Fluoxetine regulates neurogenesis in vitro through modulation of gsk-3b/b-catenin signaling

International Journal of Neuropsychopharmacology

Volumn 18, Issue 5, 2015, Pages 1-12

  Hui, Jiaojie ^a   Zhang, Jianping ^a   Kim, Hoon ^b   Tong, Chang ^c   Ying, Qilong ^a   Li, Zaiwang ^a   Mao, Xuqiang ^a   Shi, Guofeng ^a   Yan, Jie ^b   Zhang, Zhijun ^a   Xi, Guangjun ^a  

^a WUXI PEOPLE S HOSPITAL AFFILIATED TO NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c AFFILIATED ZHONGDA HOSPITAL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

B Catenin; Cell Proliferation; Fluoxetine; Glycogen Synthase Kinase 3 Beta; Neural Precursor Cells

Indexed keywords

BETA CATENIN; FLUOXETINE; GLYCOGEN SYNTHASE KINASE 3BETA; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SEROTONIN 1A RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; SEROTONIN UPTAKE INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME PHOSPHORYLATION; IN VITRO STUDY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; FEMALE; HIPPOCAMPUS; MALE; METABOLISM; NEURAL STEM CELL; PHOSPHORYLATION; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; FEMALE; FLUOXETINE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; IN VITRO TECHNIQUES; MALE; NEURAL STEM CELLS; NEUROGENESIS; PHOSPHORYLATION; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN UPTAKE INHIBITORS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84931261332     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu099     Document Type: Article

References (70)

1. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, Gotoh Y, Peltz G, Gong L, Kawase T, Alvarez-Buylla A, Okano H, Sawamoto K (2007) Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25:2827-2836
2. Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S, Price J, Pariante CM (2011) Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry 16:738-750
3. Basar K, Eren-Kocak E, Ozdemir H, Ertugrul A (2013) Effects of acute and chronic electroconvulsive shocks on glycogen syn-thase kinase 3beta level and phosphorylation in mice. J ECT 29:265-270
4. Beaulieu JM, Zhang X, Rodriguiz RM, Sotnikova TD, Cools MJ, Wetsel WC, Gainetdinov RR, Caron MG (2008) Role of GSK3 beta in behavioral abnormalities induced by serotonin deficiency. Proc Natl Acad Sci USA 105:1333-1338
5. Benninghoff J, Gritti A, Rizzi M, Lamorte G, Schloesser RJ, Schmitt A, Robel S, Genius J, Moessner R, Riederer P, Manji HK, Grunze H, Rujescu D, Moeller HJ, Lesch KP, Vescovi AL (2010) Serotonin depletion hampers survival and proliferation in neurospheres derived from adult neural stem cells. Neuropsychopharmacology 35:893-903
6. Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145:1142-1155
7. Cattaneo E, McKay R (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347:762-765
8. Chen YC, Tan QR, Dang W, Wang HN, Zhang RB, Li ZY, Lin H, Liu R (2012) The effect of citalopram on chronic stress-induced depressive-like behavior in rats through GSK3beta/betacatenin activation in the medial prefrontal cortex. Brain Res Bull 88:338-344
9. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369
10. Chiou SH, Chen SJ, Peng CH, Chang YL, Ku HH, Hsu WM, Ho LL, Lee CH (2006) Fluoxetine up-regulates expression of cellular FLICE-inhibitory protein and inhibits LPS-induced apoptosis in hippocampus-derived neural stem cell. Biochem Biophys Res Commun 343:391-400
11. Ciani L, Salinas PC (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6:351-362
12. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469-480
13. Dranovsky A, Hen R (2006) Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 59:1136-1143
14. Dromard C, Bartolami S, Deleyrolle L, Takebayashi H, Ripoll C, Simonneau L, Prome S, Puech S, Tran VB, Duperray C, Valmier J, Privat A, Hugnot JP (2007) NG2 and Olig2 expression provides evidence for phenotypic deregulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells 25:340-353
15. Duman RS, Aghajanian GK (2014) Neurobiology of rapid acting antidepressants: role of BDNF and GSK-3beta. Neuropsychopharmacology 39:233-233
16. Duman RS, Nakagawa S, Malberg J (2001) Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 25:836-844
17. Eom TY, Jope RS (2009) Blocked inhibitory serine-phosphorylation of glycogen synthase kinase-3alpha/beta impairs in vivo neural precursor cell proliferation. Biol Psychiatry 66:494-502
18. Eom TY, Roth KA, Jope RS (2007) Neural precursor cells are protected from apoptosis induced by trophic factor withdrawal or genotoxic stress by inhibitors of glycogen synthase kinase 3. J Biol Chem 282:22856-22864
19. Fukumoto S, Hsieh CM, Maemura K, Layne MD, Yet SF, Lee KH, Matsui T, Rosenzweig A, Taylor WG, Rubin JS, Perrella MA, Lee ME (2001) Akt participation in the Wnt signaling pathway through Dishevelled. J Biol Chem 276:17479-17483
20. Garza JC, Guo M, Zhang W, Lu XY (2012) Leptin restores adult hippocampal neurogenesis in a chronic unpredictable stress model of depression and reverses glucocorticoid-induced inhibition of GSK-3beta/beta-catenin signaling. Mol Psychiatry 17:790-808
21. Gensburger C, Labourdette G, Sensenbrenner M (1987) Brain basic fibroblast growth factor stimulates the proliferation of rat neuronal precursor cells in vitro. FEBS Lett 217:1-5
22. Gould TD, Einat H, Bhat R, Manji HK (2004) AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int J Neuropsychop 7:387-390
23. Gould TD, Einat H, O DK, Picchini AM, Schloesser RJ, Manji HK (2007) Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 32:2173-2183
24. Hedgepeth CM, Conrad LJ, Zhang J, Huang HC, Lee VM, Klein PS (1997) Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev Biol 185:82-91
25. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y (2004) The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791-2801
26. Huang GJ, Herbert J (2005) The role of 5-HT1A receptors in the proliferation and survival of progenitor cells in the dentate gyrus of the adult hippocampus and their regulation by corticoids. Neuroscience 135:803-813
27. Hughes K, Nikolakaki E, Plyte SE, Totty NF, Woodgett JR (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J 12:803-808
28. Inkster B, Nichols TE, Saemann PG, Auer DP, Holsboer F, Muglia P, Matthews PM (2009) Association of GSK3beta polymorphisms with brain structural changes in major depressive disorder. Arch Gen Psychiatry 66:721-728
29. Kaidanovich-Beilin O, Milman A, Weizman A, Pick CG, Eldar-Finkelman H (2004) Rapid antidepressive-like activity of specific glycogen synthase kinase-3 inhibitor and its effect on betacatenin in mouse hippocampus. Biol Psychiatry 55:781-784
30. Karege F, Perroud N, Burkhardt S, Fernandez R, Ballmann E, La Harpe R, Malafosse A (2012) Protein levels of beta-catenin and activation state of glycogen synthase kinase-3beta in major depression. A study with postmortem prefrontal cortex. J Affect Disord 136:185-188
31. Karson CN, Newton JE, Livingston R, Jolly JB, Cooper TB, Sprigg J, Komoroski RA (1993) Human brain fluoxetine concentrations. J Neuropsychiatry Clin Neurosci 5:322-329
32. Kim H, Wu J, Ye S, Tai CI, Zhou X, Yan H, Li P, Pera M, Ying QL (2013) Modulation of beta-catenin function maintains mouse epiblast stem cell and human embryonic stem cell selfrenewal. Nat Commun 4:2403
33. Kodama M, Fujioka T, Duman RS (2004) Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56:570-580
34. Komoroski RA, Newton JE, Cardwell D, Sprigg J, Pearce J, Karson CN (1994) In vivo 19F spin relaxation and localized spectroscopy of fluoxetine in human brain. Magn Reson Med 31:204-211
35. Li X, Zhu W, Roh MS, Friedman AB, Rosborough K, Jope RS (2004) In vivo regulation of glycogen synthase kinase-3beta (GSK- 3beta) by serotonergic activity in mouse brain. Neuropsychopharmacology 29:1426-1431
36. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signaling regulates adult hippocampal neurogenesis. Nature 437:1370-1375
37. Liu R, Dang W, Jianting M, Su C, Wang H, Chen Y, Tan Q (2012) Citalopram alleviates chronic stress induced depression-like behaviors in rats by activating GSK3beta signaling in dorsal hippocampus. Brain Res 1467:10-17
38. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810
39. Maguschak KA, Ressler KJ (2011) Wnt signaling in amygdaladependent learning and memory. J Neurosci 31:13057-13067
40. Maguschak KA, Ressler KJ (2012) The dynamic role of betacatenin in synaptic plasticity. Neuropharmacology 62:78-88
41. Malberg JE (2004) Implications of adult hippocampal neurogenesis in antidepressant action. J Psychiatry Neurosci 29:196-205
42. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110
43. Mao Y, Ge X, Frank CL, Madison JM, Koehler AN, Doud MK, Tassa C, Berry EM, Soda T, Singh KK, Biechele T, Petryshen TL, Moon RT, Haggarty SJ, Tsai LH (2009) Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136:1017-1031
44. Mercado-Gomez O, Hernandez-Fonseca K, Villavicencio-Queijeiro A, Massieu L, Chimal-Monroy J, Arias C (2008) Inhibition of Wnt and PI3K signaling modulates GSK-3beta activity and induces morphological changes in cortical neurons: role of tau phosphorylation. Neurochem Res 33:1599-1609
45. Morales-Garcia JA, Luna-Medina R, Alonso-Gil S, Sanz-Sancristobal M, Palomo V, Gil C, Santos A, Martinez A, Perez-Castillo A (2012) Glycogen synthase kinase 3 inhibition promotes adult hippocampal neurogenesis in vitro and in vivo. ACS Chem Neurosci 3:963-971
46. Morshead CM, Craig CG, van KD (1998) In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125:2251-2261
47. Murphy M, Drago J, Bartlett PF (1990) Fibroblast growth factor stimulates the proliferation and differentiation of neural precursor cells in vitro. J Neurosci Res 25:463-475
48. Novak A, Dedhar S (1999) Signaling through beta-catenin and Lef/Tcf. Cell Mol Life Sci 56:523-537
49. Ohira K, Takeuchi R, Shoji H, Miyakawa T (2013) Fluoxetineinduced cortical adult neurogenesis. Neuropsychopharmacology 38:909-920
50. Okamoto H, Voleti B, Banasr M, Sarhan M, Duric V, Girgenti MJ, Dileone RJ, Newton SS, Duman RS (2010) Wnt2 expression and signaling is increased by different classes of antidepressant treatments. Biol Psychiatry 68:521-527
51. Peng CH, Chiou SH, Chen SJ, Chou YC, Ku HH, Cheng CK, Yen CJ, Tsai TH, Chang YL, Kao CL (2008) Neuroprotection by Imipramine against lipopolysaccharide-induced apoptosis in hippocampus- derived neural stem cells mediated by activation of BDNF and the MAPK pathway. Eur Neuropsychopharmacol 18:128-140
52. Polter AM, Yang S, Jope RS, Li X (2012) Functional significance of glycogen synthase kinase-3 regulation by serotonin. Cell Signal 24:265-271
53. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710
54. Sairanen M, Lucas G, Ernfors P, Castren M, Castren E (2005) Brainderived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci 25:1089-1094
55. Sairanen M, O LO, Knuuttila JE, Castren E (2007) Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144:368-374
56. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809
57. Seitz R, Hackl S, Seibuchner T, Tamm ER, Ohlmann A (2010) Norrin mediates neuroprotective effects on retinal ganglion cells via activation of the Wnt/beta-catenin signaling pathway and the induction of neuroprotective growth factors in Muller cells. J Neurosci 30:5998-6010
58. Strauss WL, Unis AS, Cowan C, Dawson G, Dager SR (2002) Fluorine magnetic resonance spectroscopy measurement of brain fluvoxamine and fluoxetine in pediatric patients treated for pervasive developmental disorders. Am J Psych 159:755-760
59. Taliaz D, Stall N, Dar DE, Zangen A (2010) Knockdown of brainderived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15:80-92
60. Tang M, Villaescusa JC, Luo SX, Guitarte C, Lei S, Miyamoto Y, Taketo MM, Arenas E, Huang EJ (2010) Interactions of Wnt/ beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci 30:9280-9291
61. Thibaut R, Porte C (2008) Effects of fibrates, anti-inflammatory drugs and antidepressants in the fish hepatoma cell line PLHC-1: cytotoxicity and interactions with cytochrome P450 1A. Toxicol In Vitro 22:1128-1135
62. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034
63. Wang QM, Fiol CJ, DePaoli-Roach AA, Roach PJ (1994) Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J Biol Chem 269:14566-14574
64. Wang YX, Zhang XR, Zhang ZJ, Li L, Xi GJ, Wu D, Wang YJ (2014) Protein kinase Mzeta is involved in the modulatory effect of fluoxetine on hippocampal neurogenesis in vitro. Int J Neuropsychop 17:1429-1441
65. Warner-Schmidt JL, Duman RS (2007) VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc Natl Acad Sci USA 104:4647-4652
66. Wexler EM, Geschwind DH, Palmer TD (2008) Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol Psychiatry 13:285-292
67. Xi G, Zhang X, Zhang L, Sui Y, Hui J, Liu S, Wang Y, Li L, Zhang Z (2011) Fluoxetine attenuates the inhibitory effect of glucocorticoid hormones on neurogenesis in vitro via a two-pore domain potassium channel, TREK-1. Psychopharmacology (Berl) 214:747-759
68. Xi G, Hu P, Qu C, Qiu S, Tong C, Ying QL (2013) Induced neural stem cells generated from rat fibroblasts. Genomics Proteomics Bioinformatics 11:312-319
69. Zhang X, Gaspard JP, Chung DC (2001) Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res 61:6050-6054
70. Zusso M, Debetto P, Guidolin D, Barbierato M, Manev H, Giusti P (2008) Fluoxetine-induced proliferation and differentiation of neural progenitor cells isolated from rat postnatal cerebellum. Biochem Pharmacol 76:391-403