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Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 25, 2022 - Issue 6
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Research Article

Irreversible hippocampal changes induced by high fructose diet in rats

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References

  • Vos MB, Kimmons JE, Gillespie C, Welsh J, Blanck HM. Dietary fructose consumption among US children and adults: The Third National Health and Nutrition Examination Survey. Medscape J Med. 2008;10(7):160.
  • Hannou SA, Haslam DE, McKeown NM, Herman MA. Fructose metabolism and metabolic disease. J Clin Invest. 2018;128(2):545–55.
  • Taskinen MR, Packard CJ, Borén J. Dietary fructose and the metabolic syndrome. Nutrients. 2019;11(9):1987.
  • Tappy L. Fructose-containing caloric sweeteners as a cause of obesity and metabolic disorders. J Exp Biol. 2018;221(S1):jeb164202.
  • Softic S, Stanhope KL, Boucher J, Divanovic S, Lanaspa MA, Johnson RJ, et al. Fructose and hepatic insulin resistance. Crit Rev Clin Lab Sci. 2020;57(5):308–22.
  • Zhao S, Jang C, Liu J, Uehara K, Gilbert M, Izzo L, et al. Dietary fructose feeds hepatic lipogenesis via microbiota-derived acetate. Nature. 2020;579(7800):586–91.
  • Teff KL, Elliott SS, Tschöp M, Kieffer TJ, Rader D, Heiman M, et al. Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J Clin Endocrinol Metab. 2004;89(6):2963–72.
  • Agrawal R, Noble E, Vergnes L, Ying Z, Reue K, Gomez-Pinilla F. Dietary fructose aggravates the pathobiology of traumatic brain injury by influencing energy homeostasis and plasticity. J Cereb Blood Flow Metab. 2016;36(5):941–53.
  • Batista LO, Ramos VW, Rosas Fernández MA, Concha Vilca CM, Albuquerque KT. Oral solution of fructose promotes SREBP-1c high-expression in the hypothalamus of Wistar rats. Nutr Neurosci. 2019;22(9):648–54.
  • Sangüesa G, Roglans N, Montañés JC, Baena M, Velázquez AM, Sánchez RM, et al. Chronic liquid fructose-, but not glucose-, supplementation selectively induces visceral adipose tissue leptin resistance and hypertrophy in female Sprague-Dawley rats. Mol Nutr Food Res. 2018;62(22):e1800777.
  • Spagnuolo MS, Bergamo P, Crescenzo R, Iannotta L, Treppiccione L, Iossa S, et al. Brain Nrf2 pathway, autophagy, and synaptic function proteins are modulated by a short-term fructose feeding in young and adult rats. Nutr Neurosci. 2020;23(4):309–20.
  • Ross AP, Bartness TJ, Mielke JG, Parent MB. A high fructose diet impairs spatial memory in male rats. Neurobiol Learn Mem. 2009;92(3):410–6.
  • Liu X, Luo D, Zheng M, Hao Y, Hou L, Zhang S. Effect of pioglitazone on insulin resistance in fructose-drinking rats correlates with AGEs/RAGE inhibition and block of NADPH oxidase and NF kappa B activation. Eur J Pharmacol. 2010;629(1-3):153–8.
  • Sangüesa G, Cascales M, Griñán C, Sánchez RM, Roglans N, Pallàs M, et al. Impairment of novel object recognition memory and brain insulin signaling in fructose- but not glucose-drinking female rats. Mol Neurobiol. 2018;55(8):6984–99.
  • van der Borght K, Köhnke R, Göransson N, Deierborg T, Brundin P, Erlanson-Albertsson C, et al. Reduced neurogenesis in the rat hippocampus following high fructose consumption. Regul Pept. 2011;167(1):26–30.
  • Liu WC, Wu CW, Tain YL, Fu MH, Hung CY, Chen IC, et al. Oral pioglitazone ameliorates fructose-induced peripheral insulin resistance and hippocampal gliosis but not restores inhibited hippocampal adult neurogenesis. Biochim Biophys Acta Mol Basis Dis. 2018;1864(1):274–85.
  • Cigliano L, Spagnuolo MS, Crescenzo R, Cancelliere R, Iannotta L, Mazzoli A, et al. Short-term fructose feeding induces inflammation and oxidative stress in the hippocampus of young and adult rats. Mol Neurobiol. 2018;55(4):2869–83.
  • Yin Q, Ma Y, Hong Y, Hou X, Chen J, Shen C, et al. Lycopene attenuates insulin signaling deficits, oxidative stress, neuroinflammation, and cognitive impairment in fructose-drinking insulin resistant rats. Neuropharmacology. 2014;86:389–96.
  • Rueda-Orozco PE, Montes-Rodriguez CJ, Ruiz-Contreras AE, Mendez-Diaz M, Prospero-Garcia O. The effects of anandamide and oleamide on cognition depend on diurnal variations. Brain Res. 2017;1672:129–36.
  • Marichal-Cancino BA, Fajardo-Valdez A, Ruiz-Contreras AE, Méndez-Díaz M, Prospéro-García O. Possible role of hippocampal GPR55 in spatial learning and memory in rats. Acta Neurobiol Exp (Wars). 2018;78(1):41–50.
  • Franco-Pérez J, Manjarrez-Marmolejo J, Ballesteros-Zebadúa P, Neri-Santos A, Montes S, Suarez-Rivera N, et al. Chronic consumption of fructose induces behavioral alterations by increasing orexin and dopamine levels in the rat brain. Nutrients. 2018;10(11):1722.
  • Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 4th ed. San Diego (CA): Academic Press; 1998.
  • Lee I, Kesner RP. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci. 2003;23(4):1517–23.
  • Gómez-Pinilla F. Brain foods: the effects of nutrients on brain function. Nat Rev Neurosci. 2008;9(7):568–78.
  • Illouz T, Madar R, Clague C, Griffioen KJ, Louzoun Y, Okun E. Unbiased classification of spatial strategies in the Barnes maze. Bioinformatics. 2016;32(21):3314–20.
  • Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol. 1979;93(1):74–104.
  • Jašarević E, Williams SA, Vandas GM, Ellersieck MR, Liao C, Kannan K, et al. Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring. Horm Behav. 2013;63(1):180–9.
  • Fouquet C, Babayan BM, Watilliaux A, Bontempi B, Tobin C, Rondi-Reig L. Complementary roles of the hippocampus and the dorsomedial striatum during spatial and sequence-based navigation behavior. PLoS One. 2013;8(6):e67232.
  • Vorhees CV, Williams MT. Assessing spatial learning and memory in rodents. ILAR J. 2014;55(2):310–32.
  • Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science. 1977;197(4308):1092–4.
  • Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci. 1996;16(6):2027–33.
  • Jinno S. Topographic differences in adult neurogenesis in the mouse hippocampus: a stereology-based study using endogenous markers. Hippocampus. 2011;21(5):467–80.
  • Moser MB, Moser EI, Forrest E, Andersen P, Morris RG. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA. 1995;92(21):9697–701.
  • Pothuizen HH, Zhang WN, Jongen-Rêlo AL, Feldon J, Yee BK. Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur J Neurosci. 2004;19(3):705–12.
  • Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010;65(1):7–19.
  • Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA. 2000;97(20):11032–7.
  • Bonnet E, Touyarot K, Alfos S, Pallet V, Higueret P, Abrous DN. Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS One. 2008;3(10):e3487.
  • Mohapel P, Leanza G, Kokaia M, Lindvall O. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging. 2005;26(6):939–46.
  • Rothwell NJ, Luheshi GN. Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci. 2000;23(12):618–25.
  • Yirmiya R, Winocur G, Goshen I. Brain interleukin-1 is involved in spatial memory and passive avoidance conditioning. Neurobiol Learn Mem. 2002;78(2):379–89.
  • Moore AH, Wu M, Shaftel SS, Graham KA, O'Banion MK. Sustained expression of interleukin-1beta in mouse hippocampus impairs spatial memory. Neuroscience. 2009;164(4):1484–95.
  • Yang H, Chen C. Cyclooxygenase-2 in synaptic signaling. Curr Pharm Des. 2008;14(14):1443–51.
  • Guzmán CB, Graham KA, Grace LA, Moore AH. Sex-dependent effect of cyclooxygenase-2 inhibition on mouse spatial memory. Behav Brain Res. 2009;199(2):355–9.
  • Sharifzadeh M, Naghdi N, Khosrovani S, Ostad SN, Sharifzadeh K, Roghani A. Post-training intrahippocampal infusion of the COX-2 inhibitor celecoxib impaired spatial memory retention in rats. Eur J Pharmacol. 2005;511(2-3):159–66.
  • Chen C, Magee JC, Bazan NG. Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J Neurophysiol. 2002;87(6):2851–7.
  • Cowley TR, Fahey B, O’Mara SM. COX-2, but not COX-1, activity is necessary for the induction of perforant path long-term potentiation and spatial learning in vivo. Eur J Neurosci. 2008;27(11):2999–3008.
  • Cisternas P, Salazar P, Serrano FG, Montecinos-Oliva C, Arredondo SB, Varela-Nallar L, et al. Fructose consumption reduces hippocampal synaptic plasticity underlying cognitive performance. Biochim Biophys Acta. 2015;1852(11):2379–90.
  • Woiciechowsky C, Schöning B, Stoltenburg-Didinger G, Stockhammer F, Volk HD. Brain-IL-1 beta triggers astrogliosis through induction of IL-6: inhibition by propranolol and IL-10. Med Sci Monit. 2004;10(9):BR325–30.
  • Sticozzi C, Belmonte G, Meini A, Carbotti P, Grasso G, Palmi M. IL-1β induces GFAP expression in vitro and in vivo and protects neurons from traumatic injury-associated apoptosis in rat brain striatum via NFκB/Ca²+-calmodulin/ERK mitogen-activated protein kinase signaling pathway. Neuroscience. 2013;252:367–83.
  • Rose CF, Verkhratsky A, Parpura V. Astrocyte glutamine synthetase: pivotal in health and disease. Biochem Soc Trans. 2013;41(6):1518–24.
  • Olabarria M, Noristani HN, Verkhratsky A, Rodríguez JJ. Age-dependent decrease in glutamine synthetase expression in the hippocampal astroglia of the triple transgenic Alzheimer’s disease mouse model: mechanism for deficient glutamatergic transmission? Mol Neurodegener. 2011;6:55.
  • Burdakov D, Gerasimenko O, Verkhratsky A. Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J Neurosci. 2005;25(9):2429–33.
  • González JA, Jensen LT, Fugger L, Burdakov D. Metabolism-independent sugar sensing in central orexin neurons. Diabetes. 2008;57(10):2569–76.
  • Shu HJ, Isenberg K, Cormier RJ, Benz A, Zorumski CF. Expression of fructose sensitive glucose transporter in the brains of fructose-fed rats. Neuroscience. 2006;140(3):889–95.
  • Page KA, Chan O, Arora J, Belfort-Deaguiar R, Dzuira J, Roehmholdt B, et al. Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA. 2013;309(1):63–70.
  • Aou S, Li XL, Li AJ, Oomura Y, Shiraishi T, Sasaki K, et al. Orexin-A (hypocretin-1) impairs Morris water maze performance and CA1-Schaffer collateral long-term potentiation in rats. Neuroscience. 2003;119(4):1221–8.
  • Akbari E, Naghdi N, Motamedi F. The selective orexin 1 receptor antagonist SB-334867-A impairs acquisition and consolidation but not retrieval of spatial memory in Morris water maze. Peptides. 2007;28(3):650–6.
  • Mihara Y, Dohi K, Yofu S, Nakamachi T, Ohtaki H, Shioda S, et al. Expression and localization of the orexin-1 receptor (OX1R) after traumatic brain injury in mice. J Mol Neurosci. 2011;43(2):162–8.
  • Dohi K, Nishino S, Nakamachi T, Ohtaki H, Morikawa K, Takeda T, et al. CSF orexin A concentrations and expressions of the orexin-1 receptor in rat hippocampus after cardiac arrest. Neuropeptides. 2006;40(4):245–50.
  • Johnson RJ, Gomez-Pinilla F, Nagel M, Nakagawa T, Rodriguez-Iturbe B, Sanchez-Lozada LG, et al. Cerebral fructose metabolism as a potential mechanism driving Alzheimer’s disease. Front Aging Neurosci. 2020;12:560865.

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