Increased expression of receptor phosphotyrosine phosphatase-β/ζ is associated with molecular, cellular, behavioral and cognitive schizophrenia phenotypes

Translational Psychiatry

Volumn 1, Issue , 2011, Pages

  Takahashi, N ^a   Sakurai, T ^a,b   Bozdagi Gunal, O ^a   Dorr, N P ^a   Moy, J ^a   Krug, L ^a   Gama Sosa, M ^a   Elder, G A ^a   Koch, R J ^a   Walker, R H ^a   Hof, P R ^a   Davis, K L ^a   Buxbaum, J D ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Animal model; Dopamine; GABA; Glutamate; Neuregulin; Schizophrenia

Indexed keywords

RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE;

ADULT; ANIMAL; ARTICLE; BIOSYNTHESIS; C57BL MOUSE; COGNITIVE DEFECT; DISEASE MODEL; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MIDDLE AGED; MOUSE; PHENOTYPE; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION;

ADULT; ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; PHENOTYPE; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; UP-REGULATION; YOUNG ADULT;

EID: 79958180752     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2011.8     Document Type: Article

References (76)

1. Jaaro-Peled H, Hayashi-Takagi A, Seshadri S, Kamiya A, Brandon NJ, Sawa A. Neurodevelopmental mechanisms of schizophrenia: understanding disturbed postnatal brain maturation through neuregulin-1-ErbB4 and DISC1. Trends Neurosci 2009;32:485-495.
2. Lewis DA, Lieberman JA. Catching up on schizophrenia: natural history and neurobiology. Neuron 2000;28:325-334.
3. Lewis DA, Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 2002;25:409-432. (Pubitemid 34748023)
4. Harrison PJ, Weinberger DR. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005;10:40-68; image 45. (Pubitemid 40139588)
5. Kirov G, O'Donovan MC, Owen MJ. Finding schizophrenia genes. J Clin Invest 2005;115:1440-1448. (Pubitemid 40814648)
6. Coyle JT. The glutamatergic dysfunction hypothesis for schizophrenia. Harv Rev Psychiatry 1996;3:241-253. (Pubitemid 26058365)
7. Javitt DC, Zukin SR. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 1991;148:1301-1308.
8. Coyle JT, Tsai G. The NMDA receptor glycine modulatory site: a therapeutic target for improving cognition and reducing negative symptoms in schizophrenia. Psychopharmacology (Berl) 2004;174:32-38. (Pubitemid 38925088)
9. Snyder SH. The dopamine hypothesis of schizophrenia: focus on the dopamine receptor. Am J Psychiatry 1976;133:197-202.
10. Davis KL, Kahn RS, Ko G, Davidson M. Dopamine in schizophrenia: a review and reconceptualization. Am J Psychiatry 1991;148:1474-1486.
11. Howes OD, Kapur S. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr Bull 2009;35:549-562.
12. Lewis DA, Gonzalez-Burgos G. Pathophysiologically based treatment interventions in schizophrenia. Nat Med 2006;12:1016-1022. (Pubitemid 44353381)
13. Lewis DA, Moghaddam B. Cognitive dysfunction in schizophrenia: convergence of gammaaminobutyric acid and glutamate alterations. Arch Neurol 2006;63:1372-1376. (Pubitemid 44547546)
14. Davis KL, Stewart DG, Friedman JI, Buchsbaum M, Harvey PD, Hof PR et al. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 2003;60:443-456. (Pubitemid 36539053)
15. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 2003;362:798-805. (Pubitemid 37093922)
16. Benzel I, Bansal A, Browning BL, Galwey NW, Maycox PR, McGinnis R et al. Interactions among genes in the ErbB-neuregulin signalling network are associated with increased susceptibility to schizophrenia. Behav Brain Funct 2007;3:31.
17. Corvin AP, Morris DW, McGhee K, Schwaiger S, Scully P, Quinn J et al. Confirmation and refinement of an 'at-risk' haplotype for schizophrenia suggests the EST cluster, Hs.97362, as a potential susceptibility gene at the Neuregulin-1 locus. Mol Psychiatry 2004;9:208-213.
18. Petryshen TL, Middleton FA, Kirby A, Aldinger KA, Purcell S, Tahl AR et al. Support for involvement of neuregulin 1 in schizophrenia pathophysiology. Mol Psychiatry 2005;10:366-374, 328.
19. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002;71:877-892. (Pubitemid 135750519)
20. Norton N, Moskvina V, Morris DW, Bray NJ, Zammit S, Williams NM et al. Evidence that interaction between neuregulin 1 and its receptor erbB4 increases susceptibility to schizophrenia. Am J Med Genet B Neuropsychiatr Genet 2006;141 B: 96-101. (Pubitemid 43062550)
21. Mei L, Xiong WC. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008;9:437-452. (Pubitemid 351704944)
22. Munafo MR, Thiselton DL, Clark TG, Flint J. Association of the NRG1 gene and schizophrenia: a meta-analysis. Mol Psychiatry 2006;11:539-546.
23. Hall J, Whalley HC, Job DE, Baig BJ, McIntosh AM, Evans KL et al. A neuregulin 1 variant associated with abnormal cortical function and psychotic symptoms. NatNeurosci 2006;9:1477-1478. (Pubitemid 44862654)
24. Williams NM, Preece A, Spurlock G, Norton N, Williams HJ, Zammit S et al. Support for genetic variation in neuregulin 1 and susceptibility to schizophrenia. Mol Psychiatry 2003;8:485-487. (Pubitemid 36829690)
25. Li T, Stefansson H, Gudfinnsson E, Cai G, Liu X, Murray RM et al. Identification of a novel neuregulin 1 at-risk haplotype in Han schizophrenia Chinese patients, but no association with the Icelandic/Scottish risk haplotype. Mol Psychiatry 2004;9:698-704. (Pubitemid 38932174)
26. Corfas G, Roy K, Buxbaum JD. Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat Neurosci 2004;7:575-580. (Pubitemid 38691892)
27. Li B, Woo RS, Mei L, Malinow R. The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 2007;54:583-597. (Pubitemid 46756136)
28. Bjarnadottir M, Misner DL, Haverfield-Gross S, Bruun S, Helgason VG, Stefansson H et al. Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1+/-knock-outs compared with wild-type mice. J Neurosci 2007;27:4519-4529. (Pubitemid 46663586)
29. Roy K, Murtie JC, El-Khodor BF, Edgar N, Sardi SP, Hooks BM et al. Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 2007;104:8131-8136. (Pubitemid 47185887)
30. Wen L, Lu YS, Zhu XH, Li XM, Woo RS, Chen YJ et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci USA 2010;107:1211-1216.
31. Gu Z, Jiang Q, Fu AK, Ip NY, Yan Z. Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex. J Neurosci 2005;25:4974-4984. (Pubitemid 40712840)
32. Fazzari P, Paternain AV, Valiente M, Pla R, Lujan R, Lloyd K et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010;464:1376-1380.
33. Vullhorst D, Neddens J, Karavanova I, Tricoire L, Petralia RS, McBain CJ et al. Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 2009;29:12255-12264.
34. Woo RS, Li XM, Tao Y, Carpenter-Hyland E, Huang YZ, Weber J et al. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 2007;54:599-610. (Pubitemid 46756135)
35. Silberberg G, Darvasi A, Pinkas-Kramarski R, Navon R. The involvement of ErbB4 with schizophrenia: association and expression studies. Am J Med Genet B Neuropsychiatr Genet 2006;141 B: 142-148. (Pubitemid 43214789)
36. Shiota S, Tochigi M, Shimada H, Ohashi J, Kasai K, Kato N et al. Association and interaction analyses of NRG1 and ERBB4 genes with schizophrenia in a Japanese population. J Hum Genet 2008;53:929-935.
37. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005;47:681-694. (Pubitemid 41208007)
38. Chen S, Velardez MO, Warot X, Yu ZX, Miller SJ, Cros D et al. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 2006;26:3079-3086.
39. Tao Y, Dai P, Liu Y, Marchetto S, Xiong WC, Borg JP et al. Erbin regulates NRG1 signaling and myelination. Proc Natl Acad Sci USA 2009;106:9477-9482.
40. Harrison PJ, Law AJ. Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 2006;60:132-140.
41. Parlapani E, Schmitt A, Wirths O, Bauer M, Sommer C, Rueb U et al. Gene expression of neuregulin-1 isoforms in different brain regions of elderly schizophrenia patients. World J Biol Psychiatry 2010;11:243-250.
42. Law AJ, Lipska BK, Weickert CS, Hyde TM, Straub RE, Hashimoto R et al. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5' SNPs associated with the disease. Proc Natl Acad Sci USA 2006;103:6747-6752.
43. Keri S, Seres I, Kelemen O, Benedek G. Neuregulin 1-stimulated phosphorylation of AKT in psychotic disorders and its relationship with neurocognitive functions. Neurochem Int 2009;55:606-609.
44. Keri S, Beniczky S, Kelemen O. Suppression of the P50 evoked response and neuregulin 1-induced AKT phosphorylation in first-episode schizophrenia. Am J Psychiatry 2010;167:444-450.
45. Nicodemus KK, Law AJ, Radulescu E, Luna A, Kolachana B, Vakkalanka R et al. Biological validation of increased schizophrenia risk with NRG1, ERBB4, and AKT1 epistasis via functional neuroimaging in healthy controls. Arch Gen Psychiatry 2010;67:991-1001.
46. Nicodemus KK, Luna A, Vakkalanka R, Goldberg T, Egan M, Straub RE et al. Further evidence for association between ErbB4 and schizophrenia and influence on cognitive intermediate phenotypes in healthy controls. Mol Psychiatry 2006;11:1062-1065. (Pubitemid 44863428)
47. Zuliani R, Moorhead TW, Bastin ME, Johnstone EC, Lawrie SM, Brambilla P et al. Genetic variants in the ErbB4 gene are associated with white matter integrity. Psychiatry Res 2011;191:133-137.
48. Law AJ, Kleinman JE, Weinberger DR, Weickert CS. Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum Mol Genet 2007;16:129-141. (Pubitemid 46178996)
49. Buxbaum JD, Georgieva L, Young JJ, Plescia C, Kajiwara Y, Jiang Y et al. Molecular dissection of NRG1-ERBB4 signaling implicates PTPRZ1 as a potential schizophrenia susceptibility gene. Mol Psychiatry 2008;13:162-172.
50. Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, Cooper GM et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008;320:539-543. (Pubitemid 351590668)
51. Hahn CG, Wang HY, Cho DS, Talbot K, Gur RE, Berrettini WH et al. Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nat Med 2006;12:824-828. (Pubitemid 44050073)
52. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of realtime quantitative PCR data. Genome Biol 2007;8:R19.
53. Bozdagi O, Wang XB, Nikitczuk JS, Anderson TR, Bloss EB, Radice GL et al. Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci 2010;30:9984-9989.
54. Lilliehook C, Bozdagi O, Yao J, Gomez-Ramirez M, Zaidi NF, Wasco W et al. Altered Abeta formation and long-term potentiation in a calsenilin knock-out. J Neurosci 2003;23:9097-9106. (Pubitemid 37243810)
55. Walker RH, Koch RJ, Moore C, Meshul CK. Subthalamic nucleus stimulation and lesioning have distinct state-dependent effects upon striatal dopamine metabolism. Synapse 2009;63:136-146.
56. Elder GA, Ragnauth A, Dorr N, Franciosi S, Schmeidler J, Haroutunian V et al. Increased locomotor activity in mice lacking the low-density lipoprotein receptor. Behav Brain Res 2008;191:256-265.
57. Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP et al. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 2007;176:4-20. (Pubitemid 44879623)
58. Kvajo M, McKellar H, Arguello PA, Drew LJ, Moore H, MacDermott AB et al. 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 2008;105:7076-7081. (Pubitemid 351754532)
59. Bach ME, Simpson EH, Kahn L, Marshall JJ, Kandel ER, Kellendonk C. Transient and selective overexpression of D2 receptors in the striatum causes persistent deficits in conditional associative learning. Proc Natl Acad Sci USA 2008;105:16027-16032.
60. Kleinman JE, Law AJ, Lipska BK, Hyde TM, Ellis JK, Harrison PJ et al. Genetic neuropathology of schizophrenia: new approaches to an old question and new uses for postmortem human brains. Biol Psychiatry 2011;69:140-145.
61. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005;6:312-324. (Pubitemid 40469985)
62. Simpson EH, Kellendonk C, Kandel E. A possible role forthe striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 2010;65:585-596.
63. Laruelle M, Abi-Dargham A, Gil R, Kegeles L, Innis R. Increased dopamine transmission in schizophrenia: relationship to illness phases. Biol Psychiatry 1999;46:56-72. (Pubitemid 29296818)
64. Takahashi N, Sakurai T, Davis KL, Buxbaum JD. Linking oligodendrocyte and myelin dysfunction to neurocircuitry abnormalities in schizophrenia. Prog Neurobiol 2011;93:13-24.
65. Sim FJ, Lang JK, Waldau B, Roy NS, Schwartz TE, Pilcher WH et al. Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Ann Neurol 2006;59:763-779. (Pubitemid 43673154)
66. Csomor PA, Yee BK, Feldon J, Theodoridou A, Studerus E, Vollenweider FX. Impaired prepulse inhibition and prepulse-elicited reactivity but intact reflex circuit excitability in unmedicated schizophrenia patients: a comparison with healthy subjects and medicated schizophrenia patients. Schizophr Bull 2009;35:244-255.
67. Pantazopoulos H, Woo TU, Lim MP, Lange N, Berretta S. Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch Gen Psychiatry 2010;67:155-166.
68. Balla A, Nattini ME, Sershen H, Lajtha A, Dunlop DS, Javitt DC. GABAB/NMDA receptor interaction in the regulation of extracellular dopamine levels in rodent prefrontal cortex and striatum. Neuropharmacology 2009;56:915-921.
69. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008;31:234-242.
70. Ting AK, Chen Y, Wen L, Yin DM, Shen C, Tao Y et al. Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J Neurosci 2011;31:15-25.
71. Fujikawa A, Chow JP, Shimizu H, Fukada M, Suzuki R, Noda M. Tyrosine phosphorylation of ErbB4 is enhanced by PSD95 and repressed by protein tyrosine phosphatase receptor type Z. J Biochem 2007;142:343-350. (Pubitemid 350221837)
72. Adamsky K, Arnold K, Sabanay H, Peles E. Junctional protein MAGI-3 interacts with receptor tyrosine phosphatase beta (RPTP beta) and tyrosine-phosphorylated proteins. J Cell Sci 2003;116(Pt 7):1279-1289. (Pubitemid 36410666)
73. Makinodan M, Yamauchi T, Tatsumi K, Okuda H, Takeda T, Kiuchi K et al. Demyelination in the juvenile period, but not in adulthood, leads to long-lasting cognitive impairment and deficient social interaction in mice. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:978-985.
74. Kato T, Kasai A, Mizuno M, Fengyi L, Shintani N, Maeda S et al. Phenotypic characterization of transgenic mice overexpressing neuregulin-1. PLoS One 2010;5:e14185.
75. O'Tuathaigh CM, Kirby BP, Moran PM, Waddington JL. Mutant mouse models: genotypephenotype relationships to negative symptoms in schizophrenia. Schizophr Bull 2010;36:271-288.
76. van den Buuse M. Modeling the positive symptoms of schizophrenia in genetically modified mice: pharmacology and methodology aspects. Schizophr Bull 2010;36:246-270.