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, Behavior, and Immunity

Volumn 57, Issue , 2016, Pages 347-359

  Cai, Ming ^a   Wang, Hong ^a,b   Li, Jing jing ^a   Zhang, Yun Li ^a   Xin, Lei ^a   Li, Feng ^a   Lou, Shu jie ^a  

^a SHANGHAI UNIVERSITY OF SPORT   (China)

^b SHANGHAI UNIVERSITY OF MEDICINE AND HEALTH SCIENCES   (China)

Author keywords

Aerobic exercise; BDNF; High fat diet; Hippocampal endoplasmic reticulum stress; Obese SD rat; SYN

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CRYOPYRIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FATTY ACID TRANSPORT PROTEIN 1; FATTY ACID TRANSPORTER; GLUCOSE TRANSPORTER 3; HEME OXYGENASE 1; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AEROBIC EXERCISE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; FAT MASS; HIPPOCAMPUS; HYPERGLYCEMIA; HYPERLIPIDEMIA; INTRACELLULAR SIGNALING; LIPID DIET; MALE; METABOLIC DISORDER; NERVE CELL PLASTICITY; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; TREADMILL EXERCISE; ANIMAL; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; HYPERGLYCEMIA; HYPERLIPIDEMIAS; MALE; NEURONAL PLASTICITY; OBESITY; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTOPHYSIN;

EID: 84969506648     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.05.010     Document Type: Article

References (70)

1. Barker, P.A., Whither proBDNF?. Nat. Neurosci. 12 (2009), 105–106.
2. Barrientos, R.M., Sprunger, D.B., Campeau, S., Watkins, L.R., Rudy, J.W., Maier, S.F., BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1β administration. J. Neuroimmunol. 155 (2004), 119–126.
3. Benarroch, E.E., Insulin-like growth factors in the brain and their potential clinical implications. Neurology 79 (2012), 2148–2153.
4. Bocarsly, M.E., Fasolino, M., Kane, G.A., LaMarca, E.A., Kirschen, G.W., Karatsoreos, I.N., McEwen, B.S., Gould, E., Obesity diminishes synaptic markers, alters microglial morphology, and impairs cognitive function. Proc. Natl. Acad. Sci. USA 112 (2015), 15731–15736.
5. Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Laye, 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. 40 (2014), 9–17.
6. Calvo-Ochoa, E., Hernández-Ortega, K., Ferrera, P., Morimoto, S., Arias, C., Short-term high-fat-and-fructose feeding produces insulin signaling alterations accompanied by neurite and synaptic reduction and astroglial activation in the rat hippocampus. J. Cereb. Blood Flow Metab. 34 (2014), 1001–1008.
7. Cao, S.S., Kaufman, R.J., Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid. Redox Signal. 21 (2014), 396–413.
8. Chen, L., Miyamoto, Y., Furuya, K., Mori, N., Sokabe, M., PREGS induces LTP in the hippocampal dentate gyrus of adult rats via the tyrosine phosphorylation of NR2B coupled to ERK/CREB [corrected] signaling. J. Neurophysiol. 98 (2007), 1538–1548.
9. Cnop, M., Foufelle, F., Velloso, L.A., Endoplasmic reticulum stress, obesity and diabetes. Trends Mol. Med. 18 (2012), 59–68.
10. Deguil, J., Pineau, L., Rowland Snyder, E.C., Dupont, S., Beney, L., Gil, A., Frapper, G., Ferreira, T., Modulation of lipid-induced ER stress by fatty acid shape. Traffic 12 (2011), 349–362.
11. Dinel, A.L., André, C., Aubert, A., Ferreira, G., Layé, S., Castanon, N., Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One, 6, 2011, e24325.
12. Disanzo, B.L., You, T., Effects of exercise training on indicators of adipose tissue angiogenesis and hypoxia in obese rats. Metab. Clin. Exp. 63 (2014), 452–455.
13. Doyle, K.M., Kennedy, D., Gorman, A.M., Gupta, S., Healy, S.J., Samali, A., Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders. J. Cell. Mol. Med. 15 (2011), 2025–2039.
14. Dwyer, D.S., Vannucci, S.J., Simpson, I.A., Expression, regulation, and functional role of glucose transporters (GLUTs) in brain. Int. Rev. Neurobiol. 51 (2002), 159–188.
15. Ellis, J.M., Wong, G.W., Wolfgang, M.J., Acyl coenzyme A thioesterase 7 regulates neuronal fatty acid metabolism to prevent neurotoxicity. Mol. Cell. Biol. 33 (2013), 1869–1882.
16. Fujita, K., Yamafuji, M., Nakabeppu, Y., Noda, M., Therapeutic approach to neurodegenerative diseases by medical gases: focusing on redox signaling and related antioxidant enzymes. Oxid. Med. Cell. Longevity, 2012, 2012, 324256.
17. Ge, H.W., Hu, W.W., Ma, L.L., Kong, F.J., Endoplasmic reticulum stress pathway mediates isoflurane-induced neuroapoptosis and cognitive impairments in aged rats. Physiol. Behav. 151 (2015), 16–23.
18. Gomes da Silva, S., Simões, P.S., Mortara, R.A., Scorza, F.A., Cavalheiro, E.A., da Graça Naffah-Mazzacoratti, M., Arida, R.M., Exercise-induced hippocampal anti-inflammatory response in aged rats. J. Neuroinflammation, 10, 2013, 61.
19. Han, F., Yan, S., Shi, Y., Single-prolonged stress induces endoplasmic reticulum-dependent apoptosis in the hippocampus in a rat model of post-traumatic stress disorder. PLoS One, 8, 2013, e69340.
20. Haneklaus, M., O'Neill, L.A., NLRP3 at the interface of metabolism and inflammation. Immunol. Rev. 265 (2015), 53–62.
21. Hao, S., Dey, A., Yu, X., Stranahan, A.M., Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav. Immun. 51 (2016), 230–239.
22. Hardingham, G.E., Arnold, F.J., Bading, H., Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4 (2001), 261–267.
23. Hashimoto, K., Sigma-1 receptor chaperone and brain-derived neurotrophic factor: emerging links between cardiovascular disease and depression. Prog. Neurobiol. 100 (2013), 15–29.
24. Johnson, J.A., Johnson, D.A., Kraft, A.D., Calkins, M.J., Jakel, R.J., Vargas, M.R., Chen, P.-C., The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 1147 (2008), 61–69.
25. Kanneganti, T.D., Dixit, V.D., Immunological complications of obesity. Nat. Immunol. 13 (2012), 707–712.
26. Kim, S., Joe, Y., Jeong, S.O., Zheng, M., Back, S.H., Park, S.W., Ryter, S.W., Chung, H.T., Endoplasmic reticulum stress is sufficient for the induction of IL-1b production via activation of the NF-iB and inflammasome pathways. Innate Immun. 20 (2014), 799–815.
27. Langdon, K.D., Clarke, J., Corbett, D., Long-term exposure to high fat diet is bad for your brain: exacerbation of focal ischemic brain injury. Neuroscience 182 (2011), 82–87.
28. Leal, G., Comprido, D., Duarte, C.B., BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology 76:Pt C (2014), 639–656.
29. Li, Y., Li, J., Li, S., Li, Y., Wang, X., Liu, B., Fu, Q., Ma, S., Curcumin attenuates glutamate neurotoxicity in the hippocampus by suppression of ER stress-associated TXNIP/NLRP3 inflammasome activation in a manner dependent on AMPK. Toxicol. Appl. Pharmacol. 286 (2015), 53–63.
30. Liang, L., Chen, J., Zhan, L., Lu, X., Sun, X., Sui, H., Zheng, L., Xiang, H., Zhang, F., Endoplasmic reticulum stress impairs insulin receptor signaling in the brains of obese rats. PLoS One, 10, 2015, e0126384.
31. Liu, R.Y., Zhang, Y., Coughlin, B.L., Cleary, L.J., Byrne, J.H., Doxorubicin attenuates serotonin-induced long-term synaptic facilitation by phosphorylation of p38 mitogen-activated protein kinase. J. Neurosci. 34 (2014), 13289–13300.
32. Liu, Z., Patil, I.Y., Jiang, T., Sancheti, H., Walsh, J.P., Stiles, B.L., Yin, F., Cadenas, E., High-fat diet induces hepatic insulin resistance and impairment of synaptic plasticity. PLoS One, 10, 2015, e0128274.
33. Man, S.M., Kanneganti, T.D., Regulation of inflammasome activation. Immunol. Rev. 265 (2015), 6–21.
34. Mandl, J., Meszaros, T., Banhegyi, G., Hunyady, L., Csala, M., Endoplasmic reticulum: nutrient sensor in physiology and pathology. Trends Endocrinol. Metab. TEM 20 (2009), 194–201.
35. McEwen, B.S., Reagan, L.P., Glucose transporter expression in the central nervous system: relationship to synaptic function. Eur. J. Pharmacol. 490 (2004), 13–24.
36. Meeusen, R., Exercise, nutrition and the brain. Sports Med. 44:Suppl 1 (2014), S47–S56.
37. Menu, P., Mayor, A., Zhou, R., Tardivel, A., Ichijo, H., Mori, K., Tschopp, J., ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis., 3, 2012, e261.
38. Mergenthaler, P., Lindauer, U., Dienel, G.A., Meisel, A., Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci. 36 (2013), 587–597.
39. Mitchell, R.W., On, N.H., Del Bigio, M.R., Miller, D.W., Hatch, G.M., Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. J. Neurochem. 117 (2011), 735–746.
40. Moosavi, F., Hosseini, R., Saso, L., Firuzi, O., Modulation of neurotrophic signaling pathways by polyphenols. Drug Des. Dev. Ther. 10 (2015), 23–42.
41. Oakes, S.A., Papa, F.R., The role of endoplasmic reticulum stress in human pathology. Annu. Rev. Pathol. 10 (2015), 173–194.
42. Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R.O., Görgün, C.Z., Hotamisligil, G.S., Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313 (2006), 1137–1140.
43. Park, H.R., Park, M., Choi, J., Park, K.Y., Chung, H.Y., Lee, J., A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci. Lett. 482 (2010), 235–239.
44. Patterson, S.L., Immune dysregulation and cognitive vulnerability in the aging brain: interactions of microglia, IL-1β, BDNF and synaptic plasticity. Neuropharmacology 96:Pt A (2015), 11–18.
45. Pinnock, S.B., Blake, A.M., Platt, N.J., Herbert, J., The roles of BDNF, pCREB and Wnt3a in the latent period preceding activation of progenitor cell mitosis in the adult dentate gyrus by fluoxetine. PLoS One, 5, 2010, e13652.
46. Pistell, P.J., Morrison, C.D., Gupta, S., Knight, A.G., Keller, J.N., Ingram, D.K., Bruce-Keller, A.J., Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 219 (2010), 25–32.
47. Prieto, G.A., Snigdha, S., Baglietto-Vargas, D., Smith, E.D., Berchtold, N.C., Tong, L., Ajami, D., LaFerla, F.M., Rebek, J. Jr., Cotman, C.W., Synapse-specific IL-1 receptor subunit reconfiguration augments vulnerability to IL-1β in the aged hippocampus. Proc. Natl. Acad. Sci. USA 112 (2015), E5078–E5087.
48. Reagan, L.P., Magariños, A.M., Yee, D.K., Swzeda, L.I., Van Bueren, A., McCall, A.L., McEwen, B.S., Oxidative stress and HNE conjugation of GLUT3 are increased in the hippocampus of diabetic rats subjected to stress. Brain Res. 862 (2000), 292–300.
49. Roussel, B.D., Kruppa, A.J., Miranda, E., Crowther, D.C., Lomas, D.A., Marciniak, S.J., Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol. 12 (2013), 105–118.
50. Salkovic-Petrisic, M., Osmanovic-Barilar, J., Knezovic, A., Hoyer, S., Mosetter, K., Reutter, W., Long-term oral galactose treatment prevents cognitive deficits in male Wistar rats treated intracerebroventricularly with streptozotocin. Neuropharmacology 77 (2014), 68–80.
51. Santiago, J.F., Carvalho, F.F., Perosa, S.R., Siliano, M.R., Cruz, J.W., Fernandes, M.J., Cavalheiro, E.A., Amado, D., da Graça Naffah-Mazzacoratti, M., Effect of glycemic state in rats submitted to status epilepticus during development. Arq. Neuropsiquiatr. 64:2A (2006), 233–239.
52. Santos, A.R., Comprido, D., Duarte, C.B., Regulation of local translation at the synapse by BDNF. Prog. Neurobiol. 92 (2010), 505–516.
53. Schroder, K., Tschopp, J., The inflammasomes. Cell 140 (2010), 821–832.
54. Shefer, G., Marcus, Y., Stern, N., Is obesity a brain disease?. Neurosci. Biobehav. Rev. 37 (2013), 2489–2503.
55. Sims-Robinson, C., Bakeman, A., Glasser, R., Boggs, J., Pacut, C., Feldman, E.L., The role of endoplasmic reticulum stress in hippocampal insulin resistance. Exp. Neurol., 2016 pii: S0014-4886(16)30007-30003.
56. Sobesky, J.L., Barrientos, R.M., De May, H.S., Thompson, B.M., Weber, M.D., Watkins, L.R., Maier, S.F., High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1β, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism. Brain Behav. Immun. 42 (2014), 22–32.
57. Son, Y., Lee, J.H., Chung, H.T., Pae, H.O., Therapeutic roles of heme oxygenase-1 in metabolic diseases: curcumin and resveratrol analogues as possible inducers of heme oxygenase-1. Oxid. Med. Cell. Longevity, 2013, 2013, 639541.
58. Sour, S., Belarbi, M., Sari, N., Benammar, C.H., Baghdad, C.H., Visioli, F., Argan oil reduces, in rats, the high fat diet-induced metabolic effects of obesity. Nutr. Metab. Cardiovasc. Dis. 25 (2015), 382–387.
59. Tabas, I., Ron, D., Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13 (2011), 184–190.
60. Tong, L., Prieto, G.A., Kramar, E.A., Smith, E.D., Cribbs, D.H., Lynch, G., Cotman, C.W., Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1beta via p38 mitogen-activated protein kinase. J. Neurosci. 32 (2012), 17714–17724.
61. Tsou, Y.H., Shih, C.T., Ching, C.H., Huang, J.Y., Jen, C.J., Yu, L., Kuo, Y.M., Wu, F.S., Chuang, J.I., Treadmill exercise activates Nrf2 antioxidant system to protect the nigrostriatal dopaminergic neurons from MPP+ toxicity. Exp. Neurol. 263 (2015), 50–62.
62. van Praag, H., Fleshner, M., Schwartz, M.W., Mattson, M.P., Exercise, energy intake, glucose homeostasis, and the brain. J. Neurosci. 34 (2014), 15139–15149.
63. Wang, S.P., Yang, H., Wu, J.W., Gauthier, N., Fukao, T., Mitchell, G.A., Metabolism as a tool for understanding human brain evolution: lipid energy metabolism as an example. J. Hum. Evol. 77 (2014), 41–49.
64. Won, J.C., Jang, P.G., Namkoong, C., Koh, E.H., Kim, S.K., Park, J.Y., Lee, K.U., Kim, M.S., Central administration of an endoplasmic reticulum stress inducer inhibits the anorexigenic effects of leptin and insulin. Obesity 17 (2009), 1861–1865.
65. Wu, J., Kaufman, R.J., From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13 (2006), 374–384.
66. Wu, Q., Ortegon, A.M., Tsang, B., Doege, H., Feingold, K.R., Stahl, A., FATP1 is an insulin-sensitive fatty acid transporter involved in diet-induced obesity. Mol. Cell. Biol. 26 (2006), 3455–3467.
67. Yan, L., Chen, Y., Li, W., Huang, X., Badie, H., Jian, F., Huang, T., Zhao, Y., Cohen, S.N., Li, L., Zhang, Y.W., Luo, H., Tu, S., Xu, H., RPS23RG1 reduces Aβ oligomer-induced synaptic and cognitive deficits. Sci. Rep., 6, 2016, 18668.
68. Yu, T., Liu, R., Li, M., Li, X., Qiang, O., Huang, W., Tang, C., Effects of octreotide on fatty infiltration of the pancreas in high-fat diet induced obesity rats. Wei Sheng Yan Jiu 43 (2014), 186–192.
69. Zhong, Y., Zhu, Y., He, T., Li, W., Yan, H., Miao, Y., Rolipram-induced improvement of cognitive function correlates with changes in hippocampal CREB phosphorylation, BDNF and Arc protein levels. Neurosci. Lett. 610 (2016), 171–176.
70. Zhou, X., Han, D., Xu, R., Li, S., Wu, H., Qu, C., Wang, F., Wang, X., Zhao, Y., A model of metabolic syndrome and related diseases with intestinal endotoxemia in rats fed a high fat and high sucrose diet. PLoS One, 9, 2014, e115148.