Bardoxolone methyl prevents high-fat diet-induced alterations in prefrontal cortex signalling molecules involved in recognition memory

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 59, Issue , 2015, Pages 68-75

  Camer, Danielle ^a   Yu, Yinghua ^a   Szabo, Alexander ^a,b   Fernandez, Francesca ^a,c   Dinh, Chi H L ^a   Huang, Xu Feng ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^c Schizophrenia Research Institute   (Australia)

Author keywords

Bardoxolone methyl; Hippocampus; Obesity; Prefrontal cortex; Recognition memory

Indexed keywords

BARDOXOLONE METHYL; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE 1B; STRESS ACTIVATED PROTEIN KINASE; DIZOCILPINE MALEATE; METHYL 2-CYANO-3,12-DIOXOOLEAN-1,9-DIEN-28-OATE; NEUROPROTECTIVE AGENT; OLEANOLIC ACID; PROTEIN BINDING; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFECT; HIPPOCAMPUS; LIPID DIET; MALE; MEMORY DISORDER; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PREFRONTAL CORTEX; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ADVERSE EFFECTS; ANALOGS AND DERIVATIVES; ANIMAL; AUTORADIOGRAPHY; C57BL MOUSE; DISEASE MODEL; DRUG ADMINISTRATION; DRUG EFFECTS; EXPLORATORY BEHAVIOR; MEMORY DISORDERS; METABOLISM; NONPARAMETRIC TEST; PATHOLOGY; RECOGNITION;

ANIMALS; AUTORADIOGRAPHY; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DIZOCILPINE MALEATE; DRUG ADMINISTRATION SCHEDULE; EXPLORATORY BEHAVIOR; MALE; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; OLEANOLIC ACID; PREFRONTAL CORTEX; PROTEIN BINDING; RECOGNITION (PSYCHOLOGY); SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; TRITIUM;

EID: 84921969632     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2015.01.004     Document Type: Article

References (56)

1. Bachevalier J., Mishkin M. Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behav Brain Res 1986, 20:249-261.
2. Banks P.J., Bashir Z.I., Brown M.W. Recognition memory and synaptic plasticity in the perirhinal and prefrontal cortices. Hippocampus 2012, 22:2012-2031.
3. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
4. Camer D., Huang X.F. The endothelin pathway: a protective or detrimental target of bardoxolone methyl on cardiac function in patients with advanced chronic kidney disease?. Am J Nephrol 2014, 40:288-290.
5. Camer D., Yu Y., Szabo A., Huang X.F. The molecular mechanisms underpinning the therapeutic properties of oleanolic acid, its isomer and derivatives for type 2 diabetes and associated complications. Mol Nutr Food Res 2014, 58:1750-1759.
6. Carey A.N., Gomes S.M., Shukitt-Hale B. Blueberry supplementation improves memory in middle-aged mice fed a high-fat diet. J Agric Food Chem 2014, 62(18):3972-3978.
7. Cooke S.F., Bliss T.V. Plasticity in the human central nervous system. Brain 2006, 129:1659-1673.
8. Cunha C., Brambilla R., Thomas K.L. A simple role for BDNF in learning and memory?. Front Mol Neurosci 2010, 3:1.
9. Dumont M., Wille E., Calingasan N.Y., Tampellini D., Williams C., Gouras G.K., et al. Triterpenoid CDDO-methylamide improves memory and decreases amyloid plaques in a transgenic mouse model of Alzheimer's disease. J Neurochem 2009, 109:502-512.
10. Fernandez F., Soon I., Li Z., Kuan T.C., Min D.H., Wong E.S., et al. Wip1 phosphatase positively modulates dendritic spine morphology and memory processes through the p38MAPK signaling pathway. Cell Adhes Migr 2012, 6:333-343.
11. Forwood S.E., Winters B.D., Bussey T.J. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48h. Hippocampus 2005, 15:347-355.
12. Fuentes F., Zimmer D., Atienza M., Schottenfeld J., Penkala I., Bale T., et al. Protein tyrosine phosphatase PTP1B is involved in hippocampal synapse formation and learning. PLoS ONE 2012, 7:e41536.
13. Gomez-Pinilla F., Vaynman S., Ying Z. Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci 2008, 28:2278-2287.
14. Greenwood C.E., Winocur G. Learning and memory impairment in rats fed a high saturated fat diet. Behav Neural Biol 1990, 53:74-87.
15. Greenwood C.E., Winocur G. Cognitive impairment in rats fed high-fat diets: a specific effect of saturated fatty-acid intake. Behav Neurosci 1996, 110:451-459.
16. Hassing L.B., Johansson B., Nilsson S.E., Berg S., Pedersen N.L., Gatz M., et al. Diabetes mellitus is a risk factor for vascular dementia, but not for Alzheimer's disease: a population-based study of the oldest old. Int Psychogeriatr 2002, 14:239-248.
17. Heyward F.D., Walton R.G., Carle M.S., Coleman M.A., Garvey W.T., Sweatt J.D. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 2012, 98:25-32.
18. Jiang T., Yin F., Yao J., Brinton R.D., Cadenas E. Lipoic acid restores age-associated impairment of brain energy metabolism through the modulation of Akt/JNK signaling and PGC1alpha transcriptional pathway. Aging Cell 2013, 12:1021-1031.
19. Kanoski S.E., Meisel R.L., Mullins A.J., Davidson T.L. The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behav Brain Res 2007, 182:57-66.
20. Kolb B., Buhrmann K., McDonald R., Sutherland R.J. Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 1994, 4:664-680.
21. Langston R.F., Wood E.R. Associative recognition and the hippocampus: differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 2010, 20:1139-1153.
22. Laroche S., Davis S., Jay T.M. Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus 2000, 10:438-446.
23. Liby K.T., Sporn M.B. Synthetic oleanane triterpenoids: multifunctional drugs with a broad range of applications for prevention and treatment of chronic disease. Pharmacol Rev 2012, 64:972-1003.
24. Lu J., Wu D.M., Zheng Y.L., Hu B., Cheng W., Zhang Z.F., et al. Ursolic acid improves high fat diet-induced cognitive impairments by blocking endoplasmic reticulum stress and IkappaB kinase beta/nuclear factor-kappaB-mediated inflammatory pathways in mice. Brain Behav Immun 2011, 25:1658-1667.
25. Miller A.A., Spencer S.J. Obesity and neuroinflammation: a pathway to cognitive impairment. Brain Behav Immun 2014, 42:10-21.
26. Molteni R., Barnard R.J., Ying Z., Roberts C.K., Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002, 112:803-814.
27. Morrison C.D., Pistell P.J., Ingram D.K., Johnson W.D., Liu Y., Fernandez-Kim S.O., et al. High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J Neurochem 2010, 114:1581-1589.
28. Mumby D.G., Gaskin S., Glenn M.J., Schramek T.E., Lehmann H. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 2002, 9:49-57.
29. Newell K.A., Zavitsanou K., Huang X.F. Ionotropic glutamate receptor binding in the posterior cingulate cortex in schizophrenia patients. Neuroreport 2005, 16:1363-1367.
30. Noble E.E., Billington C.J., Kotz C.M., Wang C. The lighter side of BDNF. Am J Physiol Regul Integr Comp Physiol 2011, 300:R1053-R1069.
31. Park S.J., Lee Y., Oh H.K., Lee H.E., Ko S.Y., Kim B., et al. Oleanolic acid attenuates MK-801-induced schizophrenia-like behaviors in mice. Neuropharmacology 2014, 86C:49-56.
32. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2002, San Diego Academic Press. 1st edn ed.
33. Pergola P.E., Raskin P., Toto R.D., Meyer C.J., Huff J.W., Grossman E.B., et al. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 2011, 365:327-336.
34. Pistell P.J., Morrison C.D., Gupta S., Knight A.G., Keller J.N., Ingram D.K., et al. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol 2010, 219:25-32.
35. Pitha-Rowe I., Liby K., Royce D., Sporn M. Synthetic triterpenoids attenuate cytotoxic retinal injury: cross-talk between Nrf2 and PI3K/AKT signaling through inhibition of the lipid phosphatase PTEN. Invest Ophthalmol Vis Sci 2009, 50:5339-5347.
36. Reisman S.A., Chertow G.M., Hebbar S., Vaziri N.D., Ward K.W., Meyer C.J. Bardoxolone methyl decreases megalin and activates Nrf2 in the kidney. J Am Soc Nephrol 2012, 23:1663-1673.
37. Rose C.R., Blum R., Kafitz K.W., Kovalchuk Y., Konnerth A. From modulator to mediator: rapid effects of BDNF on ion channels. Bioessays 2004, 26:1185-1194.
38. Sakata K., Martinowich K., Woo N.H., Schloesser R.J., Jimenez D.V., Ji Y., et al. Role of activity-dependent BDNF expression in hippocampal-prefrontal cortical regulation of behavioral perseverance. Proc Natl Acad Sci U S A 2013, 110:15103-15108.
39. Singh R.B., Gupta S., Dherange P., De Meester F., Wilczynska A., Alam S.E., et al. Metabolic syndrome: a brain disease. Can J Physiol Pharmacol 2012, 90:1171-1183.
40. Sunayama J., Tsuruta F., Masuyama N., Gotoh Y. JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 2005, 170:295-304.
41. Tran T.A., McCoy M.K., Sporn M.B., Tansey M.G. The synthetic triterpenoid CDDO-methyl ester modulates microglial activities, inhibits TNF production, and provides dopaminergic neuroprotection. J Neuroinflammation 2008, 5:14.
42. Valladolid-Acebes I., Stucchi P., Cano V., Fernandez-Alfonso M.S., Merino B., Gil-Ortega M., et al. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem 2011, 95:80-85.
43. Valladolid-Acebes I., Merino B., Principato A., Fole A., Barbas C., Lorenzo M.P., et al. High-fat diets induce changes in hippocampal glutamate metabolism and neurotransmission. Am J Physiol Endocrinol Metab 2012, 302:E396-E402.
44. Val-Laillet D., Layec S., Guerin S., Meurice P., Malbert C.H. Changes in brain activity after a diet-induced obesity. Obesity (Silver Spring) 2011, 19:749-756.
45. Wang H., Garvin J.L., D'Ambrosio M.A., Falck J.R., Leung P., Liu R., et al. Heme oxygenase metabolites inhibit tubuloglomerular feedback in vivo. Am J Physiol Heart Circ Physiol 2011, 300:H1320-H1326.
46. Wang D., Fu Q., Zhou Y., Xu B., Shi Q., Igwe B., et al. Beta2 adrenergic receptor, protein kinase A (PKA) and c-Jun N-terminal kinase (JNK) signaling pathways mediate tau pathology in Alzheimer disease models. J Biol Chem 2013, 288:10298-10307.
47. Warburton E.C., Barker G.R., Brown M.W. Investigations into the involvement of NMDA mechanisms in recognition memory. Neuropharmacology 2013, 74:41-47.
48. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003, 112:1796-1808.
49. Wu A., Molteni R., Ying Z., Gomez-Pinilla F. A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience 2003, 119:365-375.
50. Wu A., Ying Z., Gomez-Pinilla F. Oxidative stress modulates Sir2alpha in rat hippocampus and cerebral cortex. Eur J Neurosci 2006, 23:2573-2580.
51. Wu J., Liu X., Fan J., Chen W., Wang J., Zeng Y., et al. Bardoxolone methyl (BARD) ameliorates aristolochic acid (AA)-induced acute kidney injury through Nrf2 pathway. Toxicology 2014, 318:22-31.
52. Xu H., Barnes G.T., Yang Q., Tan G., Yang D., Chou C.J., et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003, 112:1821-1830.
53. Yoon H., Oh Y.T., Lee J.Y., Choi J.H., Lee J.H., Baik H.H., et al. Activation of AMP-activated protein kinase by kainic acid mediates brain-derived neurotrophic factor expression through a NF-kappaB dependent mechanism in C6 glioma cells. Biochem Biophys Res Commun 2008, 371:495-500.
54. Yoshii A., Constantine-Paton M. BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 2007, 10:702-711.
55. Zhang Y.N., Zhang W., Hong D., Shi L., Shen Q., Li J.Y., et al. Oleanolic acid and its derivatives: new inhibitor of protein tyrosine phosphatase 1B with cellular activities. Bioorg Med Chem 2008, 16:8697-8705.
56. Zhao Y., Shen J., Su H., Li B., Xing D., Du L. Chronic corticosterone injections induce a decrease of ATP levels and sustained activation of AMP-activated protein kinase in hippocampal tissues of male mice. Brain Res 2008, 1191:148-156.