Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain

International Journal of Developmental Neuroscience

Volumn 26, Issue 3-4, 2008, Pages 259-268

  Desbonnet, Lieve ^a   Garrett, Lillian ^a   Daly, Emma ^b   McDermott, Kieran W ^b   Dinan, Timothy G ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

c Fos; Corticotrophin releasing factor; Gender; Maternal separation; Swim stress; Vasopressin

Indexed keywords

ARGIPRESSIN; CORTICOTROPIN RELEASING FACTOR; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALADJUSTMENT; MALE; MATERNAL DEPRIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SEX DIFFERENCE; SWIMMING; THALAMUS MIDLINE NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; ARGININE VASOPRESSIN; BRAIN; CORTICOTROPIN-RELEASING HORMONE; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; MALE; MATERNAL DEPRIVATION; NEUROSECRETORY SYSTEMS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SEX CHARACTERISTICS; SEX FACTORS; STRESS, PSYCHOLOGICAL; SWIMMING; VASOPRESSINS;

RATTUS;

EID: 41649120126     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2008.02.004     Document Type: Article

References (63)

1. Aguilera G., and Rabadan-Diehl C. Vasopressinergic regulation of the hypothalamic-pituitary-adrenal axis: implications for stress adaptation. Regul. Pept. 96 (2000) 23-29
2. Arborelius L., Owens M.J., Plotsky P.M., and Nemeroff C.B. The role of corticotropin-releasing factor in depression and anxiety disorders. J. Endocrinol. 160 1 (1999) 1-12
3. Avishai-Eliner S., Hatalski C.G., Tabachnik E., Eghbal-Ahmadi M., and Baram T.Z. Differential regulation of glucocorticoid receptor messenger RNA by maternal deprivation in immature rat hypothalamus and limbic regions. Dev. Brain Res. 114 (1999) 265-268
4. Barna I., Bálint E., Baranyi J., Bakos N., Makara G.B., and Haller J. Gender-specific effect of maternal deprivation on anxiety and corticotropin-releasing hormone mRNA expression in rats. Brain Res. Bull. 62 (2003) 85-91
5. Bingham B., Williamson M., and Viau V. Androgen and estrogen receptor-β distribution within spinal projecting and neurosecretory neurons in the paraventricular nucleus of the male rat. J. Comp. Neurol. 499 (2006) 911-923
6. Caldji C., Francis D., Sharma S., Plotsky P.M., and Meaney M.J. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22 3 (2000) 219-229
7. Cook C.J. Stress induced CRF in the paraventricular nucleus, and both CRF and GABA release in the amygdala. Physiol. Behav. 82 (2004) 751-762
8. Daniels W.M., Pietersen C.Y., Carstens M.E., and Stein D.J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 19 1-2 (2004) 3-14
9. Dinan T.G., Lavelle E., Scott L.V., Newell-Price J., Medbak S., and Grossman A.B. Desmopressin normalizes the blunted adrenocorticotropin response to corticotropin-releasing hormone in melancholic depression: evidence of enhanced vasopressinergic responsively. J. Clin. Endocrinol. Metab. 84 (1999) 2238-2240
10. Feldman S., and Weidenfeld J. The excitatory effects of the amygdala on hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res. Bull. 45 4 (1998) 389-393
11. Ferrini M.G., Grillo C.A., Piroli G., de Kloet E.R., and De Nicola A.F. Sex difference in glucocorticoid regulation of vasopressin mRNA in the paraventricular hypothalamic nucleus. Cell. Mol. Neurobiol. 17 6 (1997) 671-686
12. Greisen M.H., Bolwig T.G., Husum H., Nedergaard P., and Wörtwein G. Maternal separation affects male copulatory behaviour and hypothalamic corticotropin releasing factor in concert. Behav. Brain Res. 158 (2005) 367-375
13. Halbreich U., and Kahn L. Atypical depression, somatic depression and anxious depression in women: are they gender-preferred phenotypes?. J. Affect. Disord. 102 1-3 (2007) 245-258
14. Han T.M., and De Vries G.J. Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J. Neurosci. 54 (2003) 502-510
15. Heim C., Newport D.J., Bonsall R., Miller A.H., and Nemeroff C.B. Altered pituitary-adrenal axis responses to provocative challenge test in adult survivors of childhood abuse. Am. J. Psychiatry 158 (2001) 575-581
16. Herman J.P., Wiegand S.J., and Watson S.J. Regulation of basal corticotropin-releasing hormone and arginine vasopressin mRNA expression in the paraventricular nucleus: effects of selective hypothalamic differentiations. Endocrinology 127 5 (1990) 2408-2417
17. Hofer M.A., Brunelli S.A., and Shair H.N. Potentiation of isolation-induced vocalization by brief exposure of rat pups to maternal cues. Dev. Psychobiol. 27 8 (1994) 503-517
18. Huot R.L., Gonzalez M.E., Ladd C.O., Thrivikraman K.V., and Plotsky P.M. Foster litters prevent hypothalamic-pituitary-adrenal axis sensitization mediated by neonatal maternal separation. Psychoneuroendocrinology 29 2 (2004) 279-289
19. Huot R.L., Thrivikraman K.V., Meaney M.J., and Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 158 4 (2001) 366-373
20. Kalinyak J.E., Griffin C.A., Hamilton R.W., Bradshaw J.G., Perlman A.J., and Hoffman A.R. Developmental and hormonal regulation of GR-mRNA in the rat. J. Clin. Invest. 84 (1989) 1843-1848
21. Keck M.E. Corticotropin-releasing factor, vasopressin and receptor systems in depression and anxiety. Amino Acids 31 3 (2006) 241-250
22. Keck M.E., Ohl F., Holsboer F., and Muller M.B. Listening to mutant mice: a spotlight on the role of CRF/CRF receptor systems in affective disorders. Neurosci. Biobehav. Rev. 29 4-5 (2005) 867-889
23. Kessler R.C., Davis C.G., and Kendler K.S. Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey. Psychol. Med. 27 5 (1997) 1101-1119
24. Kovács K.J., Földes A., and Sawchenko P.E. Glucocorticoid negative feedback selectively targets vasopressin transcription in parvocellular neurosecretory neurons. J. Neurosci. 20 10 (2000) 3843-3852
25. Kovács K.J., and Mezey E. Dexamethasone inhibits corticotropin-releasing factor gene expression in the rat paraventricular nucleus. Neuroendocrinology 46 4 (1987) 365-368
26. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., and Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122 (2000) 81-103
27. Ladd C.O., Thrivikraman K.V., Huot R.L., and Plotsky P.M. Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 30 (2005) 520-533
28. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J. Neurobiol. 36 3 (1998) 357-378
29. Landgraf R. The involvement of the vasopressin system in stress related disorders. CNS Neurol. Disord. - Drug Targets 5 (2006) 167-179
30. Landgraf R., Kessler M.E., Bunck M., Murgatroyd C., Spengler D., Zimbelmann M., Nussbaumer M., Czibere L., Turck C.W., Singewald N., Rujescu D., and Frank E. Candidate genes of anxiety-related behaviour in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci. Biobehav. Rev. 31 1 (2007) 89-102
31. Lehmann J., Pryce C.R., Bettschen D., and Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 64 4 (1999) 705-715
32. Liu X., Wang C.A., Ye A.L., Jiang P., and Chen Y.Z. Effects of glucocorticoids and other steroids on arginine vasopressin release from rat hypothalamic slices. Sheng Li Xue Bao 47 2 (1995) 201-206
33. Ma X.-M., and Aguilera G. Transcriptional responses of the vasopressin and corticotropin-releasing hormone genes to acute and repeated intraperitoneal hypertonic saline injection in rats. Mol. Brain Res. 68 1-2 (1999) 129-140
34. MacMillan H.L., Fleming J.E., Streiner D.L., Lin E., Boyle M.H., Jamieson E., Duku E.K., Walsh C.A., Wong M.Y., and Beardslee W.R. Childhood abuse and lifetime psychopathology in a community sample. Am. J. Psychiatry 158 11 (2001) 1878-1883
35. Makino S., Shibasaki T., Yamauchi N., Nishioka T., Mimoto T., Wakabayashi I., Gold P.W., and Hashimoto K. Psychological stress increased corticotropin-releasing hormone mRNA and content in the central nucleus of the amygdala but not in the hypothalamic paraventricular nucleus in the rat. Brain Res. 850 1-2 (1999) 136-143
36. Matthews K., Dalley J.W., Matthews C., Tsai T.H., and Robbins T.W. Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse 40 1 (2001) 1-10
37. McIntosh J., Anisman H., and Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Dev. Brain Res. 113 (1999) 97-106
38. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., Seckl J.R., and Plotsky P.M. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 18 1-2 (1996) 49-72
39. Müller M.B., Landgraf R., and Keck M.E. Vasopressin, major depression, and hypothalamic-pituitary-adrenocortical desensitization. Biol. Psychiatry 48 (2000) 330-333
40. Patten S.B. Depressive symptoms and disorders, levels of functioning and psychosocial stress: an integrative hypothesis. Med. Hypotheses 53 3 (1999) 210-216
41. Peiffer A., Lapointe B., and Barden N. Hormonal regulation of type ll glucocorticoid receptor messenger ribonucleic acid in rat brain. Endocrinology 129 4 (1991) 2166-2174
42. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., and Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30 (2005) 2192-2204
43. Pryce C.R., and Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 27 1-2 (2003) 57-71
44. Purba J.S., Hoogendijk W.J., Hofman M.A., and Swaab D.F. Increased number of vasopressin- and oxytocin-expressing neurons in the paraventricular nucleus of the hypothalamus in depression. Arch. Gen. Psychiatry 53 2 (1996) 137-143
45. Renard G.M., Rivarola M.A., and Suarez M.M. Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int. J. Dev. Neurosci. 25 6 (2007) 373-379
46. Roskoden T., Hanke J., Yilmazer-Hanke D., and Schwegler H. Reduced number of CRF-containing neurons in the central amygdala correlated with enhanced locomotor activity following early postnatal corticosterone treatment in the Wistar rat. Behav. Brain Res. 165 (2005) 221-228
47. Sánchez M., Aguado F., Sánchez-Toscano F., and Saphier D. Neuroendocrine and immunocytochemical demonstrations of decreased hypothlamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139 (1998) 579-587
48. Schmidt M., Enthoven L., van Woezik J.H.G., Levine S., de Kloet E.R., and Oitzel M.S. The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J. Neuroendocrinol. 16 (2004) 52-57
49. Schmidt M., Levine S., Oitzel M.S., van der Mark M., Müller M.B., Holsboer F., and de Kloet E.R. Glucocorticoid receptor blockade disinherits pituitary-adrenal activity during the stress hypo responsive period of the mouse. Endocrinology 146 (2005) 1458-1464
50. Seale J.V., Wood S.A., Atkinson H.C., Lightman S.L., and Harbuz M.S. Organizational role for testosterone and estrogen on adult hypothalamic-pituitary adrenal axis in the male rat. Endocrinology 146 4 (2005) 1973-1982
51. Shapiro R.A., Xu C., and Dorsa D.M. Differential transcriptional regulation of rat vasopressin gene expression by estrogen receptor alpha and beta. Endocrinology 141 11 (2000) 4056-4064
52. Shea A., Walsh C., Macmillan H., and Steiner M. Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 30 2 (2005) 162-178
53. Slotten H.A., Kalinichev M., Hagan J.J., Marsden C.A., and Fone K.C. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res. 1097 1 (2006) 123-132
54. Suchecki D., Duarte Palma B., and Tufik S. Pituitary-adrenal axis and behavioural responses of maternally deprived juvenile rats to the open field. Behav. Brain Res. 111 1-2 (2000) 99-106
55. Swanson L.W., and Simmons D.M. Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol. 285 4 (1989) 413-435
56. Tichomirowa M.A., Keck M.E., Schneider H.J., Paez-Pereda M., Renner U., Holsboer F., and Stalla G.K. Endocrine disturbances in depression. J. Endocrinol. Invest. 28 1 (2005) 89-99
57. Vazquez D.M., Eskandari R., Phelka A., and Lopez J.F. Impact of maternal deprivation on brain corticotropin-releasing hormone circuits: prevention of CRH receptor-2 mRNA changes by desipramine treatment. Neuropsychopharmacology 28 5 (2003) 898-909
58. Veenema A.H., Blume A., Nuederle D., Buwalda B., and Neumann I.D. Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 24 (2006) 1711-1720
59. Veenema A.H., Bredewold R., and Neumann I.D. Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32 5 (2007) 437-450
60. Volpi S., Rabadan-Diehl C., and Aguilera G. Vasopressinergic regulation of the hypothalamic pituitary adrenal axis and stress adaptation. Stress 7 2 (2004) 75-83
61. Wismer Fries A.B., Ziegler T.E., Kurian J.R., Jacoris S., and Pollack S.D. Early experience in humans is associated with changes in neuropathies critical for regulating social behaviour. PNAS 102 47 (2005) 17237-17240
62. Workel J.O., Oitzl M.S., Fluttert M., Lesscher H., Karssen A., and de Kloet E.R. Differential and age dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of Brown Norway rats from youth to senescence. J. Neuroendocrinol. 13 (2001) 569-580
63. Yi S.J., Masters J.N., and Baram T.Z. Effects of specific GR antagonists on CRH gene expression in the PVN of neonatal rats. Dev. Brain Res. 73 (1993) 253-259