Chronic ethanol exposure produces tolerance to elevations in neuroactive steroids: Mechanisms and reversal by exogenous ACTH

Journal of Neurochemistry

Volumn 115, Issue 1, 2010, Pages 142-152

  Boyd, Kevin N ^a   Kumar, Sandeep ^a   O'Buckley, Todd K ^a   Morrow, A Leslie ^a  

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

Author keywords

ACTH; adrenal; brain; ethanol; GABA; neuroactive steroid

Indexed keywords

3 HYDROXYPREGNAN 20 ONE; ALCOHOL; CORTICOTROPIN; PROGESTERONE; STEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CENTRAL DEPRESSANT AGENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHOPROTEIN; PREGNENOLONE;

ALCOHOL TOLERANCE; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; LONG TERM EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; BIOSYNTHESIS; DIET; DRUG EFFECTS; DRUG TOLERANCE; IMMUNOPRECIPITATION; METABOLISM; MITOCHONDRIAL MEMBRANE; PHOSPHORYLATION; PHYSIOLOGY; RADIOIMMUNOASSAY; SPRAGUE DAWLEY RAT; TOXICITY; WESTERN BLOTTING;

RATTUS;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BLOTTING, WESTERN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIET; DRUG TOLERANCE; ETHANOL; GAMMA-AMINOBUTYRIC ACID; IMMUNOPRECIPITATION; MALE; MITOCHONDRIAL MEMBRANES; NEUROTRANSMITTER AGENTS; PHOSPHOPROTEINS; PHOSPHORYLATION; PREGNENOLONE; PROGESTERONE; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77956587996     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06904.x     Document Type: Article

References (57)

1. Adinoff B., Junghanns K., Kiefer F. Krishnan-Sarin S. (2005) Suppression of the HPA axis stress-response: implications for relapse. Alcohol. Clin. Exp. Res. 29, 1351 1355.
2. Anton R. F., Oroszi G., O'Malley S., Couper D., Swift R., Pettinati H. Goldman D. (2008) An evaluation of mu-opioid receptor (OPRM1) as a predictor of naltrexone response in the treatment of alcohol dependence: results from the Combined Pharmacotherapies and Behavioral Interventions for Alcohol Dependence (COMBINE) study. Arch. Gen. Psychiatry 65, 135 144.
3. Arakane F., King S. R., Du Y., Kallen C. B., Walsh L. P., Watari H., Stocco D. M. Strauss III. J. F. (1997) Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J. Biol. Chem. 272, 32656 32662.
4. A receptor. Nat. Rev. Neurosci. 6, 565 575.
5. Boyd K. N., O'Buckley T. K. Morrow A. L. (2008) Role of acetaldehyde in ethanol-induced elevation of the neuroactive steroid 3α-hydroxy-5α- pregnan-20-one in rats. Alcohol. Clin. Exp. Res. 32, 1774 1781.
6. Boyd K. N., Kumar S., O'Buckley T. K., Porcu P. Morrow A. L. (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 R. W. (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. Caron K. M., Soo S. C., Wetsel W. C., Stocco D. M., Clark B. J. Parker K. L. (1997) Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia. Proc. Natl Acad. Sci. USA 94, 11540 11545.
9. Cherradi N., Capponi A. M., Gaillard R. C. Pralong F. P. (2001) Decreased expression of steroidogenic acute regulatory protein: a novel mechanism participating in the leptin-induced inhibition of glucocorticoid biosynthesis. Endocrinology 142, 3302 3308.
10. Colby H. D., Malendowicz L. K., Caffrey J. L. Kitay J. I. (1974) Effects of hypophysectomy and ACTH on adrenocortical function in the rat. Endocrinology 94, 1346 1350.
11. Emanuele N. V., LaPaglia N., Steiner J., Kirsteins L. Emanuele M. A. (1999) Reversal of chronic ethanol-induced testosterone suppression in peripubertal male rats by opiate blockade. Alcohol. Clin. Exp. Res. 23, 60 66.
12. Finn D. A., Phillips T. J., Okorn D. M., Chester J. A. Cunningham C. L. (1997) Rewarding effect of the neuroactive steroid 3α-hydroxy-5α- pregnan-20-one in mice. Pharmacol. Biochem. Behav. 56, 261 264.
13. Ford M. M., Mark G. P., Nickel J. D., Phillips T. J. Finn D. A. (2007) Allopregnanolone influences the consummatory processes that govern ethanol drinking in C57BL/6J mice. Behav. Brain Res. 179, 265 272.
14. Gililland K. R. Finn D. A. (2007) The impact of gonadectomy and adrenalectomy on acute withdrawal severity in male and female C57BL/6J and DBA/2J mice following a single high dose of ethanol. Alcohol. Clin. Exp. Res. 31, 1846 1857.
15. Grant K. A., Azarov A., Bowen C. A., Mirkis S. Purdy R. H. (1996) Ethanol-like discriminative stimulus effects of the neurosteroid 3α-hydroxy-5α-pregnan-20-one in female Macaca fascicularis monkeys. Psychopharmacology 124, 340 346.
16. Griffin L. D. Mellon S. H. (2001) Biosynthesis of the neurosteroid 3 alpha-hydroxy-4-pregnen-20-one (3 alpha hp), a specific inhibitor of FSH release. Endocrinology 142, 4617 4622.
17. Hirani K., Khisti R. T. Chopde C. T. (2002) Behavioral action of ethanol in Porsolt's forced swim test: modulation by 3α-hydroxy-5α-pregnan- 20-one. Neuropharmacology 43, 1339 1350.
18. Hirani K., Sharma A. N., Jain N. S., Ugale R. R. Chopde C. T. (2005) Evaluation of GABAergic neuroactive steroid 3α-hydroxy-5α-pregnane- 20-one as a neurobiological substrate for the anti-anxiety effect of ethanol in rats. Psychopharmacology 180, 267 278.
19. Janak P. H., Redfern J. E. M. Samson H. H. (1998) The reinforcing effects of ethanol are altered by the endogenous neurosteroid, allopregnanolone. Alcohol. Clin. Exp. Res. 22, 1106 1112.
20. Janis G. C., Devaud L. L., Mitsuyama H. Morrow A. L. (1998) Effects of chronic ethanol consumption and withdrawal on the neuroactive steroid 3α-hydroxy-5α-pregnan-20-one in male and female rats. Alcohol. Clin. Exp. Res. 22, 2055 2061.
21. Jo Y., King S. R., Khan S. A. Stocco D. M. (2005) Involvement of protein kinase C and cyclic adenosine 3′, 5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in leydig cells. Biol. Reprod. 73, 244 255.
22. Kalant H. (1998) Research on tolerance: what can we learn from history? Alcohol. Clin. Exp. Res. 22, 67 76.
23. Khanna J. M., Kalant H., Shah G. Chau A. (1991) Tolerance to ethanol and cross-tolerance to pentobarbital and barbital in four rat strains. Pharmacol. Biochem. Behav. 39, 705 709.
24. Khisti R. T., Kumar S. Morrow A. L. (2003a) Ethanol rapidly induces steroidogenic acute regulatory protein expression and translocation in rat adrenal gland. Eur. J. Pharmacol. 473, 225 227.
25. Khisti R. T., VanDoren M. J., O'Buckley T. K. Morrow A. L. (2003b) Neuroactive steroid 3α-hydroxy-5α-pregnan-20-one modulates ethanol-induced loss of righting reflex in rats. Brain Res. 980, 255 265.
26. Kiefer F., Jahn H., Wolf K., Kampf P., Knaudt K. Wiedemann K. (2001) Free-choice alcohol consumption in mice after application of the appetite regulating peptide leptin. Alcohol. Clin. Exp. Res. 25, 787 789.
27. A receptors containing α1 and α4 subunits in the cerebral cortex: selective effects of chronic ethanol consumption. J. Neurochem. 82, 110 117.
28. A receptors in the acute and chronic effects of ethanol: a decade of progress. Psychopharmacology (Berl) 205, 529 564.
29. Lee S. Rivier C. (2003) Long-term influence of an initial exposure to alcohol on the rat hypothalamic-pituitary axis. Alcohol. Clin. Exp. Res. 27, 1463 1470.
30. Lee S., Schmidt E. D., Tilders F. J. Rivier C. (2001a) Effect of repeated exposure to alcohol on the response of the hypothalamic-pituitary-adrenal axis of the rat: I. Role of changes in hypothalamic neuronal activity. Alcohol. Clin. Exp. Res. 25, 98 105. (Pubitemid 32147699)
31. Lee S., Smith G. W., Vale W., Lee K. F. Rivier C. (2001b) Mice that lack corticotropin-releasing factor (CRF) receptors type 1 show a blunted ACTH response to acute alcohol despite up-regulated constitutive hypothalamic CRF gene expression. Alcohol. Clin. Exp. Res. 25, 427 433.
32. Lin D., Sugawara T., Strauss III. J. F., Clark B. J., Stocco D. M., Saenger P., Rogol A. Miller W. L. (1995) Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267, 1828 1831.
33. Lovallo W. R., Dickensheets S. L., Myers D. A., Thomas T. L. Nixon S. J. (2000) Blunted stress cortisol response in abstinent alcoholic and polysubstance-abusing men. Alcohol. Clin. Exp. Res. 24, 651 658.
34. Majewska M. D., Harrison N. L., Schwartz R. D., Barker J. L. Paul S. M. (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232, 1004 1007.
35. Matthews D. B., Morrow A. L., Tokunaga S. McDaniel J. R. (2002) Acute ethanol administration and acute allopregnanolone administration impair spatial memory in the Morris water task. Alcohol. Clin. Exp. Res. 26, 1747 1751.
36. McQuade R. Young A. H. (2000) Future therapeutic targets in mood disorders: the glucocorticoid receptor. Br. J. Psychiatry 177, 390 395.
37. Miller W. L. (1988) Molecular biology of steroid hormone synthesis. Endoc. Rev. 9, 295 318.
38. Morrow A. L. (2007) Recent developments in the significance and therapeutic relevance of neuroactive steroids - Introduction to the special issue. Pharmacol. Ther. 116, 1 6.
39. Morrow A. L. Porcu P. (2009) Neuroactive steroid biomarkers of alcohol sensitivity and alcoholism risk, in Neuropsychiatric Biomarkers, Endophenotypes, and Genes (Ritsner M. ed.), pp. 47 57. Springer Science + Business Media B.V., Dordrecht.
40. Morrow A. L., Pace J. R., Purdy R. H. Paul S. M. (1990) Characterization of steroid interactions with γ-aminobutyric acid receptor-gated chloride ion channels: evidence for multiple steroid recognition sites. Mol. Pharmacol. 37, 263 270.
41. A receptor α1 and α6 subunit mRNA levels in rat cerebellum. Mol. Cell. Neurosci. 3, 251 258.
42. Morrow A. L., VanDoren M. J., Penland S. N. Matthews D. B. (2001) The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res. Brain Res. Rev. 37, 98 109.
43. A Receptors (Smith S. H., ed.), pp. 219 245. CRC Press, Miami.
44. Morrow A. L., Porcu P., Boyd K. N. Grant K. A. (2006) Hypothalamic-pituitary-adrenal axis modulation of GABAergic neuroactive steroids influences ethanol sensitivity and drinking behavior. Dialogues Clin. Neurosci. 8, 463 477.
45. Nicolas J. M., Fernandez-Sola J., Fatjo F., Casamitjana R., Bataller R., Sacanella E., Tobias E., Badia E. Estruch R. (2001) Increased circulating leptin levels in chronic alcoholism. Alcohol. Clin. Exp. Res. 25, 83 88.
46. O'Dell L. E., Alomary A. A., Vallee M., Koob G. F., Fitzgerald R. L. Purdy R. H. (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.
47. O'Malley S. S., Krishnan-Sarin S., Farren C., Sinha R. Kreek M. J. (2002) Naltrexone decreases craving and alcohol self-administration in alcohol-dependent subjects and activates the hypothalamo-pituitary- adrenocortical axis. Psychopharmacology (Berl) 160, 19 29.
48. Oslin D. W., Berrettini W., Kranzler H. R., Pettinati H., Gelernter J., Volpicelli J. R. O'Brien C. P. (2003) A functional polymorphism of the mu-opioid receptor gene is associated with naltrexone response in alcohol-dependent patients. Neuropsychopharmacology 28, 1546 1552.
49. Porcu P., Rogers L. S. M., Morrow A. L. Grant K. A. (2006) Plasma pregnenolone levels in cynomolgus monkeys following pharmacological challenges of the hypothalamic-pituitary-adrenal axis. Pharmacol. Biochem. Behav. 84, 618 627.
50. Porcu P., O'Buckley T. K., Alward S. E., Song S. C., Grant K. A., de Wit H. Morrow A. L. (2010) Differential effects of ethanol on serum GABAergic 3α, 5α/3α, 5β neuroactive steroids in mice, rats, cynomolgus monkeys and humans. Alcohol. Clin. Exp. Res. 34, 432 442.
51. Ray L. A., Hutchison K. E., Ashenhurst J. R. Morrow A. L. (2010) Naltrexone selectively elevates GABAergic neuroactive steroid levels in heavy drinkers with the ASP40 allele of the OPRM1 gene: a pilot investigation. Alcohol. Clin. Exp. Res. 34, 1 9.
52. Rivier C. (1996) Alcohol stimulates ACTH secretion in the rat: mechanisms of action and interactions with other stimuli. Alcohol. Clin. Exp. Res. 20, 240 254.
53. Rivier C. Lee S. (2001) Effect of repeated exposure to alcohol on the response of the hypothalamic-pituitary-adrenal axis of the rat: II. Role of the length and regimen of alcohol treatment. Alcohol. Clin. Exp. Res. 25, 106 111. (Pubitemid 32147700)
54. Rivier C., Bruhn T. Vale W. (1984) Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of corticotropin-releasing factor (CRF). J. Pharmacol. Exp. Ther. 229, 127 131.
55. A receptor activity in rat hippocampus. J. Neurosci. 24, 6521 6530.
56. VanDoren M. J., Matthews D. B., Janis G. C., Grobin A. C., Devaud L. L. Morrow A. L. (2000) Neuroactive steroid 3α-hydroxy-5α-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. J. Neurosci. 20, 1982 1989.
57. Wiebe J. P., De Gannes G. C. Dallaire M. J. (1994) Synthesis of the allylic regulatory steroid, 3 alpha-hydroxy-4-pregnen-20-one, by rat granulosa cells and its regulation by gonadotropins. Biol. Reprod. 50, 956 964.