Critical prenatal and postnatal periods for persistent effects of dexamethasone on serotonergic and dopaminergic systems

Neuropsychopharmacology

Volumn 31, Issue 5, 2006, Pages 904-911

  Slotkin, Theodore A ^a   Kreider, Marisa L ^a   Tate, Charlotte A ^a   Seidler, Frederic J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antenatal glucocorticoids; Brain development; Dexamethasone; Dopaminergic systems; Preterm delivery; Serotonergic systems

Indexed keywords

BIOLOGICAL MARKER; DEXAMETHASONE; DEXAMETHASONE SODIUM PHOSPHATE; DOPAMINE; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN 2 RECEPTOR; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOPAMINERGIC SYSTEM; DOSE RESPONSE; DRUG MECHANISM; FEMALE; GESTATIONAL AGE; HIPPOCAMPUS; MALE; NERVE CELL DIFFERENTIATION; NONHUMAN; POSTNATAL DEVELOPMENT; PREMATURITY; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; SYNAPSE;

3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; BRAIN; DEVELOPMENTAL DISABILITIES; DEXAMETHASONE; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUCOCORTICOIDS; HOMOVANILLIC ACID; HUMANS; INFANT, NEWBORN; MALE; NEURAL PATHWAYS; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; UP-REGULATION;

EID: 33646125197     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300892     Document Type: Article

References (66)

1. Aghajanian GK, Charney DS, Duman RS, Heninger GR (1993). Neurobiology of Affective Disorders. Raven Press: New York.
2. Aldridge JE, Levin ED, Seidler FJ, Slotkin TA (2005a). Developmental exposure of rats to chlorpyrifos leads to behavioral alterations in adulthood, involving serotonergic mechanisms and resembling animal models of depression. Environ Health Perspect 113: 527-531.
3. Aldridge JE, Meyer A, Seidler FJ, Slotkin TA (2005b). Alterations in central nervous system serotonergic and dopaminergic synaptic activity in adulthood after prenatal or neonatal chlorpyrifos exposure. Environ Health Perspect 113: 1027-1031.
4. Aldridge JE, Seidler FJ, Meyer A, Thillai I, Slotkin TA (2003). Serotonergic systems targeted by developmental exposure to chlorpyrifos: effects during different critical periods. Environ Health Perspect 111: 1736-1743.
5. Aldridge JE, Seidler FJ, Slotkin TA (2004). Developmental exposure to chlorpyrifos elicits sex-selective alterations of serotonergic synaptic function in adulthood: critical periods and regional selectivity for effects on the serotonin transporter, receptor subtypes, and cell signaling. Environ Health Perspect 112: 148-155.
6. Arango V, Underwood MD, Boldrini M, Tamir H, Kassir SA, Hsiung S et al (2001). Serotonin-1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide victims. Neuropsychopharmacology 25: 892-903.
7. Barrington KJ (2001). The adverse neuro-developmental effects of postnatal steroids in the preterm infant: a systematic review of RCTs. BMC Pediatr 1: 1-9.
8. Blackmon LR, Bell EF, Engle WA, Kanto WP, Martin GI, Miller CA et al (2002). Postnatal corticosteroids to treat or prevent chronic lung disease in preterm infants. Pediatrics 109: 330-338.
9. Bohn MC (1984). Glucocorticoid induced teratologies of the nervous system. In: Yanai J (eds). Neurobehavioral Teratology. Elsevier: Amsterdam, pp 365-387.
10. Bowman RE, MacLusky NJ, Sarmiento Y, Frankfurt M, Gordon M, Luine VN (2004). Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145: 3778-3787.
11. Coe CL, Lubach GR (2005). Developmental consequences of antenatal dexamethasone treatment in nonhuman primates. Neurosci Biobehav Rev 29: 227-235.
12. Cooper JR, Bloom FE, Roth RH (1996). The Biochemical Basis of Neuropharmacology, 7th edn. Oxford University Press: New York, 518pp.
13. Crowther CA, Harding J (2003). Repeat doses of prenatal corticosteroids for women at risk of preterm birth for preventing neonatal respiratory disease. Cochrane Database Systemat Rev 1: CD003935.
14. Dammann O, Matthews SG (2001). Repeated antenatal glucocorticoid exposure and the developing brain. Pediatr Res 50: 563-564.
15. Dean F, Yu C, Lingas RI, Matthews SG (2001). Prenatal glucocorticoid modifies hypothalamo-pituitary-adrenal regulation in prepubertal guinea pigs. Neuroendocrinology 73: 194-202.
16. Dobbing J, Sands J (1979). Comparative aspects of the brain growth spurt. Early Human Dev 3: 79-83.
17. Felszeghy K, Bagdy G, Nyakas C (2000). Blunted pituitary-adrenocortical stress response in adult rats following neonatal dexamethasone treatment. J Neuroendocrinol 12: 1014-1021.
18. Fujita M, Charney DS, Innis RB (2000). Imaging serotonergic neurotransmission in depression: hippocampal pathophysiology may mirror global brain alterations. Biol Psychiatr 48: 801-812.
19. Fuxe K, Cintra A, Chadi G, Gustafsson JÅ, Agnati LF (1994). Central glucocorticoid receptors and neuronal plasticity. Meth Neurosci 22: 372-382.
20. Fuxe K, Diaz R, Cintra A, Bhatnagar M, Tinner B, Gustafsson JA et al (1996). On the role of glucocorticoid receptors in brain plasticity. Cell Mol Neurobiol 16: 239-258.
21. Gerardin DC, Pereira OC, Kempinas WG, Florio JC, Moreira EG, Bernardi MM (2005). Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress. Physiol Behav 84: 97-104.
22. Gilad GM, Gilad VH, Eliyayev Y, Rabey JM (1998). Developmental regulation of the brain polyamine-stress-response. Int J Dev Neurosci 16: 271-278.
23. Gilstrap LC, Christensen R, Clewell WH, D'Alton ME, Davidson EC, Escobedo MB et al (1995). Effect of corticosteroids for fetal maturation on perinatal outcomes. J Am Med Assoc 273: 413-418.
24. Gould E, Tanapat P, McEwen BS (1997). Activation of the type 2 adrenal steroid receptor can rescue granule cells from death during development. Dev Brain Res 101: 265-268.
25. Jesberger JA, Richardson JS (1985). Animal models of depression: parallels and correlates to severe depression in humans. Biol Psychiatr 20: 764-784.
26. Kelly JP, Wrynn AS, Leonard BE (1997). The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 74: 299-316.
27. Korte SM, Van Duin S, Bouws GAH, Koolhaas JM, Bohus B (1991). Involvement of hypothalamic serotonin in activation of the sympathoadrenalmedullary system and hypothalamo-pituitary-adrenocortical axis in male Wistar rats. Eur J Pharmacol 197: 225-228.
28. Kreider ML, Aldridge JE, Cousins MM, Oliver CA, Seidler FJ, Slotkin TA (2005a). Disruption of rat forebrain development by glucocorticoids: critical perinatal periods for effects on neural cell acquisition and on cell signaling cascades mediating noradrenergic and cholinergic neurotransmitter/neurotrophic responses. Neuropsychopharmacology 30: 1841-1855.
29. Kreider ML, Levin ED, Seidler FJ, Slotkin TA (2005b). Gestational dexamethasone treatment elicits sex-dependent alterations in locomotor activity, reward-based memory and hippocampal cholinergic function in adolescent and adult rats. Neuropsychopharmacology 30: 1617-1623.
30. Kreider ML, Tate CA, Cousins MM, Oliver CA, Seidler FJ, Slotkin TA (2006). Lasting effects of developmental dexamethasone treatment on neural cell number and size, synaptic activity and cell signaling: critical periods of vulnerability, dose-effect relationships, regional targets and sex selectivity. Neuropsychopharmacology 31: 12-35.
31. Lam F, Elliott J, Jones JS, Katz M, Knuppel RA, Morrison J et al (1998). Clinical issues surrounding the use of terbutaline sulfate for preterm labor. Obstet Gynecol Survey 53: S85-S95.
32. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O (2003). Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 27: 119-127.
33. Matthews SG (2000). Antenatal glucocorticoids and programming of the developing CNS. Pediatr Res 47: 291-300.
34. Matthews SG, Owen D, Banjanin S, Andrews MH (2002). Glucocorticoids, hypothalamo-pituitary-adrenal (HPA) development, and life after birth. Endocr Res 28: 709-718.
35. McEwen BS (1992). Steroid hormones: effect on brain development and function. Hormone Res 37: 1-10.
36. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C et al (1996). Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18: 49-72.
37. Muneoka K, Mikuni M, Ogawa T, Kitera K, Kamei K, Takigawa M et al (1997). Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am J Physiol 42: R1669-R1675.
38. Nemeroff CB (1998). The neurobiology of depression. Sci Am 278: 42-49.
39. Newnham JP (2001). Is prenatal glucocorticoid administration another origin of adult disease? Clin Exp Pharmacol Physiol 28: 957-961.
40. Nyirenda MJ, Welberg LA, Seckl JR (2001). Programming hyperglycaemia in the rat through prenatal exposure to glucocorticoids: fetal effect or maternal influence? J Endocrinol 170: 653-660.
41. Raff H (2004). Neonatal dexamethasone therapy: short- and long-term consequences. Trends Endocrinol Metab 15: 351-352.
42. Rhodes MC, Seidler FJ, Abdel-Rahman A, Tate CA, Nyska A, Rincavage HL et al (2004). Terbutaline is a developmental neurotoxicant: effects on neuroproteins and morphology in cerebellum, hippocampus and somatosensory cortex. J Pharmacol Exp Ther 308: 529-537.
43. Rieger M, Pirke KM, Buske-Kirschbaum A, Wurmser H, Papousek M, Hellhammer DH (2004). Influence of stress during pregnancy on HPA activity and neonatal behavior. Ann NY Acad Sci 1032: 228-230.
44. Rodier PM (1988). Structural-functional relationships in experimentally induced brain damage. Prog Brain Res 73: 335-348.
45. Seckl JR (2001). Glucocorticoid programming of the fetus: adult phenotypes and molecular mechanisms. Mol Cell Endocrinol 185: 61-71.
46. Seckl JR (2004). Prenatal glucocorticoids and long-term programming. Eur J Endocrinol 151: U49-U62.
47. Shahak H, Slotkin TA, Yanai J (2003). Alterations in PKCγ in the mouse hippocampus after prenatal exposure to heroin: a link from cell signaling to behavioral outcome. Dev Brain Res 140: 117-125.
48. Shinwell ES, Karplus M, Reich D, Weintraub Z, Blazer S, Bader D et al (2000). Early postnatal dexamethasone treatment and increased incidence of cerebral palsy. Arch Dis Child 83: F177-F181.
49. Slotkin TA, Auman JT, Seidler FJ (2003). Ontogenesis of β-adrenoceptor signaling: implications for perinatal physiology and for fetal effects of tocolytic drugs. J Pharmacol Exp Ther 306: 1-7.
50. Slotkin TA, Lappi SE, McCook EC, Tayyeb MI, Eylers JP, Seidler FJ (1992). Glucocorticoids and the development of neuronal function: effects of prenatal dexamethasone exposure on central noradrenergic activity. Biol Neonate 61: 326-336.
51. 3H]desmethylimipramine binding sites after fetal exposure to dexamethasone. Res Comm Chem Pathol Pharmacol 73: 3-19.
52. Slotkin TA, Seidler FJ, Ali SF (2000). Cellular determinants of reduced adaptability of the aging brain: neurotransmitter utilization and cell signaling responses after MDMA lesions. Brain Res 879: 163-173.
53. Song C (2000). The interaction between cytokines and neurotransmitters in depression and stress: possible mechanism of antidepressant treatments. Hum Psychopharmacol 15: 199-211.
54. Steingart RA, Barg J, Maslaton J, Nesher M, Yanai J (1998). Preand postsynaptic alterations in the septohippocampal cholinergic innervations after prenatal exposure to drugs. Brain Res Bull 46: 203-209.
55. Stokes PE, Maas JW, Davis JM, Koslow SH, Casper RC, Stoll PM (1987). Biogenic amine and metabolite levels in depressed patients with high versus normal hypothalamic-pituitary-adrenocortical activity. Am J Psychiatr 144: 868-872.
56. Trautman PD, Meyer-Bahlburg HFL, Postelnek J, New MI (1995). Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: results of a pilot study. Psychoneuroendocrinology 20: 439-449.
57. Vatury O, Barg J, Slotkin TA, Yanai J (2004). Altered localization of choline transporter sites in the mouse hippocampus after prenatal heroin exposure. Brain Res Bull 53: 25-32.
58. Weinstock M (2001). Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65: 427-451.
59. Welberg LAM, Seckl JR (2001). Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13: 113-128.
60. Xu Z, Seidler FJ, Ali SF, Slikker W, Slotkin TA (2001). Fetal and adolescent nicotine administration: effects on CNS serotonergic systems. Brain Res 914: 166-178.
61. Yanai J, Beer A, Huleihel R, Izrael M, Katz S, Levi Y et al (2004). Convergent effects on cell signaling mechanisms mediate the actions of different neurobehavioral teratogens: alterations in cholinergic regulation of PKC in chick and avian models. Ann NY Acad Sci 1025: 595-601.
62. Yatham LN, Liddle PF, Dennie J, Shiah IS, Adam MJ, Lane CJ et al (1999). Decrease in brain serotonin-2 receptor binding in patients with major depression following desipramine treatment: a positron emission tomography study with fluorine-18-labeled setoperone. Arch Gen Psychiatr 56: 705-711.
63. Yatham LN, Liddle PF, Shiah IS, Scarrow G, Lam RW, Adam MJ et al (2000). Brain serotonin-2 receptors in major depression: a positron emission tomography study. Arch Gen Psychiatr 57: 850-858.
64. Yeh TF, Lin YJ, Lin HC, Huang CC, Hsieh WS, Lin CH et al (2004). Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. N Engl J Med 350: 1304-1313.
65. Young AH (1994). Glucocorticoids, serotonin and mood. Br J Psychiatr 165: 271-272.
66. Zahalka EA, Seidler FJ, Slotkin TA (1993). Dexamethasone treatment in utero enhances neonatal cholinergic nerve terminal development in rat brain. Res Comm Chem Pathol Pharmacol 81: 191-198.