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Transcriptional immune response in mesenteric lymph nodes in pigs with different levels of resistance to Ascaris suum

Per Skallerup
  • Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
  • Animal Genetics, Bioinformatics and Breeding, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
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 / Peter Nejsum
  • Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
  • Animal Genetics, Bioinformatics and Breeding, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
  • Weitere Artikel des Autors:
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 / Susanna Cirera
  • Animal Genetics, Bioinformatics and Breeding, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
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 / Kerstin Skovgaard
  • Innate Immunology Group, National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, DK-1870 Frederiksberg C, Denmark
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  • De Gruyter OnlineGoogle Scholar
 / Christian B. Pipper
  • Department of Public Health, University of Copenhagen, Øster Farimagsgade 5, DK-1014 Copenhagen K, Denmark
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 / Merete Fredholm
  • Animal Genetics, Bioinformatics and Breeding, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
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 / Claus B. Jørgensen
  • Animal Genetics, Bioinformatics and Breeding, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
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  • De Gruyter OnlineGoogle Scholar
 / Stig M. Thamsborg
  • Korrespondenzautor
  • Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
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Online erschienen: 28.12.2016 | DOI: https://doi.org/10.1515/ap-2017-0017

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Abstract

A single nucleotide polymorphism on chromosome 4 (SNP TXNIP) has been reported to be associated with roundworm (Ascaris suum) burden in pigs. The objective of the present study was to analyse the immune response to A. suum mounted by pigs with genotype AA (n = 24) and AB (n = 23) at the TXNIP locus. The pigs were repeatedly infected with A. suum from eight weeks of age until necropsy eight weeks later. An uninfected control group (AA; n = 5 and AB; n = 5) was also included. At post mortem, we collected mesenteric lymph nodes and measured the expression of 28 selected immune-related genes. Recordings of worm burdens confirmed our previous results that pigs of the AA genotype were more resistant to infection than AB pigs. We estimated the genotype difference in relative expression levels in infected and uninfected animals. No significant change in expression levels between the two genotypes due to infection was observed for any of the genes, although IL-13 approached significance (P = 0.08; Punadjusted = 0.003). Furthermore, statistical analysis testing for the effect of infection separately in each genotype showed significant up-regulation of IL-13 (P<0.05) and CCL17 (P<0.05) following A. suum infection in the ‘resistant’ AA genotype and not in the ‘susceptible’ AB genotype. Pigs of genotype AB had higher expression of the high-affinity IgG receptor (FCGR1A) than AA pigs in both infected and non-infected animals (P = 1.85*10-11).

Keywords: Ascaris suum; pig; single nucleotide polymorphism; gene expression; qPCR; RT-qPCR; cytokine; TXNIP; immunity

References

  • Adugna S., Kebede Y., Moges F., Tiruneh M. 2007. Efficacy of mebendazole and albendazole for Ascaris lumbricoides and hookworm infections in an area with long time exposure for antihelminthes, Northwest Ethiopia. Ethiopian Medical Journal, 45, 301–306Google Scholar

  • Albers G.A., Gray G.D., Piper L.R., Barker J.S., Le Jambre L.F., Barger I.A. 1987. The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal for Parasitology, 17, 1355–1363Google Scholar

  • Andersen C.L., Jensen J.L., Orntoft T.F. 2004. Normalization of realtime quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research, 64, 5245–5250Google Scholar

  • Andronicos N., Hunt P., Windon R. 2010. Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongylus colubriformis and Haemonchus contortus. International Journal for Parasitology, 40, 417–429. CrossrefGoogle Scholar

  • Anthony R.M., Rutitzky L.I., Urban J.F., Jr., Stadecker M.J., Gause W.C. 2007. Protective immune mechanisms in helminth infection. Nature Reviews Immunology, 7, 975–987Google Scholar

  • Anthony R.M., Urban J.F., Jr, Alem F., Hamed H.A., Rozo C.T., Boucher J.L., et al. 2006. Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nature Medicine, 12, 955-960Google Scholar

  • Araujo R.N., Padilha T., Zarlenga D., Sonstegard T., Connor E.E., Van Tassel C., et al. 2009. Use of a candidate gene array to delineate gene expression patterns in cattle selected for resistance or susceptibility to intestinal nematodes. Veterinary Parasitology, 162, 106–115. CrossrefGoogle Scholar

  • Barger I.A. 1993. Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. International Journal for Parasitology, 23, 463–469Google Scholar

  • Burke M.L., McGarvey L., McSorley H.J., Bielefeldt-Ohmann H., McManus D.P., Gobert G.N. 2011. Migrating Schistosoma japonicum schistosomula induce an innate immune response and wound healing in the murine lung. Molecular Immunology, 49, 191–200. CrossrefGoogle Scholar

  • Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., et al. 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR 10.1373/clinchem.2008.112797Google Scholar

  • Cooper P.J., Figuieredo C.A. 2013. Immunology of Ascaris and immunomodulation. In: (Ed. C. V. Holland) Ascaris: The neglected parasite. Elsevier, London, 3-19Google Scholar

  • Dawson H., Solano-Aguilar G., Beal M., Beshah E., Vangimalla V., Jones E., et al. 2009. Localized Th1-, Th2, T regulatory cell, and inflammation-associated hepatic and pulmonary immune responses in Ascaris suum-infected swine are increased by retinoic acid. Infection and Immunity, 77, 2576–2587. CrossrefGoogle Scholar

  • Dawson H.D., Beshah E., Nishi S., Solano-Aguilar G., Morimoto M., Zhao A., et al. 2005. Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infection and Immunity, 73, 1116–1128Google Scholar

  • Else K.J., Hultner L., Grencis R.K. 1992. Cellular immune responses to the murine nematode parasite Trichuris muris. II. Differential induction of TH-cell subsets in resistant versus susceptible mice. Immunology, 75, 232–237Google Scholar

  • Geiger S.M., Jardim-Botelho A., Williams W., Alexander N., Diemert D.J., Bethony J.M. 2013. Serum CCL11 (eotaxin-1) and CCL17 (TARC) are serological indicators of multiple helminth infections and are driven by Schistosoma mansoni infection in humans. Tropical Medicine and International Health, 18, 750–760. CrossrefGoogle Scholar

  • Gossner A., Wilkie H., Joshi A., Hopkins J. 2013. Exploring the abomasal lymph node transcriptome for genes associated with resistance to the sheep nematode Teladorsagia circum- cincta. Veterinary Research, 44, 68. CrossrefGoogle Scholar

  • Gossner A.G., Venturina V.M., Shaw D.J., Pemberton J.M., Hopkins, J. 2012. Relationship between susceptibility of blackface sheep to Teladorsagia circumcincta infection and an inflammatory mucosal T cell response. Veterinary Research, 43, 26. CrossrefGoogle Scholar

  • Groenen M.A., Archibald A.L., Uenishi H., Tuggle C.K., Takeuchi Y., Rothschild M.F., et al. 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393–398. CrossrefGoogle Scholar

  • Gutiérrez-Gil B., Perez J., Alvarez L., Martinez-Valladares M., de la Fuente L.F., Bayon Y., et al. 2009. Quantitative trait loci for resistance to trichostrongylid infection in Spanish Churra sheep. Genetics Selection Evolution, 41, 46. CrossrefGoogle Scholar

  • Hanotte O., Ronin Y., Agaba M., Nilsson P., Gelhaus A., Horstmann R., et al. 2003. Mapping of quantitative trait loci controlling trypanotolerance in a cross of tolerant West African N’Dama and susceptible East African Boran cattle. Proceedings of the National Academy of Sciences U. S. A, 100, 7443–7448Google Scholar

  • Hartl D., Lee C.G., Da Silva C.A., Chupp G.L., Elias J.A. 2009. Novel biomarkers in asthma: Chemokines and chitinase-like proteins. Current Opinion in Allergy and Clinical Immunology, 9, 60–66. CrossrefGoogle Scholar

  • Hassan M., Good B., Hanrahan J.P., Campion D., Sayers G., Mulcahy G., Sweeney T. 2011a. The dynamic influence of the DRB1*1101 allele on the resistance of sheep to experimental Teladorsagia circumcincta infection. Veterinary Research, 42, 46. CrossrefGoogle Scholar

  • Hassan M., Hanrahan J.P., Good B., Mulcahy G., Sweeney T. 2011b. A differential interplay between the expression of Th1/Th2/Treg related cytokine genes in Teladorsagia circumcincta infected DRB1*1101 carrier lambs. Veterinary Research, 42, 45. CrossrefGoogle Scholar

  • Hindorff L.A., Sethupathy P., Junkins H.A., Ramos E.M., Mehta J.P., Collins F.S., Manolio T.A. 2009. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proceedings of the National Academy of Sciences U. S. A, 106, 9362–9367. CrossrefGoogle Scholar

  • Hothorn T., Bretz F., Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363. CrossrefGoogle Scholar

  • Ingham A., Reverter A., Windon R., Hunt P., Menzies M. 2008. Gastrointestinal nematode challenge induces some conserved gene expression changes in the gut mucosa of genetically resistant sheep. International Journal for Parasitology, 38, 431–442Google Scholar

  • Keiser J., Utzinger J. 2008. Efficacy of current drugs against soiltransmitted helminth infections: Systematic review and metaanalysis. Journal of the American Medical Association, 299, 1937–1948. CrossrefGoogle Scholar

  • LaPorte S.L., Juo Z.S., Vaclavikova J., Colf L.A., Qi X., Heller N.M., Keegan A.D., Garcia K.C. 2008. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell, 132, 259–272. CrossrefGoogle Scholar

  • Masure D., Vlaminck J., Wang T., Chiers K., Van den Broeck W., Vercruysse J., Geldhof P. 2013. A role for eosinophils in the intestinal immunity against infective Ascaris suum larvae. PLoS Neglected Tropical Diseases, 7, e2138CrossrefGoogle Scholar

  • Matika O., Pong-Wong R., Woolliams J.A., Bishop S.C. 2011. Confirmation of two quantitative trait loci regions for nematode resistance in commercial British terminal sire breeds. Animal, 5, 1149–1156. CrossrefGoogle Scholar

  • Nejsum P., Roepstorff A., Jorgensen C.B., Fredholm M., Göring H.H., Anderson T.J., Thamsborg S.M. 2009. High heritability for Ascaris and Trichuris infection levels in pigs. Heredity, 102, 357–364. CrossrefGoogle Scholar

  • Noyes H., Brass A., Obara I., Anderson S., Archibald A.L., Bradley D.G., et al. 2011. Genetic and expression analysis of cattle identifies candidate genes in pathways responding to Trypanosoma congolense infection. Proceedings of the National Academy of Sciences U. S. A, 108, 9304-9309. CrossrefGoogle Scholar

  • Oksanen A., Eriksen L., Roepstorff A., Ilsoe B., Nansen P., Lind P. 1990. Embryonation and infectivity of Ascaris suum eggs. A comparison of eggs collected from worm uteri with eggs isolated from pig faeces. Acta Veterinaria Scandinavica, 31, 393–398Google Scholar

  • Pernthaner A., Cole S.A., Morrison L., Hein W.R. 2005. Increased expression of interleukin-5 (IL-5), IL-13, and tumor necrosis factor alpha genes in intestinal lymph cells of sheep selected for enhanced resistance to nematodes during infection with Trichostrongylus colubriformis. Infection and Immunity, 73, 2175–2183Google Scholar

  • R Core Team 2013. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, AustriaGoogle Scholar

  • Reinemeyer C.R. 2012. Anthelmintic resistance in non-strongylid parasites of horses. Veterinary Parasitology, 185, 9–15. CrossrefGoogle Scholar

  • Roepstorff A., Eriksen L., Slotved H.C., Nansen, P. 1997. Experimental Ascaris suum infection in the pig: Worm population kinetics following single inoculations with three doses of infective eggs. Parasitology, 115, 443–452Google Scholar

  • Rozen S., Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology, 132, 365–386Google Scholar

  • Schaschl H., Aitman T.J., Vyse T.J. 2009. Copy number variation in the human genome and its implication in autoimmunity. Clinical and Experimental Immunology, 156, 12–16. CrossrefGoogle Scholar

  • Skallerup P., Nejsum P., Jorgensen C.B., Göring H.H., Karlskov-Mortensen P., Archibald A.L., et al. 2012. Detection of a quantitative trait locus associated with resistance to Ascaris suum infection in pigs. International Journal for Parasitology, 42, 383–391. CrossrefGoogle Scholar

  • Skallerup P., Thamsborg S.M., Jorgensen C.B., Enemark H.L., Yoshida A., Göring H.H., et al. 2014. Functional study of a genetic marker allele associated with resistance to Ascaris suum in pigs. Parasitology, 141, 777–787. CrossrefGoogle Scholar

  • Skovgaard K., Cirera S., Vasby D., Podolska A., Breum S.O., Durrwald R., et al. 2013. Expression of innate immune genes, proteins and microRNAs in lung tissue of pigs infected experimentally with influenza virus (H1N2). Innate Immunity, 19, 531–544. CrossrefGoogle Scholar

  • Slotved H.C., Barnes E.H., Eriksen L., Roepstorff A., Nansen P., Bjorn H. 1997. Use of an agar-gel technique for large scale application to recover Ascaris suum larvae from intestinal contents of pigs. Acta Veterinaria Scandinavica, 38, 207–212.Google Scholar

  • Steenhard N.R., Jungersen G., Kokotovic B., Beshah E., Dawson H.D., Urban J.F., Jr, et al. 2009. Ascaris suum infection negatively affects the response to a Mycoplasma hyopneumoniae vaccination and subsequent challenge infection in pigs. Vaccine 27, 5161–5169. CrossrefGoogle Scholar

  • Taylor M.D., van der Werf N., Maizels R.M. 2012. T cells in helminth infection: The regulators and the regulated. Trends in Immunology, 33, 181–189. CrossrefGoogle Scholar

  • Thamsborg S.M., Nejsum P., Mejer H. 2013. Impact of Ascaris suum in livestock. In: (Ed. C. V. Holland) Ascaris: The neglected parasite. Elsevier, London, 363–381Google Scholar

  • van der Poel C.E., Spaapen R.M., van de Winkel J.G., Leusen J.H. 2011. Functional characteristics of the high affinity IgG receptor, FcyRI. Journal of Immunology, 186, 2699–2704. CrossrefGoogle Scholar

  • Vlaminck J., Geldhof P. 2013. Diagnosis and control of ascariasis in pigs. In: (Ed. C. V. Holland) Ascaris: The neglected parasite. Elsevier, London, 395–425Google Scholar

  • Wakelin D. 1975. Genetic control of immune responses to parasites: Immunity to Trichuris muris in inbred and random-bred strains of mice. Parasitology 71, 51–60Google Scholar

  • Williams-Blangero S., VandeBerg J.L., Subedi J., Aivaliotis M.J., Rai D.R., Upadhayay R.P., et al. 2002. Genes on chromosomes 1 and 13 have significant effects on Ascaris infection. Proceedings of the National Academy of Sciences U. S. A, 99, 5533–5538Google Scholar

  • Williams-Blangero S., VandeBerg J.L., Subedi J., Jha B., Corrêa-Oliveira R., Blangero J. 2008. Localization of multiple quantitative trait loci influencing susceptibility to infection with Ascaris lumbricoides. The Journal of Infectious Diseases, 197, 66–71. CrossrefGoogle Scholar

  • Zaros L.G., Bricarello P.A., Amarante A.F., Rocha R.A., Kooyman F.N., De Vries E., Coutinho L.L. 2010. Cytokine gene expression in response to Haemonchus placei infections in Nelore cattle. Veterinary Parasitology, 171, 68–73. CrossrefGoogle Scholar

  • Zhu J., Yamane H., Paul W.E. 2010. Differentiation of effector CD4 T cell populations. Annual Review of Immunology, 28, 445–489. CrossrefGoogle Scholar

Artikelinformationen

Erhalten: 18.12.2015

Revidiert: 19.09.2016

Angenommen: 14.10.2016

Online erschienen: 28.12.2016

Erschienen im Druck: 01.03.2017

Quellenangabe: Acta Parasitologica, Band 62, Heft 1, Seiten 141–153, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0017.

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