Mood stabilizing drugs expand the neural stem cell pool in the adult brain through activation of Notch signaling

Stem Cells

Volumn 26, Issue 7, 2008, Pages 1758-1767

  Higashi, Mikito ^a,b   Maruta, Noriko ^c   Bernstein, Alan ^d   Ikenaka, Kazuhiro ^a,b   Hitoshi, Seiji ^a,b  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Carbamazepine; Lithium; Neural stem cell; Notch; Self renewal; Valproic acid

Indexed keywords

CARBAMAZEPINE; LITHIUM; NOTCH RECEPTOR; PRESENILIN 1; VALPROIC ACID;

ANIMAL CELL; ARTICLE; BIPOLAR DISORDER; CELL EXPANSION; CELL RENEWAL; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG EFFECT; GENE MUTATION; HUMAN; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; SIGNAL TRANSDUCTION;

AFFECT; ANIMALS; ANTIMANIC AGENTS; BRAIN; CELL CULTURE TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; NEURONS; OLFACTORY BULB; PRESENILIN-1; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 52049097861     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-1032     Document Type: Article

References (61)

1. Gage FH. Mammalian neural stem cells. Science 2000;287:1433-1438.
2. Alvarez-Buylla A, García-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci 2002;22:629-634.
3. Gheusi G, Cremer H, McLean H et al. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A 2000;97:1823-1828.
4. Carleton A, Petreanu LT, Lansford R et al. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 2003;6:507-518.
5. Shors TJ, Miesegaes G, Beylin A et al. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001;410:372-376.
6. Liu J, Solway K, Messing RO et al. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 1998;18:7768-7778.
7. Jin K, Minami M, Lan JQ et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 2001;98:4710-4715.
8. Arvidsson A, Collin T, Kirik D et al. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002;8:963-970.
9. Nakatomi H, Kuriu T, Okabe S et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002;110:429-441.
10. Yamashita T, Ninomiya M, Acosta PH et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 2006;26:6627-6636.
11. Ming G, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005;28:223-250.
12. Morshead CM, Craig CG, van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 1998;125:2251-2261.
13. Hitoshi S, Alexson T, Tropepe V et al. Notch pathway molecules are essential for the maintenance but not the generation of mammalian neural stem cells. Genes Dev 2002;16:846-858.
14. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
15. Doetsch F, Petreanu L, Caille I et al. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 2002;36:1021-1034.
16. Berridge MJ, Downes CP, Hanley MR. Neural and developmental actions of lithium: a unifying hypothesis. Cell 1989;59:411-419.
17. O'Donnell T, Rotzinger S, Nakashima TT et al. Chronic lithium and sodium valproate both decrease the concentration of myo-inositol and increase the concentration of inositol monophosphates in rat brain. Brain Res 2000;880:84-91.
18. Williams RSB, Cheng L, Mudge AW et al. A common mechanism of action for three mood-stabilizing drugs. Nature 2002;417:292-295.
19. Brandish PE, Su M, Holder DJ et al. Regulation of gene expression by lithium and depletion of inositol in slices of adult rat cortex. Neuron 2005;45:861-872.
20. Chen G, Huang LD, Jiang YM et al. The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3. J Neurochem 1999;72:1327-1330.
21. De Sarno P, Li X, Jope RS. Regulation of Akt and glycogen synthase kinase-3β phosphorylation by sodium valproate and lithium. Neuropharmacology 2002;43:1158-1164.
22. Gould TD, Chen G, Manji HK. In vivo evidence in the brain for lithium inhibition of glycogen synthase kinase-3. Molecular targets of lithium action. Neuropsychopharmacology 2004;29:32-38.
23. Wexler EM, Geschwind DH, Palmer TD. Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol Psychiat 2008;13:285-292.
24. Kopnisky KL, Chalecka-Franaszek E, Gonzalez-Zulueta M et al. Chronic lithium treatment antagonizes glutamate-induced decrease of phosphorylated CREB in neurons via reducing protein phosphatase 1 and increasing MEK activities. Neuroscience 2003;116:425-435.
25. Hao Y, Creson T, Zhang L et al. Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J Neurosci 2004;21:6590-6599.
26. Phiel CJ, Zhang F, Huang EY et al. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and tetragen. J Biol Chem 2001;276:36734-36741.
27. Coyle JT, Duman RS. Finding the intracellular signaling pathways affected by mood disorder treatments. Neuron 2003;38:157-160.
28. Chen G, Rajkowska G, Du F et al. Enhancement of hippocampal neurogenesis by lithium. J Neurochem 2000;75:1729-1734.
29. Kim JS, Chang MY, Yu IT et al. Lithium selectively increases neuronal differentiation of hippocampal neural progenitor cells both in vitro and in vivo. J Neurochem 2004;89:324-336.
30. Hashimoto R, Senatorov V, Kanai H et al. Lithium stimulates progenitor proliferation in cultured brain neurons. Neuroscience 2003;117:55-61.
31. Laeng P, Pitts RL, Lemire AL et al. The mood stabilizer valproic acid stimulates GABA neurogenesis from rat forebrain stem cells. J Neurochem 2004;91:238-251.
32. American Psychiatric Association. Practice guideline for the treatment of patients with bipolar disorder (Revision). Am. J. Psychiatry 2002;159(4 Suppl.):1-50.
33. Donoviel DB, Hadjantonakis AK, Ikeda M et al. Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev 1999;13:2801-2810.
34. Hitoshi S, Seaberg RM, Koscik C et al. Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev 2004;18:1806-1811.
35. Tropepe V, Sibilia M, Ciruna BG et al. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 1999;208:166-188.
36. Kippin TE, Cain SW, Masum Z et al. Neural stem cells show bidirectional experience-dependent plasticity in the perinatal mammalian brain. J Neurosci 2004;24:2832-2836.
37. Takahashi Y, Jeong S-Y, Ogata K et al. Human skeletal muscle calcium channel a1S is expressed in the basal ganglia: distinctive expression pattern among L-type Ca2+ channels. Neurosci Res 2003;45:129-137.
38. Nishimura M, Isaka F, Ishibashi M et al. Structure, chromosomal locus, and promoter of mouse Hes2 gene, a homologue of Drosophila hairy and Enhancer of split. Genomics 1998;49:69-75.
39. Ito T, Udaka N, Yazawa T et al. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 2000;127:3913-3921.
40. Keller II PC, Tomita T, Hayashi I et al. A faster migrating variant masquerades as NICD when performing in vitro γ-secretase assays with bacterially expressed Notch substrates. Biochemistry 2006;45:5351-5358.
41. Nye J, Kopan R, Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 1994;120:2421-2430.
42. Yamamoto N, Yamamoto S, Inagaki F et al. Role of Deltex-1 as a transcriptional regulator downstream pf the Notch receptor. J Biol Chem 2001;276:45031-45040.
43. Kagawa T, Ikenaka K, Inoue Y et al. Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron 1994;13:427-442.
44. Morshead CM, Garcia D, Sofroniew MV et al. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci 2003;18:76-84.
45. Enwere E, Shingo T, Gregg C et al. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 2004;24:8354-8365.
46. Morshead CM, Reynolds BA, Craig CG et al. Neural stem cells in the adult mammalian forebrain, a relatively quiescent subpopulation of subependymal cells. Neuron 1994;13:1071-1082.
47. Nakamura Y, Sakakibara S-i, Miyata T et al. The bHLH gene Hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 2000;20:283-293.
48. Chojnacki A, Shimazaki T, Gregg C et al. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci 2003;23:1730-1741.
49. Selkoe DJ. Notch and presenilins in vertebrates and invertebrates, implications for neuronal development and degeneration. Curr Opin Neurobiol 2000;10:50-57.
50. Singec I, Knoth R, Meyer RP et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Method 2006;3:801-806.
51. Yoon K, Gaiano N. Notch signaling in the mammalian central nervous system, insights from mouse mutants. Nat Neurosci 2005;8:709-715.
52. Stockhausen MT, Sjölund J, Manetopoulos C et al. Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br J Cancer 2005;92:751-759.
53. Zhou R, Gray N, Yuan P et al. The anti-apoptotic, glucocorticoid receptor cochaperone protein BAG-1 is a long-term target for the actions of mood stabilizers. J Neurosci 2005;25:4493-4502.
54. Chen S, Guttridge DC, You Z et al. Wnt-1 signaling inhibits apoptosis by activating β-catenin/T cell factor-mediated transcription. J Cell Biol 2001;152:87-96.
55. Hirabayashi Y, Itoh Y, Tabata H et al. The Wnt/β-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004;131:2791-2801.
56. Jacobs BL. Adult brain neurogenesis and depression. Brain Behav. Immun 2003;16:602-609.
57. Hitoshi S, Maruta N, Higashi M et al. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 2007;85:3574-3585.
58. Santarelli L, Saxe M, Gross C et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003;301:805-809.
59. Yen MH, Reed DJ. Regulation of lithium in cerebrospinal fluid of the cat by the choroid plexus isolated in situ. Arch Int Pharmacodyn Ther 1981;251:217-227.
60. Wiesser HG. Comparison of valproate concentrations in human plasma, Csf And Brain Tissue After Administration Of Different Formulations of Valproate Or Valpromide Epilepsy Res 1991;9:154-159.
61. Johannessen SI, Strandjord RE. Concentration of carbamazepine (Tegretol). in serum and in cerebrospinal fluid in patients with epilepsy. Epilepsia 1973;14:373-379.