European Neuropsychopharmacology
Volume 20, Issue 5 , Pages 288-300 , May 2010

Differential gene expression in a rat model of depression based on persistent differences in exploratory activity

  • Aet Alttoa

      Affiliations

    • Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410 Tartu, Estonia
  • ,
  • Kadri Kõiv

      Affiliations

    • Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410 Tartu, Estonia
  • ,
  • Timothy A. Hinsley

      Affiliations

    • Department of Computer Science, University of Manchester, Manchester M13 9PL, United Kingdom
  • ,
  • Andrew Brass

      Affiliations

    • Department of Computer Science, University of Manchester, Manchester M13 9PL, United Kingdom
  • ,
  • Jaanus Harro

      Affiliations

    • Department of Psychology, Estonian Centre of Behavioural and Health Sciences, University of Tartu, Tiigi 78, 50410 Tartu, Estonia
    • Corresponding Author InformationCorresponding author. Tel.: +372 7 375 911; fax: +372 7 376 152.

Received 20 May 2009 ,Revised 18 September 2009 ,Accepted 28 September 2009.

References 

  1. Ackermann TF, Hortnagl H, Wolfer DP, Colacicco G, Sohr R, Lang F, et al. Phosphatidylinositide dependent kinase deficiency increases anxiety and decreases GABA and serotonin abundance in the amygdala. Cell. Physiol. Biochem. 2008;22:735–744
  2. Alfonso J, Aguero F, Sanchez DO, Flugge G, Fuchs E, Frasch AC, et al. Gene expression analysis in the hippocampal formation of tree shrews chronically treated with cortisol. J. Neurosci. Res. 2004;78:702–710
  3. Alttoa A, Kõiv K, Eller M, Uustare A, Rinken A, Harro J. Effects of low dose N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine administration on exploratory and amphetamine-induced behavior and dopamine D2 receptor function in rats with high or low exploratory activity. Neuroscience. 2005;132:979–990
  4. Alttoa A, Eller M, Herm L, Rinken A, Harro J. Amphetamine-induced locomotion, behavioral sensitization to amphetamine, and striatal D2 receptor function in rats with high or low spontaneous exploratory activity: differences in the role of locus coeruleus. Brain Res. 2007;1131:138–148
  5. Alttoa A, Seeman P, Kõiv K, Eller M, Harro J. Rats with persistently high exploratory activity have both higher extracellular dopamine levels and higher proportion of D(2) (High) receptors in the striatum. Synapse. 2009;63:443–446
  6. Beaulieu JM. Not only lithium: regulation of glycogen synthase kinase-3 by antipsychotics and serotonergic drugs. Int. J. Neuropsychopharmacol. 2007;10:3–6
  7. Beaulieu JM, Zhang X, Rodriguiz RM, Sotnikova TD, Cools MJ, Wetsel WC, et al. Role of GSK3 beta in behavioral abnormalities induced by serotonin deficiency. Proc. Natl. Acad. Sci. U. S. A. 2008;105:1333–1338
  8. Beechey CV, Cattanach BM, Blake A, Peters J. MRC Harwell, Oxfordshire World Wide Web Site—Mouse Imprinting Data and References. http://www.har.mrc.ac.uk/research/genomic_imprinting/2008;
  9. Bhansali P, Dunning J, Singer SE, David L, Schmauss C. Early life stress alters adult serotonin 2C receptor pre-mRNA editing and expression of the alpha subunit of the heterotrimeric G-protein G q. J. Neurosci. 2007;27:1467–1473
  10. Blundell J, Tabuchi K, Bolliger MF, Blaiss CA, Brose N, Liu X, et al. Increased anxiety-like behavior in mice lacking the inhibitory synapse cell adhesion molecule neuroligin 2. Genes Brain Behav. 2009;8:114–126
  11. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics. 2003;19:185–193
  12. Boothman L, Raley J, Denk F, Hirani E, Sharp T. In vivo evidence that 5-HT2C receptors inhibit 5-HT neuronal activity via a GABAergic mechanism. Br. J. Pharmacol. 2006;149:861–869
  13. Bouras C, Kovari E, Hof PR, Riederer BM, Giannakopoulos P. Anterior cingulate cortex pathology in schizophrenia and bipolar disorder. Acta Neuropathol. 2001;102:373–379
  14. Boyce-Rustay JM, Holmes A. Genetic inactivation of the NMDA receptor NR2A subunit has anxiolytic- and antidepressant-like effects in mice. Neuropsychopharmacology. 2006;31:2405–2414
  15. Catania EH, Pimenta A, Levitt P. Genetic deletion of Lsamp causes exaggerated behavioral activation in novel environments. Behav. Brain Res. 2008;188:380–390
  16. Chen J-T, Lu D-H, Chia C-P, Ruan D-Y, Sabapathy K, Xiao Z-C. Impaired long-term potentiation in c-Jun N-terminal kinase 2-deficient mice. J. Neurochem. 2005;93:463–473
  17. Ciani L, Salinas PC. WNTS in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 2005;6:351–362
  18. Cinar R, Freund TF, Katona I, Mackie K, Szucs M. Reciprocal inhibition of G-protein signaling is induced by CB1 cannabinoid and GABAB receptor interactions in rat hippocampal membranes. Neurochem. Int. 2008;52:1402–1409
  19. Clemett DA, Punhani TS, Duxon M, Blackburn TP, Fone KCF. Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology. 2000;39:123–132
  20. Coppe A, Danieli GA, Bortoluzzi S. REEF: searching regionally enriched features in genomes. BMC Bioinformatics. 2006;7:453
  21. Deakin JFW. 5-HT, antidepressant drugs and the psychosocial origins of depression. J. Psychopharmacol. 1996;10:31–38
  22. Diehl LA, Silveira PP, Leite MC, Crema LM, Portella AK, Billodre MN, et al. Long lasting sex-specific effects upon behavior and S100b levels after maternal separation and exposure to a model of post-traumatic stress disorder in rats. Brain Res. 2007;1144:107–116
  23. Dierssen M, Gratacos M, Sahun I, Martin M, Gallego X, Amador-Arjona A, et al. Transgenic mice overexpressing the full-length neurotrophin receptor TrkC exhibit increased catecholaminergic neuron density in specific brain areas and increased anxiety-like behavior and panic reaction. Neurobiol. Dis. 2006;24:403–418
  24. Dunning MJ, Smith ML, Ritchie ME, Tavare S. beadarray: R classes and methods for Illumina bead-based data. Bioinformatics. 2007;23:2184–2185
  25. Fan Y, Zhang J, Sun XL, Gao L, Zeng XN, Ding JH, et al. Sex- and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice. J. Neurosci. Res. 2005;82:458–464
  26. Feng Y, Vetro A, Kiss E, Kapornai K, Daroczi G, Mayer L, et al. Association of the neurotrophic tyrosine kinase receptor 3 (NTRK3) gene and childhood-onset mood disorders. Am. J. Psychiatry. 2008;165:610–616
  27. Frame S, Cohen P. GSK3 takes centre stage more than 20years after its discovery. Biochem. J. 2001;359:1–16
  28. Garcia-Garcia AL, Elizalde N, Matrov D, Harro J, Wojcik SM, Venzala E, et al. Increased vulnerability to depressive-like behavior of mice with decreased expression of VGLUT1. Biol. Psychiatry. 2009;2009(66):275–282
  29. Gottschalk WA, Jiang H, Tartaglia N, Feng L, Figurov A, Lu B. Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn. Mem. 1999;6:243–256
  30. Gould TD, Chen G, Manji HK. In vivo evidence in the brain for lithium inhibition of glycogen synthase kinase-3. Neuropsychopharmacology. 2003;29:32–38
  31. Gould TD, Dow ER, O'Donnell KC, Chen G, Manji HK. Targeting signal transduction pathways in the treatment of mood disorders: recent insights into the relevance of the Wnt pathway. CNS Neurol. Disord. Drug Targets. 2007;6:193–204
  32. Gould TD, Einat H, O'Donnell KC, Picchini AM, Schloesser RJ, Manji HK. [beta]-Catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology. 2007;32:2173–2183
  33. Gould TD, O'Donnell KC, Picchini AM, Dow ER, Chen G, Manji HK. Generation and behavioral characterization of [beta]-catenin forebrain-specific conditional knock-out mice. Behav. Brain Res. 2008;189:117–125
  34. Griebel G. 5-hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30years of research. Pharmacol. Ther. 1995;65:319–395
  35. Haller J, Varga B, Ledent C, Barna I, Freund TF, Matyas F, et al. Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice. Eur. J. Neurosci. 2004;19:1906–1912
  36. Haller JA, Varga BA, Ledent CB, Freund TFA. CB1 cannabinoid receptors mediate anxiolytic effects: convergent genetic and pharmacological evidence with CB1-specific agents. Behav. Pharmacol. 2004;15:299–304
  37. Haller J, Matyas F, Soproni K, Varga B, Barsy B, Nemeth B, et al. Correlated species differences in the effects of cannabinoid ligands on anxiety and on GABAergic and glutamatergic synaptic transmission. Eur. J. Neurosci. 2007;25:2445–2456
  38. Harro J. Measurement of exploratory behaviour in rodents. In:  Conn RA editors. Methods in Neurosciences. vol. 14:San Diego: Academic Press; 1993;p. 359–377
  39. Harro J, Oreland L, Vasar E, Bradwejn J. Impaired exploratory behaviour after DSP-4 treatment in rats: implications for the increased anxiety after noradrenergic denervation. Eur. Neuropsychopharmacol. 1995;5:447–455
  40. Heasley LE, Storey B, Fanger GR, Butterfield L, Zamarripa J, Blumberg D, et al. GTPase-deficient G alpha 16 and G alpha q induce PC12 cell differentiation and persistent activation of cJun NH2-terminal kinases. Mol. Cell. Biol. 1996;16:648–656
  41. Heisler LK, Zhou L, Bajwa P, Hsu J, Tecott LH. Serotonin 5-HT2C receptors regulate anxiety-like behavior. Genes Brain Behav. 2007;6:491–496
  42. Herdegen T, Mielke K, Kallunki T. Review : c-Jun and the c-Jun amino-terminal kinases: bipotential components of the neuronal stress response. Neuroscientist. 1999;5:147–154
  43. Hino S-I, Kishida S, Michiue T, Fukui A, Sakamoto I, Takada S, et al. Inhibition of the Wnt signaling pathway by Idax, a novel Dvl-binding protein. Mol. Cell. Biol. 2001;21:330–342
  44. Hooks MS, Colvin AC, Juncos JL, Justice JB. Individual differences in basal and cocaine-stimulated extracellular dopamine in the nucleus accumbens using quantitative microdialysis. Brain Res. 1992;587:306–312
  45. Huang da W, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, et al. DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acid Res. 2007;35:W169–175
  46. Hurst LD, Pál C, Lercher MJ. The evolutionary dynamics of eukaryotic gene order. Nat. Rev., Genet. 2004;299–310
  47. Kabbaj M. Individual differences in vulnerability to drug abuse: the high responders/low responders model. CNS Neurol. Disord. Drug Targets. 2006;5:513–520
  48. Kalueff AV, Nutt DJ. Role of GABA in anxiety and depression. Depress. Anxiety. 2007;24:495–517
  49. Kantor S, Anheuer ZE, Bagdy G. High social anxiety and low aggression in Fawn-Hooded rats. Physiol. Behav. 2000;71:551–557
  50. Kantor S, Graf M, Anheuer ZE, Bagdy G. Rapid desensitization of 5-HT1A receptors in Fawn-Hooded rats after chronic fluoxetine. Eur. Neuropsychopharmacol. 2001;11:15–24
  51. Khawaja X, Xu J, Liang JJ, Barrett JE. Proteomic analysis of protein changes developing in rat hippocampus after chronic antidepressant treatment: implications for depressive disorders and future therapies. J. Neurosci. Res. 2004;75:451–460
  52. Kleppisch T, Voigt V, Allmann R, Offermanns S. G(alpha)q-deficient mice lack metabotropic glutamate receptor-dependent long-term depression but show normal long-term potentiation in the hippocampal CA1 region. J. Neurosci. 2001;21:4943–4948
  53. Kong H, Sha LL, Fan Y, Xiao M, Ding JH, Wu J, et al. Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis. Neuropsychopharmacology. 2009;34:1263–1276
  54. Landgraf R, Wigger A. High vs low anxiety-related behavior rats: an animal model of extremes in trait anxiety. Behav. Genetics. 2002;32:301–314
  55. Lesch KP, Gutknecht L. Focus on the 5-HT1A receptor: emerging role of a gene regulatory variant in psychopathology and pharmacogenetics. Int. J. Neuropsychopharmacol. 2004;7:381–385
  56. Lesch KP, Hough CJ, Aulakh CS, Wolozin BL, Tolliver TJ, Hill JL, et al. Fluoxetine modulates G protein alpha s, alpha q, and alpha 12 subunit mRNA expression in rat brain. Eur. J. Pharmacol. 1992;227:233–237
  57. Leussis MP, Andersen SL. Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse. 2008;62:22–30
  58. Li Q, Wichems CH, Ma L, Van de Kar LD, Garcia F, Murphy DL. Brain region-specific alterations of 5-HT2A and 5-HT2C receptors in serotonin transporter knockout mice. J. Neurochem. 2003;84:1256–1265
  59. Li X, Zhu W, Roh MS, Friedman AB, Rosborough K, Jope RS. In vivo regulation of glycogen synthase kinase-3beta (GSK-3beta) by serotonergic activity in mouse brain. Neuropsychopharmacology. 2004;29:1426–1431
  60. Li F, Chong ZZ, Maiese K. Vital elements of the Wnt–Frizzled signaling pathway in the nervous system. Curr. Neurovasc. Res. 2005;2:331–340
  61. Li Z, Gao L, Liu Q, Cao C, Sun XL, Ding JH, et al. Aquaporin-4 knockout regulated cocaine-induced behavior and neurochemical changes in mice. Neurosci. Lett. 2006;403:294–298
  62. Li X, Rosborough KM, Friedman AB, Zhu W, Roth KA. Regulation of mouse brain glycogen synthase kinase-3 by atypical antipsychotics. Int. J. Neuropsychopharmacol. 2007;10:7–19
  63. Liu R, Jolas T, Aghajanian G. Serotonin 5-HT2 receptors activate local GABA inhibitory inputs to serotonergic neurons of the dorsal raphe nucleus. Brain Res. 2000;873:34–45
  64. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004;20:781–810
  65. Ma XM, Kiraly DD, Gaier ED, Wang Y, Kim EJ, Levine ES, et al. Kalirin-7 is required for synaptic structure and function. J. Neurosci. 2008;28:12368–12382
  66. Ma XM, Wang Y, Ferraro F, Mains RE, Eipper BA. Kalirin-7 is an essential component of both shaft and spine excitatory synapses in hippocampal interneurons. J Neurosci. 2008;28:711–724
  67. Mällo T, Alttoa A, Kõiv K, Tõnissaar M, Eller M, Harro J. Rats with persistently low or high exploratory activity: behaviour in tests of anxiety and depression, and extracellular levels of dopamine. Behav. Brain Res. 2007;177:269–281
  68. Mällo T, Kõiv K, Koppel I, Raudkivi K, Uustare A, Rinken A, et al. Regulation of extracellular serotonin levels and brain-derived neurotrophic factor in rats with high and low exploratory activity. Brain Res. 2008;1194:110–117
  69. Margis R, Zanatto VC, Tramontina F, Vinade E, Lhullier F, Portela LV, et al. Changes in S100B cerebrospinal fluid levels of rats subjected to predator stress. Brain Res. 2004;1028:213–218
  70. Matrov D, Kolts I, Harro J. Cerebral oxidative metabolism in rats with high and low exploratory activity. Neurosci. Lett. 2007;413:154–158
  71. Menard J, Treit D. Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci. Biobehav. Rev. 1999;23:591–613
  72. Nelovkov A, Philips MA, Koks S, Vasar E. Rats with low exploratory activity in the elevated plus-maze have the increased expression of limbic system-associated membrane protein gene in the periaqueductal grey. Neurosci. Lett. 2003;352:179–182
  73. Novak G, Seeman P, Tallerico T. Increased expression of calcium/calmodulin-dependent protein kinase IIbeta in frontal cortex in schizophrenia and depression. Synapse. 2006;59:61–68
  74. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999;27:29–34
  75. Otter MH, Matto V, Sõukand R, Skrebuhhova T, Allikmets L, Harro J. Characterization of rat exploratory behavior using the exploration box test. Methods Find. Exp. Clin. Pharmacol. 1997;19:683–691
  76. Parks CL, Robinson PS, Sibille E, Shenk T, Toth M. Increased anxiety of mice lacking the serotonin1A receptor. Proc. Natl. Acad. Sci. 1998;95:10734–10739
  77. Pawlak CR, Ho Y-J, Schwarting RKW. Animal models of humans psychopathology based on individual differences in novelty-seeking and anxiety. Neurosci. Biobehav. Rev. 2008;32:1544–1568
  78. Peineau S, Bradley C, Taghibiglou C, Doherty A, Bortolotto ZA, Wang YT, et al. The role of GSK-3 in synaptic plasticity. Br. J. Pharmacol. 2008;153:S428–S437
  79. Peters J, Beechey C. Identification and characterisation of imprinted genes in the mouse. Brief Funct. Genomic Proteomic. 2004;2:320–333
  80. Piazza PV, Deminiere JM, Le Moal M, Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science. 1989;245:1511–1513
  81. Qi H, Ma J, Liu YM, Yang L, Peng L, Wang H, et al. Allostatic tumor-burden induces depression-associated changes in hepatoma-bearing mice. J. Neuro-oncol. 2009;94:367–372
  82. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene. 2007;26:3100–3112
  83. Ramboz S, Oosting R, Amara DA, Kung HF, Blier P, Mendelsohn M, et al. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. 1998;95:14476–14481
  84. Rattray M, Liu X, Sanguinetti G, Milo M, Lawrence ND. Propagating uncertainty in microarray data analysis. Brief. Bioinfomatics. 2006;7:37–47
  85. Rothermundt M, Peters M, Prehn JH, Arolt V. S100B in brain damage and neurodegeneration. Microsc. Res. Tech. 2003;60:614–632
  86. Rouge-Pont F, Deroche V, Le Moal M, Piazza PV. Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone. Eur. J. Neurosci. 1998;10:3903–3907
  87. Sahún I, Gallego X, Gratacos M, Murtra P, Trullas R, Maldonado R, et al. Differential responses to anxiogenic drugs in a mouse model of panic disorder as revealed by Fos immunocytochemistry in specific areas of the fear circuitry. Amino Acids. 2007;33:677–688
  88. Sanacora G, Zarate CA, Krystal JH, Manji HK. Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat. Rev., Drug Discov. 2008;7:426–437
  89. Scaccianoce S, Del Bianco P, Pannitteri G, Passarelli F. Relationship between stress and circulating levels of S100B protein. Brain Res. 2004;1004:208–211
  90. Serrats J, Mengod G, Cortés R. Expression of serotonin 5-HT2C receptors in GABAergic cells of the anterior raphe nuclei. J. Chem. Neuroanat. 2005;29:83–91
  91. Shiah IS, Yatham LN. GABA function in mood disorders: an update and critical review. Life Sci. 1998;63:1289–1303
  92. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 2002;22:3251–3261
  93. Sweatt JD. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 2001;76:1–10
  94. Takamori S. VGLUTs: ‘exciting’ times for glutamatergic research?. Neurosci. Res. 2006;55:343–351
  95. Tordera RM, Totterdell S, Wojcik SM, Brose N, Elizalde N, Lasheras B, et al. Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur. J. Neurosci. 2007;25:281–290
  96. Toth M. 5-HT1A receptor knockout mouse as a genetic model of anxiety. Eur. J. Pharmacol. 2003;463:177–184
  97. Urigüen L, Arteta D, Diez-alarcia R, Ferrer-Alcon M, Diaz A, Pazos A, et al. Gene expression patterns in brain cortex of three different animal models of depression. Genes Brain Behav. 2008;7:649–658
  98. Varoqueaux F, Jamain S, Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell. Biol. 2004;83:449–456
  99. Wang H, Zhu YZ, Wong PT, Farook JM, Teo AL, Lee LK, et al. cDNA microarray analysis of gene expression in anxious PVG and SD rats after cat-freezing test. Exp. Brain Res. 2003;149:413–421
  100. White DA, Kalinichev M, Holtzman SG. Locomotor response to novelty as a predictor of reactivity to aversive stimuli in the rat. Brain Res. 2007;1149:141–148
  101. Wright DE, Seroogy KB, Lundgren KH, Davis BM, Jennes L. Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J. Comp. Neurol. 1995;351:357–373
  102. Zaheer A, Weiss JL, Goyal P, Lim R. Enhanced expression of neurotrophic factors by C6 rat glioma cells after transfection with glia maturation factor. Neurosci. Lett. 1999;265:203–206
  103. Zhang X, Beaulieu J-M, Sotnikova TD, Gainetdinov RR, Caron MG. Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science. 2004;305:217
  104. Zhang X, Gainetdinov RR, Beaulieu J-M, Sotnikova TD, Burch LH, Williams RB, et al. Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron. 2005;45:11–16

PII: S0924-977X(09)00235-1

doi: 10.1016/j.euroneuro.2009.09.005

European Neuropsychopharmacology
Volume 20, Issue 5 , Pages 288-300 , May 2010