Portal de Periódicos da CAPES

The Role of Early Environmental Events in Regulating Neuroendocrine Development: Moms, Pups, Stress, and Glucocorticoid Receptors

1996; Wiley; Volume: 794; Issue: 1 Linguagem: Inglês

10.1111/j.1749-6632.1996.tb32517.x

1749-6632

Darlene Francis, Josie Diorio, Patricia LaPlante, Shelley Weaver, Jonathan R. Seckl, Michael J. Meaney,

Hormonal Regulation and Hypertension

Annals of the New York Academy of SciencesVolume 794, Issue 1 p. 136-152 The Role of Early Environmental Events in Regulating Neuroendocrine Development: Moms, Pups, Stress, and Glucocorticoid Receptors DARLENE FRANCIS, DARLENE FRANCIS Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorJOSIE DIORIO, JOSIE DIORIO Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorPATRICIA LAPLANTE, PATRICIA LAPLANTE Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorSHELLEY WEAVER, SHELLEY WEAVER Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorJONATHAN R. SECKL AND, JONATHAN R. SECKL AND Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorMICHAEL J. MEANEY, Corresponding Author MICHAEL J. MEANEY Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUAddress correspondence to Michael J. Meaney, Developmental Neuroendocrinology Laboratory, Douglas Hospital Research Centre, 6875 Boulevard LaSalle, Montreal, Quebec H4H 1R3, Canada. Tel: (514)762-3048; fax: (514) 762-3034; e-mail: [email protected]Search for more papers by this author DARLENE FRANCIS, DARLENE FRANCIS Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorJOSIE DIORIO, JOSIE DIORIO Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorPATRICIA LAPLANTE, PATRICIA LAPLANTE Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorSHELLEY WEAVER, SHELLEY WEAVER Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorJONATHAN R. SECKL AND, JONATHAN R. SECKL AND Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUSearch for more papers by this authorMICHAEL J. MEANEY, Corresponding Author MICHAEL J. MEANEY Developmental Neuroendocrinology Laboratory Douglas Hospital Research Centre Departments of Psychiatry, and Neurology and Neurosurgery McGill University Montreal, Canada, Molecular Endocrinology Laboratory Department of Medicine University of Edinburgh Edinburgh, Scotland, UK EH4 2XUAddress correspondence to Michael J. Meaney, Developmental Neuroendocrinology Laboratory, Douglas Hospital Research Centre, 6875 Boulevard LaSalle, Montreal, Quebec H4H 1R3, Canada. Tel: (514)762-3048; fax: (514) 762-3034; e-mail: [email protected]Search for more papers by this author First published: September 1996 https://doi.org/10.1111/j.1749-6632.1996.tb32517.xCitations: 87AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL References 1 Antoni, F. A. 1986. Hypothalamic control of ACTH secretion: Advances since the discovery of 41-residue corticotropin-releasing factor. Endocr. Rev. 7: 351– 370. 2 Rivier, C. and P. M. Plotsky. 1986. Mediation by corticotropin-releasing factor of adenohypophysial hormone secretion. Annu. Rev. Physiol. 48: 475– 489. 3 Whitnall, M. H. 1993. Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog. Neurobiol. 40: 573– 629. 4 Baxter, J. D. and J. B. Tyrrell. 1987. The adrenal cortex. In Endocrinology and Metabolism. P. Felig, J. D. Baxter, A. E. Broadus, and L. A. Frohman, Eds.: 385– 511. McGraw-Hill. New York . 5 Brindley, D. N. and Y. Rolland. 1989. Possible connections between stress, diabetes. obesity, hypertension and altered lipoprotein metabolism that may result in atherosclerosis. Clin. Sci. 77: 453– 461. 6 Munck, A., P. M. Guyre and N. J. Holbrook. 1984. Physiological functions of glucocorticoids in stress and their relations to pharmacological actions. Endocr. Rev. 5: 25– 44. 7 Dallman, M. F., S. Akana, C. S. Cascio, D. N. Darlington, L. Jacobson and N. Levin. 1987. Regulation of ACTH secretion: Variations on a theme of B. Recent Prog. Horm. Res. 43: 113– 173. 8 Dallman, M. F., S. F. Akana, K. A. Scribner, M. J. Bradbury, C. D. Walker, A. M. Strack and C. S. Cascio. 1993. Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J. Neuroendocrinol. 4: 517– 526. 9 De Kloet, E. R. 1991. Brain corticosteroid receptor balance and homeostatic control. Front. Neuroendocrinol. 12: 95– 164. 10 Feldman, S. and N. Conforti. 1980. Participation of the dorsal hippocampus in the glucocorticoid negative-feedback effect on adrenocortical activity. Neuroendocrinology 30: 52– 55. 11 Jacobson, L. and R. M. Sapolsky. 1991. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenal axis. Endocr. Rev. 12: 118– 134. 12 Keller-Wood, M. and M. F. Dallman. 1984. Corticosteroid inhibition of ACTH secretion. Endocr. Rev. 5: 1– 24. 13 McEwen, B. S., E. R. De Kloet, and W. H. Rostene, 1986. Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 66: 1121– 1150. 14 Diorio, D., V. Viau and M. J. Meaney. 1993. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13: 3839– 3847. 15 Bhatnagar, S., N. Shanks and M. J. Meaney. Effects of chronic stress on hypothalamic-pituitary-adrenal and immune responses to acute stress in handled and non-handled rats. Dev. Psychobiol. In press. 16 Meaney, M. J., D. O'Donnell, V. Viau, S. Bhatnagar, A. Sarrieau, J. W. Smythe, N. Shanks and C.-D. Walker. 1994. Corticosteroid receptors in rat brain and pituitary during development and hypothalamic-pituitary-adrenal (HPA) function. In Receptors and the Developing Nervous System. P. McLaughlin, and I. Zagon, Eds.: 163– 202. Chapman and Hall. London . 17 Meaney, M. J., D. H. Aitken, S. Bhatnagar, Ch. Van Berkel and R. M. Sapolsky. 1988. Postnatal handling attenuates neuroendocrine, anatomical, and cognitive impairments related to the aged hippocampus. Science 238: 766– 768. 18 Kerr, D. S., L. W. Campbell, S. -Y. Hao and P. W. Landfield. 1989. Corticosteroid modulation of hippocampal potentials: Increased effect with aging. Science 245: 1505– 1509. 19 Meaney, M. J., D. H. Aitken and R. M. Sapolsky. 1991. Environmental regulation of the adrenocortical stress response in female rats and its implications for individual differences in aging. Neurobiol. Aging 12: 31– 38. 20 Issa, A., W. Rowe, S. Gauthier and M. J. Meaney. 1990. Hypothalamic-pituitary-adrenal activity in aged cognitively impaired and cognitively unimpaired aged rats. J. Neurosci. 10: 3247– 3254. 21 Sapolsky, R. M. 1990. Glucocorticoids, hippocampal damage and the glutaminergic synapse. Prog. Brain Res. 86: 13– 23. 22 Levine, S. 1975. Psychosocial factors in growth and development. In Society, Stress and Disease. L. Levi, Ed.: 43– 50. Oxford University Press. London . 23 Leon, M., P. G. Croskerry and G. K. Smith. 1978. Thermal control of mother-infant contact in rats. Physiol. & Behav. 21: 793– 811. 24 Jans, J. Latent inhibition in nonhandled rats reared on different nest surface temperatures. Dev. Psychobiol. In press. 25 Lee, M. H. S. and D. I. Williams. 1974. Changes in licking behaviour of rat mother following handling of young. Anim. Behav. 22: 679– 681. 26 Lee, M. H. S. and D. I. Williams. 1975. Long term changes in nest condition and pup grouping following handling of rat litters. Dev. Psychobiol. 8: 91– 95. 27 Bell, R. W., W. Nitschke, T. H. Gorry and T. Zachma. 1971. Infantile stimulation and ultrasonic signaling: A possible mediator of early handing phenomena. Dev. Psychobiol. 4: 181– 191. 28 Jans, J. and B. C. Woodside. 1990. Nest temperature: Effects on maternal behavior, pup development, and interactions with handling. Dev. Psychobiol. 23: 519– 534. 29 Hennessy, M. B., J. Vogt and S. Levine. 1982. Strain of foster mother determines long-term effects of early handling: Evidence for maternal mediation. Physiol. Psychol. 10: 153– 157. 30 Meyers, M. M., S. A. Brunell, H. N. Shair, J. M. Squire and M. A. Hofer. 1989. Relationship between maternal behavior of SHR and WKY dams and adult blood pressures of cross-foctered F1 pups. Dev. Psychobiol. 22: 55– 67. 31 Calhoun, J. B. 1962. The ecology and sociology of the Norway rat. H. E. W. Public Health Service. Bethesda , Maryland . 32 Plotsky, P. M. and M. J. Meaney. 1993. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol. Brain Res. 18: 195– 200. 33 Blanchard, C., R. R. Sakai, B. S. McEwen, S. M. Weiss and R. J. Blanchard. Stress: Behavioral, brain and neuroendocrine correlates. Brain Behav. Sci. In press. 34 Sapolsky, R. M. 1982. The endocrine stress response and social status in the wild baboon. Horm. Behav. 16: 279– 292. 35 Sapolsky, R. M. 1993. The physiology of dominance in stable vs. unstable social hierarchies. In Primate Social Conflict. W. Mason, and S. Mendoza, Eds.: 171– 204. SUNY Press. New York . 36 Purves, D. 1988. A Torphic Theory of Development. University of Chicago Press. Chicago , IL . 37 Levine, S. and G. W. Lewis. 1958. The relative importance of experimenter contact in an effect produced by extrastimulation in infancy. J. Comp. Physiol. Psychol. 52: 368– 369. 38 Meaney, M. J. and D. H. Aitken. 1985. The effects of early postnatal handling on the development of hippocampal glucocorticoid receptors: Temporal parameters. Dev. Brain Res. 22: 301– 304. 39 Mohammed, A. H., B. G. Henriksson, S. Soderstrom, T. Ebendal, T. Olsson and J. R. Seckl. 1993. Environmental influences on the central nervous system and their influences for the aging rat. Behav. Brain Res. 57: 183– 191. 40 Ader, R. and L. J. Grota. 1969. Effects of early experience on adrenocortical reactivity. Physiol. & Behav. 4: 303– 305. 41 Bohn, M. C., D. Dean, S. Hussain and R. Giuliano. 1994. Development of mRNAs for glucocorticoid and mineralocorticoid receptors in rat hippocampus. Dev. Brain Res. 77: 157– 162. 42 Van Eekelen, J. A. M., W. Jiang, E. R. De Kloet and M. C. Bohn. 1988. Distribution of the mineralocorticoid and glucocorticoid receptor mRNAs in the rat hippocampus. J. Neurosci. Res. 21: 88– 94. 43 O'Donnell, D., S. Larocque, J. R. Seckl and M. J. Meaney. Developmental changes in hippocampal glucocorticoid and mineralocorticoid receptor messenger RNA expression in relation to morphological changes in cell size. Submitted. 44 Rosenfeld, P., W. Sutanto, S. Levine and E. R. De Kloet. 1988. Ontogeny of type I and type II corticosteroid receptors in the rat hippocampus. Dev. Brain Res. 42: 113– 118. 45 Sarrieau, A., S. Sharma and M. J. Meaney. 1988. Postnatal development and environmental regulation of hippocampal glucocorticoid and mineralocorticoid receptors in the rat. Dev. Brain Res. 43: 158– 162. 46 Meaney, M. J., D. H. Aitken, S. Sharma, V. Viau and A. Sarrieau. 1989. Postnatal handling increases hippocampal type II, glucocorticoid receptors and enhances adrenocortical negative-feedback efficacy in the rat. Neuroendocrinology 51: 597– 604. 47 Meaney, M. J., R. M. Sapolsky and B. S. McEwen. 1985. The development of the glucocorticoid receptor system in the rat limbic brain: I. Ontogeny and autoregulation. Dev. Brain Res. 18: 159– 164. 48 Meaney, M. J. and D. H. Aitken. 1985. [3H]Dexamethasone binding in rat frontal cortex. Brain Res. 328: 176– 180. 49 Sharma, S., J. B. Mitchell and M. J. Meaney. Interaction between thyroid hormones and central serotonin in the development of glucocorticoid receptor systems in the rat. Submitted. 50 Meaney, M. J., D. H. Aitken and R. M. Sapolsky. 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. Neuroendocrinology 45: 278– 283. 51 Banker, G. A. and M. W. Cowan. 1977. Rat hippocampal neurons in dispersed cell culture. Brain Res. 126: 397– 425. 52 Mitchell, J. B., W. Rowe. P. Boksa and M. J. Meaney. 1990. Serotonin regulates type II. corticosteroid receptor binding in cultured hippocampal cells. J. Neurosci. 10: 1745– 1752. 53 Savard, P., Y. Merand, T. Di Paolo and A. Dupont. 1984, Thyroid hormone regulation of serotonin metabolism in developing rat brain. Brain Res. 292: 99– 108. 54 Mitchell, J. B., L. J. Iny and M. J. Meaney. 1990. The role of serotonin in the development and environmental regulation of hippocampal type II corticosteroid receptors. Dev. Brain Res. 55: 231– 235. 55 Smythe, J. W., W. Rowe and M. J. Meaney. 1994. Neonatal handling alters serotonin turnover and serotonin type 2 receptor density in selected brain regions. Dev. Brain Res. 80: 183– 189. 56 Mitchell, J. B., K. Betito, W. Rowe, P. Boksa and M. J. Meaney. 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. 57 Teitler, M., R. A. Lyon, K. H. Davis and K. H. Glennon. 1987. Selectivity of serotoninergic drugs for multiple brain serotonin receptors. Biochem. Pharmacol. 36: 3265– 3271. 58 Teitler, M., S. Leonhardt, E. L. Weisberg and B. J. Hoffman. 1992. 4-[125I]Iodo-(2.5-dimethoxy)phenylisopropylamine and [3H]-ketanserin labelling of 5-hydroxy-tryptamine2 (5-HT2) receptors in mammalian cells transfected with rat 5-HT2 cDNA: Evidence for multiple states and multiple 5-HT2 receptors. Mol. Pharmacol. 42: 328– 335. 59 Holmes, M., S. Larocque, J. R. Seckl and M. J. Meaney. Developmental changes in 5-HT2A receptor binding and receptor mRNA expression in the rat forebrain. Mol. Brain Res. Submitted. 60 Sanders-Bush, E., M. Tsutsumi and K. D. Burris. 1990. Serotonin receptors and phosphatidylinositol turnover. Ann. N. Y. Acad. Sci. 600: 224– 236. 61 Yoshimasa, T., D. R. Sibley, M. Bouvier, R. J. Lefkowitz and M. G. Caron. 1987. Cross-talk between cellular signalling pathways suggested by phorbolester-induced adenylate cyclase phosphorylation. Nature 327: 67– 70. 62 Parent, A. R., S. Sharma, R. Quirion and M. J. Meaney. 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. Exp. Ther. Submitted. 63 Ike, J., H. Canton and E. Sanders-Bush. 1995. Developmental switch in the hippocampal serotonin receptor linked to phosphoinositide hydrolysis. Brain Res. 678: 49– 54. 64 Lucas, J. J. and R. Hen. 1995. New players in the 5-HT receptor field: Genes and knockouts. Trends Pharmacol. Sci. 16: 246– 262.78. 65 Pepin, M. C., S. Beaulieu and N. Barden. 1989. Antidepressants regulate glucocorticoid receptor messenger RNA concentrations in primary neuronal cultures. Mol. Brain Res. 6: 77– 83. 66 Pepin, M. C., M. V. Govidan and N. Barden. 1992. Increased glucocorticoid receptor gene promoter activity after antidepressant treatment. J. Pharmacol. Exp. Ther. 41: 1016– 1024. 67 Törk, I. 1990. Anatomy of serotonergic systems. Ann. N. Y. Acad. Sci. 600: 9– 35. 68 De Groot, R. P. and P. Sassone-Corsi. 1993. Hormonal control of gene expression: Multiplicity and versatility of cyclic adenosine 3|M',5|M'-monophosphate-responsive nuclear regulators. Mol. Endocrinol. 5: 145– 153. 69 Habener, J. 1990. Cyclic AMP response element binding proteins: A cornucopia of transcription factors. Mol. Endocrinol. 4: 1087– 1094. 70 Imagawa, M., R. Chiu and M. Karin. 1987. Transcription factor AP-2 mediates induction by two different signal-transduction pathways: Protein kinase C and cAMP. Cell 51: 251– 260. 71 Montminy, M. R., G. A. Gonzalez and K. K. Yamamoto. 1990. Regulation of cAMP-inducible genes by CREB. Trends Neurosci. 12: 184– 188. 72 Sheng, M. and M. E. Greenberg. 1990. The regulation and function of c-fos and other early immediate genes in the nervous system. Neuron 4: 477– 485. 73 Vallejo, M. 1994. Transcriptional control of gene expression by cAMP-response element binding proteins. J. Neuroendocrinol. 6: 587– 596. 74 Walton, K. M. and R. P. Rehfuss. 1992. Molecular mechanisms of cAMP-regulated gene expression. Mol. Neurobiol. 4: 197– 201. 75 Yamamoto, K. K., G. A. Gonzales, W. H. Briggs III and M. R. Montimy. 1988. Phosphorylation-induced binding and transcriptional efficiency of nuclear factor CREB. Nature 334: 494– 498. 76 Leclerc, S., B. Xie, R. Roy and M. V. Govindan. 1991. Purification of a human glucocorticoid receptor gene promoter-binding protein. J. Biol. Chem. 266: 8711– 8719. 77 Strahle, U., A. Schmidt, G. Kelsey, A. F. Stewart, T. J. Cole, W. Schmid and G. Schutz. 1992. At least three promoters direct expression of the mouse glucocorticoid receptor gene. Proc. Natl. Acad. Sci. 89: 6731– 6735. 78 Meaney, M. J., J. Diorio, J. Yau, L. Donaldson and J. R. Seckl. Neonatal handling stimulates cAMP formation and altered expression of transcription factors involved in cAMP-regulated gene expression: The role of serotonin. Submitted. 79 Delmas, V., F. Van Der Hoorn, B. Mellstrom, B. Jegou and P. Sassone-Corsi. 1993. Induction of CREM activator proteins in spermatids: Down-stream targets and implications for haploid germ cell differentiation. Mol. Endocrinol. 7: 1502– 1514. 80 Strobl, J. S. 1990. A role for DNA methylation in vertebrate gene expression. Mol. Endocrinol. 4: 181– 183. 81 Vaccarino, F. M., M. D. Hayward, H. N. Le, D. J. Hartigan, R. S. Duman and E. J. Nestler. 1993. Induction of immediate early genes by cyclic AMP in primary cultures of neurons from rat cerebral cortex. Mol. Brain Res. 19: 76– 82. Citing Literature Volume794, Issue1Understanding Aggressive Behavior in ChildrenSeptember 1996Pages 136-152 ReferencesRelatedInformation