Coordinated messenger RNA/microRNA changes in fibroblasts of patients with major depression

Biological Psychiatry

Volumn 77, Issue 3, 2015, Pages 256-265

  Garbett, Krassimira A ^a   Vereczkei, Andrea ^a,b   Kálmán, Sára ^a,c   Brown, Jacquelyn A ^a   Taylor, Warren D ^a   Faludi, Gábor ^b   Korade, Željka ^a,e   Shelton, Richard C ^d   Mirnics, Károly ^a,c,e  

^a VANDERBILT UNIVERSITY   (United States)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c UNIVERSITY OF SZEGED   (Hungary)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Biomarker; DNA microarray; Gene expression; Human fibroblasts; Major depression; miRNA

Indexed keywords

GLUTATHIONE TRANSFERASE T1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HLA D ANTIGEN; HLA DPA1 ANTIGEN; HLA DPB1 ANTIGEN; HLA DQ2 ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MICRORNA; MICRORNA 103A; MICRORNA 185; MICRORNA 186; MICRORNA 193; MICRORNA 22; MICRORNA 3176; MICRORNA 32; MICRORNA 377; MICRORNA 675; MITOGEN ACTIVATED PROTEIN KINASE 1; PERIPLAKIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN C JUN; PROTEIN S100B; PROTEIN TYROSINE PHOSPHATASE SHP 2; SCATTER FACTOR RECEPTOR; STAT3 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR SUPERFAMILY MEMBER 19; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; CELL COMMUNICATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; MAJOR DEPRESSION; MICROARRAY ANALYSIS; ONCOGENE H RAS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN BIOPSY; SKIN FIBROBLAST; ADULT; CELL CULTURE; FEMALE; FIBROBLAST; GENETICS; MALE; METABOLISM;

ADULT; CELLS, CULTURED; DEPRESSIVE DISORDER, MAJOR; FEMALE; FIBROBLASTS; GENE EXPRESSION; HUMANS; MALE; MICRORNAS; POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84928178273     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.05.015     Document Type: Article

References (86)

1. Schlaak JF, Trippler M, Hoyo-Becerra C, Erim Y, Kis B, Wang B, et al. (2012): Selective hyper-responsiveness of the interferon system in major depressive disorders and depression induced by interferon therapy. PLoS One 7:e38668.
2. Hepgul N, Cattaneo A, Zunszain PA, Pariante CM (2013): Depression pathogenesis and treatment: What can we learn from blood mRNA expression? BMC Med 11:28.
3. Myint AM (2012): Kynurenines: From the perspective of major psychiatric disorders. FEBS J 279:1375-1385.
4. Chung CP, Schmidt D, Stein CM, Morrow JD, Salomon RM (2012): Increased oxidative stress in patients with depression and its relationship to treatment. Psychiatry Res 206:213-216.
5. Suri R, Hellemann G, Cohen L, Aquino A, Altshuler L (2008): Saliva estriol levels in women with and without prenatal antidepressant treatment. Biol Psychiatry 64:533-537.
6. Raedler TJ (2011): In flammatory mechanisms in major depressive disorder. Curr Opin Psychiatry 24:519-525.
7. Craddock N, Sklar P (2013): Genetics of bipolar disorder. Lancet 381:1654-1662.
8. Israel MA, Yuan SH, Bardy C, Reyna SM, Mu Y, Herrera C, et al. (2012): Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482:216-220.
9. Hrvoj-Mihic B, Marchetto MC, Gage FH, Semendeferi K, Muotri AR (2014): Novel tools, classic techniques: Evolutionary studies using primate pluripotent stem cells. Biol Psychiatry 75:929-935.
10. Shcheglovitov A, Shcheglovitova O, Yazawa M, Portmann T, Shu R, Sebastiano V, et al. (2013): SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503:267-271.
11. Horvath S, Mirnics K (2014): Immune system disturbances in schizophrenia. Biol Psychiatry 75:316-323.
12. Shelton RC, Claiborne J, Sidoryk-Wegrzynowicz M, Reddy R, Aschner M, Lewis DA, Mirnics K (2011): Altered expression of genes involved in inflammation and apoptosis in frontal cortex in major depression. Mol Psychiatry 16:751-762.
13. Sibille E, Wang Y, Joeyen-Waldorf J, Gaiteri C, Surget A, Oh S, et al. (2009): A molecular signature of depression in the amygdala. Am J Psychiatry 166:1011-1024.
14. Tochigi M, Iwamoto K, Bundo M, Sasaki T, Kato N, Kato T (2008): Gene expression profiling of major depression and suicide in the prefrontal cortex of postmortem brains. Neurosci Res 60:184-191.
15. Kang HJ, Adams DH, Simen A, Simen BB, Rajkowska G, Stockmeier CA, et al. (2007): Gene expression profiling in postmortem prefrontal cortex of major depressive disorder. J Neurosci 27:13329-13340.
16. Evans SJ, Choudary PV, Neal CR, Li JZ, Vawter MP, Tomita H, et al. (2004): Dysregulation of the fibroblast growth factor system in major depression. Proc Natl Acad Sci U S A 101:15506-15511.
17. Edgar N, Sibille E (2012): A putative functional role for oligodendrocytes in mood regulation. Transl Psychiatry 2:e109.
18. Dwivedi Y (2011): Evidence demonstrating role of microRNAs in the etiopathology of major depression. J Chem Neuroanat 42:142-156.
19. Smalheiser NR, Lugli G, Rizavi HS, Torvik VI, Turecki G, Dwivedi Y (2012): MicroRNA expression is down-regulated and reorganized in prefrontal cortex of depressed suicide subjects. PLoS One 7:e33201.
20. Schmidt HD, Shelton RC, Duman RS (2011): Functional biomarkers of depression: Diagnosis, treatment, and pathophysiology. Neuropsychopharmacology 36:2375-2394.
21. Nemeroff CB, Goldschmidt-Clermont PJ (2012): Heartache and heart-break-the link between depression and cardiovascular disease. Nat Rev Cardiol 9:526-539.
22. Miller AH, Maletic V, Raison CL (2009): Inflammation and its discontents: The role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65:732-741.
23. Belzeaux R, Bergon A, Jeanjean V, Loriod B, Formisano-Treziny C, Verrier L, et al. (2012): Responder and nonresponder patients exhibit different peripheral transcriptional signatures during major depressive episode. Transl Psychiatry 2:e185.
24. Manier DH, Shelton RC, Ellis TC, Peterson CS, Eiring A, Sulser F (2000): Human fibroblasts as a relevant model to study signal transduction in affective disorders. J Affect Disord 61:51-58.
25. Gibson SA, Korade Z, Shelton RC (2012): Oxidative stress and glutathione response in tissue cultures from persons with major depression. J Psychiatr Res 46:1326-1332.
26. Kalman S, Garbett KA, Vereczkei A, Shelton RC, Korade Z, Mirnics K (2014): Metabolic stress-induced microRNA and mRNA expression pro files of human fibroblasts. Exp Cell Res 320:343-353.
27. Scapagnini G, Davinelli S, Drago F, De Lorenzo A, Oriani G (2012): Antioxidants as antidepressants: Fact or fiction? CNS Drugs 26:477-490.
28. Lopresti AL, Maker GL, Hood SD, Drummond PD (2014): A review of peripheral biomarkers in major depression: The potential of inflammatory and oxidative stress biomarkers. Prog Neuropsychopharmacol Biol Psychiatry 48:102-111.
29. First MB, Pincus HA (2002): The DSM-IV Text Revision: Rationale and potential impact on clinical practice. Psychiatr Serv 53:288-292.
30. Akin D, Manier DH, Sanders-Bush E, Shelton RC (2004): Decreased serotonin 5-HT2A receptor-stimulated phosphoinositide signaling in fibroblasts from melancholic depressed patients. Neuropsychopharmacology 29:2081-2087.
31. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003): Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
32. Lazarov O, Robinson J, Tang YP, Hairston IS, Korade-Mirnics Z, Lee VM, et al. (2005): Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120:701-713.
33. Unger T, Korade Z, Lazarov O, Terrano D, Schor NF, Sisodia SS, Mirnics K (2005): Transcriptome differences between the frontal cortex and hippocampus of wild-type and humanized presenilin-1 transgenic mice. Am J Geriatr Psychiatry 13:1041-1051.
34. Unger T, Korade Z, Lazarov O, Terrano D, Sisodia SS, Mirnics K (2005): True and false discovery in DNA microarray experiments: Transcriptome changes in the hippocampus of presenilin 1 mutant mice. Methods 37:261-273.
35. Arion D, Unger T, Lewis DA, Levitt P, Mirnics K (2007): Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol Psychiatry 62:711-721.
36. Glorioso C, Sabatini M, Unger T, Hashimoto T, Monteggia LM, Lewis DA, Mirnics K (2006): Specificity and timing of neocortical transcriptome changes in response to BDNF gene ablation during embryogenesis or adulthood. Mol Psychiatry 11:633-648.
37. Kuehn H, Liberzon A, Reich M, Mesirov JP (2008): Using GenePattern for gene expression analysis. Curr Protoc Bioinformatics. Chapter 7: Unit 7.12.
38. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP (2007): GSEA-P: A desktop application for gene set enrichment analysis. Bioinformatics 23:3251-3253.
39. Khoury H, Naujokas MA, Zuo D, Sangwan V, Frigault MM, Petkiewicz S, et al. (2005): HGF converts ErbB2/Neu epithelial morphogenesis to cell invasion. Mol Biol Cell 16:550-561.
40. O'Carroll D, Schaefer A (2013): General principals of miRNA biogenesis and regulation in the brain. Neuropsychopharmacology 38:39-54.
41. Wang X, El Naqa IM (2008): Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24:325-332.
42. Wang X (2008): miRDB: A microRNA target prediction and functional annotation database with a wiki interface. RNA 14:1012-1017.
43. Carrington JC, Ambros V (2003): Role of microRNAs in plant and animal development. Science 301:336-338.
44. Zhang N, Lin JK, Chen J, Liu XF, Liu JL, Luo HS, et al. (2013): MicroRNA 375 mediates the signaling pathway of corticotropin-releasing factor (CRF) regulating pro-opiomelanocortin (POMC) expression by targeting mitogen-activated protein kinase 8. J Biol Chem 288:10361-10373.
45. Friedman RC, Farh KK, Burge CB, Bartel DP (2009): Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105.
46. Maes M, Yirmyia R, Noraberg J, Brene S, Hibbeln J, Perini G, et al. (2009): The inflammatory & neurodegenerative (I&ND) hypothesis of depression: Leads for future research and new drug developments in depression. Metab Brain Dis 24:27-53.
47. Hoffmann A, Spengler D (2014): DNA memories of early social life. Neuroscience 264:64-75.
48. Stringer JM, Barrand S, Western P (2013): Fine-tuning evolution: Germ-line epigenetics and inheritance. Reproduction 146:R37-R48.
49. Organ SL, Tsao MS (2011): An overview of the c-MET signaling pathway. Ther Adv Med Oncol 3(suppl 1):S7-S19.
50. Maina F, Klein R (1999): Hepatocyte growth factor, a versatile signal for developing neurons. Nat Neurosci 2:213-217.
51. van der Voort R, Taher TE, Derksen PW, Spaargaren M, van der Neut R, Pals ST (2000): The hepatocyte growth factor/Met pathway in development, tumorigenesis, and B-cell differentiation. Adv Cancer Res 79:39-90.
52. Arnold SE, Xie SX, Leung YY, Wang LS, Kling MA, Han X, et al. (2012): Plasma biomarkers of depressive symptoms in older adults. Transl Psychiatry 2:e65.
53. Nakaguchi K, Jinnou H, Kaneko N, Sawada M, Hikita T, Saitoh S, et al. (2012): Growth factors released from gelatin hydrogel microspheres increase new neurons in the adult mouse brain. Stem Cells Int 2012:915160.
54. Tanti A, Belzung C (2013): Neurogenesis along the septo-temporal axis of the hippocampus: Are depression and the action of antidepressants region-specific? Neuroscience 252:234-252.
55. Raison CL, Capuron L, Miller AH (2006): Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends Immunol 27:24-31.
56. Raison CL, Miller AH (2011): Is depression an inflammatory disorder? Curr Psychiatry Rep 13:467-475.
57. Licinio J, Frost P (2000): The neuroimmune-endocrine axis: Pathophysiological implications for the central nervous system cytokines and hypothalamus-pituitary-adrenal hormone dynamics. Braz J Med Biol Res 33:1141-1148.
58. Pandey GN, Rizavi HS, Ren X, Fareed J, Hoppensteadt DA, Roberts RC, et al. (2011): Proinflammatory cytokines in the prefrontal cortex of teenage suicide victims. J Psychiatr Res 46:57-63.
59. Galfalvy H, Zalsman G, Huang YY, Murphy L, Rosoklija G, Dwork AJ, et al. (2013): A pilot genome wide association and gene expression array study of suicide with and without major depression. World J Biol Psychiatry 14:574-582.
60. Ripke S, Wray NR, Lewis CM, Hamilton SP, Weissman MM, Breen G, et al. (2013): A mega-analysis of genome-wide association studies for major depressive disorder. Mol Psychiatry 18:497-511.
61. Song GG, Kim JH, Lee YH (2013): Genome-wide pathway analysis in major depressive disorder. J Mol Neurosci 51:428-436.
62. Jia P, Kao CF, Kuo PH, Zhao Z (2011): A comprehensive network and pathway analysis of candidate genes in major depressive disorder. BMC Syst Biol 5(suppl 3):S12.
63. Su S, Miller AH, Snieder H, Bremner JD, Ritchie J, Maisano C, et al. (2009): Common genetic contributions to depressive symptoms and inflammatory markers in middle-aged men: The Twins Heart Study. Psychosom Med 71:152-158.
64. Wong ML, Dong C, Maestre-Mesa J, Licinio J (2008): Polymorphisms in inflammation-related genes are associated with susceptibility to major depression and antidepressant response. Mol Psychiatry 13:800-812.
65. Wong ML, Dong C, Andreev V, Arcos-Burgos M, Licinio J (2012): Prediction of susceptibility to major depression by a model of interactions of multiple functional genetic variants and environmental factors. Mol Psychiatry 17:624-633.
66. Serafini G, Pompili M, Hansen KF, Obrietan K, Dwivedi Y, Shomron N, Girardi P (2014): The involvement of microRNAs in major depression, suicidal behavior, and related disorders: A focus on miR-185 and miR- 491-3p. Cell Mol Neurobiol 34:17-30.
67. Oved K, Morag A, Pasmanik-Chor M, Oron-Karni V, Shomron N, Rehavi M, et al. (2012): Genome-wide miRNA expression profiling of human lymphoblastoid cell lines identifies tentative SSRI antidepressant response biomarkers. Pharmacogenomics 13:1129-1139.
68. Mouillet-Richard S, Baudry A, Launay JM, Kellermann O (2012): MicroRNAs and depression. Neurobiol Dis 46:272-278.
69. Xu Y, Liu H, Li F, Sun N, Ren Y, Liu Z, et al. (2010): A polymorphism in the microRNA-30e precursor associated with major depressive disorder risk and P300 waveform. J Affect Disord 127:332-336.
70. Saus E, Soria V, Escaramis G, Vivarelli F, Crespo JM, Kagerbauer B, et al. (2010): Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum Mol Genet 19:4017-4025.
71. Kim AH, Reimers M, Maher B, Williamson V, McMichael O, McClay JL, et al. (2010): MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr Res 124:183-191.
72. Muinos-Gimeno M, Espinosa-Parrilla Y, Guidi M, Kagerbauer B, Sipila T, Maron E, et al. (2011): Human microRNAs miR-22, miR-138-2, miR-148a, and miR-488 are associated with panic disorder and regulate several anxiety candidate genes and related pathways. Biol Psychiatry 69:526-533.
73. Guo AY, Sun J, Jia P, Zhao Z (2010): A novel microRNA and transcription factor mediated regulatory network in schizophrenia. BMC Syst Biol 4:10.
74. Kawashima H, Numakawa T, Kumamaru E, Adachi N, Mizuno H, Ninomiya M, et al. (2010): Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 165:1301-1311.
75. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S (2005): A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A 102:16426-16431.
76. Wayman GA, Davare M, Ando H, Fortin D, Varlamova O, Cheng HY, et al. (2008): An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci U S A 105:9093-9098.
77. Baudry A, Mouillet-Richard S, Schneider B, Launay JM, Kellermann O (2010): miR-16 targets the serotonin transporter: A new facet for adaptive responses to antidepressants. Science 329:1537-1541.
78. Smalheiser NR, Lugli G, Rizavi HS, Zhang H, Torvik VI, Pandey GN, et al. (2011): MicroRNA expression in rat brain exposed to repeated inescapable shock: Differential alterations in learned helplessness vs. nonlearned helplessness. Int J Neuropsychopharmacol 14:1315-1325.
79. Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q, et al. (2008): The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J Neurosci 28:1213-1223.
80. Deng X, Zhong Y, Gu L, Shen W, Guo J (2013): MiR-21 involve in ERK-mediated upregulation of MMP9 in the rat hippocampus following cerebral ischemia. Brain Res Bull 94:56-62.
81. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002): Identification of tissue-specific microRNAs from mouse. Curr Biol 12:735-739.
82. Lynn FC (2009): Meta-regulation: MicroRNA regulation of glucose and lipid metabolism. Trends Endocrinol Metab 20:452-459.
83. Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, Fleury-Olela F, et al. (2009): Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 23:1313-1326.
84. Akin D, Manier DH, Sanders-Bush E, Shelton RC (2005): Signal transduction abnormalities in melancholic depression. Int J Neuropsychopharmacol 8:5-16.
85. Shelton RC, Mainer DH, Sulser F (1996): cAMP-dependent protein kinase activity in major depression. Am J Psychiatry 153:1037-1042.
86. Fink KD, Crane AT, Leveque X, Dues DJ, Huffman LD, Moore AC, et al. (2014): Intrastriatal transplantation of adenovirus-generated induced pluripotent stem cells for treating neuropathological and functional deficits in a rodent model of Huntington's disease. Stem Cells Transl Med 3:620-631.