Transcriptome profiling of human hippocampus dentate gyrus granule cells in mental illness

Translational Psychiatry

Volumn 4, Issue 3, 2014, Pages

  Kohen, R ^a   Dobra, A ^b   Tracy, J H ^a   Haugen, E ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Bipolar disorder; Laser capture microdissection; Major depression; MicroRNA; RNA seq; Schizophrenia

Indexed keywords

MICRORNA 182; RNA; TRANSCRIPTOME; MICRORNA; MIRN182 MICRORNA, HUMAN;

ADULT; AGED; ARTICLE; AUTOPSY; BIPOLAR DISORDER; CELL ISOLATION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GENE EXPRESSION; GENE TARGETING; GENETIC VARIABILITY; GENOTYPE; GRANULE CELL; HETEROZYGOTE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; LASER CAPTURE MICRODISSECTION; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; MENTAL DISEASE; RNA FINGERPRINTING; RNA SEQUENCE; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; HEALTH CARE FACILITY; METABOLISM; MIDDLE AGED; PROCEDURES; STANDARDS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIPOLAR DISORDER; DENTATE GYRUS; DEPRESSIVE DISORDER, MAJOR; FEMALE; GENE EXPRESSION PROFILING; GENOTYPE; HUMANS; LASER CAPTURE MICRODISSECTION; MALE; MICRORNAS; MIDDLE AGED; SCHIZOPHRENIA; TISSUE BANKS; TRANSCRIPTOME;

EID: 84903278704     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2014.9     Document Type: Article

References (93)

1. Mathers C, Fat DM, Boerma JT, World Health Organization. The Global Burden of Disease: 2004 Update. World Health Organization: Geneva, Switzerland, 2008 vii, p 146.
2. Sullivan PF. The genetics of schizophrenia. PLoS Med 2005; 2: e212.
3. Sullivan PF, Neale MC, Kendler KS. Genetic epidemiology of major depression: review and meta-analysis. Am J Psychiatry 2000; 157: 1552-1562.
4. Smoller JW, Finn CT. Family, twin, and adoption studies of bipolar disorder. Am J Med Genet C Semin Med Genet 2003; 123C: 48-58.
5. Valles V, Van Os J, Guillamat R, Gutierrez B, Campillo M, Gento P et al. Increased morbid risk for schizophrenia in families of in-patients with bipolar illness. Schizophr Res 2000; 42: 83-90.
6. McGuffin P, Rijsdijk F, Andrew M, Sham P, Katz R, Cardno A. The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Arch Gen Psychiatry 2003; 60: 497-502.
7. Lichtenstein P, Yip BH, Bjork C, Pawitan Y, Cannon TD, Sullivan PF et al. Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 2009; 373: 234-239.
8. Blackwood DH, Pickard BJ, Thomson PA, Evans KL, Porteous DJ, Muir WJ. Are some genetic risk factors common to schizophrenia, bipolar disorder and depression? Evidence from DISC1, GRIK4 and NRG1. Neurotox Res 2007; 11: 73-83.
9. Blackwood DH, Fordyce A, Walker MTSt, Clair DM, Porteous DJ, Muir WJ. Schizophrenia and affective disorders-cosegregation with a translocation at chromosome 1q42 that directly disrupts brain-expressed genes: clinical and P300 findings in a family. Am J Hum Genet 2001; 69: 428-433.
10. Konradi C, Sillivan SE, Clay HB. Mitochondria, oligodendrocytes and inflammation in bipolar disorder: evidence from transcriptome studies points to intriguing parallels with multiple sclerosis. Neurobiol Dis 2012; 45: 37-47.
11. Clay HB, Sillivan S, Konradi C. Mitochondrial dysfunction and pathology in bipolar disorder and schizophrenia. Int J Dev Neurosci 2011; 29: 311-324.
12. Altar CA, Vawter MP, Ginsberg SD. Target identification for CNS diseases by transcriptional profiling. Neuropsychopharmacology 2009; 34: 18-54.
13. Sequeira PA, Martin MV, Vawter MP. The first decade and beyond of transcriptional profiling in schizophrenia. Neurobiol Dis 2012; 45: 23-36.
14. Elashoff M, Higgs BW, Yolken RH, Knable MB, Weis S, Webster MJ et al. Metaanalysis of 12 genomic studies in bipolar disorder. J Mol Neurosci 2007; 31: 221-243.
15. Sokolov BP. Oligodendroglial abnormalities in schizophrenia, mood disorders and substance abuse. Comorbidity, shared traits, or molecular phenocopies? Int J Neuropsychopharmacol 2007; 10: 547-555.
16. Fillman SG, Cloonan N, Catts VS, Miller LC, Wong J, McCrossin T et al. Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia. Mol Psychiatry 2013; 18: 206-214.
17. Hwang Y, Kim J, Shin JY, Kim JI, Seo JS, Webster MJ et al. Gene expression profiling by mRNA sequencing reveals increased expression of immune/inflammationrelated genes in the hippocampus of individuals with schizophrenia. Transl Psychiatry 2013; 3: e321.
18. Wu JQ, Wang X, Beveridge NJ, Tooney PA, Scott RJ, Carr VJ et al. Transcriptome sequencing revealed significant alteration of cortical promoter usage and splicing in schizophrenia. PLoS One 2012; 7: e36351.
19. DeCarolis NA, Eisch AJ. Hippocampal neurogenesis as a target for the treatment of mental illness: a critical evaluation. Neuropharmacology 2010; 58: 884-893.
20. Adriano F, Caltagirone C, Spalletta G. Hippocampal volume reduction in firstepisode and chronic schizophrenia: a review and meta-analysis. Neuroscientist 2012; 18: 180-200.
21. Shepherd AM, Laurens KR, Matheson SL, Carr VJ, Green MJ. Systematic metareview and quality assessment of the structural brain alterations in schizophrenia. Neurosci Biobehav Rev 2012; 36: 1342-1356.
22. Frey BN, Andreazza AC, Nery FG, Martins MR, Quevedo J, Soares JC et al. The role of hippocampus in the pathophysiology of bipolar disorder. Behav Pharmacol 2007; 18: 419-430.
23. Chen CH, Suckling J, Lennox BR, Ooi C, Bullmore ET. A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disord 2011; 13: 1-15.
24. Eker C, Gonul AS. Volumetric MRI studies of the hippocampus in major depressive disorder: Meanings of inconsistency and directions for future research. World J Biol Psychiatry 2010; 11: 19-35.
25. McKinnon MC, Yucel K, Nazarov A, MacQueen GM. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci 2009; 34: 41-54.
26. Konradi C, Yang CK, Zimmerman EI, Lohmann KM, Gresch P, Pantazopoulos H et al. Hippocampal interneurons are abnormal in schizophrenia. Schizophr Res 2011; 131: 165-173.
27. Konradi C, Zimmerman EI, Yang CK, Lohmann KM, Gresch P, Pantazopoulos H et al. Hippocampal interneurons in bipolar disorder. Arch Gen Psychiatry 2011; 68: 340-350.
28. Walton NM, Zhou Y, Kogan JH, Shin R, Webster M, Gross AK et al. Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Transl Psychiatry 2012; 2: e135.
29. Higgs BW, Elashoff M, Richman S, Barci B. An online database for brain disease research. BMC Genomics 2006; 7: 70.
30. Kim S, Webster MJ. 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 2010; 35: 473-482.
31. Datson NA, Meijer L, Steenbergen PJ, Morsink MC, van der Laan S, Meijer OC et al. Expression profiling in laser-microdissected hippocampal subregions in rat brain reveals large subregion-specific differences in expression. Eur J Neurosci 2004; 20: 2541-2554.
32. Lein ES, Zhao X, Gage FH. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci 2004; 24: 3879-3889.
33. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT et al. Genomic anatomy of the hippocampus. Neuron 2008; 60: 1010-1021.
34. Christensen T, Bisgaard CF, Nielsen HB, Wiborg O. Transcriptome differentiation along the dorso-ventral axis in laser-captured microdissected rat hippocampal granular cell layer. Neuroscience 2010; 170: 731-741.
35. Hanson ND, Owens MJ, Nemeroff CB. Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 2011; 36: 2589-2602.
36. Balu DT, Lucki I. Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 2009; 33: 232-252.
37. Samuels BA, Hen R. Neurogenesis and affective disorders. Eur J Neurosci 2011; 33: 1152-1159.
38. Cheng L, Zhang S, Maclennan GT, Williamson SR, Davidson DD, Wang M et al. Laser-assisted microdissection in translational research: theory, technical considerations, and future applications. Appl Immunohistochem Mol Morphol 2012; 21: 31-47.
39. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH. The stanley foundation brain collection and neuropathology consortium. Schizophr Res 2000; 44: 151-155.
40. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26: 841-842.
41. Ueda HR, Hayashi S, Matsuyama S, Yomo T, Hashimoto S, Kay SA et al. Universality and flexibility in gene expression from bacteria to human. Proc Natl Acad Sci USA 2004; 101: 3765-3769.
42. Bullard JH, Purdom E, Hansen KD, Dudoit S. Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 2010; 11: 94.
43. Wang S, Wang L, Zhu T, Gao X, Li J, Wu Y et al. Improvement of tissue preparation for laser capture microdissection: application for cell type-specific miRNA expression profiling in colorectal tumors. BMC Genomics 2010; 11: 163.
44. Li Y, Li T, Liu S, Qiu M, Han Z, Jiang Z et al. Systematic comparison of the fidelity of aRNA, mRNA and T-RNA on gene expression profiling using cDNA microarray. J Biotechnol 2004; 107: 19-28.
45. Zhu B, Xu F, Baba Y. An evaluation of linear RNA amplification in cDNA microarray gene expression analysis. Mol Genet Metab 2006; 87: 71-79.
46. Clement-Ziza M, Gentien D, Lyonnet S, Thiery JP, Besmond C, Decraene C. Evaluation of methods for amplification of picogram amounts of total RNA for whole genome expression profiling. BMC Genomics 2009; 10: 246.
47. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5: 621-628.
48. Saus E, Soria V, Escaramis G, Vivarelli F, Crespo JM, Kagerbauer B et al. Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum Mol Genet 2010; 19: 4017-4025.
49. Wei C, Li J, Bumgarner RE. Sample size for detecting differentially expressed genes in microarray experiments. BMC Genomics 2004; 5: 87.
50. Weis S, Llenos IC, Dulay JR, Elashoff M, Martinez-Murillo F, Miller CL. Quality control for microarray analysis of human brain samples: the impact of postmortem factors, RNA characteristics, and histopathology. J Neurosci Methods 2007; 165: 198-209.
51. Vawter MP, Tomita H, Meng F, Bolstad B, Li J, Evans S et al. Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders. Mol Psychiatry 2006; 117: 663-679.
52. Webster MJ. Tissue preparation and banking. Prog Brain Res 2006; 158: 3-14.
53. Chevyreva I, Faull RL, Green CR, Nicholson LF. Assessing RNA quality in postmortem human brain tissue. Exp Mol Pathol 2008; 84: 71-77.
54. Birdsill AC, Walker DG, Lue L, Sue LI, Beach TG. Postmortem interval effect on RNA and gene expression in human brain tissue. Cell Tissue Bank 2011; 12: 311-318.
55. Chan MK, Tsang TM, Harris LW, Guest PC, Holmes E, Bahn S. Evidence for disease and antipsychotic medication effects in post-mortem brain from schizophrenia patients. Mol Psychiatry 2011; 16: 1189-1202.
56. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK et al. Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 2005; 65: 4051-4058.
57. Altar CA, Jurata LW, Charles V, Lemire A, Liu P, Bukhman Y et al. Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry 2005; 58: 85-96.
58. Mellios N, Sugihara H, Castro J, Banerjee A, Le C, Kumar A et al. miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat Neurosci 2011; 14: 1240-1242.
59. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N. microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nature Neuroscience advance online publication, 8 April 2012; doi:10.1038/nn.3082.
60. Magill ST, Cambronne XA, Luikart BW, Lioy DT, Leighton BH, Westbrook GL et al. microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci USA 2010; 107: 20382-20387.
61. Lambert TJ, Storm DR, Sullivan JM. MicroRNA132 modulates short-term synaptic plasticity but not basal release probability in hippocampal neurons. PLoS One 2010; 5: e15182.
62. Luikart BW, Perederiy JV, Westbrook GL. Dentate gyrus neurogenesis, integration and microRNAs. Behav Brain Res 2012; 227: 348-355.
63. Xu B, Karayiorgou M, Gogos JA. MicroRNAs in psychiatric and neurodevelopmental disorders. Brain Res 2010; 1338: 78-88.
64. Miller BH, Wahlestedt C. MicroRNA dysregulation in psychiatric disease. Brain Res 2010; 1338: 89-99.
65. Im HI, Kenny PJ. MicroRNAs in neuronal function and dysfunction. Trends Neurosci 2012; 35: 325-334.
66. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA et al. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 2007; 8: R27.
67. Beveridge NJ, Tooney PA, Carroll AP, Gardiner E, Bowden N, Scott RJ et al. Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum Mol Genet 2008; 17: 1156-1168.
68. Zhu Y, Kalbfleisch T, Brennan MD, Li Y. A MicroRNA gene is hosted in an intron of a schizophrenia-susceptibility gene. Schizophr Res 2009; 109: 86-89.
69. Beveridge NJ, Gardiner E, Carroll AP, Tooney PA, Cairns MJ. Schizophrenia is associated with an increase in cortical microRNA biogenesis. Mol Psychiatry 2010; 15: 1176-1189.
70. Santarelli DM, Beveridge NJ, Tooney PA, Cairns MJ. Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol Psychiatry 2011; 69: 180-187.
71. Mellios N, Galdzicka M, Ginns E, Baker SP, Rogaev E, Xu J et al. Gender-specific reduction of estrogen-sensitive small RNA, miR-30b, in subjects with schizophrenia. Schizophr Bull 2012; 38: 433-443.
72. Kim AH, Reimers M, Maher B, Williamson V, McMichael O, McClay JL et al. MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr Res 2010; 124: 183-191.
73. Moreau MP, Bruse SE, David-Rus R, Buyske S, Brzustowicz LM. Altered microRNA expression profiles in postmortem brain samples from individuals with schizophrenia and bipolar disorder. Biol Psychiatry 2011; 69: 188-193.
74. Miller BH, Zeier Z, Xi L, Lanz TA, Deng S, Strathmann J et al. MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc Natl Acad Sci USA 2012; 109: 3125-3130.
75. Smalheiser NR, Lugli G, Rizavi HS, Torvik VI, Turecki G, Dwivedi Y. MicroRNA expression is down-regulated and reorganized in prefrontal cortex of depressed suicide subjects. PLoS One 2012; 7: e33201.
76. Gantier MP, McCoy CE, Rusinova I, Saulep D, Wang D, Xu D et al. Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res 2011; 39: 5692-5703.
77. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stressdependent cardiac growth and gene expression by a microRNA. Science 2007; 316: 575-579.
78. Gatfield D, Le Martelot G, Vejnar CE, Gerlach D, Schaad O, Fleury-Olela F et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev 2009; 23: 1313-1326.
79. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, Richter J et al. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 2010; 141: 618-631.
80. Sethi P, Lukiw WJ. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neocortex. Neurosci Lett 2009; 459: 100-104.
81. Beveridge NJ, Cairns MJ. MicroRNA dysregulation in schizophrenia. Neurobiol Dis 2012; 46: 263-271.
82. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A et al. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 2005; 33: 2697-2706.
83. Mihelich BL, Khramtsova EA, Arva N, Vaishnav A, Johnson DN, Giangreco AA et al. miR-183-96-182 cluster is overexpressed in prostate tissue and regulates zinc homeostasis in prostate cells. J Biol Chem 2011; 286: 44503-44511.
84. Ceribelli A, Satoh M, Chan EK. MicroRNAs and autoimmunity. Curr Opin Immunol 2012; 24: 686-691.
85. Yao E, Ventura A. A new role for miR-182 in DNA repair. Mol Cell 2011; 41: 135-137.
86. Wang XR, Zhang XM, Du J, Jiang H. MicroRNA-182 regulates otocyst-derived cell differentiation and targets T-box1 gene. Hear Res 2012; 286: 55-63.
87. Kim KM, Park SJ, Jung SH, Kim EJ, Jogeswar G, Ajita J et al. miR-182 is a negative regulator of osteoblast proliferation, differentiation, and skeletogenesis through targeting FoxO1. J Bone Miner Res 2012; 27: 1669-1679.
88. Yu B, Qian T, Wang Y, Zhou S, Ding G, Ding F et al. miR-182 inhibits Schwann cell proliferation and migration by targeting FGF9 and NTM, respectively at an early stage following sciatic nerve injury. Nucleic Acids Res 2012; 40: 10356-10365.
89. Aldrich BT, Frakes EP, Kasuya J, Hammond DL, Kitamoto T. Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience 2009; 164: 711-723.
90. Clokie SJ, Lau P, Kim HH, Coon SL, Klein DC. MicroRNAs in the pineal gland: miR-483 regulates melatonin synthesis by targeting arylalkylamine n-acetyltransferase. J Biol Chem 2012; 287: 25312-25324.
91. Pritchett D, Wulff K, Oliver PL, Bannerman DM, Davies KE, Harrison PJ et al. Evaluating the links between schizophrenia and sleep and circadian rhythm disruption. J Neural Transm 2012; 119: 1061-1075.
92. Wulff K, Dijk DJ, Middleton B, Foster RG, Joyce EM. Sleep and circadian rhythm disruption in schizophrenia. Br J Psychiatry 2012; 200: 308-316.
93. Kronfeld-Schor N, Einat H. Circadian rhythms and depression: human psychopathology and animal models. Neuropharmacology 2012; 62: 101-114.