Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-28T11:46:18.589Z Has data issue: false hasContentIssue false

Pig peripheral blood mononuclear leucocyte subsets are heritable and genetically correlated with performance

Published online by Cambridge University Press:  01 November 2008

M. Clapperton*
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Roslin Biocentre, Midlothian EH25 9PS, UK
E. J. Glass
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Roslin Biocentre, Midlothian EH25 9PS, UK
S. C. Bishop
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Roslin Biocentre, Midlothian EH25 9PS, UK
Get access

Abstract

Indicator traits used to select pigs for increased resistance to infection or improved health must be heritable and, preferably, be associated with improved performance. We estimated the heritability of a range of immune traits and their genetic and phenotypic correlations with growth performance. We measured immune traits on 589 pigs and performance on 1941 pigs from six farms, three of which were classified as ‘high health status’ (i.e. specific pathogen-free) and three were of lower health status. All pigs were apparently healthy. Immune traits were total white blood cells (WBC), and peripheral blood mononuclear leucocyte (PBML) subsets positive for CD4, CD8α, gamma delta (γδ) T cell receptor, CD11R1 (natural killer cell marker), B cell and monocyte markers at the start and the end of standard growth performance tests. At both time points, all immune traits were moderately to highly heritable except for CD8α+ cells. At end of test, heritability estimates (h2) (±s.e.) were 0.18 (±0.11) for total WBC count. For PBML subset proportions, the heritabilities were 0.52 (±0.14) for γδ TCR+ cells, 0.62 (±0.14) for CD4+ cells, 0.44 (±0.14) for CD11R1+ cells, 0.58 (±0.14) for B cells and 0.59 (±0.14) for monocytes. Farm health status affected the heritabilities for WBC, being substantially higher on lower health status farms, but did not have consistent effects on heritabilities for the PBML subsets. There were significant negative genetic correlations between numbers and proportions of various PBML subsets and performance, at both start and end of test. In particular, the proportion of PBML cells that were CD11R1+ cells, at end of test, was strongly correlated with daily gain (rg = −0.72; P < 0.01). There were also weaker but significant negative phenotypic correlations between PBML subsets measured at end of test and performance, for γδ+ T cells, CD8α+, CD11R1+ cells, B cells or monocytes. Phenotypic correlations with daily gain were generally lower at the start of test than at the end of test. These results show that most of the major pig PBML subsets are heritable, and that systemic levels of several of these PBML subsets are genetically negatively correlated with performance. This approach provides a basis for using immune trait markers when selecting boars that can produce higher-performing progeny.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmadi, KR, Hall, MA, Norman, P, Vaughan, RW, Snieder, H, Spector, TD, Lanchbury, JS 2001. Genetic determinism in the relationship between human CD4+ and CD8+ lymphocyte populations? Genes and Immunity 2, 381387.CrossRefGoogle Scholar
Cheeseman, JH, Kaiser, MG, Lamont, SJ 2004. Genetic line effect on peripheral blood leucocyte cell surface marker expression in chickens. Poultry Science 83, 911916.CrossRefGoogle ScholarPubMed
Chen, J, Harrison, DE 2002. Quantitative trait loci regulating relative lymphocyte proportions in mouse peripheral blood. Blood 99, 561566.CrossRefGoogle ScholarPubMed
Clapperton, M, Bishop, SC, Cameron, ND, Glass, EJ 2005a. Associations of weight gain and food intake with leucocyte sub-sets in Large White pigs. Livestock Production Science 96, 249260.CrossRefGoogle Scholar
Clapperton, M, Bishop, SC, Cameron, ND, Glass, EJ 2005b. Associations of acute phase protein levels with growth performance and with selection for growth performance in Large White pigs. Animal Science 81, 213220.CrossRefGoogle Scholar
Clapperton, M, Bishop, SC, Glass, EJ 2006. Selection for lean growth and food intake leads to correlated changes in innate immune traits in Large White pigs. Animal Science 82, 867876.CrossRefGoogle Scholar
Davis, WC, Haverson, K, Saalmuller, A, Yang, H, Lunney, JK, Hamilton, MJ, Pescovitz, MD 2001. Analysis of monoclonal antibodies with molecules expressed on gamma delta cells. Veterinary Immunology and Immunopathology 80, 5362.CrossRefGoogle Scholar
de Haan, G, Bystrykh, LV, Weersing, E, Dontje, B, Geiger, H, Ivanova, N, Lemischka, IR, Vellenga, E, Van Zant, G 2002. A genetic and genomic analysis identifies a cluster of genes associated with hematopoietic cell turnover. Blood 100, 20562062.CrossRefGoogle ScholarPubMed
Denham, S, Zwart, R, Whitall, JTD, Pampusch, M, Corteyn, AH, Bianchi, ATJ, Murtaugh, MP, Parkhouse, RME, Tlaksova, H, Sinkora, J, Sinkora, M, Rehakova, Z 1998. Monoclonal antibodies putatively recognising porcine B cells. Veterinary Immunology and Immunopathology 60, 317328.CrossRefGoogle Scholar
Denyer, MS, Wileman, TE, Stirling, CMA, Zuber, B, Takamatsu, HH 2006. Perforin expression can define CD8 positive lymphocyte subsets in pigs allowing phenotypic and functional analysis in natural killer, cytotoxic T, natural killer T and MHC un-restricted cytotoxic T-cells. Veterinary Immunology and Immunopathology 110, 279292.CrossRefGoogle ScholarPubMed
Duarte, N, Penta-Goncalves, C 2001. The MHC locus controls size variations in the CD4 compartment of the mouse thymus. Immunogenetics 53, 662668.CrossRefGoogle ScholarPubMed
Edfors-Lilja, I, Wattrang, E, Magnussen, U, Fossum, C 1994. Genetic variation in parameters reflecting immune competence of swine. Veterinary Immunology and Immunopathology 40, 116.CrossRefGoogle ScholarPubMed
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. Journal of Immunology 161, 829835.CrossRefGoogle ScholarPubMed
Eurell, TE, Bane, DP, Hall, WF, Schaeffer, DJ 1992. Serum haptoglobin concentration as an indicator of weight gain in pigs. Canadian Journal of Veterinary Research 56, 69.Google ScholarPubMed
Evans, DM, Frazer, IH, Martin, NG 1999. Genetic and environmental causes of variation in basal level of blood cells. Twin Research 2, 250257.CrossRefGoogle ScholarPubMed
Galina-Pantoja, L, Mellencamp, MA, Bastiaansen, J, Cabrera, R, Solano-Aguilar, G, Lunney, JK 2006. Relationship between immune cell phenotypes and pig growth in a commercial farm. Animal Biotechnology 17, 8198.CrossRefGoogle Scholar
Gheorgiou, M, Mouton, D, Lecoeur, H, Lagranderie, M, Mevel, JC, Biozzi, G 1985. Resistance of high and low antibody responder lines of mice to the growth of avirulent (BCG) and virulent (H37Rv) strains of mycobacteria. Clinical and Experimental Immunology 59, 177184.Google Scholar
Gilmour, AR, Cullis, BR, Welham, SJ, Thompson, R 2004. ASREML: program user manual. VSN International Ltd, Hemel Hempstead, UK.Google Scholar
Grellner, GF, Fangman, TJ, Carroll, JA, Wiedmeyer, CE 2002. Using serology in combination with acute phase proteins and cortisol to determine stress and immune function of early-weaned pigs. Journal of Swine Health and Production 10, 199204.Google Scholar
Hall, MA, Ahmadi, KR, Norman, P, Snieder, H, MacGregor, AJ, Vaughan, RW, Spector, TD, Lanchbury, JS 2000. Genetic influence on peripheral blood T lymphocyte levels. Genes and Immunity 1, 423427.CrossRefGoogle ScholarPubMed
Hall, MA, Norman, PJ, Thiel, B, Tiwari, H, Peiffer, A, Vaughan, RW, Prescott, S, Leppert, M, Schork, NJ, Lanchbury, JS 2002. Quantitative trait loci on chromosomes 1, 2, 3, 4, 8, 9, 11, 12 and 18 control variation in levels of T and B lymphocyte sub-populations. American Journal of Human Genetics 70, 11721182.CrossRefGoogle Scholar
Haverson, K, Bailey, M, Stokes, CR, Simon, A, LeFlufy, L, Banfield, G, Chen, Z, Hollemweguer, E, Ledbetter, JA 2001. Monoclonal antibodies raised to human cells – specificity for pig leucocytes. Veterinary Immunology and Immunopathology 80, 175186.CrossRefGoogle Scholar
Henryon, M, Berg, P, Jensen, J, Andersen, S 2001. Genetic variation for resistance to clinical and sub-clinical diseases exists in growing pigs. Animal Science 73, 375387.CrossRefGoogle Scholar
Henryon, M, Heegaard, PMH, Nielsen, J, Berg, P, Juul-Madsen, HR 2006a. Immunological traits have the potential to improve selection of pigs for resistance to clinical and sub-clinical disease. Animal Science 82, 597606.CrossRefGoogle Scholar
Henryon M, Sørenson P, Heegaard PMH, Nielsen J, Berg P and Juul-Madsen HR 2006b. Limited evidence that baseline levels of immunological traits provide useful selection criteria for resistance to clinical and sub-clinical disease in pigs. Proceedings of the 8th World Congress on Genetics Applied to Livestock Production, Communication 15-09.Google Scholar
Jayagopala Reddy, NR, Wilkie, BN, Borgs, P, Mallard, BA 2000. Cytokines in Mycoplasma hyorhinis-induced arthritis in pigs bred for high and low immune responses. Infection and Immunity 68, 11501155.CrossRefGoogle ScholarPubMed
Joling, P, Mok, KS, de Vries Relingh, G, Wever, PJ, Cornelis, RS, Oskam, JP, Henken, AM 1993. An evaluation of immune competence in different swine breeds. Veterinary Quarterly 15, 915.CrossRefGoogle ScholarPubMed
Lawes Agricultural Trust 1983. GENSTAT. A general statistical program. Numerical Algorithms Group. VSN International Ltd, Hemel Hempstead, UK.Google Scholar
Lee, WW, Nam, KN, Terao, K, Yoshikawa, Y 2003. Possible role of genetic factor(s) on age-related increase of peripheral CD4+CD8+ double positive T cells in cynomolgus monkeys. Experimental Animals 52, 309316.CrossRefGoogle ScholarPubMed
Lodoen, MB, Lanier, LL 2006. Natural killer cells as an initial defense against pathogens. Current Opinions in Immunology 18, 391398.CrossRefGoogle ScholarPubMed
Loeffen, WLA, Kamp, EM, Stockhofe-Zurwieden, N, van-Neiuwsadt, APKMI, Bongers, JH, Hunneman, WA, Elbers, WRW, Baars, J, Nell, T, van Zijderveld, FG 1999. Survey of infectious agents involved in acute respiratory disease in finishing pigs. Veterinary Record 145, 123129.CrossRefGoogle ScholarPubMed
Luhtala, M, Lassila, O, Toivanen, P, Vaino, O 1997. A novel peripheral CD4+CD8+ T cell population: inheritance of CD8α expression on CD4+ T cells. European Journal of Immunology 27, 189193.CrossRefGoogle ScholarPubMed
Lyons, DT, Freeman, AE, Kuck, AL 1991. Genetics of health traits in Holstein cattle. Journal of Dairy Science 74, 10921100.CrossRefGoogle ScholarPubMed
Mallard, BA, Wilkie, BN, Kennedy, BW 1989. Genetics and other effects on antibody and cell-mediated immune response in swine leucocyte antigen (SLA)-defined miniature pigs. Animal Genetics 20, 167178.CrossRefGoogle ScholarPubMed
Mallard BA, Wilkie BN, Kennedy BW, Gibson JP and Quinton MJ 1998. Immune responsiveness in swine, eight generations of selection for high and low immune response in Yorkshire pigs. Proceedings of the 6th World Congress on Genetics Applied to Livestock Production, vol. 27, pp. 257–264.Google Scholar
Morrison, SJ, Qian, D, Jerabek, L, Thiel, BA, Park, IK, Ford, PS, Kiel, MJ, Schork, NJ, Weissman, IJ, Clarke, MF 2002. A genetic determinant that specifically regulates the frequency of hematopoietic stem cells. Journal of Immunology 168, 635642.CrossRefGoogle ScholarPubMed
Myrick, C, DiGuisto, R, DeWolfe, J, Bowen, E, Kappler, J, Marrack, P, Wakeland, EK 2002. Linkage analysis of variations in CD4, CD8 T cell sub-sets between C57BL/6 and DBA/2. Genes and Immunity 3, 144150.CrossRefGoogle Scholar
Ober, BT, Summerfield, A, Mattlinger, C, Wiesmuller, KH, Jung, G, Pfaff, E, Saalmuller, A, Rzhia, HJ 1998. Vaccine-induced pseudorabies virus-specific extrathymic CD4+CD8+ memory T-helper cells in swine. Journal of Virology 72, 48664873.CrossRefGoogle ScholarPubMed
O’Connor, GM, Hart, OM, Gardiner, CM 2005. Putting the natural killer cell in its place. Immunology 117, 110.CrossRefGoogle Scholar
Pallarés, FJ, Gómez, S, Ramis, G, Seva, J, Muñoz, A 2000. Vaccination against swine enzootic pneumonia in field conditions: effect on clinical, pathological, zoo technical and economic parameters. Veterinary Research 31, 573582.CrossRefGoogle Scholar
Parra, MD, Fuentes, P, Tecles, F, Martínez-Subiela, S, Martínez, JS, Muñoz, A, Cerón, JJ 2006. Porcine acute phase concentrations in different diseases in field conditions. Journal of Veterinary Medicine Series B 53, 488493.CrossRefGoogle ScholarPubMed
Pedrini, SCB, Acorci, MJ, Pinto, JGG, Silveira, LVA, Oliveira, SL 2005. Immune response to the Rhodococcus equi infection in high and low antibody-producing mice (selection IV-A). Microbiology and Immunology 49, 915923.CrossRefGoogle Scholar
Petersen, HH, Ersboll, AK, Jensen, CS, Nielsen, JP 2002. Serum haptoglobin concentration in Danish slaughter pigs of different health status. Preventive Veterinary Medicine 54, 325335.CrossRefGoogle ScholarPubMed
Poppe, C, Smart, N, Khakhria, R, Johnson, W, Spika, J, Prescott, J 1998. Salmonella typhimurium DT104: a virulent and drug-resistant pathogen. Canadian Veterinary Journal 39, 559565.Google ScholarPubMed
Regula, G, Lichtensteiger, CA, Mateus-Pinilla, NE, Scherba, G, Miller, GY, Weigel, RM 2000. Comparison of serologic testing and slaughter evaluation for assessing the effects of sub-clinical infection on growth in pigs. Journal of American Veterinary Medical Association 217, 888895.CrossRefGoogle Scholar
Roberts, A, Foote, S, Alexander, WS, Scott, C, Robb, L, Metcalf, D 1997. Genetic influences determining progenitor cell mobilization and leukocytosis induced by granulocyte colony-stimulating factor. Blood 89, 27362744.CrossRefGoogle ScholarPubMed
Saalmuller, A, Kuebart, G, Hollemweguer, E, Chen, Z, Neilsen, J, Zuckermanm, F, Haverson, K 2001. Summary of workshop findings for porcine T-lymphocyte-specific monoclonal antibodies. Veterinary Immunology and Immunopathology 80, 3552.CrossRefGoogle ScholarPubMed
Segalés, J, Rosell, C, Domingo, M 2004. Pathological findings associated with naturally acquired porcine circovirus type 2 associated disease. Veterinary Microbiology 98, 137149.CrossRefGoogle ScholarPubMed
Snowder, GD, Van Vleck, LD, Cundiff, LV, Bennett, GL 2006. Bovine respiratory disease in feedlot cattle: environmental, genetic, and economic factors. Journal of Animal Science 84, 19992008.CrossRefGoogle ScholarPubMed
Spurlock, ME 1997. Regulation of metabolism and growth during immune challenge, an overview of cytokine function. Journal of Animal Science 75, 17731783.CrossRefGoogle ScholarPubMed
Tecles, F, Fuentes, P, Martínez-Subiela, S, Parra, MD, Muñoz, A, Cerón, JJ 2007. Analytical validation of commercially available methods for acute phase protein quantification in pigs. Research in Veterinary Science 83, 133139.CrossRefGoogle ScholarPubMed
Thacker, E, Summerfield, A, McCullough, K, Dominguez, J, Alonso, F, Lunney, J, Sinkora, J, Haverson, K 2001. Summary of workshop findings for porcine myelomonocytic markers. Veterinary Immunology and Immunopathology 80, 93109.CrossRefGoogle ScholarPubMed
Wonigeit, K, Washington, D, Hundrieser, J 1998. Lessons from rat models on the genetic basis of inter-individual differences in lymphocyte phenotype. Transplantation Proceedings 30, 23412343.CrossRefGoogle Scholar
Yang, H, Parkhouse, RME 1996. Phenotypic classification of porcine lymphocyte populations in blood and lymphoid tissues. Immunology 89, 7683.CrossRefGoogle Scholar
Zuckermann, FA 1999. Extrathymic CD4/CD8 double positive T cells. Veterinary Immunology and Immunopathology 72, 5566.CrossRefGoogle ScholarPubMed