Loss of function studies in mice and genetic association link receptor protein tyrosine phosphatase α to schizophrenia

Biological Psychiatry

Volumn 70, Issue 7, 2011, Pages 626-635

  Takahashi, Nagahide ^a   Nielsen, Karin Sandager ^b   Aleksic, Branko ^c   Petersen, Steffen ^b   Ikeda, Masashi ^f   Kushima, Itaru ^c   Vacaresse, Nathalie ^d   Ujike, Hiroshi ^e   Iwata, Nakao ^f   Dubreuil, Véronique ^g   Mirza, Naheed ^b   Sakurai, Takeshi ^a   Ozaki, Norio ^c   Buxbaum, Joseph D ^a   Sap, Jan ^d,g  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEUROSEARCH A S   (Denmark)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e OKAYAMA UNIVERSITY   (Japan)

^f FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Mouse model; myelination; PTPRA; RPTP ; schizophrenia; tyrosine phosphatase

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDOPHENOTYPE; GENE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PTPRA GENE; RISK ASSESSMENT; RISK FACTOR; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN SHEATH; POLYMORPHISM, GENETIC; PREFRONTAL CORTEX; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 4; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 80052865737     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.06.016     Document Type: Article

References (78)

1. S. Marenco, and D.R. Weinberger The neurodevelopmental hypothesis of schizophrenia: Following a trail of evidence from cradle to grave Dev Psychopathol 12 2000 501 527
2. Y. Hakak, J.R. Walker, C. Li, W.H. Wong, K.L. Davis, and J.D. Buxbaum Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia Proc Natl Acad Sci U S A 98 2001 4746 4751 (Pubitemid 32295047)
3. P.J. Harrison, and D.R. Weinberger Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence [image 45] Mol Psychiatry 10 2005 40 68 (Pubitemid 40139588)
4. G.D. Fischbach NRG1 and synaptic function in the CNS Neuron 54 2007 495 497 (Pubitemid 46756150)
5. P. Fazzari, A.V. Paternain, M. Valiente, R. Pla, R. Lujan, and K. Lloyd Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling Nature 464 2010 1376 1380
6. L. Mei, and W.C. Xiong Neuregulin 1 in neural development, synaptic plasticity and schizophrenia Nat Rev Neurosci 9 2008 437 452 (Pubitemid 351704944)
7. B. Li, R.S. Woo, L. Mei, and R. Malinow The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity Neuron 54 2007 583 597 (Pubitemid 46756136)
8. L. Wen, Y.S. Lu, X.H. Zhu, X.M. Li, R.S. Woo, and Y.J. Chen Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons Proc Natl Acad Sci U S A 107 2010 1211 1216
9. G. Silberberg, A. Darvasi, R. Pinkas-Kramarski, and R. Navon The involvement of ErbB4 with schizophrenia: Association and expression studies Am J Med Genet B Neuropsychiatr Genet 141B 2006 142 148 (Pubitemid 43214789)
10. J.D. Buxbaum, L. Georgieva, J.J. Young, C. Plescia, Y. Kajiwara, and Y. Jiang Molecular dissection of NRG1-ERBB4 signaling implicates PTPRZ1 as a potential schizophrenia susceptibility gene Mol Psychiatry 13 2008 162 172
11. M. Bennett Positive and negative symptoms in schizophrenia: The NMDA receptor hypofunction hypothesis, neuregulin/ErbB4 and synapse regression Aust N Z J Psychiatry 43 2009 711 721
12. C.G. Hahn, H.Y. Wang, D.S. Cho, K. Talbot, R.E. Gur, and W.H. Berrettini Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia Nat Med 12 2006 824 828 (Pubitemid 44050073)
13. M. Bjarnadottir, D.L. Misner, S. Haverfield-Gross, S. Bruun, V.G. Helgason, and H. Stefansson Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1+/- knock-outs compared with wild-type mice J Neurosci 27 2007 4519 4529 (Pubitemid 46663586)
14. G.M. Pitcher, L.V. Kalia, D. Ng, N.M. Goodfellow, K.T. Yee, and E.K. Lambe Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors Nat Med 17 2011 470 478
15. M. Poltorak, I. Khoja, J.J. Hemperly, J.R. Williams, R. el-Mallakh, and W.J. Freed Disturbances in cell recognition molecules (N-CAM and L1 antigen) in the CSF of patients with schizophrenia Exp Neurol 131 1995 266 272
16. M. Poltorak, R. Wright, J.J. Hemperly, E.F. Torrey, F. Issa, and R.J. Wyatt Monozygotic twins discordant for schizophrenia are discordant for N-CAM and L1 in CSF Brain Res 751 1997 152 154 (Pubitemid 27122148)
17. K. Sakurai, O. Migita, M. Toru, and T. Arinami An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia Mol Psychiatry 7 2002 412 415 (Pubitemid 34499363)
18. Q.Y. Chen, Q. Chen, G.Y. Feng, K. Lindpaintner, Y. Chen, and X. Sun Case-control association study of the close homologue of L1 (CHL1) gene and schizophrenia in the Chinese population Schizophr Res 73 2005 269 274 (Pubitemid 40093889)
19. M.E. Atz, B. Rollins, and M.P. Vawter NCAM1 association study of bipolar disorder and schizophrenia: Polymorphisms and alternatively spliced isoforms lead to similarities and differences Psychiatr Genet 17 2007 55 67 (Pubitemid 46586676)
20. P.F. Sullivan, R.S. Keefe, L.A. Lange, E.M. Lange, T.S. Stroup, and J. Lieberman NCAM1 and neurocognition in schizophrenia Biol Psychiatry 61 2007 902 910 (Pubitemid 46412275)
21. D.P. van Kammen, M. Poltorak, M.E. Kelley, J.K. Yao, J.A. Gurklis, and J.L. Peters Further studies of elevated cerebrospinal fluid neuronal cell adhesion molecule in schizophrenia Biol Psychiatry 43 1998 680 686 (Pubitemid 28222389)
22. V. Bodrikov, I. Leshchyns'ka, V. Sytnyk, J. Overvoorde, J. den Hertog, and M. Schachner RPTPalpha is essential for NCAM-mediated p59fyn activation and neurite elongation J Cell Biol 168 2005 127 139 (Pubitemid 40111063)
23. V. Bodrikov, V. Sytnyk, I. Leshchyns'ka, J. den Hertog, and M. Schachner NCAM induces CaMKIIalpha-mediated RPTPalpha phosphorylation to enhance its catalytic activity and neurite outgrowth J Cell Biol 182 2008 1185 1200
24. H. Ye, Y.L. Tan, S. Ponniah, Y. Takeda, S.Q. Wang, and M. Schachner Neural recognition molecules CHL1 and NB-3 regulate apical dendrite orientation in the neocortex via PTP alpha Embo J 27 2008 188 200
25. N. Vacaresse, B. Moller, E.M. Danielsen, M. Okada, and J. Sap Activation of c-Src and Fyn kinases by protein-tyrosine phosphatase RPTPalpha is substrate-specific and compatible with lipid raft localization J Biol Chem 283 2008 35815 35824
26. J. den Hertog, J. Overvoorde, and S.W. de Laat Expression of receptor protein-tyrosine phosphatase alpha mRNA and protein during mouse embryogenesis Mech Dev 58 1996 89 101 (Pubitemid 26302228)
27. A. Petrone, F. Battaglia, C. Wang, A. Dusa, J. Su, and D. Zagzag Receptor protein tyrosine phosphatase a is essential for hippocampal neuronal migration and long-term potentiation EMBO J 22 2003 4121 4131 (Pubitemid 37021741)
28. Z. Tiran, A. Peretz, T. Sines, V. Shinder, J. Sap, and B. Attali Tyrosine phosphatases epsilon and alpha perform specific and overlapping functions in regulation of voltage-gated potassium channels in Schwann cells Mol Biol Cell 17 2006 4330 4342 (Pubitemid 44522052)
29. P.S. Wang, J. Wang, Z.C. Xiao, and C.J. Pallen Protein-tyrosine phosphatase alpha acts as an upstream regulator of Fyn signaling to promote oligodendrocyte differentiation and myelination J Biol Chem 284 2009 33692 33702
30. G. Lei, S. Xue, N. Chery, Q. Liu, J. Xu, and C.L. Kwan Gain control of N-methyl-D-aspartate receptor activity by receptor-like protein tyrosine phosphatase alpha EMBO J 21 2002 2977 2989 (Pubitemid 34670382)
31. H.T. Le, L. Maksumova, J. Wang, and C.J. Pallen Reduced NMDA receptor tyrosine phosphorylation in PTPalpha-deficient mouse synaptosomes is accompanied by inhibition of four src family kinases and Pyk2: An upstream role for PTPalpha in NMDA receptor regulation J Neurochem 98 2006 1798 1809 (Pubitemid 44298246)
32. S. Ponniah, D.Z. Wang, K.L. Lim, and C.J. Pallen Targeted disruption of the tyrosine phosphatase PTPalpha leads to constitutive downregulation of the kinases src and Fyn Curr Biol 9 1999 535 538 (Pubitemid 29257109)
33. J. Su, M. Muranjan, and J. Sap Receptor protein tyrosine phosphatase alpha activates Src-family kinases and controls integrin-mediated responses in fibroblasts Curr Biol 9 1999 505 511 (Pubitemid 29257105)
34. A.H. Fanous, M.C. Neale, B.T. Webb, R.E. Straub, F.A. O'Neill, and D. Walsh Novel linkage to chromosome 20p using latent classes of psychotic illness in 270 Irish high-density families Biol Psychiatry 64 2008 121 127
35. O. Teltsh, K. Kanyas, O. Karni, A. Levi, M. Korner, and E. Ben-Asher Genome-wide linkage scan, fine mapping, and haplotype analysis in a large, inbred, Arab Israeli pedigree suggest a schizophrenia susceptibility locus on chromosome 20p13 Am J Med Genet B Neuropsychiatr Genet 147B 2008 209 215 (Pubitemid 351355282)
36. S. Butini, S. Gemma, G. Campiani, S. Franceschini, F. Trotta, and M. Borriello Discovery of a new class of potential multifunctional atypical antipsychotic agents targeting dopamine D3 and serotonin 5-HT1A and 5-HT2A receptors: Design, synthesis, and effects on behavior J Med Chem 52 2009 151 169
37. J.T. Andreasen, K.K. Andersen, E.O. Nielsen, L. Mathiasen, and N.R. Mirza Nicotine and clozapine selectively reverse a PCP-induced deficit of PPI in BALB/cByJ but not NMRI mice: comparison with risperidone Behav Brain Res 167 2006 118 127 (Pubitemid 43063146)
38. M. Ikeda, B. Aleksic, Y. Kinoshita, T. Okochi, K. Kawashima, and I. Kushima Genome-wide association study of schizophrenia in a Japanese population Biol Psychiatry 69 2011 472 478
39. I.I. Gottesman, and T.D. Gould The endophenotype concept in psychiatry: Etymology and strategic intentions Am J Psychiatry 160 2003 636 645 (Pubitemid 41079594)
40. E.R. Marcotte, D.M. Pearson, and L.K. Srivastava Animal models of schizophrenia: A critical review J Psychiatry Neurosci 26 2001 395 410 (Pubitemid 34082728)
41. M.A. Geyer, K.L. McIlwain, and R. Paylor Mouse genetic models for prepulse inhibition: An early review Mol Psychiatry 7 2002 1039 1053 (Pubitemid 36044262)
42. U. Meincke, G.A. Light, M.A. Geyer, D.L. Braff, and E. Gouzoulis-Mayfrank Sensitization and habituation of the acoustic startle reflex in patients with schizophrenia Psychiatry Res 126 2004 51 61 (Pubitemid 38479795)
43. K.L. McIlwain, M.Y. Merriweather, L.A. Yuva-Paylor, and R. Paylor The use of behavioral test batteries: effects of training history Physiol Behav 73 2001 705 717 (Pubitemid 32885560)
44. V. Voikar, E. Vasar, and H. Rauvala Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: Implications for phenotyping screens Genes Brain Behav 3 2004 27 38 (Pubitemid 38160239)
45. D.J. Lodge, and A.A. Grace Hippocampal dysfunction and disruption of dopamine system regulation in an animal model of schizophrenia Neurotox Res 14 2008 97 104
46. K.L. Davis, D.G. Stewart, J.I. Friedman, M. Buchsbaum, P.D. Harvey, and P.R. Hof White matter changes in schizophrenia: Evidence for myelin-related dysfunction Arch Gen Psychiatry 60 2003 443 456 (Pubitemid 36539053)
47. M. Hoistad, D. Segal, N. Takahashi, T. Sakurai, J.D. Buxbaum, and P.R. Hof Linking white and grey matter in schizophrenia: Oligodendrocyte and neuron pathology in the prefrontal cortex Front Neuroanat 3 2009 9
48. D. Martins-de-Souza Proteome and transcriptome analysis suggests oligodendrocyte dysfunction in schizophrenia J Psychiatr Res 44 2010 149 156
49. N. Takahashi, T. Sakurai, K.L. Davis, and J.D. Buxbaum Linking oligodendrocyte and myelin dysfunction to neurocircuitry abnormalities in schizophrenia Prog Neurobiol 93 2011 13 24
50. H. Umemori, S. Sato, T. Yagi, S. Aizawa, and T. Yamamoto Initial events of myelination involve Fyn tyrosine kinase signalling Nature 367 1994 572 576 (Pubitemid 24055518)
51. B.R. Sperber, E.A. Boyle-Walsh, M.J. Engleka, P. Gadue, A.C. Peterson, and P.L. Stein A unique role for Fyn in CNS myelination J Neurosci 21 2001 2039 2047 (Pubitemid 32221386)
52. Z. Lu, L. Ku, Y. Chen, and Y. Feng Developmental abnormalities of myelin basic protein expression in fyn knock-out brain reveal a role of Fyn in posttranscriptional regulation J Biol Chem 280 2005 389 395 (Pubitemid 40165003)
53. E.M. Kramer-Albers, and R. White From axon-glial signalling to myelination: The integrating role of oligodendroglial Fyn kinase Cell Mol Life Sci 68 2011 2003 2012
54. K. Aberg, P. Saetre, E. Lindholm, B. Ekholm, U. Pettersson, and R. Adolfsson Human QKI, a new candidate gene for schizophrenia involved in myelination Am J Med Genet B Neuropsychiatr Genet 141B 2006 84 90 (Pubitemid 43062548)
55. M.R. Skelton, S. Ponniah, D.Z. Wang, T. Doetschman, C.V. Vorhees, and C.J. Pallen Protein tyrosine phosphatase alpha (PTP alpha) knockout mice show deficits in Morris water maze learning, decreased locomotor activity, and decreases in anxiety Brain Res 984 2003 1 10 (Pubitemid 36976789)
56. K. Hattori, S. Uchino, T. Isosaka, M. Maekawa, M. Iyo, and T. Sato Fyn is required for haloperidol-induced catalepsy in mice J Biol Chem 281 2006 7129 7135 (Pubitemid 43847477)
57. M.A. Geyer, and D.L. Braff Habituation of the blink reflex in normals and schizophrenic patients Psychophysiology 19 1982 1 6 (Pubitemid 12172271)
58. G. von Wichert, G. Jiang, A. Kostic, K. De Vos, J. Sap, and M.P. Sheetz RPTP-alpha acts as a transducer of mechanical force on av/b3-integrin- cytoskeleton linkages J Cell Biol 161 2003 143 153 (Pubitemid 36459087)
59. M. Chen, S.C. Chen, and C.J. Pallen Integrin-induced tyrosine phosphorylation of protein-tyrosine phosphatase-alpha is required for cytoskeletal reorganization and cell migration J Biol Chem 281 2006 11972 11980 (Pubitemid 43855461)
60. X. Zheng, R.J. Resnick, and D. Shalloway Apoptosis of estrogen-receptor negative breast cancer and colon cancer cell lines by PTP alpha and src RNAi Int J Cancer 122 2008 1999 2007 (Pubitemid 351441188)
61. D. Krndija, H. Schmid, J.L. Eismann, U. Lother, G. Adler, and F. Oswald Substrate stiffness and the receptor-type tyrosine-protein phosphatase alpha regulate spreading of colon cancer cells through cytoskeletal contractility Oncogene 29 2010 2724 2738
62. S. Yuasa, K. Hattori, and T. Yagi Defective neocortical development in Fyn-tyrosine-kinase-deficient mice Neuroreport 15 2004 819 822 (Pubitemid 38453465)
63. J. Goto, T. Tezuka, T. Nakazawa, H. Sagara, and T. Yamamoto Loss of Fyn tyrosine kinase on the C57BL/6 genetic background causes hydrocephalus with defects in oligodendrocyte development Mol Cell Neurosci 38 2008 203 212
64. K. Kapp, J. Siemens, P. Weyrich, J.B. Schulz, H.U. Haring, and R. Lammers Extracellular domain splice variants of a transforming protein tyrosine phosphatase alpha mutant differentially activate Src-kinase dependent focus formation Genes Cells 12 2007 63 73 (Pubitemid 44971097)
65. B. Tremper-Wells, R.J. Resnick, X. Zheng, L.J. Holsinger, and D. Shalloway Extracellular domain dependence of PTPalpha transforming activity Genes Cells 15 2010 711 724
66. L. Zeng, L. D'Alessandri, M.B. Kalousek, L. Vaughan, and C.J. Pallen Protein tyrosine phosphatase alpha (PTPalpha) and contactin form a novel neuronal receptor complex linked to the intracellular tyrosine kinase fyn J Cell Biol 147 1999 707 714
67. L.S. Laursen, C.W. Chan, and C. ffrench-Constant An integrin-contactin complex regulates CNS myelination by differential Fyn phosphorylation J Neurosci 29 2009 9174 9185
68. A.G. Nikonenko, M. Sun, E. Lepsveridze, I. Apostolova, I. Petrova, and A. Irintchev Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice Eur J Neurosci 23 2006 1839 1852
69. O. Bukalo, N. Fentrop, A.Y. Lee, B. Salmen, J.W. Law, and C.T. Wotjak Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus J Neurosci 24 2004 1565 1577 (Pubitemid 38240951)
70. G.K. Wood, H. Tomasiewicz, U. Rutishauser, T. Magnuson, R. Quirion, and J. Rochford NCAM-180 knockout mice display increased lateral ventricle size and reduced prepulse inhibition of startle Neuroreport 9 1998 461 466 (Pubitemid 28109206)
71. G. Kochlamazashvili, O. Senkov, S. Grebenyuk, C. Robinson, M.F. Xiao, and K. Stummeyer Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors J Neurosci 30 2010 4171 4183
72. G.P. Demyanenko, M. Schachner, E. Anton, R. Schmid, G. Feng, and J. Sanes Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex Neuron 44 2004 423 437 (Pubitemid 39423345)
73. A. Irintchev, M. Koch, L.K. Needham, P. Maness, and M. Schachner Impairment of sensorimotor gating in mice deficient in the cell adhesion molecule L1 or its close homologue, CHL1 Brain Res 1029 2004 131 134 (Pubitemid 39463316)
74. S.G. Grant, T.J. O'Dell, K.A. Karl, P.L. Stein, P. Soriano, and E.R. Kandel Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice Science 258 1992 1903 1910 (Pubitemid 23026728)
75. H. Ishiguro, T. Saito, H. Shibuya, M. Toru, and T. Arinami Mutation and association analysis of the Fyn kinase gene with alcoholism and schizophrenia Am J Med Genet 96 2000 716 720
76. J.K. Rybakowski, A. Borkowska, M. Skibinska, and J. Hauser Polymorphisms of the Fyn kinase gene and a performance on the Wisconsin Card Sorting Test in schizophrenia Psychiatr Genet 17 2007 201 204 (Pubitemid 46716214)
77. K. Hattori, H. Fukuzako, T. Hashiguchi, S. Hamada, Y. Murata, and T. Isosaka Decreased expression of Fyn protein and disbalanced alternative splicing patterns in platelets from patients with schizophrenia Psychiatry Res 168 2009 119 128
78. L.T. Yang, K. Alexandropoulos, and J. Sap c-SRC mediates neurite outgrowth through recruitment of Crk to the scaffolding protein Sin/Efs without altering the kinetics of ERK activation J Biol Chem 277 2002 17406 17414 (Pubitemid 34967540)