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Published in: European Journal of Nutrition 4/2020

01-06-2020 | Diabetes | Review

The neuroprotective effect and action mechanism of polyphenols in diabetes mellitus-related cognitive dysfunction

Authors: Shenshen Zhang, Ran Xue, Ruizhe Hu

Published in: European Journal of Nutrition | Issue 4/2020

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Abstract

Background

Diabetes mellitus (DM) is a complex and prevalent metabolic disorder worldwide. Strong evidence has emerged that DM is a risk factor for the accelerated rate of cognitive decline and the development of dementia. Though traditional pharmaceutical agents are efficient for the management of DM and DM-related cognitive decrement, long-term use of these drugs are along with undesired side effects. Therefore, tremendous studies have focused on the therapeutic benefits of natural compounds at present. Ample evidence exists to prove that polyphenols are capable to modulate diabetic neuropathy with minimal toxicity and adverse effects.

Purpose

To describe the benefits and mechanisms of polyphenols on DM-induced cognitive dysfunction. In this review, we introduce an updated overview of associations between DM and cognitive dysfunction. The risk factors as well as pathological and molecular mechanisms of DM-induced cognitive dysfunction are summarized. More importantly, many active polyphenols that possess preventive and therapeutic effects on DM-induced cognitive dysfunction and the potential signaling pathways involved in the action are highlighted.

Conclusions

The therapeutic effects of polyphenols on DM-related cognitive dysfunction pave a novel way for the management of diabetic encephalopathy.
Literature
9.
16.
29.
go back to reference Geijselaers SLC, Sep SJS, Claessens D, Schram MT, van Boxtel MPJ, Henry RMA, Verhey FRJ, Kroon AA, Dagnelie PC, Schalkwijk CG, van der Kallen CJH, Biessels GJ, Stehouwer CDA (2017) The role of hyperglycemia, insulin resistance, and blood pressure in diabetes-associated differences in cognitive performance—the Maastricht study. Diabetes Care 40(11):1537–1547. https://doi.org/10.2337/dc17-0330 CrossRefPubMed Geijselaers SLC, Sep SJS, Claessens D, Schram MT, van Boxtel MPJ, Henry RMA, Verhey FRJ, Kroon AA, Dagnelie PC, Schalkwijk CG, van der Kallen CJH, Biessels GJ, Stehouwer CDA (2017) The role of hyperglycemia, insulin resistance, and blood pressure in diabetes-associated differences in cognitive performance—the Maastricht study. Diabetes Care 40(11):1537–1547. https://​doi.​org/​10.​2337/​dc17-0330 CrossRefPubMed
37.
go back to reference Punthakee Z, Miller ME, Launer LJ, Williamson JD, Lazar RM, Cukierman-Yaffee T, Seaquist ER, Ismail-Beigi F, Sullivan MD, Lovato LC, Bergenstal RM, Gerstein HC, Investigators AGo, Investigators A-M, (2012) Poor cognitive function and risk of severe hypoglycemia in type 2 diabetes: post hoc epidemiologic analysis of the ACCORD trial. Diabetes Care 35(4):787–793. https://doi.org/10.2337/dc11-1855 CrossRefPubMedPubMedCentral Punthakee Z, Miller ME, Launer LJ, Williamson JD, Lazar RM, Cukierman-Yaffee T, Seaquist ER, Ismail-Beigi F, Sullivan MD, Lovato LC, Bergenstal RM, Gerstein HC, Investigators AGo, Investigators A-M, (2012) Poor cognitive function and risk of severe hypoglycemia in type 2 diabetes: post hoc epidemiologic analysis of the ACCORD trial. Diabetes Care 35(4):787–793. https://​doi.​org/​10.​2337/​dc11-1855 CrossRefPubMedPubMedCentral
39.
go back to reference Zemva J, Schubert M (2014) The role of neuronal insulin/insulin-like growth factor-1 signaling for the pathogenesis of Alzheimer’s disease: possible therapeutic implications. CNS Neurol Disord Drug Targets 13(2):322–337CrossRefPubMed Zemva J, Schubert M (2014) The role of neuronal insulin/insulin-like growth factor-1 signaling for the pathogenesis of Alzheimer’s disease: possible therapeutic implications. CNS Neurol Disord Drug Targets 13(2):322–337CrossRefPubMed
41.
go back to reference 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 JAD 8(3):247–268CrossRefPubMed 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 JAD 8(3):247–268CrossRefPubMed
42.
go back to reference Biessels GJ, van der Heide LP, Kamal A, Bleys RL, Gispen WH (2002) Ageing and diabetes: implications for brain function. Eur J Pharmacol 441(1–2):1–14CrossRefPubMed Biessels GJ, van der Heide LP, Kamal A, Bleys RL, Gispen WH (2002) Ageing and diabetes: implications for brain function. Eur J Pharmacol 441(1–2):1–14CrossRefPubMed
55.
go back to reference Nadeau S, Rivest S (2000) Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor kappa B activity in the brain during endotoxemia. J Neurosci Off J Soc Neurosci 20(9):3456–3468CrossRef Nadeau S, Rivest S (2000) Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor kappa B activity in the brain during endotoxemia. J Neurosci Off J Soc Neurosci 20(9):3456–3468CrossRef
56.
go back to reference Marioni RE, Strachan MW, Reynolds RM, Lowe GD, Mitchell RJ, Fowkes FG, Frier BM, Lee AJ, Butcher I, Rumley A, Murray GD, Deary IJ, Price JF (2010) Association between raised inflammatory markers and cognitive decline in elderly people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes 59(3):710–713. https://doi.org/10.2337/db09-1163 CrossRefPubMed Marioni RE, Strachan MW, Reynolds RM, Lowe GD, Mitchell RJ, Fowkes FG, Frier BM, Lee AJ, Butcher I, Rumley A, Murray GD, Deary IJ, Price JF (2010) Association between raised inflammatory markers and cognitive decline in elderly people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes 59(3):710–713. https://​doi.​org/​10.​2337/​db09-1163 CrossRefPubMed
58.
go back to reference Lavielle P, Talavera JO, Reynoso N, Gonzalez M, Gomez-Diaz RA, Cruz M, Vazquez F, Wacher NH, Group DS (2015) Prevalence of cognitive impairment in recently diagnosed type 2 diabetes patients: are chronic inflammatory diseases responsible for cognitive decline? PLoS One 10(10):e0141325CrossRefPubMedPubMedCentral Lavielle P, Talavera JO, Reynoso N, Gonzalez M, Gomez-Diaz RA, Cruz M, Vazquez F, Wacher NH, Group DS (2015) Prevalence of cognitive impairment in recently diagnosed type 2 diabetes patients: are chronic inflammatory diseases responsible for cognitive decline? PLoS One 10(10):e0141325CrossRefPubMedPubMedCentral
63.
go back to reference Feinkohl I, Keller M, Robertson CM, Morling JR, Williamson RM, Nee LD, McLachlan S, Sattar N, Welsh P, Reynolds RM, Russ TC, Deary IJ, Strachan MW, Price JF (2013) Clinical and subclinical macrovascular disease as predictors of cognitive decline in older patients with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes Care 36(9):2779–2786CrossRefPubMedPubMedCentral Feinkohl I, Keller M, Robertson CM, Morling JR, Williamson RM, Nee LD, McLachlan S, Sattar N, Welsh P, Reynolds RM, Russ TC, Deary IJ, Strachan MW, Price JF (2013) Clinical and subclinical macrovascular disease as predictors of cognitive decline in older patients with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes Care 36(9):2779–2786CrossRefPubMedPubMedCentral
73.
go back to reference Zirpel L, Janowiak MA, Veltri CA, Parks TN (2000) AMPA receptor-mediated, calcium-dependent CREB phosphorylation in a subpopulation of auditory neurons surviving activity deprivation. J Neurosci Off J Soc Neurosci 20(16):6267–6275CrossRef Zirpel L, Janowiak MA, Veltri CA, Parks TN (2000) AMPA receptor-mediated, calcium-dependent CREB phosphorylation in a subpopulation of auditory neurons surviving activity deprivation. J Neurosci Off J Soc Neurosci 20(16):6267–6275CrossRef
74.
go back to reference Srivastava P, Dhuriya YK, Kumar V, Srivastava A, Gupta R, Shukla RK, Yadav RS, Dwivedi HN, Pant AB, Khanna VK (2018) PI3K/Akt/GSK3beta induced CREB activation ameliorates arsenic mediated alterations in NMDA receptors and associated signaling in rat hippocampus: neuroprotective role of curcumin. Neurotoxicology 67:190–205. https://doi.org/10.1016/j.neuro.2018.04.018 CrossRefPubMed Srivastava P, Dhuriya YK, Kumar V, Srivastava A, Gupta R, Shukla RK, Yadav RS, Dwivedi HN, Pant AB, Khanna VK (2018) PI3K/Akt/GSK3beta induced CREB activation ameliorates arsenic mediated alterations in NMDA receptors and associated signaling in rat hippocampus: neuroprotective role of curcumin. Neurotoxicology 67:190–205. https://​doi.​org/​10.​1016/​j.​neuro.​2018.​04.​018 CrossRefPubMed
85.
go back to reference Sato K, Suematsu A, Nakashima T, Takemoto-Kimura S, Aoki K, Morishita Y, Asahara H, Ohya K, Yamaguchi A, Takai T, Kodama T, Chatila TA, Bito H, Takayanagi H (2006) Regulation of osteoclast differentiation and function by the CaMK–CREB pathway. Nat Med 12(12):1410–1416. https://doi.org/10.1038/nm1515 CrossRefPubMed Sato K, Suematsu A, Nakashima T, Takemoto-Kimura S, Aoki K, Morishita Y, Asahara H, Ohya K, Yamaguchi A, Takai T, Kodama T, Chatila TA, Bito H, Takayanagi H (2006) Regulation of osteoclast differentiation and function by the CaMK–CREB pathway. Nat Med 12(12):1410–1416. https://​doi.​org/​10.​1038/​nm1515 CrossRefPubMed
88.
96.
go back to reference McNeilly AD, Gallagher JR, Dinkova-Kostova AT, Hayes JD, Sharkey J, Ashford ML, McCrimmon RJ (2016) Nrf2-mediated neuroprotection against recurrent hypoglycemia is insufficient to prevent cognitive impairment in a rodent model of type 1 diabetes. Diabetes 65(10):3151–3160. https://doi.org/10.2337/db15-1653 CrossRefPubMed McNeilly AD, Gallagher JR, Dinkova-Kostova AT, Hayes JD, Sharkey J, Ashford ML, McCrimmon RJ (2016) Nrf2-mediated neuroprotection against recurrent hypoglycemia is insufficient to prevent cognitive impairment in a rodent model of type 1 diabetes. Diabetes 65(10):3151–3160. https://​doi.​org/​10.​2337/​db15-1653 CrossRefPubMed
97.
go back to reference Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM, Zvartau-Hind ME, Hosford DA, Roses AD, Rosiglitazone in Alzheimer’s Disease Study G (2006) Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer’s disease. Pharmacogenom J 6(4):246–254. https://doi.org/10.1038/sj.tpj.6500369 CrossRef Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM, Zvartau-Hind ME, Hosford DA, Roses AD, Rosiglitazone in Alzheimer’s Disease Study G (2006) Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer’s disease. Pharmacogenom J 6(4):246–254. https://​doi.​org/​10.​1038/​sj.​tpj.​6500369 CrossRef
98.
go back to reference Claxton A, Baker LD, Hanson A, Trittschuh EH, Cholerton B, Morgan A, Callaghan M, Arbuckle M, Behl C, Craft S (2015) Long-acting intranasal insulin detemir improves cognition for adults with mild cognitive impairment or early-stage Alzheimer’s disease dementia. J Alzheimers Dis JAD 44(3):897–906. https://doi.org/10.3233/JAD-141791 CrossRefPubMed Claxton A, Baker LD, Hanson A, Trittschuh EH, Cholerton B, Morgan A, Callaghan M, Arbuckle M, Behl C, Craft S (2015) Long-acting intranasal insulin detemir improves cognition for adults with mild cognitive impairment or early-stage Alzheimer’s disease dementia. J Alzheimers Dis JAD 44(3):897–906. https://​doi.​org/​10.​3233/​JAD-141791 CrossRefPubMed
99.
go back to reference Alagiakrishnan K, Sankaralingam S, Ghosh M, Mereu L, Senior P (2013) Antidiabetic drugs and their potential role in treating mild cognitive impairment and Alzheimer’s disease. Discov Med 16(90):277–286PubMed Alagiakrishnan K, Sankaralingam S, Ghosh M, Mereu L, Senior P (2013) Antidiabetic drugs and their potential role in treating mild cognitive impairment and Alzheimer’s disease. Discov Med 16(90):277–286PubMed
121.
go back to reference Reddy PH, Manczak M, Yin X, Grady MC, Mitchell A, Tonk S, Kuruva CS, Bhatti JS, Kandimalla R, Vijayan M, Kumar S, Wang R, Pradeepkiran JA, Ogunmokun G, Thamarai K, Quesada K, Boles A, Reddy AP (2018) Protective effects of indian spice curcumin against amyloid-beta in Alzheimer’s disease. J Alzheimers Dis JAD 61(3):843–866. https://doi.org/10.3233/JAD-170512 CrossRefPubMed Reddy PH, Manczak M, Yin X, Grady MC, Mitchell A, Tonk S, Kuruva CS, Bhatti JS, Kandimalla R, Vijayan M, Kumar S, Wang R, Pradeepkiran JA, Ogunmokun G, Thamarai K, Quesada K, Boles A, Reddy AP (2018) Protective effects of indian spice curcumin against amyloid-beta in Alzheimer’s disease. J Alzheimers Dis JAD 61(3):843–866. https://​doi.​org/​10.​3233/​JAD-170512 CrossRefPubMed
129.
go back to reference Small GW, Siddarth P, Li Z, Miller KJ, Ercoli L, Emerson ND, Martinez J, Wong KP, Liu J, Merrill DA, Chen ST, Henning SM, Satyamurthy N, Huang SC, Heber D, Barrio JR (2018) Memory and brain amyloid and tau effects of a bioavailable form of curcumin in non-demented adults: a double-blind, placebo-controlled 18-month trial. Am J Geriatr Psychiatry Off J Am Assoc Geriatr Psychiatry 26(3):266–277. https://doi.org/10.1016/j.jagp.2017.10.010 CrossRef Small GW, Siddarth P, Li Z, Miller KJ, Ercoli L, Emerson ND, Martinez J, Wong KP, Liu J, Merrill DA, Chen ST, Henning SM, Satyamurthy N, Huang SC, Heber D, Barrio JR (2018) Memory and brain amyloid and tau effects of a bioavailable form of curcumin in non-demented adults: a double-blind, placebo-controlled 18-month trial. Am J Geriatr Psychiatry Off J Am Assoc Geriatr Psychiatry 26(3):266–277. https://​doi.​org/​10.​1016/​j.​jagp.​2017.​10.​010 CrossRef
133.
go back to reference Tian Z, Wang J, Xu M, Wang Y, Zhang M, Zhou Y (2016) Resveratrol improves cognitive impairment by regulating apoptosis and synaptic plasticity in streptozotocin-induced diabetic rats. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 40(6):1670–1677. https://doi.org/10.1159/000453216 CrossRef Tian Z, Wang J, Xu M, Wang Y, Zhang M, Zhou Y (2016) Resveratrol improves cognitive impairment by regulating apoptosis and synaptic plasticity in streptozotocin-induced diabetic rats. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 40(6):1670–1677. https://​doi.​org/​10.​1159/​000453216 CrossRef
137.
go back to reference Huber JD (2008) Diabetes, cognitive function, and the blood–brain barrier. Curr Pharm Des 14(16):1594–1600CrossRefPubMed Huber JD (2008) Diabetes, cognitive function, and the blood–brain barrier. Curr Pharm Des 14(16):1594–1600CrossRefPubMed
140.
go back to reference Schmatz R, Mazzanti CM, Spanevello R, Stefanello N, Gutierres J, Maldonado PA, Correa M, da Rosa CS, Becker L, Bagatini M, Goncalves JF, Jaques Jdos S, Schetinger MR, Morsch VM (2009) Ectonucleotidase and acetylcholinesterase activities in synaptosomes from the cerebral cortex of streptozotocin-induced diabetic rats and treated with resveratrol. Brain Res Bull 80(6):371–376. https://doi.org/10.1016/j.brainresbull.2009.08.019 CrossRefPubMed Schmatz R, Mazzanti CM, Spanevello R, Stefanello N, Gutierres J, Maldonado PA, Correa M, da Rosa CS, Becker L, Bagatini M, Goncalves JF, Jaques Jdos S, Schetinger MR, Morsch VM (2009) Ectonucleotidase and acetylcholinesterase activities in synaptosomes from the cerebral cortex of streptozotocin-induced diabetic rats and treated with resveratrol. Brain Res Bull 80(6):371–376. https://​doi.​org/​10.​1016/​j.​brainresbull.​2009.​08.​019 CrossRefPubMed
146.
go back to reference Gormaz JG, Quintremil S, Rodrigo R (2015) Cardiovascular disease: a target for the pharmacological effects of quercetin. Curr Top Med Chem 15(17):1735–1742CrossRefPubMed Gormaz JG, Quintremil S, Rodrigo R (2015) Cardiovascular disease: a target for the pharmacological effects of quercetin. Curr Top Med Chem 15(17):1735–1742CrossRefPubMed
151.
go back to reference Maciel RM, Carvalho FB, Olabiyi AA, Schmatz R, Gutierres JM, Stefanello N, Zanini D, Rosa MM, Andrade CM, Rubin MA, Schetinger MR, Morsch VM, Danesi CC, Lopes STA (2016) Neuroprotective effects of quercetin on memory and anxiogenic-like behavior in diabetic rats: role of ectonucleotidases and acetylcholinesterase activities. Biomed Pharmacother Biomedecine pharmacotherapie 84:559–568. https://doi.org/10.1016/j.biopha.2016.09.069 CrossRefPubMed Maciel RM, Carvalho FB, Olabiyi AA, Schmatz R, Gutierres JM, Stefanello N, Zanini D, Rosa MM, Andrade CM, Rubin MA, Schetinger MR, Morsch VM, Danesi CC, Lopes STA (2016) Neuroprotective effects of quercetin on memory and anxiogenic-like behavior in diabetic rats: role of ectonucleotidases and acetylcholinesterase activities. Biomed Pharmacother Biomedecine pharmacotherapie 84:559–568. https://​doi.​org/​10.​1016/​j.​biopha.​2016.​09.​069 CrossRefPubMed
156.
go back to reference Nakagawa T, Itoh M, Ohta K, Hayashi Y, Hayakawa M, Yamada Y, Akanabe H, Chikaishi T, Nakagawa K, Itoh Y, Muro T, Yanagida D, Nakabayashi R, Mori T, Saito K, Ohzawa K, Suzuki C, Li S, Ueda M, Wang MX, Nishida E, Islam S, Tana Kobori M, Inuzuka T (2016) Improvement of memory recall by quercetin in rodent contextual fear conditioning and human early-stage Alzheimer’s disease patients. NeuroReport 27(9):671–676. https://doi.org/10.1097/WNR.0000000000000594 CrossRefPubMed Nakagawa T, Itoh M, Ohta K, Hayashi Y, Hayakawa M, Yamada Y, Akanabe H, Chikaishi T, Nakagawa K, Itoh Y, Muro T, Yanagida D, Nakabayashi R, Mori T, Saito K, Ohzawa K, Suzuki C, Li S, Ueda M, Wang MX, Nishida E, Islam S, Tana Kobori M, Inuzuka T (2016) Improvement of memory recall by quercetin in rodent contextual fear conditioning and human early-stage Alzheimer’s disease patients. NeuroReport 27(9):671–676. https://​doi.​org/​10.​1097/​WNR.​0000000000000594​ CrossRefPubMed
161.
go back to reference Bonet-Costa V, Herranz-Perez V, Blanco-Gandia M, Mas-Bargues C, Ingles M, Garcia-Tarraga P, Rodriguez-Arias M, Minarro J, Borras C, Garcia-Verdugo JM, Vina J (2016) Clearing amyloid-beta through PPARgamma/ApoE activation by genistein is a treatment of experimental Alzheimer’s disease. J Alzheimers Dis JAD 51(3):701–711. https://doi.org/10.3233/JAD-151020 CrossRefPubMed Bonet-Costa V, Herranz-Perez V, Blanco-Gandia M, Mas-Bargues C, Ingles M, Garcia-Tarraga P, Rodriguez-Arias M, Minarro J, Borras C, Garcia-Verdugo JM, Vina J (2016) Clearing amyloid-beta through PPARgamma/ApoE activation by genistein is a treatment of experimental Alzheimer’s disease. J Alzheimers Dis JAD 51(3):701–711. https://​doi.​org/​10.​3233/​JAD-151020 CrossRefPubMed
170.
go back to reference Sharifzadeh M, Ranjbar A, Hosseini A, Khanavi M (2017) The effect of green tea extract on oxidative stress and spatial learning in streptozotocin-diabetic rats. Iran J Pharm Res IJPR 16(1):201–209PubMed Sharifzadeh M, Ranjbar A, Hosseini A, Khanavi M (2017) The effect of green tea extract on oxidative stress and spatial learning in streptozotocin-diabetic rats. Iran J Pharm Res IJPR 16(1):201–209PubMed
175.
go back to reference Ola MS, Aleisa AM, Al-Rejaie SS, Abuohashish HM, Parmar MY, Alhomida AS, Ahmed MM (2014) Flavonoid, morin inhibits oxidative stress, inflammation and enhances neurotrophic support in the brain of streptozotocin-induced diabetic rats. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol 35(7):1003–1008. https://doi.org/10.1007/s10072-014-1628-5 CrossRef Ola MS, Aleisa AM, Al-Rejaie SS, Abuohashish HM, Parmar MY, Alhomida AS, Ahmed MM (2014) Flavonoid, morin inhibits oxidative stress, inflammation and enhances neurotrophic support in the brain of streptozotocin-induced diabetic rats. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol 35(7):1003–1008. https://​doi.​org/​10.​1007/​s10072-014-1628-5 CrossRef
177.
go back to reference Mirshekar M, Roghani M, Khalili M, Baluchnejadmojarad T (2011) Chronic oral pelargonidin alleviates learning and memory disturbances in streptozotocin diabetic rats. Iran J Pharm Res IJPR 10(3):569–575PubMed Mirshekar M, Roghani M, Khalili M, Baluchnejadmojarad T (2011) Chronic oral pelargonidin alleviates learning and memory disturbances in streptozotocin diabetic rats. Iran J Pharm Res IJPR 10(3):569–575PubMed
178.
go back to reference Mirshekar M, Roghani M, Khalili M, Baluchnejadmojarad T, Arab Moazzen S (2010) Chronic oral pelargonidin alleviates streptozotocin-induced diabetic neuropathic hyperalgesia in rat: involvement of oxidative stress. Iran Biomed J 14(1–2):33–39PubMedPubMedCentral Mirshekar M, Roghani M, Khalili M, Baluchnejadmojarad T, Arab Moazzen S (2010) Chronic oral pelargonidin alleviates streptozotocin-induced diabetic neuropathic hyperalgesia in rat: involvement of oxidative stress. Iran Biomed J 14(1–2):33–39PubMedPubMedCentral
185.
go back to reference Semaming Y, Sripetchwandee J, Sa-Nguanmoo P, Pintana H, Pannangpetch P, Chattipakorn N, Chattipakorn SC (2015) Protocatechuic acid protects brain mitochondrial function in streptozotocin-induced diabetic rats. Appl Physiol Nutr Metab Physiologie appliquee, nutrition et metabolisme 40(10):1078–1081. https://doi.org/10.1139/apnm-2015-0158 CrossRefPubMed Semaming Y, Sripetchwandee J, Sa-Nguanmoo P, Pintana H, Pannangpetch P, Chattipakorn N, Chattipakorn SC (2015) Protocatechuic acid protects brain mitochondrial function in streptozotocin-induced diabetic rats. Appl Physiol Nutr Metab Physiologie appliquee, nutrition et metabolisme 40(10):1078–1081. https://​doi.​org/​10.​1139/​apnm-2015-0158 CrossRefPubMed
186.
go back to reference Adedara IA, Fasina OB, Ayeni MF, Ajayi OM, Farombi EO (2019) Protocatechuic acid ameliorates neurobehavioral deficits via suppression of oxidative damage, inflammation, caspase-3 and acetylcholinesterase activities in diabetic rats. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc 125:170–181. https://doi.org/10.1016/j.fct.2018.12.040 CrossRef Adedara IA, Fasina OB, Ayeni MF, Ajayi OM, Farombi EO (2019) Protocatechuic acid ameliorates neurobehavioral deficits via suppression of oxidative damage, inflammation, caspase-3 and acetylcholinesterase activities in diabetic rats. Food Chem Toxicol Int J Publ Br Ind Biol Res Assoc 125:170–181. https://​doi.​org/​10.​1016/​j.​fct.​2018.​12.​040 CrossRef
Metadata
Title
The neuroprotective effect and action mechanism of polyphenols in diabetes mellitus-related cognitive dysfunction
Authors
Shenshen Zhang
Ran Xue
Ruizhe Hu
Publication date
01-06-2020
Publisher
Springer Berlin Heidelberg
Keyword
Diabetes
Published in
European Journal of Nutrition / Issue 4/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-019-02078-2

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