Disrupted in Schizophrenia 1 Regulates Neuronal Progenitor Proliferation via Modulation of GSK3β/β-Catenin Signaling

Cell

Volumn 136, Issue 6, 2009, Pages 1017-1031

  Mao, Yingwei ^a,b   Ge, Xuecai ^a,b,c   Frank, Christopher L ^a,b   Madison, Jon M ^b   Koehler, Angela N ^d   Doud, Mary Kathryn ^d   Tassa, Carlos ^d   Berry, Erin M ^b,d   Soda, Takahiro ^a,b,c   Singh, Karun K ^a,b   Biechele, Travis ^a,e   Petryshen, Tracey L ^b,d   Moon, Randall T ^a,e   Haggarty, Stephen J ^b,d   Tsai, Li Huei ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Center for Human Genetic Research   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

HUMDISEASE; MOLNEURO

Indexed keywords

BETA CATENIN; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIPOLAR DISORDER; BRAIN DEVELOPMENT; C57BL 6 MOUSE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; MAJOR DEPRESSION; MALE; MENTAL DISEASE; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SCHIZOPHRENIA; SIGNAL TRANSDUCTION;

EID: 62149083806     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.12.044     Document Type: Article

References (46)

1. Aberle H., Bauer A., Stappert J., Kispert A., and Kemler R. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16 (1997) 3797-3804
2. Adachi K., Mirzadeh Z., Sakaguchi M., Yamashita T., Nikolcheva T., Gotoh Y., Peltz G., Gong L., Kawase T., Alvarez-Buylla A., et al. Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25 (2007) 2827-2836
3. Beaulieu J.M., Sotnikova T.D., Yao W.D., Kockeritz L., Woodgett J.R., Gainetdinov R.R., and Caron M.G. Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl. Acad. Sci. USA 101 (2004) 5099-5104
4. Beaulieu J.M., Sotnikova T.D., Marion S., Lefkowitz R.J., Gainetdinov R.R., and Caron M.G. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122 (2005) 261-273
5. Beaulieu J.M., Marion S., Rodriguiz R.M., Medvedev I.O., Sotnikova T.D., Ghisi V., Wetsel W.C., Lefkowitz R.J., Gainetdinov R.R., and Caron M.G. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 132 (2008) 125-136
6. Blackwood D.H., Fordyce A., Walker M.T., St Clair D.M., Porteous D.J., and Muir W.J. Schizophrenia and affective disorders-cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am. J. Hum. Genet. 69 (2001) 428-433
7. Chenn A., and Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297 (2002) 365-369
8. Chubb J.E., Bradshaw N.J., Soares D.C., Porteous D.J., and Millar J.K. The DISC locus in psychiatric illness. Mol. Psychiatry 13 (2008) 36-64
9. Clapcote S.J., Lipina T.V., Millar J.K., Mackie S., Christie S., Ogawa F., Lerch J.P., Trimble K., Uchiyama M., Sakuraba Y., et al. Behavioral phenotypes of Disc1 missense mutations in mice. Neuron 54 (2007) 387-402
10. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., and Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378 (1995) 785-789
11. Duan X., Chang J.H., Ge S., Faulkner R.L., Kim J.Y., Kitabatake Y., Liu X.B., Yang C.H., Jordan J.D., Ma D.K., et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130 (2007) 1146-1158
12. Farioli-Vecchioli S., Saraulli D., Costanzi M., Pacioni S., Cina I., Aceti M., Micheli L., Bacci A., Cestari V., and Tirone F. The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol. 6 (2008) e246
13. Flagstad P., Mork A., Glenthoj B.Y., van Beek J., Michael-Titus A.T., and Didriksen M. Disruption of neurogenesis on gestational day 17 in the rat causes behavioral changes relevant to positive and negative schizophrenia symptoms and alters amphetamine-induced dopamine release in nucleus accumbens. Neuropsychopharmacology 29 (2004) 2052-2064
14. Gould T.D., Einat H., O'Donnell K.C., Picchini A.M., Schloesser R.J., and Manji H.K. Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 32 (2007) 2173-2183
15. Gould T.D., O'Donnell K.C., Picchini A.M., Dow E.R., Chen G., and Manji H.K. Generation and behavioral characterization of beta-catenin forebrain-specific conditional knock-out mice. Behav. Brain Res. 189 (2008) 117-125
16. Gregorieff A., and Clevers H. Wnt signaling in the intestinal epithelium: from endoderm to cancer. Genes Dev. 19 (2005) 877-890
17. Harwood A.J. Lithium and bipolar mood disorder: the inositol-depletion hypothesis revisited. Mol. Psychiatry 10 (2005) 117-126
18. Hikida T., Jaaro-Peled H., Seshadri S., Oishi K., Hookway C., Kong S., Wu D., Xue R., Andrade M., Tankou S., et al. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc. Natl. Acad. Sci. USA 104 (2007) 14501-14506
19. Hirabayashi Y., Itoh Y., Tabata H., Nakajima K., Akiyama T., Masuyama N., and Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131 (2004) 2791-2801
20. International Schizophrenia Consortium. Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 455 (2008) 237-241
21. Kee N., Teixeira C.M., Wang A.H., and Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10 (2007) 355-362
22. Kvajo M., McKellar H., Arguello P.A., Drew L.J., Moore H., MacDermott A.B., Karayiorgou M., and Gogos J.A. A mutation in mouse Disc1 that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition. Proc. Natl. Acad. Sci. USA 105 (2008) 7076-7081
23. Leung J.Y., Kolligs F.T., Wu R., Zhai Y., Kuick R., Hanash S., Cho K.R., and Fearon E.R. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J. Biol. Chem. 277 (2002) 21657-21665
24. Li W., Zhou Y., Jentsch J.D., Brown R.A., Tian X., Ehninger D., Hennah W., Peltonen L., Lonnqvist J., Huttunen M.O., et al. Specific developmental disruption of disrupted-in-schizophrenia-1 function results in schizophrenia-related phenotypes in mice. Proc. Natl. Acad. Sci. USA 104 (2007) 18280-18285
25. Lie D.C., Colamarino S.A., Song H.J., Desire L., Mira H., Consiglio A., Lein E.S., Jessberger S., Lansford H., Dearie A.R., and Gage F.H. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437 (2005) 1370-1375
26. Lochhead P.A., Kinstrie R., Sibbet G., Rawjee T., Morrice N., and Cleghon V. A chaperone-dependent GSK3beta transitional intermediate mediates activation-loop autophosphorylation. Mol. Cell 24 (2006) 627-633
27. Ma L., Liu Y., Ky B., Shughrue P.J., Austin C.P., and Morris J.A. Cloning and characterization of Disc1, the mouse ortholog of DISC1 (Disrupted-in-Schizophrenia 1). Genomics 80 (2002) 662-672
28. Ma Y.C., Song M.R., Park J.P., Henry Ho H.Y., Hu L., Kurtev M.V., Zieg J., Ma Q., Pfaff S.L., and Greenberg M.E. Regulation of motor neuron specification by phosphorylation of neurogenin 2. Neuron 58 (2008) 65-77
29. Murdoch H., Mackie S., Collins D.M., Hill E.V., Bolger G.B., Klussmann E., Porteous D.J., Millar J.K., and Houslay M.D. Isoform-selective susceptibility of DISC1/phosphodiesterase-4 complexes to dissociation by elevated intracellular cAMP levels. J. Neurosci. 27 (2007) 9513-9524
30. Newton S.S., and Duman R.S. Neurogenic actions of atypical antipsychotic drugs and therapeutic implications. CNS Drugs 21 (2007) 715-725
31. Peters H.C., Hu H., Pongs O., Storm J.F., and Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat. Neurosci. 8 (2005) 51-60
32. Pletnikov M.V., Ayhan Y., Nikolskaia O., Xu Y., Ovanesov M.V., Huang H., Mori S., Moran T.H., and Ross C.A. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Molecular Psychiatry 13 (2008) 173-186
33. Plotkin B., Kaidanovich O., Talior I., and Eldar-Finkelman H. Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 305 (2003) 974-980
34. Reif A., Fritzen S., Finger M., Strobel A., Lauer M., Schmitt A., and Lesch K.P. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol. Psychiatry 11 (2006) 514-522
35. Ross C.A., Margolis R.L., Reading S.A., Pletnikov M., and Coyle J.T. Neurobiology of schizophrenia. Neuron 52 (2006) 139-153
36. Ross S.E., Erickson R.L., Hemati N., and MacDougald O.A. Glycogen synthase kinase 3 is an insulin-regulated C/EBPalpha kinase. Mol. Cell. Biol. 19 (1999) 8433-8441
37. Sanada K., and Tsai L.H. G protein betagamma subunits and AGS3 control spindle orientation and asymmetric cell fate of cerebral cortical progenitors. Cell 122 (2005) 119-131
38. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
39. Schuller U., and Rowitch D.H. Beta-catenin function is required for cerebellar morphogenesis. Brain Res. 1140 (2007) 161-169
40. Selenica M.L., Jensen H.S., Larsen A.K., Pedersen M.L., Helboe L., Leist M., and Lotharius J. Efficacy of small-molecule glycogen synthase kinase-3 inhibitors in the postnatal rat model of tau hyperphosphorylation. Br. J. Pharmacol. 152 (2007) 959-979
41. Stefansson H., Rujescu D., Cichon S., Pietilainen O.P., Ingason A., Steinberg S., Fossdal R., Sigurdsson E., Sigmundsson T., Buizer-Voskamp J.E., et al. Large recurrent microdeletions associated with schizophrenia. Nature 455 (2008) 232-236
42. Tetsu O., and McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (1999) 422-426
43. Thomas G.M., Frame S., Goedert M., Nathke I., Polakis P., and Cohen P. A GSK3-binding peptide from FRAT1 selectively inhibits the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett. 458 (1999) 247-251
44. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., and Moon R.T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13 (2003) 680-685
45. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., Nord A.S., Kusenda M., Malhotra D., Bhandari A., et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 320 (2008) 539-543
46. Zechner D., Fujita Y., Hulsken J., Muller T., Walther I., Taketo M.M., Crenshaw III E.B., Birchmeier W., and Birchmeier C. beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258 (2003) 406-418