Effect of naringenin on brain insulin signaling and cognitive functions in ICV-STZ induced dementia model of rats

Neurological Sciences

Volumn 35, Issue 5, 2014, Pages 741-751

  Yang, Wenqing ^a,b   Ma, Jing ^a   Liu, Zheng ^a   Lu, Yongliang ^a   Hu, Bin ^a   Yu, Huarong ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b SICHUAN PROVINCIAL PEOPLE'S HOSPITAL   (China)

Author keywords

Alzheimer's disease (AD); Amyloid beta protein; Naringenin; PPAR ; Tau

Indexed keywords

AMYLOID BETA PROTEIN; COMPLEMENTARY DNA; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR; INSULIN SENSITIZING AGENT; MESSENGER RNA; NARINGENIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; RNA 18S; STREPTOZOCIN; AMYLOID BETA-PROTEIN (1-42); GLUCOSE BLOOD LEVEL; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INSULIN DERIVATIVE; MAPT PROTEIN, RAT; PEPTIDE FRAGMENT; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN; BRAIN CORTEX; BRAIN WEIGHT; COGNITIVE DEFECT; CONTROLLED STUDY; DEGENERATIVE DISEASE; DEMENTIA; DISEASE MODEL; DRUG DOSE COMPARISON; DRUG MEGADOSE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MALE; MORRIS WATER MAZE TEST; MORTALITY; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; WESTERN BLOTTING; ANIMAL; COGNITION; COGNITION DISORDERS; DOSE RESPONSE; DRUG EFFECTS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MAZE TEST; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; BLOOD GLUCOSE; BRAIN; COGNITION; COGNITION DISORDERS; DEMENTIA; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCOGEN SYNTHASE KINASE 3; INFUSIONS, INTRAVENTRICULAR; INSULINS; MALE; MAZE LEARNING; PEPTIDE FRAGMENTS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; RNA, MESSENGER; SPATIAL MEMORY; STREPTOZOCIN; TAU PROTEINS;

EID: 84901268554     PISSN: 15901874     EISSN: 15903478     Source Type: Journal    
DOI: 10.1007/s10072-013-1594-3     Document Type: Article

References (47)

1. Mosconi L, Tsui WH, Rusinek H et al (2007) Quantitation, regional vulnerability, and kinetic modeling of brain glucose metabolism in mild Alzheimer's disease. Eur J Nucl Med Mol Imaging 34(9):1467-1479 (Pubitemid 47312590)
2. Kim EJ, Cho SS, Jeong Y et al (2005) Glucose metabolism in early onset versus late onset Alzheimer's disease: an SPM analysis of 120 patients. Brain 128:1790-1801 (Pubitemid 41373650)
3. Hoyer S (2004) Causes and consequences of disturbances of cerebral glucose metabolism in sporadic Alzheimer disease: therapeutic implications. Adv Exp Med Biol 541:135-152
4. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM (1999) Diabetes mellitus and the risk of dementia: the Rotterdam study. Neurology 53:1937-1942
5. Profenno LA, Porsteinsson AP, Faraone SV (2010) Meta-analysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biol Psychiatry 67:505-512
6. Janson J, Laedtke T, Parisi JE, O'Brien P, Petersen RC, Butler PC (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53:474-481 (Pubitemid 38174565)
7. Musicco M, Palmer K, Salamone G, Lupo F, Perri R, Mosti S, Spalletta G, di Iulio F, Pettenati C, Cravello L, Caltagirone C (2009) Predictors of progression of cognitive decline in Alzheimer's disease: the role of vascular and sociodemographic factors. J Neurol 256:1288-1295
8. Steen E, Terry BM, Rivera EJ et al (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J Alzheimers Dis 7:63-80 (Pubitemid 40387185)
9. Zhao WQ, Townsend M (2009) Insulin resistance and amyloidogenesis as common molecular foundation for type 2 diabetes and Alzheimer's disease. Biochim Biophys Acta 1792:482-496
10. Agrawal R, Tyagi E, Shukla R, Nath C (2009) A study of brain insulin receptors, AChE activity and oxidative stress in rat model of ICV STZ induced dementia. Neuropharmacology 56:779-787
11. Salkovic-Petrisic M, Hoyer S (2007) Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: an experimental approach. J Neural Transm Suppl 72:217-233
12. Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K, Wands JR, de la Monte SM (2006) Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer's disease. J Alzheimers Dis 9:13-33
13. Subramanian S, John M (2012) Intranasal administration of insulin lowers amyloid-β levels in rat model of diabetes. Indian J Exp Biol 50:41-44
14. Li Y, Duffy KB, Ottinger MA, Ray B, Bailey JA, Holloway HW, Tweedie D, Perry T, Mattson MP, Kapogiannis D, Sambamurti K, Lahiri DK, Greig NH (2010) GLP-1 receptor stimulation reduces amyloid-β peptide accumulation and cytotoxicity in cellular and animal models of Alzheimer's disease. J Alzheimers Dis 19:1205-1219
15. Pedersen WA, McMillan PJ, Kulstad JJ, Leverenz JB, Craft S, Haynatzki GR (2006) Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Exp Neurol 199:265-273 (Pubitemid 43928978)
16. Jiang Q, Heneka M, Landreth GE (2008) The role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in Alzheimer's disease. CNS Drugs 22:1-14 (Pubitemid 350243363)
17. Lee CH, Jeong TS, Choi YK, Hyun BH, Oh GT, Kim EH, Kim JR, Han JI, Bok SH (2001) Anti-atherogenic effect of citrus flavonoids, naringin and naringenin, associated with hepatic ACAT and aortic VAM-1 and MCP-1 in high cholesterol-fed rabbits. Biochem Biophys Res Commun 284:681-688 (Pubitemid 32924782)
18. Baluchnejadmojarad T, Roghani M (2006) Effect of naringenin on intracerebroventricular streptozotocin-induced cognitive deficits in rat: a behavioral analysis. Pharmacology 78:193-197 (Pubitemid 44948058)
19. Heo HJ, Kim DO, Shin SC, Kim MJ, Kim BG, Shin DH (2004) Effect of antioxidant flavanone, naringenin, from citrus junos. J Agric Food Chem 52:1520-1525
20. Christensen KB, Petersen RK, Kristiansen K, Christensen LP (2010) Identification of bioactive compounds from flowers of black elder (Sambucus nigra L.) that activate the human peroxisome proliferator-activated receptor (PPAR) gamma. Phytother Res 24:129-132
21. Kannappan S, Anuradha CV (2010) Naringenin enhances insulin-stimulated tyrosine phosphorylation and improves the cellular actions of insulin in a dietary model of metabolic syndrome. Eur J Nutr 49:101-109
22. Rocchi A, Pellegrini S, Siciliano G, Murri L (2003) Causative and susceptibility genes for Alzheimer's disease: a review. Brain Res Bull 61:1-24 (Pubitemid 36682979)
23. Nicolakakis N, Hamel E (2010) The nuclear receptor PPAR-gamma as a therapeutic target for cerebrovascular and brain dysfunction in Alzheimer's disease. Front Aging Neurosci. doi:10.3389/fnagi.2010.00021
24. Landreth G, Jiang Q, Mandrekar S, Heneka M (2008) PPARgamma agonists astherapeutics for the trentment of Alzheimer's disease. Neurotherapeutics 5:481-489 (Pubitemid 351952487)
25. Solano DC, Sironi M, Bonfini C, Solerte SB, Govoni S, Racchi M (2000) Insulin regulates soluble amyloid precursor protein release via phosphatidyl inositol 3 kinase-dependent pathway. FASEB 14:1015-1022 (Pubitemid 30241680)
26. Xie L, Helmerhorst E, Taddei K, Plewright B, Van Bronswijk W, Martins R (2002) Alzheimer's beta-amyloid peptides compete for insulin binding to the insulin receptor. J Neurosci 22:RC221
27. Lannert H, Hoyer S (1998) Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci 112:1199-1208 (Pubitemid 28519002)
28. Chen S, Liu AR, An FM, Yao WB, Gao XD (2011) Amelioration of neurodegenerative changes in cellular and rat models of diabetes-related Alzheimer's disease by exendin-4. Age (Dordr) 34:1211-1224
29. Ishrat T, Hoda MN, Khan MB, Yousuf S, Ahmad M, Khan MM, Ahmad A, Islam F (2009) Amelioration of cognitive deficits and neurodegeneration by curcumin in rat model of sporadic dementia of Alzheimer's type (SDAT). Eur Neuropsychopharmacol 19:636-647
30. Rivera EJ, Goldin A, Fulmer N, Tavares R, Wands JR, de la Monte SM (2005) Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease:Link to brain reductions in acetylcholine. J Alzheimers Dis 8:247-268
31. Shaw PC, Davies AF, Lau KF, Garcia-Barcelo M, Waye MM, Lovestone S, Miller CC, Anderton BH (1998) Isolation and chromosomal mapping of human glycogen synthase kinase-3 alpha and beta encoding gene. Genome 41:720-727 (Pubitemid 29006677)
32. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3alpha regulates prodution of Alzheimer'diease amyloid-beta peptides. Nature 423:435-439
33. Schubert M, Brazil DP, Burks DJ et al (2003) Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J Neurosci 23:7084-7092 (Pubitemid 36975873)
34. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkov EM (2002) Tau blocks traffic organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. Cell Biol 156:1051-1063 (Pubitemid 34839854)
35. Deng Y, Li B, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX (2009) Dysregulation of Insulin Signaling, Glucose Transporters, O-GlcNAcylation, and Phosphorylation of Tau and Neurofilaments in the Brain. Am J Pathol 175:2089-2098
36. Shipton OA, Leitz JR, Dworzak J et al (2011) Tau protein is required for amyloid β-induced impairment of hippocampal longterm potentiation. J Neurosci 31:1688-1692
37. Iijima K, Gatt A, Iijima-Ando K (2010) Tau Ser262 phosphorylation is critical for Ab42-induced tau toxicity in a transgenic Drosophila model of Alzheimer's disease. Hum Mol Genet 19:2947-2957
38. Walsh DM, Selkoe DJ (2004) Deciphering the molecularbasis of memory failure in Alzheimer's disease. Neuron 44:181-193 (Pubitemid 39348839)
39. Walsh DM et al (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539 (Pubitemid 34288854)
40. Correia SC, Santos RX, Perry G, Zhu X, Moreira PI, Smith MA (2011) Insulin-resistant brain state: the culprit in sporadic Alzheimer's disease? Ageing Res Rev 10:264-273
41. Gasparini L, Netzer WJ, Greengard P, Xu H (2002) Does insulin dysfunction play a role in Alzheimer's disease? Trends Pharmacol Sci 23:288-293 (Pubitemid 34655735)
42. Pérez A, Morelli L, Cresto JC, Castaño EM (2000) Degradation of soluble amyloid beta-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brain. Neurochem Res 25:247-255
43. Farris W, Mansourian S, Chang Y et al (2003) Insulin-degrading enzyme regulates the levels of insulin, amyloid h-protein, and the h-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA 100:4162-4167 (Pubitemid 36418174)
44. Du J, Zhang L, Liu S, Zhang C, Huang X, Li J, Zhao N, Wang Z (2009) PPARgamma transcriptionally regulates the expression of insulin-degrading enzyme in primary neurons. Biochem Biophys Res Commun 383(4):485-490
45. Sastre M, Dewachter I, Landreth GE et al (2003) Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-gamma agonists modulate immunostimulated processing of amyloid precursor protein through regulation of beta-secretase. Neuroscience 23:9796-9804 (Pubitemid 37371592)
46. Kannappan S, Palanisamy N, Anuradha CV (2010) Suppression of hepatic oxidative events and regulation of eNOS expression in the liver by naringenin in fructose-administered rats. Eur J Pharmacol 645:177-184
47. Khan MB, Khan MM, Khan A, Ahmed ME, Ishrat T, Tabassum R, Vaibhav K, Ahmad A, Islam F (2012) Naringenin ameliorates Alzheimer's disease (AD)-type neurodegeneration with cognitive impairment (AD-TNDCI) caused by the intracerebroventricular-streptozotocin in rat model. Neurochem Int 61:1081-1093