The endogenous and reactive depression subtypes revisited: Integrative animal and human studies implicate multiple distinct molecular mechanisms underlying major depressive disorder

BMC Medicine

Volumn 12, Issue 1, 2014, Pages

  Malki, Karim ^a   Keers, Robert ^a   Tosto, Maria G ^a,b   Lourdusamy, Anbarasu ^c   Carboni, Lucia ^d   Domenici, Enrico ^e,f   Uher, Rudolf ^a,g   McGuffin, Peter ^a   Schalkwyk, Leonard C ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e GSK   (Italy)

^f F Hoffmann La Roche   (Switzerland)

^g DALHOUSIE UNIVERSITY   (Canada)

Author keywords

DSM IV; Endogenous depression; GENDEP; mRNA; Reactive depression; Stanley brain consortium; Stress; VAMP 2

Indexed keywords

ADIPONECTIN; BTG2 PROTEIN; EXCITATORY AMINO ACID TRANSPORTER 2; FOXP1 PROTEIN; GLUCOSE TRANSPORTER 3; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOBREVIN 2; TAURINE TRANSPORTER; UNCLASSIFIED DRUG; XRN1 PROTEIN; YWHAG PROTEIN; ANTIDEPRESSANT AGENT; VAMP2 PROTEIN, HUMAN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DNA MICROARRAY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HIPPOCAMPUS; LIVER; MAJOR DEPRESSION; MALE; MATERNAL DEPRIVATION; MOUSE; NONHUMAN; PREFRONTAL CORTEX; RAT; REACTIVE DEPRESSION; SPLEEN; STRESS; ADJUSTMENT DISORDER; ANIMAL; BRAIN; CASE CONTROL STUDY; CLASSIFICATION; DEPRESSION; DEPRESSIVE DISORDER; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MENTAL STRESS; PATHOLOGY;

ADJUSTMENT DISORDERS; ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; CASE-CONTROL STUDIES; DEPRESSION; DEPRESSIVE DISORDER; DEPRESSIVE DISORDER, MAJOR; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MALE; MATERNAL DEPRIVATION; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RNA, MESSENGER; STRESS, PSYCHOLOGICAL; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84902110446     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-12-73     Document Type: Article

References (69)

1. Thase ME, Entsuah AR, Rudolph RL. Remission rates during treatment with venlafaxine or selective serotonin reuptake inhibitors. Br J Psychiatry 2001, 178:234-241.
2. Uher R, Huezo-Diaz P, Perroud N, Smith R, Rietschel M, Mors O, Hauser J, Maier W, Kozel D, Henigsberg N, Barreto M, Placentino A, Dernovsek MZ, Schulze TG, Kalember P, Zobel A, Czerski PM, Larsen ER, Souery D, Giovannini C, Gray JM, Lewis CM, Farmer A, Aitchison KJ, McGuffin P, Craig I. Genetic predictors of response to antidepressants in the GENDEP project. Pharmacogenomics J 2009, 9:225-233.
3. Keers R, Uher R. Gene-environment interaction in major depression and antidepressant treatment response. Curr Psychiatry Rep 2012, 14:129-137.
4. Paroxetine: a selective serotonin reuptake inhibitor showing better tolerance, but weaker antidepressant effect than clomipramine in a controlled multicenter study. Danish University Antidepressant Group. J Affect Disord 1990, 18:289-299.
5. Nanni V, Uher R, Danese A. Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: a meta-analysis. Am J Psychiatry 2012, 169:141-151.
6. Chen JD, Liu F, Xun GL, Chen HF, Hu MR, Guo XF, Xiao CQ, Wooderson SC, Guo WB, Zhao JP. Early and late onset, first-episode, treatment-naive depression: same clinical symptoms, different regional neural activities. J Affect Disord 2012, 143:56-63.
7. Andrus BM, Blizinsky K, Vedell PT, Dennis K, Shukla PK, Schaffer DJ, Radulovic J, Churchill GA, Redei EE. Gene expression patterns in the hippocampus and amygdala of endogenous depression and chronic stress models. Mol Psychiatry 2012, 17:49-61. 3117129,3117129, 21079605.
8. Alfonso J, Frasch AC, Flugge G. Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus. Rev Neurosci 2005, 16:43-56.
9. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, Joels M, Krugers H. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 2008, 28:6037-6045.
10. Gotlib IH, Joormann J, Minor KL, Hallmayer J. HPA axis reactivity: a mechanism underlying the associations among 5-HTTLPR, stress, and depression. Biol Psychiatry 2008, 63:847-851. 2373542, 18005940.
11. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
12. Malki K, Lourdusamy A, Binder E, Payá-Cano J, Sluyter F, Craig I, Keers R, McGuffin P, Uher R, Schalkwyk LC. Antidepressant-dependent mRNA changes in mouse associated with hippocampal neurogenesis in a mouse model of depression. Pharmacogenet Genomics 2012, 22:765-776.
13. Carboni L, Becchi S, Piubelli C, Mallei A, Giambelli R, Razzoli M, Mathe AA, Popoli M, Domenici E. Early-life stress and antidepressants modulate peripheral biomarkers in a gene-environment rat model of depression. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:1037-1048.
14. Holmes PV. Rodent models of depression: reexamining validity without anthropomorphic inference. Crit Rev Neurobiol 2003, 15:143-174.
15. GENEDEP Official Site. [http://gendep.iop.kcl.ac.uk].
16. Malki K, Tosto MG, Jumabhoy I, Lourdusamy A, Sluyter F, Craig I, Uher R, McGuffin P, Schalkwyk LC. Integrative mouse and human mRNA studies using WGCNA nominates novel candidate genes involved in the pathogenesis of major depressive disorder. Pharmacogenomics 2013, 14:1979-1990.
17. Malki K, Campbell J, Davies M, Keers R, Uher R, Ward M, Paya-Cano J, Aitchinson KJ, Binder E, Sluyter F, Kuhn K, Selzer S, Craig I, McGuffin P, Schalkwyk LC. Pharmacoproteomic investigation into antidepressant response in two mouse inbred strains. Proteomics 2012, 12:2355-2365.
18. Piubelli C, Carboni L, Becchi S, Mathe AA, Domenici E. Regulation of cytoskeleton machinery, neurogenesis and energy metabolism pathways in a rat gene-environment model of depression revealed by proteomic analysis. Neuroscience 2011, 176:349-380.
19. Binder E, Malki K, Paya-Cano JL, Fernandes C, Aitchison KJ, Mathe AA, Sluyter F, Schalkwyk LC. Antidepressants and the resilience to early-life stress in inbred mouse strains. Pharmacogenet Genom 2011, 21:779-789.
20. Nishi K, Kanemaru K, Diksic M. A genetic rat model of depression, Flinders sensitive line, has a lower density of 5-HT1A receptors, but a higher density of 5-HT1B receptors, compared to control rats. Neurochem Int 2009, 54:299-307. 2656411, 19121358.
21. Osterlund MK, Overstreet DH, Hurd YL. The Flinders Sensitive Line rats, a genetic model of depression, show abnormal serotonin receptor mRNA expression in the brain that is reversed by 17 beta-estradiol. Mol Brain Res 1999, 74:158-166.
22. Blaveri E, Kelly F, Mallei A, Harris K, Taylor A, Reid J, Razzoli M, Carboni L, Piubelli C, Musazzi L, Racagni G, Mathé A, Popoli M, Domenici E, Bates S. Expression profiling of a genetic animal model of depression reveals novel molecular pathways underlying depressive-like behaviours. Plos One 2010, 5:e12596. 2935375, 20830301.
23. Friedman EM, Becker KA, Overstreet DH, Lawrence DA. Reduced primary antibody responses in a genetic animal model of depression. Psychosom Med 2002, 64:267-273.
24. Overstreet DH. The Flinders sensitive line rats: a genetic animal model of depression. Neurosci Biobehav Rev 1993, 17:51-68.
25. Overstreet DH. Commentary: a behavioral, psychopharmacological, and neurochemical update on the Flinders Sensitive Line rat, a potential genetic animal model of depression. Behav Genet 1991, 21:67-74.
26. Overstreet DH, Wegener G. The Flinders sensitive line rat model of depression-25 years and still producing. Pharmacol Rev 2013, 65:143-155.
27. Iwamoto K, Kakiuchi C, Bundo M, Ikeda K, Kato T. Molecular characterization of bipolar disorder by comparing gene expression profiles of postmortem brains of major mental disorders. Mol Psychiatry 2004, 9:406-416.
28. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH. The Stanley Foundation Brain Collection and Neuropathology Consortium. Schizophr Res 2000, 44:151-155.
29. The Stanley Medical Research Institute. [http://www.stanleyresearch.org].
30. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
31. The R Project for Statistical Computing. [http://www.r-project.org/].
32. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 2006, 22:2825-2827.
33. Fernando RL, Nettleton D, Southey BR, Dekkers JC, Rothschild MF, Soller M. Controlling the proportion of false positives in multiple dependent tests. Genetics 2004, 166:611-619. 1470704, 15020448.
34. PANTHER Classification System. [http://www.pantherdb.org].
35. Ingenuity. [http://www.ingenuity.com/].
36. Gene Expression Omnibus. [http://www.ncbi.nlm.nih.gov/geo].
37. inSilicoMerging. http://www.bioconductor.org/packages/release/bioc/html/inSilicoMerging.html.
38. Python™. [http://www.python.org/].
39. Mouse Genome Informatics. [http://www.informatics.jax.org/].
40. Affymetrix: Biology for a better world. [http://www.affymetrix.com/analysis/index.affx].
41. Zunszain PA, Hepgul N, Pariante CM. Inflammation and depression. Curr Top Behav Neurosci 2013, 14:135-151.
42. Miller AH, Maletic V, Raison CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 2009, 65:732-741. 2680424, 19150053.
43. Gardner A, Boles RG. Beyond the serotonin hypothesis: mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:730-743.
44. Maes M. The cytokine hypothesis of depression: inflammation, oxidative & nitrosative stress (IO&NS) and leaky gut as new targets for adjunctive treatments in depression. Neuro Endocrinol Lett 2008, 29:287-291.
45. Berk M, Williams LJ, Jacka FN, O'Neil A, Pasco JA, Moylan S, Allen NB, Stuart AL, Hayley AC, Byrne ML, Maes M. So depression is an inflammatory disease, but where does the inflammation come from?. BMC Med 2013, 11:200. 3846682, 24228900.
46. Malki K, Uher R, Paya-Cano J, Binder E, Rietschel M, Zobel A, Mors O, Hauser J, Henigsberg N, Jerman B, Souery D, Placentino A, Ng MY, Cohen-Woods S, Sluyter F, Farmer A, Aitchison KJ, Craig IW, Lewis CM, McGuffin P, Schalkwyk LC. Convergent animal and human evidence suggests a role of PPM1A gene in response to antidepressants. Biol Psychiatry 2011, 69:360-365.
47. Wegener G, Harvey BH, Bonefeld B, Muller HK, Volke V, Overstreet DH, Elfving B. Increased stress-evoked nitric oxide signalling in the Flinders sensitive line (FSL) rat: a genetic animal model of depression. Int J Neuropsychopharmacol 2010, 13:461-473.
48. Carboni L, Piubelli C, Pozzato C, Astner H, Arban R, Righetti PG, Hamdan M, Domenici E. Proteomic analysis of rat hippocampus after repeated psychosocial stress. Neuroscience 2006, 137:1237-1246.
49. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS. Hippocampal volume reduction in major depression. Am J Psychiatry 2000, 157:115-118.
50. Choi JE, Hur W, Jung CK, Piao LS, Lyoo K, Hong SW, Kim SW, Yoon HY, Yoon SK. Silencing of 14-3-3zeta over-expression in hepatocellular carcinoma inhibits tumor growth and enhances chemosensitivity to cis-diammined dichloridoplatium. Cancer Lett 2011, 303:99-107.
51. Leivonen SK, Rokka A, Ostling P, Kohonen P, Corthals GL, Kallioniemi O, Perala M. Identification of miR-193b targets in breast cancer cells and systems biological analysis of their functional impact. Mol Cell Proteomics 2011, 10:M110.005322. 3134067, 21512034.
52. Zhang Z, Luo X, Ding S, Chen J, Chen T, Chen X, Zha H, Yao L, He X, Peng H. MicroRNA-451 regulates p38 MAPK signaling by targeting of Ywhaz and suppresses the mesangial hypertrophy in early diabetic nephropathy. FEBS Lett 2012, 586:20-26.
53. Li XM, Li CC, Yu SS, Chen JT, Sabapathy K, Ruan DY. JNK1 contributes to metabotropic glutamate receptor-dependent long-term depression and short-term synaptic plasticity in the mice area hippocampal CA1. Eur J Neurosci 2007, 25:391-396.
54. Clarke M, Pentz R, Bobyn J, Hayley S. Stressor-like effects of c-Jun N-terminal kinase (JNK) inhibition. Plos One 2012, 7:e44073. 3430637, 22952879.
55. Brust TB, Cayabyab FS, MacVicar BA. C-Jun N-terminal kinase regulates adenosine A1 receptor-mediated synaptic depression in the rat hippocampus. Neuropharmacology 2007, 53:906-917.
56. Miller AH, Raison CL. Cytokines, p38 MAP kinase and the pathophysiology of depression. Neuropsychopharmacology 2006, 31:2089-2090.
57. Maes M, Yirmyia R, Noraberg J, Brene S, Hibbeln J, Perini G, Kubera M, Bob P, Lerer B, Maj M. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis 2009, 24:27-53.
58. Higgs BW, Elashoff M, Richman S, Barci B. An online database for brain disease research. BMC Genomics 2006, 7:70. 1489945, 16594998.
59. Chana G, Lucero G, Salaria S, Lozach J, Du P, Woelk C, Everall I. Upregulation of NRG-1 and VAMP-1 in human brain aggregates exposed to clozapine. Schizophr Res 2009, 113:273-276. 2759675, 19502011.
60. Fung SJ, Webster MJ, Weickert CS. Expression of VGluT1 and VGAT mRNAs in human dorsolateral prefrontal cortex during development and in schizophrenia. Brain Res 2011, 1388:22-31.
61. Munakata K, Iwamoto K, Bundo M, Kato T. Mitochondrial DNA 3243A > G mutation and increased expression of LARS2 gene in the brains of patients with bipolar disorder and schizophrenia. Biol Psychiatry 2005, 57:525-532.
62. Webster MJ, Elashoff M, Weickert CS. Molecular evidence that cortical synaptic growth predominates during the first decade of life in humans. Int J Dev Neurosci 2011, 29:225-236.
63. Yamada M, Takahashi K, Tsunoda M, Nishioka G, Kudo K, Ohata H, Kamijima K, Higuchi T, Momose K, Yamada M. Differential expression of VAMP2/synaptobrevin-2 after antidepressant and electroconvulsive treatment in rat frontal cortex. Pharmacogenomics J 2002, 2:377-382.
64. Saito S, Takahashi N, Ishihara R, Ikeda M, Suzuki T, Kitajima T, Yamanouchi Y, Iwata N, Yamada M, Yoshida K, Inada T, Ozaki N. Association study between vesicle-associated membrane protein 2 gene polymorphisms and fluvoxamine response in Japanese major depressive patients. Neuropsychobiology 2006, 54:226-230.
65. Ripke S, Wray NR, Lewis CM, Hamilton SP, Weissman MM, Breen G, Byrne EM, Blackwood DH, Boomsma DI, Cichon S, Heath AC, Holsboer F, Lucae S, Madden PA, Martin NG, McGuffin P, Muglia P, Noethen MM, Penninx BP, Pergadia ML, Potash JB, Rietschel M, Lin D, Müller-Myhsok B, Shi J, Steinberg S, Grabe HJ, Lichtenstein P, Magnusson P., et al. Major Depressive Disorder Working Group of the Psychiatric GWAS Consortium A mega-analysis of genome-wide association studies for major depressive disorder. Mol Psychiatry 2013, 18:497-511. 3837431, 22472876, Major Depressive Disorder Working Group of the Psychiatric GWAS Consortium.
66. Tansey KE, Guipponi M, Perroud N, Bondolfi G, Domenici E, Evans D, Hall SK, Hauser J, Henigsberg N, Hu X, Jerman B, Maier W, Mors O, O'Donovan M, Peters TJ, Placentino A, Rietschel M, Souery D, Aitchison KJ, Craig I, Farmer A, Wendland JR, Malafosse A, Holmans P, Lewis G, Lewis CM, Stensbøl TB, Kapur S, McGuffin P, Uher R. Genetic predictors of response to serotonergic and noradrenergic antidepressants in major depressive disorder: a genome-wide analysis of individual-level data and a meta-analysis. PLoS Med 2012, 9:e1001326. 3472989, 23091423.
67. Keers R, Uher R, Gupta B, Rietschel M, Schulze TG, Hauser J, Skibinska M, Henigsberg N, Kalember P, Maier W, Zobel A, Mors O, Kristensen AS, Kozel D, Giovannini C, Mendlewicz J, Kumar S, McGuffin P, Farmer AE, Aitchison KJ. Stressful life events, cognitive symptoms of depression and response to antidepressants in GENDEP. J Affect Disord 2010, 127:337-342.
68. Piva R, Belardo G, Santoro MG. NF-kappaB: a stress-regulated switch for cell survival. Antioxid Redox Signal 2006, 8:478-486.
69. Pace TW, Mletzko TC, Alagbe O, Musselman DL, Nemeroff CB, Miller AH, Heim CM. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am J Psychiatry 2006, 163:1630-1633.