Taking a bird's eye view on a mouse model review: A comparison of findings from mouse models targeting DISC1 or DISC1-interacting proteins

Future Neurology

Volumn 6, Issue 5, 2011, Pages 661-677

  Kelly, Michy P ^a   Brandon, Nicholas J ^a  

^a PFIZER INC   (United States)

Author keywords

behavior; bipolar disorder; brain; cAMP; cyclic nucleotide; knockout; neurodevelopment; neuron; schizophrenia; transgenic

Indexed keywords

DISC1 INTERACTING PROTEIN; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DOPAMINE; DYSBINDIN; GENE PRODUCT; GLYCOGEN SYNTHASE KINASE 3; PARVALBUMIN; PHOSPHODIESTERASE 4B; PHOSPHODIESTERASE IV; TAMOXIFEN; TETRACYCLINE; UNCLASSIFIED DRUG;

ACOUSTIC STARTLE PREPULSE INHIBITION; BACTERIAL ARTIFICIAL CHROMOSOME; BEHAVIOR; BIPOLAR DISORDER; BRAIN CORTEX; BRAIN SIZE; CAMKIIALPHA GENE; CHROMOSOME 11; DENDRITIC LENGTH; DEPRESSION; DISC1 GENE; DOPAMINE RELEASE; ELECTROPORATION; FAMILY; GENE; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE FUSION; GENE MUTATION; GENE TRANSLOCATION; GENETIC MODEL; HUMAN; IN VITRO ELECTROPORATION; IN VITRO GENE TRANSFER; LATENT INHIBITION; LATERAL BRAIN VENTRICLE; LOCOMOTION; MEMORY; MONOAMINERGIC SYSTEM; NERVOUS SYSTEM PARAMETERS; NEURAL PROGENITOR PROLIFERATION; NEURONAL DENSITY; NEURONAL MIGRATION; NOCICEPTION; NONHUMAN; PHENOTYPE; PREPULSE INHIBITION; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SCHIZOPHRENIA; SOCIAL BEHAVIOR; SPINE DENSITY; STARTLE REFLEX; TRANSGENE; TRANSGENIC MOUSE; WORKING MEMORY;

EID: 80052329540     PISSN: 14796708     EISSN: 17486971     Source Type: Journal    
DOI: 10.2217/fnl.11.39     Document Type: Review

References (91)

1. Camargo LM, Collura V, Rain JC et al. Disrupted in schizophrenia 1 interactome:evidence for the close connectivity of risk genes and a potential synaptic basis for schizophrenia. Mol. Psychiatry 12(1), 74-86 (2007).
2. Bradshaw NJ, Porteous DJ. DISC1-binding proteins in neural development, signalling and schizophrenia. Neuropharmacology DOI: 10.1016/j.neuropharm.2010. 12.027 (2010) (Epub ahead of print). n Review of evidence linking DISC1 and DISC1-interacting proteins to schizophrenia.
3. Millar JK, Wilson-Annan JC, Anderson S et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 9(9), 1415-1423 (2000).
4. Leliveld SR, Hendriks P, Michel M et al. Oligomer assembly of the C-terminal DISC1 domain (640-854) is controlled by self-association motifs and disease-associated polymorphism S704C. Biochemistry 48(32), 7746-7755 (2009).
5. Clapcote SJ, Lipina TV, Millar JK et al. Behavioral phenotypes of DISC1 missense mutations in mice. Neuron 54(3), 387-402 (2007).
6. Lipina TV, Niwa M, Jaaro-Peled H et al. Enhanced dopamine function in DISC1-L100P mutant mice: Implications for schizophrenia. Genes Brain Behav. 9(7), 777-789 (2011).
7. Walsh J, Tighe O, Lai D et al. Disruption of thermal nociceptive behavior in mice mutant for the schizophrenia-associated genes NRG1, COMT and DISC1. Brain Res. 1348, 114-119 (2010).
8. Lipina TV, Wang M, Liu F, Roder JC. Synergistic interactions between PDE4B and GSK-3: DISC1 mutant mice. Neuropharmacology DOI: 10.1016/j.neuropharm. 2011.02.020 (2011) (Epub ahead of print).
9. Koike H, Arguello PA, Kvajo M, Karayiorgou M, Gogos JA. Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice. Proc. Natl Acad. Sci. USA 103(10), 3693-3697 (2006).
10. Kvajo M, McKellar H, Arguello PA 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 105(19), 7076-7081 (2008).
11. Shen S, Lang B, Nakamoto C et al. Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated DISC1. J. Neurosci. 28(43), 10893-10904 (2008).
12. Hikida T, Jaaro-Peled H, Seshadri S et al. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans Proc. Natl Acad. Sci. USA 104(36), 14501-14506 (2007).
13. Ibi D, Nagai T, Koike H et al. Combined effect of neonatal immune activation and mutant DISC1 on phenotypic changes in adulthood. Behav. Brain Res. 206(1), 32-37 (2010). nn Studies the impact of neonatal immune activation on adult DISC1-mutant mouse phenotypes. This a key approach in attempting to model schizophrenia, a disease that manifests due to gene-environment interactions during neurodevelopment.
14. Pletnikov MV, Ayhan Y, Nikolskaia O et al. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol. Psychiatry 13(2), 173-186 (2008).
15. Ayhan Y, Abazyan B, Nomura J et al. Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neurobehavioral phenotypes in transgenic mice: Evidence for neurodevelopmental origin of major psychiatric disorders. Mol. Psychiatry 16(3), 293-306 (2011). nn Takes full advantage of the tetracycline-regulated nature of the authors' transgenic system to explore the developmental impact of their genetic manipulation. Utilization of this type of technology is key to parsing out the role of a given perturbation in the development versus manifestation of schizophrenia-related phenotypes.
16. Abazyan B, Nomura J, Kannan G et al. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol. Psychiatry 68(12), 1172-1181 (2010). nn Another series of studies that demonstrates the impact of neonatal immune activation on adult DISC1-mutant mouse phenotypes. This is a key approach in attempting to model schizophrenia, a disease that manifests due to gene-environment interactions during neurodevelopment.
17. Pogorelov VM, Nomura J, Kim J et al. Mutant DISC1 affects methamphetamine-induced sensitization and conditioned place preference: A comorbidity model. Neuropharmacology DOI: 10.1016/j.neuropharm.2011.02.003 (2011) (Epub ahead of print).
18. Li W, Zhou Y, Jentsch JD et al. Specific developmental disruption of disrupted-in-schizophrenia-1 function results in schizophrenia-related phenotypes in mice. Proc. Natl Acad. Sci. USA 104(46), 18280-18285 (2007). nn Authors were able to produce schizophrenia-related phenotypes in adult mice by expressing their transgene only on postnatal day 7. Such restricted expression was achieved by using a tamoxifen-regulated expression cassette. Utilization of this type of technology is key to parsing out the role of a given perturbation in the development versus manifestation of schizophrenia-related phenotypes.
19. Niwa M, Kamiya A, Murai R et al. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron 65, 480-489 (2010). nn Authors were able to produce schizophrenia-related phenotypes in adults by knocking down DISC1 during a restricted perinatal period. Such restricted knockdown was achieved through in utero gene transfer of DISC1-knockdown constructs. Utilization of this type of technology is key to parsing out the role of a given perturbation in the development versus manifestation of schizophrenia-related phenotypes.
20. Mao Y, Ge X, Frank CL et al. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3b/b-catenin signaling. Cell 136(6), 1017-1031 (2009).
21. Kamiya A, Tan PL, Kubo K et al. Recruitment of PCM1 to the centrosome by the cooperative action of DISC1 and BBS4: A candidate for psychiatric illnesses. Arch. Gen. Psychiatry 65(9), 996-1006 (2008).
22. Kamiya A, Kubo K, Tomoda T et al. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol. 7(12), 1167-1178 (2005).
23. Singh KK, Ge X, Mao Y et al. Dixdc1 is a critical regulator of DISC1 and embryonic cortical development. Neuron 67(1), 33-48 (2010).
24. Lee FH, Fadel MP, Preston-Maher K et al. DISC1 point mutations in mice affect development of the cerebral cortex. J. Neurosci. 31(9), 3197-3206 (2010).
25. Lee FH, Kaidanovich-Beilin O, Roder JC, Woodgett JR, Wong AH. Genetic inactivation of GSK3a rescues spine deficits in DISC1-L100P mutant mice. Schizophr. Res. 129(1), 74-79 (2011).
26. Brown SM, Clapcote SJ, Millar JK et al. Synaptic modulators Nrxn1 and Nrxn3 are disregulated in a DISC1 mouse model of schizophrenia. Mol. Psychiatry 16, 585-587 (2011).
27. Kimura T, Yamashita S, Nakao S et al. GSK-3b is required for memory reconsolidation in adult brain PLoS One 3(10), E3540 (2008).
28. Prickaerts J, Moechars D, Cryns K et al. Transgenic mice overexpressing glycogen synthase kinase 3b: A putative model of hyperactivity and mania. J. Neurosci. 26(35), 9022-9029 (2006).
29. Polter A, Beurel E, Yang S et al. Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 35(8), 1761-1774 (2010). n These mice, harboring a double mutation in glycogen synthase kinase 3, show both mania-like and depressive-like behaviors. This is a rare occurrence, and this pattern of phenotypes suggests that they may be particularly relevant for modeling bipolar disorder, a disease for which very few animal models exist.
30. Kaidanovich-Beilin O, Lipina TV, Takao K et al. Abnormalities in brain structure and behavior in GSK-3a mutant mice. Mol. Brain 2, 35 (2009).
31. Zhang HT, Huang Y, Masood A et al. Anxiogenic-like behavioral phenotype of mice deficient in phosphodiesterase 4B (PDE4B). Neuropsychopharmacology 33(7), 1611-1623 (2008).
32. Siuciak JA, Chapin DS, McCarthy SA, Martin AN. Antipsychotic profile of rolipram: Efficacy in rats and reduced sensitivity in mice deficient in the phosphodiesterase-4B (PDE4B) enzyme. Psychopharmacology 192(3), 415-424 (2007).
33. Siuciak JA, McCarthy SA, Chapin DS, Martin AN. Behavioral and neurochemical characterization of mice deficient in the phosphodiesterase-4B (PDE4B) enzyme. Psychopharmacology 197(1), 115-126 (2008).
34. Zhang HT, Huang Y, Jin SL et al. Antidepressant-like profile and reduced sensitivity to rolipram in mice deficient in the PDE4D phosphodiesterase enzyme. Neuropsychopharmacology 27(4), 587-595 (2002).
35. Ikeda M, Hikita T, Taya S et al. Identification of YWHAE, a gene encoding 14-3-3e, as a possible susceptibility gene for schizophrenia. Hum. Mol. Genet. 17(20), 3212-3222 (2008).
36. Ma XM, Kiraly DD, Gaier ED et al. Kalirin-7 is required for synaptic structure and function J. Neurosci. 28(47), 12368-12382 (2008).
37. Kiraly DD, Ma XM, Mazzone CM, Xin X, Mains RE, Eipper BA. Behavioral and morphological responses to cocaine require Kalirin7. Biol. Psychiatry 68(3), 249-255 (2010).
38. Cahill ME, Xie Z, Day M et al. Kalirin regulates cortical spine morphogenesis and disease-related behavioral phenotypes. Proc. Natl Acad. Sci. USA 106(31), 13058-13063 (2009).
39. Xie Z, Cahill ME, Penzes P. Kalirin loss results in cortical morphological alterations. Mol. Cell. Neurosci. 43(1), 81-89 (2010).
40. Xie Z, Cahill ME, Radulovic J et al. Hippocampal phenotypes in Kalirin-deficient mice. Mol. Cell. Neurosci. 46(1), 45-54 (2011).
41. Paylor R, Hirotsune S, Gambello MJ, Yuva-Paylor L, Crawley JN, Wynshaw-Boris A. Impaired learning and motor behavior in heterozygous Pafah1b1 (Lis1) mutant mice. Learn Mem. 6(5), 521-537 (1999).
42. Greenwood JS, Wang Y, Estrada RC, Ackerman L, Ohara PT, Baraban SC. Seizures, enhanced excitation, and increased vesicle number in Lis1 mutant mice. Ann. Neurol. 66(5), 644-653 (2009).
43. Jones DL, Baraban SC. Characterization of inhibitory circuits in the malformed hippocampus of Lis1 mutant mice. J. Neurophysiol. 98(5), 2737-2746 (2007).
44. Jones DL, Baraban SC. Inhibitory inputs to hippocampal interneurons are reorganized in Lis1 mutant mice. J. Neurophysiol. 102(2), 648-658 (2009).
45. Feng YQ, Zhou ZY, He X et al. Dysbindin deficiency in sandy mice causes reduction of snapin and displays behaviors related to schizophrenia. Schizophr. Res. 106(2-3), 218-228 (2008).
46. Takao K, Toyama K, Nakanishi K et al. Impaired long-term memory retention and working memory in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Mol. Brain 1, 11 (2008).
47. Hattori S, Murotani T, Matsuzaki S et al. Behavioral abnormalities and dopamine reductions in sdy mutant mice with a deletion in Dtnbp1, a susceptibility gene for schizophrenia. Biochem. Biophys. Res. Commun. 373(2), 298-302 (2008).
48. Bhardwaj SK, Baharnoori M, Sharif-Askari B, Kamath A, Williams S, Srivastava LK. Behavioral characterization of dysbindin-1 deficient sandy mice. Behav. Brain Res. 197(2), 435-441 (2009).
49. Jentsch JD, Trantham-Davidson H, Jairl C, Tinsley M, Cannon TD, Lavin A. Dysbindin modulates prefrontal cortical glutamatergic circuits and working memory function in mice. Neuropsychopharmacology 34(12), 2601-2608 (2009).
50. Murotani T, Ishizuka T, Hattori S, Hashimoto R, Matsuzaki S, Yamatodani A. High dopamine turnover in the brains of sandy mice. Neurosci. Lett. 421(1), 47-51 (2007).
51. Nagai T, Kitahara Y, Shiraki A et al. Dysfunction of dopamine release in the prefrontal cortex of dysbindin deficient sandy mice, an in vivo microdialysis study. Neurosci. Lett. 470(2), 134-138 (2010).
52. Cox MM, Tucker AM, Tang J et al. Neurobehavioral abnormalities in the dysbindin-1 mutant, sandy, on a C57BL/6J genetic background. Genes Brain Behav. 8(4), 390-397 (2009).
53. Ji Y, Yang F, Papaleo F et al. Role of dysbindin in dopamine receptor trafficking and cortical GABA function. Proc. Natl Acad. Sci. USA 106(46), 19593-19598 (2009).
54. Papaleo F, Yang F, Garcia S et al. Dysbindin-1 modulates prefrontal cortical activity and schizophrenia-like behaviors via dopamine/D2 pathways. Mol. Psychiatry DOI: 10.1038/mp.2010.106 (2010) (Epub ahead of print).
55. Carlisle HJ, Fink AE, Grant SG, O'Dell TJ. Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J. Physiol. 586(Pt 24), 5885-5900 (2008).
56. Garry EM, Moss A, Delaney A et al. Neuropathic sensitization of behavioral reflexes and spinal NMDA receptor/CaM kinase II interactions are disrupted in PSD-95 mutant mice. Curr. Biol. 13(4), 321-328 (2003).
57. Migaud M, Charlesworth P, Dempster M et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396(6710), 433-439 (1998).
58. Davis RE, Swiderski RE, Rahmouni K et al. A knockin mouse model of the Bardet-Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity. Proc. Natl Acad. Sci. USA 104(49), 19422-19427 (2007). nn Mice harboring a genetic mutation observed in human patients show a number of disease-related phenotypes. Knocking in a known disease-associated genetic sequence variant is arguably the most valid means of modeling human disease in a mouse.
59. Seo S, Guo DF, Bugge K, Morgan DA, Rahmouni K, Sheffield VC. Requirement of Bardet-Biedl syndrome proteins for leptin receptor signaling. Hum. Mol. Genet. 18(7), 1323-1331 (2009).
60. Eichers ER, Abd-El-Barr MM, Paylor R et al. Phenotypic characterization of Bbs4 null mice reveals age-dependent penetrance and variable expressivity. Hum. Genet. 120(2), 211-226 (2006).
61. Kulaga HM, Leitch CC, Eichers ER et al. Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat. Genet. 36(9), 994-998 (2004).
62. Li YF, Cheng YF, Huang Y et al. Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J. Neurosci. 31(1), 172-183 (2011).
63. Pramparo T, Libiger O, Jain S et al. Global developmental gene expression and pathway analysis of normal brain development and mouse models of human. Neuronal migration defects. PLoS Genet. 7(3), E1001331 (2011).
64. Sekiguchi H, Iritani S, Habuchi C et al. Impairment of the tyrosine hydroxylase neuronal network in the orbitofrontal cortex of a genetically modified mouse model of schizophrenia. Brain Res. 1392, 47-53 (2011).
65. Sasaki S, Mori D, Toyo-oka K et al. Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol. Cell Biol. 25(17), 7812-7827 (2005).
66. Youn YH, Pramparo T, Hirotsune S, Wynshaw-Boris A. Distinct dose-dependent cortical neuronal migration and neurite extension defects in Lis1 and Ndel1 mutant mice. J. Neurosci. 29(49), 15520-15530 (2009).
67. Wang Y, Baraban SC. Granule cell dispersion and aberrant neurogenesis in the adult hippocampus of an Lis1 mutant mouse. Dev. Neurosci. 29(1-2), 91-98 (2007).
68. Wang Y, Baraban SC. Aberrant dentate gyrus cytoarchitecture and fiber lamination in Lis1 mutant mice. Hippocampus 18(8), 758-765 (2008).
69. Nasrallah IM, McManus MF, Pancoast MM, Wynshaw-Boris A, Golden JA. Analysis of non-radial interneuron migration dynamics and its disruption in Lis1+/- mice. J. Comp. Neurol. 496(6), 847-858 (2006).
70. Feng Y, Walsh CA. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44(2), 279-293 (2004).
71. Fukuda T, Sugita S, Inatome R, Yanagi S. CAMDI, a novel disrupted in schizophrenia 1 (DISC1)-binding protein, is required for radial migration. J. Biol. Chem. 285(52), 40554-40561 (2010).
72. Ma X, Fei E, Fu C, Ren H, Wang G. Dysbindin-1, a schizophrenia-related protein, facilitates neurite outgrowth by promoting the transcriptional activity of p53. Mol. Psychiatry 73(4), 287-293 (2011).
73. Nihonmatsu-Kikuchi N, Hashimoto R, Hattori S et al. Reduced rate of neural differentiation in the dentate gyrus of adult dysbindin null (sandy) mouse. PLoS One 2011 6(1), E15886 (2011).
74. Vickers CA, Stephens B, Bowen J, Arbuthnott GW, Grant SG, Ingham CA. Neurone specific regulation of dendritic spines in vivo by post synaptic density 95 protein (PSD-95). Brain Res. 1090(1), 89-98 (2006).
75. Ishizuka K, Kamiya A, Oh EC et al. DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature 473(7345), 92-96 (2011). nn Elegant report demonstrating a functional post-translational modification of DISC1.
76. Enomoto A, Asai N, Namba T et al. Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63(6), 774-787 (2009).
77. Millar JK, Christie S, Anderson S et al. Genomic structure and localisation within a linkage hotspot of disrupted in schizophrenia 1, a gene disrupted by a translocation segregating with schizophrenia. Mol. Psychiatry 6(2), 173-178 (2001).
78. Taylor MS, Devon RS, Millar JK, Porteous DJ. Evolutionary constraints on the disrupted in schizophrenia locus. Genomics 81(1), 67-77 (2003).
79. Millar JK, Pickard BS, Mackie S et al. DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 310(5751), 1187-1191 (2005).
80. Zhou X, Geyer MA, Kelsoe JR. Does disrupted-in-schizophrenia (DISC1) generate fusion transcripts? Mol. Psychiatry 3(4), 361-363 (2008).
81. Brandon NJ, Millar JK, Korth C, Sive H, Singh KK, Sawa A. Understanding the role of DISC1 in psychiatric disease and during normal development. J. Neurosci. 29(41), 12768-12775 (2009).
82. Millar JK, Christie S, Semple CA, Porteous DJ. Chromosomal location and genomic structure of the human translin-associated factor X gene (TRAX; TSNAX) revealed by intergenic splicing to DISC1, a gene disrupted by a translocation segregating with schizophrenia. Genomics 67(1), 69-77 (2000).
83. Fatemi SH, Folsom TD. The neurodevelopmental hypothesis of schizophrenia, revisited Schizophr. Bull. 35(3), 528-548 (2009).
84. Hayashi-Takagi A, Sawa A. Disturbed synaptic connectivity in schizophrenia: Convergence of genetic risk factors during neurodevelopment. Brain Res. Bull. 83(3-4), 140-146 (2010).
85. Kelly MP, Stein JM, Vecsey CG et al. Developmental etiology for neuroanatomical and cognitive deficits in mice overexpressing Gas, a G-protein subunit genetically linked to schizophrenia. Mol. Psychiatry 14(4), 398-415 (2009). n Highly intricate series of studies employing a tetracycline-regulated mouse model to demonstrate that some schizophrenia-like phenotypes were due to developmental perturbation, whereas others were due to acute disruption in the adult.
86. Brown AS, Derkits EJ. Prenatal infection and schizophrenia: A review of epidemiologic and translational studies. Am. J. Psychiatry 167(3), 261-280 (2010).
87. Jaaro-Peled H, Ayhan Y, Pletnikov MV, Sawa A. Review of pathological hallmarks of schizophrenia: Comparison of genetic models with patients and nongenetic models. Schizophr. Bull. 36(2), 301-313 (2010).
88. Kalkstein S, Hurford I, Gur RC. Neurocognition in schizophrenia. Curr. Top. Behav. Neurosci. 4, 373-390 (2010).
89. Volk DW, Lewis DA. Prefrontal cortical circuits in schizophrenia Curr. Top. Behav. Neurosci. 4, 485-508 (2010).
90. Heinz A, Schlagenhauf F. Dopaminergic dysfunction in schizophrenia: Salience attribution revisited. Schizophr. Bull. 36(3), 472-485 (2010).
91. Meisenzahl EM, Schmitt GJ, Scheuerecker J, Möller HJ. The role of dopamine for the pathophysiology of schizophrenia. Int. Rev. Psychiatry 19(4), 337-345 (2007).