Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Review Article

Dietary Flavonoids and Adult Neurogenesis: Potential Implications for Brain Aging

Author(s): Sergio Davinelli*, Alessandro Medoro, Sawan Ali, Daniela Passarella, Mariano Intrieri and Giovanni Scapagnini

Volume 21, Issue 3, 2023

Published on: 03 November, 2022

Page: [651 - 668] Pages: 18

DOI: 10.2174/1570159X21666221031103909

Price: $65

Abstract

Adult neurogenesis deficiency has been proposed to be a common hallmark in different age-related neurodegenerative diseases. The administration of flavonoids is currently reported as a potentially beneficial strategy for preventing brain aging alterations, including adult neurogenesis decline. Flavonoids are a class of plant-derived dietary polyphenols that have drawn attention for their neuroprotective and pro-cognitive effects. Although they undergo extensive metabolism and localize in the brain at low concentrations, flavonoids are now believed to improve cerebral vasculature and interact with signal transduction cascades involved in the regulation of adult neurogenesis. Furthermore, many dietary flavonoids have been shown to reduce oxidative stress and neuroinflammation, improving the neuronal microenvironment where adult neurogenesis occurs. The overall goal of this review is to summarize the evidence supporting the role of flavonoids in modulating adult neurogenesis as well as to highlight how these dietary agents may be promising candidates in restoring healthy brain function during physiological and pathological aging.

« Previous Next »
Graphical Abstract

[1]
Mattson, M.P.; Arumugam, T.V. Hallmarks of brain aging: Adaptive and pathological modification by metabolic states. Cell Metab., 2018, 27(6), 1176-1199.
[http://dx.doi.org/10.1016/j.cmet.2018.05.011] [PMID: 29874566]
[2]
Wrigglesworth, J.; Ward, P.; Harding, I.H.; Nilaweera, D.; Wu, Z.; Woods, R.L.; Ryan, J. Factors associated with brain ageing - a systematic review. BMC Neurol., 2021, 21(1), 1-23.
[http://dx.doi.org/10.1186/s12883-021-02331-4]
[3]
Culig, L.; Chu, X.; Bohr, V.A. Neurogenesis in aging and age-related neurodegenerative diseases. Ageing Res. Rev., 2022, 78, 101636.
[http://dx.doi.org/10.1016/j.arr.2022.101636] [PMID: 35490966]
[4]
Jurkowski, M.P.; Bettio, L.K.; Woo, E.; Patten, A.; Yau, S.Y.; Gil-Mohapel, J. Beyond the hippocampus and the SVZ: Adult neurogenesis throughout the brain. Front. Cell. Neurosci., 2020, 14, 576444.
[http://dx.doi.org/10.3389/fncel.2020.576444] [PMID: 33132848]
[5]
Leal-Galicia, P.; Chávez-Hernández, M.E.; Mata, F.; Mata-Luévanos, J.; Rodríguez-Serrano, L.M.; Tapia-de-Jesús, A.; Buenrostro-Jáuregui, M.H. Adult neurogenesis: A story ranging from controversial new neurogenic areas and human adult neurogenesis to molecular regulation. Int. J. Mol. Sci., 2021, 22(21), 11489.
[http://dx.doi.org/10.3390/ijms222111489] [PMID: 34768919]
[6]
Denoth-Lippuner, A.; Jessberger, S. Formation and integration of new neurons in the adult hippocampus. Nat. Rev. Neurosci., 2021, 22(4), 223-236.
[http://dx.doi.org/10.1038/s41583-021-00433-z] [PMID: 33633402]
[7]
Niklison-Chirou, M.V.; Agostini, M.; Amelio, I.; Melino, G. Regulation of adult neurogenesis in mammalian brain. Int. J. Mol. Sci., 2020, 21(14), 4869.
[http://dx.doi.org/10.3390/ijms21144869] [PMID: 32660154]
[8]
Valente, T.; Hidalgo, J.; Bolea, I.; Ramirez, B.; Anglés, N.; Reguant, J.; Morelló, J.R.; Gutiérrez, C.; Boada, M.; Unzeta, M. A diet enriched in polyphenols and polyunsaturated fatty acids, LMN diet, induces neurogenesis in the subventricular zone and hippocampus of adult mouse brain. J. Alzheimers Dis., 2009, 18(4), 849-865.
[http://dx.doi.org/10.3233/JAD-2009-1188] [PMID: 19661617]
[9]
Kim, S.J.; Son, T.G.; Park, H.R.; Park, M.; Kim, M.S.; Kim, H.S.; Chung, H.Y.; Mattson, M.P.; Lee, J. Curcumin stimulates proliferation of embryonic neural progenitor cells and neurogenesis in the adult hippocampus. J. Biol. Chem., 2008, 283(21), 14497-14505.
[http://dx.doi.org/10.1074/jbc.M708373200] [PMID: 18362141]
[10]
Torres-Pérez, M.; Tellez-Ballesteros, R.I.; Ortiz-López, L.; Ichwan, M.; Vega-Rivera, N.M.; Castro-García, M.; Gómez-Sánchez, A.; Kempermann, G.; Ramirez-Rodriguez, G.B. Resveratrol enhances neuroplastic changes, including hippocampal neurogenesis, and memory in Balb/C mice at six months of age. PLoS One, 2015, 10(12), e0145687.
[http://dx.doi.org/10.1371/journal.pone.0145687] [PMID: 26695764]
[11]
Davinelli, S.; Sapere, N.; Zella, D.; Bracale, R.; Intrieri, M.; Scapagnini, G. Pleiotropic protective effects of phytochemicals in Alzheimer’s disease. Oxid. Med. Cell. Longev., 2012, 2012, 1-11.
[http://dx.doi.org/10.1155/2012/386527] [PMID: 22690271]
[12]
Zhang, S.; Lam, K.K.H.; Wan, J.H.; Yip, C.W.; Liu, H.K.H.; Lau, Q.M.N.; Man, A.H.Y.; Cheung, C.H.; Wong, L.H.; Chen, H.B.; Shi, J.; Leung, G.P-H.; Lee, C.K-F.; Shi, Y-G.; Tang, S.C-W.; Zhang, K.Y.B. Dietary phytochemical approaches to stem cell regulation. J. Funct. Foods, 2020, 66, 103822.
[http://dx.doi.org/10.1016/j.jff.2020.103822]
[13]
Williams, R.J.; Spencer, J.P.E. Flavonoids, cognition, and dementia: Actions, mechanisms, and potential therapeutic utility for Alzheimer disease. Free Radic. Biol. Med., 2012, 52(1), 35-45.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.09.010] [PMID: 21982844]
[14]
Ali, S.; Corbi, G.; Maes, M.; Scapagnini, G.; Davinelli, S. Exploring the impact of flavonoids on symptoms of depression: A systematic review and meta-analysis. Antioxidants, 2021, 10(11), 1644.
[http://dx.doi.org/10.3390/antiox10111644] [PMID: 34829515]
[15]
Ayaz, M.; Sadiq, A.; Junaid, M.; Ullah, F.; Ovais, M.; Ullah, I.; Ahmed, J.; Shahid, M. Flavonoids as prospective neuroprotectants and their therapeutic propensity in aging associated neurological disorders. Front. Aging Neurosci., 2019, 11, 155.
[http://dx.doi.org/10.3389/fnagi.2019.00155] [PMID: 31293414]
[16]
Letenneur, L.; Proust-Lima, C.; Le Gouge, A.; Dartigues, J.; Barberger-Gateau, P. Flavonoid intake and cognitive decline over a 10-year period. Am. J. Epidemiol., 2007, 165(12), 1364-1371.
[http://dx.doi.org/10.1093/aje/kwm036] [PMID: 17369607]
[17]
Nurk, E.; Refsum, H.; Drevon, C.A.; Tell, G.S.; Nygaard, H.A.; Engedal, K.; Smith, A.D. Intake of flavonoid-rich wine, tea, and chocolate by elderly men and women is associated with better cognitive test performance. J. Nutr., 2009, 139(1), 120-127.
[http://dx.doi.org/10.3945/jn.108.095182] [PMID: 19056649]
[18]
Yeh, T.S.; Yuan, C.; Ascherio, A.; Rosner, B.A.; Willett, W.C.; Blacker, D. Long-term dietary flavonoid intake and subjective cognitive decline in US men and women. Neurology, 2021, 97(10), e1041-e1056.
[http://dx.doi.org/10.1212/WNL.0000000000012454] [PMID: 34321362]
[19]
Davinelli, S.; Maes, M.; Corbi, G.; Zarrelli, A.; Willcox, D.C.; Scapagnini, G. Dietary phytochemicals and neuro-inflammaging: From mechanistic insights to translational challenges. Immun. Ageing, 2016, 13(1), 16.
[http://dx.doi.org/10.1186/s12979-016-0070-3] [PMID: 27081392]
[20]
Haskell-Ramsay, C.; Schmitt, J.; Actis-Goretta, L. The impact of epicatechin on human cognition: The role of cerebral blood flow. Nutrients, 2018, 10(8), 986.
[http://dx.doi.org/10.3390/nu10080986] [PMID: 30060538]
[21]
Flanagan, E.; Müller, M.; Hornberger, M.; Vauzour, D. Impact of flavonoids on cellular and molecular mechanisms underlying age-related cognitive decline and neurodegeneration. Curr. Nutr. Rep., 2018, 7(2), 49-57.
[http://dx.doi.org/10.1007/s13668-018-0226-1] [PMID: 29892788]
[22]
Panche, A.N.; Diwan, A.D.; Chandra, S.R. Flavonoids: An overview. J. Nutr. Sci., 2016, 5, e47.
[http://dx.doi.org/10.1017/jns.2016.41] [PMID: 28620474]
[23]
Aherne, S.A.; O’Brien, N.M. Dietary flavonols: Chemistry, food content, and metabolism. Nutrition, 2002, 18(1), 75-81.
[http://dx.doi.org/10.1016/S0899-9007(01)00695-5] [PMID: 11827770]
[24]
Tsao, R. Chemistry and biochemistry of dietary polyphenols. Nutrients, 2010, 2(12), 1231-1246.
[http://dx.doi.org/10.3390/nu2121231] [PMID: 22254006]
[25]
Kim, K.; Vance, T.M.; Chun, O.K. Estimated intake and major food sources of flavonoids among US adults: Changes between 1999-2002 and 2007-2010 in NHANES. Eur. J. Nutr., 2015, 55(2), 833-843.
[http://dx.doi.org/10.1007/s00394-015-0942-x]
[26]
Sebastian, R.S.; Wilkinson Enns, C.; Goldman, J.D.; Martin, C.L.; Steinfeldt, L.C.; Murayi, T.; Moshfegh, A.J. A new database facilitates characterization of flavonoid intake, sources, and positive associations with diet quality among US adults. J. Nutr., 2015, 145(6), 1239-1248.
[http://dx.doi.org/10.3945/jn.115.213025] [PMID: 25948787]
[27]
Manach, C.; Scalbert, A.; Morand, C.; Rémésy, C.; Jiménez, L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr., 2004, 79(5), 727-747.
[http://dx.doi.org/10.1093/ajcn/79.5.727] [PMID: 15113710]
[28]
Iwashina, T. Flavonoid properties of five families newly incorporated into the order caryophyllales. Bull. Natl. Mus. Nat. Sci. Ser. B Bot., 2013, 39, 25-51.
[29]
Hackman, R.M.; Polagruto, J.A.; Zhu, Q.Y.; Sun, B.; Fujii, H.; Keen, C.L. Flavanols: Digestion, absorption and bioactivity. Phytochem. Rev., 2007, 7(1), 195-208.
[http://dx.doi.org/10.1007/s11101-007-9070-4]
[30]
Křížová, L.; Dadáková, K.; Kašparovská, J.; Kašparovský, T. Isoflavones. Molecules, 2019, 24(6), 1076.
[http://dx.doi.org/10.3390/molecules24061076] [PMID: 30893792]
[31]
Jaakola, L. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci., 2013, 18(9), 477-483.
[http://dx.doi.org/10.1016/j.tplants.2013.06.003] [PMID: 23870661]
[32]
Manach, C.; Williamson, G.; Morand, C.; Scalbert, A.; Rémésy, C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr., 2005, 81(1)(Suppl.), 230S-242S.
[http://dx.doi.org/10.1093/ajcn/81.1.230S] [PMID: 15640486]
[33]
Thilakarathna, S.; Rupasinghe, H. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients, 2013, 5(9), 3367-3387.
[http://dx.doi.org/10.3390/nu5093367] [PMID: 23989753]
[34]
Lotito, S.B.; Zhang, W.J.; Yang, C.S.; Crozier, A.; Frei, B. Metabolic conversion of dietary flavonoids alters their anti-inflammatory and antioxidant properties. Free Radic. Biol. Med., 2011, 51(2), 454-463.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.032] [PMID: 21571063]
[35]
Kamiloglu, S.; Tomas, M.; Ozdal, T.; Capanoglu, E. Effect of food matrix on the content and bioavailability of flavonoids. Trends Food Sci. Technol., 2021, 117, 15-33.
[http://dx.doi.org/10.1016/j.tifs.2020.10.030]
[36]
Zhang, H.; Yu, D.; Sun, J.; Liu, X.; Jiang, L.; Guo, H.; Ren, F. Interaction of plant phenols with food macronutrients: Characterisation and nutritional-physiological consequences. Nutr. Res. Rev., 2014, 27(1), 1-15.
[http://dx.doi.org/10.1017/S095442241300019X] [PMID: 24169001]
[37]
Braune, A.; Blaut, M. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes, 2016, 7(3), 216-234.
[http://dx.doi.org/10.1080/19490976.2016.1158395] [PMID: 26963713]
[38]
Sorrenti, V.; Ali, S.; Mancin, L.; Davinelli, S.; Paoli, A.; Scapagnini, G. Cocoa polyphenols and gut microbiota interplay: Bioavailability, prebiotic effect, and impact on human health. Nutrients, 2020, 12(7), 1908.
[http://dx.doi.org/10.3390/nu12071908] [PMID: 32605083]
[39]
Davinelli, S.; Scapagnini, G. Interactions between dietary polyphenols and aging gut microbiota: A review. Biofactors, 2022, 48(2), 274-284.
[http://dx.doi.org/10.1002/biof.1785] [PMID: 34559427]
[40]
Krasieva, T.B.; Ehren, J.; O’Sullivan, T.; Tromberg, B.J.; Maher, P. Cell and brain tissue imaging of the flavonoid fisetin using label-free two-photon microscopy. Neurochem. Int., 2015, 89, 243-248.
[http://dx.doi.org/10.1016/j.neuint.2015.08.003] [PMID: 26271433]
[41]
Youdim, K.A.; Qaiser, M.Z.; Begley, D.J.; Rice-Evans, C.A.; Abbott, N.J. Flavonoid permeability across an in situ model of the blood-brain barrier. Free Radic. Biol. Med., 2004, 36(5), 592-604.
[http://dx.doi.org/10.1016/j.freeradbiomed.2003.11.023] [PMID: 14980703]
[42]
Schaffer, S.; Halliwell, B. Do polyphenols enter the brain and does it matter? Some theoretical and practical considerations. Genes Nutr., 2012, 7(2), 99-109.
[http://dx.doi.org/10.1007/s12263-011-0255-5] [PMID: 22012276]
[43]
Vauzour, D. Dietary polyphenols as modulators of brain functions: Biological actions and molecular mechanisms underpinning their beneficial effects. Oxid. Med. Cell. Longev., 2012, 2012, 1-16.
[http://dx.doi.org/10.1155/2012/914273] [PMID: 22701758]
[44]
Fridén, M.; Ljungqvist, H.; Middleton, B.; Bredberg, U.; Hammarlund-Udenaes, M. Improved measurement of drug exposure in the brain using drug-specific correction for residual blood. J. Cereb. Blood Flow Metab., 2010, 30(1), 150-161.
[http://dx.doi.org/10.1038/jcbfm.2009.200] [PMID: 19756019]
[45]
Kalt, W.; Blumberg, J.B.; McDonald, J.E.; Vinqvist-Tymchuk, M.R.; Fillmore, S.A.E.; Graf, B.A.; O’Leary, J.M.; Milbury, P.E. Identification of anthocyanins in the liver, eye, and brain of blueberry-fed pigs. J. Agric. Food Chem., 2008, 56(3), 705-712.
[http://dx.doi.org/10.1021/jf071998l] [PMID: 18211026]
[46]
Milbury, P.E.; Kalt, W. Xenobiotic metabolism and berry flavonoid transport across the blood-brain barrier. J. Agric. Food Chem., 2010, 58(7), 3950-3956.
[http://dx.doi.org/10.1021/jf903529m] [PMID: 20128604]
[47]
Abd El Mohsen, M.M.; Kuhnle, G.; Rechner, A.R.; Schroeter, H.; Rose, S.; Jenner, P.; Rice-Evans, C.A. Uptake and metabolism of epicatechin and its access to the brain after oral ingestion. Free Radic. Biol. Med., 2002, 33(12), 1693-1702.
[http://dx.doi.org/10.1016/S0891-5849(02)01137-1] [PMID: 12488137]
[48]
El Mohsen, M.A.; Marks, J.; Kuhnle, G.; Moore, K.; Debnam, E.; Srai, S.K.; Rice-Evans, C.; Spencer, J.P.E. Absorption, tissue distribution and excretion of pelargonidin and its metabolites following oral administration to rats. Br. J. Nutr., 2006, 95(1), 51-58.
[http://dx.doi.org/10.1079/BJN20051596] [PMID: 16441916]
[49]
Passamonti, S.; Vrhovsek, U.; Vanzo, A.; Mattivi, F. Fast access of some grape pigments to the brain. J. Agric. Food Chem., 2005, 53(18), 7029-7034.
[http://dx.doi.org/10.1021/jf050565k] [PMID: 16131107]
[50]
Andres-Lacueva, C.; Shukitt-Hale, B.; Galli, R.L.; Jauregui, O.; Lamuela-Raventos, R.M.; Joseph, J.A. Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr. Neurosci., 2005, 8(2), 111-120.
[http://dx.doi.org/10.1080/10284150500078117] [PMID: 16053243]
[51]
Wang, J.; Ferruzzi, M.G.; Ho, L.; Blount, J.; Janle, E.M.; Gong, B.; Pan, Y.; Gowda, G.A.N.; Raftery, D.; Arrieta-Cruz, I.; Sharma, V.; Cooper, B.; Lobo, J.; Simon, J.E.; Zhang, C.; Cheng, A.; Qian, X.; Ono, K.; Teplow, D.B.; Pavlides, C.; Dixon, R.A.; Pasinetti, G.M. Brain-targeted proanthocyanidin metabolites for Alzheimer’s disease treatment. J. Neurosci., 2012, 32(15), 5144-5150.
[http://dx.doi.org/10.1523/JNEUROSCI.6437-11.2012] [PMID: 22496560]
[52]
Al Rahim, M.; Nakajima, A.; Saigusa, D.; Tetsu, N.; Maruyama, Y.; Shibuya, M.; Yamakoshi, H.; Tomioka, Y.; Iwabuchi, Y.; Ohizumi, Y.; Yamakuni, T. 4′-Demethylnobiletin, a bioactive metabolite of nobiletin enhancing PKA/ERK/CREB signaling, rescues learning impairment associated with NMDA receptor antagonism via stimulation of the ERK cascade. Biochemistry, 2009, 48(32), 7713-7721.
[http://dx.doi.org/10.1021/bi901088w] [PMID: 19601643]
[53]
Taubert, D.; Roesen, R.; Lehmann, C.; Jung, N.; Schömig, E. Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: A randomized controlled trial. JAMA, 2007, 298(1), 49-60.
[http://dx.doi.org/10.1001/jama.298.1.49] [PMID: 17609490]
[54]
Fraga, C.G.; Litterio, M.C.; Prince, P.D.; Calabró, V.; Piotrkowski, B.; Galleano, M. Cocoa flavanols: Effects on vascular nitric oxide and blood pressure. J. Clin. Biochem. Nutr., 2010, 48(1), 63-67.
[http://dx.doi.org/10.3164/jcbn.11-010FR] [PMID: 21297914]
[55]
Heiss, C.; Jahn, S.; Taylor, M.; Real, W.M.; Angeli, F.S.; Wong, M.L.; Amabile, N.; Prasad, M.; Rassaf, T.; Ottaviani, J.I.; Mihardja, S.; Keen, C.L.; Springer, M.L.; Boyle, A.; Grossman, W.; Glantz, S.A.; Schroeter, H.; Yeghiazarians, Y. Improvement of endothelial function with dietary flavanols is associated with mobilization of circulating angiogenic cells in patients with coronary artery disease. J. Am. Coll. Cardiol., 2010, 56(3), 218-224.
[http://dx.doi.org/10.1016/j.jacc.2010.03.039] [PMID: 20620742]
[56]
Murphy, K.J.; Chronopoulos, A.K.; Singh, I.; Francis, M.A.; Moriarty, H.; Pike, M.J.; Turner, A.H.; Mann, N.J.; Sinclair, A.J. Dietary flavanols and procyanidin oligomers from cocoa (Theobroma cacao) inhibit platelet function. Am. J. Clin. Nutr., 2003, 77(6), 1466-1473.
[http://dx.doi.org/10.1093/ajcn/77.6.1466] [PMID: 12791625]
[57]
Maleki, S.J.; Crespo, J.F.; Cabanillas, B. Anti-inflammatory effects of flavonoids. Food Chem., 2019, 299, 125124.
[http://dx.doi.org/10.1016/j.foodchem.2019.125124] [PMID: 31288163]
[58]
Lamport, D.J.; Pal, D.; Moutsiana, C.; Field, D.T.; Williams, C.M.; Spencer, J.P.E.; Butler, L.T. The effect of flavanol-rich cocoa on cerebral perfusion in healthy older adults during conscious resting state: A placebo controlled, crossover, acute trial. Psychopharmacology (Berl.), 2015, 232(17), 3227-3234.
[http://dx.doi.org/10.1007/s00213-015-3972-4] [PMID: 26047963]
[59]
Rendeiro, C.; Rhodes, J.S.; Spencer, J.P.E. The mechanisms of action of flavonoids in the brain: Direct versus indirect effects. Neurochem. Int., 2015, 89, 126-139.
[http://dx.doi.org/10.1016/j.neuint.2015.08.002] [PMID: 26260546]
[60]
Zhao, C.; Deng, W.; Gage, F.H. Mechanisms and functional implications of adult neurogenesis. Cell, 2008, 132(4), 645-660.
[http://dx.doi.org/10.1016/j.cell.2008.01.033] [PMID: 18295581]
[61]
Rees, A.; Dodd, G.; Spencer, J. The effects of flavonoids on cardiovascular health: A review of human intervention trials and implications for cerebrovascular function. Nutrients, 2018, 10(12), 1852.
[http://dx.doi.org/10.3390/nu10121852] [PMID: 30513729]
[62]
Cipriani, S.; Ferrer, I.; Aronica, E.; Kovacs, G.G.; Verney, C.; Nardelli, J.; Khung, S.; Delezoide, A.L.; Milenkovic, I.; Rasika, S.; Manivet, P.; Benifla, J.L.; Deriot, N.; Gressens, P.; Adle-Biassette, H. Hippocampal radial glial subtypes and their neurogenic potential in human fetuses and healthy and Alzheimer’s disease adults. Cereb. Cortex, 2018, 28(7), 2458-2478.
[http://dx.doi.org/10.1093/cercor/bhy096] [PMID: 29722804]
[63]
Flor-García, M.; Terreros-Roncal, J.; Moreno-Jiménez, E.P.; Ávila, J.; Rábano, A.; Llorens-Martín, M. Unraveling human adult hippocampal neurogenesis. Nat. Protoc., 2020, 15(2), 668-693.
[http://dx.doi.org/10.1038/s41596-019-0267-y]
[64]
Bergmann, O.; Liebl, J.; Bernard, S.; Alkass, K.; Yeung, M.S.Y.; Steier, P.; Kutschera, W.; Johnson, L.; Landén, M.; Druid, H.; Spalding, K.L.; Frisén, J. The age of olfactory bulb neurons in humans. Neuron, 2012, 74(4), 634-639.
[http://dx.doi.org/10.1016/j.neuron.2012.03.030] [PMID: 22632721]
[65]
Mich, J.K.; Signer, R.A.J.; Nakada, D.; Pineda, A.; Burgess, R.J.; Vue, T.Y.; Johnson, J.E.; Morrison, S.J. Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. eLife, 2014, 3, e02669.
[http://dx.doi.org/10.7554/eLife.02669] [PMID: 24843006]
[66]
Mizrak, D.; Levitin, H.M.; Delgado, A.C.; Crotet, V.; Yuan, J.; Chaker, Z.; Silva-Vargas, V.; Sims, P.A.; Doetsch, F. Single-cell analysis of regional differences in adult V-SVZ neural stem cell lineages. Cell Rep., 2019, 26(2), 394-406.e5.
[http://dx.doi.org/10.1016/j.celrep.2018.12.044] [PMID: 30625322]
[67]
Lazarini, F.; Gabellec, M.M.; Moigneu, C.; de Chaumont, F.; Olivo-Marin, J.C.; Lledo, P.M. Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J. Neurosci., 2014, 34(43), 14430-14442.
[http://dx.doi.org/10.1523/JNEUROSCI.5366-13.2014] [PMID: 25339754]
[68]
Lim, D.A.; Alvarez-Buylla, A. The adult ventricular-subventricular zone (V-SVZ) and olfactory bulb (OB) neurogenesis. Cold Spring Harb. Perspect. Biol., 2016, 8(5), a018820.
[http://dx.doi.org/10.1101/cshperspect.a018820] [PMID: 27048191]
[69]
Lau, B.W.M.; Yau, S.Y.; Lee, T.M.C.; Ching, Y.P.; Tang, S.W.; So, K.F. Effect of corticosterone and paroxetine on masculine mating behavior: Possible involvement of neurogenesis. J. Sex. Med., 2011, 8(5), 1390-1403.
[http://dx.doi.org/10.1111/j.1743-6109.2010.02081.x] [PMID: 20955318]
[70]
Bragado Alonso, S.; Reinert, J.K.; Marichal, N.; Massalini, S.; Berninger, B.; Kuner, T.; Calegari, F. An increase in neural stem cells and olfactory bulb adult neurogenesis improves discrimination of highly similar odorants. EMBO J., 2019, 38(6), e98791.
[http://dx.doi.org/10.15252/embj.201798791] [PMID: 30643018]
[71]
Gao, A.; Xia, F.; Guskjolen, A.J.; Ramsaran, A.I.; Santoro, A.; Josselyn, S.A.; Frankland, P.W. Elevation of hippocampal neurogenesis induces a temporally graded pattern of forgetting of contextual fear memories. J. Neurosci., 2018, 38(13), 3190-3198.
[http://dx.doi.org/10.1523/JNEUROSCI.3126-17.2018] [PMID: 29453206]
[72]
Bonaguidi, M.A.; Song, J.; Ming, G.; Song, H. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr. Opin. Neurobiol., 2012, 22(5), 754-761.
[http://dx.doi.org/10.1016/j.conb.2012.03.013] [PMID: 22503352]
[73]
Kozareva, D.A.; Cryan, J.F.; Nolan, Y.M. Born this way: Hippocampal neurogenesis across the lifespan. Aging Cell, 2019, 18(5), e13007.
[http://dx.doi.org/10.1111/acel.13007] [PMID: 31298475]
[74]
Steiner, B.; Klempin, F.; Wang, L.; Kott, M.; Kettenmann, H.; Kempermann, G. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia, 2006, 54(8), 805-814.
[http://dx.doi.org/10.1002/glia.20407] [PMID: 16958090]
[75]
Ortiz-López, L.; Vega-Rivera, N.M.; Babu, H.; Ramírez-Rodríguez, G.B. Brain-derived neurotrophic factor induces cell survival and the migration of murine adult hippocampal precursor cells during differentiation in vitro. Neurotox. Res., 2017, 31(1), 122-135.
[http://dx.doi.org/10.1007/s12640-016-9673-x] [PMID: 27663583]
[76]
Snyder, J.S.; Soumier, A.; Brewer, M.; Pickel, J.; Cameron, H.A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature, 2011, 476(7361), 458-461.
[http://dx.doi.org/10.1038/nature10287] [PMID: 21814201]
[77]
Seri, B.; García-Verdugo, J.M.; McEwen, B.S.; Alvarez-Buylla, A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci., 2001, 21(18), 7153-7160.
[http://dx.doi.org/10.1523/JNEUROSCI.21-18-07153.2001] [PMID: 11549726]
[78]
Filippov, V.; Kronenberg, G.; Pivneva, T.; Reuter, K.; Steiner, B.; Wang, L.P.; Yamaguchi, M.; Kettenmann, H.; Kempermann, G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci., 2003, 23(3), 373-382.
[http://dx.doi.org/10.1016/S1044-7431(03)00060-5] [PMID: 12837622]
[79]
Brown, J.P.; Couillard-Després, S.; Cooper-Kuhn, C.M.; Winkler, J.; Aigner, L.; Kuhn, H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol., 2003, 467(1), 1-10.
[http://dx.doi.org/10.1002/cne.10874] [PMID: 14574675]
[80]
Kronenberg, G.; Reuter, K.; Steiner, B.; Brandt, M.D.; Jessberger, S.; Yamaguchi, M.; Kempermann, G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol., 2003, 467(4), 455-463.
[http://dx.doi.org/10.1002/cne.10945] [PMID: 14624480]
[81]
Brandt, M.D.; Jessberger, S.; Steiner, B.; Kronenberg, G.; Reuter, K.; Bick-Sander, A.; Behrens, W.; Kempermann, G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol. Cell. Neurosci., 2003, 24(3), 603-613.
[http://dx.doi.org/10.1016/S1044-7431(03)00207-0] [PMID: 14664811]
[82]
Kempermann, G.; Gast, D.; Kronenberg, G.; Yamaguchi, M.; Gage, F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development, 2003, 130(2), 391-399.
[http://dx.doi.org/10.1242/dev.00203] [PMID: 12466205]
[83]
Biebl, M.; Cooper, C.M.; Winkler, J.; Kuhn, H.G. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett., 2000, 291(1), 17-20.
[http://dx.doi.org/10.1016/S0304-3940(00)01368-9] [PMID: 10962143]
[84]
Kuhn, H.G.; Biebl, M.; Wilhelm, D.; Li, M.; Friedlander, R.M.; Winkler, J. Increased generation of granule cells in adult Bcl-2-overexpressing mice: A role for cell death during continued hippocampal neurogenesis. Eur. J. Neurosci., 2005, 22(8), 1907-1915.
[http://dx.doi.org/10.1111/j.1460-9568.2005.04377.x] [PMID: 16262630]
[85]
Ge, S.; Goh, E.L.K.; Sailor, K.A.; Kitabatake, Y.; Ming, G.; Song, H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 2006, 439(7076), 589-593.
[http://dx.doi.org/10.1038/nature04404] [PMID: 16341203]
[86]
Tashiro, A.; Sandler, V.M.; Toni, N.; Zhao, C.; Gage, F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature, 2006, 442(7105), 929-933.
[http://dx.doi.org/10.1038/nature05028] [PMID: 16906136]
[87]
Imielski, Y.; Schwamborn, J.C.; Lüningschrör, P.; Heimann, P.; Holzberg, M.; Werner, H.; Leske, O.; Püschel, A.W.; Memet, S.; Heumann, R.; Israel, A.; Kaltschmidt, C.; Kaltschmidt, B. Regrowing the adult brain: NF-κB controls functional circuit formation and tissue homeostasis in the dentate gyrus. PLoS One, 2012, 7(2), e30838.
[http://dx.doi.org/10.1371/journal.pone.0030838] [PMID: 22312433]
[88]
Cancino, G.I.; Yiu, A.P.; Fatt, M.P.; Dugani, C.B.; Flores, E.R.; Frankland, P.W.; Josselyn, S.A.; Miller, F.D.; Kaplan, D.R. p63 Regulates adult neural precursor and newly born neuron survival to control hippocampal-dependent Behavior. J. Neurosci., 2013, 33(31), 12569-12585.
[http://dx.doi.org/10.1523/JNEUROSCI.1251-13.2013] [PMID: 23904595]
[89]
Ramírez-Rodríguez, G.; Babu, H.; Klempin, F.; Krylyshkina, O.; Baekelandt, V.; Gijsbers, R.; Debyser, Z.; Overall, R.W.; Nicola, Z.; Fabel, K.; Kempermann, G. The α crystallin domain of small heat shock protein b8 (Hspb8) acts as survival and differentiation factor in adult hippocampal neurogenesis. J. Neurosci., 2013, 33(13), 5785-5796.
[http://dx.doi.org/10.1523/JNEUROSCI.6452-11.2013] [PMID: 23536091]
[90]
Pellegrino, G.; Trubert, C.; Terrien, J.; Pifferi, F.; Leroy, D.; Loyens, A.; Migaud, M.; Baroncini, M.; Maurage, C.A.; Fontaine, C.; Prévot, V.; Sharif, A. A comparative study of the neural stem cell niche in the adult hypothalamus of human, mouse, rat and gray mouse lemur (Microcebus murinus). J. Comp. Neurol., 2018, 526(9), 1419-1443.
[http://dx.doi.org/10.1002/cne.24376] [PMID: 29230807]
[91]
Pierce, A.A.; Xu, A.W. De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J. Neurosci., 2010, 30(2), 723-730.
[http://dx.doi.org/10.1523/JNEUROSCI.2479-09.2010] [PMID: 20071537]
[92]
Kokoeva, M.V.; Yin, H.; Flier, J.S. Neurogenesis in the hypothalamus of adult mice: Potential role in energy balance. Science, 2005, 310(5748), 679-683.
[http://dx.doi.org/10.1126/science.1115360] [PMID: 16254185]
[93]
Bless, E.P.; Reddy, T.; Acharya, K.D.; Beltz, B.S.; Tetel, M.J. Oestradiol and diet modulate energy homeostasis and hypothalamic neurogenesis in the adult female mouse. J. Neuroendocrinol., 2014, 26(11), 805-816.
[http://dx.doi.org/10.1111/jne.12206] [PMID: 25182179]
[94]
Zhao, M.; Momma, S.; Delfani, K.; Carlén, M.; Cassidy, R.M.; Johansson, C.B.; Brismar, H.; Shupliakov, O.; Frisén, J.; Janson, A.M. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. USA, 2003, 100(13), 7925-7930.
[http://dx.doi.org/10.1073/pnas.1131955100] [PMID: 12792021]
[95]
Parent, A.; Cicchetti, F.; Beach, T.G. Calretinin-immunoreactive neurons in the human striatum. Brain Res., 1995, 674(2), 347-351.
[http://dx.doi.org/10.1016/0006-8993(95)00124-9] [PMID: 7796115]
[96]
Suzuki, S.O.; Goldman, J.E. Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: A dynamic study of glial and neuronal progenitor migration. J. Neurosci., 2003, 23(10), 4240-4250.
[http://dx.doi.org/10.1523/JNEUROSCI.23-10-04240.2003] [PMID: 12764112]
[97]
Shapiro, L.A.; Ng, K.; Zhou, Q.Y.; Ribak, C.E. Subventricular zone-derived, newly generated neurons populate several olfactory and limbic forebrain regions. Epilepsy Behav., 2009, 14(1), 74-80.
[http://dx.doi.org/10.1016/j.yebeh.2008.09.011] [PMID: 18849007]
[98]
Bernier, P.J.; Bédard, A.; Vinet, J.; Lévesque, M.; Parent, A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. USA, 2002, 99(17), 11464-11469.
[http://dx.doi.org/10.1073/pnas.172403999] [PMID: 12177450]
[99]
Magavi, S.S.; Leavitt, B.R.; Macklis, J.D. Induction of neurogenesis in the neocortex of adult mice. Nature, 2000, 405(6789), 951-955.
[http://dx.doi.org/10.1038/35016083] [PMID: 10879536]
[100]
Sachs, B.D.; Caron, M.G. Chronic fluoxetine increases extra-hippocampal neurogenesis in adult mice. Int. J. Neuropsychopharmacol., 2015, 18(4), pyu029.
[http://dx.doi.org/10.1093/ijnp/pyu029] [PMID: 25583694]
[101]
Andreotti, J.P.; Prazeres, P.H.D.M.; Magno, L.A.V.; Romano-Silva, M.A.; Mintz, A.; Birbrair, A. Neurogenesis in the postnatal cerebellum after injury. Int. J. Dev. Neurosci., 2018, 67(1), 33-36.
[http://dx.doi.org/10.1016/j.ijdevneu.2018.03.002] [PMID: 29555564]
[102]
Enwere, E.; Shingo, T.; Gregg, C.; Fujikawa, H.; Ohta, S.; Weiss, S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci., 2004, 24(38), 8354-8365.
[http://dx.doi.org/10.1523/JNEUROSCI.2751-04.2004] [PMID: 15385618]
[103]
Gage, F.H.; Temple, S. Neural stem cells: Generating and regenerating the brain. Neuron, 2013, 80(3), 588-601.
[http://dx.doi.org/10.1016/j.neuron.2013.10.037] [PMID: 24183012]
[104]
Tobin, M.K.; Musaraca, K.; Disouky, A.; Shetti, A.; Bheri, A.; Honer, W.G.; Kim, N.; Dawe, R.J.; Bennett, D.A.; Arfanakis, K.; Lazarov, O. Human hippocampal neurogenesis persists in aged adults and Alzheimer’s disease patients. Cell Stem Cell, 2019, 24(6), 974-982.e3.
[http://dx.doi.org/10.1016/j.stem.2019.05.003] [PMID: 31130513]
[105]
Hollands, C.; Tobin, M.K.; Hsu, M.; Musaraca, K.; Yu, T.S.; Mishra, R.; Kernie, S.G.; Lazarov, O. Depletion of adult neurogenesis exacerbates cognitive deficits in Alzheimer’s disease by compromising hippocampal inhibition. Mol. Neurodegener., 2017, 12(1), 64.
[http://dx.doi.org/10.1186/s13024-017-0207-7] [PMID: 28886753]
[106]
Moreno-Jiménez, E.P.; Flor-García, M.; Terreros-Roncal, J.; Rábano, A.; Cafini, F.; Pallas-Bazarra, N.; Ávila, J.; Llorens-Martín, M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med., 2019, 25(4), 554-560.
[http://dx.doi.org/10.1038/s41591-019-0375-9]
[107]
Terreros-Roncal, J.; Moreno-Jiménez, E.P.; Flor-García, M.; Rodríguez-Moreno, C.B.; Trinchero, M.F.; Cafini, F.; Rábano, A.; Llorens-Martín, M. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis. Science, 2021, 374(6571), 1106-1113.
[http://dx.doi.org/10.1126/science.abl5163] [PMID: 34672693]
[108]
Ben Abdallah, N.M.B.; Slomianka, L.; Vyssotski, A.L.; Lipp, H.P. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol. Aging, 2010, 31(1), 151-161.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.03.002] [PMID: 18455269]
[109]
Kempermann, G. Activity dependency and aging in the regulation of adult neurogenesis. Cold Spring Harb. Perspect. Biol., 2015, 7(11), a018929.
[http://dx.doi.org/10.1101/cshperspect.a018929] [PMID: 26525149]
[110]
Kase, Y.; Otsu, K.; Shimazaki, T.; Okano, H. Involvement of p38 in age-related decline in adult neurogenesis via modulation of Wnt signaling. Stem Cell Reports, 2019, 12(6), 1313-1328.
[http://dx.doi.org/10.1016/j.stemcr.2019.04.010] [PMID: 31080114]
[111]
Díaz-Moreno, M.; Armenteros, T.; Gradari, S.; Hortigüela, R.; García-Corzo, L.; Fontán-Lozano, Á.; Trejo, J.L.; Mira, H. Noggin rescues age-related stem cell loss in the brain of senescent mice with neurodegenerative pathology. Proc. Natl. Acad. Sci. USA, 2018, 115(45), 11625-11630.
[http://dx.doi.org/10.1073/pnas.1813205115] [PMID: 30352848]
[112]
Kalamakis, G.; Brüne, D.; Ravichandran, S.; Bolz, J.; Fan, W.; Ziebell, F.; Stiehl, T.; Catalá-Martinez, F.; Kupke, J.; Zhao, S.; Llorens-Bobadilla, E.; Bauer, K.; Limpert, S.; Berger, B.; Christen, U.; Schmezer, P.; Mallm, J.P.; Berninger, B.; Anders, S.; del Sol, A.; Marciniak-Czochra, A.; Martin-Villalba, A. Quiescence modulates stem cell maintenance and regenerative capacity in the aging brain. Cell, 2019, 176(6), 1407-1419.e14.
[http://dx.doi.org/10.1016/j.cell.2019.01.040] [PMID: 30827680]
[113]
Silva-Vargas, V.; Crouch, E.E.; Doetsch, F. Adult neural stem cells and their niche: A dynamic duo during homeostasis, regeneration, and aging. Curr. Opin. Neurobiol., 2013, 23(6), 935-942.
[http://dx.doi.org/10.1016/j.conb.2013.09.004] [PMID: 24090877]
[114]
Zhang, L.; Yang, X.; Yang, S.; Zhang, J. The Wnt/β-catenin signaling pathway in the adult neurogenesis. Eur. J. Neurosci., 2011, 33(1), 1-8.
[http://dx.doi.org/10.1111/j.1460-9568.2010.7483.x] [PMID: 21073552]
[115]
Austin, S.H.L.; Gabarró-Solanas, R.; Rigo, P.; Paun, O.; Harris, L.; Guillemot, F.; Urbán, N. Wnt/β-catenin signalling is dispensable for adult neural stem cell homeostasis and activation. Development, 2021, 148(20), 199629.
[http://dx.doi.org/10.1242/dev.199629] [PMID: 34557919]
[116]
Miranda, C.J.; Braun, L.; Jiang, Y.; Hester, M.E.; Zhang, L.; Riolo, M.; Wang, H.; Rao, M.; Altura, R.A.; Kaspar, B.K. Aging brain microenvironment decreases hippocampal neurogenesis through Wnt-mediated survivin signaling. Aging Cell, 2012, 11(3), 542-552.
[http://dx.doi.org/10.1111/j.1474-9726.2012.00816.x] [PMID: 22404871]
[117]
Arredondo, S.B.; Valenzuela-Bezanilla, D.; Santibanez, S.H.; Varela-Nallar, L. Wnt signaling in the adult hippocampal neurogenic niche. Stem Cells, 2022, 40(7), 630-640.
[http://dx.doi.org/10.1093/stmcls/sxac027] [PMID: 35446432]
[118]
Ortega-Martínez, S. A new perspective on the role of the CREB family of transcription factors in memory consolidation via adult hippocampal neurogenesis. Front. Mol. Neurosci., 2015, 8, 46.
[http://dx.doi.org/10.3389/fnmol.2015.00046] [PMID: 26379491]
[119]
Yu, X.W.; Oh, M.M.; Disterhoft, J.F. CREB, cellular excitability, and cognition: Implications for aging. Behav. Brain Res. 2017, 322(Pt B), 206-211.
[http://dx.doi.org/10.1016/j.bbr.2016.07.042] [PMID: 27478142]
[120]
Shetty, A.K.; Hattiangady, B.; Shetty, G.A. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: Role of astrocytes. Glia, 2005, 51(3), 173-186.
[http://dx.doi.org/10.1002/glia.20187] [PMID: 15800930]
[121]
Solano Fonseca, R.; Mahesula, S.; Apple, D.M.; Raghunathan, R.; Dugan, A.; Cardona, A.; O’Connor, J.; Kokovay, E. Neurogenic niche microglia undergo positional remodeling and progressive activation contributing to age-associated reductions in neurogenesis. Stem Cells Dev., 2016, 25(7), 542-555.
[http://dx.doi.org/10.1089/scd.2015.0319] [PMID: 26857912]
[122]
Weissmiller, A.M.; Wu, C. Current advances in using neurotrophic factors to treat neurodegenerative disorders. Transl. Neurodegener., 2012, 1(1), 14.
[http://dx.doi.org/10.1186/2047-9158-1-14] [PMID: 23210531]
[123]
Conover, J.C.; Todd, K.L. Development and aging of a brain neural stem cell niche. Exp. Gerontol., 2017, 94, 9-13.
[http://dx.doi.org/10.1016/j.exger.2016.11.007] [PMID: 27867091]
[124]
Buckwalter, M.S.; Yamane, M.; Coleman, B.S.; Ormerod, B.K.; Chin, J.T.; Palmer, T.; Wyss-Coray, T. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am. J. Pathol., 2006, 169(1), 154-164.
[http://dx.doi.org/10.2353/ajpath.2006.051272] [PMID: 16816369]
[125]
DeCarolis, N.A.; Kirby, E.D.; Wyss-Coray, T.; Palmer, T.D. The role of the microenvironmental niche in declining stem-cell functions associated with biological aging. Cold Spring Harb. Perspect. Med., 2015, 5(12), a025874.
[http://dx.doi.org/10.1101/cshperspect.a025874] [PMID: 26627453]
[126]
Conboy, I.M.; Rando, T.A. Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell Cycle, 2012, 11(12), 2260-2267.
[http://dx.doi.org/10.4161/cc.20437] [PMID: 22617385]
[127]
Kase, Y.; Shimazaki, T.; Okano, H.; Okano, H. Current understanding of adult neurogenesis in the mammalian brain: How does adult neurogenesis decrease with age? Inflamm. Regen., 2020, 40(1), 10.
[http://dx.doi.org/10.1186/s41232-020-00122-x] [PMID: 32566044]
[128]
Chantranupong, L.; Wolfson, R.L.; Sabatini, D.M. Nutrient-sensing mechanisms across evolution. Cell, 2015, 161(1), 67-83.
[http://dx.doi.org/10.1016/j.cell.2015.02.041] [PMID: 25815986]
[129]
Renault, V.M.; Rafalski, V.A.; Morgan, A.A.; Salih, D.A.M.; Brett, J.O.; Webb, A.E.; Villeda, S.A.; Thekkat, P.U.; Guillerey, C.; Denko, N.C.; Palmer, T.D.; Butte, A.J.; Brunet, A. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell, 2009, 5(5), 527-539.
[http://dx.doi.org/10.1016/j.stem.2009.09.014] [PMID: 19896443]
[130]
Paik, J.; Ding, Z.; Narurkar, R.; Ramkissoon, S.; Muller, F.; Kamoun, W.S.; Chae, S.S.; Zheng, H.; Ying, H.; Mahoney, J.; Hiller, D.; Jiang, S.; Protopopov, A.; Wong, W.H.; Chin, L.; Ligon, K.L.; DePinho, R.A. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell, 2009, 5(5), 540-553.
[http://dx.doi.org/10.1016/j.stem.2009.09.013] [PMID: 19896444]
[131]
Navarro Negredo, P.; Yeo, R.W.; Brunet, A. Aging and rejuvenation of neural stem cells and their niches. Cell Stem Cell, 2020, 27(2), 202-223.
[http://dx.doi.org/10.1016/j.stem.2020.07.002] [PMID: 32726579]
[132]
Beckervordersandforth, R.; Ebert, B.; Schäffner, I.; Moss, J.; Fiebig, C.; Shin, J.; Moore, D.L.; Ghosh, L.; Trinchero, M.F.; Stockburger, C.; Friedland, K.; Steib, K.; von Wittgenstein, J.; Keiner, S.; Redecker, C.; Hölter, S.M.; Xiang, W.; Wurst, W.; Jagasia, R.; Schinder, A.F.; Ming, G.; Toni, N.; Jessberger, S.; Song, H.; Lie, D.C. Role of mitochondrial metabolism in the control of early lineage progression and aging phenotypes in adult hippocampal neurogenesis. Neuron, 2017, 93(3), 560-573.e6.
[http://dx.doi.org/10.1016/j.neuron.2016.12.017] [PMID: 28111078]
[133]
Stoll, E.A.; Cheung, W.; Mikheev, A.M.; Sweet, I.R.; Bielas, J.H.; Zhang, J.; Rostomily, R.C.; Horner, P.J. Aging neural progenitor cells have decreased mitochondrial content and lower oxidative metabolism. J. Biol. Chem., 2011, 286(44), 38592-38601.
[http://dx.doi.org/10.1074/jbc.M111.252171] [PMID: 21900249]
[134]
Stoll, E.A.; Makin, R.; Sweet, I.R.; Trevelyan, A.J.; Miwa, S.; Horner, P.J.; Turnbull, D.M. Neural stem cells in the adult subventricular zone oxidize fatty acids to produce energy and support neurogenic activity. Stem Cells, 2015, 33(7), 2306-2319.
[http://dx.doi.org/10.1002/stem.2042] [PMID: 25919237]
[135]
Whitney, N.P.; Eidem, T.M.; Peng, H.; Huang, Y.; Zheng, J.C. Inflammation mediates varying effects in neurogenesis: Relevance to the pathogenesis of brain injury and neurodegenerative disorders. J. Neurochem., 2009, 108(6), 1343-1359.
[http://dx.doi.org/10.1111/j.1471-4159.2009.05886.x] [PMID: 19154336]
[136]
Fuster-Matanzo, A.; Llorens-Martín, M.; Hernández, F.; Avila, J. Role of neuroinflammation in adult neurogenesis and Alzheimer disease: Therapeutic approaches. Mediators Inflamm., 2013, 2013, 1-9.
[http://dx.doi.org/10.1155/2013/260925] [PMID: 23690659]
[137]
Kohman, R.A.; Rhodes, J.S. Neurogenesis, inflammation and behavior. Brain Behav. Immun., 2013, 27(1), 22-32.
[http://dx.doi.org/10.1016/j.bbi.2012.09.003] [PMID: 22985767]
[138]
Weiss, N.; Miller, F.; Cazaubon, S.; Couraud, P.O. The blood-brain barrier in brain homeostasis and neurological diseases. Biochim. Biophys. Acta Biomembr., 2009, 1788(4), 842-857.
[http://dx.doi.org/10.1016/j.bbamem.2008.10.022] [PMID: 19061857]
[139]
Yousef, H.; Czupalla, C.J.; Lee, D.; Chen, M.B.; Burke, A.N.; Zera, K.A.; Zandstra, J.; Berber, E.; Lehallier, B.; Mathur, V.; Nair, R.V.; Bonanno, L.N.; Yang, A.C.; Peterson, T.; Hadeiba, H.; Merkel, T.; Körbelin, J.; Schwaninger, M.; Buckwalter, M.S.; Quake, S.R.; Butcher, E.C.; Wyss-Coray, T. Aged blood impairs hippocampal neural precursor activity and activates microglia via brain endothelial cell VCAM1. Nat. Med., 2019, 25(6), 988-1000.
[http://dx.doi.org/10.1038/s41591-019-0440-4] [PMID: 31086348]
[140]
Yuan, T.F.; Gu, S.; Shan, C.; Marchado, S.; Arias-Carrión, O. Oxidative stress and adult neurogenesis. Stem Cell Rev. Rep., 2015, 11(5), 706-709.
[http://dx.doi.org/10.1007/s12015-015-9603-y]
[141]
Walton, N.M.; Shin, R.; Tajinda, K.; Heusner, C.L.; Kogan, J.H.; Miyake, S.; Chen, Q.; Tamura, K.; Matsumoto, M. Adult neurogenesis transiently generates oxidative stress. PLoS One, 2012, 7(4), e35264.
[http://dx.doi.org/10.1371/journal.pone.0035264] [PMID: 22558133]
[142]
Simon, M.; Czéh, B.; Fuchs, E. Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res., 2005, 1049(2), 244-248.
[http://dx.doi.org/10.1016/j.brainres.2005.05.006] [PMID: 15950198]
[143]
Singh, S.; Mishra, A.; Tiwari, V.; Shukla, S. Enhanced neuroinflammation and oxidative stress are associated with altered hippocampal neurogenesis in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treated mice. Behav. Pharmacol., 2019, 30(8), 688-698.
[http://dx.doi.org/10.1097/FBP.0000000000000516] [PMID: 31703031]
[144]
Mahmoud, R.; Wainwright, S.R.; Galea, L.A.M. Sex hormones and adult hippocampal neurogenesis: Regulation, implications, and potential mechanisms. Front. Neuroendocrinol., 2016, 41, 129-152.
[http://dx.doi.org/10.1016/j.yfrne.2016.03.002] [PMID: 26988999]
[145]
Delgado-Morales, R.; Agís-Balboa, R.C.; Esteller, M.; Berdasco, M. Epigenetic mechanisms during ageing and neurogenesis as novel therapeutic avenues in human brain disorders. Clin. Epigenetics, 2017, 9(1), 67.
[http://dx.doi.org/10.1186/s13148-017-0365-z] [PMID: 28670349]
[146]
Kahroba, H.; Ramezani, B.; Maadi, H.; Sadeghi, M.R.; Jaberie, H.; Ramezani, F. The role of Nrf2 in neural stem/progenitors cells: From maintaining stemness and self-renewal to promoting differentiation capability and facilitating therapeutic application in neurodegenerative disease. Ageing Res. Rev., 2021, 65, 101211.
[http://dx.doi.org/10.1016/j.arr.2020.101211] [PMID: 33186670]
[147]
Cichon, N.; Saluk-Bijak, J.; Gorniak, L.; Przyslo, L.; Bijak, M. Flavonoids as a natural enhancer of neuroplasticity-an overview of the mechanism of neurorestorative action. Antioxidants, (Basel, Switzerland), 2020, 9, 1-19.
[http://dx.doi.org/10.3390/antiox9111035]
[148]
Almulla, A.Y.H.; Mogulkoc, R.; Baltaci, A.K.; Dasdelen, D. Learning, neurogenesis and effects of flavonoids on learning. Mini Rev. Med. Chem., 2022, 22(2), 355-364.
[http://dx.doi.org/10.2174/1389557521666210707120719] [PMID: 34238155]
[149]
Dias, G.P.; Cavegn, N.; Nix, A.; do Nascimento Bevilaqua, M.C.; Stangl, D.; Zainuddin, M.S.A.; Nardi, A.E.; Gardino, P.F.; Thuret, S. The role of dietary polyphenols on adult hippocampal neurogenesis: Molecular mechanisms and behavioural effects on depression and anxiety. Oxid. Med. Cell. Longev., 2012, 2012, 1-18.
[http://dx.doi.org/10.1155/2012/541971] [PMID: 22829957]
[150]
Spencer, J.P.E. Flavonoids: Modulators of brain function? Br. J. Nutr. 2008, 99(Suppl 1)
[http://dx.doi.org/10.1017/S0007114508965776]
[151]
Oh, S.B.; Park, H.R.; Jang, Y.J.; Choi, S.Y.; Son, T.G.; Lee, J. Baicalein attenuates impaired hippocampal neurogenesis and the neurocognitive deficits induced by γ-ray radiation. Br. J. Pharmacol., 2013, 168(2), 421-431.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02142.x] [PMID: 22891631]
[152]
Liaquat, L.; Batool, Z.; Sadir, S.; Rafiq, S.; Shahzad, S.; Perveen, T.; Haider, S. Naringenin-induced enhanced antioxidant defence system meliorates cholinergic neurotransmission and consolidates memory in male rats. Life Sci., 2018, 194, 213-223.
[http://dx.doi.org/10.1016/j.lfs.2017.12.034] [PMID: 29287782]
[153]
Prasanna, P.; Upadhyay, A. Flavonoid-based nanomedicines in Alzheimer’s disease therapeutics: Promises made, a long way to go. ACS Pharmacol. Transl. Sci., 2021, 4(1), 74-95.
[http://dx.doi.org/10.1021/acsptsci.0c00224] [PMID: 33615162]
[154]
Wang, X.; Li, Y.; Han, L.; Li, J.; Liu, C.; Sun, C. Role of flavonoids in the treatment of iron overload. Front. Cell Dev. Biol., 2021, 9, 685364.
[http://dx.doi.org/10.3389/fcell.2021.685364] [PMID: 34291050]
[155]
Bernatoniene, J.; Kopustinskiene, D. The role of catechins in cellular responses to oxidative stress. Molecules, 2018, 23(4), 965.
[http://dx.doi.org/10.3390/molecules23040965] [PMID: 29677167]
[156]
Xu, D.; Hu, M.J.; Wang, Y.Q.; Cui, Y.L. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules, 2019, 24(6), 1123.
[http://dx.doi.org/10.3390/molecules24061123] [PMID: 30901869]
[157]
Parhiz, H.; Roohbakhsh, A.; Soltani, F.; Rezaee, R.; Iranshahi, M. Antioxidant and anti-inflammatory properties of the citrus flavonoids hesperidin and hesperetin: An updated review of their molecular mechanisms and experimental models. Phytother. Res., 2015, 29(3), 323-331.
[http://dx.doi.org/10.1002/ptr.5256] [PMID: 25394264]
[158]
Davinelli, S.; Corbi, G.; Zarrelli, A.; Arisi, M.; Calzavara-Pinton, P.; Grassi, D.; De Vivo, I.; Scapagnini, G. Short-term supplementation with flavanol-rich cocoa improves lipid profile, antioxidant status and positively influences the AA/EPA ratio in healthy subjects. J. Nutr. Biochem., 2018, 61, 33-39.
[http://dx.doi.org/10.1016/j.jnutbio.2018.07.011] [PMID: 30179727]
[159]
Cuadrado, A. Brain-protective mechanisms of transcription factor NRF2: Toward a common strategy for neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol., 2022, 62(1), 255-277.
[http://dx.doi.org/10.1146/annurev-pharmtox-052220-103416] [PMID: 34637322]
[160]
Robledinos-Antón, N.; Rojo, A.I.; Ferreiro, E.; Núñez, Á.; Krause, K.H.; Jaquet, V.; Cuadrado, A. Transcription factor NRF2 controls the fate of neural stem cells in the subgranular zone of the hippocampus. Redox Biol., 2017, 13, 393-401.
[http://dx.doi.org/10.1016/j.redox.2017.06.010] [PMID: 28667908]
[161]
Corenblum, M.J.; Ray, S.; Remley, Q.W.; Long, M.; Harder, B.; Zhang, D.D.; Barnes, C.A.; Madhavan, L. Reduced Nrf2 expression mediates the decline in neural stem cell function during a critical middle‐age period. Aging Cell, 2016, 15(4), 725-736.
[http://dx.doi.org/10.1111/acel.12482] [PMID: 27095375]
[162]
Naewla, S.; Sirichoat, A.; Pannangrong, W.; Chaisawang, P.; Wigmore, P.; Welbat, J.U. Hesperidin alleviates methotrexate-induced memory deficits via hippocampal neurogenesis in adult rats. Nutrients, 2019, 11(4), 936.
[http://dx.doi.org/10.3390/nu11040936] [PMID: 31027240]
[163]
Welbat, J.U.; Naewla, S.; Pannangrong, W.; Sirichoat, A.; Aranarochana, A.; Wigmore, P. Neuroprotective effects of hesperidin against methotrexate-induced changes in neurogenesis and oxidative stress in the adult rat. Biochem. Pharmacol., 2020, 178, 114083.
[http://dx.doi.org/10.1016/j.bcp.2020.114083] [PMID: 32522593]
[164]
Velagapudi, R.; El-Bakoush, A.; Olajide, O.A. Activation of Nrf2 pathway contributes to neuroprotection by the dietary flavonoid tiliroside. Mol. Neurobiol., 2018, 55(10), 8103-8123.
[http://dx.doi.org/10.1007/s12035-018-0975-2] [PMID: 29508282]
[165]
Crampton, S.J.; O’Keeffe, G.W. NF-κB: Emerging roles in hippocampal development and function. Int. J. Biochem. Cell Biol., 2013, 45(8), 1821-1824.
[http://dx.doi.org/10.1016/j.biocel.2013.05.037] [PMID: 23764620]
[166]
Shih, R.H.; Wang, C.Y.; Yang, C.M. NF-kappaB signaling pathways in neurological inflammation: A mini review. Front. Mol. Neurosci., 2015, 8, 77.
[http://dx.doi.org/10.3389/fnmol.2015.00077] [PMID: 26733801]
[167]
Thawkar, B.S.; Kaur, G. Inhibitors of NF-κB and P2X7/NLRP3/Caspase 1 pathway in microglia: Novel therapeutic opportunities in neuroinflammation induced early-stage Alzheimer’s disease. J. Neuroimmunol., 2019, 326, 62-74.
[http://dx.doi.org/10.1016/j.jneuroim.2018.11.010] [PMID: 30502599]
[168]
Acosta, S.; Jernberg, J.; Sanberg, C.D.; Sanberg, P.R.; Small, B.J.; Gemma, C.; Bickford, P.C. NT-020, a natural therapeutic approach to optimize spatial memory performance and increase neural progenitor cell proliferation and decrease inflammation in the aged rat. Rejuvenation Res., 2010, 13(5), 581-588.
[http://dx.doi.org/10.1089/rej.2009.1011] [PMID: 20586644]
[169]
Flowers, A.; Lee, J.Y.; Acosta, S.; Hudson, C.; Small, B.; Sanberg, C.D.; Bickford, P.C.; Grimmig, B. NT-020 treatment reduces inflammation and augments Nrf-2 and Wnt signaling in aged rats. J. Neuroinflammation, 2015, 12(1), 174.
[http://dx.doi.org/10.1186/s12974-015-0395-4] [PMID: 26376629]
[170]
Sarubbo, F.; Moranta, D.; Pani, G. Dietary polyphenols and neurogenesis: Molecular interactions and implication for brain ageing and cognition. Neurosci. Biobehav. Rev., 2018, 90, 456-470.
[http://dx.doi.org/10.1016/j.neubiorev.2018.05.011] [PMID: 29753753]
[171]
Casadesus, G.; Shukitt-Hale, B.; Stellwagen, H.M.; Zhu, X.; Lee, H.G.; Smith, M.A.; Joseph, J.A. Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutr. Neurosci., 2004, 7(5-6), 309-316.
[http://dx.doi.org/10.1080/10284150400020482] [PMID: 15682927]
[172]
Farina, F.; Lambert, E.; Commeau, L.; Lejeune, F.X.; Roudier, N.; Fonte, C.; Parker, J.A.; Boddaert, J.; Verny, M.; Baulieu, E.E.; Neri, C. The stress response factor daf-16/FOXO is required for multiple compound families to prolong the function of neurons with Huntington’s disease. Sci. Rep., 2017, 7(1), 4014.
[http://dx.doi.org/10.1038/s41598-017-04256-w] [PMID: 28638078]
[173]
Davinelli, S.; De Stefani, D.; De Vivo, I.; Scapagnini, G. Polyphenols as caloric restriction mimetics regulating mitochondrial biogenesis and mitophagy. Trends Endocrinol. Metab., 2020, 31(7), 536-550.
[http://dx.doi.org/10.1016/j.tem.2020.02.011] [PMID: 32521237]
[174]
Iwata, R.; Vanderhaeghen, P. Regulatory roles of mitochondria and metabolism in neurogenesis. Curr. Opin. Neurobiol., 2021, 69, 231-240.
[http://dx.doi.org/10.1016/j.conb.2021.05.003] [PMID: 34171617]
[175]
Prakash, A.; Shur, B.; Kumar, A. Naringin protects memory impairment and mitochondrial oxidative damage against aluminum-induced neurotoxicity in rats. Int. J. Neurosci., 2013, 123(9), 636-645.
[http://dx.doi.org/10.3109/00207454.2013.785542] [PMID: 23510099]
[176]
Schroeter, H.; Bahia, P.; Spencer, J.P.E.; Sheppard, O.; Rattray, M.; Cadenas, E.; Rice-Evans, C.; Williams, R.J. (-)Epicatechin stimulates ERK-dependent cyclic AMP response element activity and up-regulates GluR2 in cortical neurons. J. Neurochem., 2007, 101(6), 1596-1606.
[http://dx.doi.org/10.1111/j.1471-4159.2006.04434.x] [PMID: 17298385]
[177]
Lee, Y.; Jeon, S.J.; Lee, H.E.; Jung, I.H.; Jo, Y.W.; Lee, S.; Cheong, J.H.; Jang, D.S.; Ryu, J.H. Spinosin, a C-glycoside flavonoid, enhances cognitive performance and adult hippocampal neurogenesis in mice. Pharmacol. Biochem. Behav., 2016, 145, 9-16.
[http://dx.doi.org/10.1016/j.pbb.2016.03.007] [PMID: 26997033]
[178]
Lee, S.; Kim, D.H.; Lee, D.H.; Jeon, S.J.; Lee, C.H.; Son, K.H.; Jung, J.W.; Shin, C.Y.; Ryu, J.H. Oroxylin A, a flavonoid, stimulates adult neurogenesis in the hippocampal dentate gyrus region of mice. Neurochem. Res., 2010, 35(11), 1725-1732.
[http://dx.doi.org/10.1007/s11064-010-0235-y] [PMID: 20680459]
[179]
Yu, B.; Zhou, W-B.; Miao, Z-N.; Zhang, B.; Long, W.; Zheng, F-X.; Kong, J. Luteolin induces hippocampal neurogenesis in the Ts65Dn mouse model of Down syndrome. Neural Regen. Res., 2019, 14(4), 613-620.
[http://dx.doi.org/10.4103/1673-5374.248519] [PMID: 30632501]
[180]
Lin, C.W.; Wu, M.J.; Liu, I.Y.C.; Su, J.D.; Yen, J.H. Neurotrophic and cytoprotective action of luteolin in PC12 cells through ERK-dependent induction of Nrf2-driven HO-1 expression. J. Agric. Food Chem., 2010, 58(7), 4477-4486.
[http://dx.doi.org/10.1021/jf904061x] [PMID: 20302373]
[181]
Contestabile, A.; Greco, B.; Ghezzi, D.; Tucci, V.; Benfenati, F.; Gasparini, L. Lithium rescues synaptic plasticity and memory in Down syndrome mice. J. Clin. Invest., 2013, 123(1), 348-361.
[http://dx.doi.org/10.1172/JCI64650] [PMID: 23202733]
[182]
Lin, L.F.; Chiu, S.P.; Wu, M.J.; Chen, P.Y.; Yen, J.H. Luteolin induces microRNA-132 expression and modulates neurite outgrowth in PC12 cells. PLoS One, 2012, 7(8), e43304.
[http://dx.doi.org/10.1371/journal.pone.0043304] [PMID: 22916239]
[183]
Okuyama, S.; Shimada, N.; Kaji, M.; Morita, M.; Miyoshi, K.; Minami, S.; Amakura, Y.; Yoshimura, M.; Yoshida, T.; Watanabe, S.; Nakajima, M.; Furukawa, Y. Heptamethoxyflavone, a citrus flavonoid, enhances brain-derived neurotrophic factor production and neurogenesis in the hippocampus following cerebral global ischemia in mice. Neurosci. Lett., 2012, 528(2), 190-195.
[http://dx.doi.org/10.1016/j.neulet.2012.08.079] [PMID: 22985518]
[184]
Zhang, K.; Pan, X.; Wang, F.; Ma, J.; Su, G.; Dong, Y.; Yang, J.; Wu, C. Baicalin promotes hippocampal neurogenesis via SGK1- and FKBP5-mediated glucocorticoid receptor phosphorylation in a neuroendocrine mouse model of anxiety/depression. Sci. Rep., 2016, 6(1), 30951.
[http://dx.doi.org/10.1038/srep30951] [PMID: 27502757]
[185]
Xiao, Z.; Cao, Z.; Yang, J.; Jia, Z.; Du, Y.; Sun, G.; Lu, Y.; Pei, L. Baicalin promotes hippocampal neurogenesis via the Wnt/β-catenin pathway in a chronic unpredictable mild stress-induced mouse model of depression. Biochem. Pharmacol., 2021, 190, 114594.
[http://dx.doi.org/10.1016/j.bcp.2021.114594] [PMID: 33964281]
[186]
Baral, S.; Pariyar, R.; Kim, J.; Lee, H.S.; Seo, J. Quercetin-3-O-glucuronide promotes the proliferation and migration of neural stem cells. Neurobiol. Aging, 2017, 52, 39-52.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.12.024] [PMID: 28110104]
[187]
Tchantchou, F.; Lacor, P.N.; Cao, Z.; Lao, L.; Hou, Y.; Cui, C.; Klein, W.L.; Luo, Y. Stimulation of neurogenesis and synaptogenesis by bilobalide and quercetin via common final pathway in hippocampal neurons. J. Alzheimers Dis., 2009, 18(4), 787-798.
[http://dx.doi.org/10.3233/JAD-2009-1189] [PMID: 19661619]
[188]
Ma, Z.X.; Zhang, R.Y.; Rui, W.J.; Wang, Z.Q.; Feng, X. Quercetin alleviates chronic unpredictable mild stress-induced depressive-like behaviors by promoting adult hippocampal neurogenesis via FoxG1/CREB/BDNF signaling pathway. Behav. Brain Res., 2021, 406, 113245.
[http://dx.doi.org/10.1016/j.bbr.2021.113245] [PMID: 33745981]
[189]
Fang, J.L.; Luo, Y.; Jin, S.H.; Yuan, K.; Guo, Y. Ameliorative effect of anthocyanin on depression mice by increasing monoamine neurotransmitter and up-regulating BDNF expression. J. Funct. Foods, 2020, 66, 103757.
[http://dx.doi.org/10.1016/j.jff.2019.103757]
[190]
Gao, J.; Wu, Y.; He, D.; Zhu, X.; Li, H.; Liu, H.; Liu, H. Anti-aging effects of Ribes meyeri anthocyanins on neural stem cells and aging mice. Aging (Albany NY), 2020, 12(17), 17738-17753.
[http://dx.doi.org/10.18632/aging.103955] [PMID: 32920547]
[191]
Shan, X.; Chen, J.; Dai, S.; Wang, J.; Huang, Z.; Lv, Z.; Wang, Q.; Wu, Q. Cyanidin-related antidepressant-like efficacy requires PI3K/AKT/FoxG1/FGF-2 pathway modulated enhancement of neuronal differentiation and dendritic maturation. Phytomedicine, 2020, 76, 153269.
[http://dx.doi.org/10.1016/j.phymed.2020.153269] [PMID: 32593103]
[192]
Davinelli, S.; Scapagnini, G. Polyphenols: A promising nutritional approach to prevent or reduce the progression of prehypertension. High Blood Press. Cardiovasc. Prev., 2016, 23(3), 197-202.
[http://dx.doi.org/10.1007/s40292-016-0149-0] [PMID: 27115149]
[193]
Davinelli, S.; Corbi, G.; Righetti, S.; Sears, B.; Olarte, H.H.; Grassi, D.; Scapagnini, G. Cardioprotection by cocoa polyphenols and ω -3 Fatty Acids: A disease-prevention perspective on aging-associated cardiovascular risk. J. Med. Food, 2018, 21(10), 1060-1069.
[http://dx.doi.org/10.1089/jmf.2018.0002] [PMID: 29723102]
[194]
Navarrete-Yañez, V.; Garate-Carrillo, A.; Ayala, M.; Rodriguez-Castañeda, A.; Mendoza-Lorenzo, P.; Ceballos, G.; Ordoñez-Razo, R.; Dugar, S.; Schreiner, G.; Villarreal, F.; Ramirez-Sanchez, I. Stimulatory effects of (−)-epicatechin and its enantiomer (+)-epicatechin on mouse frontal cortex neurogenesis markers and short-term memory: Proof of concept. Food Funct., 2021, 12(8), 3504-3515.
[http://dx.doi.org/10.1039/D0FO03084H] [PMID: 33900336]
[195]
Brickman, A.M.; Khan, U.A.; Provenzano, F.A.; Yeung, L.K.; Suzuki, W.; Schroeter, H.; Wall, M.; Sloan, R.P.; Small, S.A. Enhancing dentate gyrus function with dietary flavanols improves cognition in older adults. Nat. Neurosci., 2014, 17(12), 1798-1803.
[http://dx.doi.org/10.1038/nn.3850] [PMID: 25344629]
[196]
Fujii, Y.; Sakata, J.; Sato, F.; Onishi, K.; Yamato, Y.; Sakata, K.; Taira, S.; Sato, H.; Osakabe, N. Impact of short-term oral dose of cinnamtannin A2, an (−)-epicatechin tetramer, on spatial memory and adult hippocampal neurogenesis in mouse. Biochem. Biophys. Res. Commun., 2021, 585, 1-7.
[http://dx.doi.org/10.1016/j.bbrc.2021.11.021] [PMID: 34781055]
[197]
Li, X.; Ma, J.; Xu, J.; Zhu, D.; Li, A.; Che, Y.; Chen, D.; Feng, X. Puerarin and amlodipine improvement of d-galactose-induced impairments of behaviour and neurogenesis in mouse dentate gyrus: Correlation with glucocorticoid receptor expression. Neurochem. Res., 2017, 42(11), 3268-3278.
[http://dx.doi.org/10.1007/s11064-017-2366-x] [PMID: 28831640]
[198]
Yamada, J.; Hatabe, J.; Tankyo, K.; Jinno, S. Cell type- and region-specific enhancement of adult hippocampal neurogenesis by daidzein in middle-aged female mice. Neuropharmacology, 2016, 111, 92-106.
[http://dx.doi.org/10.1016/j.neuropharm.2016.08.036] [PMID: 27580847]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy