Receptor subtype-dependent galanin actions on gamma-aminobutyric acidergic neurotransmission and ethanol responses in the central amygdala

Addiction Biology

Volumn 17, Issue 4, 2012, Pages 694-705

  Bajo, Michal ^a   Madamba, Samuel G ^a   Lu, Xiaoying ^a   Sharkey, Lisa M ^b   Bartfai, Tamas ^a   Siggins, George Robert ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Alcohol; antidepressant; anxiety; electrophysiology; inhibitory postsynaptic potential; synapse

Indexed keywords

4 AMINOBUTYRIC ACID; ALCOHOL; CATECHOLAMINE; GALANIN; GALANIN RECEPTOR; GALANIN RECEPTOR 1; GALANIN RECEPTOR 2; GALANIN RECEPTOR 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL;

AMYGDALA; ANIMALS; ANXIETY; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DRUG INTERACTIONS; ETHANOL; EVOKED POTENTIALS; GABAERGIC NEURONS; GALANIN; GAMMA-AMINOBUTYRIC ACID; INDOLES; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS, PSYCHOLOGICAL;

EID: 84863447552     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2011.00360.x     Document Type: Article

References (52)

1. Bajo M, Cruz MT, Siggins GR, Messing R, Roberto M, (2008) Protein kinase C epsilon mediation of CRF- and ethanol-induced GABA release in central amygdala. Proc Natl Acad Sci U S A 105: 8410-8415. (Pubitemid 351904770)
2. Bonci A, Williams JT, (1997) Increased probability of GABA release during withdrawal from morphine. J Neurosci 17: 796-803. (Pubitemid 27024591)
3. Cassell MD, Gray TS, Kiss JZ, (1986) Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological, and immunocytochemical study. J Comp Neurol 246: 478-499. (Pubitemid 16079511)
4. Cassell MD, Freedman LJ, Shi C, (1999) The intrinsic organization of the central extended amygdala. Ann N Y Acad Sci 877: 217-241. (Pubitemid 29351860)
5. Chang GQ, Karatayev O, Ahsan R, Avena NM, Lee C, Lewis MJ, Hoebel BG, Leibowitz SF, (2007) Effect of ethanol on hypothalamic opioid peptides, enkephalin, and dynorphin: relationship with circulating triglycerides. Alcohol Clin Exp Res 31: 249-259. (Pubitemid 46155224)
6. Davis M, Rainnie D, Cassell M, (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 17: 208-214. (Pubitemid 24128464)
7. Dutar P, Lamour Y, Nicoll RA, (1989) Galanin blocks the slow cholinergic EPSP in CA1 pyramidal neurons from ventral hippocampus. Eur J Pharmacol 164: 355-360. (Pubitemid 19138643)
8. Fisone G, Wu CF, Consolo S, Nordstrom O, Brynne N, Bartfai T, Melander T, Hokfelt T, (1987) Galanin inhibits acetylcholine release in the ventral hippocampus of the rat: histochemical, autoradiographic, in vivo, and in vitro studies. Proc Natl Acad Sci U S A 84: 7339-7343.
9. Gilpin NW, Mirsa K, Herman MA, Cruz MT, Roberto M, (2011) Neuropeptide y opposes alcohol effects on gamma-aminobutyric acid release in amygdala and blocks the transition to alcohol dependence. Biol Psychiatry 69: 1091-1099.
10. Hokfelt T, Xu ZQ, Shi TJ, Holmberg K, Zhang X, (1998) Galanin in ascending systems. Focus on coexistence with 5-hydroxytryptamine and noradrenaline. Ann N Y Acad Sci 863: 252-263. (Pubitemid 29047780)
11. Jhamandas JH, Petrov T, Harris KH, Vu T, Krukoff TL, (1996) Parabrachial nucleus projection to the amygdala in the rat: electrophysiological and anatomical observations. Brain Res Bull 39: 115-126. (Pubitemid 26015484)
12. Jungnickel SR, Gundlach AL, (2005) [125I]-Galanin binding in brain of wildtype, and galanin- and GalR1-knockout mice: strain and species differences in GalR1 density and distribution. Neuroscience 131: 407-421. (Pubitemid 40222449)
13. Kang-Park MH, Kieffer BL, Roberts AJ, Siggins GR, Moore SD, (2007) Presynaptic delta opioid receptors regulate ethanol actions in central amygdala. J Pharmacol Exp Ther 320: 917-925. (Pubitemid 46147976)
14. Kang-Park MH, Kieffer BL, Roberts AJ, Roberto M, Madamba SG, Siggins GR, Moore SD, (2009) Mu-opioid receptors selectively regulate basal inhibitory transmission in the central amygdala: lack of ethanol interactions. J Pharmacol Exp Ther 328: 284-293.
15. Karatayev O, Baylan J, Leibowitz SF, (2009) Increased intake of ethanol and dietary fat in galanin overexpressing mice. Alcohol 43: 571-580.
16. Karatayev O, Baylan J, Weed V, Chang S, Wynick D, Leibowitz SF, (2010) Galanin knockout mice show disturbances in ethanol consumption and expression of hypothalamic peptides that stimulate ethanol intake. Alcohol Clin Exp Res 34: 72-80.
17. Kerekes N, Mennicken F, O'Donnell D, Hokfelt T, Hill RH, (2003) Galanin increases membrane excitability and enhances Ca(2+) currents in adult, acutely dissociated dorsal root ganglion neurons. Eur J Neurosci 18: 2957-2966. (Pubitemid 38021537)
18. Khoshbouei H, Cecchi M, Dove S, Javors M, Morilak DA, (2002) Behavioral reactivity to stress: amplification of stress-induced noradrenergic activation elicits a galanin-mediated anxiolytic effect in central amygdala. Pharmacol Biochem Behav 71: 407-417. (Pubitemid 34117710)
19. Kohler C, Hallman H, Melander T, Hokfelt T, Norheim E, (1989a) Autoradiographic mapping of galanin receptors in the monkey brain. J Chem Neuroanat 2: 269-284. (Pubitemid 19242124)
20. Kohler C, Persson A, Melander T, Theodorsson E, Sedvall G, Hokfelt T, (1989b) Distribution of galanin-binding sites in the monkey and human telencephalon: preliminary observations. Exp Brain Res 75: 375-380. (Pubitemid 19110674)
21. Leibowitz SF, Avena NM, Chang GQ, Karatayev O, Chau DT, Hoebel BG, (2003) Ethanol intake increases galanin mRNA in the hypothalamus and withdrawal decreases it. Physiol Behav 79: 103-111. (Pubitemid 36734834)
22. Lewis MJ, Johnson DF, Waldman D, Leibowitz SF, Hoebel BG, (2004) Galanin microinjection in the third ventricle increases voluntary ethanol intake. Alcohol Clin Exp Res 28: 1822-1828. (Pubitemid 39665198)
23. Lu X, Barr AM, Kinney JW, Sanna P, Conti B, Behrens MM, Bartfai T, (2005a) A role for galanin in antidepressant actions with a focus on the dorsal raphe nucleus. Proc Natl Acad Sci U S A 102: 874-879. (Pubitemid 40282758)
24. Lu X, Mazarati A, Sanna P, Shinmei S, Bartfai T, (2005b) Distribution and differential regulation of galanin receptor subtypes in rat brain: effects of seizure activity. Neuropeptides 39: 147-152. (Pubitemid 40804575)
25. Lu X, Sharkey L, Bartfai T, (2007) The brain galanin receptors: targets for novel antidepressant drugs. CNS Neurol Disord Drug Targets 6: 183-192. (Pubitemid 46916250)
26. Lu X, Ross B, Sanchez-Alavez M, Zorrilla EP, Bartfai T, (2008) Phenotypic analysis of GalR2 knockout mice in anxiety- and depression-related behavioral tests. Neuropeptides 42: 387-397.
27. Lu X, Roberts E, Xia F, Sanchez-Alavez M, Liu T, Baldwin R, Wu S, Chang J, Wasterlain CG, Bartfai T, (2010) GalR2-positive allosteric modulator exhibits anticonvulsant effects in animal models. Proc Natl Acad Sci U S A 107: 15229-15234.
28. Ma X, Tong YG, Schmidt R, Brown W, Payza K, Hodzic L, Pou C, Godbout C, Hokfelt T, Xu ZQ, (2001) Effects of galanin receptor agonists on locus coeruleus neurons. Brain Res 919: 169-174. (Pubitemid 33016602)
29. Melander T, Hokfelt T, Rokaeus A, Cuello AC, Oertel WH, Verhofstad A, Goldstein M, (1986) Coexistence of galanin-like immunoreactivity with catecholamines, 5-hydroxytryptamine, GABA and neuropeptides in the rat CNS. J Neurosci 6: 3640-3654. (Pubitemid 17208548)
30. Melander T, Kohler C, Nilsson S, Hokfelt T, Brodin E, Theodorsson E, Bartfai T, (1988) Autoradiographic quantitation and anatomical mapping of 125I-galanin binding sites in the rat central nervous system. J Chem Neuroanat 1: 213-233.
31. Mennerick S, Zorumski CF, (1995) Paired-pulse modulation of fast excitatory synaptic currents in microcultures of rat hippocampal neurons. J Physiol 488: 85-101.
32. Mennicken F, Hoffert C, Pelletier M, Ahmad S, O'Donnell D, (2002) Restricted distribution of galanin receptor 3 (GalR3) mRNA in the adult rat central nervous system. J Chem Neuroanat 24: 257-268. (Pubitemid 35291193)
33. Mitsukawa K, Lu X, Bartfai T, (2009) Bidirectional regulation of stress responses by galanin in mice: involvement of galanin receptor subtype 1. Neuroscience 160: 837-846.
34. Moller C, Sommer W, Thorsell A, Heilig M, (1999) Anxiogenic-like action of galanin after intra-amygdala administration in the rat. Neuropsychopharmacology 21: 507-512. (Pubitemid 29414795)
35. Nie Z, Schweitzer P, Roberts AJ, Madamba SG, Moore SD, Siggins GR, (2004) Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303: 1512-1514. (Pubitemid 38314419)
36. Nie Z, Zorrilla EP, Madamba SG, Rice KC, Roberto M, Siggins GR, (2009) Presynaptic CRF1 receptors mediate the ethanol enhancement of GABAergic transmission in the mouse central amygdala. ScientificWorldJournal 9: 68-85.
37. Ogren SO, Hokfelt T, Kask K, Langel U, Bartfai T, (1992) Evidence for a role of the neuropeptide galanin in spatial learning. Neuroscience 51: 1-5.
38. Ogren SO, Kuteeva E, Hokfelt T, Kehr J, (2006) Galanin receptor antagonists: a potential novel pharmacological treatment for mood disorders. CNS Drugs 20: 633-654. (Pubitemid 44141491)
39. Picciotto MR, Hawes JJ, Brunzell DH, Zachariou V, (2005) Galanin can attenuate opiate reinforcement and withdrawal. Neuropeptides 39: 313-315. (Pubitemid 40804603)
40. Pich EM, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F, (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15: 5439-5447.
41. Pieribone VA, Xu ZQ, Zhang X, Grillner S, Bartfai T, Hokfelt T, (1995) Galanin induces a hyperpolarization of norepinephrine-containing locus coeruleus neurons in the brainstem slice. Neuroscience 64: 861-874.
42. Roberto M, Siggins GR, (2006) Nociceptin/orphanin FQ presynaptically decreases GABAergic transmission and blocks the ethanol-induced increase of GABA release in central amygdala. Proc Natl Acad Sci U S A 103: 9715-9720. (Pubitemid 43955890)
43. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR, (2003) Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci U S A 100: 2053-2058. (Pubitemid 36254572)
44. Roberto M, Cruz M, Bajo M, Siggins GR, Parsons LH, Schweitzer P, (2010a) The endocannabinoid system tonically regulates inhibitory transmission and depresses the effect of ethanol in central amygdala. Neuropsychopharmacology 35: 1962-1972.
45. Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, Bajo M, Cottone P, Madamba SG, Stouffer DG, Zorrilla EP, Koob GF, Siggins GR, Parsons LH, (2010b) Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol Psychiatry 67: 831-839.
46. Salin PA, Malenka RC, Nicoll RA, (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16: 797-803. (Pubitemid 26124056)
47. Sharkey LM, Madamba SG, Siggins GR, Bartfai T, (2008) Galanin alters GABAergic neurotransmission in the dorsal raphe nucleus. Neurochem Res 33: 285-291.
48. Swanson CJ, Blackburn TP, Zhang X, Zheng K, Xu ZQ, Hokfelt T, Wolinsky TD, Konkel MJ, Chen H, Zhong H, Walker MW, Craig DA, Gerald CP, Branchek TA, (2005) Anxiolytic- and antidepressant-like profiles of the galanin-3 receptor (Gal3) antagonists SNAP 37889 and SNAP 398299. Proc Natl Acad Sci U S A 102: 17489-17494. (Pubitemid 41740893)
49. Xu ZQ, Bartfai T, Langel U, Hokfelt T, (1998a) Effects of three galanin analogs on the outward current evoked by galanin in locus coeruleus. Ann N Y Acad Sci 863: 459-465. (Pubitemid 29047804)
50. Xu ZQ, Hokfelt T, (1997) Expression of galanin and nitric oxide synthase in subpopulations of serotonin neurons of the rat dorsal raphe nucleus. J Chem Neuroanat 13: 169-187. (Pubitemid 27424932)
51. Xu ZQ, Tong YG, Hokfelt T, (2001) Galanin enhances noradrenaline-induced outward current on locus coeruleus noradrenergic neurons. Neuroreport 12: 1779-1782. (Pubitemid 32521505)
52. Xu ZQ, Zhang X, Pieribone VA, Grillner S, Hokfelt T, (1998b) Galanin-5-hydroxytryptamine interactions: electrophysiological, immunohistochemical and in situ hybridization studies on rat dorsal raphe neurons with a note on galanin R1 and R2 receptors. Neuroscience 87: 79-94. (Pubitemid 28351170)