Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-24T15:32:11.478Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunomodulatory factors and infectious agents associated with the hepatic gene expression of the IGF system in nursery pigs

Published online by Cambridge University Press:  27 February 2014

M. J. Slifierz ,
R. Friendship ,
C. F. M. de Lange ,
D. Slavic ,
H. Grgic  and
A. Farzan
M. J. Slifierz*
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada, N1G 2W1
R. Friendship
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada, N1G 2W1
C. F. M. de Lange
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, ON, Canada, N1G 2W1
D. Slavic
Affiliation:
Animal Health Laboratory, Ontario Veterinary College, University of Guelph, ON, Canada, N1G 2W1
H. Grgic
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada, N1G 2W1
A. Farzan
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada, N1G 2W1
*
†E-mail: [email protected]
Get access

Abstract

Recent findings suggest there is a complex interaction between the IGF system and the inflammatory immune response. The objective of this study was to determine whether gene expression of growth factors (IGF-1, IGF-binding protein-3 (IGFBP-3) and growth hormone receptors (GHR)) in the liver is associated with gene expression of immunomodulators in the liver, including C-reactive protein (CRP), serum amyloid A (SAA), haptoglobin (Hp), interferon-α (IFN-α), IFN-γ, tumour necrosis factor-α (TNF-α), interleukin (IL)-1β, IL-6, IL-10 and IL-18, as well as with the presence of Salmonella spp., Lawsonia intracellularis, Brachyspira spp., enterotoxigenic Escherichia coli, methicillin-resistant Staphylococcus aureus, swine influenza virus, and porcine reproductive and respiratory syndrome virus (PRRSV) in nursery pigs (n=74) from commercial farms (n=4). Gene expression was quantified using reverse transcription quantitative-PCR (RT-qPCR) and the data were modelled using logistic regression methods. Pigs with elevated IGF-1 expression were less likely to have increased expression of TNF-α (odds ratio (OR)=0.14, P<0.01) and IL-18 (OR=0.19, P<0.05), and less likely to be colonized with PRRSV (OR=0.03, P<0.01). Pigs with increased expression of IGFBP-3 were more likely to have elevated IL-6 expression (OR=8.5, P<0.05). It was also observed that IGFBP-3 and IGF-1 were significantly associated when Hp expression was low (OR=30, P<0.05), but this association was not significant when Hp expression was high (P=0.54). Pigs with increased expression of GHR were less likely to have elevated expression of SAA (OR=0.01, P<0.05) and IL-1β (OR=0.03, P<0.05), but more likely to have increased expression of CRP (OR=290, P<0.01). Overall, there appears to be an inverse association between the hepatic expression of the IGF system (IGF-1, IGFBP-3, GHR) and certain cytokines (IL-1β, IL-18, TNF-α) and acute-phase proteins (SAA, Hp).

Keywords

pighealthimmunologyIGF
Type
Full Paper
Information
animal , Volume 8 , Issue 5 , May 2014 , pp. 844 - 851
Copyright
© The Animal Consortium 2014 

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

Ahlgren, R, Norstedt, G, Baumbach, WR and Mode, A 1995. Hormonal regulation of the female enriched GH receptor/binding protein mRNA in rat liver. Molecular and Cellular Endocrinology 113, 11–17.CrossRefGoogle ScholarPubMed
Baumbach, WR and Bingham, B 1995. One class of growth hormone (GH) receptor and binding protein messenger ribonucleic acid in rat liver, GHR1, is sexually dimorphic and regulated by GH. Endocrinology 136, 749–760.CrossRefGoogle ScholarPubMed
Bichell, DP, Kikuchi, K and Rotwein, P 1992. Growth hormone rapidly activates insulin-like growth factor I gene transcription in vivo . Molecular Endocrinology 6, 1899–1908.Google ScholarPubMed
Borghetti, P, Saleri, R, Ferrari, L, Morganti, M, De Angelis, E, Franceschi, V, Bottarelli, E and Martelli, P 2011. Cytokine expression, glucocorticoid and growth hormone changes after porcine reproductive and respiratory syndrome virus (PRRSV-1) infection in vaccinated and unvaccinated naturally exposed pigs. Comparative Immunology, Microbiology, and Infectious Diseases 34, 143–155.CrossRefGoogle ScholarPubMed
Clutter, AC, Spicer, LJ, Woltmann, MD, Grimes, RW, Hammond, JM and Buchanan, DS 1995. Plasma growth hormone, insulin-like growth factor I, and insulin-like growth factor binding proteins in pigs with divergent genetic merit for postweaning average daily gain. Journal of Animal Science 73, 1776–1783.CrossRefGoogle ScholarPubMed
Collado-Romero, M, Arce, C, Ramírez-Boo, M, Carvajal, A and Garrido, JJ 2010. Quantitative analysis of the immune response upon Salmonella typhimurium infection along the porcine intestinal gut. Veterinary Research 41, 23.CrossRefGoogle ScholarPubMed
Dupont, J and Holzenberger, M 2003. Biology of insulin-like growth factors in development. Birth Defects Research Part C: Embryo Today 69, 257–271.CrossRefGoogle ScholarPubMed
Jenkins, NL, Turner, JL, Dritz, SS, Durham, SK and Minton, JE 2004. Changes in circulating insulin-like growth factor-I, insulin-like growth factor binding proteins, and leptin in weaned pigs infected with Salmonella enterica serovar Typhimurium. Domestic Animal Endocrinology 26, 49–60.CrossRefGoogle ScholarPubMed
Jeschke, MG, Herndon, DN and Barrow, RE 2000. Insulin-like growth factor I in combination with insulin-like growth factor binding protein 3 affects the hepatic acute phase response and hepatic morphology in thermally injured rats. Annals of Surgery 231, 408–416.CrossRefGoogle ScholarPubMed
Khanna, T, Friendship, R, Dewey, C and Weese, JS 2008. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Veterinary Microbiology 128, 298–303.CrossRefGoogle ScholarPubMed
Kim, SR, Lee, KS, Lee, KB and Lee, YC 2012. Recombinant IGFBP-3 inhibits allergic lung inflammation, VEGF production, and vascular leak in a mouse model of asthma. Allergy 67, 869–877.CrossRefGoogle Scholar
Li, Z, Wu, Z, Ren, G, Zhao, Y and Liu, D 2013. Expression patterns of insulin-like growth factor system members and their correlations with growth and carcass traits in Landrace and Lantang pigs during postnatal development. Molecular Biology Reports 40, 3569–3576.CrossRefGoogle ScholarPubMed
Li, Z, Cao, B, Zhao, B, Yang, X, Fan, MZ and Yang, J 2009. Decreased expression of calpain and calpastatin mRNA during development is highly correlated with muscle protein accumulation in neonatal pigs. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 152, 498–503.CrossRefGoogle ScholarPubMed
Lu, C, Kumar, PA, Fan, Y, Sperling, MA and Menon, RK 2010. A novel effect of growth hormone on macrophage modulates macrophage-dependent adipocyte differentiation. Endocrinology 151, 2189–2199.CrossRefGoogle ScholarPubMed
Mohan, S and Baylink, DJ 2002. IGF-binding proteins are multifunctional and act via IGF-dependent and -independent mechanisms. Journal of Endocrinology 175, 19–31.CrossRefGoogle ScholarPubMed
Netea, MG, Joosten, LA, Lewis, E, Jensen, DR, Voshol, PJ, Kullberg, BJ, Tack, CJ, van Krieken, H, Kim, SH, Stalenhoef, AF and van de Loo, FA, Verschueren, I, Pulawa, L, Akira, S, Eckel, RH, Dinarello, CA, van den Berg, W and van der Meer, JW 2006. Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nature Medicine 12, 650–656.CrossRefGoogle ScholarPubMed
Owens, PC, Gatford, KL, Walton, PE, Morley, W and Campbell, RG 1999. The relationship between endogenous insulin-like growth factors and growth in pigs. Journal of Animal Science 77, 2098–2103.CrossRefGoogle ScholarPubMed
Pfaffl, MW, Tichopad, A, Prgomet, C and Neuvians, TP 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnology Letters 26, 509–515.CrossRefGoogle ScholarPubMed
Piñeiro, C, Piñeiro, M, Morales, J, Carpintero, R, Campbell, FM, Eckersall, PD, Toussaint, MJ, Alava, MA and Lampreave, F 2007a. Pig acute-phase protein levels after stress induced by changes in the pattern of food administration. Animal 1, 133–139.CrossRefGoogle ScholarPubMed
Piñeiro, M, Piñeiro, C, Carpintero, R, Morales, J, Campbell, FM, Eckersall, PD, Toussaint, MJ and Lampreave, F 2007b. Characterisation of the pig acute phase protein response to road transport. The Veterinary Journal 173, 669–674.CrossRefGoogle ScholarPubMed
Regula, G, Lichtensteiger, CA, Mateus-Pinilla, NE, Scherba, G, Miller, GY and Weigel, RM 2000. Comparison of serologic testing and slaughter evaluation for assessing the effects of subclinical infection on growth in pigs. Journal of the American Veterinary Medical Association 217, 888–895.CrossRefGoogle ScholarPubMed
Roberts, NE and Almond, GW 2003. Infection of growing swine with porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae–effects on growth, serum metabolites, and insulin-like growth factor-I. Canadian Veterinary Journal 44, 31–37.Google ScholarPubMed
Rutherford, KMD, Baxter, EM, D’Eath, RB, Turner, SP, Arnott, G, Roehe, R, Ask, B, Sandøe, P, Moustsen, VA, Thorup, F, Edwards, SA, Berg, P and Lawrence, AB 2013. The welfare implications of large litter size in the domestic pig I: biological factors. Animal Welfare 22, 199–218.CrossRefGoogle Scholar
Savage, MO 2013. Insulin-like growth factors, nutrition and growth. World Review of Nutrition and Dietetics 106, 52–59.CrossRefGoogle ScholarPubMed
Skopiński, P, Rogala, E, Duda-Król, B, Lipińska, A, Sommer, E, Chorostowska-Wynimko, J, Szaflik, J, Partyka, I and Skopińska-Rózewska, E 2005. Increased interleukin-18 content and angiogenic activity of sera from diabetic (Type 2) patients with background retinopathy. Journal of Diabetes and its Complications 19, 335–338.CrossRefGoogle ScholarPubMed
Slifierz, M, Friendship, R, de Lange, CFM, Rudar, M, Farzan, A 2013. An epidemiological investigation into the association between biomarkers and growth performance in nursery pigs. BioMed Central Veterinary Research 9, 247.Google ScholarPubMed
Suh, HS, Zhao, ML, Derico, L, Choi, N and Lee, SC 2013. Insulin-like growth factor 1 and 2 (IGF1, IGF2) expression in human microglia: differential regulation by inflammatory mediators. Journal of Neuroinflammation 10, 37.CrossRefGoogle ScholarPubMed
Svobodová, K, Bílek, K and Knoll, A 2008. Verification of reference genes for relative quantification of gene expression by real-time reverse transcription PCR in the pig. Journal of Applied Genetics 49, 263–265.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Thacker, EL and Halbur, PG 1997. Effect of porcine reproductive and respiratory syndrome virus (PRRSV) (isolate ATCC VR-2385) infection on bactericidal activity of porcine pulmonary intravascular macrophages (PIMs): in vitro comparisons with pulmonary alveolar macrophages (PAMs). Veterinary Immunology and Immunopathology 59, 323–335.CrossRefGoogle ScholarPubMed
Thissen, JP and Verniers, J 1997. Inhibition by interleukin-1 beta and tumor necrosis factor-alpha of the insulin-like growth factor I messenger ribonucleic acid response to growth hormone in rat hepatocyte primary culture. Endocrinology 138, 1078–1084.CrossRefGoogle ScholarPubMed
Tilg, H, Dinarello, CA and Mier, JW 1997. IL-6 and APPs: anti-inflammatory and immunosuppressive mediators. Immunology Today 18, 428–432.CrossRefGoogle ScholarPubMed
Weese, JS, Rousseau, J, Deckert, A, Gow, S and Reid-Smith, RJ 2011. Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs. BMC Veterinary Research 7, 41.CrossRefGoogle ScholarPubMed
Wolf, M, Böhm, S, Brand, M and Kreymann, G 1996. Proinflammatory cytokines interleukin 1 beta and tumor necrosis factor alpha inhibit growth hormone stimulation of insulin-like growth factor I synthesis and growth hormone receptor mRNA levels in cultured rat liver cells. European Journal of Endocrinology 135, 729–737.CrossRefGoogle ScholarPubMed
Supplementary material: File

Slifierz Supplementary Material

Table S1

Download Slifierz Supplementary Material(File)
File 24.9 KB