Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry

International Journal of Obesity

Volumn 37, Issue 3, 2013, Pages 382-389

  Sharma, S ^a   Fulton, S ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

anxiety; BDNF; CREB; depression; high fat food; striatum

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 1A RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE RECEPTOR; PHOSPHOPROTEIN DARPP 32; TRANSCRIPTION FACTOR FOSB; UNCLASSIFIED DRUG;

ACUTE STRESS; ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATIONAL STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DIET INDUCED OBESITY; IMMOBILIZATION; IMMOBILIZATION STRESS; IMMUNOBLOTTING; LIMBIC CORTEX; LIPID DIET; LOCOMOTION; MALE; MAZE TEST; MESENCEPHALON; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; OBESITY; PATHOGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VENTRAL TEGMENTUM;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CORTICOSTERONE; DEPRESSION; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NEURONAL PLASTICITY; OBESITY; PROMOTER REGIONS, GENETIC; RECEPTORS, DOPAMINE D2; REWARD; STRESS, PSYCHOLOGICAL; SWIMMING;

MUS;

EID: 84875219963     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2012.48     Document Type: Article

References (62)

1. Dong C, Sanchez LE, Price RA. Relationship of obesity to depression: a family-based study. Int J Obes Relat Metab Disord 2004; 28: 790-795.
2. Roberts RE, Deleger S, Strawbridge WJ, Kaplan GA. Prospective association between obesity and depression: evidence from the Alameda County Study. Int J Obes Relat Metab Disord 2003; 27: 514-521.
3. Simon GE, Von Korff M, Saunders K, Miglioretti DL, Crane PK, van Belle G et al. Association between obesity and psychiatric disorders in the US adult population. Arch Gen Psychiatry 2006; 63: 824-830.
4. Davis JF, Tracy AL, Schurdak JD, Tschop MH, Lipton JW, Clegg DJ et al. Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 2008; 122: 1257-1263.
5. Geiger BM, Haburcak M, Avena NM, Moyer MC, Hoebel BG, Pothos EN. Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 2009; 159: 1193-1199.
6. Teegarden SL, Nestler EJ, Bale TL. Delta FosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol Psychiatry 2008; 64: 941-950.
7. Fulton S. Appetite and reward. Front Neuroendocrinol 2010; 31: 85-103.
8. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W et al. Brain dopamine and obesity. Lancet 2001; 357: 354-357.
9. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J et al. Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. Neuroimage 2008; 42: 1537-1543
10. Fulton S, Pissios P, Manchon RP, Stiles L, Frank L, Pothos EN et al. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 2006; 51: 811-822
11. Geiger BM, Behr GG, Frank LE, Caldera-Siu AD, Beinfeld MC, Kokkotou EG et al. Evidence for defective mesolimbic dopamine exocytosis in obesity-prone rats. Faseb J 2008; 22: 2740-2746
12. Nestler EJ, Carlezon Jr WA. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 2006; 59: 1151-1159
13. Hyman SE, Malenka RC, Nestler EJ. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006; 29: 565-598
14. Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, Kumar A et al. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 2007; 10: 93-99
15. Lucki I. The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 1997; 8: 523-532
16. Porsolt RD, Bertin A, Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch Int de Pharmacodynamie et de Therapie 1977; 229: 327-336
17. Dong C, Sanchez LE, Price RA. Relationship of obesity to depression: a familybased study. Int J Obes Relat Metab Disord 2004; 28: 790-795
18. Zhao G, Ford ES, Dhingra S, Li C, Strine TW, Mokdad AH. Depression and anxiety among US adults: associations with body mass index. Int J Obes (Lond) 2009; 33: 257-266
19. Yamada N, Katsuura G, Ochi Y, Ebihara K, Kusakabe T, Hosoda K et al. Impaired CNS leptin action is implicated in depression associated with obesity. Endocrinology 2011; 152: 2634-2643
20. Maniam J, Morris MJ. Palatable cafeteria diet ameliorates anxiety and depressionlike symptoms following an adverse early environment. Psychoneuroendocrinology 2010; 35: 717-728
21. McClean PL, Irwin N, Cassidy RS, Holst JJ, Gault VA, Flatt PR. GIP receptor antagonism reverses obesity, insulin resistance, and associated metabolic disturbances induced in mice by prolonged consumption of high-fat diet. Am J Physiol Endocrinol Metab 2007; 293: 1746-1755
22. Tannenbaum BM, Brindley DN, Tannenbaum GS, Dallman MF, McArthur MD, Meaney MJ. High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat. Am J Physiol 1997; 273: E1168-E1E77
23. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ et al. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 2002; 99: 11435-11440
24. Barrot M, Wallace DL, Bolanos CA, Graham DL, Perrotti LI, Neve RL et al. Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci USA 2005; 102: 8357-8362
25. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM. Neurobiology of depression. Neuron 2002; 34: 13-25
26. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ et al. Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 2005; 25: 5553-5562
27. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, Iniguez SD et al. CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 2009; 12: 200-209
28. Carlezon Jr WA, Duman RS, Nestler EJ. The many faces of CREB. Trends Neurosci 2005; 28: 436-445
29. McPherson CS, Lawrence AJ. The nuclear transcription factor CREB: involvement in addiction, deletion models and looking forward. Curr Neuropharmacol 2007; 5: 202-212
30. Nestler EJ. Molecular neurobiology of addiction. Am J Addict 2001; 10: 201-217
31. Nestler EJ. Common molecular and cellular substrates of addiction and memory. Neurobiol Learn Mem 2002; 78: 637-647
32. Nestler EJ. Molecular mechanisms of drug addiction. Neuropharmacology 2004; 47 (Suppl 1): 24-32
33. Pandey SC, Chartoff EH, Carlezon Jr WA, Zou J, Zhang H, Kreibich AS. et al. CREB gene transcription factors: role in molecular mechanisms of alcohol and drug addiction. Alcohol Clin Exp Res 2005; 29: 176-184
34. Briand LA, Blendy JA. Molecular and genetic substrates linking stress and addiction. Brain Res 2010; 1314: 219-234
35. Carlezon Jr WA, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N et al. Regulation of cocaine reward by CREB. Science 1998; 282: 2272-2275
36. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA. Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 2001; 21: 7397-7403
37. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 2007; 85: 525-535
38. Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998; 20: 709-726
39. Conti AC, Cryan JF, Dalvi A, Lucki I, Blendy JA. cAMP response element-binding protein is essential for the upregulation of brain-derived neurotrophic factor transcription, but not the behavioral or endocrine responses to antidepressant drugs. J Neurosci 2002; 22: 3262-3268
40. Gooney M, Messaoudi E, Maher FO, Bramham CR, Lynch MA. BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol Aging 2004; 25: 1323-1331
41. Pandey SC, Zhang H, Roy A, Misra K. Central and medial amygdaloid brain-derived neurotrophic factor signaling plays a critical role in alcohol-drinking and anxietylike behaviors. J Neurosci 2006; 26: 8320-8331
42. Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, Kumar A et al. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 2007; 10: 93-99
43. Gray J, Yeo GS, Cox JJ, Morton J, Adlam AL, Keogh JM. et al. Hyperphagia, severe obesity, impaired cognitive function, and hyperactivity associated with functional loss of one copy of the brain-derived neurotrophic factor (BDNF) gene. Diabetes 2006; 55: 3366-3371
44. Han JC, Liu QR, Jones M, Levinn RL, Menzie CM, Jefferson-George KS et al. Brainderived neurotrophic factor and obesity in the WAGR syndrome. N Engl J Med 2008; 359: 918-927
45. Kernie SG, Liebl DJ, Parada LF. BDNF regulates eating behavior and locomotor activity in mice. EMBO J 2000; 19: 1290-1300
46. Lyons WE, Mamounas LA, Ricaurte GA, Coppola V, Reid SW, Bora SH et al. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci USA 1999; 96: 15239-15244
47. Cordeira JW, Frank L, Sena-Esteves M, Pothos EN, Rios M. Brain-derived neurotrophic factor regulates hedonic feeding by acting on the mesolimbic dopamine system. J Neurosci 2010; 30: 2533-2541
48. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006; 311: 864-868
49. Berton O, Nestler EJ. New approaches to antidepressant drug discovery: beyond monoamines. Nat Rev Neurosci 2006; 7: 137-151
50. Nestler EJ, Kelz MB, Chen J. [Delta]FosB: a molecular mediator of long-term neural and behavioral plasticity. Brain Res 1999; 835: 10-17
51. McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ. DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res Mol Brain Res 2004; 132: 146-154
52. Vialou V, Robison AJ, Laplant QC, Covington III HE, Dietz DM, Ohnishi YN et al. DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 2010; 13: 745-752
53. Teegarden SL, Nestler EJ, Bale TL. Delta]FosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol Psychiatry 2008; 64: 941-950
54. Bibb JA, Chen J, Taylor JR, Svenningsson P, Nishi A, Snyder GL et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 2001; 410: 376-380
55. Bibb JA, Snyder GL, Nishi A, Yan Z, Meijer L, Fienberg AA et al. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 1999; 402: 669-671
56. Rauggi R, Scheggi S, Cassanelli A, De Montis MG, Tagliamonte A, Gambarana C. The mesolimbic dopaminergic response to novel palatable food consumption increases dopamine-D1 receptor-mediated signalling with complex modifications of the DARPP-32 phosphorylation pattern. J Neurochem 2005; 92: 867-877
57. Benavides DR, Bibb JA. Role of Cdk5 in drug abuse and plasticity. Ann NY Acad Sci. [Review] 2004; 1025: 335-344
58. Alsio J, Olszewski PK, Norback AH, Gunnarsson ZE, Levine AS, Pickering C 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 2010; 171: 779-787
59. Haroon E, Raison CL, Miller AH. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 2012; 37: 137-162
60. Maniam J, Morris MJ. Voluntary exercise and palatable high-fat diet both improve behavioural profile and stress responses in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 2010; 35: 1553-1564
61. Maniam J, Morris MJ. Palatable cafeteria diet ameliorates anxiety and depressionlike symptoms following an adverse early environment. Psychoneuroendocrinology 2010; 35: 717-728
62. Finger BC, Dinan TG, Cryan JF. High-fat diet selectively protects against the effects of chronic social stress in the mouse. Neuroscience 2011; 192: 351-360.