Metformin pretreatment enhanced learning and memory in cerebral forebrain ischaemia: the role of the AMPK/BDNF/P70SK signalling pathway

References

• Ajami M, Eghtesadi S, Razaz JM, Kalantari N, Habibey R, Nilforoushzadeh MA, Zarrindast M, Pazoki-Toroudi H. 2011. Expression of Bcl-2 and Bax after hippocampal ischemia in DHA + EPA treated rats. Neurol Sci. 32:811–818.
   PubMed Web of Science ®Google Scholar
• Ashabi G, Khalaj L, Khodagholi F, Goudarzvand M, Sarkaki A. 2015. Pre-treatment with metformin activates Nrf2 antioxidant pathways and inhibits inflammatory responses through induction of AMPK after transient global cerebral ischemia. Metab Brain Dis. 30:747–754.
   PubMed Web of Science ®Google Scholar
• Ashabi G, Khodagholi F, Khalaj L, Goudarzvand M, Nasiri M. 2014. Activation of AMP-activated protein kinase by metformin protects against global cerebral ischemia in male rats: interference of AMPK/PGC-1α pathway. Metab Brain Dis. 29:47–58.
   PubMed Web of Science ®Google Scholar
• Barker PA. 2009. Whither pro BDNF? Nat Neurosci. 12:105–106.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Chen F, Dong RR, Zhong KL, Ghosh A, Tang SS, Long Y, Hu M, Miao MX, Liao JM, Sun HB, et al. 2016. Antidiabetic drugs restore abnormal transport of amyloid-beta across the blood-brain barrier and memory impairment in db/db mice. Neuropharmacology. 101:123–136.
   PubMed Web of Science ®Google Scholar
• Cummins RO, Austin D Jr, Graves JR, Hambly C. 1988. An innovative approach to medical control: semiautomatic defibrillators with solid-state memory modules for recording cardiac arrest events. Ann Emerg Med. 17:818–824.
   PubMed Web of Science ®Google Scholar
• Dichgans M. 2007. Genetics of ischaemic stroke. Lancet Neurol. 6:149–161.
   PubMed Web of Science ®Google Scholar
• Ditacchio KA, Heinemann SF, Dziewczapolski G. 2015. Metformin treatment alters memory function in a mouse model of Alzheimer's disease. J Alzheimers Dis. 44:43–48.
   PubMed Web of Science ®Google Scholar
• Fahnestock M, Garzon D, Holsinger RM, Michalski B. 2002. Neurotrophic factors and Alzheimer's disease: are we focusing on the wrong molecule? J Neural Transm Suppl. 1:241–252.
   Google Scholar
• Fang ZH, Lee CH, Seo MK, Cho H, Lee JG, Lee BJ, Park SW, Kim YH. 2013. Effect of treadmill exercise on the BDNF-mediated pathway in the hippocampus of stressed rats. Neurosci Res. 76:187–194.
   PubMed Web of Science ®Google Scholar
• Farbood Y, Sarkaki A, Khalaj L, Khodagholi F, Badavi M, Ashabi G. 2015. Targeting adenosine monophosphate-activated protein kinase by metformin adjusts post-ischemic hyperemia and extracellular neuronal discharge in transient global cerebral ischemia. Microcirculation. 22:534–541.
   PubMed Web of Science ®Google Scholar
• Globus MY, Busto R, Martinez E, Valdés I, Dietrich WD, Ginsberg MD. 1991. Comparative effect of transient global ischemia on extracellular levels of glutamate, glycine, and gamma-aminobutyric acid in vulnerable and nonvulnerable brain regions in the rat. J Neurochem. 57:470–478.
   PubMed Web of Science ®Google Scholar
• Hardie DG. 2008. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond). 32:S7–S12.
   PubMed Web of Science ®Google Scholar
• Ishizuka Y, Kakiya N, Witters LA, Oshiro N, Shirao T, Nawa H, Takei N. 2013. AMP-activated protein kinase counteracts brain-derived neurotrophic factor-induced mammalian target of rapamycin complex 1 signaling in neurons. J Neurochem. 127:66–77.
   PubMed Web of Science ®Google Scholar
• Jun KH, Lee JE, Kim SH, Jung JH, Choi HJ, Kim YI, Chin HM, Yang SH. 2015. Clinicopathological significance of N-cadherin and VEGF in advanced gastric cancer brain metastasis and the effects of metformin in preclinical models. Oncol Rep. 34:2047–2053.
   PubMed Web of Science ®Google Scholar
• Koskimaki J, Matsui N, Umemori J, Rantamäki T, Castrén E. 2015. Nimodipine activates TrkB neurotrophin receptors and induces neuroplastic and neuroprotective signaling events in the mouse hippocampus and prefrontal cortex. Cell Mol Neurobiol. 35:189–196.
   PubMed Web of Science ®Google Scholar
• Lehman JA, Calvo V, Gomez-Cambronero J. 2003. Mechanism of ribosomal p70S6 kinase activation by granulocyte macrophage colony-stimulating factor in neutrophils: cooperation of a MEK-related, THR421/SER424 kinase and a rapamycin-sensitive, m-TOR-related THR389 kinase. J Biol Chem. 278:28130–28138.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lenzser G, Kis B, Bari F, Busija DW. 2005. Diazoxide preconditioning attenuates global cerebral ischemia-induced blood–brain barrier permeability. Brain Res. 1051:72–80.
   PubMed Web of Science ®Google Scholar
• Li L, Zhang H, Meng SQ, Qian HZ. 2014. An updated meta-analysis of the efficacy and safety of acupuncture treatment for cerebral infarction. PLoS One. 9:e114057.
   Google Scholar
• Lipton SA, Rosenberg PA. 1994. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med. 330:613–622.
   PubMed Web of Science ®Google Scholar
• Lu B. 2003. Pro-region of neurotrophins: role in synaptic modulation. Neuron. 39:735–738.
   PubMed Web of Science ®Google Scholar
• Mansouri MT, Farbood Y, Sameri MJ, Sarkaki A, Naghizadeh B, Rafeirad M. 2013. Neuroprotective effects of oral gallic acid against oxidative stress induced by 6-hydroxydopamine in rats. Food Chem. 138:1028–1033.
   PubMed Web of Science ®Google Scholar
• Mousavi SM, Niazmand S, Hosseini M, Hassanzadeh Z, Sadeghnia HR, Vafaee F, Keshavarzi Z. 2015. Beneficial effects of teucrium polium and metformin on diabetes-induced memory impairments and brain tissue oxidative damage in rats. Int J Alzheimers Dis. 2015:493729.
   PubMedGoogle Scholar
• Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H. 2010. BDNF function and intracellular signaling in neurons. Histol Histopathol. 25:237–258.
   PubMed Web of Science ®Google Scholar
• Petito CK, Feldmann E, Pulsinelli WA, Plum F. 1987. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology. 37:1281–1286.
   PubMed Web of Science ®Google Scholar
• Plews RL, Mohd Yusof A, Wang C, Saji M, Zhang X, Chen CS, Ringel MD, Phay JE. 2015. A novel dual AMPK activator/mTOR inhibitor inhibits thyroid cancer cell growth. J Clin Endocrinol Metab. 100:E748–E756.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• Pulsinelli WA, Brierley JB. 1979. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke. 10:267–272.
   PubMed Web of Science ®Google Scholar
• Sarkaki A, Farbood Y, Badavi M, Khalaj L, Khodagholi F, Ashabi G. 2015. Metformin improves anxiety-like behaviors through AMPK-dependent regulation of autophagy following transient forebrain ischemia. Metab Brain Dis. 30:1139–1150.
   PubMed Web of Science ®Google Scholar
• Shi LL, Chen BN, Gao M, Zhang HA, Li YJ, Wang L, Du GH. 2011. The characteristics of therapeutic effect of pinocembrin in transient global brain ischemia/reperfusion rats. Life Sci. 88:521–528.
   PubMed Web of Science ®Google Scholar
• Truong DT, Venna VR, McCullough LD, Fitch RH. 2012. Deficits in auditory, cognitive, and motor processing following reversible middle cerebral artery occlusion in mice. Exp Neurol. 238:114–121.
   PubMed Web of Science ®Google Scholar
• Tsai SJ. 2007. The P11, tPA/plasminogen system and brain-derived neurotrophic factor: implications for the pathogenesis of major depression and the therapeutic mechanism of antidepressants. Med Hypotheses. 68:180–183.
   PubMed Web of Science ®Google Scholar
• Vorhees CV, Williams MT. 2014. Assessing spatial learning and memory in rodents. Ilar J. 55:310–332.
   PubMed Web of Science ®Google Scholar
• Walcott BP, Boehm KM, Stapleton CJ, Mehta BP, Nahed BV, Ogilvy CS. 2013. Retrievable stent thrombectomy in the treatment of acute ischemic stroke: analysis of a revolutionizing treatment technique. J Clin Neurosci. 20:1346–1349.
   PubMed Web of Science ®Google Scholar
• Wilson WJ, Cook JA. 1994. Cholinergic manipulations and passive avoidance in the rat: effects on acquisition and recall. Acta Neurobiol Exp (Wars). 54:377–391.
   PubMed Web of Science ®Google Scholar
• Wu HQ, Guo HN, Wang HQ, Chang MZ, Zhang GL, Zhao YX. 2009. Protective effects and mechanism of puerarin on learning-memory disorder after global cerebral ischemia–reperfusion injury in rats. Chin J Integr Med. 15:54–59.
   PubMed Web of Science ®Google Scholar
• Yeh FC, Kao CF, Kuo PH. 2015. Explore the features of brain-derived neurotrophic factor in mood disorders. PLoS One. 10:e0128605.
   Google Scholar
• Zare Mehrjerdi F, Aboutaleb N, Habibey R, Ajami M, Soleimani M, Arabian M, Niknazar S, Hossein Davoodi S, Pazoki-Toroudi H. 2013. Increased phosphorylation of mTOR is involved in remote ischemic preconditioning of hippocampus in mice. Brain Res. 1526:94–101.
   PubMed Web of Science ®Google Scholar
• Zhang T, Wang X, He D, Jin X, Guo P. 2014. Metformin sensitizes human bladder cancer cells to TRAIL-induced apoptosis through mTOR/S6K1-mediated downregulation of c-FLIP. Anticancer Drugs. 25:887–897.
   PubMed Web of Science ®Google Scholar
• Zhou X, Lin DS, Zheng F, Sutton MA, Wang H. 2010. Intracellular calcium and calmodulin link brain-derived neurotrophic factor to p70S6 kinase phosphorylation and dendritic protein synthesis. J Neurosci Res. 88:1420–1432.
   PubMed Web of Science ®Google Scholar