Central opioid inhibition of neuroendocrine stress responses in pregnancy in the rat is induced by the neurosteroid allopregnanolone

Journal of Neuroscience

Volumn 29, Issue 20, 2009, Pages 6449-6460

  Brunton, Paula J ^a   McKay, Ailsa J ^a   Ochȩdalski, Tomasz ^b   Piastowska, Agnieszka ^b   Rȩbas, Elzbieta ^b   Lachowicz, Agnieszka ^b   Russell, John A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 3ALPHA HYDROXYSTEROID DEHYDROGENASE; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; FINASTERIDE; INTERLEUKIN 1BETA; MESSENGER RNA; NALOXONE; NEUROSTEROID; OPIATE; PROENKEPHALIN; PROENKEPHALIN A; STEROID 5ALPHA REDUCTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CORTICOSTERONE RELEASE; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE SYSTEM; MALE; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SOLITARY TRACT NUCLEUS; STRESS; THALAMUS MIDLINE NUCLEUS; THIRD TRIMESTER PREGNANCY;

20-ALPHA-DIHYDROPROGESTERONE; ADRENOCORTICOTROPIC HORMONE; ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANESTHETICS; ANIMALS; CHROMATOGRAPHY, THIN LAYER; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FINASTERIDE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INTERLEUKIN-1BETA; NEURAL INHIBITION; NEURONS; OXIDOREDUCTASES; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PREGNANCY, ANIMAL; PREGNANOLONE; PROGESTERONE; PROGESTINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 66249088001     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0708-09.2009     Document Type: Article

References (55)

1. Agís-Balboa RC, Pinna G, Zhubi A, Maloku E, Veldic M, Costa E, Guidotti A (2006) Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc Natl Acad Sci U S A 103:14602-14607. (Pubitemid 44484796)
2. Bailey TW, Appleyard SM, Jin YH, Andresen MC (2008) Organization and properties of GABAergic neurons in solitary tract nucleus (NTS). J Neurophysiol 99:1712-1722.
3. Bali B, Kovács KJ (2003) GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur J Neurosci 18:1518-1526. (Pubitemid 37215105)
4. Beaulieu J, Champagne D, Drolet G (1996) Enkephalin innervation of the paraventricular nucleus of the hypothalamus: distribution of fibers and origins of input. J Chem Neuroanat 10:79-92. (Pubitemid 26177661)
5. Bertics SJ, Bertics PJ, Clarke JL, Karavolas HJ (1987) Distribution and ovarian control of progestin-metabolizing enzymes in various rat hypothalamic regions. J Steroid Biochem 26:321-328. (Pubitemid 17066074)
6. Blyth BJ, Hauger RL, Purdy RH, Amico JA (2000) The neurosteroid allopregnanolone modulates oxytocin expression in the hypothalamic paraventricular nucleus. Am J Physiol Regul Integr Comp Physiol 278:R684-R691. (Pubitemid 30158129)
7. Boone JB Jr, McMillen D (1994) Differential effects of prolonged restraint stress on proenkephalin gene expression in the brainstem. Brain Res Mol Brain Res 27:290-298. (Pubitemid 24379212)
8. Borsook D, Smirnova O, Behar O, Lewis S, Kobierski LA (1999) PhosphoCREB and CREM/ICER: positive and negative regulation of proenkephalin gene expression in the paraventricular nucleus of the hypothalamus. J MoI Neurosci 12:35-51.
9. Brunton PJ, Russell JA (2008) The expectant brain: adapting for motherhood. Nat Rev Neurosci 9:11-25. (Pubitemid 350295685)
10. Brunton PJ, Meddle SL, Ma S, Ochedalski T, Douglas AJ, Russell JA (2005) Endogenous opioids and attenuated hypothalamic-pituitary-adrenal axis responses to immune challenge in pregnant rats. J Neurosci 25:5117-5126. (Pubitemid 40726965)
11. Brunton PJ, Russell JA, Douglas AJ (2008) Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 20:764-776.
12. Buller K, Xu Y, Dayas C, Day T (2001) Dorsal and ventral medullary catecholamine cell groups contribute differentially to systemic interleukin-1beta-induced HPA axis responses. Neuroendocrinology 73:129-138. (Pubitemid 32217873)
13. Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, Herman JP (2007) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 27:2025-2034. (Pubitemid 46310312)
14. Compagnone NA, Mellon SH (2000) Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 21:1-56. (Pubitemid 30105920)
15. Concas A, Mostallino MC, Porcu P, Follesa P, Barbaccia ML, Trabucchi M, Purdy RH, Grisenti P, Biggio G (1998) Role of brain allopregnanolone in the plasticity of gamma-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci USA 95:13284-13289. (Pubitemid 28509563)
16. Crane JW, Buller KM, Day TA (2003) Evidence that the bed nucleus of the stria terminalis contributes to the modulation of hypophysiotropic corticotropin-releasing factor cell responses to systemic interleukin-1beta. J Comp Neurol 467:232-242. (Pubitemid 37363147)
17. Cullinan WE, Ziegler DR, Herman JP (2008) Functional role of local GABAergic influences on the HPA axis. Brain Struct Funct 213:63-72.
18. Di S, Maxson MM, Franco A, Tasker JG (2009) Glucocorticoids regulate glutamate and GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways. J Neurosci 29:393-401.
19. Douglas AJ, Johnstone H, Brunton P, Russell JA (2000) Sex-steroid induction of endogenous opioid inhibition on oxytocin secretory responses to stress. J Neuroendocrinol 12:343-350. (Pubitemid 30156527)
20. Eckersell CB, Popper P, Micevych PE (1998) Estrogen-induced alteration of mu-opioid receptor immunoreactivity in the medial preoptic nucleus and medial amygdala. J Neurosci 18:3967-3976. (Pubitemid 28225700)
21. Ericsson A, Kovács KJ, Sawchenko PE (1994) A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 14:897-913. (Pubitemid 24043940)
22. Figueiredo HF, Ulrich-Lai YM, Choi DC, Herman JP (2007) Estrogen potentiates adrenocortical responses to stress in female rats. Am J Physiol Endocrinol Metab 292:E1173-E1182. (Pubitemid 46536518)
23. Fong AY, Stornetta RL, Foley CM, Potts JT (2005) Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J Comp Neurol 493:274-290. (Pubitemid 41677481)
24. Francis K, Meddle SL, Bishop VR, Russell JA (2002) Progesterone receptor expression in the pregnant and parturient rat hypothalamus and brainstem. Brain Res 927:18-26. (Pubitemid 34114045)
25. García-García L, Harbuz MS, Manzanares J, Lightman SL, Fuentes JA (1998) RU-486 blocks stress-induced enhancement of proenkephalin gene expression in the paraventricular nucleus of rat hypothalamus. Brain Res 786:215-218. (Pubitemid 28191732)
26. Hanukoglu I, Karavolas HJ, Goy RW (1977) Progesterone metabolism in the pineal, brain stem, thalamus and corpus callosum of the female rat. Brain Res 125:313-324. (Pubitemid 8088944)
27. Harbuz MS, Lightman SL (1989) Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat. J Endocrinol 122:705-711. (Pubitemid 19220627)
28. Herd MB, Beleih D, Lambert JJ (2007) Neurosteroid modulation of synaptic and extrasynaptic GABA(A) receptors. Pharmacol Ther 116:20-34. (Pubitemid 47391030)
29. Lauber ME, Lichtensteiger W (1996) Ontogeny of 5 alpha-reductase (type 1) messenger ribonucleic acid expression in rat brain: early presence in germinal zones. Endocrinology 137:2718-2730. (Pubitemid 26192164)
30. Ma S, Shipston MJ, Morilak D, Russell JA (2005) Reduced hypothalamic vasopressin secretion underlies attenuated adrenocorticotropin stress responses in pregnant rats. Endocrinology 146:1626-1637. (Pubitemid 40289353)
31. Mahendroo MS, Cala KM, Landrum DP, Russell DW (1997) Fetal death in mice lacking 5alpha-reductase type 1 caused by estrogen excess. Mol Endocrinol 11:917-927. (Pubitemid 27241784)
32. Melcangi RC, Celotti F, Ballabio M, Poletti A, Castano P, Martini L (1988) Testosterone 5 alpha-reductase activity in the rat brain is highly concentrated in white matter structures and in purified myelin sheaths of axons. J Steroid Biochem 31:173-179. (Pubitemid 18189154)
33. Melcangi RC, Celotti F, Ballabio M, Poletti A, Martini L (1990) Testosterone metabolism in peripheral nerves: presence of the 5 alpha-reductase-3 alpha-hydroxysteroid-dehydrogenase enzymatic system in the sciatic nerve of adult and aged rats. J Steroid Biochem 35:145-148. (Pubitemid 20075412)
34. Mitev YA, Darwish M, Wolf SS, Holsboer F, Almeida OF, Patchev VK (2003) Gender differences in the regulation of 3 alpha-hydroxysteroid dehydrogenase in rat brain and sensitivity to neurosteroid-mediated stress protection. Neuroscience 120:541-549. (Pubitemid 37288788)
35. Moore SD, Guyenet PG (1983) Alpha-receptor mediated inhibition of A2 noradrenergic neurons. Brain Res 276:188-191.
36. Patchev VK, Shoaib M, Holsboer F, Almeida OF (1994) The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormoneinduced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62:265-271. (Pubitemid 24287361)
37. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. San Diego: Academic.
38. Pirog EC, Collins DC (1994) 3 Alpha-hydroxysteroid dehydrogenase activity in rat liver and skin. Steroids 59:259-264. (Pubitemid 24116705)
39. Priest CA, Roberts JL (2000) Estrogen and tamoxifen differentially regulate beta-endorphin and cFos expression and neuronal colocalization in the arcuate nucleus of the rat. Neuroendocrinology 72:293-305. (Pubitemid 32008831)
40. Purdy RH, Morrow AL, Moore PH Jr, Paul SM (1991) Stress-induced elevations of gamma-aminobutyric acid type a receptor-active steroids in the rat brain. Proc Natl Acad Sci USA 88:4553-4557. (Pubitemid 21914579)
41. Reddy DS, Rogawski MA (2002) Stress-Induced Deoxycorticosterone-Derived Neurosteroids Modulate GABAA Receptor Function and Seizure Susceptibility. J Neurosci 22:3795-3805. (Pubitemid 37465784)
42. Rivest S, Lacroix S, Vallières L, Nadeau S, Zhang J, Laflamme N (2000) How the blood talks to the brain parenchyma and the paraventricular nucleus of the hypothalamus during systemic inflammatory and infectious stimuli. Proc Soc Exp Biol Med 223:22-38. (Pubitemid 30182654)
43. Rivier C, Vale W, Brown M (1989) In the rat, interleukin-1alpha and -beta stimulate adrenocorticotropin and catecholamine release. Endocrinology 125:3096-3102.
44. Rupprecht R (2003) Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 28:139-168. (Pubitemid 36044075)
45. Saha S, Sieghart W, Fritschy JM, McWilliam PN, Batten TF (2001) Gamma-aminobutyric acid receptor (GABA(A)) subunits in rat nucleus tractus solitarii (NTS) revealed by polymerase chain reaction (PCR) and immunohistochemistry. Mol Cell Neurosci 17:241-257. (Pubitemid 32113550)
46. Sánchez P, Torres JM, Gavete P, Ortega E (2008a) Effects of swim stress on mRNA and protein levels of steroid 5alpha-reductase isozymes in prefrontal cortex of adult male rats. Neurochem Int 52:426-431.
47. Sánchez P, Torres JM, Vilchez P, Del Moral RG, Ortega E (2008b) Effects of sulpiride on prolactin and mRNA levels of steroid 5alpha-reductase isozymes in adult rat brain. Neurochem Res 33:820-825.
48. Sved AF, Curtis JT (1993) Amino acid neurotransmitters in nucleus tractus solitarius: an in vivo microdialysis study. J Neurochem 61:2089-2098. (Pubitemid 23354065)
49. Tanaka J, Mashiko N, Kawakami A, Ushigome A, Nomura M (2002) GABAergic systems in the nucleus tractus solitarius regulate noradrenaline release in the subfornical organ area in the rat. Auton Neurosci 100:58-65.
50. Terai K, Tooyama I, Kimura H (1998) Immunohistochemical localization of GABAA receptors in comparison with GABA-immunoreactive structures in the nucleus tractus solitarii of the rat. Neuroscience 82:843-852. (Pubitemid 27479622)
51. Torres JM, Ortega E (2004) Precise quantitation of steroid 5alpha lambda pi eta alpha-reductase type 1 mRNA levels by RT-PCR in female rat liver. Endocr Res 30:149-157. (Pubitemid 39243117)
52. Torres JM, Ortega E (2006) Steroid 5alpha-reductase isozymes in the adult female rat brain: central role of dihydrotestosterone. J Mol Endocrinol 36:239-245.
53. Womack MD, Pyner S, Barrett-Jolley R (2006) Inhibition by alpha-tetrahydrodeoxycorticosterone (THDOC) of pre-sympathetic parvocellular neurones in the paraventricular nucleus of rat hypothalamus. Br J Pharmacol 149:600-607. (Pubitemid 44658521)
54. Zhang J, Rivest S (1999) Distribution, regulation and colocalization of the genes encoding the EP2- and EP4-PGE2 receptors in the rat brain and neuronal responses to systemic inflammation. Eur J Neurosci 11:2651-2668. (Pubitemid 29364184)
55. Zhu YS, Pfaff DW (1995) DNA binding of hypothalamic nuclear proteins on estrogen response element and preproenkephalin promoter: modification by estrogen. Neuroendocrinology 62:454-466.