Domestic Animal Endocrinology
Volume 38, Issue 3 , Pages 146-156 , April 2010

Maternal social stress during late pregnancy affects hypothalamic-pituitary-adrenal function and brain neurotransmitter systems in pig offspring

  • W. Otten

      Affiliations

    • Behavioral Physiology Research Unit, Research Institute for the Biology of Farm Animals (FBN), Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
    • ,
  • E. Kanitz

      Affiliations

    • Behavioral Physiology Research Unit, Research Institute for the Biology of Farm Animals (FBN), Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
    • ,
  • D. Couret

      Affiliations

    • INRA, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint-Gilles, France
    • Agrocampus Ouest, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France
    • ,
  • I. Veissier

      Affiliations

    • INRA, UR1213, Unité de Recherche sur les Herbivores, F-63122 Saint-Genès-Champanelle, France
    • ,
  • A. Prunier

      Affiliations

    • INRA, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint-Gilles, France
    • Agrocampus Ouest, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France
    • ,
  • E. Merlot

      Affiliations

    • INRA, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35590 Saint-Gilles, France
    • Agrocampus Ouest, UMR1079 Systèmes d’Elevage Nutrition Animale et Humaine, F-35000 Rennes, France
    • Corresponding Author InformationCorresponding author. INRA, UMR SENAH, Domaine de la Prise, F-35590 Saint Gilles, France Tel.: +33 2 23 48 70 55; fax: +33 2 23 48 50 80.

Received 15 May 2009 ,Revised 8 September 2009 ,Accepted 14 September 2009.

References 

  1. Viltart O, Vanbesien-Mailliot CA. Impact of prenatal stress on neuroendocrine programming. Scientific World Journal 2007; 7:1493-1537.
  2. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev. 2008;32:1073–1086
  3. Merlot E, Couret D, Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav Immun. 2008;22:42–51
  4. Fowden AL, Giussani DA, Forhead AJ. Intrauterine programming of physiological systems. Physiology. 2006;21:29–37
  5. Welberg LAM, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol. 2001;13:113–128
  6. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol. 2001;65:427–451
  7. Darnaudéry M, Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev. 2008;57:571–585
  8. Von Borell E, Dobson H, Prunier A. Stress, behaviour and reproductive performance in female cattle and pigs. Horm Behav. 2007;52:130–138
  9. Otten W, Kanitz E, Tuchscherer M, Nürnberg G. Effects of prenatal restraint stress on hypothalamic-pituitary-adrenocortical and sympatho-adrenomedullary axis in neonatal pigs. Anim Sci. 2001;73:279–287
  10. Kranendonk G, Hopster H, Fillerup M, Ekkel ED, Mulder EJH, Taverne MAM. Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Horm Behav. 2006;49:663–672
  11. Haussmann MF, Carroll JA, Weesner GD, Daniels MJ, Matteri RL, Lay DC. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic-pituitary-adrenal (HPA) axis. J Anim Sci. 2000;78:2399–2411
  12. Kanitz E, Otten W, Tuchscherer M. Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. J Endocrinol. 2006;191:207–220
  13. Lay DC, Kattesh HG, Cunnick JE, Daniels MJ, McMunn KA, Toscano MJ, et al. Prenatal stress effects on pig development and response to weaning. J Anim Sci. 2008;86:1316–1324
  14. Jarvis S, Moinard C, Robson SK, Baxter E, Ormandy E, Douglas AJ, et al. Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Hormone Behav. 2006;49:68–80
  15. Breuner CW, Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol. 2002;175:99–112
  16. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci. 1995;15:110–116
  17. Shoener JA, Baig R, Page KC. Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic-pituitary-adrenal axis activity in adult male rats. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1366–R1373
  18. Takahashi LK, Turner JG, Kalin NH. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 1992;574:131–137
  19. Bowman RE, Maclusky NJ, Sarmiento Y, Frankfurt M, Gordon M, Luine VN. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology. 2004;145:3778–3787
  20. Slotkin TA, Kreider ML, Tate CA, Seidler FJ. Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems. Neuropsychopharmacology. 2006;31:904–911
  21. Hayashi A, Nagaoka M, Yamada K, Ichitani Y, Miake Y, Okado N. Maternal stress induces synaptic loss and developmental disabilities of offspring. Int J Dev Neurosci. 1998;16:209–216
  22. Van den Hove DLA, Lauder JM, Scheepens A, Prickaerts J, Blanco CE, Steinbusch HWM. Prenatal stress in the rat alters 5-HT1A receptor binding in the ventral hippocampus. Brain Res. 2006;1090:29–34
  23. Maccari S, Mormède P, Piazza PV, Simon H, Angelucci L, Le Moal M. Hippocampal type I and type II corticosteroid receptors are modulated by central noradrenergic systems. Psychoneuroendocrinology. 1992;17:103–112
  24. Andrews MH, Matthews SG. Programming of the hypothalamo-pituitary-adrenal axis: serotonergic involvement. Stress. 2004;7:15–27
  25. Otten W, Kanitz E, Tuchscherer M, Brüssow KP, Nürnberg G. Repeated administrations of adrenocorticotropic hormone during late gestation in pigs: Maternal cortisol response and effects on fetal HPA axis and brain neurotransmitter systems. Theriogenology. 2008;69:312–322
  26. Couret D, Otten W, Puppe B, Prunier A, Merlot E. Behavioural endocrine and immune responses to repeated social stress in pregnant gilts. Animal. 2009;3:118–127
  27. Klemcke HG, Christenson RK. Porcine fetal and maternal adrenocorticotropic hormone and corticosteroid concentrations during gestation and their relation to fetal size. Biol Reprod. 1997;57:99–106
  28. McPherson RL, Ji F, Wu G, Blanton JR, Kim SW. Growth and compositional changes of fetal tissues in pigs. J Anim Sci. 2004;82:2534–2540
  29. Pond WG, Boleman SL, Fiorotto ML, Ho H, Knabe DA, Mersmann HJ, et al. Perinatal ontogeny of brain growth in the domestic pig. Proc Soc Exp Biol Med. 2000;223:102–108
  30. Félix B, Léger ME, Albe-Fessard D. Stereotaxic Atlas of the Pig Brain. Amsterdam: Elsevier Science BV; 1999;
  31. Lundström K, Dahlberg E, Nyberg L, Snochowski M, Standal N, Edqvist LE. Glucocorticoid and androgen characteristics in two lines of pigs selected for rate of gain and thickness of backfat. J Anim Sci. 1983;56:401–409
  32. Kanitz E, Tuchscherer M, Tuchscherer A, Stabenow B, Manteuffel G. Neuroendocrine and immune responses to acute endotoxemia in suckling and weaned piglets. Biol Neonate. 2002;81:203–209
  33. Fiedler I, Rehfeldt C, Ender K. Histophysiologische Kriterien der Schilddrüsen- und Nebennierenaktivität neugeborener Ferkel nach Behandlung der trächtigen Sauen mit Somatotropin. J Anim Physiol Anim Nutr. 1996;76:199–209
  34. Axelrod J. Purification and properties of phenylethanolamine N-methyl transferase. J Biol Chem. 1962;237:1657–1660
  35. Waymire JC, Bjur R, Weiner N. Assay of tyrosine hydroxylase by coupled decarboxylation of DOPA formed from 1-14 C-L-tyrosine. Anal Biochem. 1971;43:588–600
  36. Lemaire V, Le Moal M, Mormède P. Regulation of catecholamine-synthesizing enzymes in adrenals of Wistar rats under chronic stress. Am J Physiol. 1993;264:R957–962
  37. Kanitz E, Manteuffel G, Otten W. Effects of weaning and restraint stress on glucocorticoid receptor binding capacity in limbic areas of domestic pigs. Brain Res. 1998;804:311–315
  38. Kanitz E, Otten W, Tuchscherer M, Manteuffel G. Effects of prenatal stress on corticosteroid receptor binding and monoamine levels in limbic areas of neonatal pigs at different ages. J Vet Med A. 2003;50:132–139
  39. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin reagent. J Biol Chem. 1951;193:265–275
  40. Löhrke B, Viergutz T, Krüger B. Polar phospholipids from bovine endogenously oxidized low density lipoprotein interfere with follicular thecal function. J Mol Endocrinol. 2005;35:531–545
  41. Siiteri PK, Murai JT, Hammond GL, Nisker JA, Raymore WJ, Kuhn RW. The serum transport of steroid hormones. Recent Prog Horm Res. 1982;38:457–510
  42. Kattesh HG, Charles SF, Baumbach GA, Gillespie BE. Plasma cortisol distribution in the pig from birth to six weeks of age. Biol Neonate. 1990;58:220–226
  43. Heo J, Kattesh HG, Roberts MP, Schneider JF. Plasma levels of cortisol and corticosteroid-binding globulin (CBG) and hepatic CBG mRNA expression in pre- and postnatal pigs. Domest Anim Endocrinol. 2003;25:263–273
  44. Roberts MP, Kattesh HG, Baumbach GA, Gillespie BE, Godkin JD, Schneider JF, et al. Age-related changes in porcine corticosteroid-binding globulin (pCBG) as determined by an enzyme-linked immunosorbent assay. Domest Anim Endocrinol. 2003;24:323–339
  45. Schroeder RJ, Henning SJ. Roles of plasma clearance and corticosteroid-binding globulin in the developmental increase in circulating corticosterone in infant rats. Endocrinology. 1989;124:2612–2618
  46. Duvaux-Ponter C, Roussel S, Tessier J, Sauvant D, Ficheux C, Boissy A. Physiological effects of repeated transport in pregnant goats and their offspring. Anim Res. 2003;52:553–566
  47. Roussel S, Boissy A, Montigny D, Hemsworth PH, Duvaux-Ponter C. Gender-specific effects of prenatal stress on emotional reactivity and stress physiology of goat kids. Hormone Behav. 2005;47:256–266
  48. Couret D, Jamin A, Kuntz-Simon G, Prunier A, Merlot E. Maternal stress during late gestation has moderate but long lasting effects on the immune system of the piglet. Vet Immunol Immunopathol. 2009;131:17–24
  49. Sloboda DM, Moss TJM, Li S, Matthews SG, Challis JRG, Newnham JP. Expression of glucocorticoid receptor, mineralocorticoid receptor, and 11ß-hydroxysteroid dehydrogenase 1 and 2 in the fetal and postnatal ovine hippocampus: ontogeny and effects of prenatal glucocorticoid exposure. J Endocrinol. 2008;197:213–220
  50. Wan S, Hao R, Sun K. Repeated maternal dexamethasone treatments in late gestation increases 11beta-hydroxysteroid dehydrogenase type 1 expression in the hippocampus of the newborn rat. Neurosci Lett. 2005;382:96–101
  51. Chan RKW, Brown ER, Ericsson A, Kovacs KJ, Sawchenko PE. A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci. 1993;13:5126–5138
  52. Kovacs KJ. c-Fos as a transcription factor: a stressful (re)view from functional map. Neurochem Int. 1998;33:287–297
  53. Palamarchouk VS, Zhang JJ, Zhou G, Swiergiel AH, Dunn AJ. Hippocampal norepinephrine-like voltammetric responses to infusion of corticotrophin-releasing factor into the locus coeruleus. Brain Res Bull. 2000;51:319–326
  54. Palamarchouk VS, Swiergiel AH, Dunn AJ. Hippocampal noradrenergic responses to CRF injected into the locus coeruleus of unanesthesized rats. Brain Res. 2002;950:31–38
  55. Luo DD, An SC, Zhang X. Involvement of hippocampal serotonin and neuropeptide Y in depression by chronic unpredicted mild stress. Brain Res Bull. 2008;77:8–12
  56. Zhou J, Li L, Tang S, Cao X, Li Z, Li W, et al. Effects of serotonin depletion on the hippocampal GR/MR and BDNF expression during the stress adaptation. Behav Brain Res. 2008;195:129–138
  57. Otten W, Kanitz E, Tuchscherer M, Puppe B, Nürnberg G. Repeated administrations of adrenocorticotropic hormone during gestation in gilts: Effects on growth, behaviour and immune responses of their piglets. Livest Sci. 2007;106:261–270

PII: S0739-7240(09)00103-9

doi: 10.1016/j.domaniend.2009.09.002

Domestic Animal Endocrinology
Volume 38, Issue 3 , Pages 146-156 , April 2010

Article Tools

* Image Usage & Resolution