ACC Glu/GABA ratio is decreased in euthymic bipolar disorder I patients: possible in vivo neurometabolite explanation for mood stabilization.


Journal

European archives of psychiatry and clinical neuroscience
ISSN: 1433-8491
Titre abrégé: Eur Arch Psychiatry Clin Neurosci
Pays: Germany
ID NLM: 9103030

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 23 04 2019
accepted: 13 01 2020
pubmed: 30 1 2020
medline: 9 11 2021
entrez: 30 1 2020
Statut: ppublish

Résumé

Bipolar disorder (BD) is characterized by unstable mood states ranging from mania to depression. Although there is some evidence that mood instability may result from an imbalance between excitatory glutamatergic and inhibitory GABA-ergic neurotransmission, few proton magnetic resonance spectroscopy (

Identifiants

pubmed: 31993746
doi: 10.1007/s00406-020-01096-0
pii: 10.1007/s00406-020-01096-0
doi:

Substances chimiques

Anticonvulsants 0
Antipsychotic Agents 0
Glutamic Acid 3KX376GY7L
gamma-Aminobutyric Acid 56-12-2
Glutamate Decarboxylase EC 4.1.1.15
glutamate decarboxylase 1 EC 4.1.1.15

Banques de données

ClinicalTrials.gov
['NCT01237158']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

537-547

Subventions

Organisme : Sao Paulo Research Foundation (FAPESP)
ID : 2012/23796-2 and 2010/12286-8

Références

Goodwin FK, Jamison KR (2007) Manic-depressive illness: bipolar and recurrent unipolar disorders, 2nd edn. Oxford University Press, New York
Stagg CJ, Bestmann S, Constantinescu AO, Moreno LM, Allman C, Mekle R et al (2011) Relationship between physiological measures of excitability and levels of glutamate and GABA in the human motor cortex. J Physiol (Lond). 589(Pt 23):5845–5855
pmcid: 3249054
Rossignol E (2011) Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast. 2011:649325
pubmed: 21876820 pmcid: 3159129
Yüksel C, Ongur D (2010) Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol Psychiatry. 68(9):785–794
pubmed: 20728076 pmcid: 2955841
Brady RO, McCarthy JM, Prescot AP, Jensen JE, Cooper AJ, Cohen BM et al (2013) Brain gamma-aminobutyric acid (GABA) abnormalities in bipolar disorder. Bipolar Disord. 15(4):434–439
pubmed: 23634979 pmcid: 5504910
Altamura CA, Mauri MC, Ferrara A, Moro AR, D'Andrea G, Zamberlan F (1993) Plasma and platelet excitatory amino acids in psychiatric disorders. Am J Psychiatry. 150(11):1731–1733
pubmed: 8214185
Petty F (1994) Plasma concentrations of gamma-aminobutyric acid (GABA) and mood disorders: a blood test for manic depressive disease? Clin Chem. 40(2):296–302
pubmed: 8313610
Post RM, Ballenger JC, Hare TA, Goodwin FK, R LC, Jimerson DC et al (1980) Cerebrospinal fluid GABA in normals and patients with affective disorders. Brain Res Bull 5(Suppl. 2):755–759
Gerner RH, Fairbanks L, Anderson GM, Young JG, Scheinin M, Linnoila M et al (1984) CSF neurochemistry in depressed, manic, and schizophrenic patients compared with that of normal controls. Am J Psychiatry. 141(12):1533–1540
pubmed: 6209989
Gigante AD, Bond DJ, Lafer B, Lam RW, Young LT, Yatham LN (2012) Brain glutamate levels measured by magnetic resonance spectroscopy in patients with bipolar disorder: a meta-analysis. Bipolar Disord. 14(5):478–487
pubmed: 22834460
Kraguljac NV, Reid M, White D, Jones R, den Hollander J, Lowman D et al (2012) Neurometabolites in schizophrenia and bipolar disorder - a systematic review and meta-analysis. Psychiatry Res. 203(2–3):111–125
pubmed: 22981426 pmcid: 3466386
Chiapponi C, Piras F, Piras F, Caltagirone C, Spalletta G (2016) GABA system in schizophrenia and mood disorders: a mini review on third-generation imaging studies. Front Psychiatry. 7:61
pubmed: 27148090 pmcid: 4835487
Lener MS, Niciu MJ, Ballard ED, Park M, Park LT, Nugent AC et al (2017) Glutamate and gamma-aminobutyric acid systems in the pathophysiology of major depression and antidepressant response to ketamine. Biol Psychiatry. 81(10):886–897
pubmed: 27449797
Rubenstein JLR, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2(5):255–267
pubmed: 14606691 pmcid: 6748642
Harada M, Taki MM, Nose A, Kubo H, Mori K, Nishitani H et al (2011) Non-invasive evaluation of the GABAergic/glutamatergic system in autistic patients observed by MEGA-editing proton MR spectroscopy using a clinical 3 tesla instrument. J Autism Dev Disord. 41(4):447–454
pubmed: 20652388
Anticevic A, Savic A, Repovs G, Yang G, McKay DR, Sprooten E et al (2015) Ventral anterior cingulate connectivity distinguished nonpsychotic bipolar illness from psychotic bipolar disorder and schizophrenia. Schizophr Bull. 41(1):133–143
pubmed: 24782562
Soeiro de Souza MG, Otaduy MCG, Machado-Vieira R, Moreno RA, Nery FG, Leite C et al (2018) Anterior cingulate cortex glutamatergic metabolites and mood stabilizers in euthymic bipolar I disorder patients: a proton magnetic resonance spectroscopy study. Biol Psychiatry Cogn Neurosci Neuroimaging. https://doi.org/10.1016/j.bpsc.2018.02.007
Colla M, Schubert F, Bubner M, Heidenreich JO, Bajbouj M, Seifert F et al (2009) Glutamate as a spectroscopic marker of hippocampal structural plasticity is elevated in long-term euthymic bipolar patients on chronic lithium therapy and correlates inversely with diurnal cortisol. Mol Psychiatry 14(7):696–704, 647
Bhagwagar Z, Wylezinska M, Jezzard P, Evans J, Ashworth F, Sule A et al (2007) Reduction in occipital cortex gamma-aminobutyric acid concentrations in medication-free recovered unipolar depressed and bipolar subjects. Biol Psychiatry. 61(6):806–812
pubmed: 17210135
Senaratne R, Milne AM, MacQueen GM, Hall GBC (2009) Increased choline-containing compounds in the orbitofrontal cortex and hippocampus in euthymic patients with bipolar disorder: a proton magnetic resonance spectroscopy study. Psychiatry Res. 172(3):205–209
pubmed: 19386476
Ehrlich A, Schubert F, Pehrs C, Gallinat J (2015) Alterations of cerebral glutamate in the euthymic state of patients with bipolar disorder. Psychiatry Res. 233(2):73–80
pubmed: 26050195
Soeiro de Souza MG, Henning A, Machado-Vieira R, Moreno RA, Pastorello BF, da Costa Leite C et al (2015) Anterior cingulate Glutamate-Glutamine cycle metabolites are altered in euthymic bipolar I disorder. Eur Neuropsychopharmacol 25(12):2221–2229
Levy LM, Degnan AJ (2013) GABA-based evaluation of neurologic conditions: MR spectroscopy. AJNR Am J Neuroradiol. 34(2):259–265
pubmed: 22268095
Schür RR, Draisma LWR, Wijnen JP, Boks MP, Koevoets MGJC, Joëls M et al (2016) Brain GABA levels across psychiatric disorders: a systematic literature review and meta-analysis of (1) H-MRS studies. Hum Brain Mapp 37(9):3337–3352
pubmed: 27145016 pmcid: 6867515
Wang PW, Sailasuta N, Chandler RA, Ketter TA (2006) Magnetic resonance spectroscopy measurement of cerebral gamma-aminobutyric acid concentrations in patients with bipolar disorders. Acta Neuropsychiatr 2(18):120–126
Kaufman RE, Ostacher MJ, Marks EH, Simon NM, Sachs GS, Jensen JE et al (2009) Brain GABA levels in patients with bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 33(3):427–434
pubmed: 19171176
Godlewska BR, Yip SW, Near J, Goodwin GM, Cowen PJ (2014) Cortical glutathione levels in young people with bipolar disorder: a pilot study using magnetic resonance spectroscopy. Psychopharmacology 231(2):327–332
pubmed: 23955702
Prisciandaro JJ, Tolliver BK, Prescot AP, Brenner HM, Renshaw PF, Brown TR et al (2017) Unique prefrontal GABA and glutamate disturbances in co-occurring bipolar disorder and alcohol dependence. Transl Psychiatry. 7(7):e1163
pubmed: 28675386 pmcid: 5538121
Wang PW, Sailasuta N, Chandler RA, Ketter TA (2006) Magnetic resonance spectroscopic measurement of cerebral gamma-aminobutyric acid concentrations in patients with bipolar disorders. Acta Neuropsychiatr 18(2):120–126
pubmed: 26989801
Ford TC, Nibbs R, Crewther DP (2017) Increased glutamate/GABA+ ratio in a shared autistic and schizotypal trait phenotype termed social disorganisation. Neuroimage Clin. 16:125–131
pubmed: 28794973 pmcid: 5537407
Ford TC, Nibbs R, Crewther DP (2017) Glutamate/GABA+ ratio is associated with the psychosocial domain of autistic and schizotypal traits. PLoS ONE 12(7):e0181961
pubmed: 28759626 pmcid: 5536272
Anwyl R (1991) Modulation of vertebrate neuronal calcium channels by transmitters. Brain Res Brain Res Rev. 16(3):265–281
pubmed: 1686417
Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7(1):91–100
pubmed: 2069816
Bu DF, Erlander MG, Hitz BC, Tillakaratne NJ, Kaufman DL, Wagner-McPherson CB et al (1992) Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc Natl Acad Sci USA 89(6):2115–2119
pubmed: 1549570
Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR et al (2000) Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry. 57(11):1061–1069
pubmed: 11074872
Heckers S, Stone D, Walsh J, Shick J, Koul P, Benes FM (2002) Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry. 59(6):521–529
pubmed: 12044194
Woo T-UW, Walsh JP, Benes FM (2004) Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch Gen Psychiatry 61(7):649–657
Fatemi SH, Hossein Fatemi S, Stary JM, Earle JA, Araghi-Niknam M, Eagan E (2005) GABAergic dysfunction in schizophrenia and mood disorders as reflected by decreased levels of glutamic acid decarboxylase 65 and 67 kDa and Reelin proteins in cerebellum. Schizophr Res. 72(2–3):109–122
pubmed: 15560956
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(11):970–977
pubmed: 19321177
Lundorf MD, Buttenschøn HN, Foldager L, Blackwood DHR, Muir WJ, Murray V et al (2005) Mutational screening and association study of glutamate decarboxylase 1 as a candidate susceptibility gene for bipolar affective disorder and schizophrenia. Am J Med Genet B Neuropsychiatr Genet. 135B(1):94–101
pubmed: 15806582
Chung Y-CE, Chen S-C, Chuang L-C, Shih W-L, Chiu Y-H, Lu M-L et al (2017) Evaluation of the interaction between genetic variants of GAD1 and miRNA in bipolar disorders. J Affect Disord 223:1–7
Marenco S, Savostyanova AA, van der Veen JW, Geramita M, Stern A, Barnett AS et al (2010) Genetic modulation of GABA levels in the anterior cingulate cortex by GAD1 and COMT. Neuropsychopharmacology. 35(8):1708–1717
pubmed: 20357758 pmcid: 2891897
Krystal JH, Sanacora G, Blumberg H, Anand A, Charney DS, Marek G et al (2002) Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry. 7(Suppl 1):S71–80
pubmed: 11986998
Mesdjian E, Ciesielski L, Valli M, Bruguerolle B, Jadot G, Bouyard P et al (1982) Sodium valproate: kinetic profile and effects on GABA levels in various brain areas of the rat. Prog Neuropsychopharmacol Biol Psychiatry. 6(3):223–233
pubmed: 6815713
Pisanu C, Papadima EM, Del Zompo M, Squassina A (2018) Understanding the molecular mechanisms underlying mood stabilizer treatments in bipolar disorder: potential involvement of epigenetics. Neurosci Lett. 16(669):24–31
Gavin DP, Kartan S, Chase K, Jayaraman S, Sharma RP (2009) Histone deacetylase inhibitors and candidate gene expression: an in vivo and in vitro approach to studying chromatin remodeling in a clinical population. J Psychiatr Res. 43(9):870–876
pubmed: 19187942
First MB, Spitzer RL, Williams JB (1996) Structured clinical interview for DSM-IV axis I disorders SCID-I. American Psychiatric Press, Washington, DC, p 1
DSM-IV PATFO (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Publishing, Inc, Washington, DC
Moreira MT, Smith LA, Foxcroft D (2009) Social norms interventions to reduce alcohol misuse in university or college students. Cochrane Database Syst Rev 2009(3):CD006748. https://doi.org/10.1002/14651858.CD006748.pub2
doi: 10.1002/14651858.CD006748.pub2
Young RC, Biggs JT, Ziegler VE, Meyer DA (1978) A rating scale for mania: reliability, validity, and sensitivity. Br J Psychiatry. 133:429–435
pubmed: 728692
Hamilton M (1967) Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol. 6(4):278–296
pubmed: 6080235
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E et al (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33 (quiz 34–57)
Schulte RF, Lange T, Beck J, Meier D, Boesiger P (2006) Improved two-dimensional J-resolved spectroscopy. NMR Biomed. 19(2):264–270
pubmed: 16541465
Tkác I, Starcuk Z, Choi IY, Gruetter R (1999) In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med. 41(4):649–656
pubmed: 10332839
Fuchs A, Boesiger P, Schulte RF, Henning A (2013) ProFit revisited. Magn Reson Med. 71(2):458–468
Schulte RF, Boesiger P (2006) ProFit: two-dimensional prior-knowledge fitting of J-resolved spectra. NMR Biomed. 19(2):255–263
pubmed: 16541464
Provencher SWS (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 30(6):672–679
pubmed: 8139448
van der Veen JW, de Beer R, Luyten PR, van Ormondt D (1988) Accurate quantification of in vivo 31P NMR signals using the variable projection method and prior knowledge. Magn Reson Med. 6(1):92–98
pubmed: 3352510
Smith SA, Levante TO, de Beer R, Luyten PR, van Ormondt D (1994) Computer simulations in magnetic resonance. An object-oriented programming approach. J Magn Reson A 106:75–105. https://doi.org/10.1006/jmra.1994.1008
doi: 10.1006/jmra.1994.1008
Fan T (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Mag Reson Spectrosc. 28:161–219
Govindaraju V, Young K, Maudsley AA (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 13(3):129–153
pubmed: 10861994
Gasparovic C, Song T, Devier D, Bockholt HJ, Caprihan A, Mullins PG et al (2006) Use of tissue water as a concentration reference for proton spectroscopic imaging. Magn Reson Med. 55(6):1219–1226
pubmed: 16688703
Mlynárik V, Gruber S, Moser E (2001) Proton T (1) and T (2) relaxation times of human brain metabolites at 3 Tesla. NMR Biomed. 14(5):325–331
pubmed: 11477653
Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 20(1):45–57
pubmed: 11293691
Cavassila S, Deval S, Huegen C, van Ormondt D, Graveron-Demilly D (2001) Cramér-Rao bounds: an evaluation tool for quantitation. NMR Biomed. 14(4):278–283
Laitinen J, Samarut J, Hölttä E (1994) A nontoxic and versatile protein salting-out method for isolation of DNA. Biotechniques 17(2):316–322
Benes FM, Berretta S (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology. 25(1):1–27
pubmed: 11377916
Brix MK, Ersland L, Hugdahl K, Grüner R, Posserud M-B, Hammar Å et al (2015) Brain MR spectroscopy in autism spectrum disorder-the GABA excitatory/inhibitory imbalance theory revisited. Front Hum Neurosci. 9:365
pubmed: 26157380 pmcid: 4475903
Bush G, Luu P, Posner M (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci (Regul Ed). 4(6):215–222
Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 25:409–432
pubmed: 12052915
Hibar DP, Westlye LT, Doan NT, Jahanshad N, Cheung JW, Ching CRK et al (2018) Cortical abnormalities in bipolar disorder: an MRI analysis of 6503 individuals from the ENIGMA Bipolar Disorder Working Group. Mol Psychiatry 23(4):932–942. https://doi.org/10.1038/mp.2017.73
doi: 10.1038/mp.2017.73 pubmed: 28461699
Sanacora G, Mason GF, Rothman DL, Krystal JH (2002) Increased occipital cortex GABA concentrations in depressed patients after therapy with selective serotonin reuptake inhibitors. Am J Psychiatry. 159(4):663–665
pubmed: 11925309
Stahl SM (2009) The Prescriber's Guide, antipsychotics and mood stabilizers. Cambridge University Press, Cambridge
Cunningham MO, Dhillon A, Wood SJ, Jones RS (2000) Reciprocal modulation of glutamate and GABA release may underlie the anticonvulsant effect of phenytoin. Neuroscience 95(2):343–351
pubmed: 10658613
Friedman SD, Dager SR, Parow A, Hirashima F, Demopulos C, Stoll AL et al (2004) Lithium and valproic acid treatment effects on brain chemistry in bipolar disorder. Biol Psychiatry. 56(5):340–348
pubmed: 15336516
Scarr E, Pavey G, Sundram S, MacKinnon A, Dean B (2003) Decreased hippocampal NMDA, but not kainate or AMPA receptors in bipolar disorder. Bipolar Disord. 5(4):257–264
pubmed: 12895203
Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH (2007) Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology. 32(9):1888–1902
pubmed: 17299517
Goto N, Yoshimura R, Kakeda S, Nishimura J, Moriya J, Hayashi K et al (2012) Six-month treatment with atypical antipsychotic drugs decreased frontal-lobe levels of glutamate plus glutamine in early-stage first-episode schizophrenia. Neuropsychiatr Dis Treat. 8:119–122
pubmed: 22536067 pmcid: 3333782
Luo J, Min S, Wei K, Li P, Dong J, Liu Y-F (2011) Propofol protects against impairment of learning-memory and imbalance of hippocampal Glu/GABA induced by electroconvulsive shock in depressed rats. J Anesth. 25(5):657–665
pubmed: 21769668
Sanacora G, Mason GF, Rothman DL, Hyder F, Ciarcia JJ, Ostroff RB et al (2003) Increased cortical GABA concentrations in depressed patients receiving ECT. Am J Psychiatry. 160(3):577–579
pubmed: 12611844
Kessing LV (2019) What is early intervention in bipolar disorder? Recommendation of a pragmatic way focusing on early intervention in patients with newly diagnosed bipolar disorder. Bipolar Disord 21(2):168–169. https://doi.org/10.1111/bdi.12733
doi: 10.1111/bdi.12733 pubmed: 30475429
Kennedy SH, Lam RW, McIntyre RS, Tourjman SV, Bhat V, Blier P et al (2016) Canadian network for mood and anxiety treatments (CANMAT) 2016 clinical guidelines for the management of adults with major Depressive Disorder: Section 3. Pharmacological Treatments. Can J Psychiatry. 61(9):540–560
pubmed: 27486148 pmcid: 4994790

Auteurs

Estêvão Scotti-Muzzi (E)

Mood Disorders Unit (GRUDA), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil.

Thais Chile (T)

Genetics and Pharmacogenetics Unit (PROGENE), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil.

Ricardo Moreno (R)

Mood Disorders Unit (GRUDA), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil.

Bruno Fraccini Pastorello (BF)

Institute of Radiology (InRad), School of Medicine FMUSP, University of Sao Paulo, São Paulo, Brazil.

Cláudia da Costa Leite (C)

Institute of Radiology (InRad), School of Medicine FMUSP, University of Sao Paulo, São Paulo, Brazil.

Anke Henning (A)

Institute for Biomedical Engineering University and ETH Zurich, Zurich, Switzerland.

Maria Concepcion Garcia Otaduy (MCG)

Institute of Radiology (InRad), School of Medicine FMUSP, University of Sao Paulo, São Paulo, Brazil.

Homero Vallada (H)

Genetics and Pharmacogenetics Unit (PROGENE), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil.

Márcio Gerhardt Soeiro-de-Souza (MG)

Mood Disorders Unit (GRUDA), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil. mgss@usp.br.
Genetics and Pharmacogenetics Unit (PROGENE), School of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil. mgss@usp.br.

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