Phenotypic characterization of transgenic mice overexpressing neuregulin-1

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Kato, Taisuke ^a   Kasai, Atsushi ^b   Mizuno, Makoto ^a   Fengyi, Liang ^c   Shintani, Norihito ^d   Maeda, Sadaaki ^b   Yokoyama, Minesuke ^a   Ozaki, Miwako ^e,f   Nawa, Hiroyuki ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b SETSUNAN UNIVERSITY   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d OSAKA UNIVERSITY   (Japan)

^e WASEDA UNIVERSITY   (Japan)

^f Waseda University   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; COMPLEMENTARY DNA; DOPAMINE; ELONGATION FACTOR 1ALPHA; GREEN FLUORESCENT PROTEIN; MYELIN BASIC PROTEIN; NEU DIFFERENTIATION FACTOR; PARVALBUMIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; FEAR; FRONTAL CORTEX; GABAERGIC SYSTEM; GENE OVEREXPRESSION; HIPPOCAMPUS; KNOCKOUT MOUSE; LOCOMOTION; MALE; MOUSE; MYELINATION; NEUROCHEMISTRY; NONHUMAN; PHENOTYPIC VARIATION; PREPULSE INHIBITION; SCHIZOPHRENIA; SCORING SYSTEM; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; SOCIAL ISOLATION; TRANSGENIC MOUSE; ALTERNATIVE RNA SPLICING; ANIMAL; CYTOLOGY; FRONTAL LOBE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; GLIA; HETEROZYGOTE; METABOLISM; MUTATION; PATHOLOGY; PHENOTYPE; PROMOTER REGION;

MUS; MUS MUSCULUS;

ALTERNATIVE SPLICING; ANIMALS; DNA, COMPLEMENTARY; DOPAMINE; FRONTAL LOBE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; MICE; MICE, TRANSGENIC; MUTATION; NEUREGULIN-1; NEUROGLIA; PHENOTYPE; PROMOTER REGIONS, GENETIC;

EID: 78650083166     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014185     Document Type: Article

References (57)

1. Stefansson H, Sarginson J, Kong A, Yates P, Steinthorsdottir V, et al. (2003) Association of neuregulin 1 with schizophrenia confirmed in a Scottish population. Am J Hum Genet 72: 83-87.
2. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71: 877-892.
3. Li D, Collier DA, He L (2006) Meta-analysis shows strong positive association of the neuregulin 1 (NRG1) gene with schizophrenia. Hum Mol Genet 15: 1995-2002.
4. Chen YJ, Johnson MA, Lieberman MD, Goodchild RE, Schobel S, et al. (2008) Type III neuregulin-1 is required for normal sensorimotor gating, memoryrelated behaviors, and corticostriatal circuit components. J Neurosci 28: 6872-6883.
5. Ehrlichman RS, Luminais SN, White SL, Rudnick ND, Ma N, et al. (2009) Neuregulin 1 Transgenic Mice Display Reduced Mismatch Negativity, Contextual Fear Conditioning and Social Interactions. Brain Res 1294: 116-127.
6. Gerlai R, Pisacane P, Erickson S (2000) Heregulin, but not ErbB2 or ErbB3, heterozygous mutant mice exhibit hyperactivity in multiple behavioral tasks. Behav Brain Res 109: 219-227.
7. Karl T, Duffy L, Scimone A, Harvey RP, Schofield PR (2007) Altered motor activity, exploration and anxiety in heterozygous neuregulin 1 mutant mice: implications for understanding schizophrenia. Genes Brain Behav 6: 677-687.
8. O'Tuathaigh CM, O'Sullivan GJ, Kinsella A, Harvey RP, Tighe O, et al. (2006) Sexually dimorphic changes in the exploratory and habituation profiles of heterozygous neuregulin-1 knockout mice. Neuroreport 17(1): 79-83.
9. O'Tuathaigh CM, Babovic D, O'Meara G, Clifford JJ, Croke DT, et al. (2007a) Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour. Neurosci Biobehav Rev 31(1): 60-78.
10. O'Tuathaigh CM, Babovic D, O'Sullivan GJ, Clifford JJ, Tighe O, et al. (2007b) Phenotypic characterization of spatial cognition and social behavior in mice with 'knockout' of the schizophrenia risk gene neuregulin 1. Neuroscience 147: 18-27.
11. O'Tuathaigh CM, O'Connor AM, O'Sullivan GJ, Lai D, Harvey R, et al. (2008) Disruption to social dyadic interactions but not emotional/anxiety-related behaviour in mice with heterozygous 'knockout' of the schizophrenia risk gene neuregulin-1. Prog Neuropsychopharmacol Biol Psychiatry 32(2): 462-466.
12. Rimer M, Barrett DW, Maldonado MA, Vock VM, Gonzalez-Lima F (2005) Neuregulin-1 immunoglobulin-like domain mutant mice: clozapine sensitivity and impaired latent inhibition. Neuroreport 16: 271-275.
13. Van den Buuse M, Wischhof L, Xi Lee R, Martin S, Karl T (2009) Neuregulin 1 hypomorphic mutant mice: enhanced baseline locomotor activity but normal psychotropic drug-induced hyperlocomotion and prepulse inhibition regulation. Int J Neuropsychopharmacol 29: 1-11.
14. Harrison PJ, Law AJ (2006) Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 60: 132-140.
15. Mei L, Xiong WC (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9: 437-452.
16. Hashimoto R, Straub RE, Weickert CS, Hyde TM, Kleinman JE, et al. (2004) Expression analysis of neuregulin-1 in the dorsolateral prefrontal cortex in schizophrenia. Mol Psychiatry 9: 299-307.
17. Law AJ, Lipska BK, Weickert CS, Hyde TM, Straub RE, et al. (2006) Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 59 SNPs associated with the disease. Proc Natl Acad Sci U S A 103: 6747-6752.
18. Petryshen TL, Middleton FA, Kirby A, Aldinger KA, Purcell S, et al. (2005) Support for involvement of neuregulin 1 in schizophrenia pathophysiology. Mol Psychiatry 328: 366-74.
19. Lachman HM, Pedrosa E, Nolan KA, Glass M, Ye K, et al. (2006) Analysis of polymorphisms in AT-rich domains of neuregulin 1 gene in schizophrenia. Am J Med Genet B Neuropsychiatr Genet 141B(1): 102-9.
20. Chong VZ, Thompson M, Beltaifa S, Webster MJ, Law AJ, et al. (2008) Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr Res 100: 270-280.
21. Hahn CG, Wang HY, Cho DS, Talbot K, Gur RE, et al. (2006) Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nat Med 12: 824-828.
22. Ozaki M, Itoh K, Miyakawa Y, Kishida H, Hashikawa T (2004) Protein processing and releases of neuregulin-1 are regulated in an activity-dependent manner. J Neurochem 91: 176-88.
23. Brinkmann BG, Agarwal A, Sereda MW, Garratt AN, Müller T, et al. (2008) Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 59: 581-595.
24. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, et al. (2004) Shortand long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44: 251-261.
25. Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54: 583-597.
26. Ozaki M, Sasner M, Yano R, Lu HS, Buonanno A (1997) Neuregulin-beta induces expression of an NMDA-receptor subunit. Nature 390: 691-694.
27. Kato T, Abe Y, Sotoyama H, Kakita A, Kominami R, et al. (2010) Transient exposure of neonatal mice to neuregulin-1 results in hyperdopaminergic states in adulthood: implication in neurodevelopmental hypothesis for schizophrenia. Mol Psychiatry doi: 10.1038/mp.2010.10.
28. Neddens J, Buonanno A (2010) Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 20: 724-744.
29. Dickerson JW, Hemmerle AM, Numan S, Lundgren KH, Seroogy KB (2009) Decreased expression of ErbB4 and tyrosine hydroxylase mRNA and protein in the ventral midbrain of aged rats. Neuroscience 163: 482-489.
30. Zhang L, Fletcher-Turner A, Marchionni MA, Apparsundaram S, Lundgren KH, et al. (2004) Neurotrophic and neuroprotective effects of the neuregulin glial growth factor-2 on dopaminergic neurons in rat primary midbrain cultures. J Neurochem 91: 1358-1368.
31. Arguello PA, Gogos JA (2006) Modeling madness in mice: one piece at a time. Neuron 52: 179-196.
32. Sams-Dodd F (1995) Distinct effects of d-amphetamine and phencyclidine on the social behaviour of rats. Behav Pharmacol 6: 55-65.
33. Sams-Dodd F (1996) Phencyclidine-induced stereotyped behaviour and social isolation in rats: a possible animal model of schizophrenia. Behav Pharmacol 7: 3-23.
34. Clemens KJ, Van Nieuwenhuyzen PS, Li KM, Cornish JL, Hunt GE, et al. (2004) MDMA ("ecstasy"), methamphetamine and their combination: long-term changes in social interaction and neurochemistry in the rat. Psychopharmacology (Berl) 173: 318-325.
35. Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325: 1017-1020.
36. Prevot V, Rio C, Cho GJ, Lomniczi A, Heger S, et al. (2003) Normal female sexual development requires neuregulin-erbB receptor signaling in hypothalamic astrocytes. J Neurosci 23: 230-239.
37. Golub MS, Germann SL, Lloyd KC (2004) Behavioral characteristics of a nervous system-specific erbB4 knock-out mouse. Behav Brain Res 153: 159-170.
38. Deakin IH, Law AJ, Oliver PL, Schwab MH, Nave KA, et al. (2009) Behavioural characterization of neuregulin 1 type I overexpressing transgenic mice. Neuroreport 20: 1523-1528.
39. Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y, et al. (2008) ErbB4- neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem 283: 32944-32956.
40. López-Bendito G, Cautinat A, Sánchez JA, Bielle F, Flames N, et al. (2006) Tangential Neuronal Migration Controls Axon Guidance: A Role for Neuregulin-1 in Thalamocortical Axon Navigation. Cell 125: 127-142.
41. Roy K, Murtie JC, El-Khodor BF, Edgar N, Sardi SP, et al. (2007) Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci U S A 104: 8131-8136.
42. Davis KL, Stewart DG, Friedman JI, Buchsbaum M, Harvey PD, et al. (2003) White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 60: 443-456.
43. Eyles DW, McGrath JJ, Reynolds GP (2002) Neuronal calcium-binding proteins and schizophrenia. Schizophr Res 57: 27-34.
44. Akbarian S, Huang HS (2006) Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev 52: 293-304.
45. Abe Y, Namba H, Zheng Y, Nawa H (2009) In situ hybridization reveals developmental regulation of ErbB1-4 mRNA expression in mouse midbrain: implication of ErbB receptors for dopaminergic neurons. Neuroscience 161: 95-110.
46. Yurek DM, Zhang L, Fletcher-Turner A, Seroogy KB (2004) Supranigral injection of neuregulin1-beta induces striatal dopamine overflow. Brain Res 1028: 116-119.
47. Zheng Y, Watakabe A, Takada M, Kakita A, Namba H, et al. (2009) Expression of ErbB4 in substantia nigra dopamine neurons of monkeys and humans. Prog Neuropsychopharmacol Biol Psychiatry 33: 701-706.
48. Fumagalli F, Gainetdinov RR, Valenzano KJ, Caron MG (1998) Role of dopamine transporter in methamphetamine-induced neurotoxicity: evidence from mice lacking the transporter. J Neurosci 18: 4861-4869.
49. Volkow ND, Chang L, Wang GJ, Fowler JS, Franceschi D, et al. (2001) Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 21: 9414-9418.
50. Ozaki M, Tohyama K, Kishida H, Buonanno A, Yano R, et al. (2000) Roles of neuregulin in synaptogenesis between mossy fibers and cerebellar granule cells. J Neurosci Res 59: 612-623.
51. Meuer S, Wittwer C, Nakagawara K (2001) Rapid Cycle Real-Time PCR: Methods and Applications. Heidelberg: Springer Press. pp 21-34.
52. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, et al. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8: 711-713.
53. Karl T, Pabst R, von Hörsten S (2003) Behavioral phenotyping of mice in pharmacological and toxicological research. Exp Toxicol Pathol 55: 69-83.
54. Kasai A, Shintani N (2007) First screening for behavioral phenotype of geneengineered mice. Nippon Yakurigaku Zasshi 130: 281-285.
55. Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, et al. (2004) Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14: 557-569.
56. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98: 427-436.
57. Mizuno M, Sotoyama H, Narita E, Kawamura H, Namba H, et al. (2007) A cyclooxygenase-2 inhibitor ameliorates behavioral impairments induced by striatal administration of epidermal growth factor. J Neurosci 27: 10116-10127.