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Effect of heat challenge on peripheral blood mononuclear cell viability: comparison of a tropical and temperate pig breed

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Abstract

We evaluated the effect of heat challenge on cell viability, concanavalin A-induced proliferation and heat shock protein (HSPs) mRNA expression in peripheral mononuclear blood cells (PBMC) isolated from Creole (CR) and Large White (LW) pigs. The PBMCs were cultured for 9 h at 37°C before being subjected to heat challenge: (1) at 42°C or 45°C for 2, 4, 6 and 9 h to monitor cell viability;(2) at 45°C for 2 and 9 h followed by stimulation for 24 h at 37°C with concanavalin A to evaluate mitogen-induced proliferation; and (3) at 45°C for 3, 6 and 9 h to measure induction of HSP70.2 and HSP90 mRNA. Cell viability was affected by breed and temperature (P < 0.01), and the viability decrease caused by heat challenge was greater for LW than CR pigs. For mitogen-stimulated PBMCs, incubation at 45°C reduced lymphoblastogenesis equally in both breeds (P < 0.01). Although heat challenge for 3 and 6 h at 45°C induced expression of HSP70.2 and HSP90 mRNA, no breed difference was observed. In conclusion, differences in heat resistance between these two breeds at the whole organism level are reflected at the cellular level. Neither HSP70.2 nor HSP90 mRNA expression levels explain this effect.

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References

  • Berbigier, P., 1975. Cutaneous Heat Exchanges of Piglets Reared in a Tropical Climate .1. Influence of Climatic Conditions and Influence of Breed. Annales De Zootechnie 24, 423–432.

    Article  Google Scholar 

  • Berbigier, P., 1988. Description des climats équatoriaux et tropicaux. INRA Ed. Bioclimatologie des ruminants domestiques en zone tropicale. INRA Publ., Paris, France., 11–18.

  • Chen, M.Y., Tu, C.F., Huang, S.Y., Lin, J.H., Tzang, B.S., Hseu, T.H., Lee, W.C., 2005. Augmentation of thermotolerance in primary skin fibroblasts from a transgenic pig overexpressing the porcine HSP70.2. Asian-Australasian Journal of Animal Sciences 18, 107–112.

    CAS  Google Scholar 

  • Cook, N.B., Bennett, T.B., Emery, K.M., Nordlund, K.V., 2002. Monitoring nonlactating cow intramammary infection dynamics using DHI somatic cell count data. Journal of Dairy Science 85, 1119–1126.

    Article  PubMed  CAS  Google Scholar 

  • Dozois, C.M., Oswald, E., Gautier, N., Serthelon, J.P., Fairbrother, J.M., Oswald, I.P., 1997. A reverse transcription-polymerase chain reaction method to analyze porcine cytokine gene expression. Veterinary Immunology and Immunopathology 58, 287–300.

    Article  PubMed  CAS  Google Scholar 

  • Elvinger, F., Hansen, P.J., Natzke, R.P., 1991. Modulation of Function of Bovine Polymorphonuclear Leukocytes and Lymphocytes by High-Temperature Invitro and Invivo. American Journal of Veterinary Research 52, 1692–1698.

    PubMed  CAS  Google Scholar 

  • Gourdine, J.L., Bidanel, J.P., Noblet, J., Renaudeau, D., 2006a. Effects of breed and season on performance of lactating sows in a tropical humid climate. Journal of Animal Science 84, 360–369.

    PubMed  CAS  Google Scholar 

  • Gourdine, J.L., Bidanel, J.P., Noblet, J., Renaudeau, D., 2006b. Effects of season and breed on the feeding behavior of multiparous lactating sows in a tropical humid climate. Journal of Animal Science 84, 469–480.

    PubMed  CAS  Google Scholar 

  • Hansen, P.J., 2004. Physiological and cellular adaptations of zebu cattle to thermal stress. In: 15th International Congress on Animal Reproduction, Porto Seguro, BRAZIL, Aug 08–12, pp. 349–360.

  • Hendrick, J.P., Hartl, F.U., 1993. Molecular Chaperone Functions of Heat-Shock Proteins. Annual Review of Biochemistry 62, 349–384.

    Article  PubMed  CAS  Google Scholar 

  • Huang, H.C., Lee, W.C., Lin, J.H., Huang, H.W., Jian, S.C., Mao, S.J.T., Yang, P.C., Huang, T.Y., Liu, Y.C., 1999. Molecular cloning and characterization of porcine cDNA encoding a 90-kDa heat shock protein and its expression following hyperthermia. Gene 226, 307–315.

    Article  PubMed  CAS  Google Scholar 

  • James, P., Pfund, C., Craig, E.A., 1997. Functional specificity among Hsp70 molecular chaperones. Science 275, 387–389.

    Article  PubMed  CAS  Google Scholar 

  • Kamwanja, L.A., Chase, C.C., Gutierrez, J.A., Guerriero, V., Olson, T.A., Hammond, A.C., Hansen, P.J., 1994, Responses of Bovine Lymphocytes to Heat-Shock as Modified by Breed and Antioxidant Status. Journal of Animal Science 72, 438–444.

    PubMed  CAS  Google Scholar 

  • Kapiszewska, M., Hopwood, L.E., 1988. Mechanisms of Membrane Damage for Cho Cells Heated in Suspension. Journal of Cancer Research and Clinical Oncology 114, 23–29.

    Article  PubMed  CAS  Google Scholar 

  • Lacetera, N., Bernabucci, U., Scalia, D., Ronchi, B., Kuzminsky, G., Nardone, A., 2005. Lymphocyte functions in dairy cows in hot environment. International Journal of Biometeorology 50, 105–110.

    Article  PubMed  Google Scholar 

  • Lacetera, N., Bernabucci, U., Scalia, D., Basirico, L., Morera, P., Nardone, A., 2006. Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. Journal of Dairy Science 89, 4606–4612.

    Article  PubMed  CAS  Google Scholar 

  • Lacetera, N., Bernabucci, U., Basirico, L., Morera, P., Nardone, A., 2009. Heat shock impairs DNA synthesis and down-regulates gene expression for leptin and Ob-Rb receptor in concanavalin A-stimulated bovine peripheral blood mononuclear cells. Veterinary Immunology and Immunopathology 127, 190–194.

    Article  PubMed  CAS  Google Scholar 

  • Le Bellego, L., van Milgen, J., Dubois, S., Noblet, J., 1999. Energy utilization of low-protein diets in growing pigs. In: 91st Annual Meeting of the American-Society-of-Animal-Science, Indianapolis, IN, Jul 21–23, pp. 1259–1271.

  • McGlone, J.J., Stansbury, W.F., Tribble, L.F., 1988. Management of Lactating Sows During Heat-Stress—Effects of Water Drip, Snout Coolers, Floor Type and a High Energy-Density Diet. Journal of Animal Science 66, 885–891.

    PubMed  CAS  Google Scholar 

  • Mizzen, L.A., Welch, W.J., 1988. Characterization of the Thermotolerant Cell .1. Effects on Protein-Synthesis Activity and the Regulation of Heat-Shock Protein-70 Expression. Journal of Cell Biology 106, 1105–1116.

    Article  PubMed  CAS  Google Scholar 

  • Moseley, P.L., 1997. Heat shock proteins and heat adaptation of the whole organism. Journal of Applied Physiology 83, 1413–1417.

    PubMed  CAS  Google Scholar 

  • Nathan, D.F., Vos, M.H., Lindquist, S., 1997. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proceedings of the National Academy of Sciences of the United States of America 94, 12949–12956.

    Article  PubMed  CAS  Google Scholar 

  • Nylandsted, J., Gyrd-Hansen, M., Danielewicz, A., Fehrenbacher, N., Lademann, U., Hoyer-Hansen, M., Weber, E., Multhoff, G., Rohde, M., Jaattela, M., 2004. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. Journal of Experimental Medicine 200, 425–435.

    Article  PubMed  CAS  Google Scholar 

  • Paula-Lopes, F.F., Chase, C.C., Al-Katanani, Y.M., Krininger, C.E., Rivera, R.M., Tekin, S., Majewski, A.C., Ocon, O.M., Olson, T.A., Hansen, P.J., 2003. Genetic divergence in cellular resistance to heat shock in cattle: Differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction 125: 285–294.

    Article  PubMed  CAS  Google Scholar 

  • Quesnel, H., Boulot, S., Le Colzer Y., 2005. Les variations saisonnières des performances de reproduction chez la truie. INRA Production Animales 18, 101–110.

    Google Scholar 

  • Renaudeau, D., 2005. Effects of short-term exposure to high ambient temperature and relative humidity on thermoregulatory responses of European (Large White) and Caribbean (Creole) restrictively-fed growing pigs. Animal Research 54, 81–93.

    Article  Google Scholar 

  • Renaudeau, D., Mandonnet, N., Tixier-Boichard, M., Noblet, J., Bidanel, J.P., 2004. Attenuate the effects of high ambient temperature on pig performance: the genetic selection. Productions Animales 17, 93–108.

    Google Scholar 

  • Renaudeau, D., Giorgi, M., Silou, F., Weisbecker, J.L., 2006a. Effect of breed (lean or fat pigs) and sex on performance and feeding behaviour of group housed growing pigs in a tropical climate. Asian-Australasian Journal of Animal Sciences 19, 593–600.

    Google Scholar 

  • Renaudeau, D., Leclercq-Smekens, M., Herin, M., 2006b. Differences in skin characteristics in European (Large White) and Caribbean (Creole) growing pigs with reference to thermoregulation. Animal Research 55, 209–217.

    Article  Google Scholar 

  • Renaudeau, D., Kerdoncuff, M., Anais, C., Gourdine, J.L., 2008. Effect of temperature level on thermal acclimation in Large White growing pigs. Animal 2, 1619–1626.

    Article  Google Scholar 

  • Robbins, K.R., Saxton, A.M., Southern, L.L. 2006. Estimation of nutrient requirements using broken-line regression analysis. Journal of Animal Science 84:E155–E165.

    PubMed  Google Scholar 

  • Silva, B.A.N., Oliveira, R.F.M., Donzele, J.L., Fernandes, H.C., Abreu, M.L.T., Noblet, J., Nunes, C.G.V., 2006. Effect of floor cooling on performance of lactating sows during summer. Livestock Science 105, 176–184.

    Article  Google Scholar 

  • Silva, B.A.N., Noblet, J., Oliveira, R.F.M., Donzele, J.L., Primot, Y., Renaudeau, D., 2009. Effects of dietary protein concentration and amino acid supplementation on the feeding behavior of multiparous lactating sows in a tropical humid climate. Journal of Animal Science 87, 2104–2112.

    Article  PubMed  CAS  Google Scholar 

  • Totte, P., Esteves, I., Gunter, N., Martinez, D., Bensaida, A., 2002. Evaluation of several flow cytometric assays for the analysis of T-cell responses, in goats. Cytometry 49, 49–55.

    Article  PubMed  Google Scholar 

  • Welch, W.J., Mizzen, L.A., 1988. Characterization of the Thermotolerant Cell .2. Effects on the Intracellular-Distribution of Heat-Shock Protein-70, Intermediate Filaments, and Small Nuclear Ribonucleoprotein Complexes. Journal of Cell Biology 106, 1117–1130.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to the team at Plateforme Tropicale d′ Experimentation Animale (PTEA), INRA-Domaine Duclos for their technical support. We acknowledge the technical staff at UMR 15 for assistance with cellular and molecular assays. J. C. Bambou was supported by a post-doctoral fellowship from le Conseil Régional de la Guadeloupe.

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Authors and Affiliations

  1. INRA UR143, Unité de Recherches Zootechniques, Centre INRA Antilles Guyane, Domaine de Duclos, Prise d’Eau, 97170, Petit Bourg, Guadeloupe (French West Indies), France

    Jean-Christophe Bambou, Jean-Luc Gourdine, Roxanne Grondin & David Renaudeau

  2. UMR 15 CIRAD/INRA, Contrôle des maladies animales exotiques et émergentes, Domaine de Duclos, Prise d’Eau, 97170, Petit Bourg, Guadeloupe (French West Indies), France

    Nathalie Vachiery

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  1. Jean-Christophe Bambou
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  2. Jean-Luc Gourdine
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  3. Roxanne Grondin
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  4. Nathalie Vachiery
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  5. David Renaudeau
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Correspondence to Jean-Christophe Bambou.

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Bambou, JC., Gourdine, JL., Grondin, R. et al. Effect of heat challenge on peripheral blood mononuclear cell viability: comparison of a tropical and temperate pig breed. Trop Anim Health Prod 43, 1535–1541 (2011). https://doi.org/10.1007/s11250-011-9838-9

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