Effects of progesterone stimulated allopregnanolone on craving and stress response in cocaine dependent men and women

Psychoneuroendocrinology

Volumn 65, Issue , 2016, Pages 44-53

  Milivojevic, Verica ^a   Fox, Helen C ^a   Sofuoglu, Mehmet ^c   Covault, Jonathan ^b   Sinha, Rajita ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Allopregnanolone; Cocaine dependence; Craving; Drug cue; Progesterone; Stress

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ANDROSTANEDIOL; COCAINE; HYDROCORTISONE; PLACEBO; PROGESTERONE; ELTANOLONE;

ACUTE STRESS; ADULT; ANDROGEN BLOOD LEVEL; ARTICLE; COCAINE DEPENDENCE; COGNITION; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG SAFETY; EMOTION; EVENING DOSAGE; FEMALE; GESTAGEN BLOOD LEVEL; GUIDED IMAGERY; HORMONE RESPONSE; HUMAN; HYDROCORTISONE BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; MOOD; MORNING DOSAGE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SEX DIFFERENCE; STRESS; STROOP TEST; WITHDRAWAL SYNDROME; BLOOD; BLOOD PRESSURE; COCAINE-RELATED DISORDERS; CRAVING; DRUG EFFECTS; DRUG THERAPY; ETIOLOGY; HEART RATE; MENTAL STRESS; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

ADULT; BLOOD PRESSURE; COCAINE-RELATED DISORDERS; CRAVING; DOUBLE-BLIND METHOD; EMOTIONS; FEMALE; HEART RATE; HUMANS; HYDROCORTISONE; MALE; MIDDLE AGED; PREGNANOLONE; PROGESTERONE; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84961380135     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.12.008     Document Type: Article

References (67)

1. Anker J.J., Holtz N.A., Zlebnik N., Carroll M.E. Effects of allopregnanolone on the reinstatement of cocaine-seeking behavior in male and female rats. Psychopharmacology (Berl.) 2009, 203(1):63-72.
2. Anker J.J., Carroll M.E. Sex differences in the effects of allopregnanolone on yohimbine-induced reinstatement of cocaine seeking in rats. Drug Alcohol Depend. 2010, 107:264-267.
3. Back S.E., Brady K.T., Jackson J.L., Salstrom S., Zinzow H. Gender differences in stress reactivity among cocaine-dependent individuals. Psychopharmacology (Berl.) 2005, 180:169-176.
4. Back S.E., Hartwell K., DeSantis S.M., Saladin M., McRae-Clark A.L., Price K.L., Moran-Santa Maria M.M., Baker N.L., Spratt E., Kreek M.J., Brady K.T. Reactivity to laboratory stress provocation predicts relapse to cocaine. Drug Alcohol Depend. 2010, 106:21-27.
5. Backstrom T., Sanders D., Leask R., Davidson D., Warner P., Bancroft J. Mood, sexuality, hormones, and the menstrual cycle. II. Hormone levels and their relationship to the premenstrual syndrome. Psychosom. Med. 1983, 45:503-507.
6. Barbaccia M.L., Roscetti G., Bolacchi F., Concas A., Mostallino M.C., Purdy R.H., Biggio G. Stress-induced increase in brain neuroactive steroids: antagonism by abecarnil. Pharmacol. Biochem. Behav. 1996, 54:205-210.
7. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 1999, 64:803-812.
8. Becker J.B., Hu M. Sex differences in drug abuse. Front. Neuroendocrinol. 2008, 29:36-47.
9. Biggio G., Concas A., Follesa P., Sanna E., Serra M. Stress, ethanol, and neuroactive steroids. Pharmacol. Ther. 2007, 116:140-171.
10. Chabbert Buffet N., Djakoure C., Maitre S.C., Bouchard P. Regulation of the human menstrual cycle. Front. Neuroendocrinol. 1998, 19:151-186.
11. Concas A., Mostallino M.C., Porcu P., Follesa P., Barbaccia M.L., Trabucchi M., Purdy R.H., Grisenti P., Biggio G. 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. U. S. A 1998, 95:13284-13289.
12. Crowley S.K., Girdler S.S. Neurosteroid, GABAergic and hypothalamic pituitary adrenal (HPA) axis regulation: what is the current state of knowledge in humans?. Psychopharmacology (Berl.) 2014, 231:3619-3634.
13. Czapla M., Simon J.J., Richter B., Kluge M., Friederich H.C., Herpertz S., Mann K., Herpertz S.C., Loeber S. The impact of cognitive impairment and impulsivity on relapse of alcohol-dependent patients: implications for psychotherapeutic treatment. Addict. Biol. 2015, 10.1111/adb.12229.
14. Evans S.M., Haney M., Foltin R.W. The effects of smoked cocaine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology (Ber.) 2002, 159:397-406.
15. Evans S.M., Foltin R.W. Exogenous progesterone attenuates the subjective effects of smoked cocaine in women, but not in men. Neuropsychopharmacology 2006, 31:659-674.
16. Festa E.D., Quinones-Jenab V. Gonadal hormones provide the biological basis for sex differences in behavioral responses to cocaine. Horm. Behav. 2004, 46:509-519.
17. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for the DSM-IV Axis I Disorders Patient Edition (SCID-I/P, Version 20, 4/97 Revision) 1997, New York State Psychiatric Institute, New York.
18. Ford M.M., Yoneyama N., Strong M.N., Fretwell A., Tanchuck M., Finn D.A. Inhibition of 5alpha-reduced steroid biosynthesis impedes acquisition of ethanol drinking in male C57BL/6 J mice. Alcohol. Clin. Exp. Res. 2008, 32:1408-1416.
19. Fox H.C., Bergquist K.L., Hong K.I., Sinha R. Stress-induced and alcohol cue-induced craving in recently abstinent alcohol-dependent individuals. Alcohol. Clin. Exp. Res. 2007, 31:395-403.
20. Fox H.C., Hong K.I., Siedlarz K., Sinha R. Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine-dependent individuals compared to social drinkers. Neuropsychopharmacology 2008, 33:796-805.
21. Fox H.C., Hong K.A., Paliwal P., Morgan P.T., Sinha R. Altered levels of sex and stress steroid hormones assessed daily over a 28-day cycle in early abstinent cocaine-dependent females. Psychopharmacology (Berl.) 2008, 195:527-536.
22. Fox H.C., Jackson E.D., Sinha R. Elevated cortisol and learning and memory deficits in cocaine dependent individuals: relationship to relapse outcomes. Psychoneuroendocrinology 2009, 34:1198-1207.
23. Fox H.C., Sofuoglu M., Morgan P.T., Tuit K.L., Sinha R. The effects of exogenous progesterone on drug craving and stress arousal in cocaine dependence: impact of gender and cue type. Psychoneuroendocrinology 2013, 38:1532-1544.
24. George O., Sanders C., Freiling J., Grigoryan E., Vu S., Allen C.D., Crawford E., Mandyam C.D., Koob G.F. Recruitment of medial prefrontal cortex neurons during alcohol withdrawal predicts cognitive impairment and excessive alcohol drinking. Proc. Natl Acad. Sci. U. S. A 2012, 109:18156-18161.
25. Girdler S.S., Straneva P.A., Light K.C., Pedersen C.A., Morrow A.L. Allopregnanolone levels and reactivity to mental stress in premenstrual dysphoric disorder. Biol. Psychiatry 2001, 49:788-797.
26. Golden C.J. Identification of brain disorders by the Stroop Color and Word Test. J. Clin. Psychol. 1976, 32:654-658.
27. Herman J.P., Mueller N.K., Figueiredo H. Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann. N. Y. Acad. Sci. 2004, 1018:35-45.
28. Holdstock L., Penland S.N., Morrow A.L., de Wit H. Moderate doses of ethanol fail to increase plasma levels of neurosteroid 3alpha-hydroxy-5alpha-pregnan-20-one-like immunoreactivity in healthy men and women. Psychopharmacology (Berl.) 2006, 186:442-450.
29. Izard C. Patterns of Emotions: A New Analysis of Anxiety and Depression 1972, Academic Press, New York.
30. Lambert J.J., Belelli D., Harney S.C., Peters J.A., Frenguelli B.G. Modulation of native and recombinant GABA(A) receptors by endogenous and synthetic neuroactive steroids. Brain Res. Brain Res. Rev. 2001, 37:68-80.
31. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 232:1004-1007.
32. Marx C.E., Stevens R.D., Shampine L.J., Uzunova V., Trost W.T., Butterfield M.I., Massing M.W., Hamer R.M., Morrow A.L., Lieberman J.A. Neuroactive steroids are altered in schizophrenia and bipolar disorder: relevance to pathophysiology and therapeutics. Neuropsychopharmacology 2006, 31:1249-1263.
33. Marx C.E., Trost W.T., Shampine L., Behm F.M., Giordano L.A., Massing M.W., Rose J.E. Neuroactive steroids, negative affect, and nicotine dependence severity in male smokers. Psychopharmacology (Berl.) 2006, 186:462-472.
34. McCance-Katz E.F., Carroll K.M., Rounsaville B.J. Gender differences in treatment-seeking cocaine abusers-implications for treatment and prognosis. Am. J. Addict. 1999, 8:300-311.
35. Milivojevic V., Covault J. Alcohol exposure during late adolescence increases drinking in adult Wistar rats, an effect that is not reduced by finasteride. Alcohol Alcohol 2013, 48:28-38.
36. Milivojevic V., Kranzler H.R., Gelernter J., Burian L., Covault J. Variation in genes encoding the neuroactive steroid synthetic enzymes 5alpha-reductase type 1 and 3alpha-reductase type 2 is associated with alcohol dependence. Alcohol. Clin. Exp. Res. 2011, 35:946-952.
37. Milivojevic V., Feinn R., Kranzler H.R., Covault J. Variation in AKR1C3, which encodes the neuroactive steroid synthetic enzyme 3alpha-HSD type 2 (17beta-HSD type 5), moderates the subjective effects of alcohol. Psychopharmacology (Berl.) 2014, 231:3597-3608.
38. Milivojevic V., Sinha R., Morgan P.T., Sofuoglu M., Fox H.C. Effects of endogenous and exogenous progesterone on emotional intelligence in cocaine-dependent men and women who also abuse alcohol. Hum. Psychopharmacol. 2014, 29:589-598.
39. Morrow A.L., Janis G.C., VanDoren M.J., Matthews D.B., Samson H.H., Janak P.H., Grant K.A. Neurosteroids mediate pharmacological effects of ethanol: a new mechanism of ethanol action?. Alcohol. Clin. Exp. Res. 1999, 23:1933-1940.
40. Morrow A.L., VanDoren M.J., Penland S.N., Matthews D.B. The role of GABAergic neuroactive steroids in ethanol action, tolerance and dependence. Brain Res. Brain Res. Rev. 2001, 37:98-109.
41. Nyberg S., Andersson A., Zingmark E., Wahlstrom G., Backstrom T., Sundstrom-Poromaa I. The effect of a low dose of alcohol on allopregnanolone serum concentrations across the menstrual cycle in women with severe premenstrual syndrome and controls. Psychoneuroendocrinology 2005, 30:892-901.
42. Patkar A.A., Mannelli P., Peindl K., Murray H.W., Meier B., Leone F.T. Changes in tobacco smoking following treatment for cocaine dependence. Am J. Drug Alcohol Abuse 2006, 32:135-148.
43. Peters J., LaLumiere R.T., Kalivas P.W. Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J. Neurosci. 2008, 28:6046-6053.
44. Pierucci-Lagha A., Covault J., Feinn R., Khisti R.T., Morrow A.L., Marx C.E., Shampine L.J., Kranzler H.R. Subjective effects and changes in steroid hormone concentrations in humans following acute consumption of alcohol. Psychopharmacology (Berl.) 2006, 186:451-461.
45. Porcu P., Sogliano C., Cinus M., Purdy R.H., Biggio G., Concas A. Nicotine-induced changes in cerebrocortical neuroactive steroids and plasma corticosterone concentrations in the rat. Pharmacol. Biochem. Behav. 2003, 74:683-690.
46. Purdy R.H., Morrow A.L., Moore P.H., Paul S.M. Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proceedings of the Proc. Natl. Acad. Sci. U. S. A. 1991, 88:4553-4557.
47. Russo S.J., Sun W.L., Minerly A.C., Weierstall K., Nazarian A., Festa E.D., Niyomchai T., Akhavan A., Luine V., Jenab S., Quinones-Jenab V. Progesterone attenuates cocaine-induced conditioned place preference in female rats. Brain Res. 2008, 1189:229-235.
48. Sanna E., Talani G., Busonero F., Pisu M.G., Purdy R.H., Serra M., Biggio G. Brain steroidogenesis mediates ethanol modulation of GABAA receptor activity in rat hippocampus. J. Neurosci. 2004, 24:6521-6530.
49. Sarkar J., Wakefield S., MacKenzie G., Moss S.J., Maguire J. Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors. J. Neurosci. 2011, 31:18198-18210.
50. Sinha R., Fuse T., Aubin L.R., O'Malley S.S. Psychological stress, drug-related cues and cocaine craving. Psychopharmacology (Berl.) 2000, 152:140-148.
51. Sinha R., Talih M., Malison R., Cooney N., Anderson G.M., Kreek M.J. Hypothalamic-pituitary-Adrenal axis and sympatho-Adreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology (Berl.) 2003, 170:62-72.
52. Sinha R., Garcia M., Paliwal P., Kreek M.J., Rounsaville B.J. Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch. Gen. Psychiatry 2006, 63:324-331.
53. Sinha R., Fox H.C., Paliwal P., Hong K.A., Morgan P.T., Bergquist K.L. Sex steroid hormones, stress response and drug craving in cocaine dependent women: implications for relapse susceptibility. Exp. Clin. Psychopharmacol. 2007, 15:445-452.
54. Sinha R. Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict. Biol. 2009, 14:84-98.
55. Sinha R., Tuit K. Imagery Script Development Procedures Manual 2012, via Amazon Press.
56. Sofuoglu M., Dudish-Poulsen S., Nelson D., Pentel P.R., Hatsukami D.K. Sex and menstrual cycle differences in the subjective effects from smoked cocaine in humans. Exp. Clin. Psychopharmacol. 1999, 7:274-283.
57. Stout R.L., Wirtz P.W., Carbonari J.P., Del Boca F.K. Ensuring balanced distribution of prognostic factors in treatment outcome research. J. Stud. Alcohol. Suppl. 1994, 12:70-75.
58. Substance Abuse and Mental Health Services Administration. Overview of findings from the 2006 National Survey on Drug Use and Health [Office of Applied Studies, NHSAA Series H- 21; DHHS pub. no. SMA 03-3774].Rockville, MD: SAMHSA, 2007.
59. Sveindottir H., Backstrom T. Prevalence of menstrual cycle symptom cyclicity and premenstrual dysphoric disorder in a random sample of women using and not using oral contraceptives. Acta Obstet. Gynecol. Scand. 2000, 79:405-413.
60. Tiffany S.T., Singleton E., Haertzen C.A., Henningfield J.E. The development of the cocaine craving questionnaire. Drug Alcohol Depend. 1993, 34:19-28.
61. Torres J.M., Ruiz E., Ortega E. Effects of CRH and ACTH administration on plasma and brain neurosteroid levels. Neurochem. Res. 2001, 26:555-558.
62. Torres J.M., Ortega E. Alcohol intoxication increases allopregnanolone levels in female adolescent humans. Neuropsychopharmacology 2003, 28:1207-1209.
63. Torres J.M., Ortega E. Alcohol intoxication increases allopregnanolone levels in male adolescent humans. Psychopharmacology (Berl.) 2004, 172:352-355.
64. Uzunova V., Sampson L., Uzunov D.P. Relevance of endogenous 3alpha-reduced neurosteroids to depression and antidepressant action. Psychopharmacology (Berl.) 2006, 186:351-361.
65. VanDoren M.J., Matthews D.B., Janis G.C., Grobin A.C., Devaud L.L., Morrow A.L. Neuroactive steroid 3alpha-hydroxy-5alpha-pregnan-20-one modulates electrophysiological and behavioral actions of ethanol. J. Neurosci. 2000, 20:1982-1989.
66. van Wingen G.A., Ossewaarde L., Backstrom T., Hermans E.J., Fernandez G. Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience 2011, 191:38-45.
67. Yonkers K.A., Forray A., Nich C., Carroll K.M., Hine C., Merry B.C., Shaw H., Shaw J., Sofuoglu M. Progesterone reduces cocaine use in postpartum women with a cocaine use disorder: a randomized, double-blind study. Lancet Psychiatry 2014, 1(5):360-367.