Role of a genetic polymorphism in the corticotropin-releasing factor receptor 1 gene in alcohol drinking and seeking behaviors of Marchigian Sardinian alcohol-preferring rats

Frontiers in Psychiatry

Volumn 4, Issue APR, 2013, Pages

  Ayanwuyi, Lydia O ^a   Carvajal, Francisca ^a   Lerma Cabrera, Jose M ^a   Domi, Esi ^a   Björk, Karl ^b   Ubaldi, Massimo ^a   Heilig, Markus ^b   Roberto, Marisa ^c   Ciccocioppo, Roberto ^a   Cippitelli, Andrea ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

CRF; msP; Relapse; Self administration; SNP; Yohimbine

Indexed keywords

ANTALARMIN; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; YOHIMBINE;

ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRINKING BEHAVIOR; DRUG DOSE COMPARISON; DRUG MECHANISM; GENETIC ASSOCIATION; GENETIC LINE; GENETIC POLYMORPHISM; INSTRUMENTAL CONDITIONING; MALE; NONHUMAN; PHENOTYPE; POINT MUTATION; RAT; REINFORCEMENT; STRESS;

EID: 84877710696     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2013.00023     Document Type: Article

References (74)

1. Abercrombie, E. D., Keller, R. W. Jr., and Zigmond, M. J. (1988). Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 27, 897-904.
2. Aghajanian, G. K., and VanderMaelen, C. P. (1982). Alpha 2-adrenoceptormediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science 215, 1394-1396.
3. Arnold, J. M., and Roberts, D. C. (1997). A critique of fixed and progressive ratio schedules used to examine the neural substrates of drug reinforcement. Pharmacol. Biochem. Behav. 57, 441-447.
4. Bhaskar, L. V., Thangaraj, K., Wasnik, S., Singh, L., and Raghavendra Rao, V. (2012). Dopamine transporter (DAT1) VNTR polymorphism and alcoholism in two culturally different populations of south India. Am. J. Addict. 21, 343-347.
5. Breese, G. R., Overstreet, D. H., and Knapp, D. J. (2005a). Conceptual framework for the etiology of alcoholism: a "kindling"/stress hypothesis. Psychopharmacology (Berl.) 178, 367-380.
6. Breese, G. R., Overstreet, D. H., Knapp, D. J., and Navarro, M. (2005b). Prior multiple ethanol withdrawals enhance stress-induced anxiety-like behavior: inhibition by CRF1and benzodiazepine-receptor antagonists and a 5-HT1a-receptor agonist. Neuropsychopharmacology 30, 1662-1669.
7. Breese, G. R., Sinha, R., and Heilig, M. (2011). Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse. Pharmacol. Ther. 129, 149-171.
8. Bremner, J. D., Krystal, J. H., Southwick, S. M., and Charney, D. S. (1996a). Noradrenergic mechanisms in stress and anxiety: I. Preclinical studies. Synapse 23, 28-38.
9. Bremner, J. D., Krystal, J. H., Southwick, S. M., and Charney, D. S. (1996b). Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse 23, 39-51.
10. Chu, K., Koob, G. F., Cole, M., Zorrilla, E. P., and Roberts, A. J. (2007). Dependence-induced increases in ethanol self-administration in mice are blocked by the CRF1 receptor antagonist antalarmin and by CRF1 receptor knockout. Pharmacol. Biochem. Behav. 86, 813-821.
11. Ciccocioppo, R. (2013). Genetically selected alcohol preferring rats to model human alcoholism. Curr. Top. Behav. Neurosci. 13, 251-269.
12. Ciccocioppo, R., Economidou, D., Cippitelli, A., Cucculelli, M., Ubaldi, M., Soverchia, L., et al. (2006). Genetically selected Marchigian Sardinian alcohol-preferring (msP) rats: an animal model to study the neurobiology of alcoholism. Addict. Biol. 11, 339-355.
13. Ciccocioppo, R., Gehlert, D. R., Ryabinin, A., Kaur, S., Cippitelli, A., Thorsell, A., et al. (2009). Stress-related neuropeptides and alcoholism: CRH, NPY, and beyond. Alcohol 43, 491-498.
14. Ciccocioppo, R., Panocka, I., Froldi, R., Colombo,G.,Gessa,G. L.,and Massi, M. (1999).Antidepressant-like effect of ethanol revealed in the forced swimming test in Sardinian alcoholpreferring rats. Psychopharmacology (Berl.) 144, 151-157.
15. Cippitelli, A., Bilbao, A., Gorriti, M. A., Navarro, M., Massi, M., Piomelli, D., et al. (2007). The anandamide transport inhibitor AM404 reduces ethanol self-administration. Eur. J. Neurosci. 26, 476-486.
16. Cippitelli, A., Cannella, N., Braconi, S., Duranti,A., Tontini,A., Bilbao,A., et al. (2008). Increase of brain endocannabinoid anandamide levels by FAAH inhibition and alcohol abuse behaviours in the rat. Psychopharmacology (Berl.) 198, 449-460.
17. Cippitelli, A., Damadzic, R., Hansson, A. C., Singley, E., Sommer, W. H., Eskay, R., et al. (2010a). Neuropeptide Y (NPY) suppresses yohimbineinduced reinstatement of alcohol seeking. Psychopharmacology (Berl.) 208, 417-426.
18. Cippitelli, A., Karlsson, C., Shaw, J. L., Thorsell, A., Gehlert, D. R., and Heilig, M. (2010b). Suppression of alcohol self-administration and reinstatement of alcohol seeking by melanin-concentrating hormone receptor 1 (MCH1-R) antagonism in Wistar rats. Psychopharmacology (Berl.) 211, 367-375.
19. Cippitelli, A., Damadzic, R., Singley, E., Thorsell, A., Ciccocioppo, R., Eskay, R. L., et al. (2012). Pharmacological blockade of corticotropin-releasing hormone receptor 1 (CRH1R) reduces voluntary consumption of high alcohol concentrations in nondependent Wistar rats. Pharmacol. Biochem. Behav. 100, 522-529.
20. Cloninger, C. R., Bohman, M., and Sigvardsson, S. (1981). Inheritance of alcohol abuse. Cross-fostering analysis of adopted men. Arch. Gen. Psychiatry 38, 861-868.
21. Colombo, G., Agabio, R., Lobina, C., Reali, R., Zocchi, A., Fadda, F., et al. (1995). Sardinian alcoholpreferring rats: a genetic animal model of anxiety. Physiol. Behav. 57, 1181-1185.
22. Edenberg, H. J., and Kranzler, H. R. (2005). The contribution of genetics to addiction therapy approaches. Pharmacol. Ther. 108, 86-93.
23. Enoch, M. A., and Goldman, D. (1999). Genetics of alcoholism and substance abuse. Psychiatr. Clin. North Am. 22, 289-299.
24. Enoch, M. A., Shen, P. H., Ducci, F., Yuan, Q., Liu, J., White, K. V., et al. (2008). Common genetic origins for EEG, alcoholism and anxiety: the role of CRH-BP. PLoS ONE 3:e3620. doi:10.1371/journal.pone.0003620
25. Erb, S., Shaham, Y., and Stewart, J. (1998). The role of corticotropinreleasing factor and corticosterone in stressand cocaine-induced relapse to cocaine seeking in rats. J. Neurosci. 18, 5529-5536.
26. Funk, C. K., O'Dell, L. E., Crawford, E. F., and Koob, G. F. (2006a). Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats. J. Neurosci. 26, 11324-11332.
27. Funk, D., Li, Z., and Le, A. D. (2006b). Effects of environmental and pharmacological stressors on cfos and corticotropin-releasing factor mRNA in rat brain: Relationship to the reinstatement of alcohol seeking. Neuroscience 138, 235-243.
28. Funk, C. K., Zorrilla, E. P., Lee, M. J., Rice, K. C., and Koob, G. F. (2007). Corticotropin-releasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats. Biol. Psychiatry 61, 78-86.
29. Gehlert, D. R., Cippitelli, A., Thorsell, A., Le, A. D., Hipskind, P. A., Hamdouchi, C., et al. (2007). 3-(4-Chloro-2morpholin-4-yl-thiazol-5-yl)-8-(1ethylpropyl)-2,6-dimethyl-imidazo [1,2-b]pyridazine: a novel brain-penetrant, orally available corticotropin-releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J. Neurosci. 27, 2718-2726.
30. Ghitza, U. E., Gray, S. M., Epstein, D. H., Rice, K. C., and Shaham, Y. (2006). The anxiogenic drug yohimbine reinstates palatable food seeking in a rat relapse model: a role of CRF1 receptors. Neuropsychopharmacology 31, 2188-2196.
31. Gilpin, N. W., and Koob, G. F. (2010). Effects of beta-adrenoceptor antagonists on alcohol drinking by alcoholdependent rats. Psychopharmacology (Berl.) 212, 431-439.
32. Gilpin, N. W., Richardson, H. N., and Koob, G. F. (2008). Effects of CRF1-receptor and opioid-receptor antagonists on dependence-induced increases in alcohol drinking by alcohol-preferring (P) rats. Alcohol. Clin. Exp. Res. 32, 1535-1542.
33. Hansson, A. C., Cippitelli, A., Sommer, W. H., Ciccocioppo, R., and Heilig, M. (2007). Region-specific downregulation of Crhr1 gene expression in alcohol-preferring msP rats following ad lib access to alcohol. Addict. Biol. 12, 30-34.
34. Hansson, A. C., Cippitelli, A., Sommer, W. H., Fedeli, A., Bjork, K., Soverchia, L., et al. (2006). Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress. Proc. Natl. Acad. Sci. U.S.A. 103, 15236-15241.
35. Heilig, M., Goldman, D., Berrettini, W., and O'Brien, C. P. (2011). Pharmacogenetic approaches to the treatment of alcohol addiction. Nat. Rev. Neurosci. 12, 670-684.
36. Heilig, M., and Koob, G. F. (2007). A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurosci. 30, 399-406.
37. Holmberg, G., and Gershon, S. (1961). Autonomic and psychic effects of yohimbine hydrochloride. Psychopharmacologia 2, 93-106.
38. Karlsson, C., Zook, M., Ciccocioppo, R., Gehlert, D. R., Thorsell, A., Heilig, M., et al. (2012). Melaninconcentrating hormone receptor 1 (MCH1-R) antagonism: reduced appetite for calories and suppression of addictive-like behaviors. Pharmacol. Biochem. Behav. 102, 400-406.
39. Koob, G. F. (2010). The role of CRF and CRF-related peptidesin thedarkside of addiction. Brain Res. 1314, 3-14.
40. Le, A. D., Harding, S., Juzytsch, W., Funk, D., and Shaham, Y. (2005). Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol selfadministration in rats. Psychopharmacology (Berl.) 179, 366-373.
41. Li,T. K.,Lumeng,L.,Doolittle,D. P.,and Carr, L. G. (1991). Molecular associations of alcohol-seeking behavior in rat lines selectively bred for high and low voluntary ethanol drinking. Alcohol. Alcohol Suppl. 1, 121-124.
42. Lovinger, D. M., and Crabbe, J. C. (2005). Laboratory models of alcoholism: treatment target identification and insight into mechanisms. Nat. Neurosci. 8, 1471-1480.
43. Lowery, E. G., Spanos, M., Navarro, M., Lyons, A. M., Hodge, C. W., and Thiele, T. E. (2010). CRF1 antagonist and CRF-2 agonist decrease binge-like ethanol drinking in C57BL/6J mice independent of the HPA axis. Neuropsychopharmacology 35, 1241-1252.
44. Marinelli, P. W., Funk, D., Juzytsch, W., Harding, S., Rice, K. C., Shaham, Y., et al. (2007). The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology (Berl.) 195, 345-355.
45. McLellan, A. T., O'Brien, C. P., Metzger, D., Alterman, A. I., Cornish, J., and Urschel, H. (1992). How effective is substance abuse treatment - compared to what? Res. Publ. Assoc. Res. Nerv. Ment. Dis. 70, 231-252.
46. Merlo Pich, E., Lorang, M., Yeganeh, M., De Fonseca, F., Raber, J., Koob, G. F., et al. (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.
47. O'Dell, L. E., Roberts, A. J., Smith, R. T., and Koob, G. F. (2004). Enhanced alcohol self-administration after intermittent versus continuous alcohol vapor exposure. Alcohol. Clin. Exp. Res. 28, 1676-1682.
48. Olive, M. F., Koenig, H. N., Nannini, M. A., and Hodge, C. W. (2002). Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake. Pharmacol. Biochem. Behav. 72, 213-220.
49. Oslin, D. W., Berrettini, W., Kranzler, H. R., Pettinati, H., Gelernter, J., Volpicelli, J. R., et al. (2003). A functional polymorphism of the mu-opioid receptor gene is associated with naltrexone response in alcohol-dependent patients. Neuropsychopharmacology 28, 1546-1552.
50. Pacak, K., Armando, I., Komoly, S., Fukuhara, K., Weise, V. K., Holmes, C., et al. (1992). Hypercortisolemia inhibits yohimbine-induced release of norepinephrine in the posterolateral hypothalamus of conscious rats. Endocrinology 131, 1369-1376.
51. Pohorecky, L. A. (1991). Stress and alcohol interaction: an update of human research. Alcohol. Clin. Exp. Res. 15, 438-459.
52. Ramchandani, V. A., Umhau, J., Pavon, F. J., Ruiz-Velasco, V., Margas, W., Sun,H.,et al. (2011).A genetic determinant of the striatal dopamine response to alcohol in men. Mol. Psychiatry 16, 809-817.
53. Ray, L. A. (2011). Stress-induced and cue-induced craving for alcohol in heavy drinkers: preliminary evidence of genetic moderation by the OPRM1 and CRH-BP genes. Alcohol. Clin. Exp. Res. 35, 166-174.
54. Rimondini, R.,Arlinde, C., Sommer,W., and Heilig, M. (2002). Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J. 16, 27-35.
55. Roberto, M., Cruz, M. T., Gilpin, N. W., Sabino, V., Schweitzer, P., Bajo, M., et al. (2010). Corticotropin releasing factor-induced amygdala gammaaminobutyric Acid release plays a key role in alcohol dependence. Biol. Psychiatry 67, 831-839.
56. Sabino, V., Cottone, P., Koob, G. F., Steardo, L., Lee, M. J., Rice, K. C., et al. (2006). Dissociation between opioid and CRF1 antagonist sensitive drinking in Sardinian alcoholpreferring rats. Psychopharmacology (Berl.) 189, 175-186.
57. Sarnyai, Z., Shaham, Y., and Heinrichs, S. C. (2001). The role of corticotropin-releasing factor in drug addiction. Pharmacol. Rev. 53, 209-243.
58. Schuckit, M. A., Li, T. K., Cloninger, C. R.,and Deitrich,R.A. (1985). Genetics of alcoholism. Alcohol. Clin. Exp. Res. 9, 475-492.
59. Shaham, Y., Funk, D., Erb, S., Brown, T. J., Walker, C. D., and Stewart, J. (1997). Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J. Neurosci. 17, 2605-2614.
60. Shaham, Y., Shalev, U., Lu, L., De Wit, H., and Stewart, J. (2003). The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl.) 168, 3-20.
61. Sinha, R. (2001). How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl.) 158, 343-359.
62. Sommer, W. H., Rimondini, R., Hansson, A. C., Hipskind, P. A., Gehlert, D. R.,Barr,C. S.,et al. (2008). Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol. Psychiatry 63, 139-145.
63. Sparta, D. R., Sparrow, A. M., Lowery, E. G., Fee, J. R., Knapp, D. J., and Thiele, T. E. (2008). Blockade of the corticotropin releasing factor type 1 receptor attenuates elevated ethanol drinking associated with drinking in the dark procedures. Alcohol. Clin. Exp. Res. 32, 259-265.
64. Stopponi, S., Somaini, L., Cippitelli, A., Cannella, N., Braconi, S., Kallupi, M., et al. (2011). Activation of nuclear PPARgamma receptors by the antidiabetic agent pioglitazone suppresses alcohol drinking and relapse to alcohol seeking. Biol. Psychiatry 69, 642-649.
65. Tovote, P., Farrokhi, C. B., Gonzales, R. M., Schnitzbauer, U., Blanchard, D. C., Blanchard, R. J., et al. (2010). Activation of central CRF receptor 1 by cortagine results in enhanced passive coping with a naturalistic threat in mice. Psychoneuroendocrinology 35, 887-895.
66. Treutlein, J., Kissling, C., Frank, J., Wiemann, S., Dong, L., Depner, M., et al. (2006). Genetic association of the human corticotropin releasing hormone receptor 1 (CRHR1) with binge drinking and alcohol intake patterns in two independent samples. Mol. Psychiatry 11, 594-602.
67. Umhau, J. C., Schwandt, M. L., Usala, J., Geyer, C., Singley, E., George, D. T., et al. (2011). Pharmacologically induced alcohol craving in treatment seeking alcoholics correlates with alcoholism severity, but is insensitive to acamprosate. Neuropsychopharmacology 36, 1178-1186.
68. Walker, B. M., and Koob, G. F. (2008). Regarding "Dynorphin is a downstream effector of striatal BDNF regulation of ethanol intake." FASEB J. 22, 2113. author reply 2113-2114.
69. Webster, E. L., Lewis, D. B., Torpy, D. J., Zachman, E. K., Rice, K. C., and Chrousos, G. P. (1996). In vivo and in vitro characterization of antalarmin, a nonpeptide corticotropinreleasing hormone (CRH) receptor antagonist: suppression of pituitary ACTH release and peripheral inflammation. Endocrinology 137, 5747-5750.
70. Wrzosek, M., Jakubczyk, A., Matsumoto, H., Lukaszkiewicz, J., Brower, K. J., and Wojnar, M. (2012). Serotonin 2A receptor gene (HTR2A) polymorphism in alcohol-dependent patients. Pharmacol. Rep. 64, 449-453.
71. Zhao, Y., Valdez, G. R., Fekete, E. M., Rivier, J. E., Vale, W. W., Rice, K. C., et al. (2007). Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxietyrelated behavior in rats. J. Pharmacol. Exp. Ther. 323, 846-854.
72. Zislis, G., Desai, T. V., Prado, M., Shah, H. P., and Bruijnzeel, A. W. (2007). Effects of the CRF receptor antagonist D-Phe CRF(12-41) and the alpha2-adrenergic receptor agonist clonidine on stress-induced reinstatement of nicotine-seeking behavior in rats. Neuropharmacology 53, 958-966.
73. Zorrilla,E. P.,Heilig,M.,DeWit,H.,and Shaham, Y. (2013). Behavioral, biological,and chemical perspectives on targeting CRF(1) receptor antagonists to treat alcoholism. Drug Alcohol Depend. 128, 175-186.
74. Zorrilla, E. P.,Valdez, G. R., and Weiss, F. (2001). Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (Berl.) 158, 374-381.