Naringin Improves Neuronal Insulin Signaling, Brain Mitochondrial Function, and Cognitive Function in High-Fat Diet-Induced Obese Mice

Cellular and Molecular Neurobiology

Volumn 35, Issue 7, 2015, Pages 1061-1071

  Wang, Dongmei ^a   Yan, Junqiang ^a   Chen, Jing ^b   Wu, Wenlan ^a   Zhu, Xiaoying ^a   Wang, Yong ^a  

^a HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b ZHENGZHOU UNIVERSITY   (China)

Author keywords

AMPK; Cognitive deficits; High fat diet; Insulin signaling; Mitochondrial dysfunction; Naringin

Indexed keywords

AURANTIIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; FLAVANONE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN MITOCHONDRION; CHOLESTEROL METABOLISM; COGNITION; CONTROLLED STUDY; DIET INDUCED OBESITY; HIPPOCAMPUS; LIPID DIET; MALE; MEMORY; MITOCHONDRIAL MEMBRANE POTENTIAL; MORRIS WATER MAZE TEST; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; MAZE TEST; METABOLISM; MITOCHONDRION; OBESITY; PHYSIOLOGY;

ANIMALS; BRAIN; COGNITION; DIET, HIGH-FAT; FLAVANONES; INSULIN; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OBESITY;

EID: 84942193634     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-015-0201-y     Document Type: Article

References (78)

1. Arnold SE, Lucki I, Brookshire BR, Carlson GC, Browne CA, Kazi H et al (2014) High fat diet produces brain insulin resistance, synaptodendritic abnormalities and altered behavior in mice. Neurobiol Dis 67:79–87
2. Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S (2011) Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol 68:51–57
3. Benedict C, Hallschmid M, Schultes B, Born J, Kern W (2007) Intranasal insulin to improve memory function in humans. Neuroendocrinology 86:136–142
4. Bevins RA, Besheer J (2006) Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc 1:1306–1311
5. Brown MR, Geddes JW, Sullivan PG (2004) Brain region-specific, age-related, alterations in mitochondrial responses to elevated calcium. J Bioenerg Biomembr 36:401–406
6. Buhl ES, Jessen N, Pold R, Ledet T, Flyvbjerg A, Pedersen SB, Pedersen O, Schmitz O, Lund S (2002) Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes 51:2199–2206
7. Chiu SL, Chen CM, Cline HT (2008) Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58:708–719
8. Choi SH, Kim YW, Kim SG (2010) AMPK-mediated GSK3beta inhibition by isoliquiritigenin contributes to protecting mitochondria against iron-catalyzed oxidative stress. Biochem Pharmacol 79:1352–1362
9. Christie JM, Wenthold RJ, Monaghan DT (1999) Insulin causes a transient tyrosine phosphorylation of NR2A and NR2B NMDA receptor subunits in rat hippocampus. J Neurochem 72:1523–1528
10. Clegg DJ, Gotoh K, Kemp C, Wortman MD, Benoit SC, Brown LM, D’Alessio D, Tso P, Seeley RJ, Woods SC (2011) Consumption of a high-fat diet induces central insulin resistance independent of adiposity. Physiol Behav 103:10–16
11. Craft S (2005) Insulin resistance syndrome and Alzheimer’s disease: age- and obesity-related effects on memory, amyloid, and inflammation. Neurobiol Aging 26(Suppl 1):65–69
12. Craft S, Baker LD, Montine TJ, Minoshima S, Watson GS, Claxton A et al (2012) Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch Neurol 69:29–38
13. Dash PK, Orsi SA, Moore AN (2006) Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. J Neurosci 26:8048–8056
14. Dong Y, Zhang M, Wang S, Liang B, Zhao Z, Liu C, Wu M, Choi HC, Lyons TJ, Zou MH (2010) Activation of AMP-activated protein kinase inhibits oxidized LDL-triggered endoplasmic reticulum stress in vivo. Diabetes 59:1386–1396
15. Dong GZ, Jang EJ, Kang SH, Cho IJ, Park SD, Kim SC, Kim YW (2013) Red ginseng abrogates oxidative stress via mitochondria protection mediated by LKB1-AMPK pathway. BMC Complement Altern Med 13:64
16. Dragicevic N, Mamcarz M, Zhu Y, Buzzeo R, Tan J, Arendash GW, Bradshaw PC (2010) Mitochondrial amyloid-beta levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer’s transgenic mice. J Alzheimers Dis 20(Suppl 2):S535–S550
17. Finocchietto PV, Holod S, Barreyro F, Peralta JG, Alippe Y, Giovambattista A, Carreras MC, Poderoso JJ (2011) Defective leptin-AMP-dependent kinase pathway induces nitric oxide release and contributes to mitochondrial dysfunction and obesity in ob/ob mice. Antioxid Redox Signal 15:2395–2406
18. Francis H, Stevenson R (2013) The longer-term impacts of Western diet on human cognition and the brain. Appetite 63:119–128
19. Gaur V, Aggarwal A, Kumar A (2009) Protective effect of naringin against ischemic reperfusion cerebral injury: possible neurobehavioral, biochemical and cellular alterations in rat brain. Eur J Pharmacol 616:147–154
20. Gauthier MS, O’Brien EL, Bigornia S, Mott M, Cacicedo JM, Xu XJ, Gokce N, Apovian C, Ruderman N (2011) Decreased AMP-activated protein kinase activity is associated with increased inflammation in visceral adipose tissue and with whole-body insulin resistance in morbidly obese humans. Biochem Biophys Res Commun 404:382–387
21. Greenwood CE, Winocur G (2005) High-fat diets, insulin resistance and declining cognitive function. Neurobiol Aging 26(Suppl 1):42–45
22. Harmel E, Grenier E, Bendjoudi Ouadda A, El Chebly M, Ziv E, Beaulieu JF, Sane A, Spahis S, Laville M, Levy E (2014) AMPK in the small intestine in normal and pathophysiological conditions. Endocrinology 155:873–888
23. Huang CC, Lee CC, Hsu KS (2004) An investigation into signal transduction mechanisms involved in insulin-induced long-term depression in the CA1 region of the hippocampus. J Neurochem 89:217–231
24. Huang H, Wu K, You Q, Huang R, Li S (2013) Naringin inhibits high glucose-induced cardiomyocyte apoptosis by attenuating mitochondrial dysfunction and modulating the activation of the p38 signaling pathway. Int J Mol Med 32:396–402
25. Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590
26. Jakobsen SN, Hardie DG, Morrice N, Tornqvist HE (2001) 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J Biol Chem 276:46912–46916
27. Johannsen DL, Ravussin E (2009) The role of mitochondria in health and disease. Curr Opin Pharmacol 9:780–786
28. Kanoski SE, Davidson TL (2011) Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol Behav 103:59–68
29. Kern W, Peters A, Fruehwald-Schultes B, Deininger E, Born J, Fehm HL (2001) Improving influence of insulin on cognitive functions in humans. Neuroendocrinology 74:270–280
30. Kim HJ, Song JY, Park HJ, Park HK, Yun DH, Chung JH (2009) Naringin protects against rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Korean J Physiol Pharmacol 13:281–285
31. Kleinridders A, Ferris HA, Cai W, Kahn CR (2014) Insulin action in brain regulates systemic metabolism and brain function. Diabetes 63:2232–2243
32. Kola B, Christ-Crain M, Lolli F, Arnaldi G, Giacchetti G, Boscaro M, Grossman AB, Korbonits M (2008) Changes in adenosine 5′-monophosphate-activated protein kinase as a mechanism of visceral obesity in Cushing’s syndrome. J Clin Endocrinol Metab 93:4969–4973
33. Kraegen EW, Saha AK, Preston E, Wilks D, Hoy AJ, Cooney GJ, Ruderman NB (2006) Increased malonyl-CoA and diacylglycerol content and reduced AMPK activity accompany insulin resistance induced by glucose infusion in muscle and liver of rats. Am J Physiol Endocrinol Metab 290:E471–E479
34. Kumar P, Kumar A (2010) Protective effect of hesperidin and naringin against 3-nitropropionic acid induced Huntington’s like symptoms in rats: possible role of nitric oxide. Behav Brain Res 206:38–46
35. Kumar A, Prakash A, Dogra S (2010) Naringin alleviates cognitive impairment, mitochondrial dysfunction and oxidative stress induced by d-galactose in mice. Food Chem Toxicol 48:626–632
36. Laczo J, Vlcek K, Vyhnalek M, Vajnerova O, Ort M, Holmerova I, Tolar M, Andel R, Bojar M, Hort J (2009) Spatial navigation testing discriminates two types of amnestic mild cognitive impairment. Behav Brain Res 202:252–259
37. Li H, Min Q, Ouyang C, Lee J, He C, Zou MH, Xie Z (2014) AMPK activation prevents excess nutrient-induced hepatic lipid accumulation by inhibiting mTORC1 signaling and endoplasmic reticulum stress response. Biochim Biophys Acta 1842:1844–1854
38. Liang KC, Hon W, Tyan YM, Liao WL (1994) Involvement of hippocampal NMDA and AMPA receptors in acquisition, formation and retrieval of spatial memory in the Morris water maze. Chin J Physiol 37:201–212
39. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S et al (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10:260–272
40. McNeilly AD, Williamson R, Sutherland C, Balfour DJ, Stewart CA (2011) High fat feeding promotes simultaneous decline in insulin sensitivity and cognitive performance in a delayed matching and non-matching to position task. Behav Brain Res 217:134–141
41. Miller RA, Buehner G, Chang Y, Harper JM, Sigler R, Smith-Wheelock M (2005) Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4:119–125
42. Mohlig M, Isken F, Ristow M (2004) Impaired mitochondrial activity and insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:2419–2421. author reply 2419-2421
43. Moloney AM, Griffin RJ, Timmons S, O’Connor R, Ravid R, O’Neill C (2010) Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer’s disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol Aging 31:224–243
44. Moran C, Sanz-Rodriguez A, Jimenez-Pacheco A, Martinez-Villareal J, McKiernan RC, Jimenez-Mateos EM et al (2013) Bmf upregulation through the AMP-activated protein kinase pathway may protect the brain from seizure-induced cell death. Cell Death Dis 4:e606
45. Ng CH, Guan MS, Koh C, Ouyang X, Yu F, Tan EK, O’Neill SP, Zhang X, Chung J, Lim KL (2012) AMP kinase activation mitigates dopaminergic dysfunction and mitochondrial abnormalities in Drosophila models of Parkinson’s disease. J Neurosci 32:14311–14317
46. Nilsson LG, Nilsson E (2009) Overweight and cognition. Scand J Psychol 50:660–667
47. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457–461
48. 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
49. Pipatpiboon N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2012) PPARgamma 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
50. Pipatpiboon N, Pintana H, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2013) DPP4-inhibitor improves neuronal insulin receptor function, brain mitochondrial function and cognitive function in rats with insulin resistance induced by high-fat diet consumption. Eur J Neurosci 37:839–849
51. Potter WB, O’Riordan KJ, Barnett D, Osting SM, Wagoner M, Burger C, Roopra A (2010) Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS ONE 5:e8996
52. Prakash A, Shur B, Kumar A (2013) Naringin protects memory impairment and mitochondrial oxidative damage against aluminum-induced neurotoxicity in rats. Int J Neurosci 123:636–645
53. Pratchayasakul W, Kerdphoo S, Petsophonsakul P, Pongchaidecha A, Chattipakorn N, Chattipakorn SC (2011) Effects of high-fat diet on insulin receptor function in rat hippocampus and the level of neuronal corticosterone. Life Sci 88:619–627
54. Pu P, Gao DM, Mohamed S, Chen J, Zhang J, Zhou XY, Zhou NJ, Xie J, Jiang H (2012) Naringin ameliorates metabolic syndrome by activating AMP-activated protein kinase in mice fed a high-fat diet. Arch Biochem Biophys 518:61–70
55. Rabol R, Boushel R, Dela F (2006) Mitochondrial oxidative function and type 2 diabetes. Appl Physiol Nutr Metab 31:675–683
56. Rajadurai M, Prince PS (2007) Preventive effect of naringin on cardiac mitochondrial enzymes during isoproterenol-induced myocardial infarction in rats: a transmission electron microscopic study. J Biochem Mol Toxicol 21:354–361
57. Ramesh E, Alshatwi AA (2013) Naringin induces death receptor and mitochondria-mediated apoptosis in human cervical cancer (SiHa) cells. Food Chem Toxicol 51:97–105
58. Reddy PH, Tripathi R, Troung Q, Tirumala K, Reddy TP, Anekonda V et al (2012) Abnormal mitochondrial dynamics and synaptic degeneration as early events in Alzheimer’s disease: implications to mitochondria-targeted antioxidant therapeutics. Biochim Biophys Acta 1822:639–649
59. Saha AK, Xu XJ, Lawson E, Deoliveira R, Brandon AE, Kraegen EW, Ruderman NB (2010) Downregulation of AMPK accompanies leucine- and glucose-induced increases in protein synthesis and insulin resistance in rat skeletal muscle. Diabetes 59:2426–2434
60. Schubert M, Gautam D, Surjo D, Ueki K, Baudler S, Schubert D et al (2004) Role for neuronal insulin resistance in neurodegenerative diseases. Proc Natl Acad Sci USA 101:3100–3105
61. Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24:855–872
62. Sellbom KS, Gunstad J (2012) Cognitive function and decline in obesity. J Alzheimers Dis 30(Suppl 2):S89–S95
63. Shin SM, Cho IJ, Kim SG (2009) Resveratrol protects mitochondria against oxidative stress through AMP-activated protein kinase-mediated glycogen synthase kinase-3beta inhibition downstream of poly(ADP-ribose)polymerase-LKB1 pathway. Mol Pharmacol 76:884–895
64. Skeberdis VA, Lan J, Zheng X, Zukin RS, Bennett MV (2001) Insulin promotes rapid delivery of N-methyl-d-aspartate receptors to the cell surface by exocytosis. Proc Natl Acad Sci USA 98:3561–3566
65. So FV, Guthrie N, Chambers AF, Moussa M, Carroll KK (1996) Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr Cancer 26:167–181
66. Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, Egan JM, Mattson MP (2008) Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18:1085–1088
67. Taddeo EP, Laker RC, Breen DS, Akhtar YN, Kenwood BM, Liao JA et al (2014) Opening of the mitochondrial permeability transition pore links mitochondrial dysfunction to insulin resistance in skeletal muscle. Mol Metab 3:124–134
68. Takamura A, Okamoto Y, Kawarabayashi T, Yokoseki T, Shibata M, Mouri A et al (2011) Extracellular and intraneuronal HMW-AbetaOs represent a molecular basis of memory loss in Alzheimer’s disease model mouse. Mol Neurodegener 6:20
69. van der Heide LP, Kamal A, Artola A, Gispen WH, Ramakers GM (2005) Insulin modulates hippocampal activity-dependent synaptic plasticity in a N-methyl-d-aspartate receptor and phosphatidyl-inositol-3-kinase-dependent manner. J Neurochem 94:1158–1166
70. Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, Becker LE, MacDonald JF, Wang YT (1997) Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388:686–690
71. Wang L, Brautigan DL (2013) Alpha-SNAP inhibits AMPK signaling to reduce mitochondrial biogenesis and dephosphorylates Thr172 in AMPKalpha in vitro. Nat Commun 4:1559
72. Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635–647
73. Wang D, Gao K, Li X, Shen X, Zhang X, Ma C, Qin C, Zhang L (2012) Long-term naringin consumption reverses a glucose uptake defect and improves cognitive deficits in a mouse model of Alzheimer’s disease. Pharmacol Biochem Behav 102:13–20
74. Wang DM, Yang YJ, Zhang L, Zhang X, Guan FF, Zhang LF (2013) Naringin enhances CaMKII activity and improves long-term memory in a mouse model of Alzheimer’s disease. Int J Mol Sci 14:5576–5586
75. Warren BE, Lou PH, Lucchinetti E, Zhang L, Clanachan AS, Affolter A, Hersberger M, Zaugg M, Lemieux H (2014) Early mitochondrial dysfunction in glycolytic muscle, but not oxidative muscle, of the fructose-fed insulin-resistant rat. Am J Physiol Endocrinol Metab 306:E658–E667
76. Xu XJ, Gauthier MS, Hess DT, Apovian CM, Cacicedo JM, Gokce N, Farb M, Valentine RJ, Ruderman NB (2012) Insulin sensitive and resistant obesity in humans: AMPK activity, oxidative stress, and depot-specific changes in gene expression in adipose tissue. J Lipid Res 53:792–801
77. Yano M, Watanabe K, Yamamoto T, Ikeda K, Senokuchi T, Lu M et al (2011) Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J Biol Chem 286:3992–4002
78. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J et al (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108:1167–1174