Taurine increases hippocampal neurogenesis in aging mice

Stem Cell Research

Volumn 14, Issue 3, 2015, Pages 369-379

  Gebara, Elias ^a   Udry, Florian ^a   Sultan, Sébastien ^a   Toni, Nicolas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; DOUBLECORTIN; EOMESODERMIN; GREEN FLUORESCENT PROTEIN; NESTIN; SODIUM CHLORIDE; T BOX TRANSCRIPTION FACTOR; TAURINE;

ADULT; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; MALE; MICROGLIA; MIDDLE AGED; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FISCHER 344 RAT; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY;

MUS;

AGING; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; DENTATE GYRUS; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; RATS, INBRED F344; TAURINE;

EID: 84927622884     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2015.04.001     Document Type: Article

References (58)

1. Altman J., Das G.D. Post-natal origin of microneurones in the rat brain. Nature 1965, 207:953-956.
2. Banay-Schwartz M., Lajtha A., Palkovits M. Changes with aging in the levels of amino acids in rat CNS structural elements. II. Taurine and small neutral amino acids. Neurochem. Res. 1989, 14:563-570.
3. Bella D.L., Hirschberger L.L., Hosokawa Y., Stipanuk M.H. Mechanisms involved in the regulation of key enzymes of cysteine metabolism in rat liver in vivo. Am. J. Physiol. 1999, 276:E326-335.
4. Benrabh H., Bourre J.M., Lefauconnier J.M. Taurine transport at the blood-brain barrier: an in vivo brain perfusion study. Brain Res. 1995, 692:57-65.
5. Bernal G.M., Peterson D.A. Phenotypic and gene expression modification with normal brain aging in GFAP-positive astrocytes and neural stem cells. Aging Cell 2011, 10:466-482.
6. Bolognin S., Buffelli M., Puolivali J., Iqbal K. Rescue of cognitive-aging by administration of a neurogenic and/or neurotrophic compound. Neurobiol. Aging 2014, 35:2134-2146.
7. Bonaguidi M.A., Wheeler M.A., Shapiro J.S., Stadel R.P., Sun G.J., Ming G.L., Song H. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011, 145:1142-1155.
8. Calzolari F., Michel J., Baumgart E.V., Theis F., Gotz M., Ninkovic J. Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat. Neurosci. 2015, 18:490-492.
9. Chan C.Y., Sun H.S., Shah S.M., Agovic M.S., Friedman E., Banerjee S.P. Modes of direct modulation by taurine of the glutamate NMDA receptor in rat cortex. Eur. J. Pharmacol. 2014, 728:167-175.
10. Chen S.W., Kong W.X., Zhang Y.J., Li Y.L., Mi X.J., Mu X.S. Possible anxiolytic effects of taurine in the mouse elevated plus-maze. Life Sci. 2004, 75:1503-1511.
11. Choe K.Y., Olson J.E., Bourque C.W. Taurine release by astrocytes modulates osmosensitive glycine receptor tone and excitability in the adult supraoptic nucleus. J. Neurosci. 2012, 32:12518-12527.
12. Drew M.R., Hen R. Adult hippocampal neurogenesis as target for the treatment of depression. CNS Neurol. Disord. Drug Targets 2007, 6:205-218.
13. El Idrissi A. Taurine improves learning and retention in aged mice. Neurosci. Lett. 2008, 436:19-22.
14. El Idrissi A., Messing J., Scalia J., Trenkner E. Prevention of epileptic seizures by taurine. Adv. Exp. Med. Biol. 2003, 526:515-525.
15. Encinas J.M., Sierra A. Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav. Brain Res. 2012, 227:433-439.
16. Encinas J.M., Michurina T.V., Peunova N., Park J.H., Tordo J., Peterson D.A., Fishell G., Koulakov A., Enikolopov G. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 2011, 8:566-579.
17. Foos T.M., Wu J.Y. The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem. Res. 2002, 27:21-26.
18. Frank M.G., Barrientos R.M., Biedenkapp J.C., Rudy J.W., Watkins L.R., Maier S.F. mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 2006, 27:717-722.
19. Gebara E., Sultan S., Kocher-Braissant J., Toni N. Adult hippocampal neurogenesis inversely correlates with microglia in conditions of voluntary running and aging. Front. Neurosci. 2013, 7:145.
20. Gil-Mohapel J., Brocardo P.S., Choquette W., Gothard R., Simpson J.M., Christie B.R. Hippocampal neurogenesis levels predict WATERMAZE search strategies in the aging brain. PLoS One 2013, 8:e75125.
21. Hernandez-Benitez R., Ramos-Mandujano G., Pasantes-Morales H. Taurine stimulates proliferation and promotes neurogenesis of mouse adult cultured neural stem/progenitor cells. Stem Cell Res. 2012, 9:24-34.
22. Hodge R.D., Kowalczyk T.D., Wolf S.A., Encinas J.M., Rippey C., Enikolopov G., Kempermann G., Hevner R.F. Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J. Neurosci. 2008, 28:3707-3717.
23. Huxtable R.J. Physiological actions of taurine. Physiol. Rev. 1992, 72:101-163.
24. Katsimpardi L., Litterman N.K., Schein P.A., Miller C.M., Loffredo F.S., Wojtkiewicz G.R., Chen J.W., Lee R.T., Wagers A.J., Rubin L.L. Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 2014, 344:630-634.
25. Kheirbek M.A., Klemenhagen K.C., Sahay A., Hen R. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat. Neurosci. 2012, 15:1613-1620.
26. Kim C., Cha Y.N. Taurine chloramine produced from taurine under inflammation provides anti-inflammatory and cytoprotective effects. Amino Acids 2014, 46:89-100.
27. Kim J.W., Kim C. Inhibition of LPS-induced NO production by taurine chloramine in macrophages is mediated though Ras-ERK-NF-kappaB. Biochem. Pharmacol. 2005, 70:1352-1360.
28. Kim H.Y., Kim H.V., Yoon J.H., Kang B.R., Cho S.M., Lee S., Kim J.Y., Kim J.W., Cho Y., Woo J., Kim Y. Taurine in drinking water recovers learning and memory in the adult APP/PS1 mouse model of Alzheimer's disease. Sci. Rep. 2014, 4:7467.
29. Kohman R.A. Aging microglia: relevance to cognition and neural plasticity. Methods Mol. Biol. 2012, 934:193-218.
30. 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, 467:455-463.
31. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 1996, 16:2027-2033.
32. Leon R., Wu H., Jin Y., Wei J., Buddhala C., Prentice H., Wu J.Y. Protective function of taurine in glutamate-induced apoptosis in cultured neurons. J. Neurosci. Res. 2009, 87:1185-1194.
33. Mathieu P., Battista D., Depino A., Roca V., Graciarena M., Pitossi F. The more you have, the less you get: the functional role of inflammation on neuronal differentiation of endogenous and transplanted neural stem cells in the adult brain. J. Neurochem. 2010, 112:1368-1385.
34. Menzie J., Prentice H., Wu J.Y. Neuroprotective mechanisms of taurine against ischemic stroke. Brain Sci. 2013, 3:877-907.
35. Miller T.J., Hanson R.D., Yancey P.H. Developmental changes in organic osmolytes in prenatal and postnatal rat tissues. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2000, 125:45-56.
36. Muth-Kohne E., Pachernegg S., Karus M., Faissner A., Hollmann M. Expression of NMDA receptors and Ca2+-impermeable AMPA receptors requires neuronal differentiation and allows discrimination between two different types of neural stem cells. Cell. Physiol. Biochem. 2010, 26:935-946.
37. Namba T., Maekawa M., Yuasa S., Kohsaka S., Uchino S. The Alzheimer's disease drug memantine increases the number of radial glia-like progenitor cells in adult hippocampus. Glia 2009, 57:1082-1090.
38. Neuwirth L.S., Volpe N.P., El Idrissi A. Taurine effects on emotional learning and memory in aged mice: neurochemical alterations and differentiation in auditory cued fear and context conditioning. Adv. Exp. Med. Biol. 2013, 775:195-214.
39. Palmer T.D., Takahashi J., Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 1997, 8:389-404.
40. Preissler J., Grosche A., Lede V., Le Duc D., Krugel K., Matyash V., Szulzewsky F., Kallendrusch S., Immig K., Kettenmann H., Bechmann I., Schoneberg T., Schulz A. Altered microglial phagocytosis in GPR34-deficient mice. Glia 2015, 63:206-215.
41. Ramos-Mandujano G., Hernandez-Benitez R., Pasantes-Morales H. Multiple mechanisms mediate the taurine-induced proliferation of neural stem/progenitor cells from the subventricular zone of the adult mouse. Stem Cell Res. 2014, 12:690-702.
42. Ripps H., Shen W. Review: taurine: a "very essential" amino acid. Mol. Vis. 2012, 18:2673-2686.
43. Schaffer S.W., Azuma J., Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can. J. Physiol. Pharmacol. 2009, 87:91-99.
44. Schmidt-Hieber C., Jonas P., Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004, 429:184-187.
45. Seri B., Garcia-Verdugo J.M., Collado-Morente L., McEwen B.S., Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 2004, 478:359-378.
46. Streit W.J., Walter S.A., Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 1999, 57:563-581.
47. Sturman J.A., Moretz R.C., French J.H., Wisniewski H.M. Postnatal taurine deficiency in the kitten results in a persistence of the cerebellar external granule cell layer: correction by taurine feeding. J. Neurosci. Res. 1985, 13:521-528.
48. Sultan S., Gebara E.G., Moullec K., Toni N. d-serine increases adult hippocampal neurogenesis. Front. Neurosci. 2013, 7:155.
49. Sultan S., Gebara E., Toni N. Doxycycline increases neurogenesis and reduces microglia in the adult hippocampus. Front. Neurosci. 2013, 7:131.
50. 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, 442:929-933.
51. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 2007, 53:198-214.
52. Thuret S., Toni N., Aigner S., Yeo G.W., Gage F.H. Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 2009, 19:658-669.
53. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 2005, 25:8680-8685.
54. 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.
55. Walter J., Keiner S., Witte O.W., Redecker C. Age-related effects on hippocampal precursor cell subpopulations and neurogenesis. Neurobiol. Aging 2011, 32:1906-1914.
56. Wu J.Y., Tang X.W., Schloss J.V., Faiman M.D. Regulation of taurine biosynthesis and its physiological significance in the brain. Adv. Exp. Med. Biol. 1998, 442:339-345.
57. Wu H., Jin Y., Wei J., Jin H., Sha D., Wu J.Y. Mode of action of taurine as a neuroprotector. Brain Res. 2005, 1038:123-131.
58. Yamaguchi M., Saito H., Suzuki M., Mori K. Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 2000, 11:1991-1996.