Increased cellular turnover in response to fluoxetine in neuronal precursors derived from human embryonic stem cells

International Journal of Developmental Biology

Volumn 54, Issue 4, 2010, Pages 707-715

  Chang, Eun Ah ^a   Beyhan, Zeki ^a   Yoo, Myung Sik ^a   Siripattarapravat, Kannika ^a   Ko, Tak ^a   Lookingland, Keith J ^b   Madhukar, Burra V ^b   Cibelli, Jose B ^a,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Programa Andaluz de Terapia Celular y Medicina Regenerativa   (Spain)

Author keywords

Cellular turnover; Fluoxetine; Human embryonic stem cell; Neuronal precursor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FLUOXETINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR; SEROTONIN;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG MECHANISM; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS;

ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; APOPTOSIS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DEPRESSIVE DISORDER; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FLUOXETINE; HUMANS; NERVE GROWTH FACTORS; NEURONAL PLASTICITY; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77950538530     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.092851ec     Document Type: Article

References (54)

1. BARTHOLOMA, P., ERLANDSSON, N., KAUFMANN, K., ROSSLER, O.G., BAUMANN, B., WIRTH, T., GIEHL, K.M. and THIEL, G. (2002). Neuronal cell death induced by antidepressants: lack of correlation with Egr-1, NF-kappa B and extracellular signal-regulated protein kinase activation. Biochem Pharmacol 63: 1507-1516.
2. BENNINGHOFF, J., SCHMITT, A., MOSSNER, R. and LESCH, K.P. (2002). When cells become depressed: focus on neural stem cells in novel treatment strategies against depression. J Neural Transm 109: 947-962.
3. BLENDY, J.A. (2006). The role of CREB in depression and antidepressant treatment. Biol Psychiatry 59: 1144-1150.
4. CASTREN, E. (2005). Is mood chemistry? Nat Rev Neurosci 6: 241-246.
5. CASTREN, E., VOIKAR, V. and RANTAMAKI, T. (2007). Role of neurotrophic factors in depression. Curr Opin Pharmacol 7: 18-21.
6. CHEN, B., DOWLATSHAHI, D., MACQUEEN, G.M., WANG, J.F. and YOUNG, L.T. (2001). Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 50: 260-265.
7. CHEN, H., PANDEY, G.N. and DWIVEDI, Y. (2006). Hippocampal cell proliferation regulation by repeated stress and antidepressants. Neuroreport 17: 863-867.
8. CHEN, S.J., KAO, C.L., CHANG, Y.L., YEN, C.J., SHUI, J.W., CHIEN, C.S., CHEN, I.L., TSAI, T.H., KU, H.H. and CHIOU, S.H. (2007). Antidepressant administration modulates neural stem cell survival and serotoninergic differentiation through bcl-2. Curr Neurovasc Res 4: 19-29.
9. CHIOU, S.H., CHEN, S.J., PENG, C.H., CHANG, Y.L., KU, H.H., HSU, W.M., HO, L.L. and LEE, C.H. (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.
10. DE FOUBERT, G., CARNEY, S.L., ROBINSON, C.S., DESTEXHE, E.J., TOMLINSON, R., HICKS, C.A., MURRAY, T.K., GAILLARD, J.P., DEVILLE, C., XHENSEVAL, V. et al. (2004). Fluoxetine-induced change in rat brain expression of brain-derived neurotrophic factor varies depending on length of treatment. Neuroscience 128: 597-604.
11. DHARA, S.K., HASNEEN, K., MACHACEK, D.W., BOYD, N.L., RAO, R.R. and STICE, S.L. (2008). Human neural progenitor cells derived from embryonic stem cells in feeder-free cultures. Differentiation.
12. DI LIETO, A., LEO, D., VOLPICELLI, F., DI PORZIO, U. and COLUCCI-D'AMATO, L. (2007). FLUOXETINE modifies the expression of serotonergic markers in a differentiation-dependent fashion in the mesencephalic neural cell line A1 mes c-myc. Brain Res 1143: 1-10.
13. DIAS, B.G., BANERJEE, S.B., DUMAN, R.S. and VAIDYA, V.A. (2003). Differential regulation of brain derived neurotrophic factor transcripts by antidepressant treatments in the adult rat brain. Neuropharmacology 45: 553-563.
14. ENCINAS, J.M., VAAHTOKARI, A. and ENIKOLOPOV, G. (2006). Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 103: 8233-8238.
15. GENSCHOW, E., SPIELMANN, H., SCHOLZ, G., SEILER, A., BROWN, N., PIERSMA, A., BRADY, M., CLEMANN, N., HUUSKONEN, H., PAILLARD, F. et al. (2002). The ECVAM international validation study on in vitro embryotoxicity tests: results of the definitive phase and evaluation of prediction models. European Centre for the Validation of Alternative Methods. Altern Lab Anim 30: 151-176.
16. GOTTLIEB, D.I. (2002). Large-scale sources of neural stem cells. Annu Rev Neurosci 25: 381-407.
17. GROTE, H.E., BULL, N.D., HOWARD, M.L., VAN DELLEN, A., BLAKEMORE, C., BARTLETT, P.F. and HANNAN, A.J. (2005). Cognitive disorders and neurogenesis deficits in Huntington's disease mice are rescued by fluoxetine. Eur J Neurosci 22: 2081-2088.
18. HISAOKA, K., TAKEBAYASHI, M., NISHIDA, A., TSUCHIOKA, M., YAMAWAKI, S. and NAKATA, Y. (2005). [Mechanisms of antidepressants and serotonin (5-HT)-induced glial cell line-derived neurotrophic factor (GDNF) releases in rat C6 gliobrastoma cells]. Nihon Shinkei Seishin Yakurigaku Zasshi 25: 25-31.
19. HISAOKA, K., TAKEBAYASHI, M., TSUCHIOKA, M., MAEDA, N., NAKATA, Y. and YAMAWAKI, S. (2007). Antidepressants Increase Glial Cell Line-Derived Neurotrophic Factor Production through Monoamine-Independent Activation of Protein Tyrosine Kinase and Extracellular Signal-Regulated Kinase in Glial Cells. J Pharmacol Exp Ther 321: 148-157.
20. HUANG, G.J. and HERBERT, J. (2006). Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 59: 619-624.
21. JOSSELYN, S.A. and NGUYEN, P.V. (2005). CREB, synapses and memory disorders: past progress and future challenges. Curr Drug Targets CNS Neurol Disord 4: 481-497.
22. KISS, J.Z. and ROUGON, G. (1997). Cell biology of polysialic acid. Curr Opin Neurobiol 7: 640-646.
23. KOCH, J.M., KELL, S. and ALDENHOFF, J.B. (2003). Differential effects of fluoxetine and imipramine on the phosphorylation of the transcription factor CREB and cell-viability. J Psychiatr Res 37: 53-59.
24. KODAMA, M., FUJIOKA, T. and DUMAN, R.S. (2004). Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56: 570-580.
25. LEE, H.J., KIM, J.W., YIM, S.V., KIM, M.J., KIM, S.A., KIM, Y.J., KIM, C.J. and CHUNG, J.H. (2001). Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Mol Psychiatry 6: 610, 725-618.
26. LEVKOVITZ, Y., GIL-AD, I., ZELDICH, E., DAYAG, M. and WEIZMAN, A. (2005). Differential induction of apoptosis by antidepressants in glioma and neuroblastoma cell lines: evidence for p-c-Jun, cytochrome c, and caspase-3 involvement. J Mol Neurosci 27: 29-42.
27. LIN, T.M., TSAI, J.L., LIN, S.D., LAI, C.S. and CHANG, C.C. (2005). Accelerated growth and prolonged lifespan of adipose tissue-derived human mesenchymal stem cells in a medium using reduced calcium and antioxidants. Stem Cells Dev 14: 92-102.
28. MALBERG, J.E. (2004). Implications of adult hippocampal neurogenesis in antide-pressant action. J Psychiatry Neurosci 29: 196-205.
29. MALBERG, J.E. and BLENDY, J.A. (2005). Antidepressant action: to the nucleus and beyond. In Trends Pharmacol Sci, vol. 26 (ed., pp. 631-638.
30. MALBERG, J.E. and DUMAN, R.S. (2003). Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28: 1562-1571.
31. MALBERG, J.E., EISCH, A.J., NESTLER, E.J. and DUMAN, R.S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110.
32. MANEV, H., UZ, T., SMALHEISER, N.R. and MANEV, R. (2001). Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro. Eur J Pharmacol 411: 67-70.
33. MORRISON, J.L., RIGGS, K.W. and RURAK, D.W. (2005). Fluoxetine during pregnancy: impact on fetal development. Reprod Fertil Dev 17: 641-650.
34. NAHON, E., ISRAELSON, A., ABU-HAMAD, S. and VARDA, S.B. (2005). Fluoxetine (Prozac) interaction with the mitochondrial voltage-dependent anion channel and protection against apoptotic cell death. FEBS Lett 579: 5105-5110.
35. NAKAGAWA, S., KIM, J.E., LEE, R., CHEN, J., FUJIOKA, T., MALBERG, J., TSUJI, S. and DUMAN, R.S. (2002). Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 22: 9868-9876.
36. NESTLER, E.J., BARROT, M., DILEONE, R.J., EISCH, A.J., GOLD, S.J. and MONTEGGIA, L.M. (2002). Neurobiology of depression. Neuron 34: 13-25.
37. NIBUYA, M., MORINOBU, S. and DUMAN, R.S. (1995). Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15: 7539-7547.
38. NIBUYA, M., NESTLER, E.J. and DUMAN, R.S. (1996). Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16: 2365-2372.
39. ONGUR, D., DREVETS, W.C. and PRICE, J.L. (1998). Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 95: 13290-13295.
40. POUTON, C.W. and HAYNES, J.M. (2007). Embryonic stem cells as a source of models for drug discovery. Nat Rev Drug Discov 6: 605-616.
41. RAJKOWSKA, G., MIGUEL-HIDALGO, J.J., WEI, J., DILLEY, G., PITTMAN, S.D., MELTZER, H.Y., OVERHOLSER, J.C., ROTH, B.L. and STOCKMEIER, C.A. (1999). Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 45: 1085-1098.
42. SAIRANEN, M., LUCAS, G., ERNFORS, P., CASTREN, M. and CASTREN, E. (2005). Brain-derived 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.
43. SAMBROOK, J. and RUSSELL, D.W. (2001). Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
44. SANTARELLI, L., SAXE, M., GROSS, C., SURGET, A., BATTAGLIA, F., DULAWA, S., WEISSTAUB, N., LEE, J., DUMAN, R., ARANCIO, O. et al. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809.
45. SCHECHTER, L.E., RING, R.H., BEYER, C.E., HUGHES, Z.A., KHAWAJA, X., MALBERG, J.E. and ROSENZWEIG-LIPSON, S. (2005). Innovative approaches for the development of antidepressant drugs: current and future strategies. NeuroRx 2: 590-611.
46. SCHOLZ, G., POHL, I., GENSCHOW, E., KLEMM, M. and SPIELMANN, H. (1999). Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells Tissues Organs 165: 203-211.
47. SERAFEIM, A., HOLDER, M.J., GRAFTON, G., CHAMBA, A., DRAYSON, M.T., LUONG, Q.T., BUNCE, C.M., GREGORY, C.D., BARNES, N.M. and GORDON, J. (2003). Selective serotonin reuptake inhibitors directly signal for apoptosis in biopsy-like Burkitt lymphoma cells. Blood 101: 3212-3219.
48. THOMSON, J.A., ITSKOVITZ-ELDOR, J., SHAPIRO, S.S., WAKNITZ, M.A., SWIERGIEL, J.J., MARSHALL, V.S. and JONES, J.M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
49. VAREA, E., BLASCO-IBANEZ, J.M., GOMEZ-CLIMENT, M.A., CASTILLO-GOMEZ, E., CRESPO, C., MARTINEZ-GUIJARRO, F.J. and NACHER, J. (2006). Chronic Fluoxetine Treatment Increases the Expression of PSA-NCAM in the Medial Prefrontal Cortex. Neuropsychopharmacology.
50. WOBUS, A.M. and BOHELER, K.R. (2005). Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 85: 635-678.
51. WOBUS, A.M., KLEPPISCH, T., MALTSEV, V. and HESCHELER, J. (1994). Cardiomyocyte-like cells differentiated in vitro from embryonic carcinoma cells P19 are characterized by functional expression of adrenoceptors and Ca2+ channels. In vitro Cell Dev Biol Anim 30A: 425-434.
52. WOBUS, A.M., WALLUKAT, G. and HESCHELER, J. (1991). Pluripotent mouse embryonic stem cells are able to differentiate into cardiomyocytes expressing chronotropic responses to adrenergic and cholinergic agents and Ca2+ channel blockers. Differentiation 48: 173-182.
53. WONG, D.T., PERRY, K.W. and BYMASTER, F.P. (2005). Case history: the discovery of fluoxetine hydrochloride (Prozac). Nat Rev Drug Discov 4: 764-774.
54. ZHANG, S.C., WERNIG, M., DUNCAN, I.D., BRUSTLE, O. and THOMSON, J.A. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19: 1129-1133.