Preventive Effects of Different Aerobic Exercise Intensities on the Decline of Cognitive Function in High-Fat Diet-Induced Obese Growing Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals and Obesity Induction
2.2. Exercise Intervention
2.3. Cognitive Function Test
2.4. Protein Level Analysis
2.5. Statistical Analysis
3. Results
3.1. HFD Caused Obesity and Increased Fat Mass, but That Was Prevented by Regular Exercise
3.2. Lipolytic Enzymes in Adipose Tissue Increased in Training Groups, and High-Intensity Training Was More Effective than That of Low-Intensity
3.3. Cognitive Function and Neurotrophic Factors Were Improved by Regular Exercise Regardless of the Exercise Intensity
4. Discussion
5. Conclusions
Funding
Conflicts of Interest
References
- Langin, D. Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome. Pharmacol. Res. 2006, 53, 482–491. [Google Scholar] [CrossRef]
- Boitard, C.; Cavaroc, A.; Sauvant, J.; Aubert, A.; Castanon, N.; Layé, S.; Ferreira, G. Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain. Behav. Immun. 2014, 40, 9–17. [Google Scholar] [CrossRef] [PubMed]
- Stevens, G.A.; Singh Lu, Y.; Danaei, G.; Lin, J.K.; Finucane, M.M.; Bahalim, A.N.; McIntire, R.K.; Gutierrez, H.R.; Cowan, M.; Paciorek, C.J.; et al. Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Body Mass Index). National, regional, and global trends in adult overweight and obesity prevalences. Popul. Health Metr. 2012, 10, 22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Güngör, N.K. Overweight and obesity in children and adolescents. J. Clin. Res. Pediatr. Endocrinol. 2014, 6, 129–143. [Google Scholar] [CrossRef] [PubMed]
- Spear, L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24, 417–463. [Google Scholar] [CrossRef]
- Biegler, R.; McGregor, A.; Krebs, J.R.; Healy, S.D. A larger hippocampus is associated with longer-lasting spatial memory. Proc. Natl. Acad. USA. 2001, 98, 6941–6944. [Google Scholar] [CrossRef] [Green Version]
- Phillips, C. Lifestyle Modulators of Neuroplasticity: How Physical Activity, Mental Engagement, and Diet Promote Cognitive Health during Aging. Neural. Plast. 2017, 2017, 3589271. [Google Scholar] [CrossRef] [PubMed]
- Kruk-Slomka, M.; Boguszewska-Czubara, A.; Slomka, T.; Budzynska, B.; Biala, G. Correlations between the Memory-Related Behavior and the Level of Oxidative Stress Biomarkers in the Mice Brain, Provoked by an Acute Administration of CB Receptor Ligands. Neural. Plast. 2016, 2016, 9815092. [Google Scholar] [CrossRef] [Green Version]
- Skaper, S.D. Neurotrophic Factors: An Overview. Methods Mol. Biol. 2018, 1727, 1–17. [Google Scholar]
- Dreyfus, C.F. Effects of nerve growth factor on cholinergic brain neurons. Trends Pharmacol. Sci. 1989, 10, 145–149. [Google Scholar] [CrossRef]
- Deinhardt, K.; Chao, M.V. Shaping neurons: Long and short range effects of mature and proBDNF signalling upon neuronal structure. Neuropharmacology 2014, 76, 603–609. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosenthal, A.; Goeddel, D.V.; Nguyen, T.; Lewis, M.; Shih, A.; Laramee, G.R.; Nikolics, K.; Winslow, J.W. Primary structure and biological activity of a novel human neurotrophic factor. Neuron 1990, 4, 767–773. [Google Scholar] [CrossRef]
- Kucera, J.; Fan, G.; Jaenisch, R.; Linnarsson, S.; Ernfors, P. Dependence of developing group la afferents on neurotrophin-3. J. Comp. Neurol. 1995, 363, 307–320. [Google Scholar] [CrossRef] [PubMed]
- Park, H.S.; Cho, H.S.; Kim, T.W. Physical exercise promotes memory capability by enhancing hippocampal mitochondrial functions and inhibiting apoptosis in obesity-induced insulin resistance by high fat diet. Metab. Brain Dis. 2018, 33, 283–292. [Google Scholar] [CrossRef]
- Cheng, J.; Chen, L.; Han, S.; Qin, L.; Chen, N.; Wan, Z. Treadmill Running and Rutin Reverse High Fat Diet Induced Cognitive Impairment in Diet Induced Obese Mice. J. Nutr. Health Aging. 2016, 20, 503–508. [Google Scholar] [CrossRef]
- Coetsee, C.; Terblanche, E. The effect of three different exercise training modalities on cognitive and physical function in a healthy older population. Eu.r Rev. Aging Phys. Act. 2017, 10, 14:13. [Google Scholar] [CrossRef]
- Cui, M.Y.; Lin, Y.; Sheng, J.Y.; Zhang, X.; Cui, R.J. Exercise Intervention Associated with Cognitive Improvement in Alzheimer’s Disease. Neural. Plast. 2018, 11, 9234105. [Google Scholar] [CrossRef]
- Da Silva, F.C.; Iop, R.D.R.; de Oliveira, L.C.; Boll, A.M.; de Alvarenga, J.G.S.; Gutierres Filho, P.J.B.; de Melo, L.M.A.B.; Xavier, A.J.; da Silva, R. Effects of physical exercise programs on cognitive function in Parkinson’s disease patients: A systematic review of randomized controlled trials of the last 10 years. PLoS ONE 2018, 13, e0193113. [Google Scholar] [CrossRef] [Green Version]
- van Praag, H.; Shubert, T.; Zhao, C.; Gage, F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25, 8680–8685. [Google Scholar] [CrossRef]
- Birch, A.M.; McGarry, N.B.; Kelly, A.M. Short-term environmental enrichment, in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time-dependent manner. Hippocampus 2013, 23, 437–450. [Google Scholar] [CrossRef]
- Woo, J.; Shin, K.O.; Park, S.Y.; Jang, K.S.; Kang, S. Effects of exercise and diet change on cognition function and synaptic plasticity in high fat diet induced obese rats. Lipids Health Dis. 2013, 12, 144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boitard, C.; Etchamendy, N.; Sauvant, J.; Aubert, A.; Tronel, S.; Marighetto, A.; Layé, S.; Ferreira, G. Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice. Hippocampus 2012, 22, 2095–2100. [Google Scholar] [CrossRef] [PubMed]
- Hopkins, M.E.; Nitecki, R.; Bucci, D.J. Physical exercise during adolescence versus adulthood: Differential effects on object recognition memory and brain-derived neurotrophic factor levels. Neuroscience 2011, 194, 84–94. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aucouturier, J.; Baker, J.S.; Duché, P. Fat and carbohydrate metabolism during submaximal exercise in children. Sport Med. 2008, 38, 213–238. [Google Scholar] [CrossRef]
- Boutcher, S.H. High-intensity intermittent exercise and fat loss. J. Obes. 2011, 2011, 868305. [Google Scholar] [CrossRef] [Green Version]
- Lattier, G.; Millet, G.Y.; Martin, A.; Martin, V. Fatigue and recovery after high-intensity exercise part I: Neuromuscular fatigue. Int. J. Sports Med. 2004, 25, 450–456. [Google Scholar] [CrossRef]
- Ferreira, J.C.; Rolim, N.P.; Bartholomeu, J.B.; Gobatto, C.A.; Kokubun, E.; Brum, P.C. Maximal lactate steady state in running mice: Effect of exercise training. Clin. Exp. Pharmacol. Physiol. 2007, 34, 760–765. [Google Scholar] [CrossRef]
- Duarte, J.M.; Agostinho, P.M.; Carvalho, R.A.; Cunha, R.A. Caffeine consumption prevents diabetes-induced memory impairment and synaptotoxicity in the hippocampus of NONcZNO10/LTJ mice. PLoS ONE 2012, 7, e21899. [Google Scholar] [CrossRef] [Green Version]
- Lalonde, R. The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 2002, 26, 91–104. [Google Scholar] [CrossRef]
- Sarnyai, Z.; Sibille, E.L.; Pavlides, C.; Fenster, R.J.; McEwen, B.S.; Toth, M. Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin (1A) receptors. Proc. Natl. Acad. Sci. USA 2000, 97, 14731–14736. [Google Scholar] [CrossRef] [Green Version]
- Kraeuter, A.K.; Guest, P.C.; Sarnyai, Z. The Y-Maze for Assessment of Spatial Working and Reference Memory in Mice. Pre-Clin. Models. 2019, 1916, 105–111. [Google Scholar]
- Bae, J.Y. Aerobic Exercise Increases Meteorin-Like Protein in Muscle and Adipose Tissue of Chronic High-Fat Diet-Induced Obese Mice. Biomed Res. Int. 2018, 2018, 6283932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dias, K.A.; Coombes, J.S.; Green, D.J.; Gomersall, S.R.; Keating, S.E.; Tjonna, A.E.; Hollekim-Strand, S.M.; Hosseini, M.S.; Ro, T.B.; Haram, M.; et al. Effects of exercise intensity and nutrition advice on myocardial function in obese children and adolescents: A multicentre randomised controlled trial study protocol. BMJ Open. 2016, 6, e010929. [Google Scholar] [CrossRef] [Green Version]
- Frühbeck, G.; Méndez-Giménez, L.; Fernández-Formoso, J.A.; Fernández, S.; Rodríguez, A. Regulation of adipocyte lipolysis. Nutr. Res. Rev. 2014, 27, 63–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bae, J.Y.; Woo, J.; Kang, S.; Shin, K.O. Effects of detraining and retraining on muscle energy-sensing network and meteorin-like levels in obese mice. Lipids Health Dis. 2018, 17, 97. [Google Scholar] [CrossRef] [Green Version]
- Duncan, R.E.; Ahmadian, M.; Jaworski, K.; Sarkadi-Nagy, E.; Sul, H.S. Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 2007, 27, 79–101. [Google Scholar] [CrossRef] [Green Version]
- Knechtle, B. Exercise intensity and fat burning--theoretical principles and practical considerations. Praxis 2002, 91, 915–919. [Google Scholar] [CrossRef] [PubMed]
- Friedlander, A.L.; Casazza, G.A.; Horning, M.A.; Usaj, A.; Brooks, G.A. Endurance training increases fatty acid turnover, but not fat oxidation, in young men. J. Appl. Physiol. 1999, 86, 2097–2105. [Google Scholar] [CrossRef]
- Lennox, R.; Moffett, R.C.; Porter, D.W.; Irwin, N.; Gault, V.A.; Flatt, P.R. Effects of glucose-dependent insulinotropic polypeptide receptor knockout and a high-fat diet on cognitive function and hippocampal gene expression in mice. Mol. Med. Rep. 2015, 12, 1544–1548. [Google Scholar] [CrossRef] [Green Version]
- Zafonte, R.D.; Shih, S.L.; Iaccarino, M.A.; Tan, C.O. Neurologic benefits of sports and exercise. Handb. Clin. Neurol. 2018, 158, 463–471. [Google Scholar]
- Fordyce, D.E.; Farrar, R.P. Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav. Brain Res. 1991, 46, 123–133. [Google Scholar] [CrossRef]
- Van Praag, H. Neurogenesis and exercise: Past and future directions. Neuromolecular Med. 2008, 10, 128–140. [Google Scholar] [CrossRef] [PubMed]
- Sun, L.N.; Li, X.L.; Wang, F.; Zhang, J.; Wang, D.D.; Yuan, L.; Wu, M.N.; Wang, Z.J.; Qi, J.S. High-intensity treadmill running impairs cognitive behavior and hippocampal synaptic plasticity of rats via activation of inflammatory response. J. Neurosci. Res. 2017, 95, 1611–1620. [Google Scholar] [CrossRef] [PubMed]
- Baker, J.S.; Bailey, D.M.; Hullin, D.; Young, I.; Davies, B. Metabolic implications of resistive force selection for oxidative stress and markers of muscle damage during 30 s of high-intensity exercise. Eur. J. Appl. Physiol. 2004, 92, 321–327. [Google Scholar] [CrossRef] [PubMed]
Period (Week) | Speed (m/min) | Time (Min) | Frequency (Day/Week) | Grade (°) | ||
---|---|---|---|---|---|---|
Low Intensity | High Intensity | |||||
1 | Adaptation | 5 | 5 | 5–20 | 5 | 0 |
2~8 | Exercise | 5 | 5 | 10 | 5 | 0 |
8 | 14 | 30 | ||||
5 | 5 | 10 |
© 2020 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bae, J.Y. Preventive Effects of Different Aerobic Exercise Intensities on the Decline of Cognitive Function in High-Fat Diet-Induced Obese Growing Mice. Medicina 2020, 56, 331. https://doi.org/10.3390/medicina56070331
Bae JY. Preventive Effects of Different Aerobic Exercise Intensities on the Decline of Cognitive Function in High-Fat Diet-Induced Obese Growing Mice. Medicina. 2020; 56(7):331. https://doi.org/10.3390/medicina56070331
Chicago/Turabian StyleBae, Ju Yong. 2020. "Preventive Effects of Different Aerobic Exercise Intensities on the Decline of Cognitive Function in High-Fat Diet-Induced Obese Growing Mice" Medicina 56, no. 7: 331. https://doi.org/10.3390/medicina56070331