Green tea compound epigallo-catechin-3-gallate (EGCG) increases neuronal survival in adult hippocampal neurogenesis in vivo and in vitro

Neuroscience

Volumn 322, Issue , 2016, Pages 208-220

  Ortiz Lopez L ^a   Marquez Valadez B ^a,b,c   Gomez Sanchez A ^a   Silva Lucero, M D C ^a,c   Torres Perez M ^a   Tellez Ballesteros R I ^a   Ichwan, M ^d,e   Meraz Rios M A ^c   Kempermann, G ^d,f   Ramirez Rodriguez G B ^a  

^a INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

^b Biological Sciences of UNAM   (Mexico)

^c DEPARTAMENTO DE FÍSICA   (Mexico)

^d CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^e UNIVERSITY OF SUMATERA UTARA   (Indonesia)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Adult neurogenesis; EGCG; Hippocampus; Nutrition; PI3K Akt; Survival

Indexed keywords

DOUBLECORTIN; EPIGALLOCATECHIN GALLATE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 42; MITOGEN ACTIVATED PROTEIN KINASE 44; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; CATECHIN; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; NEUROPROTECTIVE AGENT; TEA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; BRAIN NERVE CELL; CAMELLIA SINENSIS; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DENDRITE; DOSE RESPONSE; DRUG MEGADOSE; ENZYME PHOSPHORYLATION; EX VIVO STUDY; HIPPOCAMPUS; IN VIVO STUDY; LOW DRUG DOSE; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY; TEA;

ANIMALS; CATECHIN; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; MALE; MICE, INBRED BALB C; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; NEUROPROTECTIVE AGENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; TEA;

EID: 84959449929     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.02.040     Document Type: Article

References (52)

1. An L., Zhang Y.Z., Yu N.J., Liu X.M., Zhao N., Yuan L., Chen H.X., Li Y.F. The total flavonoids extracted from Xiaobuxin-Tang up-regulate the decreased hippocampal neurogenesis and neurotrophic molecules expression in chronically stressed rats. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:1484-1490.
2. Babu H., Cheung G., Kettenmann H., Palmer T.D., Kempermann G. Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS One 2007, 2:e388.
3. Babu H., Claasen J.H., Kannan S., Runker A.E., Palmer T., Kempermann G. A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front Neurosci 2011, 5:89.
4. Bhattacharya T.K., Pence B.D., Ossyra J.M., Gibbons T.E., Perez S., McCusker R.H., Kelley K.W., Johnson R.W., Woods J.A., Rhodes J.S. Exercise but not (-)-epigallocatechin-3-gallate or beta-alanine enhances physical fitness, brain plasticity, and behavioral performance in mice. Physiol Behav 2015, 145:29-37.
5. Biasibetti R., Tramontina A.C., Costa A.P., Dutra M.F., Quincozes-Santos A., Nardin P., Bernardi C.L., Wartchow K.M., Lunardi P.S., Goncalves C.A. Green tea (-)epigallocatechin-3-gallate reverses oxidative stress and reduces acetylcholinesterase activity in a streptozotocin-induced model of dementia. Behav Brain Res 2013, 236:186-193.
6. Brazil D.P., Park J., Hemmings B.A. PKB binding proteins. Getting in on the Akt. Cell 2002, 111:293-303.
7. Brazil D.P., Yang Z.Z., Hemmings B.A. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 2004, 29:233-242.
8. Chung J.H., Han J.H., Hwang E.J., Seo J.Y., Cho K.H., Kim K.H., Youn J.I., Eun H.C. Dual mechanisms of green tea extract (EGCG)-induced cell survival in human epidermal keratinocytes. FASEB J 2003, 17:1913-1915.
9. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Boghdahn U., Winkler J., Kuhn H.G., Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 2005, 21:1-14.
10. De la Torre R., De Sola S., Pons M., Duchon A., de Lagran M.M., Farre M., Fito M., Benejam B., Langohr K., Rodriguez J., Pujadas M., Bizot J.C., Cuenca A., Janel N., Catuara S., Covas M.I., Blehaut H., Herault Y., Delabar J.M., Dierssen M. Epigallocatechin-3-gallate, a DYRK1A inhibitor, rescues cognitive deficits in Down syndrome mouse models and in humans. Mol Nutr Food Res 2014, 58:278-288.
11. Dias G.P., Cavegn N., Nix A., do Nascimento Bevilaqua M.C., Stangl D., Zainuddin M.S., 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, 2012:541971.
12. Gibbons T.E., Pence B.D., Petr G., Ossyra J.M., Mach H.C., Bhattacharya T.K., Perez S., Martin S.A., McCusker R.H., Kelley K.W., Rhodes J.S., Johnson R.W., Woods J.A. Voluntary wheel running, but not a diet containing (-)-epigallocatechin-3-gallate and beta-alanine, improves learning, memory and hippocampal neurogenesis in aged mice. Behav Brain Res 2014, 272:131-140.
13. Govoni S., Amadio M., Battaini F., Pascale A. Senescence of the brain: focus on cognitive kinases. Curr Pharm Des 2010, 16:660-671.
14. Guedj F., Sebrie C., Rivals I., Ledru A., Paly E., Bizot J.C., Smith D., Rubin E., Gillet B., Arbones M., Delabar J.M. Green tea polyphenols rescue of brain defects induced by overexpression of DYRK1A. PLoS One 2009, 4:e4606.
15. Haque A.M., Hashimoto M., Katakura M., Tanabe Y., Hara Y., Shido O. Long-term administration of green tea catechins improves spatial cognition learning ability in rats. J Nutr 2006, 136:1043-1047.
16. Harada N., Zhao J., Kurihara H., Nakagata N., Okajima K. Resveratrol improves cognitive function in mice by increasing production of insulin-like growth factor-I in the hippocampus. J Nutr Biochem 2011, 22:1150-1159.
17. Ishii T., Ichikawa T., Minoda K., Kusaka K., Ito S., Suzuki Y., Akagawa M., Mochizuki K., Goda T., Nakayama T. Human serum albumin as an antioxidant in the oxidation of (-)-epigallocatechin gallate: participation of reversible covalent binding for interaction and stabilization. Biosci Biotechnol Biochem 2011, 75:100-106.
18. Jang S., Jeong H.S., Park J.S., Kim Y.S., Jin C.Y., Seol M.B., Kim B.C., Lee M.C. Neuroprotective effects of (-)-epigallocatechin-3-gallate against quinolinic acid-induced excitotoxicity via PI3K pathway and NO inhibition. Brain Res 2010, 1313:25-33.
19. Jia N., Han K., Kong J.J., Zhang X.M., Sha S., Ren G.R., Cao Y.P. (-)-Epigallocatechin-3-gallate alleviates spatial memory impairment in APP/PS1 mice by restoring IRS-1 signaling defects in the hippocampus. Mol Cell Biochem 2013, 380:211-218.
20. Joo S.Y., Song Y.A., Park Y.L., Myung E., Chung C.Y., Park K.J., Cho S.B., Lee W.S., Kim H.S., Rew J.S., Kim N.S., Joo Y.E. Epigallocatechin-3-gallate inhibits LPS-induced NF-kappaB and MAPK signaling pathways in Bone Marrow-derived macrophages. Gut Liver 2012, 6:188-196.
21. Kalfon L., Youdim M.B., Mandel S.A. Green tea polyphenol (-)-epigallocatechin-3-gallate promotes the rapid protein kinase C- and proteasome-mediated degradation of Bad: implications for neuroprotection. J Neurochem 2007, 100:992-1002.
22. 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, 130:391-399.
23. Kempermann G., Kuhn H.G., Gage F.H. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A 1997, 94:10409-10414.
24. Kim H., Sakamoto K. (-)-Epigallocatechin gallate suppresses adipocyte differentiation through the MEK/ERK and PI3K/Akt pathways. Cell Biol Int 2012, 36:147-153.
25. Kim J.Y., Duan X., Liu C.Y., Jang M.H., Guo J.U., Pow-anpongkul N., Kang E., Song H., Ming G.L. DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 2009, 63:761-773.
26. Kim J.Y., Liu C.Y., Zhang F., Duan X., Wen Z., Song J., Feighery E., Lu B., Rujescu D., St Clair D., Christian K., Callicott J.H., Weinberger D.R., Song H., Ming G.L. Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 2012, 148:1051-1064.
27. Lee M.J., Maliakal P., Chen L., Meng X., Bondoc F.Y., Prabhu S., Lambert G., Mohr S., Yang C.S. Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability. Cancer Epidemiol Biomarkers Prev 2002, 11:1025-1032.
28. Lee S.J., Jia Y. The effect of bioactive compounds in tea on lipid metabolism and obesity through regulation of peroxisome proliferator-activated receptors. Curr Opin Lipidol 2015, 26:3-9.
29. Lin L.C., Wang M.N., Tseng T.Y., Sung J.S., Tsai T.H. Pharmacokinetics of (-)-epigallocatechin-3-gallate in conscious and freely moving rats and its brain regional distribution. J Agric Food Chem 2007, 55:1517-1524.
30. Liu M., Chen F., Sha L., Wang S., Tao L., Yao L., He M., Yao Z., Liu H., Zhu Z., Zhang Z., Zheng Z., Sha X., Wei M. (-)-Epigallocatechin-3-gallate ameliorates learning and memory deficits by adjusting the balance of TrkA/p75NTR signaling in APP/PS1 transgenic mice. Mol Neurobiol 2014, 49:1350-1363.
31. Loftis J.M., Wilhelm C.J., Huckans M. Effect of epigallocatechin gallate supplementation in schizophrenia and bipolar disorder: an 8-week, randomized, double-blind, placebo-controlled study. Ther Adv Psychopharmacol 2013, 3:21-27.
32. Madhyastha S., Sekhar S., Rao G. Resveratrol improves postnatal hippocampal neurogenesis and brain derived neurotrophic factor in prenatally stressed rats. Int J Dev Neurosci 2013, 31:580-585.
33. Mandel S., Weinreb O., Amit T., Youdim M.B. Cell signaling pathways in the neuroprotective actions of the green tea polyphenol (-)-epigallocatechin-3-gallate: implications for neurodegenerative diseases. J Neurochem 2004, 88:1555-1569.
34. Mandel S.A., Avramovich-Tirosh Y., Reznichenko L., Zheng H., Weinreb O., Amit T., Youdim M.B. Multifunctional activities of green tea catechins in neuroprotection. Modulation of cell survival genes, iron-dependent oxidative stress and PKC signaling pathway. Neurosignals 2005, 14:46-60.
35. Menard C., Bastianetto S., Quirion R. Neuroprotective effects of resveratrol and epigallocatechin gallate polyphenols are mediated by the activation of protein kinase C gamma. Front Cell Neurosci 2013, 7:281.
36. Mereles D., Hunstein W. Epigallocatechin-3-gallate (EGCG) for clinical trials: more pitfalls than promises?. Int J Mol Sci 2011, 12:5592-5603.
37. Moriya J., Chen R., Yamakawa J., Sasaki K., Ishigaki Y., Takahashi T. Resveratrol improves hippocampal atrophy in chronic fatigue mice by enhancing neurogenesis and inhibiting apoptosis of granular cells. Biol Pharm Bull 2011, 34:354-359.
38. Plumpe T., Ehninger D., Steiner B., Klempin F., Jessberger S., Brandt M., Romer B., Rodriguez G.R., Kronenberg G., Kempermann G. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006, 7:77.
39. Pocernich C.B., Lange M.L., Sultana R., Butterfield D.A. Nutritional approaches to modulate oxidative stress in Alzheimer's disease. Curr Alzheimer Res 2011, 8:452-469.
40. Pu F., Mishima K., Irie K., Motohashi K., Tanaka Y., Orito K., Egawa T., Kitamura Y., Egashira N., Iwasaki K., Fujiwara M. Neuroprotective effects of quercetin and rutin on spatial memory impairment in an 8-arm radial maze task and neuronal death induced by repeated cerebral ischemia in rats. J Pharmacol Sci 2007, 104:329-334.
41. Ramirez-Rodriguez G., Klempin F., Babu H., Benitez-King G., Kempermann G. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 2009, 34:2180-2191.
42. Ramirez-Rodriguez G., Ocana-Fernandez M.A., Vega-Rivera N.M., Torres-Perez O.M., Gomez-Sanchez A., Estrada-Camarena E., Ortiz-Lopez L. Environmental enrichment induces neuroplastic changes in middle age female BalbC mice and increases the hippocampal levels of BDNF, p-Akt and p-MAPK1/2. Neuroscience 2014, 260:158-170.
43. Rasoolijazi H., Joghataie M.T., Roghani M., Nobakht M. The beneficial effect of (-)-epigallocatechin-3-gallate in an experimental model of Alzheimer's disease in rat: a behavioral analysis. Iran Biomed J 2007, 11:237-243.
44. Rezai-Zadeh K., Arendash G.W., Hou H., Fernandez F., Jensen M., Runfeldt M., Shytle R.D., Tan J. Green tea epigallocatechin-3-gallate (EGCG) reduces beta-amyloid mediated cognitive impairment and modulates tau pathology in Alzheimer transgenic mice. Brain Res 2008, 1214:177-187.
45. Sonmez U., Sonmez A., Erbil G., Tekmen I., Baykara B. Neuroprotective effects of resveratrol against traumatic brain injury in immature rats. Neurosci Lett 2007, 420:133-137.
46. Stangl D., Thuret S. Impact of diet on adult hippocampal neurogenesis. Genes Nutr 2009, 4:271-282.
47. Suganuma M., Okabe S., Oniyama M., Tada Y., Ito H., Fujiki H. Wide distribution of [3H](-)-epigallocatechin gallate, a cancer preventive tea polyphenol, in mouse tissue. Carcinogenesis 1998, 19:1771-1776.
48. van Praag H., Lucero M.J., Yeo G.W., Stecker K., Heivand N., Zhao C., Yip E., Afanador M., Schroeter H., Hammerstone J., Gage F.H. Plant-derived flavanol (-)epicatechin enhances angiogenesis and retention of spatial memory in mice. J Neurosci 2007, 27:5869-5878.
49. Wang Y., Li M., Xu X., Song M., Tao H., Bai Y. Green tea epigallocatechin-3-gallate (EGCG) promotes neural progenitor cell proliferation and sonic hedgehog pathway activation during adult hippocampal neurogenesis. Mol Nutr Food Res 2012, 56:1292-1303.
50. Weinreb O., Amit T., Mandel S., Youdim M.B. Neuroprotective molecular mechanisms of (-)-epigallocatechin-3-gallate: a reflective outcome of its antioxidant, iron chelating and neuritogenic properties. Genes Nutr 2009, 4:283-296.
51. Yoo K.Y., Choi J.H., Hwang I.K., Lee C.H., Lee S.O., Han S.M., Shin H.C., Kang I.J., Won M.H. (-)-Epigallocatechin-3-gallate increases cell proliferation and neuroblasts in the subgranular zone of the dentate gyrus in adult mice. Phytother Res 2010, 24:1065-1070.
52. Zainuddin M.S., Thuret S. Nutrition, adult hippocampal neurogenesis and mental health. Br Med Bull 2012, 103:89-114.