Functions of flavonoids in the central nervous system: Astrocytes as targets for natural compounds

Neurochemistry International

Volumn 95, Issue , 2016, Pages 85-91

  Matias, Isadora ^a   Buosi, Andrea Schmidt ^a   Gomes, Flávia Carvalho Alcantara ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Astrocyte; Cognition; Flavonoids; Synapse

Indexed keywords

FLAVONOID; NATURAL PRODUCT; THROMBOSPONDIN 1; BIOLOGICAL PRODUCT;

ASTROCYTE; CELL FUNCTION; CELL SURVIVAL; CELLS BY BODY ANATOMY; CENTRAL NERVOUS SYSTEM; COGNITION; DRUG MECHANISM; DRUG TARGETING; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; METABOLISM; PROCEDURES;

ANIMALS; ASTROCYTES; BIOLOGICAL PRODUCTS; CENTRAL NERVOUS SYSTEM; DRUG DELIVERY SYSTEMS; FLAVONOIDS; HUMANS;

EID: 84957927257     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2016.01.009     Document Type: Review

References (83)

1. M.M. Abd El Mohsen, G. Kuhnle, A.R. Rechner, H. Schroeter, S. Rose, P. Jenner, and C.A. Rice-Evans Uptake and metabolism of epicatechin and its access to the brain after oral ingestion Free Radic. Biol. Med. 33 2002 1693 1702
2. D. Albrecht, F.J. Lopez-Murcia, A.P. Perez-Gonzalez, G. Lichtner, C. Solsona, and A. Llobet SPARC prevents maturation of cholinergic presynaptic terminals Mol. Cell Neurosci. 49 2012 364 374
3. N.J. Allen, M.L. Bennett, L.C. Foo, G.X. Wang, C. Chakraborty, S.J. Smith, and B.A. Barres Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors Nature 486 2012 410 414
4. P.K. Bahia, M. Rattray, and R.J. Williams Dietary flavonoid (-)epicatechin stimulates phosphatidylinositol 3-kinase-dependent anti-oxidant response element activity and up-regulates glutathione in cortical astrocytes J. Neurochem. 106 2008 2194 2204
5. G.R. Beecher Overview of dietary flavonoids: nomenclature, occurrence and intake J. Nutr. 133 2003 3248S 3254S
6. D. Blackburn, S. Sargsyan, P.N. Monk, and P.J. Shaw Astrocyte function and role in motor neuron disease: a future therapeutic target? Glia 57 2009 1251 1264
7. A.M. Brickman, U.A. Khan, F.A. Provenzano, L.K. Yeung, W. Suzuki, H. Schroeter, M. Wall, R.P. Sloan, and S.A. Small Enhancing dentate gyrus function with dietary flavanols improves cognition in older adults Nat. Neurosci. 17 2014 1798 1803
8. L. Buee, P.R. Hof, D.D. Roberts, A. Delacourte, J.H. Morrison, and H.M. Fillit Immunohistochemical identification of thrombospondin in normal human brain and in Alzheimer's disease Am. J. Pathol. 141 1992 783 788
9. J. Chakraborty, R. Singh, D. Dutta, A. Naskar, U. Rajamma, and K.P. Mohanakumar Quercetin improves behavioral deficiencies, restores astrocytes and microglia, and reduces serotonin metabolism in 3-nitropropionic acid-induced rat model of Huntington's Disease CNS Neurosci. Ther. 20 2014 10 19
10. C. Chen, P. Jiang, H. Xue, S.E. Peterson, H.T. Tran, A.E. McCann, M.M. Parast, S. Li, D.E. Pleasure, L.C. Laurent, J.F. Loring, Y. Liu, and W. Deng Role of astroglia in Down's syndrome revealed by patient-derived human-induced pluripotent stem cells Nat. Commun. 5 2014 4430
11. K.S. Christopherson, E.M. Ullian, C.C. Stokes, C.E. Mullowney, J.W. Hell, A. Agah, J. Lawler, D.F. Mosher, P. Bornstein, and B.A. Barres Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis Cell 120 2005 421 433
12. G.T. Corbett, A. Roy, and K. Pahan Sodium phenylbutyrate enhances astrocytic neurotrophin synthesis via protein kinase C (PKC)-mediated activation of cAMP-response element-binding protein (CREB): implications for Alzheimer disease therapy J. Biol. Chem. 288 2013 8299 8312
13. D.C. Crawford, X. Jiang, A. Taylor, and S. Mennerick Astrocyte-derived thrombospondins mediate the development of hippocampal presynaptic plasticity in vitro J. Neurosci. 32 2012 13100 13110
14. K.D. Croft The chemistry and biological effects of flavonoids and phenolic acids Ann. N. Y. Acad. Sci. 854 1998 435 442
15. A. Currais, M. Prior, R. Dargusch, A. Armando, J. Ehren, D. Schubert, O. Quehenberger, and P. Maher Modulation of p25 and inflammatory pathways by fisetin maintains cognitive function in Alzheimer's disease transgenic mice Aging Cell 13 2014 379 390
16. T.C. de Sampaio e Spohr, J. Stipursky, A.C. Sasaki, P.R. Barbosa, V. Martins, C.F. Benjamim, N.F. Roque, S.L. Costa, and F.C. Gomes Effects of the flavonoid casticin from Brazilian Croton betulaster in cerebral cortical progenitors in vitro: direct and indirect action through astrocytes J. Neurosci. Res. 88 2010 530 541
17. S.T. DeKosky, S.W. Scheff, and S.D. Styren Structural correlates of cognition in dementia: quantification and assessment of synapse change Neurodegeneration 5 1996 417 421
18. L. Devi, and M. Ohno 7,8-dihydroxyflavone, a small-molecule TrkB agonist, reverses memory deficits and BACE1 elevation in a mouse model of Alzheimer's disease Neuropsychopharmacology 37 2012 434 444
19. E.E. Devore, J.H. Kang, M.M. Breteler, and F. Grodstein Dietary intakes of berries and flavonoids in relation to cognitive decline Ann. Neurol. 72 2012 135 143
20. L.P. Diniz, J.C. Almeida, V. Tortelli, C. Vargas Lopes, P. Setti-Perdigao, J. Stipursky, S.A. Kahn, L.F. Romao, J. de Miranda, S.V. Alves-Leon, J.M. de Souza, N.G. Castro, R. Panizzutti, and F.C. Gomes Astrocyte-induced synaptogenesis is mediated by transforming growth factor beta signaling through modulation of D-serine levels in cerebral cortex neurons J. Biol. Chem. 287 2012 41432 41445
21. L.P. Diniz, I.C. Pereira Matias, M. Garcia, and F.C. Alcantara Gomes Astrocytic control of neural circuit formation: highlights on TGF-beta signaling Neurochem. Int. 78 2014 Dec 18 27 10.1016/j.neuint.2014.07.008 Epub 2014 Aug 11. Review. Erratum in: Neurochem Int. 2015 Apr-May; 83-84():48
22. L.P. Diniz, V. Tortelli, M.N. Garcia, A.P. Araujo, H.M. Melo, G.S. Seixas da Silva, F.G. De Felice, S.V. Alves-Leon, J.M. de Souza, L.F. Romao, N.G. Castro, and F.C. Gomes Astrocyte transforming growth factor beta 1 promotes inhibitory synapse formation via CaM kinase II signaling Glia 62 12 2014 Dec 1917 1931 10.1002/glia.22713 Epub 2014 Jul 10
23. M.C. Dodla, J. Mumaw, and S.L. Stice Role of astrocytes, soluble factors, cells adhesion molecules and neurotrophins in functional synapse formation: implications for human embryonic stem cell derived neurons Curr. Stem Cell Res. Ther. 5 2010 251 260
24. F. Donato, M.G. de Gomes, A.T. Goes, C.B. Filho, L. Del Fabbro, M.S. Antunes, L.C. Souza, S.P. Boeira, and C.R. Jesse Hesperidin exerts antidepressant-like effects in acute and chronic treatments in mice: possible role of l-arginine-NO-cGMP pathway and BDNF levels Brain Res. Bull. 104 2014 19 26
25. Y. Dong, and E.N. Benveniste Immune function of astrocytes Glia 36 2001 180 190
26. M.G. Ferruzzi, J.K. Lobo, E.M. Janle, B. Cooper, J.E. Simon, Q.L. Wu, C. Welch, L. Ho, C. Weaver, and G.M. Pasinetti Bioavailability of gallic acid and catechins from grape seed polyphenol extract is improved by repeated dosing in rats: implications for treatment in Alzheimer's disease J. Alzheimers Dis. 18 2009 113 124
27. Y. Fuentes-Medel, J. Ashley, R. Barria, R. Maloney, M. Freeman, and V. Budnik Integration of a retrograde signal during synapse formation by glia-secreted TGF-beta ligand Curr. Biol. 22 2012 1831 1838
28. O. Garcia, M. Torres, P. Helguera, P. Coskun, and J. Busciglio A role for thrombospondin-1 deficits in astrocyte-mediated spine and synaptic pathology in Down's syndrome PLoS One 5 2010 e14200
29. C.K. Glass, K. Saijo, B. Winner, M.C. Marchetto, and F.H. Gage Mechanisms underlying inflammation in neurodegeneration Cell 140 2010 918 934
30. M.E. Gomez-Casati, J.C. Murtie, C. Rio, K. Stankovic, M.C. Liberman, and G. Corfas Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression Proc. Natl. Acad. Sci. U. S. A. 107 2010 17005 17010
31. C. Henneberger, T. Papouin, S.H. Oliet, and D.A. Rusakov Long-term potentiation depends on release of D-serine from astrocytes Nature 463 2010 232 236
32. L. Hennekinne, S. Colasse, A. Triller, and M. Renner Differential control of thrombospondin over synaptic glycine and AMPA receptors in spinal cord neurons J. Neurosci. 33 2013 11432 11439
33. R. Hu, W.Q. Cai, X.G. Wu, and Z. Yang Astrocyte-derived estrogen enhances synapse formation and synaptic transmission between cultured neonatal rat cortical neurons Neuroscience 144 2007 1229 1240
34. S.W. Jang, X. Liu, M. Yepes, K.R. Shepherd, G.W. Miller, Y. Liu, W.D. Wilson, G. Xiao, B. Blanchi, Y.E. Sun, and K. Ye A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone Proc. Natl. Acad. Sci. U. S. A. 107 2010 2687 2692
35. E.V. Jones, Y. Bernardinelli, Y.C. Tse, S. Chierzi, T.P. Wong, and K.K. Murai Astrocytes control glutamate receptor levels at developing synapses through SPARC-beta-integrin interactions J. Neurosci. 31 2011 4154 4165
36. P. Knekt, R. Jarvinen, A. Reunanen, and J. Maatela Flavonoid intake and coronary mortality in Finland: a cohort study BMJ 312 1996 478 481
37. M. Kodali, V.K. Parihar, B. Hattiangady, V. Mishra, B. Shuai, and A.K. Shetty Resveratrol prevents age-related memory and mood dysfunction with increased hippocampal neurogenesis and microvasculature, and reduced glial activation Sci. Rep. 5 2015 8075
38. H. Kucukdereli, N.J. Allen, A.T. Lee, A. Feng, M.I. Ozlu, L.M. Conatser, C. Chakraborty, G. Workman, M. Weaver, E.H. Sage, B.A. Barres, and C. Eroglu Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC Proc. Natl. Acad. Sci. U. S. A. 108 2011 E440 E449
39. E. Lee, H.R. Park, S.T. Ji, Y. Lee, and J. Lee Baicalein attenuates astroglial activation in the 1-methyl-4-phenyl-1,2,3,4-tetrahydropyridine-induced Parkinson's disease model by downregulating the activations of nuclear factor-kappaB, ERK, and JNK J. Neurosci. Res. 92 2014 130 139
40. Y.J. Lee, D.Y. Choi, Y.P. Yun, S.B. Han, K.W. Oh, and J.T. Hong Epigallocatechin-3-gallate prevents systemic inflammation-induced memory deficiency and amyloidogenesis via its anti-neuroinflammatory properties J. Nutr. Biochem. 24 2013 298 310
41. R.T. Liu, J.T. Tang, L.B. Zou, J.Y. Fu, and Q.J. Lu Liquiritigenin attenuates the learning and memory deficits in an amyloid protein precursor transgenic mouse model and the underlying mechanisms Eur. J. Pharmacol. 669 2011 76 83
42. X. Liu, C.B. Chan, S.W. Jang, S. Pradoldej, J. Huang, K. He, L.H. Phun, S. France, G. Xiao, Y. Jia, H.R. Luo, and K. Ye A synthetic 7,8-dihydroxyflavone derivative promotes neurogenesis and exhibits potent antidepressant effect J. Med. Chem. 53 2010 8274 8286
43. P. Maher, T. Akaishi, and K. Abe Flavonoid fisetin promotes ERK-dependent long-term potentiation and enhances memory Proc. Natl. Acad. Sci. U. S. A. 103 2006 16568 16573
44. C. Manach, A. Scalbert, C. Morand, C. Remesy, and L. Jimenez Polyphenols: food sources and bioavailability Am. J. Clin. Nutr. 79 2004 727 747
45. D.H. Mauch, K. Nagler, S. Schumacher, C. Goritz, E.C. Muller, A. Otto, and F.W. Pfrieger CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357
46. K.K. Modi, M. Sendtner, and K. Pahan Up-regulation of ciliary neurotrophic factor in astrocytes by aspirin: implications for remyelination in multiple sclerosis J. Biol. Chem. 288 2013 18533 18545
47. J.H. Morrison, and M.G. Baxter The ageing cortical synapse: hallmarks and implications for cognitive decline Nat. Rev. Neurosci. 13 2012 240 250
48. M. Nedergaard, B. Ransom, and S.A. Goldman New roles for astrocytes: redefining the functional architecture of the brain Trends Neurosci. 26 2003 523 530
49. R.J. Nijveldt, E. van Nood, D.E. van Hoorn, P.G. Boelens, K. van Norren, and P.A. van Leeuwen Flavonoids: a review of probable mechanisms of action and potential applications Am. J. Clin. Nutr. 74 2001 418 425
50. J. Nones, A.P. Costa, R.B. Leal, F.C. Gomes, and A.G. Trentin The flavonoids hesperidin and rutin promote neural crest cell survival Cell Tissue Res. 350 2012 305 315
51. J. Nones, T.C. Spohr, and F.C. Gomes Effects of the flavonoid hesperidin in cerebral cortical progenitors in vitro: indirect action through astrocytes Int. J. Dev. Neurosci. 30 2012 303 313
52. J. Nones, J. Stipursky, S.L. Costa, and F.C. Gomes Flavonoids and astrocytes crosstalking: implications for brain development and pathology Neurochem. Res. 35 2010 955 966
53. J. Nones, E.S. TC, and F.C. Gomes Hesperidin, a flavone glycoside, as mediator of neuronal survival Neurochem. Res. 36 2011 1776 1784
54. M. Pekny, and M. Nilsson Astrocyte activation and reactive gliosis Glia 50 2005 427 434
55. K.V. Rama Rao, K.M. Curtis, J.T. Johnstone, and M.D. Norenberg Amyloid-beta inhibits thrombospondin 1 release from cultured astrocytes: effects on synaptic protein expression J. Neuropathol. Exp. Neurol. 72 2013 735 744
56. C. Rendeiro, D. Vauzour, R.J. Kean, L.T. Butler, M. Rattray, J.P. Spencer, and C.M. Williams Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats Psychopharmacol. Berl. 223 2012 319 330
57. C. Rendeiro, J.S. Rhodes, and J.P. Spencer The mechanisms of action of flavonoids in the brain: direct versus indirect effects Neurochem. Int. 89 2015 126 139
58. C.A. Rice-Evans, N.J. Miller, and G. Paganga Structure-antioxidant activity relationships of flavonoids and phenolic acids Free Radic. Biol. Med. 20 1996 933 956
59. W.C. Risher, S. Patel, I.H. Kim, A. Uezu, S. Bhagat, D.K. Wilton, L.J. Pilaz, J. Singh Alvarado, O.Y. Calhan, D.L. Silver, B. Stevens, N. Calakos, S.H. Soderling, and C. Eroglu Astrocytes refine cortical connectivity at dendritic spines Elife 3 2014
60. R.M. Ritzel, A.R. Patel, S. Pan, J. Crapser, M. Hammond, E. Jellison, and L.D. McCullough Age- and location-related changes in microglial function Neurobiol. Aging 36 2015 2153 2163
61. A. Rodriguez-Mateos, D. Vauzour, C.G. Krueger, D. Shanmuganayagam, J. Reed, L. Calani, P. Mena, D. Del Rio, and A. Crozier Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update Arch. Toxicol. 88 2014 1803 1853
62. J.J. Rodriguez, C.Y. Yeh, S. Terzieva, M. Olabarria, M. Kulijewicz-Nawrot, and A. Verkhratsky Complex and region-specific changes in astroglial markers in the aging brain Neurobiol. Aging 35 2014 15 23
63. B.P. Rutten, N.M. Van der Kolk, S. Schafer, M.A. van Zandvoort, T.A. Bayer, H.W. Steinbusch, and C. Schmitz Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice Am. J. Pathol. 167 2005 161 173
64. P. Saiko, A. Szakmary, W. Jaeger, and T. Szekeres Resveratrol and its analogs: defense against cancer, coronary disease and neurodegenerative maladies or just a fad? Mutat. Res. 658 2008 68 94
65. H. Schroeter, P. Bahia, J.P. Spencer, O. Sheppard, M. Rattray, E. Cadenas, C. Rice-Evans, and R.J. Williams (-)Epicatechin stimulates ERK-dependent cyclic AMP response element activity and up-regulates GluR2 in cortical neurons J. Neurochem. 101 2007 1596 1606
66. V. Sharma, M. Mishra, S. Ghosh, R. Tewari, A. Basu, P. Seth, and E. Sen Modulation of interleukin-1beta mediated inflammatory response in human astrocytes by flavonoids: implications in neuroprotection Brain Res. Bull. 73 2007 55 63
67. Q. Shi, K.J. Colodner, S.B. Matousek, K. Merry, S. Hong, J.E. Kenison, J.L. Frost, K.X. Le, S. Li, J.C. Dodart, B.J. Caldarone, B. Stevens, and C.A. Lemere Complement C3-deficient mice fail to display age-related hippocampal decline J. Neurosci. 35 2015 13029 13042
68. S.A. Sloan, and B.A. Barres Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders Curr. Opin. Neurobiol. 27 2014 75 81
69. S.M. Son, D.W. Nam, M.Y. Cha, K.H. Kim, J. Byun, H. Ryu, and I. Mook-Jung Thrombospondin-1 prevents amyloid beta-mediated synaptic pathology in Alzheimer's disease Neurobiol. Aging 36 2015 3214 3227
70. T.C. Spohr, J.W. Choi, S.E. Gardell, D.R. Herr, S.K. Rehen, F.C. Gomes, and J. Chun Lysophosphatidic acid receptor-dependent secondary effects via astrocytes promote neuronal differentiation J. Biol. Chem. 283 2008 7470 7479
71. D. Stellwagen, and R.C. Malenka Synaptic scaling mediated by glial TNF-alpha Nature 440 2006 1054 1059
72. J. Stipursky, and F.C. Gomes TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development Glia 55 2007 1023 1033
73. F. Tchantchou, P.N. Lacor, Z. Cao, L. Lao, Y. Hou, C. Cui, W.L. Klein, and Y. Luo Stimulation of neurogenesis and synaptogenesis by bilobalide and quercetin via common final pathway in hippocampal neurons J. Alzheimers Dis. 18 2009 787 798
74. M. Tian, Y. Zeng, Y. Hu, X. Yuan, S. Liu, J. Li, P. Lu, Y. Sun, L. Gao, D. Fu, Y. Li, S. Wang, and S.M. McClintock 7, 8-Dihydroxyflavone induces synapse expression of AMPA GluA1 and ameliorates cognitive and spine abnormalities in a mouse model of fragile X syndrome Neuropharmacology 89 2015 43 53
75. K. Vafeiadou, D. Vauzour, H.Y. Lee, A. Rodriguez-Mateos, R.J. Williams, and J.P. Spencer The citrus flavanone naringenin inhibits inflammatory signalling in glial cells and protects against neuroinflammatory injury Arch. Biochem. Biophys. 484 2009 100 109
76. C.M. Williams, M.A. El Mohsen, D. Vauzour, C. Rendeiro, L.T. Butler, J.A. Ellis, M. Whiteman, and J.P. Spencer Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels Free Radic. Biol. Med. 45 2008 295 305
77. R.J. Williams, and J.P. Spencer Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease Free Radic. Biol. Med. 52 2012 35 45
78. S.L. Xu, C.W. Bi, R.C. Choi, K.Y. Zhu, A. Miernisha, T.T. Dong, and K.W. Tsim Flavonoids induce the synthesis and secretion of neurotrophic factors in cultured rat astrocytes: a signaling response mediated by estrogen receptor Evid. Based Complement. Altern. Med. 2013 2013 127075
79. S.L. Xu, K.Y. Zhu, C.W. Bi, R.C. Choi, A. Miernisha, A.L. Yan, M. Maiwulanjiang, S.W. Men, T.T. Dong, and K.W. Tsim Flavonoids induce the expression of synaptic proteins, synaptotagmin, and postsynaptic density protein-95 in cultured rat cortical neuron Planta Med. 79 2013 1710 1714
80. Y. Zeng, F. Lv, L. Li, H. Yu, M. Dong, and Q. Fu 7,8-dihydroxyflavone rescues spatial memory and synaptic plasticity in cognitively impaired aged rats J. Neurochem. 122 2012 800 811
81. F. Zhang, Y.F. Lu, Q. Wu, J. Liu, and J.S. Shi Resveratrol promotes neurotrophic factor release from astroglia Exp. Biol. Med. Maywood 237 2012 943 948
82. Z. Zhang, X. Liu, J.P. Schroeder, C.B. Chan, M. Song, S.P. Yu, D. Weinshenker, and K. Ye 7,8-dihydroxyflavone prevents synaptic loss and memory deficits in a mouse model of Alzheimer's disease Neuropsychopharmacology 39 2014 638 650
83. S. Zhao, X. Gao, W. Dong, and J. Chen The role of 7,8-dihydroxyflavone in preventing dendrite degeneration in cortex after moderate traumatic brain injury Mol. Neurobiol. 2015