Activation of the hypothalamic-pituitary-adrenal axis by addictive drugs: Different pathways, common outcome

Trends in Pharmacological Sciences

Volumn 31, Issue 7, 2010, Pages 318-325

  Armario, Antonio ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; AMPHETAMINE; CANNABINOID; COCAINE; CORTICOTROPIN; GLUCOCORTICOID; NICOTINE; OPIATE; PROTEIN C FOS; CENTRAL NERVOUS SYSTEM AGENTS; NARCOTIC ANALGESIC AGENT;

ALCOHOLISM; CORTICOTROPIN RELEASE; DRUG DEPENDENCE; GENE EXPRESSION; HOMEOSTASIS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MENTAL STRESS; NEUROCHEMISTRY; NEUROENDOCRINE SYSTEM; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THALAMUS MIDLINE NUCLEUS; TOBACCO DEPENDENCE; ADDICTION; ANIMAL; DRUG EFFECTS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; TREATMENT OUTCOME;

AMPHETAMINE; ANALGESICS, OPIOID; ANIMALS; CANNABINOIDS; CENTRAL NERVOUS SYSTEM AGENTS; COCAINE; ETHANOL; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; METABOLIC NETWORKS AND PATHWAYS; NICOTINE; PITUITARY-ADRENAL SYSTEM; SUBSTANCE-RELATED DISORDERS; TREATMENT OUTCOME;

EID: 77954033594     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2010.04.005     Document Type: Review

References (100)

1. Koob G. A role for brain stress systems in addiction. Neuron 2008, 59:11-34.
2. Charmandari E., et al. Endocrinology of the stress response. Annu. Rev. Physiol. 2005, 67:259-284.
3. Herman J.P., et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front. Neuroendocrinol. 2003, 24:151-180.
4. Armario A. The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors?. CNS Neurol. Disord. Drug Targets 2006, 5:485-501.
5. Kovacs K.J., Sawchenko P.E. Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J. Neurosci. 1996, 16:262-273.
6. Rivier C., Lee S. Acute alcohol administration stimulates the activity of hypothalamic neurons that express corticotrophin-releasing factor and vasopressin. Brain Res. 1996, 726:1-10.
7. Hauger R.L., et al. Corticotropin-releasing factor receptors and pituitary adrenal responses during immobilization stress. Endocrinology 1988, 123:396-405.
8. Vinson G.P., et al. The neuroendocrinology of the adrenal cortex. J. Neuroendocrinol. 1994, 6:235-246.
9. De Kloet E.R., et al. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
10. De Kloet E.R., et al. Corticosteroid hormones in the central stress response: quick-and-slow. Front. Neuroendocrinol. 2008, 29:268-272.
11. Vuong C., et al. The Effects of Opioids and Opioid Analogs on Animal and Human Endocrine Systems. Endocr. Rev. 2010, 31:98-132.
12. Pfeiffer A., Herz A. Endocrine actions of opioids. Horm. Metab. Res. 1984, 16:386-397.
13. Bartolome M.B., Kuhn C.M. Endocrine effects of methadone in rats; acute effects in adults. Eur. J. Pharmacol. 1983, 95:231-238.
14. Haracz J.L., et al. Effect of intraventricular beta-endorphin and morphine on hypothalamic-pituitary-adrenal activity and the release of pituitary beta-endorphin. Neuroendocrinology 1981, 33:170-175.
15. Pfeiffer A., et al. Central kappa- and mu-opiate receptors mediate ACTH-release in rats. Endocrinology 1985, 116:2688-2690.
16. Iyengar S., et al. Mu-, delta-, kappa- and epsilon-opioid receptor modulation of the hypothalamic-pituitary-adrenocortical (HPA) axis: subchronic tolerance studies of endogenous opioid peptides. Brain Res. 1987, 435:220-226.
17. Roy S., et al. Role of hypothalamic-pituitary axis in morphine-induced alteration in thymic cell distribution using mu-opioid receptor knockout mice. J. Neuroimmunol. 2001, 116:147-155.
18. Buckingham J.C. Secretion of corticotrophin and its hypothalamic releasing factor in response to morphine and opioid peptides. Neuroendocrinology 1982, 35:111-116.
19. Nikolarakis K., et al. The role of CRF in the release of ACTH by opiate agonists and antagonists in rats. Brain Res. 1987, 421:373-376.
20. Lightman S.L., Young W.S. Corticotrophin-releasing factor, vasopressin and pro-opiomelanocortin mRNA responses to stress and opiates in the rat. J. Physiol. 1988, 403:511-523.
21. Zhou Y., et al. Hypothalamic-pituitary-adrenal activity and pro-opiomelanocortin mRNA levels in the hypothalamus and pituitary of the rat are differentially modulated by acute intermittent morphine with or without water restriction stress. J Endocrinol 1999, 163:261-267.
22. Laorden M.L., et al. Activation of c-fos expression in hypothalamic nuclei by mu- and kappa-receptor agonists: correlation with catecholaminergic activity in the hypothalamic paraventricular nucleus. Endocrinology 2000, 141:1366-1376.
23. Wang X.Q., et al. Intracerebroventricular administration of beta-endorphin increases the expression of c-fos and of corticotropin-releasing factor messenger ribonucleic acid in the paraventricular nucleus of the rat. Brain Res. 1996, 707:189-195.
24. Reed B., et al. Extracellular biotransformation of β-endorphin in rat striatum and cerebrospinal fluid. J. Neuroendocrinol. 2008, 20:606-616.
25. Mansour A., et al. Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 1995, 18:22-29.
26. Jezova D., et al. ACTH and corticosterone response to naloxone and morphine in normal, hypophysectomized and dexamethasone-treated rats. Life Sci. 1982, 31:307-314.
27. Jezova D. Stimulation of ACTH release by naloxone: central or peripheral action?. Life Sci. 1985, 37:1007-1013.
28. Siegel R.A., et al. Effects of naloxone on basal and stress-induced ACTH and corticosterone secretion in the male rat--site and mechanism of action. Brain Res. 1982, 249:103-109.
29. Rivier C. Alcohol stimulates ACTH secretion in the rat: mechanisms of action and interactions with other stimuli. Alcohol Clin. Exp. Res. 1996, 20:240-254.
30. Richardson H.N., et al. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur. J. Neurosci. 2008, 28:1641-1653.
31. Lee S., et al. Site of action of acute alcohol administration in stimulating the rat hypothalamic-pituitary-adrenal axis: comparison between the effect of systemic and intracerebroventricular injection of this drug on pituitary and hypothalamic responses. Endocrinology 2004, 145:4470-4479.
32. Ogilvie K.M., et al. Divergence in the expression of molecular markers of neuronal activation in the parvocellular paraventricular nucleus of the hypothalamus evoked by alcohol administration via different routes. J. Neurosci. 1998, 18:4344-4352.
33. Quertemont E., et al. The role of acetaldehyde in the neurobehavioral effects of ethanol: a comprehensive review of animal studies. Prog. Neurobiol. 2005, 75:247-274.
34. Kinoshita H., et al. Acetaldehyde, a metabolite of ethanol, activates the hypothalamic-pituitary-adrenal axis in the rat. Alcohol Alcohol. 2001, 36:59-64.
35. Pastor R., et al. Brain catalase activity inhibition as well as opioid receptor antagonism increases ethanol-induced HPA axis activation. Alcohol Clin. Exp. Res. 2004, 28:1898-1906.
36. Rivier C., et al. Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of corticotropin-releasing factor (CRF). J. Pharmacol. Exp. Ther. 1984, 229:127-131.
37. Lee S., et al. 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. 2001, 25:427-433.
38. Lolait S.J., et al. Attenuated stress response to acute lipopolysaccharide challenge and ethanol administration in vasopressin V1b receptor knockout mice. J. Neuroendocrinol. 2007, 19:543-551.
39. Ogilvie K.M., et al. Role of arginine vasopressin and corticotropin-releasing factor in mediating alcohol-induced adrenocorticotropin and vasopressin secretion in male rats bearing lesions of the paraventricular nuclei. Brain Res. 1997, 744:83-95.
40. Li Z., et al. Effect of ethanol on the regulation of corticotropin-releasing factor (CRF) gene expression. Mol. Cell. Neurosci. 2005, 29:345-354.
41. Steiner M.A., Wotjak C.T. Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis. Prog. Brain Res. 2008, 170:397-432.
42. Weidenfeld J., et al. Effect of the brain constituent anandamide, a cannabinoid receptor agonist, on the hypothalamo-pituitary-adrenal axis in the rat. Neuroendocrinology 1994, 59:110-112.
43. Manzanares J., et al. Opioid and cannabinoid receptor-mediated regulation of the increase in adrenocorticotropin hormone and corticosterone plasma concentrations induced by central administration of delta(9)-tetrahydrocannabinol in rats. Brain Res. 1999, 839:173-179.
44. Puder M., et al. Corticotrophin and corticosterone secretion following delta 1-Tetrahydrocannabinol, in intact and in hypothalamic deafferentated male rats. Exp Brain Res 1982, 46:85-88.
45. Cota D., et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 2003, 112:423-431.
46. Saber-Tehrani A., et al. Cannabinoids and their interactions with diazepam on modulation of serum corticosterone concentration in male mice. Neurochem. Res. 2010, 35:60-66.
47. Wenger T., et al. Arachidonyl ethanolamide (anandamide) activates the parvocellular part of hypothalamic paraventricular nucleus. Biochem. Biophys. Res. Commun. 1997, 237:724-728.
48. Wenger T., et al. The endogenous cannabinoid, anandamide, activates the hypothalamo-pituitary-adrenal axis in CB1 cannabinoid receptor knockout mice. Neuroendocrinology 2003, 78:294-300.
49. Wade M.R., et al. Cannabinoid CB1 receptor antagonism modulates plasma corticosterone in rodents. Eur. J. Pharmacol. 2006, 551:162-167.
50. Patel S., et al. Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 2004, 145:5431-5438.
51. Steiner M.A., et al. Impaired cannabinoid receptor type 1 signaling interferes with stress-coping behavior in mice. Pharmacogenomics J. 2008, 8:196-208.
52. Di S., et al. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 2003, 23:4850-4857.
53. Ganon-Elazar E., Akirav I. Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J. Neurosci. 2009, 29:11078-11088.
54. Hill M.N., et al. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 2009, 34:2733-2745.
55. Rodriguez de Fonseca F., et al. Corticotropin-releasing factor (CRF) antagonist [D-Phe12,Nle21, 38,C alpha MeLeu37]CRF attenuates the acute actions of the highly potent cannabinoid receptor agonist HU-210 on defensive-withdrawal behavior in rats. J. Pharmacol. Exp. Ther. 1996, 276:56-64.
56. McLaughlin R.J., et al. Monoaminergic neurotransmission contributes to cannabinoid-induced activation of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 2009, 624:71-76.
57. Cam G.R., et al. The action of nicotine on the pituitary-adrenal cortical axis. Arch. Int. Pharmacodyn. Ther. 1979, 237:49-66.
58. Donny E.C., et al. Differential effects of response-contingent and response-independent nicotine in rats. Eur. J. Pharmacol. 2000, 402:231-240.
59. Chen H., et al. Chronic nicotine self-administration augments hypothalamic-pituitary-adrenal responses to mild acute stress. Neuropsychopharmacology 2008, 33:721-730.
60. Weidenfeld J., et al. Further studies on the stimulatory action of nicotine on adrenocortical function in the rat. Neuroendocrinology 1989, 50:132-138.
61. Matta S.H., et al. Nicotine stimulates the expression of cFos protein in the parvocellular paraventricular nucleus and brainstem catecholaminergic regions. Endocrinology 1993, 132:2149-2156.
62. Matta S.H., et al. Nicotinic activation of CRH neurons in extrahypothalamic regions of the rat brain. Endocrine 1997, 7:245-253.
63. Loughlin S.E., et al. Nicotine modulation of stress-related peptide neurons. J. Comp. Neurol. 2006, 497:575-588.
64. Matta S.G., et al. Response of the hypothalamo-pituitary-adrenal axis to nicotine. Psychoneuroendocrinology 1998, 23:103-113.
65. Matta S.H., et al. Nicotine elevates rat plasma ACTH by a central mechanism. J. Pharmacol. Exp. Ther. 1987, 243:217-226.
66. Matta S.H., et al. Role of the fourth cerebroventricle in mediating rat plasma ACTH responses to intravenous nicotine. J. Pharmacol. Exp. Ther. 1990, 252:623-630.
67. Matta S.H., et al. selective administration of nicotine into catecholaminergic regions of rat brainstem stimulates adrenocorticotropin secretion. Endocrinology 1993, 133:2935-2942.
68. Valentine J.D., et al. Nicotine-induced cFos expression in the hypothalamic paraventricular nucleus is dependent on brainstem effects: correlations with cFos in catecholaminergic and noncatecholaminergic neurons in the nucleus tractus solitarius. Endocrinology 1996, 137:622-630.
69. Matta S.H., et al. Catecholamines mediate nicotine-induced adrenocorticotropin secretion via α-adrenergic receptors. Endocrinology 1990, 127:1646-1655.
70. Fu Y., et al. Adrenocorticotropin response and nicotine-induced norepinephrine secretion in the rat paraventricular nucleus are mediated through brainstem receptors. Endocrinology 1997, 138:1935-1943.
71. Fu Y., et al. Nicotine-induced norepinephrine release in the rat amygdala and hippocampus is mediated through brainstem nicotinic cholinergic receptors. J. Pharmacol. Exp. Ther. 1998, 284:1188-1196.
72. Zhao R., et al. Nicotine-induced norepinephrine release in hypothalamic paraventricular nucleus and amygdala is mediated by N-methyl-D-aspartate receptors and nitric oxide in the nucleus tractus solitarius. J. Pharmacol. Exp. Ther. 2007, 320:837-844.
73. Okada S., et al. Extrahypothalamic corticotropin-releasing hormone mediates (-)-nicotine-induced elevation of plasma corticosterone in rats. Eur. J. Pharmacol. 2003, 473:217-223.
74. Rivier C., Vale W. Cocaine stimulates adrenocorticotropin (ACTH) secretion through a corticotropin-releasing factor (CRF)-mediated mechanism. Brain Res. 1987, 422:403-406.
75. Sarnyai Z., et al. Cocaine-induced elevation of plasma corticosterone is mediated by different neurotransmitter systems in rats. Pharmacol. Biochem. Behav. 1993, 45:209-214.
76. Torres G., Rivier C. Differential effects of intermittent or continuous exposure to cocaine on the hypothalamic-pituitary-adrenal axis and c-fos expression. Brain Res. 1992, 571:204-211.
77. Mantsch J.R., et al. Effects of cocaine self-administration on plasma corticosterone and prolactin in rats. J. Pharmacol. Exp. Ther. 2000, 294:239-247.
78. Mantsch J.R., et al. Neuroendocrine alterations in a high-dose, extended-access rat self-administration model of escalating cocaine use. Psychoneuroendocrinology 2003, 28:836-862.
79. Galici R., et al. Comparison of noncontingent versus contingent cocaine administration on plasma corticosterone levels in rats. Eur. J. Pharmacol. 2000, 387:59-62.
80. Palamarchouk V., et al. Self-administered and passive cocaine infusions produce different effects on corticosterone concentrations in the medial prefrontal cortex (MPC) of rats. Pharmacol. Biochem. Behav. 2009, 94:163-168.
81. Levy A.D., et al. Cocaine-induced elevation of plasma adrenocorticotropin hormone and corticosterone is mediated by serotonergic neurons. J. Pharmacol. Exp. Ther. 1991, 259:495-500.
82. Saphier D., et al. Effects of intracerebroventricular and intrahypothalamic cocaine administration on adrenocortical secretion. Neuroendocrinology 1993, 57:54-62.
83. Rivier C., Lee S. Stimulatory effect of cocaine on ACTH secretion: role of the hypothalamus. Mol. Cell Neurosci. 1994, 5:189-195.
84. Calogero A.E., et al. Cocaine stimulates rat hypothalamic corticotropin-releasing hormone secretion in vitro. Brain Res. 1989, 505:7-11.
85. Ikemoto S., Goeders N.E. Microinjections of dopamine agonists and cocaine elevate plasma corticosterone: dissociation effects among the ventral and dorsal striatum and medial prefrontal cortex. Brain Res. 1998, 814:171-178.
86. Sarnyai Z., et al. The cocaine-induced elevation of plasma corticosterone is mediated by endogenous corticotropin-releasing factor (CRF) in rats. Brain Res. 1992, 589:154-156.
87. Borowsky B., Kuhn C.M. Monoamine mediation of cocaine-induced hypothalamo-pituitary-adrenal activation. J. Pharmacol. Exp. Ther. 1991, 256:204-210.
88. Spangler R., et al. Behavioral stereotypies induced by " binge' cocaine administration are independent of drug-induced increases in corticosterone levels. Behav. Brain Res. 1997, 86:201-204.
89. Zhou Y., et al. Effects of selective D1- or D2-like dopamine receptor antagonists with acute " binge" pattern cocaine on corticotropin-releasing hormone and proopiomelanocortin mRNA levels in the hypothalamus. Brain Res. Mol. Brain Res. 2004, 130:61-67.
90. Zhou Y., et al. Effects of chronic 'Binge' cocaine administration on plasma ACTH and corticosterone levels in mice deficient in DARPP-32. Neuroendocrinology 1999, 70:196-199.
91. Torres G., et al. A ketamine mixture anesthetic inhibits neuroendocrine and behavioral consequences of cocaine administration. Brain Res. 1994, 656:33-42.
92. Damianopoulos E.N., Carey R.J. Evidence for N-methyl-D-aspartate receptor mediation of cocaine induced corticosterone release and cocaine conditioned stimulant effects. Behav. Brain Res. 1995, 68:219-228.
93. Elliott J.M., Beveridge T.J. Psychostimulants and monoamine transporters: upsetting the balance. Curr. Opin. Pharmacol. 2005, 5:94-100.
94. Knych E.T., Eisenberg R.M. Effect of amphetamine on plasma corticosterone in the conscious rat. Neuroendocrinology 1979, 29:110-118.
95. Swerdlow N.R., et al. Pituitary-adrenal axis responses to acute amphetamine in the rat. Pharmacol. Biochem. Behav. 1993, 45:629-637.
96. Gagliano H., et al. Repeated amphetamine administration in rats revealed consistency across days and a complete dissociation between locomotor and hypothalamic-pituitary-adrenal axis effects of the drug. Psychopharmacology (Berl) 2009, 207:447-459.
97. Rotllant D., et al. Differential effects of stress and amphetamine administration on Fos-like protein expression in corticotropin releasing factor-neurons of the rat brain. Dev. Neurobiol. 2007, 67:702-714.
98. Williams M.T., et al. Ontogeny of the adrenal response to (+)-methamphetamine in neonatal rats: the effect of prior drug exposure. Stress 2006, 9:153-163.
99. Nash J.F., et al. Elevation of serum prolactin and corticosterone concentrations in the rat after the administration of 3,4-methylenedioxymethamphetamine. J. Pharmacol. Exp. Ther. 1988, 245:873-879.
100. Doyle J.R., Yamamoto B.K. Serotonin 2 receptor modulation of hyperthermia, corticosterone, and hippocampal serotonin depletions following serial exposure to chronic stress and methamphetamine. Psychoneuroendocrinology 2009, [Epub ahead of print].