Analysis of the 5q31-33 locus shows an association between single nucleotide polymorphism variants in the IL-5 gene and symptomatic infection with the human blood fluke, Schistosoma japonicum

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8366-8371

  Ellis, Magda K ^a,b   Zhen, Zhen Zhao ^b   Chen, Hong Gen ^c   Montgomery, Grant W ^b   Li, Yue Sheng ^a,d   McManus, Donald P ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c Jiangxi Provincial Institute of Parasitic Diseases   (China)

^d WORLD HEALTH ORGANIZATION   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5;

3' UNTRANSLATED REGION; ADULT; AGED; ARTICLE; DNA PURIFICATION; EXON; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE MAP; HUMAN; HUMAN GENOME; IMMUNE RESPONSE; INFECTION SENSITIVITY; INFLAMMATION; INTRON; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; REINFECTION; SAMPLING; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; SINGLE NUCLEOTIDE POLYMORPHISM; TREMATODIASIS; FEMALE; GENETIC PREDISPOSITION; GENETICS; HAPLOTYPE; IMMUNOLOGY; MALE;

3' UNTRANSLATED REGIONS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; INTERLEUKIN-5; LINKAGE DISEQUILIBRIUM; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; SCHISTOSOMIASIS JAPONICA;

EID: 40049105449     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8366     Document Type: Article

References (48)

1. Zhou, X. N., Q. W. Jiang, L. P. Sun, T. P. Wang, Q. B. Hong, G. M. Zhao, L. Y. Wen, Z. C. Ying, X. H. Wu, and D. D. Lin. 2005. Control and surveillance of schistosomiasis in China. Chin. J. Schisto. Contr. 17: 161-165.
2. Ross, A. G., D. Vickers, G. R. Olds, S. M. Shah, and D. P. McManus. 2007. Katayama syndrome. Lancet Infect. Dis. 7: 218-224.
3. Acosta, L. P., G. D. Aligui, W. U. Tiu, D. P. McManus, and R. M. Olveda. 2002. Immune correlate study on human Schistosoma japonicum in a well-defined population in Leyte, Philippines, I: assessment of 'resistance' versus 'susceptibility' to S. japonicum infection. Acta Trop. 84: 127-136.
4. Ellis, M. K., Y. Li, Z. Rong, H. Chen, and D. P. McManus. 2006. Familial aggregation of human infection with Schistosoma japonicum in the Poyang Lake region, China. Int. J. Parasitol. 36: 71-77.
5. Bethony, J., A. Gazzinelli, A. Lopes, W. Pereira, L. Alves-Oliveira, S. Williams-Blangero, J. Blangero, P. Loverde, and R. Correa-Oliveira. 2001. Genetic epidemiology of fecal egg excretion during Schistosoma mansoni infection in an endemic area in Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz 96 (Suppl.): 49-55.
6. Bethony, J., J. T. Williams, J. Blangero, H. Kloos, A. Gazzinelli, B. Soares-Filho, L. Coelho, L. Alves-Fraga, S. Williams-Blangero, P. T. Loverde, and R. Correa-Oliveira. 2002. Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. Am. J. Trop. Med. Hyg. 67: 336-343.
7. Abel, L., F. Demenais, A. Prata, 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.
8. Marquet, S., L. Abel, D. Hillaire, and A. Dessein. 1999. Full results of the genome-wide scan which localises a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Eur. J. Hum. Genet. 7: 88-97.
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. Muller-Myhsok, B., F. F. Stelma, F. Guisse-Sow, B. Muntau, T. Thye, G. D. Burchard, B. Gryseels, and R. D. Horstmann. 1997. Further evidence suggesting the presence of a locus, on human chromosome 5q31-q33, influencing the intensity of infection with Schistosoma mansoni. Am. J. Hum. Genet. 61: 452-454.
11. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15: 505-533.
12. Gause, W. C., J. F. Urban, Jr., and M. J. Stadecker. 2003. The immune response to parasitic helminths: insights from murine models. Trends Immunol/ 24: 269-277.
13. Cooper, P. J., M. E. Chico, C. Sandoval, I. Espinel, A. Guevara, M. W. Kennedy, J. F. Urban Jr., G. E. Griffin, and T. B. Nutman. 2000. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J. Infect. Dis. 182: 1207-1213.
14. Jackson, J. A., J. D. Turner, L. Rentoul, H. Faulkner, J. M. Behnke, M. Hoyle, R. K. Grencis, K. J. Else, J. Kamgno, M. Boussinesq, and J. E. Bradley. 2004. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J. Infect. Dis. 190: 1804-1811.
15. Jackson, J. A., J. D. Turner, L. Rentoul, H. Faulkner, J. M. Behnke, M. Hoyle, R. K. Grencis, K. J. Else, J. Kamgno, J. E. Bradley, and M. Boussinesq. 2004. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int. J. Parasitol. 34: 1237-1244.
16. Quinnell, R. J., D. I. Pritchard, A. Raiko, A. P. Brown, and M. A. Shaw. 2004. Immune responses in human necatoriasis: association between interleukin-5 responses and resistance to reinfection. J. Infect. Dis. 190: 430-438.
17. Turner, J. D., H. Faulkner, J. Kamgno, F. Cormont, J. Van Snick, K. J. Else, R. K. Grencis, J. M. Behnke, M. Boussinesq, and J. E. Bradley. 2003. Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J. Infect. Dis. 188: 1768-1775.
18. Al-Sherbiny, M., A. Osman, R. Barakat, H. El Morshedy, R. Bergquist, and R. Olds. 2003. In vitro cellular and humoral responses to Schistosoma mansoni vaccine candidate antigens. Acta Trop. 88: 117-130.
19. Leenstra, T., L. P. Acosta, H. W. Wu, G. C. Langdon, J. S. Solomon, D. L. Manalo, L. Su, M. Jiz, B. Jarilla, A. O. Pablo, et al. 2006. T-helper-2 cytokine responses to Sj97 predict resistance to reinfection with Schistosoma japonicum. Infect. Immun. 74: 370-381.
20. Kouriba, B., C. Chevillard, J. H. Bream, L. Argiro, H. Dessein, V. Arnaud, L. Sangare, A. Dabo, A. H. Beavogui, C. Arama, et al. 2005. Analysis of the 5q31-q33 locus shows an association between IL13-1055C/T IL-13-591A/G polymorphisms and Schistosoma haematobium infections. J. Immunol. 174: 6274-6281.
21. Ross, A. G., L. Yuesheng, A. S. Sleigh, L. Yi, G. M. Williams, W. Z. Wu, L. Xinsong, H. Yongkang, and D. P. McManus. 1997. Epidemiologic features of Schistosoma japonicum among fishermen and other occupational groups in the Dongting Lake region (Hunan Province) of China. Am. J. Trop. Med. Hyg. 57: 302-308.
22. Bugawan, T. L., D. B. Mirel, A. M. Valdes, A. Panelo, P. Pozzilli, and H. A. Erlich. 2003. Association and interaction of the IL4R, IL4, and IL13 loci with type 1 diabetes among Filipinos. Am. J. Hum. Genet. 72: 1505-1514.
23. He, J. Q., M. Chan-Yeung, A. B. Becker, H. Dimich-Ward, A. C. Ferguson, J. Manfreda, W. T. Watson, and A. J. Sandford. 2003. Genetic variants of the IL13 and IL4 genes and atopic diseases in at-risk children. Genes Immun. 4: 385-389.
24. Ohashi, J., I. Naka, J. Patarapotikul, H. Hananantachai, S. Looareesuwan, and K. Tokunaga. 2003. A single-nucleotide substitution from C to T at position -1055 in the IL-13 promoter is associated with protection from severe malaria in Thailand. Genes Immun. 4: 528-531.
25. Wang, M., Z. M. Xing, C. Lu, Y. X. Ma, D. L. Yu, Z. Yan, S. W. Wang, and L. S. Yu. 2003. A common IL-13 Arg130Gln single nucleotide polymorphism among Chinese atopy patients with allergic rhinitis. Hum. Genet. 113: 387-390.
26. Wei, C. L., W. Cheung, C. K. Heng, N. Arty, S. S. Chong, B. W. Lee, K. L. Puah, and H. K. Yap. 2005. Interleukin-13 genetic polymorphisms in Singapore Chinese children correlate with long-term outcome of minimal-change disease. Nephrol. Dial. Transplant. 20: 728-734.
27. Barrett, J. C., B. Fry, J. Maller, and M. J. Daly. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265.
28. Gabriel, S. B., S. F. Schaffner, H. Nguyen, J. M. Moore, J. Roy, B. Blumenstiel, J. Higgins, M. DeFelice, A. Lochner, M. Faggart, et al. 2002. The structure of haplotype blocks in the human genome. Science 296: 2225-2229.
29. Dutra, W. O., R. Correa-Oliveira, D. Dunne, L. F. Cecchini, L. Fraga, M. Roberts, A. M. Soares-Silveira, M. Webster, H. Yssel, and K. J. Gollob. 2002. Polarized Th2 like cells, in the absence of Th0 cells, are responsible for lymphocyte produced IL-4 in high IgE-producer schistosomiasis patients. BMC Immunol. 3: 8.
30. Fitzsimmons, C. M., T. J. Stewart, K. F. Hoffmann, J. L. Grogan, M. Yazdanbakhsh, and D. W. Dunne. 2004. Human IgE response to the Schistosoma haematobium 22.6 kDa antigen. Parasite Immunol. 26: 371-376.
31. McKenzie, G. J., P. G. Fallon, C. L. Emson, R. K. Grencis, and A. N. McKenzie. 1999. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J. Exp. Med. 189: 1565-1572.
32. Balzar, S., M. Strand, D. Rhodes, and S. E. Wenzel. 2007. IgE expression pattern in lung: relation to systemic IgE and asthma phenotypes. J. Allergy Clin. Immunol. 119: 855-862.
33. Holgate, S. T. 1999. The epidemic of allergy and asthma. Nature 402: B2-B4.
34. Kabesch, M., M. Depner, I. Dahmen, S. K. Weiland, C. Vogelberg, B. Niggemann, S. Lau, T. Illig, N. Klopp, U. Wahn, et al. 2007. Polymorphisms in eosinophil pathway genes, asthma and atopy. Allergy 62: 423-428.
35. Chiang, C. H., Y. C. Tang, M. W. Lin, and M. Y. Chung. 2007. Association between the IL-4 promoter polymorphisms and asthma or severity of hyperresponsiveness in Taiwanese. Respirology 12: 42-48.
36. Hosseini-Farahabadi, S., J. Tavakkol-Afshari, H. Rafatpanah, R. Farid Hosseini, and M. Khaje Daluei. 2007. Association between the polymorphisms of IL-4 gene promoter (-590C>T), IL-13 coding region (R130Q) and IL-16 gene promoter (-295T>C) and allergic asthma. Iran J. Allergy Asthma Immunol. 6: 9-14.
37. Nagarkatti, R., R. Kumar, S. K. Sharma, and B. Ghosh. 2004. Association of IL4 gene polymorphisms with asthma in North Indians. Int. Arch. Allergy Immunol. 134: 206-212.
38. Noguchi, E., M. Shibasaki, T. Arinami, K. Takeda, Y. Yokouchi, T. Kawashima, H. Yanagi, A. Matsui, and H. Hamaguchi. 1998. Association of asthma and the interleukin-4 promoter gene in Japanese. Clin. Exp. Allergy 28: 449-453.
39. Maier, L. M., J. M. Howson, N. Walker, G. P. Spickett, R. W. Jones, S. M. Ring, W. L. McArdle, C. E. Lowe, R. Bailey, F. Payne, et al. 2006. Association of IL13 with total IgE: evidence against an inverse association of atopy and diabetes. J. Allergy Clin. Immunol. 117: 1306-1313.
40. Sadeghnejad, A., W. Karmaus, S. Hasan Arshad, and S. Ewart. 2007. IL13 gene polymorphism association with cord serum immunoglobulin E. Pediatr. Allergy Immunol. 18: 288-292.
41. Medhat, A., M. Shehata, K. Bucci, S. Mohamed, A. D. Dief, S. Badary, H. Galal, M. Nafeh, and C. L. King. 1998. Increased interleukin-4 and interleukin-5 production in response to Schistosoma haematobium adult worm antigens correlates with lack of reinfection after treatment. J. Infect. Dis. 178: 512-519.
42. Rodrigues, V., Jr., K. Piper, P. Couissinier-Paris, O. Bacelar, H. Dessein, and A. J. Dessein. 1999. Genetic control of schistosome infections by the SM1 locus of the 5q31-q33 region is linked to differentiation of type 2 helper T lymphocytes. Infect. Immun. 67: 4689-4692.
43. Bierman, W. F., J. C. Wetsteyn, and T. van Gool. 2005. Presentation and diagnosis of imported schistosomiasis: relevance of eosinophilia, microscopy for OVA, and serology. J. Travel Med. 12: 9-13.
44. de Jesus, A. R., A. Silva, L. B. Santana, A. Magalhaes, A. A. de Jesus, R. P. de Almeida, M. A. Rego, M. N. Burattini, E. J. Pearce, and E. M. Carvalho. 2002. Clinical and immunologic evaluation of 31 patients with acute Schistosomiasis mansoni. J. Infect. Dis. 185: 98-105.
45. Bradley, J. E., and J. A. Jackson. 2004. Immunity, immunoregulation and the ecology of trichuriasis and ascariasis. Parasite Immunol. 26: 429-441.
46. Akagawa, H., A. Tajima, Y. Sakamoto, B. Krischek, T. Yoneyama, H. Kasuya, H. Onda, T. Hori, M. Kubota, T. Machida, et al. 2006. A haplotype spanning two genes. ELN and LIMK1, decreases their transcripts and confers susceptibility to intracranial aneurysms. Hum. Mol. Genet. 15: 1722-1734.
47. Bertram, L., M. Parkinson, M. B. McQueen, K. Mullin, M. Hsiao, R. Menon, T. J. Moscarillo, D. Blacker, and R. E. Tanzi. 2005. Further evidence for LBP-1c/CP2/LSF association in Alzheimer's disease families. J. Med. Genet. 42: 857-862.
48. Day, D. A., and M. F. Tuite. 1998. Post-transcriptional gene regulatory mechanisms in eukaryotes: an overview. J. Endocrinol. 157: 361-371.