Lithium suppresses astrogliogenesis by neural stem and progenitor cells by inhibiting stat3 pathway independently of glycogen synthase kinase 3 beta

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Zhu, Zhenzhong ^a,b   Kremer, Penny ^b   Tadmori, Iman ^b   Ren, Yi ^b   Sun, Dongming ^b   He, Xijing ^a   Young, Wise ^b  

^a THE SECOND AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; 5 AMINOIMIDAZOLE 4 CARBOXAMIDE 1 BETA RIBOFURANOSIDE; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM; NITROIMIDAZOLE DERIVATIVE; STAT3 PROTEIN; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INDOLE DERIVATIVE; JANUS KINASE; MALEIMIDE DERIVATIVE; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROGLIOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; GLIA RESTRICTED PROGENITOR CELL; NEURAL STEM CELL; NEWBORN; NONHUMAN; PROTEIN DOMAIN; RAT; SUBVENTRICULAR ZONE; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; METABOLISM; NERVE CELL; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

RATTUS;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; INDOLES; JANUS KINASES; LITHIUM; MALEIMIDES; NEURAL STEM CELLS; NEURONS; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; RATS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 80052588138     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023341     Document Type: Article

References (79)

1. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, et al. (2001) Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167: 48-58.
2. Nakamura M, Okada S, Toyama Y, Okano H, (2005) Role of IL-6 in spinal cord injury in a mouse model. Clin Rev Allergy Immunol 28: 197-204.
3. Mukaino M, Nakamura M, Okada S, Toyama Y, Liu M, et al. (2008) [Role of IL-6 in regulation of inflammation and stem cell differentiation in CNS trauma]. Nihon Rinsho Meneki Gakkai Kaishi 31: 93-98.
4. Lee MY, Kim CJ, Shin SL, Moon SH, Chun MH, (1998) Increased ciliary neurotrophic factor expression in reactive astrocytes following spinal cord injury in the rat. Neurosci Lett 255: 79-82.
5. Tripathi RB, McTigue DM, (2008) Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J Comp Neurol 510: 129-144.
6. Kurek JB, Bennett TM, Bower JJ, Muldoon CM, Austin L, (1998) Leukaemia inhibitory factor (LIF) production in a mouse model of spinal trauma. Neurosci Lett 249: 1-4.
7. Weible MW 2nd, Chan-Ling T, (2007) Phenotypic characterization of neural stem cells from human fetal spinal cord: synergistic effect of LIF and BMP4 to generate astrocytes. Glia 55: 1156-1168.
8. Ogawa Y, Sawamoto K, Miyata T, Miyao S, Watanabe M, et al. (2002) Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 69: 925-933.
9. Okano H, Ogawa Y, Nakamura M, Kaneko S, Iwanami A, et al. (2003) Transplantation of neural stem cells into the spinal cord after injury. Semin Cell Dev Biol 14: 191-198.
10. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, et al. (2005) Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102: 14069-14074.
11. Okada S, Ishii K, Yamane J, Iwanami A, Ikegami T, et al. (2005) In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. Faseb J 19: 1839-1841.
12. Parr AM, Kulbatski I, Tator CH, (2007) Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma 24: 835-845.
13. Sahni V, Kessler JA, (2010) Stem cell therapies for spinal cord injury. Nature Reviews Neurology 6: 363-372.
14. Young W, (2009) Review of lithium effects on brain and blood. Cell Transplant 18: 951-975.
15. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK, (2000) Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75: 1729-1734.
16. Vazey EM, Connor B, (2009) In vitro priming to direct neuronal fate in adult neural progenitor cells. Exp Neurol 216: 520-524.
17. Lyoo IK, Dager SR, Kim JE, Yoon SJ, Friedman SD, et al. (2010) Lithium-induced gray matter volume increase as a neural correlate of treatment response in bipolar disorder: a longitudinal brain imaging study. Neuropsychopharmacology 35: 1743-1750.
18. Kempton MJ, Geddes JR, Ettinger U, Williams SC, Grasby PM, (2008) Meta-analysis, database, and meta-regression of 98 structural imaging studies in bipolar disorder. Arch Gen Psychiatry 65: 1017-1032.
19. Bearden CE, Thompson PM, Dutton RA, Frey BN, Peluso MA, et al. (2008) Three-dimensional mapping of hippocampal anatomy in unmedicated and lithium-treated patients with bipolar disorder. Neuropsychopharmacology 33: 1229-1238.
20. Sassi RB, Nicoletti M, Brambilla P, Mallinger AG, Frank E, et al. (2002) Increased gray matter volume in lithium-treated bipolar disorder patients. Neurosci Lett 329: 243-245.
21. Su H, Chu TH, Wu W, (2007) Lithium enhances proliferation and neuronal differentiation of neural progenitor cells in vitro and after transplantation into the adult rat spinal cord. Exp Neurol 206: 296-307.
22. Dill J, Wang H, Zhou F, Li S, (2008) Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J Neurosci 28: 8914-8928.
23. Yick LW, So KF, Cheung PT, Wu WT, (2004) Lithium chloride reinforces the regeneration-promoting effect of chondroitinase ABC on rubrospinal neurons after spinal cord injury. J Neurotrauma 21: 932-943.
24. Boku S, Nakagawa S, Masuda T, Nishikawa H, Kato A, et al. (2009) Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway. Neuropsychopharmacology 34: 805-815.
25. Wexler EM, Geschwind DH, Palmer TD, (2008) Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol Psychiatry 13: 285-292.
26. Kim JS, Chang MY, Yu IT, Kim JH, Lee SH, et al. (2004) Lithium selectively increases neuronal differentiation of hippocampal neural progenitor cells both in vitro and in vivo. J Neurochem 89: 324-336.
27. Jope RS, (2003) Lithium and GSK-3: one inhibitor, two inhibitory actions, multiple outcomes. Trends Pharmacol Sci 24: 441-443.
28. Lenox RH, Wang L, (2003) Molecular basis of lithium action: integration of lithium-responsive signaling and gene expression networks. Mol Psychiatry 8: 135-144.
29. Beurel E, Jope RS, (2008) Differential regulation of STAT family members by glycogen synthase kinase-3. J Biol Chem 283: 21934-21944.
30. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, et al. (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278: 477-483.
31. Lois C, Alvarez-Buylla A, (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 90: 2074-2077.
32. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354.
33. Farr GH 3rd, Ferkey DM, Yost C, Pierce SB, Weaver C, et al. (2000) Interaction among GSK-3, GBP, axin, and APC in Xenopus axis specification. J Cell Biol 148: 691-702.
34. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS, (2003) Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 278: 33067-33077.
35. Hedgepeth CM, Deardorff MA, Klein PS, (1999) Xenopus axin interacts with glycogen synthase kinase-3 beta and is expressed in the anterior midbrain. Mech Dev 80: 147-151.
36. Hedgepeth CM, Deardorff MA, Rankin K, Klein PS, (1999) Regulation of glycogen synthase kinase 3beta and downstream Wnt signaling by axin. Mol Cell Biol 19: 7147-7157.
37. Lendahl U, Zimmerman LB, McKay RD, (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
38. Rao MS, Mayer-Proschel M, (1997) Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 188: 48-63.
39. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS, (1997) Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19: 773-785.
40. Su H, Zhang W, Guo J, Guo A, Yuan Q, et al. (2009) Lithium enhances the neuronal differentiation of neural progenitor cells in vitro and after transplantation into the avulsed ventral horn of adult rats through the secretion of brain-derived neurotrophic factor. J Neurochem 108: 1385-1398.
41. Fernando P, Brunette S, Megeney LA, (2005) Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. FASEB J 19: 1671-1673.
42. Park DS, So HS, Lee JH, Park HY, Lee YJ, et al. (2009) Simvastatin treatment induces morphology alterations and apoptosis in murine cochlear neuronal cells. Acta Otolaryngol 129: 166-174.
43. Hacker G, (2000) The morphology of apoptosis. Cell Tissue Res 301: 5-17.
44. Lucas FR, Salinas PC, (1997) WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev Biol 192: 31-44.
45. Endl E, Gerdes J, (2000) The Ki-67 protein: fascinating forms and an unknown function. Exp Cell Res 257: 231-237.
46. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, et al. (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133: 1710-1715.
47. Cao F, Hata R, Zhu P, Nakashiro KI, Sakanaka M, (2010) Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun.
48. Zhu P, Hata R, Cao F, Gu F, Hanakawa Y, et al. (2008) Ramified microglial cells promote astrogliogenesis and maintenance of neural stem cells through activation of Stat3 function. FASEB J 22: 3866-3877.
49. Ni CW, Hsieh HJ, Chao YJ, Wang DL, (2003) Shear flow attenuates serum-induced STAT3 activation in endothelial cells. J Biol Chem 278: 19702-19708.
50. Ma J, Zhang T, Novotny-Diermayr V, Tan AL, Cao X, (2003) A novel sequence in the coiled-coil domain of Stat3 essential for its nuclear translocation. J Biol Chem 278: 29252-29260.
51. Zang Y, Yu LF, Pang T, Fang LP, Feng X, et al. (2008) AICAR induces astroglial differentiation of neural stem cells via activating the JAK/STAT3 pathway independently of AMP-activated protein kinase. J Biol Chem 283: 6201-6208.
52. Hedgepeth CM, Conrad LJ, Zhang J, Huang HC, Lee VM, et al. (1997) Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev Biol 185: 82-91.
53. Orre K, Wennstrom M, Tingstrom A, (2009) Chronic lithium treatment decreases NG2 cell proliferation in rat dentate hilus, amygdala and corpus callosum. Prog Neuropsychopharmacol Biol Psychiatry 33: 503-510.
54. Beurel E, Jope RS, (2009) Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-3 and STAT3 in the brain. J Neuroinflammation 6: 9.
55. Beurel E, Jope RS, (2009) Glycogen synthase kinase-3 promotes the synergistic action of interferon-gamma on lipopolysaccharide-induced IL-6 production in RAW264.7 cells. Cell Signal 21: 978-985.
56. York JD, Ponder JW, Majerus PW, (1995) Definition of a metal-dependent/Li(+)-inhibited phosphomonoesterase protein family based upon a conserved three-dimensional core structure. Proc Natl Acad Sci U S A 92: 5149-5153.
57. Phiel CJ, Klein PS, (2001) Molecular targets of lithium action. Annu Rev Pharmacol Toxicol 41: 789-813.
58. Hallcher LM, Sherman WR, (1980) The effects of lithium ion and other agents on the activity of myo-inositol-1-phosphatase from bovine brain. J Biol Chem 255: 10896-10901.
59. Sherman WR, Gish BG, Honchar MP, Munsell LY, (1986) Effects of lithium on phosphoinositide metabolism in vivo. Fed Proc 45: 2639-2646.
60. Chalecka-Franaszek E, Chuang DM, (1999) Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci U S A 96: 8745-8750.
61. Ghosh MK, Sharma P, Harbor PC, Rahaman SO, Haque SJ, (2005) PI3K-AKT pathway negatively controls EGFR-dependent DNA-binding activity of Stat3 in glioblastoma multiforme cells. Oncogene 24: 7290-7300.
62. Justicia C, Gabriel C, Planas AM, (2000) Activation of the JAK/STAT pathway following transient focal cerebral ischemia: signaling through Jak1 and Stat3 in astrocytes. Glia 30: 253-270.
63. Acarin L, Gonzalez B, Castellano B, (2000) STAT3 and NFkappaB activation precedes glial reactivity in the excitotoxically injured young cortex but not in the corresponding distal thalamic nuclei. J Neuropathol Exp Neurol 59: 151-163.
64. Cao F, Hata R, Zhu P, Nakashiro K, Sakanaka M, (2010) Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun 394: 843-847.
65. Kim OS, Park EJ, Joe EH, Jou I, (2002) JAK-STAT signaling mediates gangliosides-induced inflammatory responses in brain microglial cells. J Biol Chem 277: 40594-40601.
66. Huang C, Ma R, Sun S, Wei G, Fang Y, et al. (2008) JAK2-STAT3 signaling pathway mediates thrombin-induced proinflammatory actions of microglia in vitro. J Neuroimmunol 204: 118-125.
67. Caldwell GM, Jones CE, Soon Y, Warrack R, Morton DG, et al. (2008) Reorganisation of Wnt-response pathways in colorectal tumorigenesis. Br J Cancer 98: 1437-1442.
68. Le Floch N, Rivat C, De Wever O, Bruyneel E, Mareel M, et al. (2005) The proinvasive activity of Wnt-2 is mediated through a noncanonical Wnt pathway coupled to GSK-3beta and c-Jun/AP-1 signaling. Faseb J 19: 144-146.
69. Merdek KD, Nguyen NT, Toksoz D, (2004) Distinct activities of the alpha-catenin family, alpha-catulin and alpha-catenin, on beta-catenin-mediated signaling. Mol Cell Biol 24: 2410-2422.
70. Bordonaro M, Lazarova DL, Carbone R, Sartorelli AC, (2004) Modulation of Wnt-specific colon cancer cell kill by butyrate and lithium. Oncol Res 14: 427-438.
71. Edwards CM, Edwards JR, Lwin ST, Esparza J, Oyajobi BO, et al. (2008) Increasing Wnt signaling in the bone marrow microenvironment inhibits the development of myeloma bone disease and reduces tumor burden in bone in vivo. Blood 111: 2833-2842.
72. Erdal E, Ozturk N, Cagatay T, Eksioglu-Demiralp E, Ozturk M, (2005) Lithium-mediated downregulation of PKB/Akt and cyclin E with growth inhibition in hepatocellular carcinoma cells. Int J Cancer 115: 903-910.
73. Gould TD, Gray NA, Manji HK, (2003) Effects of a glycogen synthase kinase-3 inhibitor, lithium, in adenomatous polyposis coli mutant mice. Pharmacol Res 48: 49-53.
74. He B, You L, Xu Z, Mazieres J, Lee AY, et al. (2004) Activity of the suppressor of cytokine signaling-3 promoter in human non-small-cell lung cancer. Clin Lung Cancer 5: 366-370.
75. He B, You L, Uematsu K, Matsangou M, Xu Z, et al. (2003) Cloning and characterization of a functional promoter of the human SOCS-3 gene. Biochem Biophys Res Commun 301: 386-391.
76. Angelucci F, Aloe L, Jimenez-Vasquez P, Mathe AA, (2003) Lithium treatment alters brain concentrations of nerve growth factor, brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor in a rat model of depression. Int J Neuropsychopharmacol 6: 225-231.
77. Frey BN, Andreazza AC, Rosa AR, Martins MR, Valvassori SS, et al. (2006) Lithium increases nerve growth factor levels in the rat hippocampus in an animal model of mania. Behav Pharmacol 17: 311-318.
78. Machado-Vieira R, Manji HK, Zarate CA Jr, (2009) The role of lithium in the treatment of bipolar disorder: convergent evidence for neurotrophic effects as a unifying hypothesis. Bipolar Disord 11 (Suppl 2): 92-109.
79. Walz JC, Frey BN, Andreazza AC, Cereser KM, Cacilhas AA, et al. (2008) Effects of lithium and valproate on serum and hippocampal neurotrophin-3 levels in an animal model of mania. J Psychiatr Res 42: 416-421.