Corticotropin-releasing factor (CRF) sensitization of ethanol withdrawal-induced anxiety-like behavior is brain site specific and mediated by CRF-1 receptors: Relation to stress-induced sensitization

Journal of Pharmacology and Experimental Therapeutics

Volumn 332, Issue 1, 2010, Pages 298-307

  Huang, Mae M ^a   Overstreet, David H ^a   Knapp, Darin J ^a,c   Angel, Robert ^a   Wills, Tiffany A ^a,c   Navarro, Montserrat ^b   Rivier, Jean ^d   Vale, Wylie ^d   Breese, George R ^a,c  

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

^b University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 CHLORO 4 METHOXY 5 METHYLPHENYL) N [2 CYCLOPROPYL 1 (3 FLUORO 4 METHYLPHENYL)ETHYL] 5 METHYL N (2 PROPYNYL) 2 THIAZOLAMINE; BUTYL[2,5 DIMETHYL 7 (2,4,6 TRIMETHYLPHENYL) 7H PYRROLO[2,3 D]PYRIMIDIN 4 YL]ETHYLAMINE; CORTICOTROPIN RELEASING FACTOR; UROCORTIN III;

ADAPTATION; ALCOHOL WITHDRAWAL; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; EXPOSURE; HYPOTHALAMUS; MALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; STRESS; STRIA TERMINALIS;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; BRAIN MAPPING; CORTICOTROPIN-RELEASING HORMONE; ETHANOL; MALE; MICROINJECTIONS; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS, PSYCHOLOGICAL; SUBSTANCE WITHDRAWAL SYNDROME; UROCORTINS;

EID: 73949139173     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.159186     Document Type: Article

References (53)

1. Akirav I and Richter-Levin G (1999) Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 19:10530-10535.
2. Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985: 185-205.
3. Baldwin HA, Rassnick S, Rivier J, Koob GF, and Britton KT (1991) CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology (Berl) 103:227-232.
4. Bale TL and ValeWW(2004) CRF and CRF receptors: Role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525-557.
5. Ballenger JC and Post RM (1978) Kindling as a model for alcohol withdrawal syndromes. Br J Psychiatry 133:1-14.
6. Breese GR, Chu K, Dayas CV, Funk D, Knapp DJ, Koob GF, Lê DA, O'Dell LE, Overstreet DH, Roberts AJ, et al. (2005a) Stress enhancement of craving during sobriety: Risk of relapse. Alcohol Clin Exp Res 29:185-195.
7. Breese GR, Knapp DJ, and Overstreet DH (2004) Stress sensitization of ethanol withdrawal-induced reduction in social interaction: inhibition by CRF-1 and benzodiazepine receptor antagonists and a 5-HT1A-receptor agonist. Neuropsychopharmacology 29:470-482.
8. Breese GR, Overstreet DH, and Knapp DJ (2005b) Conceptual framework for the etiology of alcoholism - a "kindling"/stress hypothesis. Psychopharmacology (Berl) 178:367-380.
9. Breese GR, Overstreet DH, Knapp DJ, and NavarroM(2005c) Prior multiple ethanol withdrawals enhance stress-induced anxiety-like behavior-like behavior: inhibition by CRF1- and benzodiazepine-receptor antagonists and a 5-HT1a-receptor agonist. Neuropsychopharmacology 30:1662-1669.
10. Conger JJ (1956) Alcoholism: theory, problem and challenge. Reinforcement theory and the dynamics of alcoholism. Q J Stud Alcohol 17:296-305.
11. Cummings S, Elde R, Ells J, and Lindall A (1983) Corticotropin-releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study. J Neurosci 3:1355-1368.
12. Davis M, Walker DL, and Lee Y (1997) Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety-like behavior measured with the acoustic startle reflex. Philos Trans R Soc Lond B Biol Sci 352:1675-1687.
13. De Souza EB, Insel TR, Perrin MH, Rivier J, Vale WW, and Kuhar MJ (1985) CRF receptors are widely distributed with the rat central nervous system: an autoradiographic study. J Neurosci 5:3189-3203.
14. Dong HW, Petrovich GD, and Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38:192-246.
15. Egli RE and Winder DG (2003) Dorsal and ventral distribution of excitable and synaptic properties of neurons of the bed nucleus of the stria terminalis. J Neurophysiol 90:405-414.
16. File S (1980) The use of social interaction as a method for detecting anxiolytic activity of chlordiazepoxide-like drugs. J Neurosci Meth 2:219-238.
17. File SE and Seth P (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463:35-53.
18. Frye GD, McCown TJ, and Breese GR (1983) Characterization of susceptibility of audiogenic seizures in ethanol-dependent rats after microinjection of gammaaminobutyric acid (GABA) agonists into the inferior colliculus, substantia nigra, or medial septum. J Pharmacol Exp Ther 227:663-670.
19. Griebel G, Simiand J, Steinberg R, Jung M, Gully D, Roger P, Geslin M, Scatton B, Maffrand JP, and Soubrié P (2002) 4-(2-Chloro-4-methoxy-5- methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4-methylphenyl)ethyl] 5-methyl-N-(2-propynyl)-1, 3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophin-releasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J Pharmacol Exp Ther 301:333-345.
20. Hauger RL, Grigoriadis DE, Dallman MF, Plotsky PM, Vale WW, and Dautzenberg FM (2003) International Union of Pharmacology. XXXVI. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacol Rev 55:21-26.
21. Heilig M and Koob GF (2007) A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurol Sci 30:399-408.
22. Heilig M, Thorsell A, Cippitelli A, Gehlert D, and Ciccocioppo R (2007) Negative affect and excessive alcohol drinking driven by central CRF systems: Reversal by the novel CRF1 antagonist MTIP. Alcoholism Clin Exp Res 31:283A.
23. Huang M, Navarro M, Wills T, Knapp DJ, Overstreet DH, Angel R, and Breese GR (2008) Corticotropin releasing factor (CRF) has brain region specific effects on ethanol withdrawal-induced anxiety: relation to stress-induced drinking. Alcohol Clin Exp Res 32:79A.
24. Knapp DJ, Overstreet DH, Angel RA, Navarro M, and Breese GR (2007) The amygdala regulates the antianxiety sensitization effect of flumazenil during repeated chronic ethanol or repeated stress. Alcohol Clin Exp Res 31:1872-1882.
25. Koob GF (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27:232-243.
26. Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11-34.
27. Koob GF and Heinrichs SC (1999) A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Res 848:141-152.
28. Lee Y, Fitz S, Johnson PL, and Shekhar A (2008) Repeated stimulation of CRF receptors in the BNST of rats selectively induces social but not panic-like anxiety. Neuropsychopharmacology 33:2586-2594.
29. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, Donaldson C, Vaughan J, Reyes TM, Gulyas J, Fischer W, et al. (2001) Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci U S A 98:7570-7575.
30. Liang J, Zhang N, Cagetti E, Houser CR, Olsen RW, and Spigelman I (2006) Chronic intermittent ethanol-induced switch of ethanol actions from extrasynaptic to synaptic hippocampal GABAA receptors. J Neurosci 26:1749-1758.
31. McCown TJ and Breese GR (1990) Multiple withdrawals from chronic ethanol "kindles" inferior collicular seizure activity: evidence for kindling of seizures associated with alcoholism. Alcohol Clin Exp Res 14:394-399.
32. McEwen BS (2001) Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 933:265-277.
33. 2C ligands. Psychopharmacology (Berl) 187:1-12.
34. Overstreet DH, Knapp DJ, and Breese GR (2002) Accentuated decrease in social interaction in rats subjected to repeated ethanol withdrawals. Alcohol Clin Exp Res 26:1259-1268.
35. Overstreet DH, Knapp DJ, and Breese GR (2004) Modulation of multiple ethanol withdrawal-induced anxiety-like behavior by CRF and CRF1 receptors. Pharmacol Biochem Behav 77:405-413.
36. Overstreet DH, Knapp DJ, and Breese GR (2007) Drug challenges reveal differences in mediation of stress facilitation of voluntary alcohol drinking and withdrawal-induced anxiety in alcohol-preferring P rats. Alcohol Clin Exp Res 31:1473-1481.
37. Overstreet DH, Knapp DJ, Moy SS, and Breese GR (2003) A 5-HT1A agonist and a 5-HT2C antagonist reduce social interaction deficit induced by multiple ethanol withdrawals in rats. Psychopharmacology 167:344-352.
38. Paxinos G and Watson C (2005) The Rat Brain in Stereotaxic Coordinates, 5th ed., Elsevier Academic Press, Oxford, United Kingdom.
39. Rassnick S, Heinrichs SC, Britton KT, and Koob GF (1993) Microinjection of CRF antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Res 605:25-32.
40. Rivier J, Spiess J, and Vale W (1983) Characterization of the rat hypothalamic corticotropin-releasing factor. Proc Natl Acad Sci U S A 80:4851-4855.
41. Sahuque LL, Kullberg EF, Mcgeehan AJ, Kinder JR, Hicks MP, Blanton MG, Janak PH, and Olive MF (2006) Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology (Berl) 186:122-132.
42. Schulz DW, Mansbach RS, Sprouse J, Braselton JP, Collins J, Corman M, Dunaiskis A, Faraci S, Schmidt AW, Seeger T, et al. (1996) CP-154,526: a potent and selective nonpeptide antagonist of corticotropin releasing factor receptors. Proc Natl Acad Sci U S A 93:10477-10482.
43. Sheth A, Berretta S, Lange N, and Eichenbaum H (2008) The amygdala modulates neuronal activation in the hippocampus in response to spatial novelty. Hippocampus. 18:169-181.
44. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343-359.
45. Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105-130.
46. Sinha R, Fox HC, Hong KA, Bergquist K, Bhagwagar Z, and Siedlarz KM (2009) Enhanced negative emotion and alcohol craving, and altered physiological responses following stress and cue exposure in alcohol dependent individuals. Neuropsychopharmacology 34:1198-1208.
47. Spina MG, Merlo-Pich E, Akwa Y, Balducci C, Basso AM, Zorrilla EP, Britton KT, Rivier J, Vale WW, and Koob GF (2002) Time-dependent induction of anxiogeniclike effects after central infusion of urocortin or corticotropin-releasing factor in the rat. Psychopharmacology (Berl) 160:113-121.
48. Swanson LW, Sawchenko PE, Rivier J, and Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165-186.
49. Valdez GR, Zorrilla EP, Roberts AJ, and Koob GF (2003) Antagonism of corticotropin-releasing factor attenuates the enhanced responsiveness to stress observed during protracted ethanol abstinence. Alcohol 29:55-60.
50. Vale W, Spiess J, Rivier C, and Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotrophin and betaendorphin. Science 213:1394-1397.
51. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, and Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
52. Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, Sutton S, Chan R, Turnbull AV, Lovejoy D, and Rivier C (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and the corticotopin-releasing factor. Nature 378: 287-292.
53. Yoon G, Kim SW, Thuras P, Grant JE, and Westermeyer J (2006) Alcohol craving in outpatients with alcohol dependence: rate and clinical correlates. J Stud Alcohol 67:770-777.