotherapy. J. Infect. Dis. 168: 1000-1008.
37. Hagan, P. 1996. Immunity and morbidity in infection due to Schistosoma haematobium. Am. J. Trop. Med. Hyg. 55: 116-120.
38. Wachholz, P. A., and S. R. Durham. 2003. Induction of 'blocking' IgG antibodies during immunotherapy. Clin. Exp. Allergy 33: 1171-1174.
39. Mothes, N., M. Heinzkill, K. J. Drachenberg, W. R. Sperr, M. T. Krauth, Y. Majlesi, H. Semper, P. Valent, V. Niederberger, D. Kraft, and R. Valenta. 2003. Allergen-specific immunotherapy with a monophosphoryl lipid A-adjuvanted vaccine: reduced seasonally boosted immunoglobulin E production and inhibition of basophil histamine release by therapy-induced blocking antibodies. Clin. Exp. Allergy 33: 1198-1208.
40. Till, S. J., J. N. Francis, K. Noun-Aria, and S. R. Durham. 2004. Mechanisms of immunotherapy. J. Allergy Clin. Immunol. 113: 1025-1034.
41. Kimata, H., A. Yoshida, C. Ishioka, M. Fujimoto, I. Lindley, and K. Furusho. 1996. RANTES and macrophage inflammatory protein 1α selectively enhance immunoglobulin (IgE) and IgG4 production by human B cells. J. Exp. Med. 183: 2397-2402.
42. Lin, Y. C., C. C. Lu, H. J. Su, C. Y. Shen, H. Y. Lei, and Y. L. Guo. 2002. The association between tumor necrosis factor, HLA-DR alleles, and IgE-mediated asthma in Taiwanese adolescents. Allergy 57: 831-834.
43. Kim, Y. K., S. Y. Oh, H. B. Oh, B. J. Lee, J. W. Son, S. H. Cho, Y. Y. Kim, and K. U. Min. 2002. Positive association between HLA-DRB1*07 and specific IgE responses to purified major allergens of D. pteronyssinus (Der p 1 and Der p 2). Ann. Allergy Asthma Immunol. 88: 170-174.
44. Low, A. S., I. Azmy, N. Sharaf, C. Cannings, and A. G. Wilson. 2002. Association between two tumor necrosis factor intronic polymorphisms and HLA alleles. Eur. J. Immunogenet. 29: 31-34.
45. Abel, L., F. Demenais, A. Praia, A. E. Souza, and A. Dessein. 1991. Evidence for the segregation of a major gene in human susceptibility/resistance to infection by Schistosoma mansoni. Am. J. Hum. Genet. 48: 959-970.
46. Zinn-Justin, A., S. Marquet, D. Hillaire, A. Dessein, and L. Abel. 2001. Genome search for additional human loci controlling infection levels by Schistosoma mansoni. Am. J. Trop. Med. Hyg. 65: 754-758.
47. Hohler, T., C. U. Meyer, A. Notghi, B. Stradmann-Bellinghausen, P. M. Schneider, R. Starke, F. Zepp, R. Sanger, R. Clemens, K. H. Meyer zum Buschenfelde, and C. Rittner. 1998. The influence of major histocompatibility complex class II genes and T-cell Vβ repertoire on response to immunization with HBsAg. Hum. Immunol. 59: 212-218.
48. Thursz, M. R., D. Kwiatkowski, C. E. Allsopp, B. M. Greenwood, H. C. Thomas, and A. V. Hill. 1995. Association between an MHC class II allele and clearance of hepatitis B virus in the Gambia. N. Engl. J. Med. 332: 1065-1069.
49. Hohler, T., G. Gerken, A. Notghi, P. Knolle, R. Lubjuhn, H. Taheri, P. M. Schneider, K. H. Meyer zum Buschenfelde, and C. Rittner. 1997. MHC class II genes influence the susceptibility to chronic active hepatitis C. J. Hepatol. 27: 259-264.
50. Fanning, L. J., J. Levis, E. Kenny-Walsh, M. Whelton, K. O'Sullivan, and F. Shanahan. 2001. HLA class II genes determine the natural variance of hepatitis C viral load. Hepatology 33: 224-230.
51. Malhotra, U., S. Holte, S. Dutta, M. M. Berrey, E. Delpit, D. M. Koelle, A. Sette, L. Corey, and M. J. McElrath. 2001. Role for HLA class II molecules in HIV-1 suppression and cellular immunity following antiretroviral treatment. J. Clin. Invest. 107: 505-517.
52. Sastre-Garau, X., I. Cartier, N. Jourdan-Da Silva, P. De Cremoux, V. Lepage, and D. Charron. 2004. Regression of low-grade cervical intraepithelial neoplasia in patients with HLA-DRB1*13 genotype. Obstet. Gynecol. 104: 751-755.