Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress; pp. 61–72

Developmental Neuroscience

Volumn 18, Issue 1-2, 1996, Pages 61-72

  Meaney, Michael J ^a   Diorio, Josie ^a   Francis, Darlene ^a   Widdowson, Judith ^a,b   La Plante, Patricia ^a   Caldji, Christian ^a   Sharma, Shalcti ^a   Jonathan, R ^a   Paul, Seckl ^b   Plotsky, M ^c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glucocorticoid receptors; Hippocampus; HPA axis; Neuronal differentiation; Serotonin; Stress

Indexed keywords

ARGIPRESSIN; BRAIN RECEPTOR; CATECHOLAMINE DERIVATIVE; CORTICOSTEROID; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; ENDOTOXIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYPOPHYSIS HORMONE; MESSENGER RNA; SEROTONIN; THYROID HORMONE; TRANSCORTIN;

ADRENERGIC SYSTEM; ANIMAL CELL; ANIMAL EXPERIMENT; BRAIN NERVE CELL; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; ENVIRONMENTAL FACTOR; FOREBRAIN; FRONTAL CORTEX; GENE EXPRESSION REGULATION; HOMEOSTASIS; HORMONE RELEASE; HORMONE SYNTHESIS; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MATERNAL DEPRIVATION; NEGATIVE FEEDBACK; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DENSITY; REVIEW; SIGNAL TRANSDUCTION; STRESS; THALAMUS MIDLINE NUCLEUS;

ADRENAL CORTEX; ANIMALS; ENVIRONMENT; GENE EXPRESSION REGULATION; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; PROSENCEPHALON; RECEPTORS, GLUCOCORTICOID; STRESS;

EID: 0030038741     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000111396     Document Type: Article

References (139)

1. Adcr R, Grata U (1969) Effects of early experience on adrenocortical reactivity. Physiol Behav 4:303-305.
2. Akana SF, Jacobson L. Cascio CS, Shinsako J, Dallman MF (1988) Constant corticosterone replacement normalizes basal adrenocorti-cotropin (ACTH) but permits sustained ACTH hypersecretion after stress in adrenalectomized rats. Endocrinology 122:1337-1342.
3. Antoni FA (1986) Hypothalamic control of ACTH secretion: Advances since the discovery of 41 -residue corticotropin-releasing factor. Endocr Rev 7:351-370.
4. Banker GA. Cowan MW (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126:397-425.
5. Baxter JD, Tyrrell JB (1987) The adrenal cortex; in Felig P, Baxter JD. Broadus AE, Frohman LA (eds): Endocrinology and Metabolism. New York, McGraw-Hill, pp 385-511.
6. Bell RW. Nitschkc W, Gorry TH. Zachman T (1971) Infantile stimulation and ultrasonic signaling: A possible mediator of early handing phenomena. Dev Psychobiol 4:181-191.
7. Bhatnagar S. Shanks N. Mcancy MJ (1995) Hypothalamic-pituitary-adrenal function in handled and nonhandled rats in response to chronic stress. J Neuroendocrinology 7:107- 119.
8. Bhatnagar S. Shanks N. Mcancy MJ: Effects of chronic stress on hypothalamic-piluitary-adre-nal and immune responses to acute stress in handled and nonhandled rats. Dev Psychobiol, in press.
9. Blanchard C. Sakai RR. Me Ewen BS. Weiss SM. Blanchard RJ: Subordination stress: Behavioral. brain and neuroendocrine correlates. Brain Behav Sci, in press.
10. Bodnoff SR, Suranyi-Cadotte BE. Quirion R. Meaney MJ (1987) Postnatal handling reduces novelty-induced fear and increases ['H]fluni-trazepam binding in rat brain. Eur J Pharmacol 144:105-108.
11. Bodnoff SR. Suranyi-Cadotte BE. Quirion R. Meaney MJ (1989) Role of the central benzodiazepine receptor system in behavioral habituation to novelty. Behav Neurosci 103:209-212.
12. Bradbury MJ. Cascio CS. Scribner KA. Dallman MF (1991) Stress-induced adrcnocoriicotropin secretion: Diurnal responses and decreases during stress in the evening are not dependent on corticosterone. Endocrinology 129:99-108.
13. Brindley DN. Rolland Y (1989) Possible connections between stress, diabetes, obesity, hypertension and altered lipoprotein metabolism that may result in atherosclerosis. Clinical Sci 77: 453-461.
14. Calhoun JB (1962) The ecology and sociology of the Norway rat. Belhesda, H.E.W. Public-Health Service.
15. Chrousos GP. Gold PW (1992) The concepts of stress and stress system disorders. JAMA 267: 1244-1252.
16. Daly M (1973) Early stimulation of rodents: A critical review of present interpretations. Br J Psychol 64:435-460.
17. Dallman MF. Akana S. Cascio CS. Darlington DN. Jacobson L. Levin N (1987) Regulation of ACTH secretion: Variations on a theme of B. Rec Prog Horm Res 43:113-173.
18. Dallman MF. Akana SF. Scribner KA. Bradbury MJ. Walker C-D. Strack AM. Cascio CS (1993) Stress, feedback and facilitation in the hypo-thalamo-pituitary-adrenal axis. J Neuroendo-crinol 4:517-526.
19. de Goeij DCE, Kvetnansky R. Whitnall MH. Jezova D. Berkcnbosch F. Tildcrs FJH (1991) Repeated stress-induced activation of corti-eoirophin-relcasing factor neurons enhances vasopressin stores and colocalization with cor-ticotrophin-releasing factor in the median eminence of rats. Neuroendocrinology 53:150-159.
20. de Groot RP. Sassonc-Corsi P (1993) Hormonal control of gene expression: Multiplicity and versatility of cyclic adenosine 3’, 5’-monophos-phate-responsive nuclear regulators. Mol Endocrinol 5:145- 153.
21. De Kloet ER (1991) Brain corticosteroid receptor balance and homeostatic control. Front Neu-roendocrinol 12:95-164.
22. Dencnberg VII (1964) Critical periods, stimulu input, and emotional reactivity: A theory of infantile stimulation. Psychol Rev 71:335-351.
23. Diorio D. Viau V. Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypolhalamic-pituitary-adrenal responses to stress. J Neurosci 13: 3839-3847.
24. Feldman S. Conforti N (1980) Participation of the dorsal hippocampus in the glucocorticoid negative feedback effect on adrenocortical activity. Ncurocndocrinology 30:52-55.
25. Feldman S, Weidenfeld J (1995) Neural mechanisms involved in the corticosteroid feedback effects on the hypothalamo-pituitary-adreno-eortical axis. Prog Neurobiol 45:129-141.
26. Femandcz-Tcrucl A. Escorihucla RM. Driscoll P. Tobena A, Battig K (1992a) Differential effects of early stimulation and/or perinatal fiumazcnil treatment in young Roman low- and high-avoidance rats. Psychopharmacology 108: 170-176.
27. Fcmandcz-Tcrucl A, Escorihucla RM. Nunez JF. Goma M. Driscoll P and Tobena A (1992b) Early stimulation effects on novelty-induced behavior in two psychogenetically-selecled rat lines with divergent cmtionality profiles. Ncu-rosci Lett 137:185-188.
28. Ferre P. Nunez JF, Garcia E. Tobena A, Escorihucla RM, Femandez-Teruel A: Postnatal handling reduces anxiety as measured by emotionality rating and hyponcophagia in female rats. Pharmacol Biochcm Behav. in press.
29. Francis D, Plolsky PM. Meaney MJ: Handling increases CRH mRNA expression in selected hypothalamic neuronal populations, submitted.
30. Gray J A (1987) The Psychology of Fear and Stress. Cambridge. Cambridge Publications.
31. Habener J (1990) Cyclic AMP response element binding proteins: A cornucopia of transcription factors. Mol Endocrinol 4:1087-1094.
32. Hennessy MB. Vogt J, Levine S (1982) Strain of foster mother determines long-term effects of early handling: Evidence for maternal mediation. Physiol Psychol 10:153-157.
33. Herman JP. Schafer MK-H. Young EA. Thompson R. Douglass J. Akil H and Watson SJ (1989) Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pitu-ilary-adrcnocortical axis. J Neurosci 9:3072-3082.
34. Hess JL. Dencnberg VH. Jarrow MX. Pfeifer WD (1969) Modification of the corticosterone response curve as a function of handling in infancy. Physiol Behav 4:109-112.
35. I lilakivi-Clarkc LA, Turkka J. Lister RG, Linnoila M (1991) Effects of early postanatal handling on brain b-adrenoceptors and behavior in tests related to stress. Brain Res 542:286-292.
36. Holmes M. Larocque S, Seckl JR. Mcancy MJ: Developmental changes in 5-HT2A receptor binding and receptor mRNA expression in the rat forebrain. Mol Brain Res. submitted.
37. Ike J. Canton H, Sanders-Bush E (1995) Developmental switch in the hippocampal serotonin receptor linked to phosphoinosilide hydrolysis. Brain Res 678:49-54.
38. Imagawa M. Chiu R, Karin M (l987)Transcription factor AP-2 mediates induction by two different signal-transduction pathways: Protein kinase C and cAMP. Cell 51:251-260.
39. Imaki T. Nahan J-L, Rivicr C, Sawchenko PE, Vale W (1991) Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J Neurosci 11:585-599.
40. Issa A. Rowe W, Gauthier S. Meaney MJ (1990) Hypothalamic-pituitary-adrenal activity in aged cognitively impaired and cognitively unimpaired aged rats. J Neurosci 10:3247-3254.
41. Jacobson L, Akana SF. Cascio CS, Shinsako J, Dallman MF (1988) Circadian variations in plasma corticosterone permit normal termination of adrcnocoriicotropin responses to stress. Endocrinology 122:1342-1348.
42. Jacobson L. Sapolsky RM (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituilary-adrcnal axis. Endocr Rev 12:118-134.
43. Jans J. Woodside BC (1990) Nest temperature: Effects on maternal behavior, pup development. interactions with handling. Dev Psychobiol 23:519-534.
44. Jans J: Latent inhibition in nonhandled rats reared on different nest surface temperatures. Dev Psychobiol. in press.
45. Keller-Wood M, Dallman MF (1984) Corticosteroid inhibition of ACTH secretion. Endocr Rev 5:1-24.
46. Kerr DS. Campbell LW. Hao S-Y. Landfield PW(1989) Corticosteroid modulation of hippocampal potentials: Increased effect with aging. Science 245:1505-1509.
47. Lazar G Jr. Duda E. Lazar G (1992) Effect of RU 38486 on TNF production and toxicity. Fed Eur Biochcm Soc 308:137-140.
48. Leclerc S. Xic B, Roy R, Govindan MV (1991) Purification of a human glucocorticoid receptor gene promoter-binding protein. J Biol Chcm 266:8711-8719.
49. LeDoux JE (1992) Emotion and the amygdala: in Agglcton JP (ed): The amygdala: Ncurobio-logical aspects of emotion, memory, and mental dysfunction. New York. Wilcy-Liss, pp 339-351.
50. Lee MHS, Williams DI (1974) Changes in licking behaviour of rat mother following handling of young. Anim Behav 22:679-681.
51. Lee MHS, Williams DI (1975) Long term changes in nest condition and pup grouping following handling of rat litters. Dev Psychobiol 8:91-95.
52. Leon M. Croskerry PG, Smith GK (1978) Thermal control of mother-infant contact in rats. Physiol Behav 21:793-811.
53. Levin N. Akana SF, Jacobson L. Kuhn RW, Siitcri PK, Dallman MF (1987) Plasma ACTH is more sensitive than transcortin production or thymus weight to inhibition by corticosterone in rats. Endocrinology 121:1104-1110.
54. Levine S (1957) Infantile experience and resistcnce to physiological stress. Science 126:405-406.
55. Levine S (1962) Plasma-free corticosteroid response to electric shock in rats stimulated in infancy. Science 135:795-796.
56. Levine S (1975) Psychosocial factors in growth and development; in Levi L (ed): Society, Stress and Disease. London. Oxford University Press, pp 43-50.
57. Levine S. Haltmcyer GC. Karas GG. Denenberg VH (1967) Physiological and behavioral effects of infantile stimulation. Physiol Bchav 2:55-63.
58. Lightman SL, Harbuz MS (1993) Expression of corticotropin-relcasing factor mRNA in response to stress. Ciba Found Syntp 172:173-187.
59. Lucas JJ. Hen R (1995) New players in the 5-HT receptor field: Genes and knockouts. Trends Pharmacol Sci 16:246-262.
60. Maccari S. Piazza PV, Kabbaj M. Barbazanges A, Simon H. Le Moal M (1994) Adoption reverses the long-term impairments in glucocorticoid feedback induced by prenatal stress. J Ncurosci 15:110-116.
61. Mason D (1991) Genetic variation in the stress response: Susceptibility to experimental allergic encephalomyelitis and implications for human inflammatory disease. Immunol Today 12:57-60.
62. McCormick CM. Smythe J. Sharma S. Meancy MJ (1994) Sex-dependent effects of prenatal stress on the development of brain corticosteroid receptor systems and hypothalamic-pituitary-adrenal responses to stress. Dev Brain Res 79: 260-266.
63. McEwen BS. de Kloet ER. Rostenc WH (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121-1150.
64. McEwen BS, Steller E (1993) Stress and the individual: Mechanisms leading to disease. Arch Intern Med 153:2093-2101.
65. Meaney MJ. Aitken DH (1985a) The effects of early postnatal handling on the development of hippocampal glucocorticoid receptors: Temporal parameters. Dev Brain Res 22:301-304.
66. Meancy MJ, Aitken DH (1985b) HlDexametha-sone binding in rat frontal cortex. Brain Res 328:176-180.
67. Meancy MJ. Aitken DH. Bhatnagar S. Van Berkel Ch. Sapolsky RM (1988) Postnatal handling attenuates neuroendocrine, anatomical, and cognitive impairments related to the aged hippocampus. Science 238:766-768.
68. Meaney MJ, Aitken D, Bodnoff SR. Iny LJ, Tatarcwicz JE. Sapolsky RM (1985a) Early, postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Bchav Neurosci 99:760-765.
69. Meaney MJ. Aitken DH. Sapolsky RM (1987) Thyroid hormones influence the development of hippocampal glucocorticoid receptors in the rat: A mechanism for the effects of postnatal handling on the development of the adrenocortical stress response. Ncuroendocrinology 45: 278-283.
70. Meaney MJ. Aitken DH. Sapolsky RM (1991) Environmental regulation of the adrenocortical stress response in female rats and its implications for individual differences in aging. Ncu-robiol Aging 12:31-38.
71. Meaney MJ. Aitken DH, Sharma S. Viau V. Sar-rieau A (1989) Postnatal handling increases hippocampal type II. glucocorticoid receptors and enhances adrcncocortical negative-feedback efficacy in the rat. Ncuroendocrinology 51:597-604.
72. Meaney MJ, Aitken DH. Sharma S. Viau V (1992) Basal ACTH. corticosterone, and corticosterone-binding globulin levels over the diurnal cycle, and hippocampal type I and type 11 corticosteroid receptors in young and old, handled and nonhandled rats. Neuroendocrinology 55: 204-213.
73. Meaney MJ. Bodnoff SR. O'Donnell D, Rowe W, Sarrieau A. Rose GM. Poirier J. Scckl JR (1993) Glucocorticoids as regulators of neuron survival and repair in the aged brain: in Cuello AC (ed): Restorative Neurology. Amsterdam, Elsevier, vol 6, pp 267-289.
74. Meaney MJ. Diorio J, Widdowson J, LaPlante P, Caldji C, Scckl JR. Plotsky PM: Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress, submitted.
75. Meaney MJ. Diorio J. Yau J. Donaldson L, Seckl JR: Neonatal handling stimulates cAMP formation and altered expression of transcription factors involved in cAMP-regulatcd gene expression: The role of serotonin, submitted.
76. Meancy MJ. O'Donnell D, Viau V. Bhatnagar S, Sarrieau A. Smythe JV. Shanks N. Walker C-D (1994) Corticosteroid Receptors in Rat Brain and Pituitary’ During Development and Hypo-thalamic-Pituitary-Adrcnal (HPA) Function; in McLaughlin P. Zagon I (eds): Receptors and the Developing Nervous System. London. Chapman and Hall, pp 163-202.
77. Meaney MJ. Sapolsky RM, McEwen BS (1985c) The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Dev Brain Res 18:159-164.
78. Mitchell JB. Betito K. Rowe W. Boksa P. Meaney MJ (1992) Serotonergic regulation of type II corticosteroid receptor binding in cultured hippocampal cells: The role of serotonin-induced increases in cAMP levels. Neuroscience 48: 631-639.
79. Mitchell JB. Iny U. Meaney MJ (1990a) The role of serotonin in the development and environmental regulation of hippocampal type 11 corticosteroid receptors. Dev Brain Res 55:231-235.
80. Mitchell JB. Rowe W. Boksa P. Meaney MJ (1990b) Serotonin regulates type II. corticosteroid receptor binding in cultured hippocampal cells. J Ncurosci 10: 1745-1752.
81. Mohammed AH, Henriksson BG. Soderstrom S. Ebcndal T. Olsson T. Seckl JR (1993) Environmental influences on the central nervous system and their influences for the aging rat. Behav Brain Res 57:183-191.
82. Montminy MR. Gonzalez GA. Yamamoto KK(1990) Regulation of cAMP-inducible genes by CREB. Trends Neurosci 16:184-188.
83. Munck A, Guyre PM. Holbrook NJ (1984) Physiological functions of glucocorticoids in stress and their relations to pharmacological actions. Endocr Rev 5:25-44.
84. O'Donnell D. Larocque S. Seckl JR. Meaney MJ (1994) Postnatal handling alters glucocorticoid, but not mineralocorticoid mRNA expression in adult rats. Mol Brain Res 26:242-248.
85. O'Donnell D. Larocque S. Seckl JR. Meaney MJ: Developmental changes in hippocampal glucocorticoid and mineralocorticoid receptor messenger RNA expression in relation to morphological changes in cell size, submitted.
86. Pacak K. Kvetnansky R. Palkovits M. Fukuhara K. Yadid G, Kopin IJ. Goldstein DS (1993) Adrenalectomy augments in vivo release of norcpincphcrinc in the paraventricular nucleus during immobilization stress. Endocrinology 133:1404-1410.
87. Parent AR, Sharma S. Quirion R. Meaney MJ: Developmental profile of diacylglycerol and inositol phosphate production induced by the stimulation of muscarinic, glutamate, metabotropic, serotonin and endothelin receptors in the hippocampus of neonatally handled rats. J Pharmacol ExpThcr. submitted.
88. Pepin MC. Beaulieu S. Barden N (1989) Antidepressants regulate glucocorticoid receptor messenger RNA concentrations in primary neuronal cultures. Mol Brain Res 6:77-83.
89. Pepin MC, Govidan MV. Barden N (1992) Increased glucocorticoid receptor gene promoter activity after antidepressant treatment. J Pharmacol Exp Titer 41:1016-1024.
90. Plotsky PM. Cunningham ET. Widmaicr EP (1989) Catecholaminergic modulation of corticotropin-releasing factor and adrenocorticotropin secretion. Endocr Rev 10:437-458.
91. Plotsky PM. Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotropin-relcasing factor (CRF) ntRNA. median eminence CRF content and stress-induced release in adult rats. Mol Brain Res 18:195-200.
92. Plotsky PM. Otto S, Sapolsky RM (1986) Inhibition of immunoreactive corticotropin-releasing factor secretion into the hypophysial-portal circulation by delayed glucocorticoid feedback. Endocrinology 119:1126-1130.
93. Plotsky PM, Sawchenko PE (1987) Hypophysial-portal plasma levels, median eminence content and immunohistochcmical staining of corticotropin releasing factor, arginine vasopressin and oxytocin following pharmacological adrenalectomy. Endocrinology 120:1361-1369.
94. Plotsky PM. Vale W (1984) Hemorrhage-induced secretion of corticotropin-relcasing factor-like immunorcactivity into rat hypophysial portal circulation and its inhibition by glucocorticoids. Endocrinology 114:164-169.
95. Purves D (1988) A Trophic Theory of Development. University of Chicago Press. Chicago.
96. Ramchandra RN. Sehon A. Berczi I (1992) Neuro-hormonal defense in endotoxin shock. Brain Behav Immunol 6:157-169.
97. Rivier C. Plotsky PM (1986) Mediation by corticotropin-releasing factor of adenohypophysial hormone secretion. Annu Rev Physiol 48: 475-489.
98. Rosenfold P. Sulanlo SV. Levine S. De Kloet ER (1988) Ontogeny of type I and type II corticosteroid receptors in the rat hippocampus. Dev Brain Res 42:113-118.
99. Sanders-Bush H, Tsutsumi M, Burris KD (1990) Serotonin receptors and phosphatidylinositol turnover. Ann NY Acad Sci 600:224-235.
100. Sapotsky RM (1982) The endocrine stress response and social status in the wild baboon. Hoim Bchav 16:279-292.
101. Sapolsky RM (1993) The physiology of dominance in stable vs. unstable social hierarchies; in Mason W, Mendoza S (eds): Primate Social Conflict. New York. SUNY Press, pp 171- 204.
102. Sapolsky RM. Armanini MP. Packan DR, Sutton SW. Plotsky PM (1990) Glucocorticoid feedback inhibition of adrenocorticotropic hormone secretagogue release: Relationship to corticosteroid receptor occupancy in various limbic sites. Neuroendocrinology 51:328-336.
103. Sapolsky RM. Donnelly TM (1985) Vulnerability to stress-induced tumor growth increases with age in rats: Role of glucocorticoids. Endocrinology 117:662-666.
104. Sapolsky RM, Krey LC. McEwen BS (1984) Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Nat Acad Sci USA 81: 6174-6177.
105. Sapolsky RM. McEwen BS (1985) Down-regulation of neural corticosterone receptors by corticosterone and dexamethasone. Brain Res 339: 161-165.
106. Sarrieau A. Sharma S. Meaney MJ (1988) Postnatal development and environmental regulation of hippocampal glucocorticoid and mineralo-corticoid receptors in the rat. Dev Brain Res 43:158-162.
107. Savard P. Merand Y. Di Paolo T, Dupont A (1984) Thyroid hormone regulation of serotonin metabolism in developing rat brain. Brain Res 292: 99-108.
108. Sawchenko PE (1987) Adrenalectomy-induced enhancement of CRF and vasopressin immunore-activity in parvocellular neurosecretory neurons: Anatomic, peptide, and steroid specificity. J Neurosci 7:1093-1106.
109. Seckl JR, Meaney MJ (1994) Early life events and later development of ischaemic heart disease. Lancet 342:1236.
110. Shanks N. Larocque S, Meaney MJ (1995) Neonatal endotoxin exposure alters the development of the hypothalamic-pituilary-adrenal axis: Early illness and later responsivity to stress. J Neurosci 15:376-384.
111. Shanks N, Meaney MJ (1994) Hypothalamic-pitu-itary-adrenal responses to endotoxin challenge in neonatal rats: Mediation via CRH. J Neu-roendocrino! 6:375-383.
112. Sharma S, Mitchell JB. Meaney MJ: Interaction between thyroid hormones and central serotonin in the development of glucocorticoid receptor systems in the rat, submitted.
113. Sheng M, Greenberg ME (1990) The regulation and function of c-fos and other early immediate genes in the nervous system. Neuron 4:477-485.
114. Smythe JW, McCormick CM, Meaney MJ: Median eminence corticotrophin-rclcasing hormone (CRH) content following prenatal stress and postnatal handling. Behav Brain Res, in press.
115. Smythe JW, McCormick CM, Rochford J, Meaney MJ (1994a) The interaction between prenatal stress and neonatal handling on nociceptive response latencies in male and female rats. Physiol Behav 55:971-974.
116. Smythe JW, Rowe W, Meaney MJ (1994b) Neonatal handling alters serotonin turnover and serotonin type 2 receptor density in selected brain regions. Dev Brain Res 80:183-189.
117. Spencer RL, Miller AH, Stein M, McEwen BS(1991) Corticosterone regulation of type I and type II adrenal steroid receptors in brain, pituitary, and immune system. Brain Res 549:236-246.
118. Sternberg EM, Young Jr WS. Bemardini R, Gold PW (1989) A central nervous defect in the stress response is associated with susceptibility to streptococcal cell wall arthritis in Lewis rats. Proc Nat Acad Sci USA 86:2374-2378.
119. Strahlc U, Schmidt A, Kelsey G. Stewart AF, Cole TJ, Schmid W, Schutz G (1992) At least three promoters direct expression of the mouse glucocorticoid receptor gene. Proc Natl Acad Sci USA 89:6731-6735.
120. Strobl JS (1990) A role for DNA methylation in vertebrate gene expression. Mol Endocrinol 4: 181-183.
121. Teitler M, Leonhardt S, Weisberg EL, Hoffman BJ(1992) 4-[5-I]Iodo-(2,5,-dimethoxy) phenyl-isopropylamine and [’HJ-ketanserin labelling of 5-hydroxytryptamine2 (5-HT,) receptors in mammalian cells transfected with rat 5-HT, cDNA: Evidence for multiple states and multiple 5-HT: receptors. Mol Pharmacol 42:328-335.
122. Teitler M, Lyon RA, Davis KH, Glennon KH (1987) Selectivity of serotoninergic drugs for multiple brain serotonin receptors. Biochem Pharmacol 36:3265-3271.
123. Thrivikraman KV, Plotsky PM (1993a) Absence of glucocorticoid negative feedback to moderate hemorrhage in conscious rats. Am J Physiol 264:E497-E503.
124. Thrivikraman KV, Plotsky PM (1993b) Stressor-specific susceptibility of HPA-axis activity to fast-feedback in conscious rats (abstract No 357). 75th Annu Endocr Soc Meet, Las Vegas.
125. Tork I (1990) Anatomy of serotonergic systems. Ann NY Acad Sci 600:9-35.
126. Vaccarino FM, Hayward MD, Le HN, Hartigan DJ, Duman RS, Nestler EJ (1993) Induction of immediate early genes by cyclic AMP in primary cultures of neurons from rat cerebral cortex. Mol Brain Res 19:76-82.
127. Vallejo M (1994) Transcriptional control of gene expression by cAMP-response element binding proteins. J Neuroendocrinol 6:587-596.
128. Van Eekclen JAM, Jiang W, De Kloet ER, Bohn MC (1988) Distribution of the mineralocorti-coid and glucocorticoid receptor mRN As in the rat hippocampus. J Neurosci Res 21:88-94.
129. Viau V, Meaney MJ: The inhibitory effect of testosterone on hypothalamic-pituilary-adrenal responses to stress in the male rat: Role of the medial preoptic area. J Neurosci, in press.
130. Viau V, Sharma S, Plotsky PM, Meaney MJ (1993) The hypothalamic-pituitary-adrenal response to stress in handled and nonhandled rats: Differences in stress-induced plasma ACTH secretion are not dependent upon increased corticosterone levels. J Neurosci 13:1097-1105.
131. Vinogradova OS (1975) Functional organization of the limbic system in the process of registration of information: Facts and hypotheses; in: Isaacson RL, Pribram K (eds): The Hippocampus. New York, Plenum Press, vol 2, pp 1-70.
132. Weinstock M, Matlina E, Maor GI, Rosen H, McEwen BS (1992) Prenatal stress selectively alters reactivity of the hypothalamic-pituitary-adrenal system in the female rat. Brain Res 595:195-198.
133. Walton KM, Rehfuss RP (1992) Molecular mechanisms of cAMP-reguiated gene expression. Mol Neurobiol 4:197-201.
134. Whitnall MH (1993) Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 40:573-629.
135. Williams RF (1981) Colonisation of the developing body by bacteria: in Davis JA, Dobbing J (eds): Scientific Foundations of Paediatrics. London, William Heinemann Medical Books, pp 1045-1065.
136. Woodside B, Jans J, Plotsky PM, Meaney MJ: Maternal behavior of mothers of handled and nonhandled rat pups, submitted.
137. Yamamoto KK, Gonzales GA, Briggs III WH, Montimy MR (1988) Phosphorylation-induced binding and transcriptional efficiency of nuclear factor CREB. Nature 334:494-498.
138. Yoshimasa T, Sibley DR, Bouvier M, Lefkowitz RJ, Caron MG (1987) Cross-talk between cellular signalling pathways suggested by phor-bol-ester-induced adenylate cyclase phosphorylation. Nature 327:67-70.
139. Zarrow MX, Campbell PS, Denenberg VH (1972) Handling in infancy: Increased levels of the hypothalamic corticotropin releasing factor (CRF) following exposure to a novel situation. Proc Soc Exp Biol Med 356:141-143.