Endogenous GDNF in ventral tegmental area and nucleus accumbens does not play a role in the incubation of heroin craving

Addiction Biology

Volumn 16, Issue 2, 2011, Pages 261-272

  Airavaara, Mikko ^a   Pickens, Charles L ^a   Stern, Anna L ^a   Wihbey, Kristina A ^a   Harvey, Brandon K ^a   Bossert, Jennifer M ^a   Liu, Qing Rong ^a   Hoffer, Barry J ^a   Shaham, Yavin ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

CDNF; craving; drug self administration; extinction; GDNF; incubation; MANF; neurotrophic factors; nucleus accumbens; reinstatement; relapse; ventral tegmental area

Indexed keywords

ANTI GDNF MONOCLONAL NEUTRALIZING ANTIBODY; DIAMORPHINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; DRUG SEEKING BEHAVIOR; GENE EXPRESSION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME;

ANIMALS; ASSOCIATION LEARNING; CUES; EXTINCTION, PSYCHOLOGICAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HEROIN; HEROIN DEPENDENCE; MALE; NARCOTICS; NUCLEUS ACCUMBENS; RATS; RATS, LONG-EVANS; RNA, MESSENGER; SUBSTANCE WITHDRAWAL SYNDROME; VENTRAL TEGMENTAL AREA;

EID: 79952491194     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2010.00281.x     Document Type: Article

References (67)

1. Airavaara M, Tuomainen H, Piepponen TP, Saarma M, Ahtee L, (2007) Effects of repeated morphine on locomotion, place preference and dopamine in heterozygous glial cell line-derived neurotrophic factor knockout mice. Genes Brain Behav 6: 287-298. (Pubitemid 46587989)
2. Alvarez-Jaimes L, Polis I, Parsons LH, (2008) Attenuation of cue-induced heroin-seeking behavior by cannabinoid CB1 antagonist infusions into the nucleus accumbens core and prefrontal cortex, but not basolateral amygdala. Neuropsychopharmacology 33: 2483-2493.
3. Beninger RJ, Gerdjikov T, (2004) The role of signaling molecules in reward-related incentive learning. Neurotox Res 6: 91-104.
4. Boger HA, Middaugh LD, Huang P, Zaman V, Smith AC, Hoffer BJ, Tomac AC, Granholm AC, (2006) A partial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Exp Neurol 202: 336-347. (Pubitemid 44692677)
5. Bossert JM, Gray SM, Lu L, Shaham Y, (2006) Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology 31: 2197-2209. (Pubitemid 44413197)
6. Bossert JM, Poles GC, Wihbey KA, Koya E, Shaham Y, (2007) Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J Neurosci 27: 12655-12663. (Pubitemid 350127821)
7. Caprioli D, Celentano M, Dubla A, Lucantonio F, Nencini P, Badiani A, (2009) Ambience and drug choice: cocaine- and heroin-taking as a function of environmental context in humans and rats. Biol Psychiatry 65: 893-899.
8. Caprioli D, Celentano M, Paolone G, Lucantonio F, Bari A, Nencini P, Badiani A, (2008) Opposite environmental regulation of heroin and amphetamine self-administration in the rat. Psychopharmacology (Berl) 198: 395-404.
9. Carnicella S, Ahmadiantehrani S, Janak PH, Ron D, (2009a) GDNF is an endogenous negative regulator of ethanol-mediated reward and of ethanol consumption after a period of abstinence. Alcohol Clin Exp Res 33: 1012-1024.
10. Carnicella S, Amamoto R, Ron D, (2009b) Excessive alcohol consumption is blocked by glial cell line-derived neurotrophic factor. Alcohol 43: 35-43.
11. Carnicella S, Ron D, (2009) GDNF-a potential target to treat addiction. Pharmacol Ther 122: 9-18.
12. Conrad KL, Tseng KY, Uejima JL, Reimers JM, Heng LJ, Shaham Y, Marinelli M, Wolf ME, (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454: 118-121. (Pubitemid 351931970)
13. Crombag H, Bossert JM, Koya E, Shaham Y, (2008) Context-induced relapse to drug seeking: a review. Philos Trans R Soc Lond B Biol Sci 363: 3233-3243.
14. Das KP, Chao SL, White LD, Haines WT, Harry GJ, Tilson HA, Barone S, Jr, (2001) Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience 103: 739-761. (Pubitemid 32239339)
15. Ettenberg A, Pettit HO, Bloom FE, Koob GF, (1982) Heroin and cocaine intravenous self-administration in rats: mediation by separate neural systems. Psychopharmacology 78: 204-209. (Pubitemid 13250843)
16. Fallon JH, Moore RY, (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J Comp Neurol 180: 545-580.
17. Feltenstein MW, See RE, (2008) The neurocircuitry of addiction: an overview. Br J Pharmacol 154: 261-274. (Pubitemid 351670601)
18. Freeman WM, Patel KM, Brucklacher RM, Lull ME, Erwin M, Morgan D, Roberts DC, Vrana KE, (2008) Persistent alterations in mesolimbic gene expression with abstinence from cocaine self-administration. Neuropsychopharmacology 33: 1807-1817. (Pubitemid 351832593)
19. Gash DM, Gerhardt GA, Hoffer BJ, (1998) Effects of glial cell line-derived neurotrophic factor on the nigrostriatal dopamine system in rodents and nonhuman primates. Adv Pharmacol 42: 911-915.
20. Ghitza UE, Zhai H, Wu P, Airavaara M, Shaham Y, Lu L, (2010) Role of BDNF and GDNF in drug reward and relapse: a review. Neurosci Biobehav Rev 35: 157-171.
21. Girault JA, Valjent E, Caboche J, Herve D, (2007) ERK2: a logical AND gate critical for drug-induced plasticity? Curr Opin Pharmacol 7: 77-85. (Pubitemid 46238037)
22. Green-Sadan T, Kinor N, Roth-Deri I, Geffen-Aricha R, Schindler CJ, Yadid G, (2003) Transplantation of glial cell line-derived neurotrophic factor-expressing cells into the striatum and nucleus accumbens attenuates acquisition of cocaine self-administration in rats. Eur J Neurosci 18: 2093-2098. (Pubitemid 37372392)
23. Grimm JW, Hope BT, Wise RA, Shaham Y, (2001) Incubation of cocaine craving after withdrawal. Nature 412: 141-142. (Pubitemid 32674700)
24. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y, (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23: 742-747. (Pubitemid 36206164)
25. Groenewegen HJ, Mulder AB, Beijer AVJ, Wright CI, Lopez DA Silva FH, Pennartz CM, (1999) Hippocampal and amygdaloidinteractions in the nucleus accumbens. Psychobiology 27: 149-164.
26. He DY, McGough NN, Ravindranathan A, Jeanblanc J, Logrip ML, Phamluong K, Janak PH, Ron D, (2005) Glial cell line-derived neurotrophic factor mediates the desirable actions of the anti-addiction drug ibogaine against alcohol consumption. J Neurosci 25: 619-628.
27. Hoffer BJ, Hoffman A, Bowenkamp K, Huettl P, Hudson J, Martin D, Lin LF, Gerhardt GA, (1994) Glial cell line-derived neurotrophic factor reverses toxin-induced injury to midbrain dopaminergic neurons in vivo. Neurosci Lett 182: 107-111. (Pubitemid 24362034)
28. Hollander JA, Carelli RM, (2007) Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. J Neurosci 27: 3535-3539. (Pubitemid 46515120)
29. Hudson J, Granholm AC, Gerhardt GA, Henry MA, Hoffman A, Biddle P, Leela NS, Mackerlova L, Lile JD, Collins F, Hoffer BJ, (1995) Glial cell line-derived neurotrophic factor augments midbrain dopaminergic circuits in vivo. Brain Res Bull 36: 425-432.
30. Koya E, Uejima JM, Wihbey KA, Bossert JM, Hope BT, Shaham Y, (2009) Role of ventral medial prefrontal cortex in incubation of cocaine craving. Neuropharmacology 56 (Suppl 1): 117-185.
31. Lee JL, Milton AL, Everitt BJ, (2006) Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26: 5881-5887. (Pubitemid 44318352)
32. Li YQ, Li FQ, Wang XY, Wu P, Zhao M, Xu CM, Shaham Y, Lu L, (2008) Central amygdala extracellular signal-regulated kinase signaling pathway is critical to incubation of opiate craving. J Neurosci 28: 13248-13257.
33. Lin LF, Doherty DH, Lile JD, Bektesh S, Collins F, (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260: 1130-1132. (Pubitemid 23186789)
34. Lindholm P, Voutilainen MH, Lauren J, Peranen J, Leppanen VM, Andressoo JO, Lindahl M, Janhunen S, Kalkkinen N, Timmusk T, Tuominen RK, Saarma M, (2007) Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448: 73-77. (Pubitemid 47037006)
35. Lu L, Dempsey J, Liu SY, Bossert JM, Shaham Y, (2004a) A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J Neurosci 24: 1604-1611. (Pubitemid 38240955)
36. Lu L, Grimm JW, Dempsey J, Shaham Y, (2004b) Cocaine seeking over extended withdrawal periods in rats: different time courses of responding induced by cocaine cues versus cocaine priming over the first 6 months. Psychopharmacology 176: 101-108. (Pubitemid 39506373)
37. Lu L, Grimm JW, Hope BT, Shaham Y, (2004c) Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47 (Suppl 1): 214-226. (Pubitemid 39298266)
38. Lu L, Hope BT, Dempsey J, Liu SY, Bossert JM, Shaham Y, (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8: 212-219. (Pubitemid 40194052)
39. Lu L, Koya E, Zhai H, Hope BT, Shaham Y, (2006) Role of ERK in cocaine addiction. Trends Neurosci 29: 695-703. (Pubitemid 44794537)
40. Lu L, Wang X, Wu P, Xu C, Zhao M, Morales M, Harvey BK, Hoffer BJ, Shaham Y, (2009) Role of ventral tegmental area glial cell line-derived neurotrophic factor in incubation of cocaine craving. Biol Psychiatry 66: 137-145.
41. Martin D, Miller G, Cullen T, Fischer N, Dix D, Russell D, (1996) Intranigral or intrastriatal injections of GDNF: effects on monoamine levels and behavior in rats. Eur J Pharmacol 317: 247-256. (Pubitemid 27014028)
42. McDonald AJ, (1991) Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44: 15-33.
43. Messer CJ, Eisch AJ, Carlezon WA, Jr, Whisler K, Shen L, Wolf DH, Westphal H, Collins F, Russell DS, Nestler EJ, (2000) Role for GDNF in biochemical and behavioral adaptations to drugs of abuse. Neuron 26: 247-257.
44. Neisewander JL, Baker DA, Fuchs RA, Tran-Nguyen LT, Palmer A, Marshall JF, (2000) Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 20: 798-805. (Pubitemid 30225582)
45. O'Brien CP, Ehrman RN, Ternes JW, (1986) Classical conditioning in human opioid dependence. In:, Goldberg S, Stolerman I, eds. Behavioral Analysis of Drug Dependence, pp. 329-356. Orlando, FL: Academic Press.
46. Petrova P, Raibekas A, Pevsner J, Vigo N, Anafi M, Moore MK, Peaire AE, Shridhar V, Smith DI, Kelly J, Durocher Y, Commissiong JW, (2003) MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J Mol Neurosci 20: 173-188.
47. Pierce RC, Kumaresan V, (2006) The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30: 215-238. (Pubitemid 41821810)
48. Riccio DC, Ackil J, Burch-Vernon A, (1992) Forgetting of stimulus attributes: methodological implications for assessing associative phenomena. Psychol Bull 112: 433-445.
49. Robbins TW, (1975) The potentiation of conditioned reinforcement by psychomotor stimulant drugs: a test of Hill's hypothesis. Psychopharmacologia 45: 103-114.
50. Rogers JL, Ghee S, See RE, (2008) The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 151: 579-588.
51. Russo SJ, Mazei-Robison MS, Ables JL, Nestler EJ, (2009) Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56 (Suppl 1): 73-82.
52. Salvatore MF, Zhang JL, Large DM, Wilson PE, Gash CR, Thomas TC, Haycock JW, Bing G, Stanford JA, Gash DM, Gerhardt GA, (2004) Striatal GDNF administration increases tyrosine hydroxylase phosphorylation in the rat striatum and substantia nigra. J Neurochem 90: 245-254. (Pubitemid 38879178)
53. Self DW, (2004) Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system. Neuropharmacology 47 (Suppl 1): 242-255. (Pubitemid 39298268)
54. Self DW, Nestler EJ, (1998) Relapse to drug-seeking: neural and molecular mechanisms. Drug Alcohol Depend 51: 49-69.
55. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J, (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168: 3-20. (Pubitemid 36851158)
56. Shalev U, Grimm JW, Shaham Y, (2002) Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54: 1-42. (Pubitemid 34208828)
57. Shalev U, Morales M, Hope B, Yap J, Shaham Y, (2001) Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology 156: 98-107. (Pubitemid 32646331)
58. Sorge RE, Stewart J, (2005) The contribution of drug history and time since termination of drug taking to footshock stress-induced cocaine seeking in rats. Psychopharmacology 183: 210-217. (Pubitemid 41609273)
59. Stinus L, Cador M, Le Moal M, (1992) Interaction between endogenous opiods and dopamine within the nucleus accumbens. Ann N Y Acad Sci 654: 254-273.
60. Tomac A, Widenfalk J, Lin LF, Kohno T, Ebendal T, Hoffer BJ, Olson L, (1995) Retrograde axonal transport of glial cell line-derived neurotrophic factor in the adult nigrostriatal system suggests a trophic role in the adult. Proc Natl Acad Sci U S A 92: 8274-8278.
61. Wang J, Carnicella S, Ahmadiantehrani S, He DY, Barak S, Kharazia V, Hamida SBAZ, Shippenberg TS, Ron D, (2010) Nucleus accumbens-derived GDNF Is a retrograde enhancer of dopaminergic tone in the mesocorticolimbic system (in press).
62. Wikler A, (1973) Dynamics of drug dependence, implication of a conditioning theory for research and treatment. Arch Gen Psychiatry 28: 611-616.
63. Wise RA, (2009) Roles for nigrostriatal-not just mesocorticolimbic- dopamine in reward and addiction. Trends Neurosci 32: 517-524.
64. Wise RA, Hoffman DC, (1992) Localization of drug reward mechanisms by intracranial injections. Synapse 10: 247-263.
65. Wolf ME, (2003) Effects of psychomotor stimulants on glutamate receptor expression. Methods Mol Med 79: 13-31.
66. Yan Y, Yamada K, Niwa M, Nagai T, Nitta A, Nabeshima T, (2007) Enduring vulnerability to reinstatement of methamphetamine-seeking behavior in glial-cell-line-derived neurotrophic factor mutant mice. Faseb J 21: 1994-2004. (Pubitemid 47026435)
67. Zhou W, Zhang F, Liu H, Tang S, Lai M, Zhu H, Kalivas PW, (2009) Effects of training and withdrawal periods on heroin seeking induced by conditioned cue in an animal of model of relapse. Psychopharmacology 203: 677-684.