Thymol improves high-fat diet-induced cognitive deficits in mice via ameliorating brain insulin resistance and upregulating NRF2/HO-1 pathway

Metabolic Brain Disease

Volumn 32, Issue 2, 2017, Pages 385-393

  Li, Hongyan ^a   Qin, Tingting ^a   Li, Min ^a   Ma, Shiping ^a  

^a China PharmaceuticalUniversity ^*  (China)

Author keywords

Cognitive deficits; High fat diet; Insulin signaling; Nrf2; Oxidative stress; Thymol

Indexed keywords

AMYLOID BETA PROTEIN; CONGO RED; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; HEME OXYGENASE 1; INSULIN; INTERLEUKIN 1BETA; MALONALDEHYDE; METFORMIN; PROTEIN KINASE B; SUPEROXIDE DISMUTASE; TAU PROTEIN; THYMOL; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; ANTIDIABETIC AGENT; ANTIOXIDANT; CYTOKINE; NEUROPROTECTIVE AGENT; NFE2L2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; COGNITION; COGNITIVE DEFECT; COMPARATIVE STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; INFLAMMATION; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; MEMORY DISORDER; MORRIS WATER MAZE TEST; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; WEIGHT GAIN; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DRUG EFFECTS; GENETICS; LEARNING DISORDER; METABOLISM; PSYCHOLOGY;

ANIMALS; ANTIOXIDANTS; COGNITION DISORDERS; CYTOKINES; DIET, HIGH-FAT; HEME OXYGENASE-1; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; LEARNING DISORDERS; MALE; MEMORY DISORDERS; METFORMIN; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; THYMOL; UP-REGULATION;

EID: 84991777396     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-016-9921-z     Document Type: Article

References (55)

1. Allard JS, Perez EJ, Fukui K, Carpenter P, Ingram DK, de Cabo R (2016) Prolonged metformin treatment leads to reduced transcription of Nrf2 and neurotrophic factors without cognitive impairment in older C57BL/6 J mice. Behav Brain Res 301:1–9
2. Arnold SE, Lucki I, Brookshire BR, Carlson GC, Browne CA, Kazi H, Bang S, Choi BR, Chen Y, McMullen MF, Kim SF (2014) High fat diet produces brain insulin resistance, synaptodendritic abnormalities and altered behavior in mice. Neurobiol Dis 67:79–87
3. Azizi Z, Ebrahimi S, Saadatfar E, Kamalinejad M, Majlessi N (2012) Cognitive- enhancing activity of thymol and carvacrol in two rat models of dementia. Behav Pharmacol 23(3):241–249
4. Banks WA (2004) The source of cerebral insulin. Eur J Pharmacol 490:5–12
5. Biessels GJ, Reagan LP (2015) Hippocampal insulin resistance and cognitive dysfunction. Nat Rev Neurosci 16:660–671
6. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, Lee VM (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer’s disease recapitulates development and contributes to reduced microtubule binding. Neuron 10:1089–1099
7. Cai M, Wang H, Li JJ, Zhang YL, Xin L, Li F, Lou SJ (2016) The signaling mechanisms of hippocampal endoplasmic reticulum stress affecting neuronal plasticity-related protein levels in high fat diet-induced obese rats and the regulation of aerobic exercise. Brain Behav Immun 57:347–359
8. Chen L, Magliano DJ, Zimmet PZ (2012) The worldwide epidemiology of type 2 diabetes mellitus--present and future perspectives. Nat Rev Endocrinol 8:228–236
9. Chen J, Deng X, Liu N, Li M, Liu B, Fu Q, Ma S (2016) Quercetin attenuates tau hyperphosphorylation and improves cognitive disorder via suppression of ER stress in a manner dependent on AMPK pathway. J Funct Foods 22:463–476
10. Chiang MC, Nicol CJ, Cheng YC, Lin KH, Yen CH, Lin CH (2016) Rosiglitazone activation of PPARγ-dependent pathways is neuroprotective in human neural stem cells against amyloid-beta–induced mitochondrial dysfunction and oxidative stress. Neurobiol Aging 40:181–190
11. Costa RO, Ferreiro E, Oliveira CR, Pereira CM (2013) Inhibition of mitochondrial cytochrome c oxidase potentiates Aβ-induced ER stress and cell death in cortical neurons. Mol Cell Neurosci 52:1–8
12. D’Apolito M, Du X, Zong H, Catucci A, Maiuri L, Trivisano T, Brownlee M (2010) Urea-induced ROS generation causes insulin resistance in mice with chronic renal failure. J Clin Invest 120:203–213
13. Deng XY, Li HY, Chen JJ, Li RP, Qu R, Fu Q, Ma SP (2015) Thymol produces an antidepressant-like effect in a chronic unpredictable mild stress model of depression in mice. Behav Brain Res 291:12–19
14. Fujita K, Yamafuji M, Nakabeppu Y, Noda M (2012) Therapeutic approach to neurodegenerative diseases by medical gases: focusing on redox signaling and related antioxidant enzymes Oxid Med Cell Longev 2012
15. Greenwood CE, Winocur G (2005) High-fat diets, insulin resistance and declining cognitive function. Neurobiol Aging 26:42–45
16. Grillo CA, Piroli GG, Lawrence RC, Wrighten SA, Green AJ, Wilson SP, Sakai RR, Kelly SJ, Wilson MA, Mott DD, Reagan LP (2015) Hippocampal insulin resistance impairs spatial learning and synaptic plasticity. Diabetes 64:3927–3936
17. Hao J, Chen C, Huang K, Huang J, Li J, Liu P, Huang H (2014) Polydatin improves glucose and lipid metabolism in experimental diabetes through activating the Akt signaling pathway. Eur J Pharmacol 745:152–165
18. Heni M, Kullmann S, Preissl H, Fritsche A, Häring HU (2015) Impaired insulin action in the human brain: causes and metabolic consequences. Nat Rev Endocrinol 11:701–711
19. Hong Y, An Z (2015) Hesperidin attenuates learning and memory deficits in APP/PS1 mice through activation of Akt/Nrf2 signaling and inhibition of RAGE/NF-κB signaling. Arch Pharm Res:1–9. doi:10.1007/s12272-015-0662-z
20. Hoozemans JJ, Van Haastert ES, Nijholt DA, Rozemuller AJ, Scheper W (2012) Activation of the unfolded protein response is an early event in Alzheimer’s and Parkinson’s disease. Neurodegener Dis 10:212–215
21. Jo C, Gundemir S, Pritchard S, Jin YN, Rahman I, Johnson GV (2014) Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat Commun 5. doi:10.1038/ncomms4496
22. Joshi G, Gan KA, Johnson DA, Johnson JA (2015) Increased Alzheimer’s disease-like pathology in the APP/PS1ΔE9 mouse model lacking Nrf2 through modulation of autophagy. Neurobiol Aging 36:664–679
23. Kang S, Tsai LT, Rosen ED (2016) Nuclear mechanisms of insulin resistance. Trends Cell Biol 26:341–351
24. Kido Y, Burks DJ, Withers D, Bruning JC, Kahn CR, White MF, Accili D (2000) Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J Clin Invest 105:199–205
25. Kwon SH, Ma SX, Hwang JY, Lee SY, Jang CG (2015) Involvement of the Nrf2/HO-1 signaling pathway in sulfuretin-induced protection against amyloid beta 25-35 neurotoxicity. Neuroscience 304:14–28
26. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440:352–357
27. Li HH, Lin SL, Huang CN, Lu FJ, Chiu PY, Huang WN, Lai TJ, Lin CL (2016) MIR-302 attenuates amyloid-β-induced neurotoxicity through activation of Akt signaling. J Alzheimers Dis 50:1083–1098
28. Liang D, Li F, Fu Y, Cao Y, Song X, Wang T, Wang W, Guo M, Zhou E, Li D, Yang Z, Zhang N (2014) Thymol inhibits LPS-stimulated inflammatory response via down-regulation of NF-κB and MAPK signaling pathways in mouse mammary epithelial cells. Inflammation 37:214–222
29. Lim HJ, Lee KS, Lee S, Park JH, Choi HE, Go SH, Kwak HJ, Park HY (2007) 15d-PGJ 2 stimulates HO-1 expression through p38 MAP kinase and Nrf-2 pathway in rat vascular smooth muscle cells. Toxicol Appl Pharmacol 223:20–27
30. Liu J, Feng L, Ma D, Zhang M, Gu J, Wang S, Fu Q, Song Y, Lan Z, Qu R, Ma S (2013) Neuroprotective effect of paeonol on cognition deficits of diabetic encephalopathy in streptozotocin-induced diabetic rat. Neurosci Lett 549:63–68
31. Marín LD, Sánchez-Borzone M, García DA (2011) Comparative antioxidant properties of some GABAergic phenols and related compounds, determined for homogeneous and membrane systems. Med Chem 7:317–324
32. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S (2008) Increased oxidative stress precedes the onset of high-fat diet–induced insulin resistance and obesity. Metabolism 57:1071–1077
33. Miladi H, Zmantar T, Chaabouni Y, Fedhila K, Bakhrouf A, Mahdouani K, Chaieb K (2016) Antibacterial and efflux pump inhibitors of thymol and carvacrol against food-borne pathogens. Microb Pathog 99:95–100
34. Mittal K, Katare DP (2016) Shared links between type 2 diabetes mellitus and Alzheimer’s disease: a review. Diabetol Metab Syndr 10:144–149
35. Moore EM, Mander AG, Ames D, Kotowicz MA, Carne RP, Brodaty H, Woodward M, Boundy K, Ellis KA, Bush AI, Faux NG, Martins R, Szoeke C, Rowe C, Watters DA, Investigators AIBL (2013) Increased risk of cognitive impairment in patients with diabetes is associated with metformin. Diabetes Care 36:2981–2987
36. Moreira PI, Santos MS, Seiça R, Oliveira CR (2007) Brain mitochondrial dysfunction as a link between Alzheimer’s disease and diabetes. J Neurol Sci 257:206–214
37. Morrison CD, Pistell PJ, Ingram DK, Johnson WD, Liu Y, Fernandez-Kim SO, White CL, Purpera MN, Uranga RM, Bruce-Keller AJ, Keller JN (2010) High fat diet increases hippocampal oxidative stressand cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J Neurochem 114:1581–1589
38. Najem D, Bamji-Mirza M, Yang Z, Zhang W (2016) Aβ-induced insulin resistance and the effects of insulin on the cholesterol synthesis pathway and Aβ secretion in neural cells. Neurosci Bull 32:227–238
39. Nicolai, A, Li M, Kim DH, Peterson SJ, Vanella L, Positano V, Gastaldelli A, Rezzani R, Rodella LF, Drummond G, Kusmic C, L’Abbate A, Kappas A, Abraham NG (2009) Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension 53: 508–515
40. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3α regulates production of Alzheimer’s disease amyloid-β peptides. Nature 423:435–439
41. Pintana H, Apaijai N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2012) Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci 91:409–414
42. Pipatpiboon N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2012) PPARγ agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term high-fat diets. Endocrinology 153:329–338
43. Saei-Dehkordi SS, Fallah AA, Saei-Dehkordi SS, Kousha S (2012) Chemical composition and antioxidative activity of Echinophora platyloba DC. Essential oil, and its interaction with natural antimicrobials against food-borne pathogens and spoilage organisms. J Food Sci 77:631–637
44. Saravanan S, Pari L (2015) Role of thymol on hyperglycemia and hyperlipidemia in high fat diet-induced type 2 diabetic C57BL/6 J mice. Eur J Pharmacol 761:279–287
45. Saravanan S, Pari L (2016) Protective effect of thymol on high fat diet induced diabetic nephropathy in C57BL/6 J mice. Chem Biol Interact 245:1–11
46. Sosa-Ortiz AL, Acosta-Castillo I, Prince MJ (2012) Epidemiology of dementias and Alzheimer’s disease. Arch Med Res 43:600–608
47. Steculorum SM, Solas M, Brüning JC (2014) The paradox of neuronal insulin action and resistance in the development of aging-associated diseases. Alzheimers Dement 10:3–11
48. Tucsek Z, Toth P, Sosnowska D, Gautam T, Mitschelen M, Koller A, Szalai G, Sonntag WE, Ungvari Z, Csiszar A (2014) Obesity in aging exacerbates blood-brain barrier disruption, neuroinflammation, and oxidative stress in the mouse hippocampus: effects on expression of genes involved in beta-amyloid generation and Alzheimer’s disease. J Gerontol A Biol Sci Med Sci 69:1212–1226
49. Verdile G, Keane KN, Cruzat VF, Medic S, Sabale M, Rowles J, Wijesekara N, Martins RN, Fraser PE, Newsholme P (2015) Inflammation and oxidative stress: the molecular connectivity between insulin resistance, obesity, and Alzheimer’s disease. Mediat Inflamm 2015:17
50. Wang X, Gu C, He W, Ye X, Chen H, Zhang X, Hai C (2012) Glucose oxidase induces insulin resistance via influencing multiple targets in vitro and in vivo: the central role of oxidative stress. Biochimie 94:1705–1717
51. Wang Y, Miao Y, Mir AZ, Cheng L, Wang L, Zhao L, Cui Q, Zhao W, Wang H (2016) Inhibition of beta-amyloid-induced neurotoxicity by pinocembrin through Nrf2/HO-1 pathway in SH-SY5Y cells. J Neurol Sci 368:223–230
52. Yin Z, Yu H, Chen S, Ma C, Ma X, Xu L, Ma Z, Qu R, Ma S (2015) Asiaticoside attenuates diabetes-induced cognition deficits by regulating PI3K/Akt/NF-κB pathway. Behav Brain Res 292:288–299
53. Youdim KA, Deans SG (2000) Effect of thyme oil and thymol dietary supplementation on the antioxidant status and fatty acid composition of the ageing rat brain. Br J Nutr 83:87–93
54. Zheng W, Huang LZ, Zhao L, Wang B, Xu HB, Wang GY, Wang ZL, Zhou H (2008) Superoxide dismutase activity and malondialdehyde level in plasma and morphological evaluation of acute severe hemorrhagic shock in rats. Am J Emerg Med 26:54–58
55. Zou Y, Hong B, Fan L, Zhou L, Liu Y, Wu Q, Zhang X, Dong M (2013) Protective effect of puerarin against beta-amyloid-induced oxidative stress in neuronal cultures from rat hippocampus: involvement of the GSK-3β/Nrf2 signaling pathway. Free Radic Res 47:55–63