High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling - PubMed (original) (raw)
High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling
Christopher D Morrison et al. J Neurochem. 2010 Sep.
Abstract
Long term consumption of a high fat diet (HFD) contributes to increased morbidity and mortality. Yet the specific effects of HFD consumption on brain aging are poorly understood. In the present study 20-month old male C57Bl/6 mice were fed either 'western diet' (41% fat), very high fat lard diet (60% fat), or corresponding control diets for 16 weeks and then assessed for changes in metabolism and brain homeostasis. Although both HFDs increased adiposity and fasting blood glucose, only the high fat lard diet increased age-related oxidative damage (protein carbonyls) and impaired retention in the behavioral test. This selective increase in oxidative damage and cognitive decline was also associated with a decline in NF-E2-related factor 2 (Nrf2) levels and Nrf2 activity, suggesting a potential role for decreased antioxidant response. Taken together, these data suggest that while adiposity and insulin resistance following HFD consumption are linked to increased morbidity, the relationship between these factors and brain homeostasis during aging is not a linear relationship. More specifically, these data implicate impaired Nrf2 signaling and increased cerebral oxidative stress as mechanisms underlying HFD-induced declines in cognitive performance in the aged brain.
© 2010 The Authors. Journal Compilation © 2010 International Society for Neurochemistry.
Figures
Figure 1. Changes in body weight and total adiposity
Twenty-month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or their respective control diets (WD-C,HFL-C) for 16 weeks and analyzed for changes in body weight (A) or total body fat using NMR (B). Data are presented as the mean and S.E.M. from 12 animals per group. *P < 0.01 for each high fat diet vs. its control; †P < 0.01 for HFL vs. WD.
Figure 2. Changes in individual fat pad weight
Twenty month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or the respective control diets (WD-C,HFL-C) for 16 weeks and analyzed for changes in fat pad weight, which were manually dissected and weighed. Animals were analyzed for total fad pad weight (A), retroperitoneal fat pad (B), epididymal fat pad (C), and visceral fat pad weight (D). Data are presented as the mean and S.E.M. from 12 animals per group. *P < 0.01 for each high fat diet vs. its control; †P < 0.01 for HFL vs. WD.
Figure 3. Changes in fasting insulin, glucose, and leptin levels
Twenty month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or the respective control diets (WD-C,HFL-C) for 16 weeks and analyzed for changes in fasting glucose (measured at 13 weeks; A), fasting insulin (B), and fasting leptin levels (C). Data are presented as the mean and S.E.M. from 12 animals per group. *P < 0.01 for each high fat diet vs. its control; †P < 0.01 for HFL vs. WD.
Figure 4. High fat lard, but not Western diet, consumption promotes increased oxidative stress
Twenty month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or the respective control diets (WD-C,HFL-C) for 16 weeks and analyzed for changes in protein oxidation (protein carbonyls) within the hippocampus. Data are presented as the mean and S.E.M. from 8 animals per group. *P < 0.01 for HFL vs. its control diet.
Figure 5. High fat lard, but not Western diet, consumption promotes decreases in Nrf2 levels and Nrf2 DNA binding activity
Twenty month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or the respective control diets (WD-C,HFL-C) for 16 weeks and analyzed for changes in Nrf2 protein levels (A), in the NRF2 responsive proteins HO-1 and NQO-1 (B), or changes in Nrf2 DNA binding activity (C). *P < 0.01 for HFL vs. control.
Figure 6. High fat lard, but not Western diet, consumption promotes increased cognitive decline
Twenty month old male C57Bl/6 mice were placed on Western diet (WD), High Fat Lard diet (HFL), or the respective control diets (WD-C,HFL-C) and cognitive performance was assessed in a 14-Unit T-maze. A. Mean errors during the acquisition training across 15 trials (collapsed into 3 trial blocks). B. Mean errors during the final acquisition trial. C. Mean errors during the retention trial, 7 days following acquisition. *P < 0.05 vs control.
Similar articles
- Thymol improves high-fat diet-induced cognitive deficits in mice via ameliorating brain insulin resistance and upregulating NRF2/HO-1 pathway.
FangFang, Li H, Qin T, Li M, Ma S. FangFang, et al. Metab Brain Dis. 2017 Apr;32(2):385-393. doi: 10.1007/s11011-016-9921-z. Epub 2016 Oct 20. Metab Brain Dis. 2017. PMID: 27761760 - Nrf2/antioxidant pathway mediates β cell self-repair after damage by high-fat diet-induced oxidative stress.
Abebe T, Mahadevan J, Bogachus L, Hahn S, Black M, Oseid E, Urano F, Cirulli V, Robertson RP. Abebe T, et al. JCI Insight. 2017 Dec 21;2(24):e92854. doi: 10.1172/jci.insight.92854. JCI Insight. 2017. PMID: 29263299 Free PMC article. - Nrf2 Deficiency Exacerbates Obesity-Induced Oxidative Stress, Neurovascular Dysfunction, Blood-Brain Barrier Disruption, Neuroinflammation, Amyloidogenic Gene Expression, and Cognitive Decline in Mice, Mimicking the Aging Phenotype.
Tarantini S, Valcarcel-Ares MN, Yabluchanskiy A, Tucsek Z, Hertelendy P, Kiss T, Gautam T, Zhang XA, Sonntag WE, de Cabo R, Farkas E, Elliott MH, Kinter MT, Deak F, Ungvari Z, Csiszar A. Tarantini S, et al. J Gerontol A Biol Sci Med Sci. 2018 Jun 14;73(7):853-863. doi: 10.1093/gerona/glx177. J Gerontol A Biol Sci Med Sci. 2018. PMID: 29905772 Free PMC article. - Intersection between metabolic dysfunction, high fat diet consumption, and brain aging.
Uranga RM, Bruce-Keller AJ, Morrison CD, Fernandez-Kim SO, Ebenezer PJ, Zhang L, Dasuri K, Keller JN. Uranga RM, et al. J Neurochem. 2010 Jul;114(2):344-61. doi: 10.1111/j.1471-4159.2010.06803.x. Epub 2010 May 6. J Neurochem. 2010. PMID: 20477933 Free PMC article. Review. - The emerging role of IGF-1 deficiency in cardiovascular aging: recent advances.
Ungvari Z, Csiszar A. Ungvari Z, et al. J Gerontol A Biol Sci Med Sci. 2012 Jun;67(6):599-610. doi: 10.1093/gerona/gls072. Epub 2012 Mar 26. J Gerontol A Biol Sci Med Sci. 2012. PMID: 22451468 Free PMC article. Review.
Cited by
- Mixture of Peanut Skin Extract and Fish Oil Improves Memory in Mice via Modulation of Anti-Oxidative Stress and Regulation of BDNF/ERK/CREB Signaling Pathways.
Xiang L, Cao XL, Xing TY, Mori D, Tang RQ, Li J, Gao LJ, Qi JH. Xiang L, et al. Nutrients. 2016 Apr 28;8(5):256. doi: 10.3390/nu8050256. Nutrients. 2016. PMID: 27136583 Free PMC article. - Detrimental effects of a high fat/high cholesterol diet on memory and hippocampal markers in aged rats.
Ledreux A, Wang X, Schultzberg M, Granholm AC, Freeman LR. Ledreux A, et al. Behav Brain Res. 2016 Oct 1;312:294-304. doi: 10.1016/j.bbr.2016.06.012. Epub 2016 Jun 22. Behav Brain Res. 2016. PMID: 27343935 Free PMC article. - Tocotrienols Influence Body Weight Gain and Brain Protein Expression in Long-Term High-Fat Diet-Treated Mice.
Kato Y, Aoki Y, Fukui K. Kato Y, et al. Int J Mol Sci. 2020 Jun 25;21(12):4533. doi: 10.3390/ijms21124533. Int J Mol Sci. 2020. PMID: 32630592 Free PMC article. - The complex relationship between obesity and neurodegenerative diseases: an updated review.
Neto A, Fernandes A, Barateiro A. Neto A, et al. Front Cell Neurosci. 2023 Nov 9;17:1294420. doi: 10.3389/fncel.2023.1294420. eCollection 2023. Front Cell Neurosci. 2023. PMID: 38026693 Free PMC article. Review. - Mitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases.
Giorgi C, Marchi S, Simoes ICM, Ren Z, Morciano G, Perrone M, Patalas-Krawczyk P, Borchard S, Jędrak P, Pierzynowska K, Szymański J, Wang DQ, Portincasa P, Węgrzyn G, Zischka H, Dobrzyn P, Bonora M, Duszynski J, Rimessi A, Karkucinska-Wieckowska A, Dobrzyn A, Szabadkai G, Zavan B, Oliveira PJ, Sardao VA, Pinton P, Wieckowski MR. Giorgi C, et al. Int Rev Cell Mol Biol. 2018;340:209-344. doi: 10.1016/bs.ircmb.2018.05.006. Epub 2018 Jun 22. Int Rev Cell Mol Biol. 2018. PMID: 30072092 Free PMC article. Review.
References
- Barbieri M, Gambardella A, Paolisso G, Varricchio M. Metabolic aspects of the extreme longevity. Exp Gerontol. 2008;43:74–78. - PubMed
- Barbieri M, Rizzo MR, Manzella D, Paolisso G. Age-related insulin resistance: is it an obligatory finding? The lesson from healthy centenarians. Diabetes Metab Res Rev. 2001;17:19–26. - PubMed
- Cecarini V, Gee J, Fioretti E, Amici M, Angeletti M, Eleuteri AM, Keller JN. Protein oxidation and cellular homeostasis: Emphasis on metabolism. Biochim Biophys Acta. 2007;1773:93–104. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- 2P01 AG005119/AG/NIA NIH HHS/United States
- P20 RR021945/RR/NCRR NIH HHS/United States
- 1P30-DK072476/DK/NIDDK NIH HHS/United States
- R03 NS051570/NS/NINDS NIH HHS/United States
- P20-RR021945/RR/NCRR NIH HHS/United States
- P01 AG005119-220011/AG/NIA NIH HHS/United States
- R03-NS051570/NS/NINDS NIH HHS/United States
- P01 AG005119/AG/NIA NIH HHS/United States
- P30 DK072476/DK/NIDDK NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical