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Neural Plasticity
Volume 2017, Article ID 9498247, 14 pages
https://doi.org/10.1155/2017/9498247
Research Article

Autism-Like Behaviours and Memory Deficits Result from a Western Diet in Mice

1Department of Neuroscience, School for Mental Health and Neuroscience, Maastricht University, Universiteitssingel 40, 6200 MD Maastricht, Netherlands
2Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow 119991, Russia
3Faculty of Medicine, Neuroscience Research Center of Lyon, C. Bernard University, 8 Av. Rockefeller, 69373 Lyon, France
4Department of Anaesthesiology, Queen Mary Hospital, The University of Hong Kong, 102 Pokfulam, Hong Kong
5Department of Normal Physiology, Sechenov First Moscow State Medical University, Moscow 119991, Russia
6Laboratory of Biomolecular Screening, Institute of Physiologically Active Compounds, Russian Academy of Sciences, Moscow Region, Russia
7Division of Molecular Psychiatry, Laboratory of Translational Neuroscience, Department of Psychiatry, Psychosomatics and Psychotherapy, University of Würzburg, Fuechsleinstrasse 15, 97080 Würzburg, Germany
8Department of Pharmacology, Oxford University, Mansfield Road, Oxford OX1 3QT, UK

Correspondence should be addressed to Daniel C. Anthony; ku.ca.xo.mrahp@ynohtna.leinad and Tatyana Strekalova; ln.ytisrevinuthcirtsaam@avolakerts.t

Received 7 January 2017; Revised 9 March 2017; Accepted 20 March 2017; Published 8 June 2017

Academic Editor: Bruno Poucet

Copyright © 2017 Ekaterina Veniaminova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. B. Sonawalla, G. I. Papakostas, T. J. Petersen et al., “Elevated cholesterol levels associated with nonresponse to fluoxetine treatment in major depressive disorder,” Psychosomatics, vol. 43, no. 4, pp. 310–316, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. J. C. Felger and F. E. Lotrich, “Inflammatory cytokines in depression: neurobiological mechanisms and therapeutic implications,” Neuroscience, vol. 246, pp. 199–229, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Zilkha, Y. Kuperman, and T. Kimchi, “High-fat diet exacerbates cognitive rigidity and social deficiency in the BTBR mouse model of autism,” Neuroscience, vol. 345, pp. 142–154, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Pohl, M. Sheppard, G. N. Luheshi, and B. Woodside, “Diet-induced weight gain produces a graded increase in behavioral responses to an acute immune challenge,” Brain, Behavior, and Immunity, vol. 35, pp. 43–50, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. M. D. Parrott and C. E. Greenwood, “Dietary influences on cognitive function with aging: from high-fat diets to healthful eating,” Annals of the New York Academy of Sciences, vol. 1114, no. 1, pp. 389–397, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. T. M. Comhair, S. C. Garcia Caraballo, C. H. Dejong, W. H. Lamers, and S. E. Köhler, “Dietary cholesterol, female gender and n-3 fatty acid deficiency are more important factors in the development of non-alcoholic fatty liver disease than the saturation index of the fat,” Nutrition & Metabolism (London), vol. 8, no. 1, p. 4, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Winocur and C. E. Greenwood, “The effects of high fat diets and environmental influences on cognitive performance in rats,” Behavioural Brain Research, vol. 101, no. 2, pp. 153–161, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. J. G. Mielke, K. Nicolitch, V. Avellaneda et al., “Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice,” Behavioural Brain Research, vol. 175, no. 2, pp. 374–382, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Thirumangalakudi, A. Prakasam, R. Zhang et al., “High cholesterol-induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice,” Journal of Neurochemistry, vol. 106, no. 1, pp. 475–485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Winocur and C. E. Greenwood, “Studies of the effects of high fat diets on cognitive function in a rat model,” Neurobiology of Aging, vol. 26, Supplement 1, pp. 46–49, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. Z. Wang, J. Fan, J. Wang et al., “Protective effect of lycopene on high-fat diet-induced cognitive impairment in rats,” Neuroscience Letters, vol. 627, pp. 185–191, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Ledreux, X. Wang, M. Schultzberg, A. C. Granholm, and L. R. Freeman, “Detrimental effects of a high fat/high cholesterol diet on memory and hippocampal markers in aged rats,” Behavioural Brain Research, vol. 312, pp. 294–304, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. J. R. Kaplan, S. B. Manuck, and C. Shively, “The effects of fat and cholesterol on social behavior in monkeys,” Psychosomatic Medicine, vol. 53, no. 6, pp. 634–642, 1991. View at Publisher · View at Google Scholar
  14. N. Connolly, J. Anixt, P. Manning, L. D. Ping-I, K. A. Marsolo, and K. Bowers, “Maternal metabolic risk factors for autism spectrum disorder—an analysis of electronic medical records and linked birth data,” Autism Research, vol. 9, no. 8, pp. 829–837, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. S. A. Buffington, G. V. Di Prisco, T. A. Auchtung, N. J. Ajami, J. F. Petrosino, and M. Costa-Mattioli, “Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring,” Cell, vol. 165, no. 7, pp. 1762–1775, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. A. L. Burgueño, R. Cabrerizo, M. N. Gonzales, S. Sookoian, and C. J. Pirola, “Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A,” The Journal of Nutritional Biochemistry, vol. 24, no. 1, pp. 6–13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. D. L. Williams, G. Goldstein, and N. J. Minshew, “The profile of memory function in children with autism,” Neuropsychology, vol. 20, no. 1, pp. 21–29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Solomon, J. B. McCauley, A. M. Iosif, C. S. Carter, and J. D. Ragland, “Cognitive control and episodic memory in adolescents with autism spectrum disorders,” Neuropsychologia, vol. 89, pp. 31–41, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Dufour, Q. Y. Liu, P. Gusev, D. Alkon, and M. Atzori, “Cholesterol-enriched diet affects spatial learning and synaptic function in hippocampal synapses,” Brain Research, vol. 1103, no. 1, pp. 88–98, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Micale, G. Scapagnini, C. Colombrita, C. Mazzola, D. L. Alkon, and F. Drago, “Behavioral effects of dietary cholesterol in rats tested in experimental models of mild stress and cognition tasks,” European Neuropsychopharmacology, vol. 18, no. 6, pp. 462–471, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. A. C. Granholm, H. A. Bimonte-Nelson, A. B. Moore, M. E. Nelson, L. R. Freeman, and K. Sambamurti, “Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat,” Journal of Alzheimer's Disease, vol. 14, no. 2, pp. 133–145, 2008. View at Google Scholar
  22. L. L. Hwang, C. H. Wang, T. L. Li et al., “Sex differences in high-fat diet-induced obesity, metabolic alterations and learning, and synaptic plasticity deficits in mice,” Obesity (Silver Spring), vol. 18, no. 3, pp. 463–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. N. F. Gould, M. K. Holmes, B. D. Fantie et al., “Performance on a virtual reality spatial memory navigation task in depressed patients,” The American Journal of Psychiatry, vol. 164, no. 3, pp. 516–519, 2007. View at Publisher · View at Google Scholar
  24. R. C. Scarpulla, “Nuclear activators and coactivators in mammalian mitochondrial biogenesis,” Biochimica et Biophysica Acta, vol. 1576, no. 1-2, pp. 1–14, 2002. View at Google Scholar
  25. J. Lin, P. H. Wu, P. T. Tarr et al., “Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice,” Cell, vol. 119, no. 1, pp. 121–135, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. T. C. Leone, J. J. Lehman, B. N. Finck et al., “PGC-1α deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis,” PLoS Biology, vol. 3, no. 4, article e101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Qin, V. Haroutunian, P. Katsel et al., “PGC-1α expression decreases in the Alzheimer disease brain as a function of dementia,” Archives of Neurology, vol. 66, no. 3, pp. 352–361, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. A. F. Bartley, E. K. Lucas, L. J. Brady et al., “Interneuron transcriptional dysregulation causes frequency-dependent alterations in the balance of inhibition and excitation in hippocampus,” The Journal of Neuroscience, vol. 35, no. 46, pp. 15276–15290, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. J. L. Rubenstein and M. M. Merzenich, “Model of autism: increased ratio of excitation/inhibition in key neural systems,” Genes, Brain, and Behavior, vol. 2, no. 5, pp. 255–267, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Strekalova, M. Evans, J. Costa-Nunes et al., “Tlr4 upregulation in the brain accompanies depression- and anxiety-like behaviors induced by a high-cholesterol diet,” Brain, Behavior, and Immunity, vol. 48, pp. 42–47, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Strekalova, J. P. Costa-Nunes, E. Veniaminova et al., “Insulin receptor sensitizer, dicholine succinate, prevents both Toll-like receptor 4 (TLR4) upregulation and affective changes induced by a high-cholesterol diet in mice,” Journal of Affective Disorders, vol. 196, pp. 109–116, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Veniaminova, R. Cespuglio, N. Markova et al., “Behavioral features of mice fed with a cholesterol-enriched diet: deficient novelty exploration and unaltered aggressive behavior,” Translational Neuroscience and Clinics, vol. 2, no. 2, pp. 87–95, 2016. View at Publisher · View at Google Scholar
  33. R. M. Deacon, A. Croucher, and J. N. Rawlins, “Hippocampal cytotoxic lesion effects on species-typical behaviours in mice,” Behavioural Brain Research, vol. 132, no. 2, pp. 203–213, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Strekalova and H. W. Steinbusch, “Measuring behavior in mice with chronic stress depression paradigm,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, vol. 34, no. 2, pp. 348–361, 2010. View at Google Scholar
  35. E. Malatynska, H. W. Steinbusch, O. Redkozubova et al., “Anhedonic-like traits and lack of affective deficits in 18-month-old C57BL/6 mice: implications for modeling elderly depression,” Experimental Gerontology, vol. 47, no. 8, pp. 552–564, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Couch, D. C. Anthony, O. Dolgov et al., “Microglial activation, increased TNF and SERT expression in the prefrontal cortex define stress-altered behaviour in mice susceptible to anhedonia,” Brain, Behavior, and Immunity, vol. 29, pp. 136–146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. R. C. Mantella, R. R. Vollmer, and J. A. Amico, “Corticosterone release is heightened in food or water deprived oxytocin deficient male mice,” Brain Research, vol. 1058, no. 1-2, pp. 56–61, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Arakawa, D. C. Blanchard, and R. J. Blanchard, “Central oxytocin regulates social familiarity and scent marking behavior that involves amicable odour signals between male mice,” Physiology & Behavior, vol. 146, pp. 36–46, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. M. E. Hahn, “Genetic “artifacts” an aggressive behavior,” Aggressive Behavior: Genetic and Neural Approaches, Lawrence Erlbaum Associates, Hillsdale, NJ, 1983. View at Google Scholar
  40. Y. Couch, A. Trofimov, N. Markova et al., “Low-dose lipopolysaccharide (LPS) inhibits aggressive and augments depressive behaviours in a chronic mild stress model in mice,” Journal of Neuroinflammation, vol. 13, no. 1, p. 108, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Strekalova, B. Zörner, C. Zacher, G. Sadovska, T. Herdegen, and P. Gass, “Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus,” Genes, Brain, and Behavior, vol. 2, no. 1, pp. 3–10, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Vignisse, H. W. Steinbusch, V. Grigoriev et al., “Concomitant manipulation of murine NMDA- and AMPA-receptors to produce pro-cognitive drug effects in mice,” European Neuropsychopharmacology, vol. 24, no. 2, pp. 309–320, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Koolhaas, S. M. Korte, S. F. De Boer et al., “Coping styles in animals: current status in behavior and stress-physiology,” Neuroscience and Biobehavioral Reviews, vol. 23, no. 7, pp. 925–993, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Krishna, M. M. Keralapurath, Z. Lin et al., “Neurochemical and electrophysiological deficits in the ventral hippocampus and selective behavioral alterations caused by high-fat diet in female C57BL/6 mice,” Neuroscience, vol. 297, pp. 170–181, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Koizumi, K. Hashimoto, and M. Iyo, “Dietary restriction changes behaviours in brain-derived neurotrophic factor heterozygous mice: role of serotonergic system,” The European Journal of Neuroscience, vol. 24, no. 8, pp. 2335–2344, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. J. M. Pérez-Ortiz, A. Galiana-Simal, E. Salas, C. González-Martín, M. García-Rojo, and L. F. Alguacil, “A high-fat diet combined with food deprivation increases food seeking and the expression of candidate biomarkers of addiction,” Addiction Biology, pp. 12–19, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Vucetic, J. L. Carlin, K. Totoki, and T. M. Reyes, “Epigenetic dysregulation of the dopamine system in diet-induced obesity,” Journal of Neurochemistry, vol. 120, no. 6, pp. 891–898, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. N. M. Grissom, R. George, and T. M. Reyes, “The hypothalamic transcriptional response to stress is severely impaired in offspring exposed to adverse nutrition during gestation,” Neuroscience, vol. 342, pp. 200–211, 2015. View at Publisher · View at Google Scholar
  49. T. South and X. F. Huang, “Temporal and site-specific brain alterations in CB1 receptor binding in high fat diet-induced obesity in C57Bl/6 mice,” Journal of Neuroendocrinology, vol. 20, no. 11, pp. 1288–1294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. M. A. Labouesse, U. Stadlbauer, W. Langhans, and U. Meyer, “Chronic high fat diet consumption impairs sensorimotor gating in mice,” Psychoneuroendocrinology, vol. 38, no. 11, pp. 2562–2574, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. N. M. Grissom and T. M. Reyes, “Gestational overgrowth and undergrowth affect neurodevelopment: similarities and differences from behavior to epigenetics,” International Journal of Developmental Neuroscience, vol. 31, no. 6, pp. 406–414, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. M. M. Kaczmarczyk, A. S. Machaj, G. S. Chiu et al., “Methylphenidate prevents high-fat diet (HFD)-induced learning/memory impairment in juvenile mice,” Psychoneuroendocrinology, vol. 38, no. 9, pp. 1553–1564, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. J. L. Sobesky, R. M. Barrientos, H. S. De May et al., “High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1β, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism,” Brain, Behavior, and Immunity, vol. 42, pp. 22–32, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. S. S. Kang, P. R. Jeraldo, A. Kurti et al., “Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition,” Molecular Neurodegeneration, vol. 9, no. 1, p. 36, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. F. D. Heyward, R. G. Walton, M. S. Carle, M. A. Coleman, W. T. Garvey, and J. D. Sweatt, “Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression,” Neurobiology of Learning and Memory, vol. 98, no. 1, pp. 25–32, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. R. M. Deacon, “Burrowing in rodents: a sensitive method for detecting behavioral dysfunction,” Nature Protocols, vol. 1, no. 1, pp. 118–121, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J. L. Teeling, L. M. Felton, R. M. Deacon, C. Cunningham, J. N. Rawlins, and V. H. Perry, “Sub-pyrogenic systemic inflammation impacts on brain and behavior, independent of cytokines,” Brain, Behavior, and Immunity, vol. 21, no. 6, pp. 836–850, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. D. M. Richman, L. Barnard-Brak, A. Bosch, S. Thompson, L. Grubb, and L. Abby, “Predictors of self-injurious behaviour exhibited by individuals with autism spectrum disorder,” Journal of Intellectual Disability Research, vol. 57, no. 5, pp. 429–439, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Kalaivanisailaja, V. Manju, and N. Nalini, “Lipid profile in mice fed a high-fat diet after exogenous leptin administration,” Polish Journal of Pharmacology, vol. 55, no. 5, pp. 763–769, 2003. View at Google Scholar
  60. Y. Fujita and K. Maki, “High-fat diet-induced obesity triggers alveolar bone loss and spontaneous periodontal disease in growing mice,” BMC Obesity, vol. 3, no. 1, p. 1, 2016. View at Publisher · View at Google Scholar
  61. M. Milanski, A. P. Arruda, A. Coope et al., “Inhibition of hypothalamic inflammation reverses diet-induced insulin resistance in the liver,” Diabetes, vol. 61, no. 6, pp. 1455–1462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. D. A. Rossignol and R. E. Frye, “Mitochondrial dysfunction in autism spectrum disorders: a systematic review and meta-analysis,” Molecular Psychiatry, vol. 17, no. 3, pp. 290–314, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. M. R. Herbert and J. A. Buckley, “Autism and dietary therapy: case report and review of the literature,” Journal of Child Neurology, vol. 28, no. 8, pp. 975–982, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. P. B. Gorelick, “Role of inflammation in cognitive impairment: results of observational epidemiological studies and clinical trials,” Annals of the New York Academy of Sciences, vol. 1207, no. 1, pp. 155–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. M. J. Engelhart, M. I. Geerlings, J. Meijer et al., “Inflammatory proteins in plasma and the risk of dementia: the rotterdam study,” Archives of Neurology, vol. 61, no. 5, pp. 668–672, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. J. C. D. Nguyen, A. S. Killcross, and T. A. Jenkins, “Obesity and cognitive decline: role of inflammation and vascular changes,” Frontiers in Neuroscience, vol. 8, p. 375, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Napoli, C. Ross-Inta, S. Wong et al., “Mitochondrial dysfunction in pten haplo-insufficient mice with social deficits and repetitive behavior: interplay between Pten and p53,” PloS One, vol. 7, no. 8, article e42504, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Mancuso, V. Calsolaro, D. Orsucci et al., “Mitochondria, cognitive impairment, and Alzheimer’s disease,” International Journal of Alzheimer's Disease, vol. 2009, Article ID 951548, 8 pages, 2009. View at Publisher · View at Google Scholar
  69. T. Ruhl, A. Jonas, N. I. Seidel et al., “Oxidation and cognitive impairment in the aging zebrafish,” Gerontology, vol. 62, no. 1, pp. 47–57, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Giugliano, A. Ceriello, and K. Esposito, “The effects of diet on inflammation: emphasis on the metabolic syndrome,” Journal of the American College of Cardiology, vol. 48, no. 4, pp. 677–685, 2006. View at Google Scholar
  71. L. C. Graham, J. M. Harder, I. Soto, W. N. de Vries, S. W. M. John, and G. R. Howella, “Chronic consumption of a western diet induces robust glial activation in aging mice and in a mouse model of Alzheimer’s disease,” Scientific Reports, vol. 6, p. 21568, 2016. View at Publisher · View at Google Scholar · View at Scopus
  72. A. A. Farooqui, Inflammation and Oxidative Stress in Neurological Disorders. Effect of Lifestyle, Genes, and Age. Chapter: The Effects of Diet, Exercise, and Sleep on Brain Metabolism and Function, Springer International Publishing, Switzerland, 2014. View at Publisher · View at Google Scholar
  73. F. A. Neves, E. Cortez, A. F. Bernardo et al., “Heart energy metabolism impairment in Western-diet induced obese mice,” The Journal of Nutritional Biochemistry, vol. 25, no. 1, pp. 50–57, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. I. A. Pomytkin, B. H. Cline, D. C. Anthony, H. W. Steinbusch, K. P. Lesch, and T. Strekalova, “Endotoxaemia resulting from decreased serotonin tranporter (5-HTT) function: a reciprocal risk factor for depression and insulin resistance?” Behavioural Brain Research, vol. 276, pp. 111–117, 2015. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Herzig, F. Long, U. S. Jhala et al., “CREB regulates hepatic gluconeogenesis through the coactivator PGC-1,” Nature, vol. 413, no. 6852, pp. 179–183, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. F. D. Heyward, D. Gilliam, M. A. Coleman et al., “Obesity weighs down memory through a mechanism involving the neuroepigenetic dysregulation of Sirt1,” The Journal of Neuroscience, vol. 36, no. 4, pp. 1324–1335, 2016. View at Publisher · View at Google Scholar · View at Scopus
  77. T. A. Larkina, A. L. Sazanova, K. A. Fomichev et al., “HMG1A and PPARG are differently expressed in the liver of fat and lean broilers,” Journal of Applied Genetics, vol. 52, no. 2, pp. 225–228, 2011. View at Publisher · View at Google Scholar · View at Scopus