γ-aminobutyric acid-type A receptor deficits cause hypothalamic-pituitary-adrenal axis hyperactivity and antidepressant drug sensitivity reminiscent of melancholic forms of depression

Biological Psychiatry

Volumn 68, Issue 6, 2010, Pages 512-520

  Shen, Qiuying ^a   Lal, Rachnanjali ^a   Luellen, Beth A ^a   Earnheart, John C ^a,d   Andrews, Anne Milasincic ^a,b,e   Luscher, Bernhard ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anhedonia; anxious depression; corticosterone; desipramine; fluoxetine; stress

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CORTICOSTERONE; DESIPRAMINE; FLUOXETINE; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; EMBRYO DEVELOPMENT; FEMALE; FORCED SWIMMING TEST; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MOUSE; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; TREATMENT RESPONSE;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; CORTICOSTERONE; DEPRESSIVE DISORDER; DESIPRAMINE; DISEASE MODELS, ANIMAL; FEMALE; FLUOXETINE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MICE; MICE, KNOCKOUT; PITUITARY-ADRENAL SYSTEM; RECEPTORS, GABA-A; SEROTONIN UPTAKE INHIBITORS;

EID: 77956118577     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2010.04.024     Document Type: Article

References (70)

1. K.S. Kendler Major depression and generalised anxiety disorder Same genes, (partly) different environmentsrevisited Br J Psychiatry Suppl 1996 68 75
2. T.C. Eley, D. Bolton, T.G. O'Connor, S. Perrin, P. Smith, and R. Plomin A twin study of anxiety-related behaviours in pre-school children J Child Psychol Psychiatry 44 2003 945 960
3. J. Kaufman, and D. Charney Comorbidity of mood and anxiety disorders Depress Anxiety 12 suppl 1 2000 69 76
4. J.M. Murphy, N.J. Horton, N.M. Laird, R.R. Monson, A.M. Sobol, and A.H. Leighton Anxiety and depression: A 40-year perspective on relationships regarding prevalence, distribution, and comorbidity Acta Psychiatr Scand 109 2004 355 375
5. M. Fava, A.J. Rush, J.E. Alpert, G.K. Balasubramani, S.R. Wisniewski, and C.N. Carmin Difference in treatment outcome in outpatients with anxious versus nonanxious depression: A STAR (*)D report Am J Psychiatry 165 2008 342 351
6. K.S. Kendler, L.M. Karkowski, and C.A. Prescott Causal relationship between stressful life events and the onset of major depression Am J Psychiatry 156 1999 837 841
7. B.S. McEwen Early life influences on life-long patterns of behavior and health Ment Retard Dev Disabil Res Rev 9 2003 149 154
8. S.J. Lupien, B.S. McEwen, M.R. Gunnar, and C. Heim Effects of stress throughout the lifespan on the brain, behaviour and cognition Nat Rev Neurosci 10 2009 434 445
9. E.S. Brown, F.P. Varghese, and B.S. McEwen Association of depression with medical illness: Does cortisol play a role? Biol Psychiatry 55 2004 1 9
10. M.A. Tichomirowa, M.E. Keck, H.J. Schneider, M. Paez-Pereda, U. Renner, F. Holsboer, and G.K. Stalla Endocrine disturbances in depression J Endocrinol Invest 28 2005 89 99
11. J.M. Hennings, T. Owashi, E.B. Binder, S. Horstmann, A. Menke, and S. Kloiber Clinical characteristics and treatment outcome in a representative sample of depressed inpatientsFindings from the Munich Antidepressant Response Signature (MARS) project J Psychiatr Res 43 2009 215 229
12. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 4th Ed. 2000 American Psychiatric Association Washington, DC Text Revision
13. Z. Merali, L. Du, P. Hrdina, M. Palkovits, G. Faludi, M.O. Poulter, and H. Anisman Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region J Neurosci 24 2004 1478 1485
14. G. Sanacora, R. Gueorguieva, C.N. Epperson, Y.T. Wu, M. Appel, and D.L. Rothman Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression Arch Gen Psychiatry 61 2004 705 713
15. Z. Bhagwagar, M. Wylezinska, P. Jezzard, J. Evans, E. Boorman, and P.M. Matthews Low GABA concentrations in occipital cortex and anterior cingulate cortex in medication-free, recovered depressed patients Int J Neuropsychopharmacol 11 2008 255 260
16. M.O. Poulter, L. Du, I.C. Weaver, M. Palkovits, G. Faludi, and Z. Merali GABAA receptor promoter hypermethylation in suicide brain: Implications for the involvement of epigenetic processes Biol Psychiatry 64 2008 645 652
17. A. Sequeira, F. Mamdani, C. Ernst, M.P. Vawter, W.E. Bunney, and V. Lebel Global brain gene expression analysis links glutamatergic and GABAergic alterations to suicide and major depression PLoS ONE 4 2009 e6585
18. N. Craddock, L. Jones, I.R. Jones, G. Kirov, E.K. Green, and D. Grozeva Strong genetic evidence for a selective influence of GABA(A) receptors on a component of the bipolar disorder phenotype Mol Psychiatry 15 2010 146 153
19. T.A. Klempan, A. Sequeira, L. Canetti, A. Lalovic, C. Ernst, J. ffrench-Mullen, and G. Turecki Altered expression of genes involved in ATP biosynthesis and GABAergic neurotransmission in the ventral prefrontal cortex of suicides with and without major depression Mol Psychiatry 14 2009 175 189
20. A.J. Levinson, P.B. Fitzgerald, G. Favalli, D.M. Blumberger, M. Daigle, and Z.J. Daskalakis Evidence of cortical inhibitory deficits in major depressive disorder Biol Psychiatry 67 2010 458 464
21. M. Orchinik, S.S. Carroll, Y.H. Li, B.S. McEwen, and N.G. Weiland Heterogeneity of hippocampal GABA(A) receptors: Regulation by corticosterone J Neurosci 21 2001 330 339
22. A receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice Neuropsychopharmacology 29 2004 1344 1352
23. N. Maggio, and M. Segal Differential corticosteroid modulation of inhibitory synaptic currents in the dorsal and ventral hippocampus J Neurosci 29 2009 2857 2866
24. A. Surget, Y. Wang, S. Leman, Y. Ibarguen-Vargas, N. Edgar, and G. Griebel Corticolimbic transcriptome changes are state-dependent and region-specific in a rodent model of depression and of antidepressant reversal Neuropsychopharmacology 34 2008 1363 1380
25. J. Tuomisto, and P. Mannisto Neurotransmitter regulation of anterior pituitary hormones Pharmacol Rev 37 1985 249 332
26. W.E. Cullinan, D.R. Ziegler, and J.P. Herman Functional role of local GABAergic influences on the HPA axis Brain Struct Funct 213 2008 63 72
27. A-receptor clustering results in enhanced anxiety and a bias for threat cues Nat Neurosci 2 1999 833 839
28. J.C. Earnheart, C. Schweizer, F. Crestani, T. Iwasato, S. Itohara, H. Mohler, and B. Lscher GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states J Neurosci 27 2007 3845 3854
29. A receptors is required for maintenance of receptors at mature synapses Mol Cell Neurosci 24 2003 442 450
30. L. Santarelli, M. Saxe, C. Gross, A. Surget, F. Battaglia, and S. Dulawa Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants Science 301 2003 805 809
31. I. Lucki The forced swimming test as a model for core and component behavioral effects of antidepressant drugs Behav Pharmacol 8 1997 523 532
32. A. Bilkei-Gorzo, I. Racz, K. Michel, and A. Zimmer Diminished anxiety- and depression-related behaviors in mice with selective deletion of the Tac1 gene J Neurosci 22 2002 10046 10052
33. L. Steru, R. Chermat, B. Thierry, and P. Simon The tail suspension test: A new method for screening antidepressants in mice Psychopharmacology 85 1985 367 370
34. S.R. Bodnoff, B. Suranyi-Cadotte, D.H. Aitken, R. Quirion, and M.J. Meaney The effects of chronic antidepressant treatment in an animal model of anxiety Psychopharmacology 95 1988 298 302
35. J.M. Gorman, M.R. Liebowitz, A.J. Fyer, D. Goetz, R.B. Campeas, and M.R. Fyer An open trial of fluoxetine in the treatment of panic attacks J Clin Psychopharmacol 7 1987 329 332
36. S. Monleon, P. D'Aquila, A. Parra, V.M. Simon, P.F. Brain, and P. Willner Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine Psychopharmacology 117 1995 453 457
37. J. Fawcett, D.C. Clark, W.A. Scheftner, and R.D. Gibbons Assessing anhedonia in psychiatric patients: The pleasure scale Arch Gen Psychiatry 40 1983 79 84
38. G. Aston-Jones, Y. Zhu, and J.P. Card Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: Possible interneuronal pool J Neurosci 24 2004 2313 2321
39. S.J. Judge, C.D. Ingram, and S.E. Gartside GABA receptor modulation of 5-HT neuronal firing: Characterization and effect of moderate in vivo variations in glucocorticoid levels Neurochem Int 45 2004 1057 1065
40. A. Holmes, R.J. Yang, K.P. Lesch, J.N. Crawley, and D.L. Murphy Mice lacking the serotonin transporter exhibit 5-HT(1A) receptor-mediated abnormalities in tests for anxiety-like behavior Neuropsychopharmacology 28 2003 2077 2088
41. T.A. Mathews, D.E. Fedele, F.M. Coppelli, A.M. Avila, D.L. Murphy, and A.M. Andrews Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression J Neurosci Methods 140 2004 169 181
42. T. Iwasato, R. Nomura, R. Ando, T. Ikeda, M. Tanaka, and S. Itohara Dorsal telencephalon-specific expression of Cre recombinase in PAC transgenic mice Genesis 38 2004 130 138
43. F. Holsboer, and N. Barden Antidepressants and hypothalamic-pituitary- adrenocortical regulation Endocr Rev 17 1996 187 205
44. M. Ising, S. Horstmann, S. Kloiber, S. Lucae, E.B. Binder, and N. Kern Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depressionA potential biomarker? Biol Psychiatry 62 2007 47 54
45. R.J. Donati, Y. Dwivedi, R.C. Roberts, R.R. Conley, G.N. Pandey, and M.M. Rasenick Postmortem brain tissue of depressed suicides reveals increased Gs alpha localization in lipid raft domains where it is less likely to activate adenylyl cyclase J Neurosci 28 2008 3042 3050
46. L.H. Jacobson, and J.F. Cryan Feeling strained? Influence of genetic background on depression-related behavior in mice: A review Behav Genet 37 2007 171 213
47. Y. Sugimoto, Y. Kajiwara, K. Hirano, S. Yamada, N. Tagawa, and Y. Kobayashi Mouse strain differences in immobility and sensitivity to fluvoxamine and desipramine in the forced swimming test: Analysis of serotonin and noradrenaline transporter binding Eur J Pharmacol 592 2008 116 122
48. J.C. Fournier, R.J. DeRubeis, S.D. Hollon, S. Dimidjian, J.D. Amsterdam, R.C. Shelton, and J. Fawcett Antidepressant drug effects and depression severity: A patient-level meta-analysis JAMA 303 2010 47 53
49. E.A. Young, M. Altemus, J.F. Lopez, J.H. Kocsis, A.F. Schatzberg, C. DeBattista, and J.K. Zubieta HPA axis activation in major depression and response to fluoxetine: A pilot study Psychoneuroendocrinology 29 2004 1198 1204
50. C.M. Swartz, and G. Guadagno Melancholia with onset during treatment with SSRIs Ann Clin Psychiatry 10 1998 177 179
51. P.J. Perry Pharmacotherapy for major depression with melancholic features: Relative efficacy of tricyclic versus selective serotonin reuptake inhibitor antidepressants J Affect Disord 39 1996 1 6
52. M. Bauer, P.C. Whybrow, J. Angst, M. Versiani, and H.J. Moller World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of unipolar depressive disorders, part 1: Acute and continuation treatment of major depressive disorder World J Biol Psychiatry 3 2002 5 43
53. G.E. Clerc, P. Ruimy, and J. Verdeau-Palles A double-blind comparison of venlafaxine and fluoxetine in patients hospitalized for major depression and melancholia The Venlafaxine French Inpatient Study Group Int Clin Psychopharmacol 9 1994 139 143
54. S.P. Roose, A.H. Glassman, E. Attia, and S. Woodring Comparative efficacy of selective serotonin reuptake inhibitors and tricyclics in the treatment of melancholia Am J Psychiatry 151 1994 1735 1739
55. G. Parker, P. Mitchell, K. Wilhelm, D. Menkes, J. Snowdon, and I. Schweitzer Are the newer antidepressant drugs as effective as established physical treatments? Results from an Australasian clinical panel review Aust N Z J Psychiatry 33 1999 874 881
56. G. Parker, K. Roy, K. Wilhelm, and P. Mitchell Assessing the comparative effectiveness of antidepressant therapies: A prospective clinical practice study J Clin Psychiatry 62 2001 117 125
57. R.B. Price, D.C. Shungu, X. Mao, P. Nestadt, C. Kelly, and K.A. Collins Amino acid neurotransmitters assessed by proton magnetic resonance spectroscopy: Relationship to treatment resistance in major depressive disorder Biol Psychiatry 65 2009 792 800
58. J.W. Kasckow, D. Baker, and T.D. Geracioti Jr Corticotropin-releasing hormone in depression and post-traumatic stress disorder Peptides 22 2001 845 851
59. F. Contreras, J.M. Menchon, M. Urretavizcaya, M.A. Navarro, J. Vallejo, and G. Parker Hormonal differences between psychotic and non-psychotic melancholic depression J Affect Disord 100 2007 65 73
60. C.C. Weber, G.P. Eckert, and W.E. Muller Effects of antidepressants on the brain/plasma distribution of corticosterone Neuropsychopharmacology 31 2006 2443 2448
61. H. Meltzer, B. Bastani, K. Jayathilake, and M. Maes Fluoxetine, but not tricyclic antidepressants, potentiates the five-hydroxytryptophan-mediated increase in plasma cortisol and prolactin secretion in subjects with major depression or with obsessive compulsive disorder Neuropsychopharmacology 17 1997 1 11
62. M. Santibanez, K. Gysling, and M.I. Forray Desipramine prevents the sustained increase in corticotropin-releasing hormone-like immunoreactivity induced by repeated immobilization stress in the rat central extended amygdala J Neurosci Res 84 2006 1270 1281
63. T.J. Connor, P. Kelliher, Y. Shen, A. Harkin, J.P. Kelly, and B.E. Leonard Effect of subchronic antidepressant treatments on behavioral, neurochemical, and endocrine changes in the forced-swim test Pharmacol Biochem Behav 65 2000 591 597
64. I.J. Heuser, U. Schweiger, U. Gotthardt, J. Schmider, C.H. Lammers, and M. Dettling Pituitary-adrenal-system regulation and psychopathology during amitriptyline treatment in elderly depressed patients and normal comparison subjects Am J Psychiatry 153 1996 93 99
65. P. Linkowski, J. Mendlewicz, M. Kerkhofs, R. Leclercq, J. Golstein, and M. Brasseur 24-hour profiles of adrenocorticotropin, cortisol, and growth hormone in major depressive illness: Effect of antidepressant treatment J Clin Endocrinol Metab 65 1987 141 152
66. J.P. Herman, A. Renda, and B. Bodie Norepinephrine-gamma-aminobutyric acid (GABA) interaction in limbic stress circuits: Effects of reboxetine on GABAergic neurons Biol Psychiatry 53 2003 166 174
67. M.P. Austin, P. Mitchell, K. Wilhelm, G. Parker, I. Hickie, and H. Brodaty Cognitive function in depression: A distinct pattern of frontal impairment in melancholia? Psychol Med 29 1999 73 85
68. M.A. Rogers, M.A. Bellgrove, E. Chiu, C. Mileshkin, and J.L. Bradshaw Response selection deficits in melancholic but not nonmelancholic unipolar major depression J Clin Exp Neuropsychol 26 2004 169 179
69. M. Banasr, and R.S. Duman Regulation of neurogenesis and gliogenesis by stress and antidepressant treatment CNS Neurol Disord Drug Targets 6 2007 311 320
70. B. Czeh, and P.J. Lucassen What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 257 2007 250 260