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Identification of QTL affecting resistance/susceptibility to acute Actinobacillus pleuropneumoniae infection in swine

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Abstract

Actinobacillus pleuropneumoniae is among the most important pathogens worldwide in pig production. The agent can cause severe economic losses due to decreased performance, acute or chronic pleuropneumonia and an increased incidence of death. Therapeutics cannot be used in a sustainable manner, and vaccination is not always available, but discovering more about host defence and disease mechanisms might lead to new methods of prophylaxis. The aim of the present study was to detect quantitative trait loci (QTL) associated with resistance/susceptibility to A. pleuropneumoniae. Under controlled conditions, 170 F2 animals of a Hampshire/Landrace family, with known differences in founder populations regarding A. pleuropneumoniae resistance, were challenged with an A. pleuropneumoniae serotype 7 aerosol followed by a detailed clinical, radiographic, ultrasonographic, pathological and bacteriological examination. F2 pigs were genotyped with 159 microsatellite markers. Significant QTL were identified on Sus scrofa chromosomes (SSC) 2, 6, 12, 13, 16, 17 and 18. They explained 6–22 % of phenotypic variance. One QTL on SSC2 reached significance on a genome-wide level for five associated phenotypic traits. A multiple regression analysis revealed a combinatory effect of markers SWR345 (SSC2) and S0143 (SSC12) on Respiratory Health Score, Clinical Score and the occurrence of death. The results indicate the genetic background of A. pleuropneumoniae resistance in swine and provide new insights into the genetic architecture of resistance/susceptibility to porcine pleuropneumonia. The results will be helpful in identifying the underlying genes and mechanisms.

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References

  • Aschard H, Bouzigon E, Corda E, Ulgen A, Dizier MH, Gormand F, Lathrop M, Kauffmann F, Demenais F, EGEA Cooperative Group (2009) Sex-specific effect of IL9 polymorphisms on lung function and polysensitization. Genes Immun 10:559–565

    Google Scholar 

  • Baltes N, Topitak W, Gerlach GF, Hennig-Pauka I, Hoffmann-Moujahid M, Ganter M, Rothkotter HJ (2001) Actinobacillus pleuropneumoniae iron transport and urease activity: effects on bacterial virulence and host immune response. Infect Immun 69:472–478

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baltes N, Hennig-Pauka I, Jacobsen I, Gruber AD, Gerlach GF (2003a) Identification of dimethyl sulfoxide reductase in Actinobacillus pleuropneumoniae and its role in infection. Infect Immun 71:6784–6792

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baltes N, Tonpitak W, Hennig-Pauka I, Gruber AD, Gerlach GF (2003b) Actinobacillus pleuropneumoniae serotype 7 siderophore receptor FhuA is not required for virulence. FEMS Microbiol Lett 220:41–48

    Article  CAS  PubMed  Google Scholar 

  • Boddicker N, Rowland R, Lunney JK, Garrick DJ, Reecy J, Dekkers JCM (2012) A major QTL associated with host response to porcine reproductive and respiratory syndrome virus challenge. J Anim Sci 90:1733–1746

    Article  CAS  PubMed  Google Scholar 

  • Casanova JL, Holland SM, Notarangelo LD (2012) Inborn errors of human JAKs and STATs. Immunity 36:515–528

    Google Scholar 

  • Chiers K, De Waele T, Pasmans F, Ducatelle R, Hasebrouck F (2010) Virulence factors of Actinobacillus pleuropneumoniae involved in colonization, persistence and induction of lesions in its porcine host. Vet Res 41:65

    Google Scholar 

  • Cho WS, Jung K, Kim J, Ha Y, Chae C (2005) Expression of mRNA encoding interleukin (IL)-10, IL-12p35 and IL-12p40 in lungs from pigs experimentally infected with Actinobacillus pleuropneumoniae. Vet Res Commun 29:111–122

    Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cleveland-Nielsen A, Nielsen EO, Ersbol AK (2002) Chronic pleuritis in Danish slaughter pig herds. Prev Vet Med 55:121–135

    Article  CAS  PubMed  Google Scholar 

  • Danilowicz E, Martinez-Arias R, Dolf G, Singh M, Probst I, Tümmler B, Höltig D, Waldmann KH, Gerlach GF, Stanke F, Leeb T, The IRAS Consortium (2009) Characterization of the porcine transferrin gene (TF) and its association with disease severity following an experimental Actinobacillus pleuropneumoniae infection. Anim Genet 41:424–427

  • Dreyfus A, Schaller A, Nivollet S, Segers RPAM, Kobisch M, Mieli L, Soerensen V, Hussy D, Miserez R, Zimmermann W, Inderbitzin F, Frey J (2004) Use of recombinant ApxIV in serodiagnosis of Actinobacillus pleuropneumoniae infections, development and prevalidation of the Apx IV Elisa. Vet Microbiol 99:227–238

    Article  CAS  PubMed  Google Scholar 

  • Edfors-Lilja I, Wattrang E, Marklund L, Moller M, Andersson-Eklund L, Andersson L, Fossum C (1998) Mapping quantitative trait loci for immune capacity in the pig. J Immunol 161:829–835

    CAS  PubMed  Google Scholar 

  • Fenwick B, Henry S (1994) Porcine pleuropneumonia. J Am Vet Med Assoc 204:1334–1340

    CAS  PubMed  Google Scholar 

  • Gottschalk M, Taylor DJ (2006) Actinobacillus pleuropneumoniae. In: Taylor DJ, Straw BE, Zimmermann JJ, D′Allaire S (eds) Diseases of swine. Blackwell Publishing, Ames, pp 563–576

    Google Scholar 

  • Green P, Falls K, Crooks S (1990) Documentation for CRI-MAP, version 2.4. Washington University School of Medicine, St. Louis

    Google Scholar 

  • Gregersen VR, Sørensen KK, Christensen OF, Busch ME, Vingborg RKK, Velander IH, Lund MS, Bendixen C (2010) Identification of QTL for dorso-caudal chronic pleuritis in 12 crossbred porcine families. Anim Genet 41:509–514

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Martín CB, García Del Blanco N, Blanco M, Navas J, Rodríguez-Ferri EF (2006) Changes in antimicrobial susceptibility of Actinobacillus pleuropneumoniae isolated from pigs in Spain during the last decade. Vet Microbiol 115:218–222

    Article  PubMed  Google Scholar 

  • Haesebrouck F, Chiers K, Van Overbeke I, Ducatelle R (1997) Actinobacillus pleuropneumoniae infections in pigs: the role of virulence factors in pathogenesis and protection. Vet Microbiol 58:239–249

    Article  CAS  PubMed  Google Scholar 

  • Haley CS, Andersson L (1997) Linkage mapping of quantitative trait loci in plants and animals. In: Dear PH (ed) Genome mapping. IRL Press, Oxford, pp 49–71

    Google Scholar 

  • Haley CS, Knott SA, Elsen J-M (1994) Mapping quantitative trait loci in crosses between outbred lines using least squares. Genetics 136:1195–1207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hannan PC, Bhogal BS, Fish JP (1982) Tylosin tartrate and tiamutilin effects on experimental piglet pneumonia induced with pig lung homogenate containing mycoplasmas, bacteria and viruses. Res Vet Sci 33:76–88

    CAS  PubMed  Google Scholar 

  • Higgins R, Lariviere S, Mittal KR, Martineau GP, Rousseau P, Cameron J (1985) Evaluation of a killed vaccine against porcine pleuropneumoniae due to Haemophilus pleuropneumoniae. Can Vet J 26:86–89

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoeltig D, Hennig-Pauka I, Thies K, Rehm T, Beyerbach M, Strutzberg-Minder K, Gerlach GF, Waldmann KH, FUGATO-consortium IRAS (2009) A novel Respiratory Health Score (RHS) supports a role of acute lung damage and pig breed in the course of an Actinobacillus pleuropneumoniae infection. BMC Vet Res 5:14

    Article  PubMed Central  PubMed  Google Scholar 

  • Holl JW, Cassady JP, Johnson RK (2004) A genome scan for quantitative trait loci and imprinted regions affecting reproduction in pigs. J Anim Sci 82:3421–3429

    CAS  PubMed  Google Scholar 

  • Jacobsen MJ, Nielsen JP (1995) Development and evaluation of a selective and indicative medium for isolation of Actinobacillus pleuropneumoniae. Vet Microbiol 47:191–197

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen MJ, Nielsen JP, Nielsen R (1996) Comparison of virulence of different Actinobacillus pleuropneumoniae serotypes and biotypes using an aerosol infection model. Vet Microbiol 49:159–168

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen I, Hennig-Pauka I, Baltes N, Trost M, Gerlach GF (2005) Enzymes involved in anaerobic respiration appear to play a role in Actinobacillus pleuropneumoniae virulence. Infect Immun 73:226–234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jirawattanapong P, Stockhofe-Zurwieden N, van Leengoed L, Wisselink H, Raymakers R, Cruijsen T, van der Peet-Schwering C, Nielen M, van Nes A (2008) Pleuritis in slaughter pigs: relations between lung lesions and bacteriology in 10 herds with high pleuritis. Res Vet Sci 88:11–15

    Article  Google Scholar 

  • Leiner G, Franz B, Strutzberg K, Gerlach GF (1999) A novel enzymelinked immunosorbent assay using the recombinant Actinobacillus pleuropneumoniae ApxII antigen for diagnosis of pleuropneumonia in pig herds. Clin Diagn Lab Immunol 6:630–632

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lu X, Fu WX, Luo YR, Ding XD, Zhou JP, Liu Y, Liu JF, Zhang Q (2012) Genome-wide association study for T lymphocyte subpopulations in swine. Genomics 13:488

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lunney JK, Steibel JP, Reecy JM, Fritz E, Rothschild MF, Kerrigan M, Trible B, Rowland RRR (2011) Probing genetic control of swine responses to PRRSV infection: current progress of the PRRS host genetics consortium. BMC Proc 5(Suppl 4):30

    Article  Google Scholar 

  • Maas A, Meens J, Baltes N, Hennig-Pauka I, Gerlach GF (2006) Development of a DIVA subjunit vaccine against Actinobacillus pleuropneumoniae infection. Vaccine 24:7226–7237

    Article  CAS  PubMed  Google Scholar 

  • Noyes EP, Feeney D, Pijoan C (1990) Comparison of the effect of pneumonia detected during lifetime with pneumonia detected at slaughter on growth in swine. J Am Vet Med Assoc 197:1025–1029

    CAS  PubMed  Google Scholar 

  • Ramos AM, Crooijmans RPMA, Affara NA, Amaral AJ, Archibald AL et al (2009) Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS One 4:e6524. doi:10.1371/journal.pone.0006524

    Article  PubMed Central  PubMed  Google Scholar 

  • Reiner G (2009) Investigations on genetic disease resistance in swine—a contribution to the reduction of pain, suffering and damage in farm animals. Appl Anim Behav Sci 118:217–221

    Article  Google Scholar 

  • Reiner G, Melchinger E, Kramarova M, Pfaff E, Büttner M, Saalmüller A, Geldermann H (2002) Detection of quantitative trait loci for resistance/susceptibility to the pseudorabies virus in swine. J Gen Virol 83:167–172

    CAS  PubMed  Google Scholar 

  • Reiner G, Kliemt D, Willems H, Berge T, Fischer R, Köhler F, Hepp S, Hertrampf B, Daugschies A, Geldermann H, Mackenstedt U, Zahner H (2007) Mapping of quantitative trait loci affecting resistance/susceptibility to Sarcocystis miescheriana in swine. Genomics 89:638–646

    Article  CAS  PubMed  Google Scholar 

  • Reiner G, Fischer R, Hepp S, Berge T, Köhler F, Willems H (2008) Quantitative trait loci for white blood cell numbers in swine. Anim Genet 39:163–168

    Google Scholar 

  • Seaton G, Hernandez J, Grunchec JA, White I, Allen J, De Koning DJ, Wei W, Berry D, Haley C, Knott S (2006) GridQTL: a grid portal for QTL mapping of compute intensive datasets. Proceedings of the 8th world congress on genetics applied to livestock production, Belo Horizonte, Brazil, 13–18 Aug 2006

  • Shao M, Wang Y, Wang C, Guo Y, Peng Y, Liu J, Li G, Liu H, Liu S (2010) Evaluation of multicomponent recombinant vaccines against Actinobacillus pleuropneumoniae in mice. Acta Veterinaria Scand 52:52

    Article  Google Scholar 

  • Sjölund S, Wallgren P (2010) Field experience with two different vaccination strategies aiming to control infections with Actinobacillus pleuropneumoniae in a fattening pig herd. Acta Vet Scand 52:23

    Article  PubMed Central  PubMed  Google Scholar 

  • Sorensen KK, Gregersen VR, Christensen OF, Velander IH, Bendixen C (2011) Genomic regions associated with ventro-cranial chronic pleuritis in pig. Anim Breed Genet 128:314–318

    Article  CAS  Google Scholar 

  • Spindel J, Wright M, Chen C, Cobb J, Gage J, Harrington S, Lorieux M, Ahmadi N, McCouch S (2013) Bridging the genotyping gap: using genotyping by sequencing (GBS) to add high-density SNP markers and new value to traditional bi-parental mapping and breeding populations. Theor Appl Genet 126:2699–2716

    Article  CAS  PubMed  Google Scholar 

  • Tonpitak W, Baltes N, Hennig-Pauka I, Gerlach GF (2002) Construction of an Actinobacillus pleuropneumoniae serotype 2 prototype live negative-marker vaccine. Infect Immun 70:7120–7125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsai TH, Chen SF, Huang TY, Tzeng CF, Chiang AS, Kou YR, Lee TS, Shyue SK (2011) Impaired CD14 and CD36 expression, bacterial clearance, and Toll-like receptor 4YMYD88 signaling in Caveolin-1Y deleted macrophages and mice. Shock 35:92–99

    Google Scholar 

  • Tumamao JQ, Bowles RE, van den Bosch H, Klaasen HL, Fenwick BW, Storie GJ, Blackall PJ (2004) Comparison of the efficacy of a subunit and a live streptomycin-dependent porcine pleuropneumonia vaccine. Aust Vet J 82:370–374

    Article  CAS  PubMed  Google Scholar 

  • Uddin MJ, Cinar MU, Große-Brinkhaus C, Tesfaye D, Tholen E, Juengst H, Looft C, Wimmers K, Phatsara C, Schellander K (2011) Mapping quantitative trait loci for innate immune response in the pig. Int J Immunogenet 36:121–131

    Article  Google Scholar 

  • Van Oirschot JT (1994) Vaccination in food animal populations. Vaccine 12:415–418

    Article  PubMed  Google Scholar 

  • White DG, Zhao S, Simjee S, Wagner DD, McDermott PF (2002) Antimicrobial resistance of food born pathogens. Microbes Infect 4:405–412

    Article  CAS  PubMed  Google Scholar 

  • Wimmers K, Jonas E, Schreinemachers HJ, Tesfaye D, Ponsuksili S, Tholen E, Juengst H, Schellander K, Phatsara C (2008a) Verification of chromosomal regions affecting the innate immunity in pigs using linkage mapping. Dev Biol (Basel) 132:279–283

    CAS  Google Scholar 

  • Wimmers K, Murani E, Schellander K, Ponsuksili S (2008b) QTL for traits related to humoral immune response estimated from data of a porcine F2 resource population. Int J Immunogenet 36:141–151

    Article  Google Scholar 

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Acknowledgments

The authors thank the German Ministry of Education and Research (BMBF) and the Development Association for Biotechnology (FBF) for financial support.

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Authors and Affiliations

  1. Department of Veterinary Clinical Sciences, Justus-Liebig-University, Frankfurter Strasse 112, 35392, Giessen, Germany

    Gerald Reiner, Natalie Bertsch & Hermann Willems

  2. Clinic of Swine and Small Ruminants, Forensic Medicine and Ambulatory Service, University of Veterinary Medicine, Bischofsholer Damm 15, 30173, Hannover, Germany

    Doris Hoeltig & Karl Heinz Waldmann

  3. Department of Infectious Diseases, Institute for Microbiology, University of Veterinary Medicine Hannover Foundation, Bischofsholer Damm 15, 30173, Hannover, Germany

    Martin Selke

  4. Department of Pediatrics, Hannover Medical School (MHH), Carl-Neuberg-Strasse 1, 30625, Hannover, Germany

    Burkhard Tuemmler & Inga Probst

  5. Department of Vertebrate Genomics, Max-Planck Institute for Molecular Genetics Berlin (MPI-MG), Ihnestr. 73, 14195, Berlin, Germany

    Ralf Herwig

  6. ATLAS Biolabs GmbH, Friedrichstraße 147, 10117, Berlin, Germany

    Mario Drungowski

  7. Innovative Veterinary Diagnostics LTD (IVD), Heisterbergallee 12, 30453, Hannover, Germany

    Gerald Friedrich Gerlach

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  1. Gerald Reiner
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  2. Natalie Bertsch
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Correspondence to Gerald Reiner.

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Reiner, G., Bertsch, N., Hoeltig, D. et al. Identification of QTL affecting resistance/susceptibility to acute Actinobacillus pleuropneumoniae infection in swine. Mamm Genome 25, 180–191 (2014). https://doi.org/10.1007/s00335-013-9497-4

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