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Selection for lean growth and food intake leads to correlated changes in innate immune traits in Large White pigs

Published online by Cambridge University Press:  13 March 2007

M. Clapperton*
Affiliation:
Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, UK
S.C. Bishop
Affiliation:
Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, UK
E.J. Glass
Affiliation:
Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, UK
*
E-mail: [email protected]
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Abstract

Genetic selection is well established as a means of improving productivity in pigs, but the effects of continued selection for increased performance on immunity are not well understood, nor are genetic relationships between performance and immunity. This study compared differences in the levels of a range of immune traits between lines of Large White pigs divergently selected for a number of productivity traits. Selection lines compared were high v. low lean growth under restricted feeding (31 high line v. 10 control v. 38 low line pigs), high v. low lean growth under ad libitum feeding (18 high line v. 10 control v. 19 low line pigs), and high v. low food intake (24 high line v. 26 low line pigs). Immune traits measured were total white blood cell numbers (WBC), and the numbers of leukocyte subsets: neutrophils, monocytes, eosinophils, lymphocytes, CD4+ cells, CD8α+ cells, B cells, γδ T cells and CD11R1+ Natural killer (NK) cells. CD4+, γδ T cells and CD11R1+ cells were subdivided into subpopulations that were positive or negative for the CD8α marker, and conventional CD8αhigh+ cytotoxic T cells were also determined. Pigs were tested under ad libitum feeding conditions from 14 to 24 weeks, and immune traits were assessed at ages 18 and 24 weeks. Line differences were estimated using residual maximum likelihood techniques. Consistent differences in immune trait levels were evident between pigs previously selected for high and low lean growth under restricted feeding: at age 24 weeks, high line pigs had higher basal levels of WBC (39·6 v. 27·8×106 cells per ml, s.e.d. 2·09, for high v. low line pigs) mainly explained by higher levels of lymphocytes (25·5 v. 17·3×106 cells per ml, s.e.d. 1·54, for high v. low line pigs) with increased numbers of CD8α+ cells (8·19 v. 5·15×106 cells per ml, s.e.d. 0·14) and CD11R1+ cells (5·23 v. 2·46×106 cells per ml, s.e.d. 0·43), predominantly the CD11R1+ CD8α? subpopulation ((3·20 v. 1·64×106 cells per ml, s.e.d. 0·11). High line pigs also had increased numbers of monocytes (2·64 v. 1·83×106 cells per ml, s.e.d. 0·35). Similar results were obtained at age 18 weeks. There were no consistent differences between divergent lines in pigs selected for lean growth under ad libitum feeding or food intake. This is the first report to demonstrate that selection for some aspects of performance can influence WBC and leukocyte subset numbers in pigs.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 2006

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References

Amadori, A.Zamarchi, R.Chiero-Bianchi, L. (1996) CD4:CD8 ratio and HIV infections; the “tap and drain” hypothesis Immunology Today 17: 414417CrossRefGoogle ScholarPubMed
Balaji, R.Wright, K. J.Hill, C. M.Dritz, S. S.Knoppel, E. L.Minton, J. E. (2000) Acute phase responses of pigs challenged orally with Salmonella typhimurium Journal of Animal Science 78: 18851891CrossRefGoogle ScholarPubMed
Bjornson, B. H.Harvey, J. M.Rose, L. (1985) Differential effect of hydrocortisone on eosinophil and neutrophil proliferation Journal of Clinical Investigation 76: 924929CrossRefGoogle ScholarPubMed
Cameron, N. D. (1994) Selection for components of efficient lean growth-rate in pigs 1. Selection pressure applied and direct responses in a large white herd Animal Production 59: 251262Google Scholar
Carbo, N.Lopez-Soriano, J.Costelli, P.Alvarez, B.Busquets, S.Baccinom, F. M.Quinn, L. S.Lopez-Soriano, F. J.Argiles, J. M. (2001) Interleukin-15 mediates reciprocal regulation of adipose and muscle mass: a potential role in body weight control Biochimica et Biophysica Acta 1526: 1724CrossRefGoogle Scholar
Carding, S. R.Egan, P. J. (2000) The importance of gamma delta T cells in the resolution of pathogen-induced inflammatory immune responses Immunological Reviews 173: 99107CrossRefGoogle ScholarPubMed
Cheeseman, J. H.Kaiser, M. G.Lamont, S. J. (2004) Genetic line effect on peripheral blood leukocyte cell surface marker expression in chickens Poultry Science 83: 911916CrossRefGoogle ScholarPubMed
Chen, J.Harrison, D. E. (2002) Quantitative trait loci regulating relative lymphocyte proportions in mouse peripheral blood Blood 99: 561566CrossRefGoogle ScholarPubMed
Clapperton, M.Bishop, S. C.Cameron, N. D.Glass, E. J. (2005a) Associations of acute phase protein levels with growth performance and with selection for growth performance in Large White pigs Animal Science 81: 213220CrossRefGoogle Scholar
Clapperton, M.Bishop, S. C.Cameron, N. D.Glass, E. J. (2005b) Associations of weight gain and food intake with leukocyte sub-sets in Large White pigs Livestock Production Science 96: 249260CrossRefGoogle Scholar
Clapperton, M.Bishop, S. C.Glass, E. J. (2005c) Innate immune traits differ between Meishan and Large White pigs Veterinary Immunology and Immunopathology 104: 131144CrossRefGoogle ScholarPubMed
Colditz, I. G. (2002) Effects of the immune system on metabolism: implications for production and disease resistance in livestock Livestock Production Science 75: 257268CrossRefGoogle Scholar
Cooper, M. A.Fehniger, T. A. Caligari, M. A. (2001) The biology of human natural killer-cell subsets Trends in Immunology 22: 633640CrossRefGoogle ScholarPubMed
Davis, W. C.Haverson, K.Saalmuller, A.Yang, H.Lunney, J. K.Hamilton, M. J.Pescovitz, M. D. (2001) Analysis of monoclonal antibodies with molecules expressed on gamma delta cells Veterinary Immunology and Immunopathology 80: 5362CrossRefGoogle Scholar
Denham, S.Zwart, R.Whittall, J. T. D.Pampusch, M.Corteyn, A. H.Bianchi, A. T. J.Murtaugh, M. P.Parkhouse, R. M. E.Tlaksova, H.Sinkora, J.Sinkora, M.Rehakova, Z. (1998) Monoclonal antibodies putatively recognising porcine B cells Veterinary Immunology and Immunopathology 60: 317328CrossRefGoogle Scholar
Edfors-Lilja, I.Wattrang, E.Andersson, L.Fossum, C. (2000) Mapping quantitative trait loci for stress-induced alterations in porcine leukocyte numbers and functions Animal Genetics 31: 186193CrossRefGoogle 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: 116CrossRefGoogle 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 Journal of Immunology 160: 829835CrossRefGoogle Scholar
Evans, D. M.Frazer, I. H.Martin, N. G. (1999) Genetic and environmental causes of variation in basal levels of blood cells Twin Research 2: 250257CrossRefGoogle ScholarPubMed
Fearon, D. T.Locksley, R. M. (1996) The instructive role of innate immunity in the acquired immune response Science 272: 5060CrossRefGoogle ScholarPubMed
Freitas, A. A.Rocha, B. (2000) The flight for survival Annual Reviews in Immunology 18: 83111CrossRefGoogle ScholarPubMed
Furmanczyk, P.S.Quinn, L. S. (2003) Interleukin-15 increases myosin accretion in human skeletal myogenic cultures Cell Biology International 27: 845881CrossRefGoogle ScholarPubMed
Greiner, L. L.Stahly, T. S. (2000) Quantitative relationship of systemic virus concentration on growth and immune response in pigs Journal of Animal Science 78: 26902695CrossRefGoogle ScholarPubMed
Grimm, R. H.Neaton, J. D.Ludwig, W. (1985) Prognostic importance of the white blood cell count for coronary, cancer, and all-cause mortality Journal of the American Medical Association 254: 19321937CrossRefGoogle ScholarPubMed
Hall, M. A.Norman, P. J.Thiel, B.Tiwari, H.Peiffer, A.Vaugham, R. W.Prescott, S.Leppert, M.Schork, N. J.Lauchberg, J. S. (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 subpopulations American Journal of Human Genetics 70: 11721182CrossRefGoogle ScholarPubMed
Haverson, K.Bailey, M.Stokes, C. R.Simon, A.LeFlufy, L.Banfield, G.Chen, Z.Hollemweguer, E.Ledbetter, J. A. (2001) Monoclonal antibodies raised to human cells – specificity for pigs leukocytes Veterinary Immunology and Immunopathology 80: 175186CrossRefGoogle ScholarPubMed
Henryon, M.Berg, P.Jensen, J.Andersen, S. (2001) Genetic variation for resistance to clinical and subclinical diseases exists in growing pigs Animal Science 73: 375378CrossRefGoogle Scholar
Henryon, M., Juul-Madson, H. R. and Berg, P. 2002. Genetic variation for total and differential numbers of leukocytes exist in growing pigs. Proceedings of the seventh world congress on genetics applied to livestock production, communication 13–02Google Scholar
Hetherington, S. V.Quie, P. G. (1985) Human polymorphonuclear leucocytes of the bone marrow, circulation and marginated pool: function and granule protein content American Journal of Hematology 20: 235246CrossRefGoogle ScholarPubMed
Knapp, P. W. and Bishop, S. C. 2000. Relationships between genetic change and infectious disease in domestic livestock. In The challenge of genetic change in animal production (ed. Hill, W. G.Bishop, S. C.McGuirk, B.McKay, J. C.Simm, G. and Webb, A. J.), BSAS occasional publication, number 27, pp. 6580. http:www.BSAS.org.uk/publs/genchg/contents.pdfGoogle Scholar
Lang, T. J. (2004) Estrogen as an immunomodulator Clinical Immunology 113: 224230CrossRefGoogle ScholarPubMed
Lawes Agricultural Trust (1983) GENSTAT: a general statistical program Oxford Numerical Algorithms GroupGoogle Scholar
Mallard, B. A.Wilkie, B. N.Kennedy, B. W.Gibson, J.Quinton, M. (1998) Immune responsiveness in swine: Eight generations of selection for high and low immune response in Yorkshire pigs Proceeding of the Sixth World Congress on Genetics in Applied Livestock Production 27: 257264Google Scholar
Marple, D. N.Cassens, R. G.Topel, D. G.Christian, L. L. (1974) Porcine corticosteroid-binding globulin: binding properties and levels in stress susceptible swine Journal of Animal Science 38: 12241228CrossRefGoogle ScholarPubMed
Medzhitov, R.Janeway, C. (2000) Innate immune recognition: mechanisms and pathways Immunological Reviews 173: 8997CrossRefGoogle ScholarPubMed
Merchav, S.Lake, MSkottner, A (1993) Comparative studies of the granulopoietic enhancing effects of biosynthetic human insulin-like growth factors I and II Journal of Cell Physiology 157: 178183CrossRefGoogle ScholarPubMed
Merks, J. W. M. (1989) Genotype×environment interactions in pig breeding programmes. VI Genetic relations between performances in central test, on-farm test and commercial fattening Livestock Production Science 22: 325339CrossRefGoogle Scholar
Nguyen, V. P.Wong, C. W.Hinch, G. N.Singh, D.Colditz, I. D. (1998) Variation in the immune status of two Australian pig breeds Australian Veterinary Journal 76: 613617CrossRefGoogle ScholarPubMed
Quinn, L. S.Anderson, B. G.Drivdahl, R. H.Alvarez, B.Argiles, J. M. (2002) Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders Experimental Cell Research 280: 5563CrossRefGoogle ScholarPubMed
Raymond, C.Wilkie, B.Mallard, B.Quinton, M. (1998) Natural killer cell frequency and function in Yorkshire pigs selectively bred for high and low antibody and cell-mediated immune response Natural Immunity 16: 127136CrossRefGoogle ScholarPubMed
Saalmuller, A.Kuebart, G.Hollmweguer, E.Chen, Z.Neilsen, J.Zuckermann, F.Haverson, K. (2001) Summary of workshop findings for porcine T-lymphocyte specific monoclonal antibodies Veterinary Immunology and Immunopathology 80: 3552CrossRefGoogle ScholarPubMed
Schwartz, G. N.Warren, M. K.Sakano, K.Szabo, J. M.Kessler, S. W.Pasta, A.Gress, R. E.Perdue, J. F. (1996) Comparative effects of insulin-like growth factor II (IGF-II): IGF-II mutants specific for IGF-II/CIM6-P or IGF-I receptor on in vitro hematopoiesis Stem Cells 14: 337350CrossRefGoogle ScholarPubMed
Spurlock, M. E. (1997) Regulation of metabolism and growth during immune challenge: an overview of cytokine function Journal of Animal Science 75: 17731783CrossRefGoogle ScholarPubMed
Suffredini, A. F. Fantuzzi, G.Badolato, R.Oppenheim, J. J.O'Grady, N. P. (1999) New insights into the biology of the acute phase response Journal of Clinical Immunology 19: 203214CrossRefGoogle 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: 83109CrossRefGoogle ScholarPubMed
Van Laere, A. S. Nguyen, M.Braunschweig, M.Nezer, C.Collette, C.Moreau, L.Archibald, A. L.Haley, C. S.Buys, N.Tally, M.Andersson, G.Georges, M.Andersson, L. (2003) A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig Nature 425: 832836CrossRefGoogle Scholar
Visscher, A. H.Janss, L. L. G.Niewold, T. A.de Greef, K. H. (2002) Disease incidence and immunological traits for the selection of healthy pigs. A review Veterinary Quarter 24: 2934Google ScholarPubMed
Williams, N. S.Klem, J.Puzanov, I. J.Sivakumar, P. V.Schatzle, J. D.Bennet, M.Kumar, V. (1998) Natural killer differentiation: insights from knockout and transgenic mouse models and in vitro systems Immunological Reviews 165: 4761CrossRefGoogle ScholarPubMed
Wonigeit, K.Washington, DHundrieser, J (1998) Lessons from rat models on the genetic basis of interindividual differences in lymphocyte phenotype Transplantation Proceedings 30: 23412343CrossRefGoogle ScholarPubMed
Wunderlich, F.Benten, W. P. M.Lieberher, M.Guo, Z.Stamm, O.Wrehlke, C.Sekeris, C. E.Mossmann, H. (2002) Testosterone signaling in T cells and macrophages Steroids 67: 535538CrossRefGoogle Scholar
Yamamoto, Y.Saito, H.Setogawa, T.Tomioka, H. (1991) Sex differences in host resistance to Mycobacterium marinum infection in mice Infection and Immunity 59: 40894096CrossRefGoogle ScholarPubMed
Yang, H.Parkhouse, R. M. E. (1996) Phenotypic classification of porcine lymphocyte subpopulations in blood and lymphoid tissues Immunology 89: 4552CrossRefGoogle ScholarPubMed
Yang, H.Parkhouse, R. M. E. (1997) Differential expression of CD8 epitopes amongst porcine CD8-positive functional lymphocyte sub-sets Immunology 92: 4552CrossRefGoogle Scholar
Zhang, C. C.Lodish, H. F. (2004) Insulin-like growth factor 2 expressed in a novel fetal liver cell population is a growth factor for hematopoietic stem cells Blood 103: 25132521CrossRefGoogle Scholar