Ethanol alters local cellular levels of (3α,5α)-3- hydroxypregnan-20-one (3α,5α-THP) independent of the adrenals in subcortical brain regions

Neuropsychopharmacology

Volumn 39, Issue 8, 2014, Pages 1978-1987

  Cook, Jason B ^a,b   Nelli, Stephanie M ^a   Neighbors, Mackenzie R ^a   Morrow, Danielle H ^a   O'Buckley, Todd K ^a   Maldonado Devincci, Antoniette M ^a   Morrow, A Leslie ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ALCOHOL; CARRIER PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; CENTRAL DEPRESSANT AGENT; ELTANOLONE;

ADRENAL GLAND; ADRENALECTOMY; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN LEVEL; CELL POPULATION; CENTRAL NUCLEUS (AMYGDALA); CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DENTATE HILUS; HIPPOCAMPAL CA1 REGION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRIA TERMINALIS; SUBCORTEX; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; PREFRONTAL CORTEX; WISTAR RAT;

ADRENAL GLANDS; ADRENALECTOMY; ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; MALE; PREFRONTAL CORTEX; PREGNANOLONE; RATS; RATS, WISTAR;

EID: 84902545764     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.46     Document Type: Article

References (49)

1. Agis-Balboa RC, Graziano P, Zhubi A, Maloku E, Veldic M, Costa E et al (2006). Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc Natl Acad Sci USA 103: 14602-14607.
2. Akk G, Covey DF, Evers AS, Steinbach JH, Zorumski CF, Mennerick S (2007). Mechanisms of neurosteroid interactions with GABA(A) receptors. Pharmacol Ther 116: 35-57.
3. Amaral DG, Scharfman HE, Lavenex P (2007). The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163: 3-22.
4. Armario A (2010). Activation of the hypothalamic-pituitaryadrenal axis by addictive drugs: different pathways, common outcome. Trends Pharmacol Sci 31: 318-325.
5. Barbaccia ML, Affricano D, Trabucchi M, Purdy RH, Colombo G, Agabio R et al (1999). Ethanol markedly increases 'GABAergic' neurosteroids in alcohol-preferring rats. Eur J Pharmacol 384: R1-R2.
6. Boyd KN, Kumar S, O'Buckley TK, Porcu P, Morrow AL (2010). Ethanol induction of steroidogenesis in rat adrenal and brain is dependent upon pituitary ACTH release and de novo adrenal StAR synthesis. J Neurochem 112: 784-796.
7. Cagetti E, Pinna G, Guidotti A, Baicy K, Olsen RW (2004). Chronic intermittent ethanol (CIE) administration in rats decreases levels of neurosteroids in hippocampus, accompanied by altered behavioral responses to neurosteroids and memory function. Neuropharmacology 46: 570-579.
8. Cook JB, Dumitru AM, O'Buckley TK, Morrow AL (2014). Ethanol administration produces divergent changes in GABAergic neuroactive steroid immunohistochemistry in the rat brain. Alcohol Clin Exp Res 38: 90-99.
9. Cui C, Noronha A, Morikawa H, Alvarez VA, Stuber GD, Szumlinski KK et al (2012). New insights on neurobiological mechanisms underlying alcohol addiction. Neuropharmacology 67C: 223-232.
10. Dazzi L, Serra M, Seu E, Cherchi G, Pisu MG, Purdy RH et al (2002). Progesterone enhances ethanol-induced modulation of mesocortical dopamine neurons: antagonism by finasteride. J Neurochem 83: 1103-1109.
11. Follesa P, Biggio F, Talani G, Murru L, Serra M, Sanna E et al (2006). Neurosteroids, GABAA receptors, and ethanol dependence. Psychopharmacology 186: 267-280.
12. Ford MM, Mark GP, Nickel JD, Phillips TJ, Finn DA (2007). Allopregnanolone influences the consummatory processes that govern ethanol drinking in C57BL/6J mice. Behav Brain Res 179: 265-272.
13. Ford MM, Nickel JD, Phillips TJ, Finn DA (2005). Neurosteroid modulators of GABAA receptors differentially modulate ethanol intake patterns in male C57BL/6J mice. Alcohol Clin Exp Res 29: 1630-1640.
14. Gonzales RA, Job MO, Doyon WM (2004). The role of mesolimbic dopamine in the development and maintenance of ethanol reinforcement. Pharmacol Ther 103: 121-146.
15. Herd MB, Belelli D, Lambert JJ (2007). Neurosteroid modulation of synaptic and extrasynaptic GABAA receptors. Pharmacol Ther 116: 20-34.
16. Hirani K, Khisti RT, Chopde CT (2002). Behavioral action of ethanol in Porsolt's forced swim test: modulation by 3a-hydroxy-5apregnan- 20-one. Neuropharmacology 43: 1339-1350.
17. Hirani K, Sharma AN, Jain NS, Ugale RR, Chopde CT (2005). Evaluation of GABAergic neuroactive steroid 3a-hydroxy-5apregnane- 20-one as a neurobiological substrate for the anti-anxiety effect of ethanol in rats. Psychopharmacology 180: 267-278.
18. Hosie AM, Wilkins ME, da Silva HM, Smart TG (2006). Endogenous neurosteroids regulate GABAA receptors through two discrete transmembrane sites. Nature 444: 486-489.
19. Janak PH, Michael Gill T (2003). Comparison of the effects of allopregnanolone with direct GABAergic agonists on ethanol self-administration with and without concurrently available sucrose. Alcohol 30: 1-7.
20. Janak PH, Redfern JEM, Samson HH (1998). The reinforcing effects of ethanol are altered by the endogenous neurosteroid, allopregnanolone. Alcohol Clin Exp Res 22: 1106-1112.
21. Khisti RT, VanDoren MJ, O'Buckley TK, Morrow AL (2003). Neuroactive steroid 3a-hydroxy-5a-pregnan-20-one modulates ethanol-induced loss of righting reflex in rats. Brain Res 980: 255-265.
22. Kim HJ, Ha M, Park CH, Park SJ, Youn SM, Kang SS et al (2003). StAR and steroidogenic enzyme transcriptional regulation in the rat brain: effects of acute alcohol administration. Mol Brain Res 115: 39-49.
23. Koob GF (2013). Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci 13: 3-30.
24. Marx CE, Stevens RD, Shampine LJ, Uzunova V, Trost WT, Butterfield MI et al (2006). Neuroactive steroids are altered in schizophrenia and bipolar disorder: relevance to pathophysiology and therapeutics. Neuropsychopharmacology 31: 1249-1263.
25. McBride WJ (2002). Central nucleus of the amygdala and the effects of alcohol and alcohol-drinking behavior in rodents. Pharmacol Biochem Behav 71: 509-515.
26. Morrow AL (2007). Recent developments in the significance and therapeutic relevance of neuroactive steroids - Introduction to the special issue. Pharmacol Ther 116: 1-6.
27. Morrow AL, Suzdak PD, Paul SM (1987). Steroid hormone metabolites potentiate GABA receptor-mediated chloride ion flux with nanomolar potency. Eur J Pharmacol 142: 483-485.
28. Morrow AL, VanDoren MJ, Penland SN, Matthews DB (2001). The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res Brain Res Rev 37: 98-109.
29. Motzo C, Porceddu ML, Maira G, Flore G, Concas A, Dazzi L et al (1996). Inhibition of basal and stress-induced dopamine release in the cerebral cortex and nucleus accumbens of freely moving rats by the neurosteroid allopregnanolone. JPsychopharmacol 10: 266-272.
30. O'Dell LE, Alomary AA, Vallee M, Koob GF, Fitzgerald RL, Purdy RH (2004). Ethanol-induced increases in neuroactive steroids in the rat brain and plasma are absent in adrenalectomized and gonadectomized rats. Eur J Pharmacol 484: 241-247.
31. Owens MJ, Ritchie JC, Nemeroff CB (1992). 5a-Pregnane-3a,21- diol-20-one (THDOC) attenuates mild stress-induced increases in plasma corticosterone via a non-glucocorticoid mechanism: comparison with alprazolam. Brain Res 573: 353-355.
32. Patchev VK, Hassan AHS, Holsboer F, Almeida OFX (1996). The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15: 533-540.
33. Patchev VK, Shoaib M, Holsboer F, Almeida OFX (1994). The neurosteroid tetrahydroprogesterone counteracts corticotropinreleasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62: 265-271.
34. Paxinos G, Watson C (1998). The Rat Brain. Academic Press: San Diego.
35. Pierucci-Lagha A, Covault J, Feinn R, Nellissery M, Hernandez- Avila C, Oncken C et al (2005). GABRA2 alleles moderate the subjective effects of alcohol, which are attenuated by finasteride. Neuropsychopharmacology 30: 1193-1203.
36. Porcu P, O'Buckley TK, Alward SE, Marx CE, Shampine LJ, Girdler SS et al (2009). Simultaneous quantification of GABAergic 3a,5a/ 3a,5b neuroactive steroids in human and rat serum. Steroids 74: 463-473.
37. Porcu P, Sogliano C, Ibba C, Piredda M, Tocco S, Marra C et al (2004). Failure of g-hydroxybutyric acid both to increase neuroactive steroid concentrations in adrenalectomized-orchiectomized rats and to induce tolerance to its steroidogenic effect in intact animals. Brain Res 1012: 160-168.
38. Rasmusson AM, Pinna G, Paliwal P, Weisman D, Gottschalk C, Charney D et al (2006). Decreased cerebrospinal fluid allopregnanolone levels in women with posttraumatic stress disorder. Biol Psychiatry 60: 704-713.
39. Rivier C, Bruhn T, Vale W (1984). Effect of ethanol on the hypothalamic- pituitary-adrenal axis in the rat: role of corticotropinreleasing factor (CRF). J Pharmacol Exp Ther 229: 127-131.
40. Rouge-Pont F, Mayo W, Marinelli M, Gingras M, Le Moal M, Piazza PV (2002). The neurosteroid allopregnanolone increases dopamine release and dopaminergic response to morphine in the rat nucleus accumbens. Eur J Neurosci 16: 169-173.
41. Rupprecht R, Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N et al (2010). Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov 9: 971-988.
42. Saalmann YB, Kirkcaldie MT, Waldron S, Calford MB (2007). Cellular distribution of the GABAA receptor-modulating 3alphahydroxy, 5alpha-reduced pregnane steroids in the adult rat brain. J Neuroendocrinol 19: 272-284.
43. Sanna E, Talani G, Busonero F, Pisu MG, Purdy RH, Serra M et al (2004). Brain steroidogenesis mediates ethanol modulation of GABAA receptor activity in rat hippocampus. J Neurosci 24: 6521-6530.
44. Sarkar J, Wakefield S, MacKenzie G, Moss SJ, Maguire J (2011). Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors. J Neurosci 31: 18198-18210.
45. Strohle A, Romeo E, di Michele F, Pasini A, Yassouridis A, Holsboer F et al (2002). GABA(A) receptor-modulating neuroactive steroid composition in patients with panic disorder before and during paroxetine treatment. Am J Psychiatry 159: 145-147.
46. Tokuda K, Izumi Y, Zorumski CF (2011). Ethanol enhances neurosteroidogenesis in hippocampal pyramidal neurons by paradoxical NMDA receptor activation. J Neurosci 31: 9905-9909.
47. Tokunaga S, McDaniel JR, Morrow AL, Matthews DB (2003). Effect of acute ethanol administration and acute allopregnanolone administration on spontaneous hippocampal pyramidal cell neural activity. Brain Res 967: 273-280.
48. Uzunova V, Sheline Y, Davis JM, Rasmusson A, Uzunov DP, Costa E et al (1998). Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proc Natl Acad Sci USA 95: 3239-3244.
49. VanDoren MJ, Matthews DB, Janis GC, Grobin AC, Devaud LL, Morrow AL (2000). Neuroactive steroid 3a-hydroxy-5a-pregnan- 20-one modulates electrophysiological and behavioral actions of ethanol. J Neurosci 20: 1982-1989.