An association between the reduced levels of SLC1A2 and GAD1 in the dorsolateral prefrontal cortex in major depressive disorder: Possible involvement of an attenuated RAF/MEK/ERK signaling pathway

Journal of Neural Transmission

Volumn 121, Issue 7, 2014, Pages 783-792

  Oh, Dong Hoon ^a   Oh, Daeyoung ^d   Son, Hyeon ^a   Webster, Maree J ^b   Weickert, Cyndi S ^c   Kim, Seok Hyeon ^a  

^a Hanyang University   (South Korea)

^b Stanley Medical Research Institute   (United States)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^d CHA University   (South Korea)

Author keywords

Dorsolateral prefrontal cortex; Glutamate transporters; Glutamic acid decarboxylase; Major depressive disorder; MEK ERK pathway

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMATE DECARBOXYLASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; RAF PROTEIN; GLUTAMATE DECARBOXYLASE 1; GLUTAMATE TRANSPORTER; SLC1A2 PROTEIN, HUMAN;

ADULT; ARTICLE; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DATA BASE; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN TISSUE; MAJOR DEPRESSION; MALE; NEUROPATHOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STANLEY NEUROPATHOLOGY CONSORTIUM INTEGRATIVE DATABASE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; POSTMORTEM CHANGE;

ADULT; DEPRESSIVE DISORDER, MAJOR; FEMALE; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; POSTMORTEM CHANGES; PREFRONTAL CORTEX; RAF KINASES; RNA, MESSENGER;

EID: 84903274647     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-014-1189-z     Document Type: Article

References (48)

1. Alcaro A, Panksepp J, Witczak J, Hayes DJ, Northoff G (2010) Is subcortical-cortical midline activity in depression mediated by glutamate and GABA? A cross-species translational approach. Neurosci Biobehav Rev 34:592-605. doi:10.1016/j.neubiorev.2009.11.023
2. Almeida RD, Manadas BJ, Melo CV, Gomes JR, Mendes CS, Graos MM, Carvalho RF, Carvalho AP, Duarte CB (2005) Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 12:1329-1343. doi:10.1038/sj.cdd.4401662 (Pubitemid 41486103)
3. Banasr M, Chowdhury GM, Terwilliger R, Newton SS, Duman RS, Behar KL, Sanacora G (2010) Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry 15:501-511. doi:10.1038/mp.2008.106
4. Beart PM, O'Shea RD (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol 150:5-17. doi:10.1038/sj.bjp.0706949 (Pubitemid 46094664)
5. Bender R, Lange S (2001) Adjusting for multiple - when and how? J Clin Epidemiol 54:343-349. doi:10.1016/S0895-4356(00)00314-0
6. Choudary PV, Molnar M, Evans SJ, Tomita H, Li JZ, Vawter MP, Myers RM, Bunney WE Jr, Akil H, Watson SJ, Jones EG (2005) Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc Natl Acad Sci USA 102:15653-15658. doi:10.1073/pnas.0507901102 (Pubitemid 41528111)
7. Davidson RJ, Putnam KM, Larson CL (2000) Dysfunction in the neural circuitry of emotion regulation - a possible prelude to violence. Science 289:591-594. doi:10.1126/science.289.5479.591 (Pubitemid 30622056)
8. Duman CH, Schlesinger L, Kodama M, Russell DS, Duman RS (2007) A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment. Biol Psychiatry 61:661-670. doi:10.1016/j.biopsych.2006.05.047 (Pubitemid 46328865)
9. Dwivedi Y, Rizavi HS, Roberts RC, Conley RC, Tamminga CA, Pandey GN (2001) Reduced activation and expression of ERK1/2 MAP kinase in the post-mortem brain of depressed suicide subjects. J Neurochem 77:916-928. doi:10.1046/j.1471-4159.2001.00300.x (Pubitemid 32466788)
10. Dwivedi Y, Rizavi HS, Conley RR, Roberts RC, Tamminga CA, Pandey GN (2003) Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch Gen Psychiatry 60:804-815. doi:10.1001/archpsyc.60.8.804 (Pubitemid 36960912)
11. Dwivedi Y, Rizavi HS, Conley RR, Pandey GN (2006) ERK MAP kinase signaling in post-mortem brain of suicide subjects: differential regulation of upstream Raf kinases Raf-1 and B-Raf. Mol Psychiatry 11:86-98. doi:10.1038/sj.mp.4001744 (Pubitemid 43251091)
12. Dwivedi Y, Rizavi HS, Zhang H, Roberts RC, Conley RR, Pandey GN (2009) Aberrant extracellular signal-regulated kinase (ERK)1/2 signalling in suicide brain: role of ERK kinase 1 (MEK1). Int J Neuropsychopharmacol 12:1337-1354. doi:10.1017/S1461145709990575
13. Egan MF, Straub RE, Goldberg TE, Yakub I, Callicott JH, Hariri AR, Mattay VS, Bertolino A, Hyde TM, Shannon-Weickert C, Akil M, Crook J, Vakkalanka RK, Balkissoon R, Gibbs RA, Kleinman JE, Weinberger DR (2004) Variation in GRM3 affects cognition, prefrontal glutamate, and risk for schizophrenia. Proc Natl Acad Sci USA 101:12604-12609. doi:10.1073/pnas.0405077101 (Pubitemid 39122071)
14. Hashimoto R, Takei N, Shimazu K, Christ L, Lu B, Chuang DM (2002) Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: an essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology 43:1173-1179. doi:10.1016/S0028-3908(02)00217- 4 (Pubitemid 36009371)
15. Higgs BW, Elashoff M, Richman S, Barci B (2006) An online database for brain disease research. BMC Genom 7:70. doi:10.1186/1471-2164-7-70
16. Hu WH, Walters WM, Xia XM, Karmally SA, Bethea JR (2003) Neuronal glutamate transporter EAAT4 is expressed in astrocytes. Glia 44:13-25. doi:10.1002/glia.10268 (Pubitemid 37176316)
17. Karolewicz B, Maciag D, O'Dwyer G, Stockmeier CA, Feyissa AM, Rajkowska G (2010) Reduced level of glutamic acid decarboxylase-67 kDa in the prefrontal cortex in major depression. Int J Neuropsychopharmacol 13:411-420. doi:10.1017/S1461145709990587
18. Kim S, Webster MJ (2010) The stanley neuropathology consortium integrative database: a novel, web-based tool for exploring neuropathological markers in psychiatric disorders and the biological processes associated with abnormalities of those markers. Neuropsychopharmacology 35:473-482. doi:10.1038/npp.2009.151
19. Kim K, Lee SG, Kegelman TP, Su ZZ, Das SK, Dash R, Dasgupta S, Barral PM, Hedvat M, Diaz P, Reed JC, Stebbins JL, Pellecchia M, Sarkar D, Fisher PB (2011) Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: opportunities for developing novel therapeutics. J Cell Physiol 226:2484-2493. doi:10.1002/jcp.22609
20. Kim S, Zavitsanou K, Gurguis G, Webster MJ (2012) Neuropathology markers and pathways associated with molecular targets for antipsychotic drugs in postmortem brain tissues: exploration of drug targets through the stanley neuropathology integrative database. Eur Neuropsychopharmacol 22:683-694. doi:10.1016/j.euroneuro.2012.01.010
21. Koenigs M, Grafman J (2009) The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 201:239-243. doi:10.1016/j.bbr.2009.03.004
22. Lopez-Figueroa AL, Norton CS, Lopez-Figueroa MO, Armellini-Dodel D, Burke S, Akil H, Lopez JF, Watson SJ (2004) Serotonin 5-HT1A, 5-HT1B, and 5-HT2A receptor mRNA expression in subjects with major depression, bipolar disorder, and schizophrenia. Biol Psychiatry 55:225-233. doi:10.1016/j.biopsych.2003.09. 017 (Pubitemid 38117158)
23. McCubrey JA, Steelman LS, Abrams SL, Lee JT, Chang F, Bertrand FE, Navolanic PM, Terrian DM, Franklin RA, D'Assoro AB, Salisbury JL, Mazzarino MC, Stivala F, Libra M (2006) Roles of the RAF/MEK/ERK and PI3 K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul 46:249-279. doi:10.1016/j.advenzreg.2006.01.004 (Pubitemid 44301348)
24. Milham MP, Banich MT, Webb A, Barad V, Cohen NJ, Wszalek T, Kramer AF (2001) The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. Brain Res Cogn Brain Res 12:467-473. doi:10.1016/s0926-6410(01)00076-3 (Pubitemid 33022701)
25. Mueller HT, Meador-Woodruff JH (2004) NR3A NMDA receptor subunit mRNA expression in schizophrenia, depression and bipolar disorder. Schizophr Res 71:361-370. doi:10.1016/j.schres.2004.02.016 (Pubitemid 39330514)
26. Oh DH, Son H, Hwang S, Kim SH (2012) Neuropathological abnormalities of astrocytes, GABAergic neurons, and pyramidal neurons in the dorsolateral prefrontal cortices of patients with major depressive disorder. Eur Neuropsychopharmacol 22:330-338. doi:10.1016/j.euroneuro.2011.09.001
27. Pandey GN, Ren X, Rizavi HS, Conley RR, Roberts RC, Dwivedi Y (2008) Brain-derived neurotrophic factor and tyrosine kinase B receptor signalling in post-mortem brain of teenage suicide victims. Int J Neuropsychopharmacol 11:1047-1061. doi:10.1017/s1461145708009000
28. Peyssonnaux C, Eychene A (2001) The Raf/MEK/ERK pathway: new concepts of activation. Biol Cell 93:53-62. doi:10.1016/S0248-4900(01)01125-X (Pubitemid 33040860)
29. Popoli M, Yan Z, McEwen BS, Sanacora G (2011) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13:22-37. doi:10.1038/nrn3138
30. Qi X, Lin W, Li J, Li H, Wang W, Wang D, Sun M (2008) Fluoxetine increases the activity of the ERK-CREB signal system and alleviates the depressive-like behavior in rats exposed to chronic forced swim stress. Neurobiol Dis 31:278-285. doi:10.1016/j.nbd.2008.05.003
31. Qi H, Mailliet F, Spedding M, Rocher C, Zhang X, Delagrange P, McEwen B, Jay TM, Svenningsson P (2009) Antidepressants reverse the attenuation of the neurotrophic MEK/MAPK cascade in frontal cortex by elevated platform stress; reversal of effects on LTP is associated with GluA1 phosphorylation. Neuropharmacology 56:37-46. doi:10.1016/j.neuropharm.2008.06.068
32. Rajkowska G, O'Dwyer G, Teleki Z, Stockmeier CA, Miguel-Hidalgo JJ (2007) GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropharmacology 32:471-482. doi:10.1038/sj.npp.1301234 (Pubitemid 46106953)
33. Rogers MA, Kasai K, Koji M, Fukuda R, Iwanami A, Nakagome K, Fukuda M, Kato N (2004) Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence. Neurosci Res 50:1-11. doi:10.1016/j.neures.2004.05.003 (Pubitemid 39024296)
34. Sanacora G, Gueorguieva R, Epperson CN, Wu YT, Appel M, Rothman DL, Krystal JH, Mason GF (2004) Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression. Arch Gen Psychiatry 61:705-713. doi:10.1001/archpsyc.61.7.705 (Pubitemid 38890805)
35. Sanchez-Huertas C, Rico B (2011) CREB-dependent regulation of GAD65 transcription by BDNF/TrkB in cortical interneurons. Cereb Cortex 21:777-788. doi:10.1093/cercor/bhq150
36. Sequeira A, Mamdani F, Ernst C, Vawter MP, Bunney WE, Lebel V, Rehal S, Klempan T, Gratton A, Benkelfat C, Rouleau GA, Mechawar N, Turecki G (2009) Global brain gene expression analysis links glutamatergic and GABAergic alterations to suicide and major depression. PLoS ONE 4:e6585. doi:10.1371/journal.pone.0006585
37. Sibille E, Morris HM, Kota RS, Lewis DA (2011) GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol 14:721-734. doi:10.1017/S1461145710001616
38. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183. doi:10.1038/nrn1346 (Pubitemid 38252474)
39. Thompson M, Weickert CS, Wyatt E, Webster MJ (2009) Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J Psychiatr Res 43:970-977. doi:10.1016/j.jpsychires.2009.02.005
40. Tordera RM, Garcia-Garcia AL, Elizalde N, Segura V, Aso E, Venzala E, Ramirez MJ, Del Rio J (2011) Chronic stress and impaired glutamate function elicit a depressive-like phenotype and common changes in gene expression in the mouse frontal cortex. Eur Neuropsychopharmacol 21:23-32. doi:10.1016/j. euroneuro.2010.06.016
41. Torrey EF, Bowcut JC (2013) SMRI contributions to drug development for schizophrenia and bipolar disorder. Schizophr Bull 39:481-482. doi:10.1093/schbul/sbt039
42. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH (2000) The stanley foundation brain collection and neuropathology consortium. Schizophr Res 44:151-155. doi:10.1016/S0920-9964(99)00192-9 (Pubitemid 30411930)
43. Tzingounis AV, Wadiche JI (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8:935-947. doi:10.1038/nrn2274 (Pubitemid 350146934)
44. Xing G, Chavko M, Zhang LX, Yang S, Post RM (2002) Decreased calcium-dependent constitutive nitric oxide synthase (cNOS) activity in prefrontal cortex in schizophrenia and depression. Schizophr Res 58:21-30. doi:10.1016/S0920-9964(01)00388-7 (Pubitemid 35291183)
45. Xing GQ, Russell S, Webster MJ, Post RM (2004) Decreased expression of mineralocorticoid receptor mRNA in the prefrontal cortex in schizophrenia and bipolar disorder. Int J Neuropsychopharmacol 7:143-153. doi:10.1017/ s1461145703004000 (Pubitemid 38823281)
46. Yuan P, Zhou R, Wang Y, Li X, Li J, Chen G, Guitart X, Manji HK (2010) Altered levels of extracellular signal-regulated kinase signaling proteins in postmortem frontal cortex of individuals with mood disorders and schizophrenia. J Affect Disord 124:164-169. doi:10.1016/j.jad.2009.10.017
47. Zink M, Vollmayr B, Gebicke-Haerter PJ, Henn FA (2010) Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression. Neuropharmacology 58:465-473. doi:10.1016/j. neuropharm.2009.09.005
48. Zink M, Rapp S, Donev R, Gebicke-Haerter PJ, Thome J (2011) Fluoxetine treatment induces EAAT2 expression in rat brain. J Neural Transm 118:849-855. doi:10.1007/s00702-010-0536-y