Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T16:55:07.797Z Has data issue: false hasContentIssue false
  • English
  • Français

The cortisol response to ACTH in pigs, heritability and influence of corticosteroid-binding globulin

Published online by Cambridge University Press:  24 August 2015

C. Larzul ,
E. Terenina ,
A. Foury ,
Y. Billon ,
I. Louveau ,
E. Merlot  and
P. Mormede
C. Larzul
Affiliation:
INRA, Génétique Animale et Biologie Intégrative (GABI), F-78352 Jouy-en-Josas, France INRA, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), F-31326 Castanet-Tolosan, France INP, ENSAT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31326 Castanet-Tolosan, France INP, ENVT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31076 Toulouse, France
E. Terenina
Affiliation:
INRA, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), F-31326 Castanet-Tolosan, France INP, ENSAT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31326 Castanet-Tolosan, France INP, ENVT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31076 Toulouse, France
A. Foury
Affiliation:
INRA, Nutrition et Neurobiologie Intégrée (NutriNeuro), F-33076 Bordeaux, France
Y. Billon
Affiliation:
INRA, Génétique, Expérimentation et Systèmes Innovants (GenESI), F-17700 Saint-Pierre-d’Amilly, France
I. Louveau
Affiliation:
INRA, Physiologie, Environnement et Génétique pour l’Animal et les Systèmes d’Elevage (UMR1348 PEGASE), F-35590 Saint-Gilles, France Agrocampus Ouest, Physiologie, Environnement et Génétique pour l’Animal et les Systèmes d’Elevage (UMR1348 PEGASE), F-35000 Rennes, France
E. Merlot
Affiliation:
INRA, Physiologie, Environnement et Génétique pour l’Animal et les Systèmes d’Elevage (UMR1348 PEGASE), F-35590 Saint-Gilles, France Agrocampus Ouest, Physiologie, Environnement et Génétique pour l’Animal et les Systèmes d’Elevage (UMR1348 PEGASE), F-35000 Rennes, France
P. Mormede*
Affiliation:
INRA, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), F-31326 Castanet-Tolosan, France INP, ENSAT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31326 Castanet-Tolosan, France INP, ENVT, Génétique, Physiologie et Systèmes d’Elevage (GenPhySE), Université de Toulouse, F-31076 Toulouse, France
*
†E-mail: Pierre.Mormede@toulouse.inra.fr
Get access

Abstract

In the search for biological basis of robustness, this study aimed (i) at the determination of the heritability of the cortisol response to ACTH in juvenile pigs, using restricted maximum likelihood methodology applied to a multiple trait animal model, and (ii) at the study of the relationships between basal and stimulated cortisol levels with corticosteroid-binding globulin (CBG), IGF-I and haptoglobin, all important players in glucose metabolism and production traits. At 6 weeks of age, 298 intact male and female piglets from 30 litters (30 dams and 30 boars) were injected with 250 µg ACTH(1–24) (Synacthen). Blood was taken before ACTH injection to measure basal levels of cortisol, glucose, CBG, IGF-I and haptoglobin, and 60 min later to measure stimulated cortisol levels and glucose. Cortisol increased 2.8-fold after ACTH injection, with a high correlation between basal and stimulated levels (phenotypic correlation, rp=0.539; genetic correlation, rg=0.938). Post-ACTH cortisol levels were highly heritable (h2=0.684) and could therefore be used for genetic selection of animals with a more reactive hypothalamic–pituitary–adrenocortical axis. CBG binding capacity correlated with cortisol levels measured in basal conditions in males only. No correlation was found between CBG binding capacity and post-ACTH cortisol levels. Basal IGF-I concentration was positively correlated with BW at birth and weaning, and showed a high correlation with CBG binding capacity with a strong sexual dimorphism, the correlation being much higher in males than in females. Basal haptoglobin concentrations were negatively correlated with CBG binding capacity and IGF-I concentrations. Complex relationships were also found between circulating glucose levels and these different variables that have been shown to be related to glucose resistance in humans. These data are therefore valuable for the genetic selection of animals to explore the consequences on production and robustness traits, but also point at pigs as a relevant model to explore the underlying mechanisms of the metabolic syndrome including the contribution of genetic factors.

Keywords

ACTH stimulation testcortisolCBGrobustnesspig
Type
Research Article
Information
animal , Volume 9 , Issue 12 , December 2015 , pp. 1929 - 1934
Copyright
© The Animal Consortium 2015 

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

Barat, P, Duclos, M, Gatta, B, Roger, P, Mormede, P and Moisan, MP 2005. Corticosteroid binding globulin gene polymorphism influences cortisol driven fat distribution in obese women. Obesity Research 13, 1485–1490.CrossRefGoogle ScholarPubMed
Berryman, DE, Glad, CAM, List, EO and Johannsson, G 2013. The GH/IGF-1 axis in obesity: pathophysiology and therapeutic considerations. Nature Review Endocrinology 9, 346–356.Google Scholar
Braun, T, Challis, JR, Newnham, JP and Sloboda, DM 2013. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocrine Reviews 34, 885–916.Google Scholar
Carroll, JA, Gaines, AM, Spencer, JD, Allee, GL, Kattesh, HG, Roberts, MP and Zannelli, ME 2003. Effect of menhaden fish oil supplementation and lipopolysaccharide exposure on nursery pigs. I. Effects on the immune axis when fed diets containing spray-dried plasma. Domestic Animal Endocrinology 24, 341–351.Google Scholar
Collier, CT, Williams, PN, Carroll, JA, Welsh, TH and Laurenz, JC 2011. Effect of maternal restraint stress during gestation on temporal lipopolysaccharide-induced neuroendocrine and immune responses of progeny. Domestic Animal Endocrinology 40, 40–50.Google Scholar
Cooper, TA, Roberts, MP, Kattesh, HG and Kojima, CJ 2009. Effects of transport stress, sex, and weaning weight on postweaning performance in pigs. Professional Animal Scientist 25, 189–194.CrossRefGoogle Scholar
Dallman, MF, Akana, SF, Pecoraro, NC, Warne, JP, la Fleur, SE and Foster, MT 2007. Glucocorticoids, the etiology of obesity and the metabolic syndrome. Current Alzheimer Research 4, 199–204.Google Scholar
Desautes, C, Bidanel, JP, Milan, D, Iannuccelli, N, Amigues, Y, Bourgeois, F, Caritez, JC, Renard, C, Chevalet, C and Mormede, P 2002. Genetic linkage mapping of quantitative trait loci for behavioral and neuroendocrine stress response traits in pigs. Journal of Animal Science 80, 2276–2285.Google Scholar
Desautes, C, Bidanel, JP and Mormede, P 1997. Genetic study of behavioral and pituitary-adrenocortical reactivity in response to an environmental challenge in pigs. Physiology and Behavior 62, 337–345.Google Scholar
Edens, FW and Siegel, HS 1975. Adrenal responses in high and low ACTH response lines of chickens during acute heat stress. General and Comparative Endocrinology 25, 64–73.Google Scholar
Fernandez-Real, JM, Pugeat, M, Grasa, M, Broch, M, Vendrell, J, Brun, J and Ricart, W 2002. Serum corticosteroid-binding globulin concentration and insulin resistance syndrome: a population study. Journal of Clinical Endocrinology and Metabolism 87, 4686–4690.Google Scholar
Foury, A, Devillers, T, Sanchez, MP, Griffon, H, Le Roy, P and Mormede, P 2005. Stress hormones, carcass composition and meat quality in Large White x Duroc pigs. Meat Science 69, 703–707.Google Scholar
Foury, A, Geverink, NA, Gil, M, Gispert, M, Hortos, M, Furnols, MFI, Carrion, D, Blott, SC, Plastow, GS and Mormede, P 2007. Stress neuroendocrine profiles in five pig breeding lines and the relationship with carcass composition. Animal 1, 973–982.Google Scholar
Foury, A, Tribout, T, Bazin, C, Billon, Y, Bouffaud, M, Gogué, JM, Bidanel, JP and Mormede, P 2009. Estimation of genetic trends from 1977 to 2000 for stress-responsive systems in French large white and landrace pig populations using frozen semen. Animal 3, 1681–1687.Google Scholar
Garrel, DR 1996. Corticosteroid-binding globulin during inflammation and burn injury: nutritional modulation and clinical implications. Hormone Research 45, 245–251.Google Scholar
Geverink, NA, Foury, A, Plastow, GS, Gil, M, Gispert, M, Hortos, M, Furnols, MFI, Gort, G and Moisan, MP 2006. Cortisol-binding globulin and meat quality in five European lines of pigs. Journal of Animal Science 84, 204–211.Google Scholar
Heegaard, PMH, Stockmarr, A, Piñeiro, M, Carpintero, R, Lampreave, F, Campbell, FM, Eckersall, PD, Toussaint, MJM, Gruys, E and Sorensen, NS 2011. Optimal combinations of acute phase proteins for detecting infectious disease in pigs. Veterinary Research 42, 50.Google Scholar
Hennessy, DP 1986. Metabolic clearance rate of cortisol in pigs: relationship to adrenal responsiveness. Research in Veterinary Science 41, 361–364.Google Scholar
Hennessy, DP and Jackson, PN 1987. Relationship between adrenal responsiveness and growth rate, Manipulating Pig Production: proceedings of the Inaugural Conference of the Australasian Pig Science Association (A.P.S.A.), 23–25 November, Albury, NSW, Australia, pp. 23.Google Scholar
Hennessy, DP, Stelmasiak, T, Johnston, NE, Jackson, PN and Outch, KH 1988. Consistent capacity for adrenocortical response to ACTH administration in pigs. American Journal of Veterinary Research 49, 1276–1283.Google Scholar
Heo, J, Kattesh, HG, Roberts, MP, Morrow, JL, Dailey, JW and Saxton, AM 2005. Hepatic corticosteroid-binding globulin (CBG) messenger RNA expression and plasma CBG concentrations in young pigs in response to heat and social stress. Journal of Animal Science 83, 208–215.Google Scholar
Kadarmideen, HN and Janss, LLG 2007. Population and systems genetics analyses of cortisol in pigs divergently selected for stress. Physiological Genomics 29, 57–65.Google Scholar
Kanitz, E, Otten, W and Tuchscherer, M 2006. Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. Journal of Endocrinology 191, 207–220.Google Scholar
Kranendonk, G, Mulder, EJH, Parvizi, N and Taverne, MAM 2008. Prenatal stress in pigs: experimental approaches and field observations. Experimental and Clinical Endocrinology & Diabetes 116, 413–422.Google Scholar
Lassarre, C, Hardouin, S, Daffos, F, Forestier, F, Frankenne, F and Binoux, M 1991. Serum insulin-like growth factors and insulin-like growth factor binding proteins in the human fetus. Relationships with growth in normal subjects and in subjects with intrauterine growth retardation. Pediatric Research 29, 219–225.Google Scholar
Louveau, I and Bonneau, M 1996. Effect of a growth hormone infusion on plasma insulin-like growth factor-I in Meishan and Large White pigs. Reproduction, Nutrition, Development 36, 301–310.Google Scholar
Mazziotti, G and Giustina, A 2013. Glucocorticoids and the regulation of growth hormone secretion. Nature Reviews Endocrinology 9, 265–276.Google Scholar
Moisan, MP 2010. Genotype-phenotype associations in understanding the role of corticosteroid-binding globulin in health and disease animal models. Molecular and Cellular Endocrinology 316, 35–41.Google Scholar
Moisan, MP 2013. CBG: a cortisol reservoir rather than a transporter. Nature Reviews Endocrinology 9, 78.Google Scholar
Mormede, P, Foury, A, Barat, P, Corcuff, JB, Terenina, E, Marissal-Arvy, N and Moisan, MP 2011a. Molecular genetics of hypothalamic-pituitary-adrenal axis activity and function. Annals of the New York Academy of Science 1220, 127–136.Google Scholar
Mormede, P, Foury, A, Terenina, E and Knap, PW 2011b. Breeding for robustness: the role of cortisol. Animal 5, 651–657.Google Scholar
Mormede, P and Terenina, E 2012. Molecular genetics of the adrenocortical axis and breeding for robustness. Domestic Animal Endocrinology 43, 116–131.Google Scholar
Neggers, SJCMM and van der Lely, AJ 2011. Modulation of glucocorticoid metabolism by the GH-IGF-I axis. Endocrine Development 20, 181–186.Google Scholar
Neumaier, A and Groeneveld, E 1998. Restricted maximum likelihood estimation of covariances in sparse linear models. Genetics, Selection, Evolution 30, 3–26.Google Scholar
Ousova, O, Guyonnet-Duperat, V, Iannuccelli, N, Bidanel, JP, Milan, D, Genet, C, Llamas, B, Yerle, M, Gellin, J, Chardon, P, Emptoz-Bonneton, A, Pugeat, M, Mormede, P and Moisan, MP 2004. Corticosteroid binding globulin: a new target for cortisol-driven obesity. Molecular Endocrinology 18, 1687–1696.Google Scholar
Óvilo, C, González-Bulnes, A, Benítez, R, Ayuso, M, Barbero, A, Pérez-Solana, ML, Barragan, C, Astiz, S, Fernandez, A and López-Bote, C 2014. Prenatal programming in an obese swine model: sex-related effects of maternal energy restriction on morphology, metabolism and hypothalamic gene expression. The British Journal of Nutrition 111, 735–746.Google Scholar
Pastorelli, H, Le Floc’h, N, Merlot, E, Meunier-Salaün, MC, van Milgen, J and Montagne, L 2012. Sanitary housing conditions modify the performance and behavioural response of weaned pigs to feed- and housing-related stressors. Animal 6, 1811–1820.Google Scholar
Perogamvros, I, Ray, DW and Trainer, PJ 2012. Regulation of cortisol bioavailability – effects on hormone measurement and action. Nature Reviews Endocrinology 8, 717–727.CrossRefGoogle ScholarPubMed
Piñeiro, C, Piñeiro, M, Morales, J, Carpintero, R, Campbell, FM, Eckersall, PD, Toussaint, MJM, 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.Google Scholar
Piñeiro, M, Piñeiro, C, Carpintero, R, Morales, J, Campbell, FM, Eckersall, PD, Toussaint, MJM and Lampreave, F 2007b. Characterisation of the pig acute phase protein response to road transport. The Veterinary Journal 173, 669–674.Google Scholar
Pugeat, MM, Chrousos, GP, Nisula, BC, Loriaux, DL, Brandon, D and Lipsett, MB 1984. Plasma cortisol transport and primate evolution. Endocrinology 115, 357–361.Google Scholar
Richard, E, Fernandez-Real, JM, Lopez-Bermejo, A, Ricart, W, Dechaud, H, Pugeat, M and Moisan, MP 2009. Corticosteroid binding globulin and glucocorticoid receptor genotypes influence body composition in a male population. International Journal of Genetics and Molecular Biology 1, 59–63.Google Scholar
Roberts, MP, Kattesh, HG, Baumbach, GA, Gillespie, BE, Godkin, JD, Schneider, JF and Saxton, AM 2003. Age-related changes in porcine corticosteroid-binding globulin (pCBG) as determined by an enzyme-linked immunosorbent assay. Domestic Animal Endocrinology 24, 323–339.Google Scholar
Weiler, U, Claus, R, Schnoebelen-Combes, S and Louveau, I 1998. Influence of age and genotype on endocrine parameters and growth performance: a comparative study in Wild boars, Meishan and Large White boars. Livestock Production Science 54, 21–31.Google Scholar
Zhang, SH, Hennessy, DP and Cranwell, PD 1990. Pituitary and adrenocortical responses to corticotropin-releasing factor in pigs. American Journal of Veterinary Research 51, 1021–1025.Google Scholar