Nutrition
Volume 26, Issue 4 , Pages 411-422 , April 2010

Effect of high-fat feeding on expression of genes controlling availability of dopamine in mouse hypothalamus

  • Alex K. Lee, B.Sc.

      Affiliations

    • Nutritional Sciences Division, King's College London, London, United Kingdom
  • ,
  • Marjan Mojtahed-Jaberi, M.Sc.

      Affiliations

    • Nutritional Sciences Division, King's College London, London, United Kingdom
  • ,
  • Theodosios Kyriakou, Ph.D.

      Affiliations

    • Nutritional Sciences Division, King's College London, London, United Kingdom
    • Present address: Procardis Group, The Wellcome Trust Centre for Human Genetics, Oxford, United Kingdom.
  • ,
  • Estibaliz Aldecoa-Otalora Astarloa, Ph.D.

      Affiliations

    • Genomics Centre, King's College London, London, United Kingdom
  • ,
  • Matthew Arno, Ph.D.

      Affiliations

    • Genomics Centre, King's College London, London, United Kingdom
  • ,
  • Nichola J. Marshall, B.Sc.

      Affiliations

    • Cardiovascular Division, King's College London, London, United Kingdom
  • ,
  • Susan D. Brain, Ph.D.

      Affiliations

    • Cardiovascular Division, King's College London, London, United Kingdom
  • ,
  • Sandra D. O'Dell, D.Phil.

      Affiliations

    • Nutritional Sciences Division, King's College London, London, United Kingdom
    • Corresponding Author InformationCorresponding author. Tel.: +44-20-7848-3177; fax: +44-20-7848-4195.

Received 24 October 2008 ,Accepted 8 May 2009.

References 

  1. Lam TK, Schwartz GJ, Rossetti L. Hypothalamic sensing of fatty acids. Nat Neurosci. 2005;8:579–584
  2. Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature. 2000;404:661–671
  3. Sun G. Application of DNA microarrays in the study of human obesity and type 2 diabetes. OMICS. 2007;11:25–40
  4. Mobbs CV, Yen K, Mastaitis J, Nguyen H, Watson E, Wurmbach E, et al. Mining microarrays for metabolic meaning: nutritional regulation of hypothalamic gene expression. Neurochem Res. 2004;29:1093–1103
  5. Zhao X, Lein ES, He A, Smith SC, Aston C, Gage FH. Transcriptional profiling reveals strict boundaries between hippocampal subregions. J Comp Neurol. 2001;441:187–196
  6. Bonaventure P, Guo H, Tian B, Liu X, Bittner A, Roland B, et al. Nuclei and subnuclei gene expression profiling in mammalian brain. Brain Res. 2002;943:38–47
  7. Middleton FA, Ramos EJ, Xu Y, Diab H, Zhao X, Das UN, et al. Application of genomic technologies: DNA microarrays and metabolic profiling of obesity in the hypothalamus and in subcutaneous fat. Nutrition. 2004;20:14–25
  8. De Souza CT, Araujo EP, Bordin S, Ashimine R, Zollner RL, Boschero AC, et al. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology. 2005;146:4192–4199
  9. Draghici S, Khatri P, Martins RP, Ostermeier GC, Krawetz SA. Global functional profiling of gene expression. Genomics. 2003;81:98–104
  10. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–29
  11. Meguid MM, Fetissov SO, Blaha V, Yang ZJ. Dopamine and serotonin VMN release is related to feeding status in obese and lean Zucker rats. Neuroreport. 2000;11:2069–2072
  12. Orosco M, Rouch C, Meile MJ, Nicolaidis S. Spontaneous feeding-related monoamine changes in rostromedial hypothalamus of the obese Zucker rat: a microdialysis study. Physiol Behav. 1995;57:1103–1106
  13. Martel P, Fantino M. Mesolimbic dopaminergic system activity as a function of food reward: a microdialysis study. Pharmacol Biochem Behav. 1996;53:221–226
  14. Kelley AE, Baldo BA, Pratt WE, Will MJ. Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav. 2005;86:773–795
  15. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reactions assays. J Mol Endocrinol. 2000;25:169–193
  16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408
  17. Kalra SP, Dube MG, Pu S, Xu B, Horvarth TL, Kalra PS. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr Rev. 1999;20:68–100
  18. Li JY, Lescure PA, Misek DE, Lai YM, Chai BX, Kuick R, et al. Food deprivation- induced expression of minoxidil sulfotransferase in the hypothalamus uncovered by microarray analysis. J Biol Chem. 2002;277:9069–9076
  19. Li JY, Kuick R, Thompson RC, Misek DE, Lai YM, Liu YQ, et al. Arcuate nucleus transcriptome profiling identifies ankyrin repeat and suppressor of cytokine signalling box-containing protein 4 as a gene regulated by fasting in central nervous system feeding circuits. J Neuroendocrinol. 2005;17:394–404
  20. Heijboer AC, Voshol PJ, Donga E, van Eden CG, Havekes LM, Romijn JA, et al. High fat diet induced hepatic insulin resistance is not related to changes in hypothalamic mRNA expression of NPY, AgRP, POMC and CART in mice. Peptides. 2005;26:2554–2558
  21. Bullen JW, Ziotopoulou M, Ungsunan L, Misra J, Alevizos I, Kokkotou E, et al. Short-term resistance to diet-induced obesity in A/J mice is not associated with regulation of hypothalamic neuropeptides. Am J Physiol Endocrinol Metab. 2004;287:E662–E670
  22. Frederich RC, Lollmann B, Hamann A, Napolitano-Rosen A, Kahn BB, Lowell BB, et al. Expression of ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. J Clin Invest. 1995;96:1658–1663
  23. Cowley MA, Smart JL, Rubinstein M, Cerdan MG, Diano S, Horvath TL, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 2001;411:480–484
  24. Huang XF, Han M, South T, Storlien L. Altered levels of POMC, AgRP and MC4-R mRNA expression in the hypothalamus and other parts of the limbic system of mice prone or resistant to chronic high-energy diet-induced obesity. Brain Res. 2003;992:9–19
  25. Tian DR, Li XD, Shi YS, Wan Y, Wang XM, Chang JK, et al. Changes of hypothalamic alpha-MSH and CART peptide expression in diet-induced obese rats. Peptides. 2004;25:2147–2153
  26. Yu Y, South T, Wang Q, Huang XF. Differential expression of hypothalamic CART mRNA in response to body weight change following different dietary interventions. Neurochem Int. 2008;52:1422–1430
  27. Guan XM, Yu H, Trumbauer M, Frazier E, Van der Ploeg LH, Chen H. Induction of neuropeptide Y expression in dorsomedial hypothalamus of diet-induced obese mice. Neuroreport. 1998;9:3415–3419
  28. Bergen HT, Mizuno T, Taylor J, Mobbs CV. Resistance to diet-induced obesity is associated with increased proopiomelanocortin mRNA and decreased neuropeptide Y mRNA in the hypothalamus. Brain Res. 1999;851:198–203
  29. Ziotopoulou M, Mantzoros CS, Hileman SM, Flier JS. Differential expression of hypothalamic neuropeptides in the early phase of diet-induced obesity in mice. Am J Physiol Endocrinol Metab. 2000;279:E838–E845
  30. Levin BE, Dunn-Meynell AA. Dysregulation of arcuate nucleus preproneuropeptide Y mRNA in diet-induced obese rats. Am J Physiol Regul Integr Comp Physiol. 1997;272:R1365–R1370
  31. Takahashi N, Patel HR, Qi Y, Dushay J, Ahima RS. Divergent effects of leptin in mice susceptible or resistant to obesity. Horm Metab Res. 2002;34:691–697
  32. Huang XF, Han M, Storlien LH. The level of NPY receptor mRNA expression in diet-induced obese and resistant mice. Brain Res Mol Brain Res. 2003;115:21–28
  33. Huang XF, Xin X, McLennan P, Storlien L. Role of fat amount and type in ameliorating diet-induced obesity: insights at the level of hypothalamic arcuate nucleus leptin receptor, neuropeptide Y and pro-opiomelanocortin mRNA expression. Diabetes Obes Metab. 2004;6:35–44
  34. Park ES, Yi SJ, Kim JS, Lee HS, Lee IS, Seong JK, et al. Changes in orexin-A and neuropeptide Y expression in the hypothalamus of the fasted and high-fat diet fed rats. J Vet Sci. 2004;5:295–302
  35. Beck B. Neuropeptide Y in normal eating and in genetic and dietary-induced obesity. Phil Trans R Soc Lond B Biol Sci. 2006;361:1159–1185
  36. Wang C, Yang N, Wu S, Liu L, Sun X, Nie S. Difference of NPY and its receptor gene expressions between obesity and obesity-resistant rats in response to high-fat diet. Horm Metab Res. 2007;39:262–267
  37. Wang H, Storlien LH, Huang XF. Effects of dietary fat types on body fatness, leptin, and ARC leptin receptor, NPY, and AgRP mRNA expression. Am J Physiol Endocrinol Metab. 2002;282:E1352–E1359
  38. Patel HR, Qi Y, Hawkins EJ, Hileman SM, Elmquist JK, Imai Y, et al. Neuropeptide Y deficiency attenuates responses to fasting and high-fat diet in obesity-prone mice. Diabetes. 2006;55:3091–3098
  39. Bi S, Chen J, Behles RR, Hyun J, Kopin AS, Moran TH. Differential body weight and feeding responses to high-fat diets in rats and mice lacking cholecystokinin 1 receptors. Am J Physiol Regul Integr Comp Physiol. 2007;293:R55–R63
  40. Staszkiewicz J, Horswell R, Argyropoulos G. Chronic consumption of a low-fat diet leads to increased hypothalamic agouti-related protein and reduced leptin. Nutrition. 2007;23:665–671
  41. Kaushik P, Gorin F, Vali S. Dynamics of tyrosine hydroxylase mediated regulation of dopamine synthesis. J Comput Neurosci. 2007;22:147–160
  42. Zheng G, Dwoskin LP, Crooks PA. Vesicular monoamine transporter 2: role as a novel target for drug development. AAPS J. 2006;8:E682–E692
  43. Perez RG, Waymire JC, Lin E, Liu JJ, Guo F, Zigmond MJ. A role for alpha-synuclein in the regulation of dopamine biosynthesis. J Neurosci. 2002;22:3090–3099
  44. Senior SL, Ninkina N, Deacon R, Bannerman D, Buchman VL, Cragg SJ, et al. Increased striatal dopamine release and hyperdopaminergic-like behaviour in mice lacking both alpha-synuclein and gamma-synuclein. Eur J Neurosci. 2008;27:947–957
  45. Meister B, Elde R. Dopamine transporter mRNA in neurons of the rat hypothalamus. Neuroendocrinology. 1993;58:388–395
  46. Garrett MC, Soares-da-Silva P. Role of type A and B monoamine oxidase on the formation of 3,4-dihydroxyphenylacetic acid (DOPAC) in tissues from the brain of the rat. Neuropharmacology. 1990;29:875–879
  47. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. Dopamine receptors: from structure to function. Physiol Rev. 1998;78:189–225
  48. Baptista T, Araujo de Baptista E, Ying Kin NM, Beaulieu S, Walker D, Joober R, et al. Comparative effects of the antipsychotics sulpiride or risperidone in rats. I: bodyweight, food intake, body composition, hormones and glucose tolerance. Brain Res. 2002;957:144–151
  49. Kuo DY. Co-administration of dopamine D1 and D2 agonists additively decreases daily food intake, body weight and hypothalamic neuropeptide Y level in rats. J Biomed Sci. 2002;9:126–132
  50. Yang ZJ, Meguid MM. LHA dopaminergic activity in obese and lean Zucker rats. Neuroreport. 1995;6:1191–1194
  51. Fetissov SO, Meguid MM, Sato T, Zhang LH. Expression of dopaminergic receptors in the hypothalamus of lean and obese Zucker rats and food intake. Am J Physiol Regul Integr Comp Physiol. 2002;283:R905–R910
  52. Nicola SM. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci. 2000;23:185–215
  53. Martel P, Fantino M. Influence of the amount of food ingested on mesolimbic dopaminergic system activity: a microdialysis study. Pharmacol Biochem Behav. 1996;55:297–302
  54. Comings DE, Blum K. Reward deficiency syndrome: genetic aspects of behavioral disorders. Prog Brain Res. 2000;126:325–341
  55. 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
  56. Chan M-Y, Zhao Y, Heng C-K. Sequential responses to high-fat and high-calorie feeding in an obese mouse model. Obesity. 2008;16:972–978
  57. Krugel U, Schraft T, Kittner H, Kiess W, Illes P. Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin. Eur J Pharmacol. 2003;482:185–187
  58. Fulton S, Woodside B, Shizgal P. Modulation of brain reward circuitry by leptin. Science. 2000;287:125–128
  59. Figlewicz DP, Bennett J, Evans SB, Kaiyala K, Sipols AJ, Benoit SC. Intraventricular insulin and leptin reverse place preference conditioned with high-fat diet in rats. Behav Neurosci. 2004;118:479–487
  60. Blouquit MF, Gripois D, Roffi J. Influence of cold exposure on dopamine content in rat brown adipose tissue. Horm Metab Res. 1996;28:122–127
  61. Ootsuka Y, Heidbreder CA, Hagan JJ, Blessing WW. Dopamine D2 receptor stimulation inhibits cold-initiated thermogenesis in brown adipose tissue in conscious rats. Neuroscience. 2007;147:127–135

 This work was supported by the Wellcome Trust project grant 073142. A. K. Lee is supported by an MRC Doctoral training account and N. J. Marshall by a BHF studentship.

PII: S0899-9007(09)00228-7

doi: 10.1016/j.nut.2009.05.007

Nutrition
Volume 26, Issue 4 , Pages 411-422 , April 2010