Chronic Swimming Exercise Ameliorates Low-Soybean-Oil Diet-Induced Spatial Memory Impairment by Enhancing BDNF-Mediated Synaptic Potentiation in Developing Spontaneously Hypertensive Rats
- 112 Downloads
Exercise and low-fat diets are common lifestyle modifications used for the treatment of hypertension besides drug therapy. However, unrestrained low-fat diets may result in deficiencies of low-unsaturated fatty acids and carry contingent risks of delaying neurodevelopment. While aerobic exercise shows positive neuroprotective effects, it is still unclear whether exercise could alleviate the impairment of neurodevelopment that may be induced by certain low-fat diets. In this research, developing spontaneously hypertensive rats (SHR) were treated with chronic swimming exercise and/or a low-soybean-oil diet for 6 weeks. We found that performance in the Morris water maze was reduced and long-term potentiation in the hippocampus was suppressed by the diet, while a combination treatment of exercise and diet alleviated the impairment induced by the specific low-fat diet. Moreover, the combination treatment effectively increased the expression of brain-derived neurotrophic factor (BDNF) and N-methyl-d-aspartic acid receptor (NMDAR), which were both down-regulated by the low-soybean-oil diet in the hippocampus of developing SHR. These findings suggest that chronic swimming exercise can ameliorate the low-soybean-oil diet-induced learning and memory impairment in developing SHR through the up-regulation of BDNF and NMDAR expression.
KeywordsChronic swimming exercise Low-soybean-oil diet Cognitive function Developing spontaneously hypertensive rats
This research was supported by grants from the Natural Science Foundation of China (Grant Nos. 81501950 and 81672044) and from the Tianjin Research Program of Application Foundation and Advanced Technology (Grant No. 15JCQNJC12000). We thank Tian Xin for special help with conducting the animal experiments and Xiulan Zhao for technical assistance.
Compliance with Ethical Standards
Conflict of interest
The authors declare that they have no conflict of interest.
All animal protocols were approved by the Intramural Ethic Committee of Tianjin Medical University (ethics code: TMUaMEC 2015009), and conformed to the guidelines of the Chinese Council on Animal Protection.
- 1.Leyvraz M, Taffé P, Chatelan A, Paradis G, Tabin R, Bovet P, Bochud M, Chiolero A (2016) Sodium intake and blood pressure in children and adolescents: protocol for a systematic review and meta-analysis. BMJ Open 6(9):e012518. https://doi.org/10.1136/bmjopen-2016-012518 CrossRefPubMedPubMedCentralGoogle Scholar
- 2.Appel LJ, Champagne CM, Harsha DW, Cooper LS, Obarzanek E, Elmer PJ, Stevens VJ, Vollmer WM, Lin PH, Svetkey LP, Stedman SW, Young DR, Writing Group of the PREMIER Collaborative Research Group (2003) Effects of comprehensive lifestyle modification on blood pressure control: main results of the PREMIER clinical trial. JAMA 289(16):2083–2093. https://doi.org/10.1001/jama.289.16.2083 PubMedGoogle Scholar
- 7.Dinoff A, Herrmann N, Swardfager W, Liu CS, Sherman C, Chan S, Lanctôt KL (2016) The effect of exercise training on resting concentrations of peripheral brain-derived neurotrophic factor (BDNF): a meta-analysis. PLoS ONE 11(9):e0163037. https://doi.org/10.1371/journal.pone.0163037 CrossRefPubMedPubMedCentralGoogle Scholar
- 8.Giralt A, Rodrigo T, Martín ED, Gonzalez JR, Milà M, Ceña V, Dierssen M, Canals JM, Alberch J (2009) Brain-derived neurotrophic factor modulates the severity of cognitive alterations induced by mutant huntingtin: involvement of phospholipaseCgamma activity and glutamate receptor expression. Neuroscience 158(4):1234–1250. https://doi.org/10.1016/j.neuroscience.2008.11.024 CrossRefPubMedGoogle Scholar
- 10.Melik E, Babar E, Ozen E, Ozgunen T (2006) Hypofunction of the dorsal hippocampal NMDA receptors impairs retrieval of memory to partially presented foreground context in a single-trial fear conditioning in rats. Eur Neuropsychopharmacol 16(4):241–247. https://doi.org/10.1016/j.euroneuro.2005.07.008 CrossRefPubMedGoogle Scholar
- 11.Vasuta C, Caunt C, James R, Samadi S, Schibuk E, Kannangara T, Titterness AK, Christie BR (2007) Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus 17(12):1201–1208. https://doi.org/10.1002/hipo.20349 CrossRefPubMedGoogle Scholar
- 12.Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR (2004) Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague–Dawley rats in vivo. Neuroscience 124(1):71–79. https://doi.org/10.1016/j.neuroscience.2003.09.029 CrossRefPubMedGoogle Scholar
- 20.Iemitsu M, Miyauchi T, Maeda S, Tanabe T, Takanashi M, Matsuda M, Yamaguchi I (2004) Exercise training improves cardiac function-related gene levels through thyroid hormone receptor signaling in aged rats. Am J Physiol Heart Circ Physiol 286(5):H1696–H1705. https://doi.org/10.1152/ajpheart.00761.2003 CrossRefPubMedGoogle Scholar
- 28.Yin P, Cao AH, Yu L, Guo LJ, Sun RP, Lei GF (2014) ABT-724 alleviated hyperactivity and spatial learning impairment in the spontaneously hypertensive rat model of attention-deficit/ hyperactivity disorder. Neurosci Lett 580:142–146. https://doi.org/10.1016/j.neulet.2014.08.008 CrossRefPubMedGoogle Scholar
- 29.Azimi M, Gharakhanlou R, Naghdi N, Khodadadi D, Heysieattalab S (2018) Moderate treadmill exercise ameliorates amyloid-β-induced learning and memory impairment, possibly via increasing AMPK activity and up-regulation of the PGC-1α/FNDC5/BDNF pathway. Peptides. https://doi.org/10.1016/j.peptides.2017.12.027 PubMedGoogle Scholar
- 30.Jensen V, Rinholm JE, Johansen TJ, Medin T, Storm-Mathisen J, Sagvolden T, Hvalby O, Bergersen LH (2009) N-methyl-d-aspartate receptor subunit dysfunction at hippocampal glutamatergic synapses in an animal model of attention-deficit/hyperactivity disorder. Neuroscience 158(1):353–364. https://doi.org/10.1016/j.neuroscience.2008.05.016 CrossRefPubMedGoogle Scholar
- 32.Knöchel C, Voss M, Grüter F, Alves GS, Matura S, Sepanski B, Stäblein M, Wenzler S, Prvulovic D, Carvalho AF, Oertel-Knöchel V (2015) Omega 3 fatty acids: novel neurotherapeutic targets for cognitive dysfunction in mood disorders and schizophrenia? Curr Neuropharmacol 13(5):663–680CrossRefPubMedPubMedCentralGoogle Scholar
- 33.Nascimento LF, Souza GF, Morari J, Barbosa GO, Solon C, Moura RF, Victório SC, Ignácio-Souza LM, Razolli DS, Carvalho HF, Velloso LA (2016) n-3 fatty acids induce neurogenesis of predominantly POMC-expressing cells in the hypothalamus. Diabetes 65(3):673–686. https://doi.org/10.2337/db15-0008 CrossRefPubMedGoogle Scholar
- 34.Janssen CI, Zerbi V, Mutsaers MP, de Jong BS, Wiesmann M, Arnoldussen IA, Geenen B, Heerschap A, Muskiet FA, Jouni ZE, van Tol EA, Gross G, Homberg JR, Berg BM, Kiliaan AJ (2015) Impact of dietary n-3 polyunsaturated fatty acids on cognition, motor skills and Hippocampal neurogenesis in developing C57BL/6J mice. J Nutr Biochem 26(1):24–35. https://doi.org/10.1016/j.jnutbio.2014.08.002 CrossRefPubMedGoogle Scholar
- 36.Arcego DM, Krolow R, Lampert C, Toniazzo AP, Berlitz C, Lazzaretti C, Schmitz F, Rodrigues AF, Wyse AT, Dalmaz C (2016) Early life adversities or high fat diet intake reduce cognitive function and alter BDNF signaling in adult rats: Interplay of these factors changes these effects. Int J Dev Neurosci 50:16–25. https://doi.org/10.1016/j.ijdevneu.2016.03.001 CrossRefPubMedGoogle Scholar
- 37.Verdelho A, Madureira S, Ferro JM, Baezner H, Blahak C, Poggesi A, Hennerici M, Pantoni L, Fazekas F, Scheltens P, Waldemar G, Wallin A, Erkinjuntti T, Inzitari D, LADIS Study (2012) Physical activity prevents progression for cognitive impairment and vascular dementia: results from the LADIS (Leukoaraiosis and Disability) study. Stroke 43(12):3331–3335. https://doi.org/10.1116/STROKEAHA.112.661793 CrossRefPubMedGoogle Scholar
- 43.Lee JM, Park JM, Song MK, Oh YJ, Kim CJ, Kim YJ (2017) The ameliorative effects of exercise on cognitive impairment and white matter injury from blood–brain barrier disruption induced by chronic cerebral hypoperfusion in adolescent rats. Neurosci Lett 638:83–89. https://doi.org/10.1013/j.neulet.2016.12.018 CrossRefPubMedGoogle Scholar
- 45.Griesbach GS, Hovda DA, Gomez-Pinilla F, Sutton RL (2008) Voluntary exercise or Amphetamine treatment, but not the combination, increases hippocampal brain-derived neurotrophic Factor and synapsin I following cortical contusion injury in rats. Neuroscience 154(2):530–540. https://doi.org/10.1016/j.neuroscience.2008.04.003 CrossRefPubMedPubMedCentralGoogle Scholar
- 46.Fahimi A, Baktir MA, Moghadam S, Mojabi FS, Sumanth K, McNerney MW, Ponnusamy R, Salehi A (2017) Physical exercise induces structural alterations in the hippocampal astrocytes: exploring the role of BDNF-TrkB signaling. Brain Struct Funct 222(4):1797–1808. https://doi.org/10.1007/s00429-016-1308-8 CrossRefPubMedGoogle Scholar
- 47.Ghodrati-Jaldbakhan S, Ahmadalipour A, Rashidy-Pour A, Vafaei AA, Miladi-Gorji H, Alizadeh M (2017) Low- and high-intensity treadmill exercise attenuates chronic morphine-induced anxiogenesis and memory impairment but not reductions in hippocampal BDNF in female rats. Brain Res 1663:20–28. https://doi.org/10.1016/j.brainres.2017.02.024 CrossRefPubMedGoogle Scholar
- 52.Nakai T, Nagai T, Tanaka M, Itoh N, Asai N, Enomoto A, Asai M, Yamada S, Saifullah AB, Sokabe M, Takahashi M, Yamada K (2014) Girdin phosphorylation is crucial for synaptic plasticity and memory: a potential role in the interaction of BDNF/TrkB/Akt signaling with NMDA receptor. J Neurosci 34(45):14995–15008. https://doi.org/10.1523/JNEUROSCI.2228-14.2014 CrossRefPubMedGoogle Scholar