Genetic predisposition to helminthiasis

Abstract

Helminthes accompany human beings from the early period of the formation, there is a long-term coevolution between parasite and human, helminthes represent a major selective force for human immune genes. Data on genetic control of the intensity and clinical traits of helminthinfection in different populations, including results obtained by whole-genome studies are presented and concept of common genes of susceptibility to helminth infection and allergic diseases are discussed.

Keywords

Helminth / helminthiasis / Single Nucleotide Polymorphism / gene / genome scan / Immune Response

References

[1] Бычков В. Г., Сергиев В. П., Сабиров А. Х. и др., 2007. Молекулярно-генетические подходы в паразитологии (на примере описторхоза) // Мед. паразитол. Т. 2. С. 1–7.

[2] Ильинских Е. Н., 2002. Актуальные вопросы изучения проблемы описторхоза в Сибири // Бюллетень сибирской медицины. T. 1. C. 63–70.

[3] Лепехин А. В., Мефодиев В. В., Филатов В. Г., Бужак Н. С., 1992. Эпидемиология, клиника и профилактика описторхоза. Томск: Изд-во Том. ун-та. C. 232.

[4] Лукманова Г. И., Гумеров А. А., Билалов Ф. С. и др., 2008. Ассоциации генотипов гена CY1A1 с предрасположенностью к эхинококкозу, вызванному штаммом GL Echinicoccus granulosus // Мед. паразитол. Т. 3. С. 17–19.

[5] Лукманова Г. И., Комиссарова М. А., Гумеров А. А., Викторова Т. В, 2006. Полиморфизм генов глютатион-s-трансферазML и TL и риск заболевания детей эхинококкозом // Мед. паразитол. Т. 3. С. 15–18.

[6] Салтыкова И. В. Патогенетика иммунного ответа у больных бронхиальной астмой и описторхозом: автореф. дис.. на соиск. учен. степ. канд. мед. наук (03.02.07). СибГМУРосздрава. Томск, 2010. 20 с.

[7] Щербаков A. M., Монхе-Барредо П. А., 1989. Распределение антигенов системы HLA среди больных эхинококкозами // Мед. паразитол. Т. 6. С. 75.

[8] Abdel-Salam E., Abdel Khalik A., Abdel-Meguid A. et al., 1986. Association of HLA class I antigens (A1, B5, B8 and CW2) with disease manifestations and infection in human Schistosomiasis mansoni in Egypt // Tissue Antigens. Vol. 27. P. 142–146.

[9] Abel L., Demenais F., Prata A. et al., 1991. Evidence for the segregation of a major gene in human susceptibility / resistance to infection by Schistosoma mansoni // Am. J. Hum. Genet. Vol. 48. P. 959–970.

[10] Acevedo N., Mercado D., Vergara C. et al., 2009. Association between total immunoglobulin E and antibody responses to naturally acquired Ascarislum bricoides infection and polymorphisms of immune system-related LIG4, TNFSF13B and IRS2 genes // Clin. Exp. Immunol. Vol. 157. P.282–90.

[11] Ali M. M., ElghazaliG., MontgomeryS. M. et al., 2007. Fc gamma RIIa (CD32) polymorphism and onchocercal skin disease: implications for the development of severe reactive onchodermatitis (ROD) // Am. J. Trop. Med. Hyg. Vol. 77. P. 1074–1078.

[12] Azab M. E., Bishara S. A., Helmy H. et al., 2004. Association of some HLA-DRB1 antigens with Echinococcus granulosus specific humoral immune response // J. Egypt Soc. Parasitol. Vol. 34. — P. 183–96.

[13] Bethony J., Gazzinelli A., Lopes A. et al., 2001. Genetic epidemiology of fecal egg excretion during Schistosoma mansoni infection in an endemic area in Minas Gerais, Brazil. // Mem Inst. Oswaldo. Cruz. Vol. 96. P. 49–55.

[14] Bethony J., Williams J. T., Blangero J. et al., 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. Vol. 67. — P. 336–343.

[15] Bin Dajem S. M., Mostafa O. M., El-Said F. G., 2008. Susceptibility of two strains of mice to the infection with Schistosoma mansoni: parasitological and biochemical studies // Parasitol Res. Vol. 103. — P. 1059–1063.

[16] Buvanendran V., Sooriyamoorthy T., Ogunsusi R. A., Adu I. F., 1981. Haemoglobin polymorphism and resistance to helminths in Red Sokoto goats // Trop Anim. Health Prod. Vol. 13. P. 217–221.

[17] Chan L., Bundy D. A. P., Kan S. P., 1994. Aggregation and predisposition to Ascaris lumbricoides and Trichuri strichiura at the familial level // Transactions of the Royal Society of Tropical Medicine and Hygiene. Vol. 88. P. 46–48.

[18] Chevillard C., Moukoko C. E., Elwali N. E. et al. IFN-gamma polymorphisms (IFN-gamma +2109 and IFN-gamma +3810) are associated with severe hepatic fibrosis in human hepatic schistosomiasis (Schistosoma mansoni) //J. Immunol. Vol. 171. P. 5596–5601.

[19] Chiarella J. M., Goldberg A. C., Abel L. et al., 1998. Absence of linkage between MHC and a gene involved in susceptibility to human schistosomiasis // Braz. J. Med. Biol. Res. Vol. 31. P. 665–670.

[20] Choi E. H., Zimmerman P. A., Foster C. B. et al., 2001. Genetic polymorphisms in molecules of innate immunity and susceptibility to infection with Wuchereria bancrofti in South India // Genes. Immun. Vol. 2. — P. 248–53.

[21] Cooper P. J., Guevara A. E., Guderian R. H., 1993. Intestinal helminthiases in Ecuador: the relationship between prevalence, genetic, and socioeconomic factors // Rev. Soc. Bras. Med. Trop. Vol. 26. — P. 175–180.

[22] Cuenco K. T., Ottesen E. A., Williams S. A. et al., 2009. Heritable factors play a major role in determining host responses to Wuchereria bancrofti infection in an isolated South Pacific island population // J Infect Dis. Vol. 200. P. 1271–1278.

[23] Dawkins H. J., Windon R. G., Eagleson G. K., 1989. Eosinophil responses in sheep selected for high and low responsiveness to Trichostrongy luscolubriformis // J. Helminthol. Vol. 63. P. 302–306.

[24] Debrah A. Y., Batsa L., Albers A. et al., 2011. Transforming growth factor-β1 variant Leu10Pro is associated with both lack of microfilariae and differential microfilarial loads in the blood of persons infected with lymphatic filariasis // Hum. Immunol. Vol. 72. — P. 1143–1148.

[25] Dessein A., Chevillard C., Arnaud V. et al., 2009. Variants of CTGF are associated with hepatic fibrosis in Chinese, Sudanese, and Brazilians infected with schistosomes // J. Exp. Med. Vol. 206. P. 2321–2328.

[26] Dessein A. J., Hillaire D., Elwali N. E. et al., 1999. Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene // Am. J. Hum. Genet. Vol. 65. P. 709–721.

[27] Dessein A. J., Hillaire D., Elwali N. E. et al., 1999. Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene // Am. J. Hum. Genet. Vol. 65. P. 709–721.

[28] Eiermann T. H., Bettens F., Tiberghien P. et al., 1998. HLA and alveolar echinococcosis // Tissue Antigens. Vol. 52. P. 124–129.

[29] Ellis M. K., Raso G., Li Y. S. et al., 2007. Familial aggregation of human susceptibility to coand multiple helminth infections in a population from the Poyang Lake region, China // Int. J. Parasitol. Vol. 37. P. 1153–1161.

[30] Fanning M. M., Kazura J. W., 1983. Genetic association of murine susceptibility to Brugiamalayi microfilaraemia // Parasite. Immunol. Vol. 5. P. 305–316.

[31] Forrester J. E., Scott M. E., Bundy D. A., Golden M. H., 1990. Predisposition of individuals and families in Mexico to heavy infection with Ascarislum bricoides and Trichuri strichiura // Trans. R. Soc. Trop. Med. Hyg. Vol. 84. P. 272–276.

[32] Fumagalli M., Pozzoli U., Cagliani R. et al., 2009. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions // J. Exp. Med. Vol. 206, N 6. P. 1395–408.

[33] Garcia A., Abel L., Cot M. et al., 1999. Genetic epidemiology of host predisposition microfilaraemia in human loiasis // Trop. Med. Int. Health. Vol. 4. — P. 567–574.

[34] Gatlin M. R., Black C. L., Mwinzi P. N. et al., 2009. Association of the gene polymorphisms IFN-gamma +874, IL-13 –1055 and IL-4 –590 with patterns of reinfection with Schistosoma mansoni // PLoSNegl Trop Dis. Vol. 3. P. e375.

[35] Gibbens J. C., Harrison L. J., Parkhouse R. M., 1986. Immunoglobulin class responses to Taeniatae niaeformis in susceptible and resistant mice // Parasite Immunol. Vol. 8. P. 491–502.

[36] Hirayama K., Chen H., Kikuchi M. et al., 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. Vol. 53. P. 269–274.

[37] Hise A. G., Hazlett F. E., Bockarie M. J. et al., 2003. Polymorphisms of innate immunity genes and susceptibility to lymphatic filariasis // Genes. Immun. Vol. 4. P. 524–527.

[38] Holland C. V., Crompton D. W., Asaolu S. O. et al., 1992. A possible genetic factor influencing protection from infection with Ascarislum bricoides in Nigerian children // J. Parasitol. Vol. 78. P. 915–916.

[39] Idris Z. M., Miswan N., Muhi J. et al., 2011. Association of CTLA4 gene polymorphisms with lymphatic filariasis in an East Malaysian population // Hum Immunol. Vol. 72. P. 607–612.

[40] Ishii A. I., Sano M., 2004. Strain-dependent differences in susceptibility of mice to experimental Angiostrongy luscostaricensis infection // Am. J. Trop. Med. Hyg. Vol. 70. P. 57–62.

[41] Isnard A., Kouriba B., Doumbo O., Chevillard C., 2011. Association of rs7719175, located in the IL13 gene promoter, with Schistosoma haematobium infection levels and identification of a susceptibility haplotype // Genes Immun. Vol. 12. P. 31–39.

[42] Junpee A., Tencomnao T., Sanprasert V., Nuchprayoon S. 2010. Association between Toll-like receptor 2 (TLR2) polymorphisms and asymptomatic bancroftian filariasis // Parasitol Res. Vol. 107. — P. 807–816.

[43] Kariuki H. C., Mbugua G., Magak P. et al., 2001. Prevalence and familial aggregation of schistosomal liver morbidity in Kenya: evaluation by new ultrasound criteria // J Infect Dis. Vol. 183. P. 960–966.

[44] Kassim O. O., Ejezie G. C., 1982. ABO blood groups in malaria and schistosomiasis haematobium // Acta. Trop. Vol. 39. P. 179–184.

[45] Keller A. E., Leathers W. S., Knox J. C., 1937. The present status of hookworm infestation in North Carolina // Am. J. Hyg. Vol. 26. P. 437–454.

[46] King C. H., Blanton R. E., Muchiri E. M. et al., 1999. Low heritable component of risk for infection intensity and infection-associated disease in urinary schistosomiasis among Wadigo village populations in Coast Province, Kenya // Trop. Med. Int. Health. Vol. 4. P. 565–574.

[47] Kiper N., Gerçeker F., Utine E. et al., 2010. TAP1 and TAP2 gene polymorphisms in childhood cystic echinococcosis // Parasitol Int. Vol. 59. P. 283–285.

[48] Kouriba B., Chevillard C., Bream J. H. 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. Vol. 174. P. 6274–6281.

[49] Kroeze W. K., Tanner C. E., 1989. Echinococcusmultilocularis: Susceptibility and responses to infection in inbred mice // Int. J. Parasitol. Vol. 19. P. 199–205.

[50] Lammas D. A., Mitchell L. A., Wakelin D., 1990. Genetic influences upon eosinophilia and resistance in mice infected with Mesocestoi descorti // Parasitology. Vol. 101. P. 291–299.

[51] Marquet S., Abel L., Hillaire D. et al., 1996. Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33 // Nat. Genet. Vol. 14. P. 181–184.

[52] May J., Kremsner P. G., Milovanovic D., 1998. HLA-DP control of human Schistosoma haematobium infection // Am. J. Trop. Med. Hyg. Vol. 59. P. 302–306.

[53] McCallum H. I., 1990 Covariance in parasite burdens: the effect of predisposition to infection // Parasitology. Vol. 100. P. 153–159.

[54] Meyer C. G., Gallin M., Erttmann K. D. et al., 1994. HLA–D alleles associated with generalized disease, localized disease, and putative immunity in Onchocerca volvulus infection // Proc. Natl Acad. Sci. USA Vol. 91. P. 7515–7519.

[55] Meyrowitsch D. W., Simonsen P. E., Garred P. et al., 2010. Association between mannose-binding lectin polymorphisms and Wuchereria bancrofti infection in two communities in north-eastern Tanzania // Tropical Medicine and Hygiene. Vol. 82. P. 115–120.

[56] Moller M., Gravenor M. B., Roberts S. E. et al., 2007. Genetic haplotypes of Th-2 immune signalling link allergy to enhanced protection to parasitic worms // Hum. Mol. Genet.Vol. 16. P. 1828–1836.

[57] Müller-Myhsok B., Stelma F. F., Guissé-Sow F. et al., 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. Vol. 61. P. 452–454.

[58] Ndamba J., Gomo E., Nyazema N. et al., 1997. Schistosomiasis infection in relation to the ABO blood groups among school children in Zimbabwe // Ottesen E. A., Mendell N. R., MacQueen J. M. et al., 1981. Familial predisposition to filarial infection — not linked to HLA-A or-B locus specificities // Acta Trop. Vol. 38. P. 205–216.

[59] Ouf E. A., Ojurongbe O., Akindele A. A. et al., 2012. Ficolin-2 levels and FCN2 genetic polymorphisms as a susceptibility factor in schistosomiasis // J Infect Dis. Vol. 206. P. 562–570.

[60] Panda A. K., Sahoo P. K., Kerketta A. S. et al., 2011. Human lymphatic filariasis: genetic polymorphism of endothelin-1 and tumor necrosis factor receptor II correlates with development of chronic disease // J. Infect. Dis. Vol. 204. P.315–322.

[61] Parate P. N., Wang de Y., Chew F. T. et al., 2010. Linkage disequilibrium pattern in asthma candidate genes from 5q31-q33 in the Singapore Chinese population // Ann. Hum. Genet. Vol. 74. P. 137–45.

[62] Peisong G., Yamasaki A., Mao X. Q. et al., 2004. An asthma-associated genetic variant of STAT6 predicts low burden of ascaris worm infestation // Genes Immun. Vol. 5. P. 58–62.

[63] Pullan R.L, Bethony J.M, Geiger S. M. et al., 2010 Human helminth co-infection: no evidence of common genetic control of hookworm and Schistosoma mansoni infection intensity in a Brazilian community // Int. J. Parasitol. Vol. 1. P. 299–306.

[64] Ramsay C. E., Hayden C. M., Tiller K. J. et al., Association of polymorphisms in the beta2-adrenoreceptor gene with higher levels of parasitic infection // Rupert J., Quinnell., 2003. Genetics of susceptibility to human helminth infection // International Journal for Parasitology. Vol. 33. P. 1219–1231.

[65] StoreyN., Wakelin D., Behnke J. M., 1985. The genetic control of host responses to Dipetalonema viteae (Filarioidea) infections in mice // Parasite. immunology. Vol. 7. P. 349–58.

[66] Tangkawattana S., Kaewkes S., Pairojkul C. et al., 2008. Mutations of KRAS and TP53 in a minor proportion of Opisthorchis viverrini-associated cholangiocarcinomas in a hamster model // Asian. Pac. J. Cancer. Prev.Vol. 9. P. 101–106.

[67] Timmann C., van der Kamp E., Kleensang A. et al., 2008. Human genetic resistance to Onchocerca volvulus: evidence for linkage to chromosome 2p from an autosome-wide scan // J. Infect. Dis. Vol. 198. P. 427–33.

[68] Trangle K. L., Goluska M. J., O'Leary M. J., Douglas S. D., 1979. Distribution of blood groups and secretor status in schistosomiasis // Parasite Immunol. Vol. 1. P. 133–140.

[69] Williams J. T., Blangero J., 1999. Power of variance component linkage analysis to detect quantitative trait loci // Ann. Hum. Genet. Vol. 63. P. 545–563.

[70] Williams-Blangero S., VandeBerg J. L., Subedi J. et al., 2002. Genes on chromosomes 1 and 13 have significant effects on Ascaris infection // ProcNatlAcadSci U S A. Vol. 99. P. 5533–5538.

[71] Williams-Blangero S., Vandeberg J. L., Subedi J. et al., 2008. Two quantitative trait loci influence whipworm (Trichuri strichiura) infection in a Nepalese population // J. Infect. Dis. Vol. 197. P. 1198–1203.

[72] Yalcin E., Kiper N., Tan C. et al., 2010. The role of human leucocyte antigens in children with hydatid disease: their association with clinical condition and prognosis // Parasitol Res. Vol. 106. P. 795–800.

[73] Yazdanbakhsh M., Sartono E., Kruize Y. C. et al., 1995. HLA and elephantiasis in lymphatic filariasis // Hum. Immunol. Vol. 44. P. 58–61.

[74] Zhang S., Penfornis A., Harraga S. et al., 2003.Polymorphisms of the TAP1 and TAP2 genes in human alveolar echinococcosis // Eur. J. Immunogenet. Vol. 30. P. 133–139.

[75] Zinn-Justin A., Marquet S., Hillaire D. et al., 2001. Genome search for additional human loci controlling infection levels by Schistosoma mansoni // Am. J. Trop. Med. Hyg. Vol. 65. P. 754–758.

RIGHTS & PERMISSIONS

Saltykova I.V., Freydin M.B., Ogorodova L.M., Puzyrev V.P.