Changes in mu-opioid receptor expression and function in the mesolimbic system after long-term access to a palatable diet

Pharmacology and Therapeutics

Volumn 154, Issue , 2015, Pages 110-119

  Pitman, Kimberley A ^a,b   Borgland, Stephanie L ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

High fat diet; Mu opioid receptor; Nucleus accumbens; Obesity; Ventral tegmental area

Indexed keywords

DOPAMINE; MESSENGER RNA; MU OPIATE RECEPTOR;

FEEDING BEHAVIOR; LIMBIC SYSTEM; LIPID DIET; MATERNAL NUTRITION; NONHUMAN; PALATABILITY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; ANIMAL; BIOSYNTHESIS; BRAIN; DIET; FEMALE; METABOLISM; MOTIVATION; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; BRAIN; DIET; DIET, HIGH-FAT; FEEDING BEHAVIOR; FEMALE; MOTIVATION; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RECEPTORS, OPIOID, MU; RNA, MESSENGER;

EID: 84941422341     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.07.005     Document Type: Review

References (134)

1. J. Alsiö, P.K. Olszewski, A.H. Norbäck, Z.E.A. Gunnarsson, A.S. Levine, C. Pickering, and et al. Dopamine D1 receptor gene expression decreases in the nucleus accumbens upon long-term exposure to palatable food and differs depending on diet-induced obesity phenotype in rats Neuroscience 171 2010 779 787
2. F. Ambroggi, A. Ghazizadeh, S.M. Nicola, and H.L. Fields Roles of nucleus accumbens core and shell in incentive-cue responding and behavioral inhibition J Neurosci 31 2011 6820 6830
3. A.M. Basso, and A.E. Kelley Feeding induced by GABA(A) receptor stimulation within the nucleus accumbens shell: regional mapping and characterization of macronutrient and taste preference Behav Neurosci 113 1999 324 336
4. S.A. Bayol, S.J. Farrington, and N.C. Stickland A maternal 'junk food' diet in pregnancy and lactation promotes an exacerbated taste for 'junk food' and a greater propensity for obesity in rat offspring Br J Nutr 98 2007 843 851
5. T.R. Beckman, Q. Shi, A.S. Levine, and C.J. Billington Amygdalar opioids modulate hypothalamic melanocortin-induced anorexia Physiol Behav 96 2009 568 573
6. N.T. Bello, J.W. Coughlin, G.W. Redgrave, E.E. Ladenheim, T.H. Moran, and A.S. Guarda Dietary conditions and highly palatable food access alter rat cannabinoid receptor expression and binding density Physiol Behav 105 2012 720 726
7. A. Bergevin, D. Girardot, M.-J. Bourque, and L.E. Trudeau Presynaptic mu-opioid receptors regulate a late step of the secretory process in rat ventral tegmental area GABAergic neurons Neuropharmacology 42 2002 1065 1078
8. F. Berrendero, B.L. Kieffer, and R. Maldonado Attenuation of nicotine-induced antinociception, rewarding effects, and dependence in mu-opioid receptor knock-out mice J Neurosci 22 2002 10935 10940
9. K.C. Berridge Food reward: brain substrates of wanting and liking Neurosci Biobehav Rev 20 1996 1 25
10. K.C. Berridge Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns Neurosci Biobehav Rev 24 2000 173 198
11. K.C. Berridge The debate over dopamine's role in reward: the case for incentive salience Psychopharmacology 191 2007 391 431
12. H.R. Berthoud Neural control of appetite: cross-talk between homeostatic and non-homeostatic systems Appetite 43 2004 315 317
13. J.A. Blendy, A. Strasser, C.L. Walters, K.A. Perkins, F. Patterson, R. Berkowitz, and et al. Reduced nicotine reward in obesity: cross-comparison in human and mouse Psychopharmacology 180 2005 306 315
14. J.M. Bossert, G.C. Poles, K.A. Wihbey, E. Koya, and Y. Shaham 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 2007 12655 12663
15. P. Brawarsky, N.E. Stotland, R.A. Jackson, E. Fuentes-Afflick, G.J. Escobar, N. Rubashkin, and et al. Pre-pregnancy and pregnancy-related factors and the risk of excessive or inadequate gestational weight gain Int J Gynecol Obstet 91 2005 125 131
16. M.A. Brion, A.R. Ness, I. Rogers, P. Emmett, V. Cribb, G. Davey Smith, and et al. Maternal macronutrient and energy intakes in pregnancy and offspring intake at 10 y: exploring parental comparisons and prenatal effects Am J Clin Nutr 91 2010 748 756
17. J.P. Britt, and D.S. McGehee Presynaptic opioid and nicotinic receptor modulation of dopamine overflow in the nucleus accumbens J Neurosci 28 2008 1672 1681
18. J.S. Brog, A. Salyapongse, A.Y. Deutch, and D.S. Zahm The patterns of afferent innervation of the core and shell in the 'accumbens' part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold J Comp Neurol 338 1993 255 278
19. B. Buzas, J. Rosenberger, and B.M. Cox Mu and delta opioid receptor gene expression after chronic treatment with opioid agonist Neuroreport 7 1996 1505 1508
20. A. Caixàs, L. Albert, I. Capel, and M. Rigla Naltrexone sustained-release/bupropion sustained-release for the management of obesity: review of the data to date J Drug Des Devel Ther 8 2014 1419 1427
21. J. Carlin, R. George, and T.M. Reyes Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology PLoS One 8 2013 e63549
22. M.P. Castelli, M. Melis, M. Mameli, P. Fadda, G. Diaz, and G.L. Gessa Chronic morphine and naltrexone fail to modify mu-opioid receptor mRNA levels in the rat brain Mol Brain Res 45 1997 149 153
23. D.C. Castro, and K.C. Berridge Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness 'liking' and 'wanting' J Neurosci 34 2014 4239 4250
24. G. Chandorkar, C. Ampasavate, J. Stobaugh, and K. Audus Peptide transport and metabolism across the placenta Adv Drug Deliv Rev 38 1999 59 67
25. G.Q. Chang, O. Karatayev, J.R. Barson, S.Y. Chang, and S.F. Leibowitz Increased enkephalin in brain of rats prone to overconsuming a fat-rich diet Physiol Behav 101 2010 360 369
26. N. Chaudhri, L.L. Sahuque, W.W. Schairer, and P.H. Janak Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking Neuropsychopharmacology 35 2010 783 791
27. C. Colantuoni, J. Schwenker, J. McCarthy, P. Rada, B. Ladenheim, J.L. Cadet, and et al. Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain Neuroreport 12 2001 3549 3552
28. M.A. Cornier, K.L. McFadden, E.A. Thomas, J.L. Bechtell, L.S. Eichman, D.H. Bessesen, and et al. Differences in the neuronal response to food in obesity-resistant as compared to obesity-prone individuals Physiol Behav 110-111 2013 122 128
29. M.A. Cornier, A.K. Salzberg, D.C. Endly, D.H. Bessesen, D.C. Rojas, and J.R. Tregellas The effects of overfeeding on the neuronal response to visual food cues in thin and reduced-obese individuals PLoS One 4 2009 e6310
30. M.A. Cornier, M.E. Shott, E.A. Thomas, J.L. Bechtell, D.H. Bessesen, J.R. Tregellas, and et al. The effects of energy balance, obesity-proneness and sex on the neuronal response to sweet taste Behav Brain Res 278C 2014 446 452
31. G. Cossu, C. Ledent, L. Fattore, A. Imperato, G.A. Böhme, M. Parmentier, and et al. Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse Behav Brain Res 118 2001 61 65
32. J.J. Day, M.F. Roitman, R.M. Wightman, and R.M. Carelli Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens Nat Neurosci 10 2007 1020 1028
33. J. Delarue, and C. Magnan Free fatty acids and insulin resistance Curr Opin Clin Nutr Metab Care 10 2007 142 148
34. G. Di Chiara, and A. Imperato Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats J Pharmacol Exp Ther 244 1988 1067 1080
35. D. Dowling, and F.M. McAuliffe The molecular mechanisms of offspring effects from obese pregnancy Obes Facts 6 2013 134 145
36. S.B. Floresco, R.J. McLaughlin, and D.M. Haluk Opposing roles for the nucleus accumbens core and shell in cue-induced reinstatement of food-seeking behavior Neuroscience 154 2008 877 884
37. E.S. Ford, L.M. Maynard, and C. Li Trends in mean waist circumference and abdominal obesity among US adults, 1999-2012 JAMA 312 2014 1151 1153
38. K. Gach, M. Piestrzeniewicz, J. Fichna, B. Stefanska, J. Szemraj, and A. Janecka Opioid-induced regulation of mu-opioid receptor gene expression in the MCF-7 breast cancer cell line Biochem Cell Biol 86 2008 217 226
39. B. Gago, K. Fuxe, L. Agnati, A. Peñafiel, A. De La Calle, and A. Rivera Dopamine D(4) receptor activation decreases the expression of mu-opioid receptors in the rat striatum J Comp Neurol 502 2007 358 366
40. D. Gaillard, P. Passilly-Degrace, and P. Besnard Molecular mechanisms of fat preference and overeating Ann N Y Acad Sci 1141 2008 163 175
41. J.O. Gan, M.E. Walton, and P.E.M. Phillips Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine Nat Neurosci 13 2010 25 27
42. S. Ghozland, H.W.D. Matthes, F. Simonin, D. Filliol, B.L. Kieffer, and R. Maldonado Motivational effects of cannabinoids are mediated by mu-opioid and kappa-opioid receptors J Neurosci 22 2002 1146 1154
43. C.C. Gotay, P.T. Katzmarzyk, I. Janssen, M.Y. Dawson, K. Aminoltejari, and N.L. Bartley Updating the Canadian obesity maps: an epidemic in progress Can J Public Health 104 2013 e64 e68
44. A.A. Grace, and B.S. Bunney The control of firing pattern in nigral dopamine neurons: burst firing J Neurosci 4 1984 2877 2890
45. A.A. Grace, and B.S. Bunney The control of firing pattern in nigral dopamine neurons: single spike firing J Neurosci 4 1984 2866 2876
46. N.M. Grissom, R. Lyde, L. Christ, I.E. Sasson, J. Carlin, A.P. Vitins, and et al. Obesity at conception programs the opioid system in the offspring brain Neuropsychopharmacology 39 2014 801 810
47. H.C. Grossman, M.M. Hadjimarkou, R.M. Silva, S.Q. Giraudo, and R.J. Bodnar Interrelationships between mu opioid and melanocortin receptors in mediating food intake in rats Brain Res 991 2003 240 244
48. J.R. Gugusheff, Z.Y. Ong, and B.S. Muhlhausler A maternal 'junk-food' diet reduces sensitivity to the opioid antagonist naloxone in offspring postweaning FASEB J 27 2013 1275 1284
49. J.R. Gugusheff, Z.Y. Ong, and B.S. Muhlhausler Naloxone treatment alters gene expression in the mesolimbic reward system in 'junk food' exposed offspring in a sex-specific manner but does not affect food preferences in adulthood Physiol Behav 133 2014 14 21
50. B. Gustafson, S. Gogg, S. Hedjazifar, L. Jenndahl, A. Hammarstedt, and U. Smith Inflammation and impaired adipogenesis in hypertrophic obesity in man Am J Physiol Endocrinol Metab 297 2009 E999 E1003
51. M.E. Hamilton, and M.A. Bozarth Feeding elicited by dynorphin (1-13) microinjections into the ventral tegmental area in rats Life Sci 43 1988 941 946
52. M.R. Harb, and O.F.X. Almeida Altered motivation masks appetitive learning potential of obese mice Front Behav Neurosci 8 2014 377
53. C.K. Hwang, C.S. Kim, D.K. Kim, P. Law, L. Wei, and H.H. Loh Up-regulation of the mu-opioid receptor gene is mediated through chromatin remodeling and transcriptional factors in differentiated neuronal cells Mol Pharmacol 78 2010 58 68
54. C.K. Hwang, K.Y. Song, C.S. Kim, H.S. Choi, X.H. Guo, P.Y. Law, and et al. Evidence of endogenous mu opioid receptor regulation by epigenetic control of the promoters Mol Cell Biol 27 2007 4720 4736
55. F. Jenck, R. Quirion, and R.A. Wise Opioid receptor subtypes associated with ventral tegmental facilitation and periaqueductal gray inhibition of feeding Brain Res 423 1987 39 44
56. P.M. Johnson, and P.J. Kenny Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats Nat Neurosci 13 2010 635 641
57. S.W. Johnson, and R.A. North Opioids excite dopamine neurons by hyperpolarization of local interneurons J Neurosci 12 1992 483 488
58. Y. Katsuura, and S.A. Taha Mu opioid receptor antagonism in the nucleus accumbens shell blocks consumption of a preferred sucrose solution in an anticipatory contrast paradigm Neuroscience 261 2014 144 152
59. A.E. Kelley, E.P. Bless, and C.J. Swanson Investigation of the effects of opiate antagonists infused into the nucleus accumbens on feeding and sucrose drinking in rats J Pharmacol Exp Ther 278 1996 1499 1507
60. A.E. Kelley, and C.J. Swanson Feeding induced by blockade of AMPA and kainate receptors within the ventral striatum: a microinfusion mapping study Behav Brain Res 89 1997 107 113
61. E.W. Kraegen, G.J. Cooney, J. Ye, and A.L. Thompson Triglycerides, fatty acids and insulin resistance - hyperinsulinemia Exp Clin Endocrinol Diabetes 109 2001 S516 S526
62. E.F. Langsdorf, and S.L. Chang Methamphetamine-mediated modulation of MOR expression in the SH-SY5Y neuroblastoma cell line Synapse 65 2011 858 865
63. J. Le Merrer, J.A.J. Becker, K. Befort, and B.L. Kieffer Reward processing by the opioid system in the brain Physiol Rev 89 2009 1379 1412
64. M. Le Naour, E. Akgün, A. Yekkirala, M.M. Lunzer, M.D. Powers, A.E. Kalyuzhny, and et al. Bivalent ligands that target μ opioid (MOP) and cannabinoid1 (CB 1) receptors are potent analgesics devoid of tolerance J Med Chem 56 2013 5505 5513
65. P.W. Lee, and Y.-M. Lee Transcriptional regulation of mu opioid receptor gene by cAMP pathway Mol Pharmacol 64 2003 1410 1418
66. N.R. Lenard, H. Zheng, and H.R. Berthoud Chronic suppression of μ-opioid receptor signaling in the nucleus accumbens attenuates development of diet-induced obesity in rats Int. J. Obes. 34 2010 1001 1010
67. P. Lin, and W.E. Pratt Inactivation of the nucleus accumbens core or medial shell attenuates reinstatement of sugar-seeking behavior following sugar priming or exposure to food-associated cues PLoS One 9 2014 e99301
68. N.M. Long, D.C. Rule, M.J. Zhu, P.W. Nathanielsz, and S.P. Ford Maternal obesity upregulates fatty acid and glucose transporters and increases expression of enzymes mediating fatty acid biosynthesis in fetal adipose tissue depots J Anim Sci 90 2012 2201 2210
69. Y.Y. Ma, C. Cepeda, P. Chatta, L. Franklin, C.J. Evans, and M.S. Levine Regional and cell-type-specific effects of DAMGO on striatal D1 and D2 dopamine receptor-expressing medium-sized spiny neurons ASN Neuro 4 2012 59 70
70. A.F. MacDonald, C.J. Billington, and A.S. Levine Alterations in food intake by opioid and dopamine signaling pathways between the ventral tegmental area and the shell of the nucleus accumbens Brain Res 1018 2004 78 85
71. C.S. Maldonado-Irizarry, and A.E. Kelley Differential behavioral effects following microinjection of an NMDA antagonist into nucleus accumbens subregions Psychopharmacology (Berl) 116 1994 65 72
72. A. Mansour, M.T. Hoversten, L.P. Taylor, S.J. Watson, and H. Akil The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores Brain Res 700 1995 89 98
73. C.E. Markowitz, K.M. Berkowitz, S.B. Jaffe, and S.L. Wardlaw Effect of opioid receptor antagonism on proopiomelanocortin peptide levels and gene expression in the hypothalamus Mol Cell Neurosci 3 1992 184 190
74. M. Martin, C. Ledent, M. Parmentier, R. Maldonado, and O. Valverde Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice Eur J Neurosci 12 2000 4038 4046
75. S.I. Martire, J. Maniam, T. South, N. Holmes, R.F. Westbrook, and M.J. Morris Extended exposure to a palatable cafeteria diet alters gene expression in brain regions implicated in reward, and withdrawal from this diet alters gene expression in brain regions associated with stress Behav Brain Res 265C 2014 132 141
76. M.S. Mascia, M.C. Obinu, C. Ledent, M. Parmentier, G.A. Böhme, A. Imperato, and et al. Lack of morphine-induced dopamine release in the nucleus accumbens of cannabinoid CB(1) receptor knockout mice Eur J Pharmacol 383 1999 R1 R2
77. A. Matsui, and J.T. Williams Opioid-sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons J Neurosci 31 2011 17729 17735
78. G.E. Meredith, B.A. Baldo, M.E. Andrezjewski, and A.E. Kelley The structural basis for mapping behavior onto the ventral striatum and its subdivisions Brain Struct Funct 213 2008 17 27
79. R.F. Mucha, and S.D. Iversen Increased food intake after opioid microinjections into nucleus accumbens and ventral tegmental area of rat Brain Res 397 1986 214 224
80. P.J. Nathan, and E.T. Bullmore From taste hedonics to motivational drive: central μ-opioid receptors and binge-eating behaviour Int J Neuropsychopharmacol 12 2009 995 1008
81. R. Nogueiras, A. Romero-Picó, M.J. Vazquez, M.G. Novelle, M. López, and C. Diéguez The opioid system and food intake: homeostatic and hedonic mechanisms Obes Facts 5 2012 196 207
82. E. Oken, E.M. Taveras, K.P. Kleinman, J.W. Rich-Edwards, and M.W. Gillman Gestational weight gain and child adiposity at age 3 years Am J Obstet Gynecol 196 322 2007 e1 e8
83. E.B. Oleson, R.N. Gentry, V.C. Chioma, and J.F. Cheer Subsecond dopamine release in the nucleus accumbens predicts conditioned punishment and its successful avoidance J Neurosci 32 2012 14804 14808
84. P.K. Olszewski, M.M. Wirth, M.K. Grace, A.S. Levine, and S.Q. Giraudo Evidence of interactions between melanocortin and opioid systems in regulation of feeding Neuroreport 12 2001 1727 1730
85. Z.Y. Ong, and B.S. Muhlhausler Maternal 'junk-food' feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring FASEB J. 25 2011 2167 2179
86. Z.Y. Ong, A.F. Wanasuria, M.Z.P. Lin, J. Hiscock, and B.S. Muhlhausler Chronic intake of a cafeteria diet and subsequent abstinence. Sex-specific effects on gene expression in the mesolimbic reward system Appetite 65 2013 189 199
87. L. Pan, H.M. Blanck, B. Sherry, K. Dalenius, and L.M. Grummer-Strawn Trends in the prevalence of extreme obesity among US preschool-aged children living in low-income families, 1998-2010 JAMA 308 2012 2563 2565
88. F. Papaleo, B.L. Kieffer, A. Tabarin, and A. Contarino Decreased motivation to eat in mu-opioid receptor-deficient mice Eur J Neurosci 25 2007 3398 3405
89. J.A. Parkinson, P.J. Willoughby, T.W. Robbins, and B.J. Everitt Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems Behav Neurosci 114 2000 42 63
90. S. Peciña Opioid reward 'liking' and 'wanting' in the nucleus accumbens Physiol Behav 94 2008 675 680
91. S. Peciña, and K.C. Berridge Opioid site in nucleus accumbens shell mediates eating and hedonic 'liking' for food: map based on microinjection Fos plumes Brain Res 863 2000 71 86
92. S. Peciña, and K.C. Berridge Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25 2005 11777 11786
93. S. Peciña, K.C. Berridge, and L.A. Parker Pimozide does not shift palatability: separation of anhedonia from sensorimotor suppression by taste reactivity Pharmacol Biochem Behav 58 1997 801 811
94. S. Peciña, B. Cagniard, K.C. Berridge, J.W. Aldridge, and X. Zhuang Hyperdopaminergic mutant mice have higher 'wanting' but not 'liking' for sweet rewards J Neurosci 23 2003 9395 9402
95. S. Peciña, and K.S. Smith Hedonic and motivational roles of opioids in food reward: implications for overeating disorders Pharmacol Biochem Behav 97 2010 34 46
96. A. Peeters, E. Gearon, K. Backholer, and B. Carstensen Trends in the skewness of the body mass index distribution among urban Australian adults, 1980 to 2007 Ann Epidemiol 25 2015 26 33
97. P.E.M. Phillips, G.D. Stuber, M.L.A.V. Heien, R.M. Wightman, and R.M. Carelli Subsecond dopamine release promotes cocaine seeking Nature 422 2003 614 618
98. L. Pulvirenti, R. Berrier, M. Kreifeldt, and G.F. Koob Modulation of locomotor activity by NMDA receptors in the nucleus accumbens core and shell regions of the rat Brain Res 664 1994 231 236
99. P.J. Randle, P.B. Garland, C.N. Hales, and E.A. Newsholme The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus Lancet 1 1963 785 789
100. A.S. Reece Hypothalamic opioid-Melanocortin appetitive balance and addictive craving Med Hypotheses 76 2011 132 137
101. J.J. Rodriguez, K. Mackie, and V.M. Pickel Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat Caudate putamen nucleus J Neurosci 21 2001 823 833
102. S. Sharma, and S. Fulton Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry Int J Obes 37 2013 382 389
103. B. Sherry, Z. Mei, K.S. Scanlon, A.H. Mokdad, and L.M. Grummer-Strawn Trends in state-specific prevalence of overweight and underweight in 2- through 4-year-old children from low-income families from 1989 through 2000 Arch Pediatr Adolesc Med 158 2004 1116 1124
104. Y. Shoji, J. Delfs, and J.T. Williams Presynaptic inhibition of GABA(B)-mediated synaptic potentials in the ventral tegmental area during morphine withdrawal J Neurosci 19 1999 2347 2355
105. S.L. Smith, J.A. Harrold, and G. Williams Diet-induced obesity increases mu opioid receptor binding in specific regions of the rat brain Brain Res 953 2002 215 222
106. K.L. Smith, R.R. Rao, C. Velázquez-Sánchez, M. Valenza, C. Giuliano, B.J. Everitt, and et al. The uncompetitive N-methyl-D-aspartate antagonist memantine reduces binge-like eating, food-seeking behavior, and compulsive eating: role of the nucleus accumbens shell Neuropsychopharmacology 40 2015 1163 1171
107. T. South, and X.F. Huang High-fat diet exposure increases dopamine D2 receptor and decreases dopamine transporter receptor binding density in the nucleus accumbens and caudate putamen of mice Neurochem Res 33 2008 598 605
108. R. Spanagel, A. Herz, and T.S. Shippenberg The effects of opioid peptides on dopamine release in the nucleus accumbens: an in vivo microdialysis study J Neurochem 55 1990 1734 1740
109. R. Spanagel, A. Herz, and T.S. Shippenberg Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway Proc Natl Acad Sci 89 1992 2046 2050
110. R. Spangler, K.M. Wittkowski, N.L. Goddard, N.M. Avena, B.G. Hoebel, and S.F. Leibowitz Opiate-like effects of sugar on gene expression in reward areas of the rat brain Brain Res Mol Brain Res 124 2004 134 142
111. J.A. Sugam, J.J. Day, R.M. Wightman, and R.M. Carelli Phasic nucleus accumbens dopamine encodes risk-based decision-making behavior Biol Psychiatry 71 2012 199 205
112. A. Tabarin, Y. Diz-Chaves, Y.D. Chaves, M. del Carmona, C. Catargi, B. Zorrilla, and et al. Resistance to diet-induced obesity in mu-opioid receptor-deficient mice: evidence for a 'thrifty gene' Diabetes 54 2005 3510 3516
113. S.A. Taha Preference or fat? Revisiting opioid effects on food intake Physiol Behav 100 2010 429 437
114. S.A. Taha, Y. Katsuura, D. Noorvash, A. Seroussi, and H.L. Fields Convergent, not serial, striatal and pallidal circuits regulate opioid-induced food intake Neuroscience 161 2009 718 733
115. G. Tanda, and G. Di Chiara A dopamine-mu1 opioid link in the rat ventral tegmentum shared by palatable food (Fonzies) and non-psychostimulant drugs of abuse Eur J Neurosci 10 1998 1179 1187
116. S.L. Teegarden, A.N. Scott, and T.L. Bale Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling Neuroscience 162 2009 924 932
117. J.R. Tregellas, K.P. Wylie, D.C. Rojas, J. Tanabe, J. Martin, E. Kronberg, and et al. Altered default network activity in obesity Obesity 19 2011 2316 2321
118. D. Treit, and K.C. Berridge A comparison of benzodiazepine, serotonin, and dopamine agents in the taste-reactivity paradigm Pharmacol Biochem Behav 37 1990 451 456
119. R.J. Van Lieshout, V.H. Taylor, and M.H. Boyle Pre-pregnancy and pregnancy obesity and neurodevelopmental outcomes in offspring: a systematic review Obes Rev 12 2011 e548 e559
120. J.M. Van Ree, R.J. Niesink, L. Van Wolfswinkel, N.F. Ramsey, M.M. Kornet, W.R. Van Furth, and et al. Endogenous opioids and reward Eur J Pharmacol 405 2000 89 101
121. Z. Vucetic, J.L. Carlin, K. Totoki, and T.M. Reyes Epigenetic dysregulation of the dopamine system in diet-induced obesity J Neurochem 120 2012 891 898
122. Z. Vucetic, J. Kimmel, and T.M. Reyes Chronic high-fat diet drives postnatal epigenetic regulation of μ-opioid receptor in the brain Neuropsychopharmacology 36 2011 1199 1206
123. Z. Vucetic, J. Kimmel, K. Totoki, E. Hollenbeck, and T.M. Reyes Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes Endocrinology 151 2010 4756 4764
124. J.M. Walsh, R. Mahony, J. Byrne, M. Foley, and F.M. McAuliffe The association of maternal and fetal glucose homeostasis with fetal adiposity and birthweight Eur J Obstet Gynecol Reprod Biol 159 2011 338 341
125. L.N. Wei, and H.H. Loh Transcriptional and epigenetic regulation of opioid receptor genes: present and future Annu Rev Pharmacol Toxicol 51 2011 75 97
126. M.J. Will, W.E. Pratt, and A.E. Kelley Pharmacological characterization of high-fat feeding induced by opioid stimulation of the ventral striatum Physiol Behav 89 2006 226 234
127. C.I. Wright, A.V. Beijer, and H.J. Groenewegen Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized J Neurosci 16 1996 1877 1893
128. C.L. Wyvell, and K.C. Berridge Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward 'wanting' without enhanced 'liking' or response reinforcement J Neurosci 20 2000 8122 8130
129. Y. Yogev, and P.M. Catalano Pregnancy and obesity Obstet. Gynecol. Clin. North Am. 36 2009 285 300
130. M. Yoshikawa, H. Nakayama, S. Ueno, M. Hirano, H. Hatanaka, and H. Furuya Chronic fentanyl treatments induce the up-regulation of mu opioid receptor mRNA in rat pheochromocytoma cells Brain Res 859 2000 217 223
131. M. Zhang, B.A. Gosnell, and A.E. Kelley Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens J Pharmacol Exp Ther 285 1998 908 914
132. M.J. Zhu, Y. Ma, N.M. Long, M. Du, and S.P. Ford Maternal obesity markedly increases placental fatty acid transporter expression and fetal blood triglycerides at midgestation in the ewe Am. J. Physiol. Regul. Integr. Comp. Physiol. 299 2010 R1224 R1231
133. H. Ziauddeen, S.R. Chamberlain, P.J. Nathan, A. Koch, K. Maltby, M. Bush, and et al. Effects of the mu-opioid receptor antagonist GSK1521498 on hedonic and consummatory eating behaviour: a proof of mechanism study in binge-eating obese subjects Mol Psychiatry 18 2013 1287 1293
134. A.R. Zuberi, L. Townsend, L. Patterson, H. Zheng, and H.-R. Berthoud Increased adiposity on normal diet, but decreased susceptibility to diet-induced obesity in mu-opioid receptor-deficient mice Eur J Pharmacol 585 2008 14 23