Differential metformin dose-dependent effects on cognition in rats: role of Akt

Psychopharmacology

Volumn 233, Issue 13, 2016, Pages 2513-2524

  Mostafa, Dalia K ^a   Ismail, Cherine A ^a   Ghareeb, Doaa A ^b  

^a ALEXANDRIA UNIVERSITY   (Egypt)

^b Alexandria University Faculty Of Science   (Egypt)

Author keywords

Acetyl cholinesterase activity; Akt; Cognitive impairment; Metformin; Phosphorylated tau; Scopolamine

Indexed keywords

ACETYLCHOLINESTERASE; MALONALDEHYDE; METFORMIN; NITRIC OXIDE; PROTEIN KINASE B; RIVASTIGMINE; SCOPOLAMINE; SODIUM CHLORIDE; TAU PROTEIN; TUMOR NECROSIS FACTOR ALPHA; ANTIDIABETIC AGENT; CHOLINERGIC RECEPTOR BLOCKING AGENT; SCOPOLAMINE BROMIDE; TUMOR NECROSIS FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BIOACCUMULATION; BRAIN CORTEX; COGNITIVE DEFECT; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; ENZYME ACTIVITY; FRONTAL CORTEX; HIPPOCAMPUS; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; MORNING DOSAGE; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PASSIVE AVOIDANCE TEST; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; CHEMICALLY INDUCED; COGNITION; DISEASE MODEL; DRUG EFFECTS; MAZE TEST; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; WISTAR RAT;

ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CHOLINERGIC ANTAGONISTS; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; HYPOGLYCEMIC AGENTS; MALE; MALONDIALDEHYDE; MAZE LEARNING; MEMORY DISORDERS; METFORMIN; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; RATS; RATS, WISTAR; SCOPOLAMINE HYDROBROMIDE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84964432741     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-016-4301-2     Document Type: Article

References (60)

1. Abdel-Salam OM, Khadrawy YA, Mohammed NA, Youness ER (2012) The effect of gabapentin on oxidative stress in a model of toxic demyelination in rat brain. J Basic Clin Physiol Pharmacol 23(2):61–68
2. Abel T, Lattal KM (2001) Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11:180–187
3. Allami N, Javadi-Paydar M, Rayatnia F, Sehhat K, Rahimian R, Norouzi A, Dehpour AR (2011) Suppression of nitric oxide synthesis by L-NAME reverses the beneficial effects of pioglitazone on scopolamine-induced memory impairment in mice. Eur J Pharmacol 650(1):240–248
4. Allard JS, Sankavaram K, Perez E, Minor R, De Cabo R (2011) Metformin treatment increases mRNA levels of inflammatory factors and decreases mRNA levels of neurotrophic factors in brains of C57BL/6 mice. 2011 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience Online
5. Bagul PK, Middela H, Matapally S, Padiya R, Bastia T, Madhusudana K, Reddy BR, Chakravarty S, Banerjee SK (2012) Attenuation of insulin resistance, metabolic syndrome and hepatic oxidative stress by resveratrol in fructose-fed rats. Pharmacol Res 66(3):260–268
6. Barreto-Torres G, Hernandez JS, Jang S, Rodríguez-Muñoz AR, Torres-Ramos CA, Basnakian AG, Javadov S (2015) The beneficial effects of AMP kinase activation against oxidative stress are associated with prevention of PPARα-cyclophilin D interaction in cardiomyocytes. Am J Physiol Heart Circ Physiol 308(7):H749–H758. doi:10.1152/ajpheart.00414.2014
7. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, Rosen N (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 277(42):39858–39866
8. Bejar C, Wang RH, Weinstock M (1999) Effect of rivastigmine on scopolamine-induced memory impairment in rats. Eur J Pharmacol 383(3):231–240
9. Belkhelfa M, Rafa H, Medjeber O, Arroul-Lammali A, Behairi N, Abada-Bendib M, Makrelouf M, Belarbi S, Masmoudi AN, Tazir M, Touil-Boukoffa C (2014) IFN-γ and TNF-α are involved during Alzheimer disease progression and correlate with nitric oxide production: a study in Algerian patients. J Interferon Cytokine Res 34(11):839–847
10. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8(10):766–775
11. Cavallucci V, D’Amelio M, Cecconi F (2012) Aβ toxicity in Alzheimer’s disease. Mol Neurobiol 45(2):366–378
12. Chen Y, Zhou K, Wang R, Liu Y, Kwak YD, Ma T, Thompson RC, Zhao Y, Smith L, Gasparini L, Luo Z, Xu H, Liao FF (2009) Antidiabetic drug metformin (GlucophageR) increases biogenesis of Alzheimer’s amyloid peptides via up-regulating BACE1 transcription. Proc Natl Acad Sci U S A 106(10):3907–3912
13. de la Monte SM (2014) Type 3 diabetes is sporadic Alzheimer’s disease: mini-review. Eur Neuropsychopharmacol 24(12):1954–1960. doi:10.1016/j.euroneuro.2014.06.008
14. Deiana S, Harrington CR, Wischik CM, Riedel G (2009) Methylthioninium chloride reverses cognitive deficits induced by scopolamine: comparison with rivastigmine. Psychopharmacol (Berl) 202(1–3):53–65
15. Dickey CA, Koren J, Zhang YJ, Xu YF, Jinwal UK, Birnbaum MJ, Monks B, Sun M, Cheng JQ, Patterson C, Bailey RM, Dunmore J, Soresh S, Leon C, Morgan D, Petrucelli L (2008) Akt and CHIP coregulate tau degradation through coordinated interactions. Proc Natl Acad Sci U S A 105(9):3622–3627
16. Ellman GL, Courtney KD, Andres VJ, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
17. El-Mir MY, Detaille D, R-Villanueva G, Delgado-Esteban M, Guigas B, Attia S, Fontaine E, Almeida A, Leverve X (2008) Neuroprotective role of antidiabetic drug metformin against apoptotic cell death in primary cortical neurons. J Mol Neurosci 34(1):77–87
18. González CR, Caminos JE, Vázquez MJ, Garcés MF, Cepeda LA, Angel A, González AC, García-Rendueles ME, Sangiao-Alvarellos S, López M, Bravo SB, Nogueiras R, Diéguez C (2009) Regulation of visceral adipose tissue-derived serine protease inhibitor by nutritional status, metformin, gender and pituitary factors in rat white adipose tissue. J Physiol 587(Pt 14):3741–3750
19. Gupta A, Bisht B, Dey CS (2011) Peripheral insulin sensitizer drug metformin ameliorate neuronal insulin resistance and Alzheimer’s like changes. Neuropharmacology 60(6):910–920
20. Hooper C, Killick R, Lovestone S (2008) The GSK3 hypothesis of Alzheimer’s disease. J Neurochem 104(6):1433–1439
21. Hsieh MT, Hsieh CL, Lin LW, Wu CR, Huang GS (2003) Differential gene expression of scopolamine-treated rat hippocampus-application of cDNA microarray technology. Life Sci 73(8):1007–1016
22. Hu Y, Zhu DY (2014) Hippocampus and nitric oxide. Vitam Horm 96:127–160
23. Imfeld P, Bodmer M, Jick SS, Meier CR (2012) Metformin, other antidiabetic drugs, and risk of Alzheimer’s disease: a population-based case–control study. J Am Geriatr Soc 60(5):916–921, Alzheimer’s disease is type 3 diabetes—evidence reviewed
24. 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(9):636–647. doi:10.1016/j.euroneuro.2009.02.002
25. Jang YJ, Kim J, Shim J, Kim CY, Jang JH, Lee KW, Lee HJ (2013) Decaffeinated coffee prevents scopolamine-induced memory impairment in rats. Behav Brain Res 245:113–119
26. Javadi-Paydar M, Zakeri M, Norouzi A, Rastegar H, Mirazi N, Dehpour AR (2012) Involvement of nitric oxide in granisetron improving effect on scopolamine induced memory impairment in mice. Brain Res 429:61–71
27. Jeong EJ, Lee KY, Kim SH, Sung SH, Kim YC (2008) Cognitive enhancing and antioxidant activities of iridoid glycosides from Scrophularia buergeriana in scopolamine-treated mice. Eur J Pharmacol 588(1):78–84
28. Kwon SH, Ma SX, Joo HJ, Lee SY, Jang CG (2013) Inhibitory effects of Eucommia ulmoides Oliv. bark on scopolamine-induced learning and memory deficits in mice. Biomol Ther 21(6):462–469
29. Lee B, Shim I, Lee H, Hahm DH (2011) Rehmannia glutinosa ameliorates scopolamine-induced learning and memory impairment in rats. J Microbiol Biotechnol 21(8):874–883
30. Lee B, Sur B, Shim I, Lee H, Hahm DH (2012) Phellodendron amurense and its major alkaloid compound, berberine ameliorates scopolamine-induced neuronal impairment and memory dysfunction in rats. Korean J Physiol Pharmacol 16(2):79–89
31. Lennox R, Porter DW, Flatt PR, Holscher C, Irwin N, Gault VA (2014) Comparison of the independent and combined effects of sub-chronic therapy with metformin and a stable GLP-1 receptor agonist on cognitive function, hippocampal synaptic plasticity and metabolic control in high-fat fed mice. Neuropharmacology 86:22–30
32. Li J, Deng J, Sheng W, Zuo Z (2012) Metformin attenuates Alzheimer’s disease like neuropathology in obese, leptin resistant mice. Pharmacol Biochem Behav 101(4):564–574
33. Lowry H, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
34. Mathis DM, Furman JL, Norris CM (2011) Preparation of acute hippocampal slice from rats and transgenic mice for the study of synaptic alteration during aging and amyloid pathology. J Vis Exp 49:2330–2337
35. McNeilly AD, Williamson R, Balfour DJ, Stewart CA, Sutherland C (2012) A high-fat-diet-induced cognitive deficit in rats that is not prevented by improving insulin sensitivity with metformin. Diabetologia 55(11):3061–3070
36. Melo JB, Agostinho P, Oliveira CR (2003) Involvement of oxidative stress in the enhancement of acetylcholinesterase activity induced by amyloid beta-peptide. Neurosci Res 45(1):117–127
37. Mohamed AR, Soliman GY, Ismail CA, Manaa HF (2015) Neuroprotective role of vitamin D3 in colchicine-induced Alzheimer’s disease in rats. Alex J Med 51(2):127–136
38. Montgomery HAC, Dymock JF (1961) The determination of nitrite in water. Analyst 86:414–416
39. Moore EM, Mander AG, Ames D, Kotowicz MA, Carne RP, Brodaty H, Woodward M, Boundy K, Ellis KA, Bush AI, Faux NG, Martins R, Szoeke C, Rowe C, Watters DA, Investigators AIBL (2013) Increased risk of cognitive impairment in patients with diabetes is associated with metformin. Diabetes Care 36(10):2981–2987
40. Moosavi M, Khales GY, Abbasi L, Zarifkar A, Rastegar K (2012) Agmatine protects against scopolamine-induced water maze performance impairment and hippocampal ERK and Akt inactivation. Neuropharmacology 62:2018–2023
41. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11(1):47–60
42. Ng TP, Feng L, Yap KB, Lee TS, Tan CH, Winblad B (2014) Long-term metformin usage and cognitive function among older adults with diabetes. J Alzheimers Dis 41(1):61–68
43. Patrone C, Eriksson O, Lindholm D (2014) Diabetes drugs and neurological disorders: new views and therapeutic possibilities. Lancet Diabetes Endocrinol 2(3):256–262
44. 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(11–12):409–414
45. Rojas LB, Gomes MB (2013) Metformin: an old but still the best treatment for type 2 diabetes. Diabetol Metab Syndr 5(1):6
46. Samy DM, Ismail CA, Nassra RA, Zeitoun TM, Nomair AM (2016) Downstream modulation of extrinsic apoptotic pathway in streptozotocin-induced Alzheimer’s dementia in rats: erythropoietin versus curcumin. Eur J Pharmacol 770:52–60
47. Scali C, Casamenti F, Bellucci A, Costagli C, Schmidt B, Pepeu G (2002) Effect of subchronic administration of metrifonate, rivastigmine and donepezil on brain acetylcholine in aged F344 rats. J Neural Transm 109(7–8):1067–1080
48. Shifrin H, Nadler-Milbauer M, Shoham S, Weinstock M (2013) Rivastigmine alleviated experimentally induced colitis in mice and rats by acting at central and peripheral sites to modulate immune responses. PLoS One 8(2):e57668
49. Soraya H, Khorrami A, Garjani A, Maleki-Dizaji N, Garjani A (2012) Acute treatment with metformin improves cardiac function following isoproterenol induced myocardial infarction in rats. Pharmacol Rep 64(6):1476–1484
50. Stevens R (1981) Scopolamine impairs spatial maze performance in rats. Physiol Behav 27:385–386
51. Tang XQ, Fang HR, Zhou CF, Zhuang YY, Zhang P, Gu HF, Hu B (2013) A novel mechanism of formaldehyde neurotoxicity: inhibition of hydrogen sulfide generation by promoting overproduction of nitric oxide. PLoS One 8(1):e54829
52. Thornton C, Bright NJ, Sastre M, Muckett PJ, Carling D (2011) AMP-activated protein kinase (AMPK) is a tau kinase, activated in response to amyloid β-peptide exposure. Biochem J 434(3):503–512
53. Utkan T, Gocmez SS, Regunathan S, Aricioglu F (2012) Agmatine, a metabolite of L-arginine, reverses scopolamine-induced learning and memory impairment in rats. Pharmacol Biochem Behav 102:578–584
54. Wang J, Gallagher D, DeVito LM, Cancino GI, Tsui D, He L, Keller GM, Frankland PW, Kaplan DR, Miller FD (2012) Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation. Cell Stem Cell 11(1):23–35
55. Wessels B, Ciapaite J, van den Broek NM, Nicolay K, Prompers JJ (2014) Metformin impairs mitochondrial function in skeletal muscle of both lean and diabetic rats in a dose-dependent manner. PLoS One 9(6):e100525
56. Wills ED (1966) Mechanisms of lipid peroxide formation in animal tissues. Biochem J 99:667–676
57. Xu PX, Wang SW, Yu XL, Su YJ, Wang T, Zhou WW, Zhang H, Wang YJ, Liu RT (2014) Rutin improves spatial memory in Alzheimer’s disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behav Brain Res 264:173–180
58. Zhao WQ, De Felice FG, Fernandez S, Chen H, Lambert MP, Quon MJ, Krafft GA, Klein WL (2008) Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEBJ 22(1):246–260
59. Zhao RR, Xu XC, Xu F, Zhang WL, Zhang WL, Liu LM, Wang WP (2014) Metformin protects against seizures, learning and memory impairments and oxidative damage induced by pentylenetetrazole-induced kindling in mice. Biochem Biophys Res Commun 448(4):414–417
60. Zhou Y, Fang R, Liu LH, Chen SD, Tang HD (2015) Clinical characteristics for the relationship between type-2 diabetes mellitus and cognitive impairment: a cross-sectional study. Aging Dis 6(4):236–244