Influence of Perinatal Stress on the Hormone Content in Immune Cells of Adult Rats: Dominance of ACTH

Abstract

Rat dams were stressed by total deprivation of food and water for 48 h just before or directly after delivery and the offspring were studied when adult. The immune cells’ hormone content (ACTH, histamine, serotonin, and T₃) was measured by immunocytochemical flow cytometry. The elevation of ACTH content in males was convincing in each cell type (lymphocytes, monocytes and granulocytes, and mast cells). The change in histamine and T₃ content was inconsistent, while serotonin level did not change at all. As ACTH is the key hormone in the General Adaptation Syndrome, it seems likely that the perinatal stress primarily caused elevation in ACTH level and it was provoking the life-long hormonal imprinting. There was a difference between the reaction of males and females (with males’ advance), which points to the gender dependence of the phenomenon. It is important that the effect of stress on the offspring was similar in case of direct (prenatal, in the mother) and indirect (postnatal, transmitted by milk) stress treatment, which calls attention to the danger of stress during this latter period.

Key words

prenatal stress - postnatal stress - hormones - ACTH - immunity - hormonal imprinting

References

• 1 Selye H. A syndrome produced by diverse nocuous agents.  Nature. 1936;  138 32
• 2 Goldstein DS, Kopin IJ. Evolution of concepts of stress.  Stress. 2007;  10 109-120
• 3 Kopin IJ. Definitions of stress and sympathetic neuronal responses.  Ann NY Acad Sci. 1995;  771 19-30
• 4 Kyrou I, Tsigos C. Stress mechanisms and metabolic complications.  Horm Metab Res. 2007;  39 430-438
• 5 Berczi I. The stress concept and neuroimmunoregulation in modern biology.  Ann N Y Acad Sci. 1998;  851 3-12
• 6 Redei EE. Molecular genetics of the stress-responsive adrenocortical axis.  Ann Med. 2008;  40 139-148
• 7 Csaba G, Kovács P, Pállinger É. Immunologically demonstrable hormone-like molecules (triiodothyronine, insulin, digoxin) in rat white blood cells and mast cells.  Cell Biol Int. 2004;  28 487-490
• 8 Blalock JE. β-endorphin in immune cells.  Immunol Today. 1998;  19 191-192
• 9 Smith EM, Morrill AC, Meyer WJ, Blalock JE. Corticotropin releasing factor induction of leukocyte-derived immunoreactive ACTH and endorphins.  Nature. 1986;  321 881-882
• 10 Panerai AE, Sacerdote P. Endorphin in immune system: a role at last.  Immunol Today. 1997;  18 317-319
• 11 Csaba G, Pállinger É. β-endorphin in granulocytes.  Cell Biol Int. 2002;  26 741-743
• 12 Blalock JE. Proopiomelanocortin and the immune-neuroendocrine connection.  Ann N Y Acad Sci. 1999;  885 161-172
• 13 Csaba G, Kovács P, Pállinger É. In vitro effect of biogenic amines on the hormone content of immune cells of the peritoneal fluid and thymus. Is there a hormonal network inside the immune system?.  Cell Biol Int. 2007;  31 224-228
• 14 Pállinger É, Csaba G. Influence of acute stress on the triiodothyronine (T₃) and serotonin content of rat's immune cells.  Acta Physiol Hung. 2005;  92 47-52
• 15 Csaba G, Kovács P, Tóthfalusi L, Pállinger É. Prolonged effect of stress (water and food deprivation) at weaning or in adult age on the triiodothyronine and histamine content of immune cells.  Horm Metab Res. 2005;  37 711-715
• 16 Inczefi-Gonda Á, Csaba G, Dobozy O. Effect of neonatal insulin treatment on adult receptor binding capacity in rats.  Horm Metab Res. 1982;  14 221-222
• 17 Csaba G. The present state in the phylogeny and ontogeny of hormone receptors.  Horm Metab Res. 1984;  16 329-335
• 18 Klein SL, Rager DR. Prenatal stress alters immune function in the offspring of rat.  Dev Psychobiol. 1995;  28 321-336
• 19 Tuchscherer M, Kanitz E, Otten W, Tuchscherer A. Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs.  Vet Immunol Immunopathol. 2002;  86 195-203
• 20 Götz AA, Wittlinger S, Stefanski V. Maternal social stress during pregnancy alters immune function and immune cell numbers in adult male Long-Evans rat offspring during stressful life-events.  Neuroimmunol. 2007;  185 95-102
• 21 Ruiz RJ, Avant KC. Effects of maternal prenatal stress on infant outcomes: a synthesis of literature.  ANS Adv Nurs Sci. 2005;  28 345-355
• 22 Merlot E, Couret D, Otten W. Prenatal stress, fetal imprinting and immunity.  Brain Behav Immun. 2008;  22 42-51
• 23 Vanbesien-Mailliot CC, Wolowczuk I, Mairesse J, Vitart O, Delacre M, Khalife J, Chartier-Harlin MC, Maccari S. Prenatal stress has pro-inflammatory consequences on the immune system in adult rats.  Psychoneuroendocrinology. 2007;  32 114-124
• 24 Park MK, Hoang TA, Belluzzi JD, Leslie FM. Gender specific effect of neonatal handling on stress reactivity of adolescent rats.  Neuroendocrinol. 2003;  15 289-295
• 25 Slotten HA, Kalinchev M, Hagan JJ, Marsden CA, Fone KC. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects.  Brain Res. 2006;  1097 123-132
• 26 Makara GB, Domokos A, Mergi Z, Csabai K, Barna I, Zelena D. Gender-specific regulation of the hypothalamo-pituitary-adrenal axis and the role of vasopressin during the neonatal period.  Ann N Y Acad Sci. 2008;  1148 439-445
• 27 Csaba G. Phylogeny and ontogeny of hormone receptors: the selection theory of receptor formation and hormonal imprinting.  Biol Rev. 1980;  55 47-63
• 28 Csaba G. Hormonal imprinting: its role in the evolution and development of hormones and receptors.  Cell Biol Int. 2000;  24 407-414
• 29 Tchernitchin A, Tchernitchin N. Imprinting of heterodifferentation by prenatal or perinatal exposure to hormones, pharmaceuticals, pollutants and other agents and conditions.  Med Sci Res. 1992;  20 391-397
• 30 Csaba G, Inczefi-Gonda Á. Life-long effect of a single neonatal treatment with estradiol or progesterone on rat uterine estrogen receptor binding capacity.  Horm Metab Res. 1992;  24 167-171
• 31 Csaba G, Karabélyos C, Inczefi-Gonda Á, Pállinger É. Three-generation investigation on serotonin content in rat immune cells long after beta-endorphin exposure in late pregnancy.  Horm Metab Res. 2005;  37 172-177
• 32 Csaba G, Inczefi-Gonda Á. Transgenerational effect of a single neonatal benzpyrene treatment on the glucocorticoid receptor of the rat thymus.  Hum Exp Toxicol. 1998;  17 88-92
• 33 Csaba G, Karabélyos C. Transgenerational effect of a single neonatal benzpyrene treatment (imprinting) on the sexual behavior of adult female rats.  Hum Exp Toxicol. 1997;  16 553-556
• 34 Csaba G, Kovács P, Pállinger É. Transgenerational effect of neonatal vitamin A or D treatment (hormonal imprinting) on the hormone content of rat immune cells.  Horm Metab Res. 2007;  39 197-201
• 35 Tekes K, Gyenge M, Folyovich A, Csaba G. Influence of neonatal vitamin A or vitamin D treatment on the concentration of biogenic amines and their metabolites in the adult rat brain.  Horm Metab Res. 2008;  , December 3 [Epub ahead of print]
• 36 Nelson KG, Sakay Y, Eitzman B, Steel T, MacLachlan JA. Exposure to diethylstilbestrol during a critical developmental period of the mouse reproductive tract leads to persistent induction of two estrogen-regulated genes.  Cell Growth Diff. 1994;  5 115-119

Correspondence