Journal of Experimental & Clinical Medicine
Volume 4, Issue 1 , Pages 1-7 , February 2012

Modes of Action of Taurine and Granulocyte Colony-stimulating Factor in Neuroprotection

  • Chandana Buddhala
    • ,
  • Howard Prentice
    • ,
  • Jang-Yen Wu

      Affiliations

    • Corresponding Author InformationCorresponding author. Jang-Yen Wu, Schmidt Senior Fellow and Distinguished Professor, Florida Atlantic University, Charles E. Schmidt College of Medicine, 777 Glades Road, P.O. Box 3091, Boca Raton, FL 33431-0991, USA.

Received 22 September 2011 ,Accepted 19 October 2011.

References 

  1. Vitvitsky V, Garg SK, Banerjee R. Taurine biosynthesis by neurons and astrocytes. J Biol Chem. 2011;286:32002–32010
  2. Oja SS, Saransaari P. Pharmacology of taurine. Proc West Pharmacol. 2007;50:8–15
  3. Sun M, Zhao Y, Gu Y, Xu C. Anti-inflammatory mechanism of taurine against ischemic stroke is related to down-regulation of PARP and NF-kappaB. Amino Acids. 2011;
  4. Miao J, Zhang J, Zheng L, Yu X, Zhu W, Zou S. Taurine attenuates Streptococcus uberis-induced mastitis in rats by increasing T regulatory cells. Amino Acids. 2011;
  5. Schaffer S, Takahashi K, Azuma J. Role of osmoregulation in the actions of taurine. Amino Acids. 2000;19:527–546
  6. Schaffer SW, Azuma J, Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol. 2009;87:91–99
  7. Hernandez-Benitez R, Pasantes-Morales H, Saldana IT, Ramos-Mandujano G. Taurine stimulates proliferation of mice embryonic cultured neural progenitor cells. J Neurosci Res. 2010;88:1673–1681
  8. Lima L, Cubillos S. Taurine might be acting as a trophic factor in the retina by modulating phosphorylation of cellular proteins. J Neurosci Res. 1998;53:377–384
  9. Chen WQ, Jin H, Nguyen M, Carr J, Lee YJ, Hsu CC, et al Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J Neurosci Res. 2001;66:612–619
  10. El Idrissi A, Trenkner E. Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism. J Neurosci. 1999;19:9459–9468
  11. Foos TM, Wu JY. The role of taurine in the central nervous system and the modulation of intracellular calcium homeostasis. Neurochem Res. 2002;27:21–26
  12. Bidri M, Choay P. Taurine: a particular aminoacid with multiple functions. Ann Pharm Fr. 2003;61:385–391
  13. Birdsall TC. Therapeutic applications of taurine. Altern Med Rev. 1998;3:128–136
  14. Lin CT, Song GX, Wu JY. Ultrastructural demonstration of L-glutamate decarboxylase and cysteinesulfinic acid decarboxylase in rat retina by immunocytochemistry. Brain Res. 1985;331:71–80
  15. Magnusson KR, Clements JR, Wu JY, Beitz AJ. Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the hippocampus of the rat. Synapse. 1989;4:55–69
  16. Magnusson KR, Madl JE, Clements JR, Wu JY, Larson AA, Beitz AJ. Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the cerebellum of the rat with monoclonal antibodies against taurine. J Neurosci. 1988;8:4551–4564
  17. Kontro P, Marnela KM, Oja SS. Free amino acids in the synaptosome and synaptic vesicle fractions of different bovine brain areas. Brain Res. 1980;184:129–141
  18. Philibert RA, Rogers KL, Dutton GR. Stimulus-coupled taurine efflux from cerebellar neuronal cultures: on the roles of Ca++ and Na+. J Neurosci Res. 1989;22:167–171
  19. Pin JP, Weiss S, Sebben M, Kemp DE, Bockaert J. Release of endogenous amino acids from striatal neurons in primary culture. J Neurochem. 1986;47:594–603
  20. Wu JY, Tang XW, Tsai WH. Taurine receptor: kinetic analysis and pharmacological studies. Adv Exp Med Biol. 1992;315:263–268
  21. Frosini M, Sesti C, Saponara S, Ricci L, Valoti M, Palmi M, et al A specific taurine recognition site in the rabbit brain is responsible for taurine effects on thermoregulation. Br J Pharmacol. 2003;139:487–494
  22. Wu J, Kohno T, Georgiev SK, Ikoma M, Ishii H, Petrenko AB, et al. Taurine activates glycine and gamma-aminobutyric acid A receptors in rat substantia gelatinosa neurons. Neuroreport. 2008;19:333–337
  23. Heller-Stilb B, van Roeyen C, Rascher K, Hartwig HG, Huth A, Seeliger MW, et al Disruption of the taurine transporter gene (taut) leads to retinal degeneration in mice. FASEB J. 2002;16:231–233
  24. Warskulat U, Borsch E, Reinehr R, Heller-Stilb B, Roth C, Witt M, et al. Taurine deficiency and apoptosis: findings from the taurine transporter knockout mouse. Arch Biochem Biophys. 2007;462:202–209
  25. Warskulat U, Heller-Stilb B, Oermann E, Zilles K, Haas H, Lang F, et al. Phenotype of the taurine transporter knockout mouse. Methods Enzymol. 2007;428:439–458
  26. Besson MT, Re DB, Moulin M, Birman S. High affinity transport of taurine by the Drosophila aspartate transporter dEAAT2. J Biol Chem. 2005;280:6621–6626
  27. Chan-Palay V, Lin CT, Palay S, Yamamoto M, Wu JY. Taurine in the mammalian cerebellum: demonstration by autoradiography with [3H]taurine and immunocytochemistry with antibodies against the taurine-synthesizing enzyme, cysteine-sulfinic acid decarboxylase. Proc Natl Acad Sci (USA). 1982;79:2695–2699
  28. Hanretta AT, Lombardini JB. Is taurine a hypothalamic neurotransmitter? A model of the differential uptake and compartmentalization of taurine by neuronal and glial cell particles from the rat hypothalamus. Brain Res. 1987;434:167–201
  29. Fykse EM, Fonnum F. Amino acid neurotransmission: dynamics of vesicular uptake. Neurochem Res. 1996;21:1053–1060
  30. Hess DC, Borlongan CV. Stem cells and neurological diseases. Cell Prolif. 2008;41(suppl. 1):94–114
  31. Schneider A, Kuhn HG, Schabitz WR. A role for G-CSF (granulocyte-colony stimulating factor) in the central nervous system. Cell Cycle. 2005;4:1753–1757
  32. Meuer K, Pitzer C, Teismann P, Kruger C, Goricke B, Laage R, et al Granulocyte-colony stimulating factor is neuroprotective in a model of Parkinson’s disease. J Neurochem. 2006;97:675–686
  33. Zhao C, Xie Z, Wang P, Wang Y, Lai C, Zhu Z, et al Granulocyte-colony stimulating factor protects memory impairment in the senescence-accelerated mouse (SAM)-P10. Neurol Res. 2011;33:354–359
  34. Bennett CL, Smith TJ, Weeks JC, Bredt AB, Feinglass J, Fetting JH, et al Use of hematopoietic colony-stimulating factors: the American Society of Clinical Oncology survey. The Health Services Research Committee of the American Society of Clinical Oncology. J Clin Oncol. 1996;14:2511–2520
  35. Schneider A, Kruger C, Steigleder T, Weber D, Pitzer C, Laage R, et al The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest. 2005;115:2083–2098
  36. Zhao LR, Navalitloha Y, Singhal S, Mehta J, Piao CS, Guo WP, et al Hematopoietic growth factors pass through the blood-brain barrier in intact rats. Exp Neurol. 2007;204:569–573
  37. Lee ST, Park JE, Kim DH, Kim S, Im WS, Kang L, et al Granulocyte-colony stimulating factor attenuates striatal degeneration with activating survival pathways in 3-nitropropionic acid model of Huntington’s disease. Brain Res. 2008;1194:130–137
  38. Sevimli S, Diederich K, Strecker JK, Schilling M, Klocke R, Nikol S, et al Endogenous brain protection by granulocyte-colony stimulating factor after ischemic stroke. Exp Neurol. 2009;217:328–335
  39. Paschen W. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium. 2001;29:1–11
  40. Pivovarova NB, Andrews SB. Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J. 2010;277:3622–3636
  41. Tang TS, Slow E, Lupu V, Stavrovskaya IG, Sugimori M, Llinas R, et al Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington’s disease. Proc Natl Acad Sci U S A. 2005;102:2602–2607
  42. Lau A, Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010;460:525–542
  43. Wu H, Jin Y, Wei J, Jin H, Sha D, Wu JY. Mode of action of taurine as a neuroprotector. Brain Res. 2005;1038:123–131
  44. Wu JY, Chen W, Tang XW, Jin H, Foos T, Schloss JV, et al Mode of action of taurine and regulation dynamics of its synthesis in the CNS. Adv Exp Med Biol. 2000;483:35–44
  45. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, et al Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci. 1999;19:4449–4461
  46. Riedel G, Platt B, Micheau J. Glutamate receptor function in learning and memory. Behav Brain Res. 2003;140:1–47
  47. Wang Y, Qin ZH. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis. 2010;15:1382–1402
  48. Leon R, Wu H, Jin Y, Wei J, Buddhala C, Prentice H, et al. Protective function of taurine in glutamate-induced apoptosis in cultured neurons. J Neurosci Res. 2009;87:1185–1194
  49. Khan SH, Banigesh A, Baziani A, Todd KG, Miyashita H, Eweida M, et al. The role of taurine in neuronal protection following transient global forebrain ischemia. Neurochem Res. 2000;25:217–223
  50. Tang XC, Rao MR, Hu G, Wang H. Alterations of amino acid levels from striatum, hippocampus, and cerebral cortex induced by global cerebral ischemia in gerbil. Acta Pharmacol Sin. 2000;21:819–823
  51. Saransaari P, Oja SS. Modulation of taurine release in ischemia by glutamate receptors in mouse brain stem slices. Amino Acids. 2010;38:739–746
  52. Gao X, Yang X, Zhang B. Neuroprotection of taurine against bilirubin-induced elevation of apoptosis and intracellular free calcium ion. in vivo. Toxicol Mech Methods. 2011;21:383–387
  53. Taranukhin AG, Taranukhina EY, Saransaari P, Podkletnova IM, Pelto-Huikko M, Oja SS. Neuroprotection by taurine in ethanol-induced apoptosis in the developing cerebellum. J Biomed Sci. 2010;17(suppl. 1):S12
  54. Taranukhin AG, Taranukhina EY, Saransaari P, Djatchkova IM, Pelto-Huikko M, Oja SS. Taurine reduces caspase-8 and caspase-9 expression induced by ischemia in the mouse hypothalamic nuclei. Amino Acids. 2008;34:169–174
  55. Sun M, Xu C. Neuroprotective mechanism of taurine due to up-regulating calpastatin and down-regulating calpain and caspase-3 during focal cerebral ischemia. Cell Mol Neurobiol. 2008;28:593–611
  56. Castro RE, Sola S, Ramalho RM, Steer CJ, Rodrigues CM. The bile acid tauroursodeoxycholic acid modulates phosphorylation and translocation of bad via phosphatidylinositol 3-kinase in glutamate-induced apoptosis of rat cortical neurons. J Pharmacol Exp Ther. 2004;311:845–852
  57. Sola S, Castro RE, Laires PA, Steer CJ, Rodrigues CM. Tauroursodeoxycholic acid prevents amyloid-beta peptide-induced neuronal death via a phosphatidylinositol 3-kinase-dependent signaling pathway. Mol Med. 2003;9:226–234
  58. Duan WM, Rodrigues CM, Zhao LR, Steer CJ, Low WC. Tauroursodeoxycholic acid improves the survival and function of nigral transplants in a rat model of Parkinson’s disease. Cell Transplant. 2002;11:195–205
  59. Keene CD, Rodrigues CM, Eich T, Linehan-Stieers C, Abt A, Kren BT, et al A bile acid protects against motor and cognitive deficits and reduces striatal degeneration in the 3-nitropropionic acid model of Huntington’s disease. Exp Neurol. 2001;171:351–360
  60. Chen K, Zhang Q, Wang J, Liu F, Mi M, Xu H, et al Taurine protects transformed rat retinal ganglion cells from hypoxia-induced apoptosis by preventing mitochondrial dysfunction. Brain Res. 2009;1279:131–138
  61. Dykens JA. Isolated cerebral and cerebellar mitochondria produce free radicals when exposed to elevated CA2+ and Na+: implications for neurodegeneration. J Neurochem. 1994;63:584–591
  62. Lievre V, Becuwe P, Bianchi A, Bossenmeyer-Pourie C, Koziel V, Franck P, et al Intracellular generation of free radicals and modifications of detoxifying enzymes in cultured neurons from the developing rat forebrain in response to transient hypoxia. Neuroscience. 2001;105:287–297
  63. Jana S, Sinha M, Chanda D, Roy T, Banerjee K, Munshi S, et al Mitochondrial dysfunction mediated by quinone oxidation products of dopamine: implications in dopamine cytotoxicity and pathogenesis of Parkinson’s disease. Biochim Biophys Acta. 2011;1812:663–673
  64. Rodrigues CM, Stieers CL, Keene CD, Ma X, Kren BT, Low WC, et al. Tauroursodeoxycholic acid partially prevents apoptosis induced by 3-nitropropionic acid: evidence for a mitochondrial pathway independent of the permeability transition. J Neurochem. 2000;75:2368–2379
  65. Zhao P, Huang YL, Cheng JS. Taurine antagonizes calcium overload induced by glutamate or chemical hypoxia in cultured rat hippocampal neurons. Neurosci Lett. 1999;268:25–28
  66. El Idrissi A. Taurine increases mitochondrial buffering of calcium: role in neuroprotection. Amino Acids. 2008;34:321–328
  67. Palmi M, Youmbi GT, Sgaragli G, Meini A, Benocci A, Fusi F, et al The mitochondrial permeability transition and taurine. Adv Exp Med Biol. 2000;483:87–96
  68. Sun M, Gu Y, Zhao Y, Xu C. Protective functions of taurine against experimental stroke through depressing mitochondria-mediated cell death in rats. Amino Acids. 2011;40:1419–1429
  69. Patel AJ, Lauritzen I, Lazdunski M, Honore E. Disruption of mitochondrial respiration inhibits volume-regulated anion channels and provokes neuronal cell swelling. J Neurosci. 1998;18:3117–3123
  70. Harvey VL, Saul MW, Garner C, McDonald RL. A role for the volume regulated anion channel in volume regulation in the murine CNS cell line, CAD. Acta Physiol (Oxf). 2010;198:159–168
  71. Pasantes-Morales H, Tuz K. Volume changes in neurons: hyperexcitability and neuronal death. Contrib Nephrol. 2006;152:221–240
  72. Kreisman NR, Olson JE. Taurine enhances volume regulation in hippocampal slices swollen osmotically. Neuroscience. 2003;120:635–642
  73. Ricci L, Valoti M, Sgaragli G, Frosini M. Protection by taurine of rat brain cortical slices against oxygen glucose deprivation- and reoxygenation-induced damage. Eur J Pharmacol. 2009;621:26–32
  74. Chakrabarti A, Chen AW, Varner JD. A review of the mammalian unfolded protein response. Biotechnol Bioeng. 2011;108:2777–2793
  75. Paschen W, Mengesdorf T. Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium. 2005;38:409–415
  76. Martinez JA, Zhang Z, Svetlov SI, Hayes RL, Wang KK, Larner SF. Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis. 2010;15:1480–1493
  77. Ilieva EV, Kichev A, Naudi A, Ferrer I, Pamplona R, Portero-Otin M. Mitochondrial dysfunction and oxidative and endoplasmic reticulum stress in argyrophilic grain disease. J Neuropathol Exp Neurol. 2011;70:253–263
  78. Smaili S, Hirata H, Ureshino R, Monteforte PT, Morales AP, Muler ML, et al Calcium and cell death signaling in neurodegeneration and aging. An Acad Bras Cienc. 2009;81:467–475
  79. Pan C, Giraldo GS, Prentice H, Wu JY. Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress. J Biomed Sci. 2010;17(suppl 1):S17
  80. Pan C, Gupta A, Prentice H, Wu JY. Protection of taurine and granulocyte colony-stimulating factor against excitotoxicity induced by glutamate in primary cortical neurons. J Biomed Sci. 2010;17(suppl. 1):S18
  81. Louzada PR, Paula Lima AC, Mendonca-Silva DL, Noel F, De Mello FG, Ferreira ST. Taurine prevents the neurotoxicity of beta-amyloid and glutamate receptor agonists: activation of GABA receptors and possible implications for Alzheimer’s disease and other neurological disorders. FASEB J. 2004;18:511–518
  82. Okamoto K, Kimura H, Sakai Y. Taurine-induced increase of the Cl-conductance of cerebellar Purkinje cell dendrites in vitro. Brain Res. 1983;259:319–323
  83. Demetri GD, Griffin JD. Granulocyte colony-stimulating factor and its receptor. Blood. 1991;78:2791–2808
  84. McCollum M, Ma Z, Cohen E, Leon R, Tao R, Wu JY, et al Post-MPTP treatment with granulocyte colony-stimulating factor improves nigrostriatal function in the mouse model of Parkinson’s disease. Mol Neurobiol. 2010;41:410–419
  85. Wu JY, Maharaj D. Method of treating neurodegenerative diseases. United States Patent and Trademark Office; 2008;Publication No. US-2008-0300176-A1
  86. Lu CZ, Xiao BG. Neuroprotection of G-CSF in cerebral ischemia. Front Biosci. 2007;12:2869–2875
  87. Yata K, Matchett GA, Tsubokawa T, Tang J, Kanamaru K, Zhang JH. Granulocyte-colony stimulating factor inhibits apoptotic neuron loss after neonatal hypoxia-ischemia in rats. Brain Res. 2007;1145:227–238
  88. Nishio Y, Koda M, Kamada T, Someya Y, Kadota R, Mannoji C, et al Granulocyte colony-stimulating factor attenuates neuronal death and promotes functional recovery after spinal cord injury in mice. J Neuropathol Exp Neurol. 2007;66:724–731
  89. Pitzer C, Klussmann S, Kruger C, Letellier E, Plaas C, Dittgen T, et al The hematopoietic factor granulocyte-colony stimulating factor improves outcome in experimental spinal cord injury. J Neurochem. 2010;113:930–942
  90. Solaroglu I, Tsubokawa T, Cahill J, Zhang JH. Anti-apoptotic effect of granulocyte-colony stimulating factor after focal cerebral ischemia in the rat. Neuroscience. 2006;143:965–974
  91. Henriques A, Pitzer C, Dupuis L, Schneider A. G-CSF protects motoneurons against axotomy-induced apoptotic death in neonatal mice. BMC Neurosci. 2010;11:25
  92. Tsai RK, Chang CH, Sheu MM, Huang ZL. Anti-apoptotic effects of human granulocyte colony-stimulating factor (G-CSF) on retinal ganglion cells after optic nerve crush are PI3K/AKT-dependent. Exp Eye Res. 2010;90:537–545
  93. Huang HY, Lin SZ, Kuo JS, Chen WF, Wang MJ. G-CSF protects dopaminergic neurons from 6-OHDA-induced toxicity via the ERK pathway. Neurobiol Aging. 2007;28:1258–1269
  94. Jung KH, Chu K, Lee ST, Kim SJ, Sinn DI, Kim SU, et al Granulocyte colony-stimulating factor stimulates neurogenesis via vascular endothelial growth factor with STAT activation. Brain Res. 2006;1073-1074:190–201
  95. Schabitz WR, Kollmar R, Schwaninger M, Juettler E, Bardutzky J, Scholzke MN, et al Neuroprotective effect of granulocyte colony-stimulating factor after focal cerebral ischemia. Stroke. 2003;34:745–751

PII: S1878-3317(11)00155-0

doi: 10.1016/j.jecm.2011.11.001

Journal of Experimental & Clinical Medicine
Volume 4, Issue 1 , Pages 1-7 , February 2012

Article Tools

* Image Usage & Resolution