Naturally occurring Toll-like receptor 11 (TLR11) and Toll-like receptor 12 (TLR12) polymorphisms are not associated with Toxoplasma gondii infection in wild wood mice

Infection, Genetics and Evolution

Volumn 26, Issue , 2014, Pages 180-184

  Morger, Jennifer ^a   Bajnok, Jaroslav ^b   Boyce, Kellyanne ^b   Craig, Philip S ^b   Rogan, Michael T ^b   Lun, Zhao Rong ^b,c   Hide, Geoff ^b   Tschirren, Barbara ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF SALFORD   (United Kingdom)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

Apodemus sylvaticus; Immunogenetics; Parasite resistance; Toll like receptors; Toxoplasma gondii; Zoonotic disease

Indexed keywords

TOLL LIKE RECEPTOR 11; TOLL LIKE RECEPTOR;

ANIMAL TISSUE; APODEMUS SYLVATICUS; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAPLOTYPE; HOST PARASITE INTERACTION; HOST RESISTANCE; INFECTION RESISTANCE; MALE; MOUSE; NATURAL POPULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TOLL LIKE RECEPTOR 11 GENE; TOLL LIKE RECEPTOR 12 GENE; TOXOPLASMOSIS; ANIMAL; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; MURINE; PARASITOLOGY; RODENT DISEASE; TOXOPLASMA;

ANIMALS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HAPLOTYPES; MOLECULAR SEQUENCE DATA; MURINAE; POLYMORPHISM, GENETIC; RODENT DISEASES; TOLL-LIKE RECEPTORS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

EID: 84902982385     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.05.032     Document Type: Article

References (65)

1. Abolins S.R., Pocock M.J.O., Hafalla J.C.R., Riley E.M., Viney M.E. Measures of immune function of wild mice, Mus musculus. Mol. Ecol. 2011, 20:881-892.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Alexopoulou L., Thomas V., Schnare M., Lobet Y., Anguita J., Schoen R.T., Medzhitov R., Fikrig E., Flavell R.A. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat. Med. 2002, 8:878-884.
4. Andrade W.A., Souza M.D., Ramos-Martinez E., Nagpal K., Dutra M.S., Melo M.B., Bartholomeu D.C., Ghosh S., Golenbock D.T., Gazzinelli R.T. Combined action of nucleic acid-sensing toll-like receptors and TLR11/TLR12 heterodimers imparts resistance to Toxoplasma gondii in mice. Cell Host Microbe 2013, 13:42-53.
5. Apanius V., Penn D., Slev P.R., Ruff L.R., Potts W.K. The nature of selection on the major histocompatibility complex. Crit. Rev. Immunol. 1997, 17:179-224.
6. Bajnok, J., Boyce, K., Rogan, M.T., Craig, P.S., Lun, Z.R., Hide, G., submitted. Prevalence of Toxoplasma gondii in localised populations of Apodemus sylvaticus is linked to population genotype not to population location. Parasitology.
7. Boyce K., Hide G., Craig P., Reynolds C., Hussain M., Bodell A., Bradshaw H., Pickles A., Rogan M. A molecular and ecological analysis of the trematode Plagiorchis elegans in the wood mouse Apodemus sylvaticus from a periaquatic ecosystem in the UK. J. Helminthol. 2013, 19:1-11.
8. Boyce K., Hide G., Craig P.S., Harris P.D., Reynolds C., Pickles A., Rogan M.T. Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). Parasitology 2012, 139:1630-1639.
9. Boysen P., Eide D.M., Storset A.K. Natural killer cells in free-living Mus musculus have a primed phenotype. Mol. Ecol. 2011, 20:5103-5110.
10. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., Bleharski J.R., Maitland M., Norgard M.V., Plevy S.E., Smale S.T., Brennan P.J., Bloom B.R., Godowski P.J., Modlin R.L. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999, 285:732-736.
11. Clement M., Posada D., Crandall K.a. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 2000, 9:1657-1659.
12. Drummond A.J., Ashton B., Cheung M., Heled J., Kearse M., Moir R., Stones-Havas S., Thierer T., Wilson A. Geneious v4.6 2009, (Available at http://www.geneious.com).
13. Fumagalli M., Pozzoli U., Cagliani R., Comi G.P., Riva S., Clerici M., Bresolin N., Sironi M. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J. Exp. Med. 2009, 206:1395-1408.
14. Garantziotis S., Hollingsworth J.W., Zaas A.K., Schwartz D.A. The effect of toll-like receptors and toll-like receptor genetics in human disease. Ann. Rev. Med. 2008, 59:343-359.
15. Gong J., Wei T., Zhang N., Jamitzky F., Heckl W.M., Rössle S.C., Stark R.W. TollML: a database of toll-like receptor structural motifs. J. Mol. Mod. 2010, 16:1283-1289.
16. Grigg M.E., Bonnefoy S., Hehl A.B., Suzuki Y., Boothroyd J.C. Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries. Science 2001, 294:161-165.
17. Grueber C.E., Wallis G.P., King T.M., Jamieson I.G. Variation at innate immunity toll-like receptor genes in a bottlenecked population of a New Zealand robin. PLoS ONE 2012, 7(9):e45011. 10.1371/journal.pone.0045011.
18. Haroon F., Ulrike H., Angenstein F., Goldschmidt J., Kreutzmann P., Lison H., Fischer K.D., Scheich H., Wetzel W., Schlüter D., Budinger E. Toxoplasma gondii actively inhibits neuronal function in chronically infected mice. PLoS ONE 2012, 7:e35516.
19. Hedrick P.W. Pathogen resistance and genetic variation at MHC loci. Evolution 2002, 56:1902-1908.
20. Hide G., Morley E.K., Hughes J.M., Gerwash O., Elmahaishi M.S., Elmahaishi K.H., Thomasson D., Wright E.A., Williams R.H., Murphy R.G., Smith J.E. Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitology 2009, 136:1877-1885.
21. Hill A.V.S. The genomics and genetics of human infectious disease susceptibility. Annu. Rev. Genomics Hum. Genet. 2001, 2:373-400.
22. Hodkova H., Kodym P., Flegr J. Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism?. Parasitology 2007, 134:1329-1337.
23. Hrdá S., Votýpka J., Kodym P., Flegr J. Transient nature of Toxoplasma gondii-induced behavioral changes in mice. J. Parasitol. 2000, 86:657-663.
24. Jackson J.A., Friberg I.M., Bolch L., Lowe A., Ralli C., Harris P.D., Behnke J.M., Bradley J.E. Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals. BMC Biol. 2009, 7. 10.1186/1741-7007-7-16.
25. Kaslow R.A., McNicholl J., Hill A.V.S. Genetic Susceptibility to Infectious Diseases 2008, Oxford University Press, New York.
26. Koblansky A.A., Jankovic D., Oh H., Hieny S., Sungnak W., Mathur R., Hayden M.S., Akira S., Sher A., Ghosh S. Recognition of profilin by toll-like receptor 12 is critical for host resistance to Toxoplasma gondii. Immunity 2013, 38:119-130.
27. Kucera K., Koblansky A.A., Saunders L.P., Frederick K.B., De La Cruz E.M., Ghosh S., Modis Y. Structure-based analysis of Toxoplasma gondii profilin: a parasite-specific motif is required for recognition by toll-like receptor 11. J. Mol. Biol. 2010, 403:616-629.
28. Li C., Corraliza I., Langhorne J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect. Immun. 1999, 67:4435-4442.
29. Maizels R.M., Nussey D.H. Into the wild: digging at immunology's evolutionary roots. Nat. Immunol. 2013, 14:879-883.
30. McConkey G.A., Martin H.L., Bristow G.C., Webster J.P. Toxoplasma gondii infection and behaviour: location, location, location?. J. Exp. Biol. 2013, 216:113-119.
31. Mukherjee S., Sarkar-Roy N., Wagener D.K., Majumder P.P. Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:7073-7078.
32. Pedersen A.B., Babayan S.A. Wild immunology. Mol. Ecol. 2011, 20:872-880.
33. Pifer R., Yarovinsky F. Innate responses to Toxoplasma gondii in mice and humans. Trends Parasitol. 2011, 27:388-393.
34. Peig J., Green A.J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 2009, 118:1883-1891.
35. Plattner F., Yarovinsky F., Romero S., Didry D., Carlier M.F., Sher A., Soldati-Favre D. Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 2008, 3:77-87.
36. R Development Core Team, 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: , ISBN 3-900051-07-0. http://www.R-project.org.
37. Raetz M., Kibardin A., Sturge C.R., Pifer R., Li H.Y., Burstein E., Ozato K., Larin S., Yarovinsky F. Cooperation of TLR12 and TLR11 in the IRF8-dependent IL-12 response to Toxoplasma gondii profilin. J. Immunol. 2013, 191:4818-4827.
38. Roach J.C., Glusman G., Rowen L., Kaur A., Purcell M.K., Smith K.D., Hood L.E., Aderem A. The evolution of vertebrate toll-like receptors. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9577-9582.
39. Rozen S., Skaletsky H.J. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000, 365-386. Humana Press, Totowa, NJ. S. Krawetz, S. Misener (Eds.).
40. Sackton T.B., Lazzaro B.P., Schlenke T.A., Evans J.D., Hultmark D., Clark A.G. Dynamic evolution of the innate immune system in Drosophila. Nat. Genet. 2007, 39:1461-1468.
41. Saeij J.P.J., Boyle J.P., Boothroyd J.C. Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol. 2005, 21:476-481.
42. Scanga C.A., Aliberti J., Jankovic D., Tilloy F., Bennouna S., Denkers E.Y., Medzhitov R., Sher A. Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J. Immunol. 2002, 168:5997-6001.
43. Stephens M., Smith N.J., Donnelly P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 2001, 68:978-989.
44. Tenter A.M., Heckeroth A.R., Weiss L.M. Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 2000, 30:1217-1258.
45. Texereau J., Chiche J.D., Taylor W., Choukroun G., Comba B., Mira J.P. The importance of toll-like receptor 2 polymorphisms in severe infections. Clin. Infect. Dis. 2005, 41:S408-S415.
46. Thomasson D., Wright E.A., Hughes J.M., Dodd N.S., Cox A.P., Boyce K., Gerwash O., Abushahma M., Lun Z.R., Murphy R.G., Rogan M.T., Hide G. Prevalence and co-infection of Toxoplasma gondii and Neospora caninum in Apodemus sylvaticus in an area relatively free of cats. Parasitology 2011, 138:1117-1123.
47. Tiffin P., Moeller D.A. Molecular evolution of plant immune system genes. Trends Genet. 2006, 22:662-670.
48. Tschirren B., Andersson A., Scherman K., Westerdahl H., Mittl P., Råberg L. Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population. Proc. R. Soc. B 2013, 280. 10.1098/rspb.2013.0364.
49. Tschirren B., Andersson M., Scherman K., Westerdahl H., Råberg L. Contrasting patterns of diversity and population differentiation at the innate immunity gene toll-like receptor 2 (TLR2) across populations of two sympatric rodent species. Evolution 2012, 66:720-731.
50. Tschirren B., Råberg L., Westerdahl H. Signatures of selection acting on the innate immunity gene toll-like receptor 2 (TLR2) during the evolutionary history of rodents. J. Evol. Biol. 2011, 24:1232-1240.
51. Turner A.K., Begon M., Jackson J.A., Bradley J.E., Paterson S. Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLoS Genet. 2011, 7:e1002343. doi:1002310.1001371/journal.pgen.1002343.
52. Turner A.K., Begon M., Jackson J.a., Paterson S. Evidence for selection at cytokine loci in a natural population of field voles (Microtus agrestis). Mol. Ecol. 2012, 21:1632-1646.
53. Turner A.K., Paterson S. Wild rodents as a model to discover genes and pathways underlying natural variation in infectious disease susceptibility. Parasite Immunol. 2013, 35:386-395.
54. Vyas A., Kim S.-K., Giacomini N., Boothroyd J.C., Sapolsky R.M. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:6442-6447.
55. Webster J.P. The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr. Bull. 2007, 33:752-756.
56. Webster J.P., McConkey G.A. Toxoplasma gondii-altered host behaviour: clues as to mechanism of action. Folia Parasitol. 2010, 57:95-104.
57. Wlasiuk G., Nachman M.W. Adaptation and constraint at toll-like receptors in primates. Mol. Biol. Evol. 2010, 27:2172-2186.
58. Woolhouse M.E.J., Webster J.P., Domingo E., Charlesworth B., Levin B.R. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 2002, 32:569-577.
59. Wooten R.M., Ma Y., Yoder R.A., Brown J.P., Weis J.H., Zachary J.F., Kirschning C.J., Weis J.J. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 2002, 168:348-355.
60. Worth A.R., Lymbery A.J., Thompson R.C.A. Adaptive host manipulation by Toxoplasma gondii: fact or fiction?. Trends Parasitol. 2013, 29:150-155.
61. Xiao J., Kannan G., Jones-Brando L., Brannock C., Krasnova I.N., Cadet J.L., Pletnikov M., Yolken R.H. Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience 2012, 206:39-48.
62. Yarovinsky F. Toll-like receptors and their role in host resistance to Toxoplasma gondii. Immunol. Lett. 2008, 119:17-21.
63. Yarovinsky F. Innate immunity to Toxoplasma gondii infection. Nat. Rev. Immunol. 2014, 14:109-121.
64. Yarovinsky F., Zhang D.K., Andersen J.F., Bannenberg G.L., Serhan C.N., Hayden M.S., Hieny S., Sutterwala F.S., Flavell R.A., Ghosh S., Sher A. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 2005, 308:1626-1629.
65. Zenner L., Darcy F., Capron A., Cesbron-Delauw M.F. Toxoplasma gondii: kinetics of the dissemination in the host tissues during the acute phase of infection of mice and rats. Exp. Parasitol. 1998, 90:86-94.