Altered WNT Signaling in Human Induced Pluripotent Stem Cell Neural Progenitor Cells Derived from Four Schizophrenia Patients

Biological Psychiatry

Volumn 78, Issue 6, 2015, Pages e29-e34

  Topol, Aaron ^a   Zhu, Shijia ^a   Tran, Ngoc ^a   Simone, Anthony ^b   Fang, Gang ^a   Brennand, Kristen J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BETA CATENIN; BETAIII TUBULIN; RNA; TUBULIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ADULT; ARTICLE; CASE REPORT; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; FOREBRAIN; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOSPITALIZATION; HUMAN; HUMAN CELL; MALE; MULTIDIMENSIONAL SCALING; NEURAL STEM CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RNA SEQUENCE; SCHIZOPHRENIA; TRANSCRIPTION INITIATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; YOUNG ADULT; CELL CULTURE; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PILOT STUDY;

ADULT; CELLS, CULTURED; COHORT STUDIES; FEMALE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; NEURAL STEM CELLS; PILOT PROJECTS; PROSENCEPHALON; SCHIZOPHRENIA; WNT SIGNALING PATHWAY; YOUNG ADULT;

EID: 84939572016     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.12.028     Document Type: Letter

References (46)

1. D.R. Weinberger Implications of normal brain development for the pathogenesis of schizophrenia Arch Gen Psychiatry 44 1987 660 669
2. O. Marin, J. Baker, L. Puelles, and J.L. Rubenstein Patterning of the basal telencephalon and hypothalamus is essential for guidance of cortical projections Development 129 2002 761 773
3. A. Guilmatre, C. Dubourg, A.L. Mosca, S. Legallic, A. Goldenberg, V. Drouin-Garraud, and et al. Recurrent rearrangements in synaptic and neurodevelopmental genes and shared biologic pathways in schizophrenia, autism, and mental retardation Arch Gen Psychiatry 66 2009 947 956
4. L.F. Jarskog, S. Miyamoto, and J.A. Lieberman Schizophrenia: New pathological insights and therapies Annu Rev Med 58 2007 49 61
5. F.H. Gage Molecular and cellular mechanisms contributing to the regulation, proliferation and differentiation of neural stem cells in the adult dentate gyrus Keio J Med 59 2010 79 83
6. C.Y. Pietersen, S.A. Mauney, S.S. Kim, E. Passeri, M.P. Lim, R.J. Rooney, and et al. Molecular profiles of parvalbumin-immunoreactive neurons in the superior temporal cortex in schizophrenia J Neurogenet 28 2014 70 85
7. D. Cotter, R. Kerwin, S. al-Sarraji, J.P. Brion, A. Chadwich, S. Lovestone, and et al. Abnormalities of Wnt signalling in schizophrenia - evidence for neurodevelopmental abnormality Neuroreport 9 1998 1379 1383
8. O. Durak, F.C. de Anda, K.K. Singh, M.P. Leussis, T.L. Petryshen, P. Sklar, and et al. Ankyrin-G regulates neurogenesis and Wnt signaling by altering the subcellular localization of beta-catenin [published online ahead of print May 13] Mol Psychiatry. 2014
9. K.K. Singh, X. Ge, Y. Mao, L. Drane, K. Meletis, B.A. Samuels, and et al. Dixdc1 is a critical regulator of DISC1 and embryonic cortical development Neuron 67 2010 33 48
10. L.P. Sutton, and W.J. Rushlow Regulation of Akt and Wnt signaling by the group II metabotropic glutamate receptor antagonist LY341495 and agonist LY379268 J Neurochem 117 2011 973 983
11. E.M. Hur, and F.Q. Zhou GSK3 signalling in neural development Nat Rev Neurosci 11 2010 539 551
12. Z. Freyberg, S.J. Ferrando, and J.A. Javitch Roles of the Akt/GSK-3 and Wnt signaling pathways in schizophrenia and antipsychotic drug action Am J Psychiatry 167 2010 388 396
13. K. Brennand, J.N. Savas, Y. Kim, N. Tran, A. Simone, K. Hashimoto-Torii, and et al. Phenotypic differences in hiPSC NPCs derived from patients with schizophrenia [published online ahead of print Apr 1] Mol Psychiatry. 2014
14. K.J. Brennand, A. Simone, J. Jou, C. Gelboin-Burkhart, N. Tran, S. Sangar, and et al. Modelling schizophrenia using human induced pluripotent stem cells Nature 473 2011 221 225
15. M.D. Robinson, D.J. McCarthy, and G.K. Smyth edgeR: A Bioconductor package for differential expression analysis of digital gene expression data Bioinformatics 26 2010 139 140
16. C. Hodar, R. Assar, M. Colombres, A. Aravena, L. Pavez, M. Gonzalez, and et al. Genome-wide identification of new Wnt/beta-catenin target genes in the human genome using CART method BMC Genomics 11 2010 348
17. J. Roose, M. Molenaar, J. Peterson, J. Hurenkamp, H. Brantjes, P. Moerer, and et al. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors Nature 395 1998 608 612
18. M.T. Veeman, D.C. Slusarski, A. Kaykas, S.H. Louie, and R.T. Moon Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements Curr Biol 13 2003 680 685
19. J. De Calisto, C. Araya, L. Marchant, C.F. Riaz, and R. Mayor Essential role of non-canonical Wnt signalling in neural crest migration Development 132 2005 2587 2597
20. H.O. Kalkman Altered growth factor signaling pathways as the basis of aberrant stem cell maturation in schizophrenia Pharmacol Ther 121 2009 115 122
21. G.J. Woodhead, C.A. Mutch, E.C. Olson, and A. Chenn Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation J Neurosci 26 2006 12620 12630
22. R. Verani, I. Cappuccio, P. Spinsanti, R. Gradini, A. Caruso, M.C. Magnotti, and et al. Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid J Neurochem 100 2007 242 250
23. S.T. Patil, L. Zhang, F. Martenyi, S.L. Lowe, K.A. Jackson, B.V. Andreev, and et al. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: A randomized Phase 2 clinical trial Nat Med 13 2007 1102 1107
24. S.L. Patterson, C. Pittenger, A. Morozov, K.C. Martin, H. Scanlin, C. Drake, and et al. Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase Neuron 32 2001 123 140
25. B.A. Parr, M.J. Shea, G. Vassileva, and A.P. McMahon Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds Development 119 1993 247 261
26. D.C. Lie, S.A. Colamarino, H.J. Song, L. Desire, H. Mira, A. Consiglio, and et al. Wnt signalling regulates adult hippocampal neurogenesis Nature 437 2005 1370 1375
27. O. Robicsek, R. Karry, I. Petit, N. Salman-Kesner, F.J. Muller, E. Klein, and et al. Abnormal neuronal differentiation and mitochondrial dysfunction in hair follicle-derived induced pluripotent stem cells of schizophrenia patients Mol Psychiatry 18 2013 1067 1076
28. D.X. Yu, F.P. Di Giorgio, J. Yao, M.C. Marchetto, K. Brennand, R. Wright, and et al. Modeling hippocampal neurogenesis using human pluripotent stem cells Stem Cell Reports 2 2014 295 310
29. S.M. Chambers, C.A. Fasano, E.P. Papapetrou, M. Tomishima, M. Sadelain, and L. Studer Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling Nat Biotechnol 27 2009 275 280
30. S. Kriks, J.W. Shim, J. Piao, Y.M. Ganat, D.R. Wakeman, Z. Xie, and et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease Nature 480 2011 547 551
31. A.M. Maroof, S. Keros, J.A. Tyson, S.W. Ying, Y.M. Ganat, F.T. Merkle, and et al. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells Cell Stem Cell 12 2013 559 572
32. C.R. Nicholas, J. Chen, Y. Tang, D.G. Southwell, N. Chalmers, D. Vogt, and et al. Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development Cell Stem Cell 12 2013 573 586
33. L. Aubry, A. Bugi, N. Lefort, F. Rousseau, M. Peschanski, and A.L. Perrier Striatal progenitors derived from human ES cells mature into DARPP32 neurons in vitro and in quinolinic acid-lesioned rats Proc Natl Acad Sci U S A 105 2008 16707 16712
34. N. Zhang, M.C. An, D Montoro, and L.M. Ellerby Characterization of human Huntington's disease cell model from induced pluripotent stem cells PLoS Curr 2:RRN1 2010 193
35. V. Hook, K. Brennand, Y. Kim, T. Toneff, L. Funkelstein, M. Ziegler, and et al. Human iPSC neurons display activity-dependent neurotransmitter secretion: Aberrant catecholamine levels in schizophrenia neurons Stem Cell Reports 3 2014 531 538
36. T.A. Atkin, A.F. MacAskill, N.J. Brandon, and J.T. Kittler Disrupted in Schizophrenia-1 regulates intracellular trafficking of mitochondria in neurons Mol Psychiatry 16 2011 122 124 121
37. K. Hashimoto-Torii, M. Torii, M. Fujimoto, A. Nakai, R. El Fatimy, V. Mezger, and et al. Roles of heat shock factor 1 in neuronal response to fetal environmental risks and its relevance to brain disorders Neuron 82 2014 560 572
38. S. Paulsen BDa, R. de Moraes Maciel, A. Galina, M.S. Souza da Silveira, C. dos Santos Souza, H. Drummond, and et al. Altered oxygen metabolism associated to neurogenesis of induced pluripotent stem cells derived from a schizophrenic patient Cell Transplant 21 2012 1547 1559
39. S. Kano, C. Colantuoni, F. Han, Z. Zhou, Q. Yuan, A. Wilson, and et al. Genome-wide profiling of multiple histone methylations in olfactory cells: Further implications for cellular susceptibility to oxidative stress in schizophrenia Mol Psychiatry 18 2013 740 742
40. M.A. Essers, L.M. de Vries-Smits, N. Barker, P.E. Polderman, B.M. Burgering, and H.C. Korswagen Functional interaction between beta-catenin and FOXO in oxidative stress signaling Science 308 2005 1181 1184
41. G.Z. Tao, N. Lehwald, K.Y. Jang, J. Baek, B. Xu, M.B. Omary, and et al. Wnt/beta-catenin signaling protects mouse liver against oxidative stress-induced apoptosis through the inhibition of forkhead transcription factor FoxO3 J Biol Chem 288 2013 17214 17224
42. N. Coant, S. Ben Mkaddem, E. Pedruzzi, C. Guichard, X. Treton, R. Ducroc, and et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon Mol Cell Biol 30 2010 2636 2650
43. Y. Funato, T. Michiue, M. Asashima, and H. Miki The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled Nat Cell Biol 8 2006 501 508
44. S. Kajla, A.S. Mondol, A. Nagasawa, Y. Zhang, M. Kato, K. Matsuno, and et al. A crucial role for Nox 1 in redox-dependent regulation of Wnt-beta-catenin signaling FASEB J 26 2012 2049 2059
45. Y. Zhang, Y. Sun, F. Wang, Z. Wang, Y. Peng, and R. Li Downregulating the canonical Wnt/beta-catenin signaling pathway attenuates the susceptibility to autism-like phenotypes by decreasing oxidative stress Neurochem Res 37 2012 1409 1419
46. F.E. Emiliani, T.W. Sedlak, and A. Sawa Oxidative stress and schizophrenia: recent breakthroughs from an old story Curr Opin Psychiatry 27 2014 185 190