Synaptic depression via mGluR1 positive allosteric modulation suppresses cue-induced cocaine craving

Nature Neuroscience

Volumn 17, Issue 1, 2014, Pages 73-80

  Loweth, Jessica A ^a   Scheyer, Andrew F ^a   Milovanovic, Mike ^a   Lacrosse, Amber L ^b   Flores Barrera, Eden ^a   Werner, Craig T ^a   Li, Xuan ^a   Ford, Kerstin A ^a   Le, Tuan ^a   Olive, M Foster ^b   Szumlinski, Karen K ^c   Tseng, Kuei Y ^a   Wolf, Marina E ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893716354     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3590     Document Type: Article

References (52)

1. Pickens, C.L. et al. Neurobiology of the incubation of drug craving. Trends Neurosci. 34, 411-420 (2011).
2. Reichel, C.M. & Bevins, R.A. Forced abstinence model of relapse to study pharmacological treatments of substance use disorder. Curr. Drug Abuse Rev. 2, 184-194 (2009).
3. Sesack, S.R. & Grace, A.A. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47 (2010).
4. Kalivas, P.W. & Volkow, N.D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 162, 1403-1413 (2005).
5. Wolf, M.E. & Tseng, K.Y. Calcium-permeable AMPA receptors in the VTA and nucleus accumbens after cocaine exposure: when, how and why? Front. Mol. Neurosci. 5, 72 (2012).
6. Conrad, K.L. et al. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454, 118-121 (2008).
7. Mameli, M. et al. Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat. Neurosci. 12, 1036-1041 (2009).
8. Purgianto, A. et al. Different adaptations in AMPA receptor transmission in the nucleus accumbens after short versus long access cocaine self-administration regimens. Neuropsychopharmacology 38, 1789-1797 (2013).
9. Ferrario, C.R. et al. Alterations in AMPA receptor subunits and TARPs in the rat nucleus accumbens related to the formation of Ca2+-permeable AMPA receptors during the incubation of cocaine craving. Neuropharmacology 61, 1141-1151 (2011).
10. McCutcheon, J.E. et al. Group I mGluR activation reverses cocaine-induced accumulation of calcium-permeable AMPA receptors in nucleus accumbens synapses via a protein kinase C-dependent mechanism. J. Neurosci. 31, 14536-14541 (2011).
11. McCutcheon, J.E., Wang, X., Tseng, K.Y., Wolf, M.E. & Marinelli, M. Calcium-permeable AMPA receptors are present in nucleus accumbens synapses after prolonged withdrawal from cocaine self-administration but not experimenter-administered cocaine. J. Neurosci. 31, 5737-5743 (2011).
12. Bellone, C. & Lüscher, C. mGluRs induce a long-term depression in the ventral tegmental area that involves a switch of the subunit composition of AMPA receptors. Eur. J. Neurosci. 21, 1280-1288 (2005).
13. Bellone, C. & Lüscher, C. Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat. Neurosci. 9, 636-641 (2006).
14. Mameli, M., Balland, B., Luján, R. & Lüscher, C. Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530-533 (2007).
15. Kelly, L., Farrant, M. & Cull-Candy, S.G. Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat. Neurosci. 12, 593-601 (2009).
16. Clem, R.L. & Huganir, R.L. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330, 1108-1112 (2010).
17. Robbe, D., Kopf, M., Remaury, A., Bockaert, J. & Manzoni, O.J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 99, 8384-8388 (2002).
18. Lovinger, D.M. Presynaptic modulation by endocannabinoids. Handb. Exp. Pharmacol. 184, 435-477 (2008).
19. Milton, A.L. & Everitt, B.J. The persistence of maladaptive memory: addiction, drug memories and anti-relapse treatments. Neurosci. Biobehav. Rev. 36, 1119-1139 (2012).
20. Vanderschuren, L.J. & Ahmed, S.H. Animal studies of addictive behavior. Cold Spring Harb. Perspect. Med. 3, a011932 (2013).
21. Ngomba, R.T. et al. Protective role for type-1 metabotropic glutamate receptors against spike and wave discharges in the WAG/Rij rat model of absence epilepsy. Neuropharmacology 60, 1281-1291 (2011).
22. Kalivas, P.W. The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572 (2009).
23. Reimers, J.M., Milovanovic, M. & Wolf, M.E. Quantitative analysis of AMPA receptor subunit composition in addiction-related brain regions. Brain Res. 1367, 223-233 (2011).
24. Bellone, C., Mameli, M. & Lüscher, C. In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA. Nat. Neurosci. 14, 1439-1446 (2011).
25. Szumlinski, K.K., Ary, A.W. & Lominac, K.D. Homers regulate drug-induced neuroplasticity: implications for addiction. Biochem. Pharmacol. 75, 112-133 (2008).
26. Xiao, B. et al. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707-716 (1998).
27. Kammermeier, P.J., Xiao, B., Tu, J.C., Worley, P.F. & Ikeda, S.R. Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J. Neurosci. 20, 7238-7245 (2000).
28. Kammermeier, P.J. & Worley, P.F. Homer 1a uncouples metabotropic glutamate receptor 5 from postsynaptic effects. Proc. Natl. Acad. Sci. USA 104, 6055-6060 (2007).
29. Kammermeier, P.J. Endogenous Homer proteins regulate metabotropic glutamate receptor signaling in neurons. J. Neurosci. 28, 8560-8567 (2008).
30. Ben-Shahar, O. et al. Extended daily access to cocaine results in distinct alterations in Homer 1b/c and NMDA receptor subunit expression within the medial prefrontal cortex. Synapse 63, 598-609 (2009).
31. Hu, J.-H. et al. Preso1 dynamically regulates group I metabotropic glutamate receptors. Nat. Neurosci. 15, 836-844 (2012).
32. Szumlinski, K.K. et al. Homer proteins regulate sensitivity to cocaine. Neuron 43, 401-413 (2004).
33. Szumlinski, K.K. et al. Homer isoforms differentially regulate cocaine-induced neuroplasticity. Neuropsychopharmacology 31, 768-777 (2006).
34. Edwards, S., Bachtell, R.K., Guzman, D., Whisler, K.N. & Self, D.W. Emergence of context-associated GluR1 and ERK phosphorylation in the nucleus accumbens core during withdrawal from cocaine self-administration. Addict. Biol. 16, 450-457 (2011).
35. Fourgeaud, L. et al. A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J. Neurosci. 24, 6939-6945 (2004).
36. Moussawi, K. et al. N-Acetylcysteine reverses cocaine-induced metaplasticity. Nat. Neurosci. 12, 182-189 (2009).
37. Grueter, B.A., Brasnjo, G. & Malenka, R.C. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci. 13, 1519-1525 (2010).
38. Huang, C.C. et al. Cocaine withdrawal impairs metabotropic glutamate receptor-dependent long-term depression in the nucleus accumbens. J. Neurosci. 31, 4194-4203 (2011).
39. Olive, M.F. Metabotropic glutamate receptor ligands as potential therapeutics for addiction. Curr. Drug Abuse Rev. 2, 83-98 (2009).
40. Dravolina, O.A., Danysz, W. & Bespalov, A.Y. Effects of group I metabotropic glutamate receptor antagonists on the behavioral sensitization to motor effects of cocaine in rats. Psychopharmacology (Berl.) 187, 397-404 (2006).
41. Olive, M.F., Cleva, R.M., Kalivas, P.W. & Malcolm, R.J. Glutamatergic medications for the treatment of drug and behavioral addictions. Pharmacol. Biochem. Behav. 100, 801-810 (2012).
42. Argilli, E., Sibley, D.R., Malenka, R.C., England, P.M. & Bonci, A. Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J. Neurosci. 28, 9092-9100 (2008).
43. Olive, M.F. Cognitive effects of Group I metabotropic glutamate receptor ligands in the context of drug addiction. Eur. J. Pharmacol. 639, 47-58 (2010).
44. Loweth, J.A., Tseng, K.Y. & Wolf, M.E. Using metabotropic glutamate receptors to modulate cocaine's synaptic and behavioral effects: mGluR1 finds a niche. Curr. Opin. Neurobiol. 23, 500-506 (2013).
45. Gardner, S.M. et al. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915 (2005).
46. Lobo, M.K. et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390 (2010).
47. Bock, R. et al. Strengthening the accumbal indirect pathway promotes resilience to compulsive cocaine use. Nat. Neurosci. 16, 632-638 (2013).
48. Lee, B.R. et al. Maturation of silent synapses in amygdala-accumbens projection contributes to incubation of cocaine craving. Nat. Neurosci. 16, 1644-1651 (2013).
49. Vieira, E. et al. Fluorinated 9H-xanthene-9-carboxlic acid oxazol-2-yl-amides as potent, orally available mGlu1 receptor enhances. Bioorg. Med. Chem. Lett. 19, 1666-1669 (2009).
50. Jingami, H., Nakanishi, S. & Morikawa, K. Structure of the metabotropic gluatame receptor. Curr. Opin. Neurobiol. 13, 271-278 (2003).
51. Klugmann, M. & Szumlinski, K.K. Targeting Homer genes using adeno-associated viral vector: lessons learned from behavioural and neurochemical studies. Behav. Pharmacol. 19, 485-500 (2008).
52. Lominac, K.D. et al. Distinct roles for different Homer1 isoforms in behaviors and associated prefrontal cortex function. J. Neurosci. 25, 11586-11594 (2005).