Sucrose ingestion induces Rapid AMPA receptor trafficking

Journal of Neuroscience

Volumn 33, Issue 14, 2013, Pages 6123-6132

  Tukey, David S ^a   Ferreira, Jainne M ^a,c   Antoine, Shannon O ^a   D'Amour, James A ^a   Ninan, Ipe ^a   de Vaca, Soledad Cabeza ^a   Incontro, Salvatore ^a,d   Wincott, Charlotte ^a   Horwitz, Julian K ^a   Hartner, Diana T ^a   Guarini, Carlo B ^a   Khatri, Latika ^a   Goffer, Yossef ^a   Xu, Duo ^a   Titcombe, Roseann F ^a   Khatri, Megna ^a   Marzan, Dave S ^a   Mahajan, Shahana S ^a,e   Wang, Jing ^a   Froemke, Robert C ^a,b   Carr, Kenneth D ^a   Aoki, Chiye ^b   Ziff, Edward B ^a   more..

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; DOPAMINE 1 RECEPTOR; SACCHARIN; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANNULA; CELL FRACTIONATION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; FEMALE; INGESTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

ANIMALS; CONDITIONING, OPERANT; DOPAMINE BETA-HYDROXYLASE; EXCITATORY POSTSYNAPTIC POTENTIALS; LOCOMOTION; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; NUCLEUS ACCUMBENS; PHOSPHOPROTEINS; POST-SYNAPTIC DENSITY; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SUBCELLULAR FRACTIONS; SUCROSE; SWEETENING AGENTS; SYNAPTOSOMES;

EID: 84875985402     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4806-12.2013     Document Type: Article

References (55)

1. Avena NM, Rada P, Hoebel BG (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32:20-39. CrossRef Medline
2. Basar K, Sesia T, Groenewegen H, Steinbusch HW, Visser-Vandewalle V, Temel Y (2010) Nucleus accumbens and impulsivity. Prog Neurobiol 92:533-557. CrossRef Medline
3. Berridge KC (2009) 'Liking' and 'wanting' food rewards: brain substrates and roles in eating disorders. Physiol Behav 97:537-550. CrossRef Medline
4. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225. CrossRef Medline
5. Boudreau AC, Reimers JM, Milovanovic M, Wolf ME (2007) Cell surface AMPA receptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases. J Neurosci 27: 10621-10635. CrossRef Medline
6. Brebner K, Wong TP, Liu L, Liu Y, Campsall P, Gray S, Phelps L, Phillips AG, Wang YT (2005) Nucleus accumbens long-term depression and the expression of behavioral sensitization. Science 310:1340-1343. CrossRef Medline
7. Cacciapaglia F, Saddoris MP, Wightman RM, Carelli RM (2012) Differential dopamine release dynamics in the nucleus accumbens core and shell track distinct aspects of goal-directed behavior for sucrose. Neuropharmacology 62:2050-2056. CrossRef Medline
8. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G (1992) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12:4224-4233. Medline
9. Carr KD, Chau LS, Cabeza de Vaca S, Gustafson K, Stouffer M, Tukey DS, Restituito S, Ziff EB (2010) AMPA receptor subunit GluR1 downstream of D-1 dopamine receptor stimulation in nucleus accumbens shell mediates increased drug reward magnitude in food-restricted rats. Neuroscience 165:1074-1086. CrossRef Medline
10. 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. CrossRef Medline
11. Day JJ, Carelli RM (2007) The nucleus accumbens and Pavlovian reward learning. Neuroscientist 13:148-159. CrossRef Medline
12. de Araujo IE, Oliveira-Maia AJ, Sotnikova TD, Gainetdinov RR, Caron MG, Nicolelis MA, Simon SA (2008) Food reward in the absence of taste receptor signaling. Neuron 57:930-941. CrossRef Medline
13. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54:447-460. CrossRef Medline
14. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143. CrossRef Medline
15. Gerfen CR, Surmeier DJ (2011) Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34:441-466. CrossRef Medline
16. Grueter BA, Brasnjo G, Malenka RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13:1519-1525. CrossRef Medline
17. He K, Song L, Cummings LW, Goldman J, Huganir RL, Lee HK (2009) Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proc Natl Acad Sci U S A 106: 20033-20038. Medline
18. Hu FB, Malik VS (2010) Sugar-sweetened beverages and risk of obesity and type 2 diabetes: epidemiologic evidence. Physiol Behav 100:47-54. CrossRef Medline
19. Isaac JT, Ashby MC, McBain CJ (2007) The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54:859-871. CrossRef Medline
20. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA (2004) Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics 3:857-871. CrossRef Medline
21. Kalivas PW, Pierce RC, Cornish J, Sorg BA (1998) A role for sensitization in craving and relapse in cocaine addiction. J Psychopharmacol 12:49-53. CrossRef Medline
22. Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A (2001) Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun 283:236-242. CrossRef Medline
23. Kourrich S, Rothwell PE, Klug JR, Thomas MJ (2007) Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 27:7921-7928. CrossRef Medline
24. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622-626. CrossRef Medline
25. LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iñiguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolaños CA, Kabbaj M, et al. (2010) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137-1143. CrossRef Medline
26. Liu SJ, Zukin RS (2007) Ca2+-permeableAMPAreceptors in synaptic plasticity and neuronal death. Trends Neurosci 30:126-134. CrossRef Medline
27. Lu W, Isozaki K, Roche KW, Nicoll RA (2010) Synaptic targeting of AMPA receptors is regulated by a CaMKII site in the first intracellular loop of GluA1. Proc Natl Acad Sci U S A 107:22266-22271. CrossRef Medline
28. Lüscher C, Malenka RC (2011) Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69:650-663. CrossRef Medline
29. Lu W, Roche KW (2012) Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol 22:470-479. Medline
30. Makino H, Malinow R (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64:381-390. CrossRef Medline
31. Mameli M, Halbout B, Creton C, Engblom D, Parkitna JR, Spanagel R, Lüscher C (2009) Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat Neurosci 12:1036-1041. CrossRef Medline
32. Masuda K, Koizumi A, Nakajima K, Tanaka T, Abe K, Misaka T, IshiguroM (2012) Characterization of the modes of binding between human sweet taste receptor and low-molecular-weight sweet compounds. PloS One 7:e35380. CrossRef Medline
33. Matthews K, Wilkinson LS, Robbins TW (1996) Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol Behav 59:99-107. CrossRef Medline
34. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28:58-63. CrossRef Medline
35. McCutcheon JE, Wang X, Tseng KY, Wolf ME, Marinelli M (2011a) 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. CrossRef Medline
36. McCutcheon JE, Loweth JA, Ford KA, Marinelli M, Wolf ME, Tseng KY (2011b) 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. CrossRef Medline
37. McCutcheon JE, Beeler JA, Roitman MF (2012) Sucrose-predictive cues evoke greater phasic dopamine release than saccharin-predictive cues. Synapse 66:346-351. CrossRef Medline
38. Nedelescu H, Kelso CM, Lázaro-Muñoz G, Purpura M, Cain CK, Ledoux JE, AokiC (2010) Endogenous GluR1-containingAMPAreceptors translocate to asymmetric synapses in the lateral amygdala during the early phase of fear memory formation: an electron microscopic immunocytochemical study. J Comp Neurol 518:4723-4739. CrossRef Medline
39. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381-390. CrossRef Medline
40. Oh MC, Derkach VA, Guire ES, Soderling TR (2006) Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281:752-758. Medline
41. Pascoli V, Turiault M, Lüscher C (2012) Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 481:71-75. Medline
42. Plant K, Pelkey KA, Bortolotto ZA, Morita D, Terashima A, McBain CJ, Collingridge GL, Isaac JT (2006) Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci 9:602-604. CrossRef Medline
43. Rada P, Avena NM, Hoebel BG (2005) Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134:737-744. CrossRef Medline
44. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on theAMPAreceptor GluR1 subunit. Neuron 16:1179-1188. CrossRef Medline
45. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83-88. CrossRef Medline
46. Sainz E, Korley JN, Battey JF, Sullivan SL (2001) Identification of a novel member of the T1R family of putative taste receptors. J Neurochem 77: 896-903. CrossRef Medline
47. Serulle Y, Zhang S, Ninan I, Puzzo D, McCarthy M, Khatri L, Arancio O, Ziff EB (2007) A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron 56:670-688. CrossRef Medline
48. Sesack SR, Grace AA (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27-47. CrossRef Medline
49. Smith GP (2004) Accumbens dopamine mediates the rewarding effect of orosensory stimulation by sucrose. Appetite 43:11-13. CrossRef Medline
50. Smith WB, Starck SR, Roberts RW, Schuman EM (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45: 765-779. CrossRef Medline
51. Sun X, Zhao Y, Wolf ME (2005) Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J Neurosci 25:7342-7351. CrossRef Medline
52. Sun X, Milovanovic M, Zhao Y, Wolf ME (2008) Acute and chronic dopamine receptor stimulation modulates AMPA receptor trafficking in nucleus accumbens neurons cocultured with prefrontal cortex neurons. J Neurosci 28:4216-4230. CrossRef Medline
53. Thomas MJ, Beurrier C, Bonci A, Malenka RC (2001) Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat Neurosci 4:1217-1223. CrossRef Medline
54. Ungless MA, Whistler JL, Malenka RC, Bonci A (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583-587. CrossRef Medline
55. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097. CrossRef Medline