Involvement of Arginine Vasopressin and V1b Receptor in Alcohol Drinking in Sardinian Alcohol-Preferring Rats
Yan Zhou
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorGiancarlo Colombo
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorMauro A. M. Carai
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorAnn Ho
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorGian Luigi Gessa
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorMary Jeanne Kreek
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorYan Zhou
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorGiancarlo Colombo
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorMauro A. M. Carai
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorAnn Ho
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorGian Luigi Gessa
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorMary Jeanne Kreek
From the Laboratory of the Biology of Addictive Diseases (YZ, AH, MJK), The Rockefeller University, New York, New York; and Section of Cagliari (GC, MAMC, GLG), CNR Neuroscience Institute, Monserrato (CA), Italy.
Search for more papers by this authorYZ and GC contributed equally to this work.
Abstract
Background: Recent animal studies have shown that the level of stress-responsive arginine vasopressin (AVP) gene expression in the amygdala is increased during early withdrawal from long-term heroin or cocaine administration. The selective AVP V1b receptor antagonist SSR149415 (capable of exerting antidepressant-like and anxiolytic effects in animal models) also blocked stress-induced reinstatement of drug-seeking behavior. This study was undertaken to investigate the effects of alcohol and to determine whether (i) there are genetically determined differences in basal AVP mRNA levels in the medial/central amygdala (Me/CeA) and medial hypothalamus (MH) between selectively bred Sardinian alcohol-preferring (sP) and alcohol-nonpreferring (sNP) rats; (ii) the AVP mRNA levels are altered by long-term alcohol drinking in sP rats; and (iii) the V1b receptor antagonist SSR149415 alters alcohol drinking in sP rats.
Methods: In Experiment 1, AVP mRNA levels were measured in the Me/CeA and MH of alcohol-naïve sP and sNP rats, and sP rats exposed to the standard, homecage 2-bottle “alcohol versus water” choice regimen 24 h/d for 17 days. In Experiment 2, SSR149415 (0, 3, 10, or 30 mg/kg; intraperitoneal) was acutely administered 30 minutes before lights off to alcohol-experienced sP rats. Alcohol, water, and food intake were monitored 6 and 24 hours later.
Results: We found higher basal AVP mRNA levels in both Me/CeA and MH of alcohol-naïve sP than sNP rats; alcohol consumption decreased AVP mRNA levels in both brain regions of sP rats, suggesting genetically determined differences between the 2 rat lines and in the effects of alcohol drinking in sP rats. Acute treatment with SSR149415 significantly reduced alcohol intake of sP rats.
Conclusion: The stress-responsive AVP/V1b receptor system is 1 component of the neural circuitry underlying high alcohol drinking in sP rats.
References
- Agabio R, Carai MAM, Lobina C, Pani M, Reali R, Vacca G, Gessa GL, Colombo G (2001) Alcohol stimulates motor activity in selectively bred Sardinian alcohol-preferring (sP), but not in Sardinian alcohol-nonpreferring (sNP), rats. Alcohol 23: 123–126.
- Cagiano R, Cassano T, Coluccia A, Gaetani S, Giustino A, Steardo L, Tattoli M, Trabace L, Cuomo V (2002) Genetic factors involved in the effects of developmental low-level alcohol induced behavioral alterations in rats. Neuropsychopharmacology 26: 191–203.
- Caldwell HK, Stewart J, Wiedholz LM, Millstein RA, Iacangelo A, Holmes A, Young WS 3rd, Wersinger SR (2006) The acute intoxicating effects of ethanol are not dependent on the vasopressin 1a or 1b receptors. Neuropeptides 40: 325–337.
- Ciccocioppo R, Panocka I, Froldi R, Colombo G, Gessa G, Massi M (1998) Antidepressant-like effect of ethanol revealed in forced swimming test in Sardinian alcohol-preferring rats. Psychopharmacology 144: 151–157.
- Colombo G, Agabio R, Lobina C, Reali R, Zocchi A, Fadda F, Gessa GL (1995) Sardinian alcohol-preferring rats: a genetic animal model of anxiety. Physiol Behav 57: 1181–1185.
- Colombo G, Lobina C, Carai MAM, Gessa GL (2006) Phenotypic characterization of genetically selected Sardinian alcohol-preferring (sP) and -non preferring (sNP) rats. Addict Biol 11: 324–338.
- Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322: 900–904.
- Ebner K, Wotjak C, Landgraf R, Engelmann M (2002) Forced swimming triggers vasopressin release within the amygdala to modulate stress-coping strategies in rats. Eur J Neurosci 15: 384–388.
- Griebel G, Simiand J, Serradeil-Le Gal C, Wagnon J, Pascal M, Scatton B, Maffrand JP, Soubrie P (2002) Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc Natl Acad Sci USA 99: 6370–6375.
- Gulya K, Dave JR, Hoffman PL (1991) Chronic ethanol ingestion decreases vasopressin mRNA in hypothalamic and extrahypothalamic nuclei of mouse brain. Brain Res 557: 129–135.
- Harding AJ, Halliday GM, Ng JL, Harper CG, Kril JJ (1996) Loss of vasopressin-immunoreactive neurons in alcoholics is dose-related and time-dependent. Neuroscience 72: 699–708.
- Hernando F, Schoots O, Lolait SJ, Burbach JP (2001) Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin. Endocrinology 142: 1659–1668.
- Hodgson RA, Higgins GA, Guthrie DH, Lu SX, Pond AJ, Mullins DE, Guzzi MF, Parker EM, Varty GB (2007) Comparison of the V1b antagonist, SSR149415, and the CRF1 antagonist, CP-154,526, in rodent models of anxiety and depression. Pharmacol Biochem Behav 86: 431–440.
- Hwang BH, Froehlich JC, Hwang WS, Lumeng L, Li T-K (1998) More vasopressin mRNA in the paraventricular hypothalamic nucleus of alcohol-preferring rats and high alcohol-drinking rats selectively bred for high alcohol preference. Alcohol Clin Exp Res 22: 664–669.
- Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65: 768–779.
- Ishizawa H, Dave JR, Liu LI, Tabakoff B, Hoffman PL (1990) Hypothalamic vasopressin mRNA levels in mice are decreased after chronic ethanol ingestion. Eur J Pharmacol 189: 119–127.
- Ishizuka Y, Abe H, Tanoue A, Kannan H, Ishida Y (2010) Involvement of vasopressin V1b receptor in anti-anxiety action of SSRI and SNRI in mice. Neurosci Res 66: 233–237.
- Kornet M, Goosen C, Ribbens LG, Van Ree JM (1991) The effect of desglycinamide-(Arg8)-vasopressin (DGAVP) on the acquisition of free-choice alcohol drinking in rhesus monkeys. Alcohol Clin Exp Res 15: 72–79.
- Leggio B, Masi F, Grappi S, Nanni G, Gambarana C, Colombo G, de Montis MG (2003) Sardinian alcohol-preferring and non-preferring rats show different reactivity to aversive stimuli and a similar response to a natural reward. Brain Res 973: 275–284.
- Lolait SJ, O’Carroll AM, Mahan LC, Felder CC, Button DC, Young WS 3rd, Mezey E, Brownstein MJ (1995) Extrapituitary expression of the rat V1b vasopressin receptor gene. Proc Natl Acad Sci USA 92: 6783–6787.
- Overstreet DH, Griebel G (2005) Antidepressant-like effects of the vasopressin V1b receptor antagonist SSR149415 in the Flinders Sensitive Line rat. Pharmacol Biochem Behav 82: 223–227.
- Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. 2nd ed. Academic Press, New York, NY.
- Richter RM, Zorrilla EP, Basso AM, Koob GF, Weiss F (2000) Altered amygdala CRF release and increased anxiety-like behavior in Sardinian alcohol-preferring rats: a microdialysis and behavioral study. Alcohol Clin Exp Res 24: 1765–1772.
- Rigter H, Crabbe JC (1985) Vasopressin and ethanol preference. I. Effects of vasopressin and the fragment DGAVP on altered ethanol preference in Brattleboro diabetes insipidus rats. Peptides 6: 669–676.
- Rodríguez-Borrero E, Rivera-Escalera F, Candelas F, Montalvo J, Muñoz-Miranda WJ, Walker JR, Maldonado-Vlaar CS (2010) Arginine vasopressin gene expression changes within the nucleus accumbens during environment elicited cocaine-conditioned response in rats. Neuropharmacology 58: 88–101.
- Roman E, Colombo G (2009) Lower risk taking and exploratory behavior in alcohol-preferring sP rats than in alcohol non-preferring sNP rats in the multivariate concentric square field™ (MCSF) test. Behav Brain Res 205: 249–258.
- Salome N, Stemmelin J, Cohen C, Griebel G (2006) Differential roles of amygdaloid nuclei in the anxiolytic- and antidepressant-like effects of the V1b receptor antagonist, SSR149415, in rats. Psychopharmacology 187: 237–244.
- Sanbe A, Takagi N, Fujiwara Y, Yamauchi J, Endo T, Mizutani R, Takeo S, Tsujimoto G, Tanoue A (2008) Alcohol preference in mice lacking the Avpr1a vasopressin receptor. Am J Physiol Regul Integr Comp Physiol 294: R1482–R1490.
- Sarnyai Z, Vecsernyés M, Laczi F, Bíró E, Szabó G, Kovács GL (1992) Effects of cocaine on the contents of neurohypophyseal hormones in the plasma and in different brain structures in rats. Neuropeptides 23: 27–31.
- Serradeil-Le Gal C, Derick S, Brossard G, Manning M, Simiand J, Gaillard R, Griebel G, Guillon G (2003) Functional and pharmacological characterization of the first specific agonist and antagonist for the V1b receptor in mammals. Stress 6: 199–206.
- Silva SM, Madeira MD, Ruela C, Paula-Barbosa MM (2002) Prolonged alcohol intake leads to irreversible loss of vasopressin and oxytocin neurons in the paraventricular nucleus of the hypothalamus. Brain Res 925: 76–88.
- Szot P, Dorsa DM (1994) Expression of cytoplasmic and nuclear vasopressin RNA following castration and testosterone replacement: evidence for transcriptional regulation. Mol Cell Neurosci 5: 1–10.
- Van Ree JM, de Wied D (1977) Heroin self-administration is under control of vasopressin. Life Sci 21: 315–319.
- Van Ree JM, Gerrits MAFM, Vanderschuren LJMJ (1999) Opioids, reward and addiction: an encounter of biology, psychology, and medicine. Pharmacol Rev 51: 341–396.
-
Veinante P,
Freund-Mercier MJ (1997) Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study.
J Comp Neurol
383: 305–325.
10.1002/(SICI)1096-9861(19970707)383:3<305::AID-CNE3>3.0.CO;2-7 CAS PubMed Web of Science® Google Scholar
- de Wied D, Greven HM, Lande S, Witter A (1972) Dissociation of the behavioral and endocrine effects of lysine vasopressin by tryptic digestion. Br J Pharmacol 45: 118–122.
- Wigger A, Sánchez MM, Mathys KC, Ebner K, Frank E, Liu D, Kresse A, Neumann ID, Holsboer F, Plotsky PM, Landgraf R (2004) Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29: 1–14.
- Zhou Y, Bendor J, Hofmann L, Randesi M, Ho A, Kreek MJ (2006) Mu opioid receptor and orexin/hypocretin mRNA levels in the lateral hypothalamus and striatum are enhanced by morphine withdrawal. J Endocrinol 191: 137–145.
- Zhou Y, Bendor JT, Yuferov V, Schlussman SD, Ho A, Kreek MJ (2005) Amygdalar vasopressin mRNA increases in acute cocaine withdrawal: evidence for opioid receptor modulation. Neuroscience 134: 1391–1397.
- Zhou Y, Leri F, Cumming E, Hoeschele M, Kreek MJ (2008) Involvement of arginine vasopressin and its V1b receptor in heroin withdrawal and heroin seeking precipitated by stress and by heroin. Neuropsychopharmacology 33: 226–236.
