MicroRNA profiling of neurons generated using induced pluripotent stem cells derived from patients with schizophrenia and schizoaffective disorder, and 22q11.2 del

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Zhao, Dejian ^a   Lin, Mingyan ^a   Chen, Jian ^a   Pedrosa, Erika ^a   Hrabovsky, Anastasia ^a   Fourcade, H Matthew ^a   Zheng, Deyou ^a   Lachman, Herbert M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

ADULT; ARTICLE; AUTOPSY; BLOOD SAMPLING; CHROMOSOME DELETION 22Q11; CLINICAL ARTICLE; CONTROLLED STUDY; DGCR8 GENE; DOWN REGULATION; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; GENE MAPPING; GENETIC ASSOCIATION; HAPLOINSUFFICIENCY; HUMAN; HUMAN CELL; MALE; MENTAL DISEASE; MENTAL PATIENT; METHODOLOGY; NERVE CELL; NEUROLOGIC DISEASE; PLURIPOTENT STEM CELL; RNA SEQUENCE; RNA SYNTHESIS; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; UPREGULATION; CHROMOSOME 22; CHROMOSOME DELETION; GENE REGULATORY NETWORK; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MIDDLE AGED; PATHOLOGY; PSYCHOSIS; SEQUENCE ANALYSIS;

ADULT; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, PAIR 22; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICRORNAS; MIDDLE AGED; NEURONS; PSYCHOTIC DISORDERS; SCHIZOPHRENIA; SEQUENCE ANALYSIS, RNA;

EID: 84940780822     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132387     Document Type: Article

References (147)

1. Liu J, Githinji J, Mclaughlin B, Wilczek K, Nolta J. Role of miRNAs in neuronal differentiation from human embryonic stem cell-derived neural stem cells. Stem Cell Rev. 2012; 8: 1129-1137. doi: 10.1007/s12015-012-9411-6 PMID: 23054963
2. Hsu R, Schofield CM, Dela Cruz CG, Jones-Davis DM, Blelloch R, Ullian EM. Loss of microRNAs in pyramidal neurons leads to specific changes in inhibitory synaptic transmission in the prefrontal cortex. Mol Cell Neurosci. 2012; 50: 283-292. doi: 10.1016/j.mcn.2012.06.002 PMID: 22728723
3. Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, Mouri G, et al. Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med. 2012; 18: 1087-1094. doi: 10.1038/nm.2834 PMID: 22683779
4. Konopka W, Kiryk A, Novak M, Herwerth M, Parkitna JR, Wawrzyniak M, et al. MicroRNA loss enhances learning and memory in mice. J Neurosci. 2010; 30: 14835-14842. doi: 10.1523/JNEUROSCI.3030-10.2010 PMID: 21048142
5. 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. doi: 10.1371/journal.pone.0015182 PMID: 21206919
6. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA. 2003; 9: 1274-1281. PMID: 13130141
7. Smalheiser NR, Lugli G. microRNA regulation of synaptic plasticity. Neuromolecular Med. 2009; 11: 133-140. doi: 10.1007/s12017-009-8065-2 PMID: 19458942
8. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004; 5: R13. doi: 10.1186/gb-2004-5-3-r13 PMID: 15003116
9. Meza-Sosa KF, Pedraza-Alva G, Perez-Martinez L. microRNAs: Key triggers of neuronal cell fate. Front Cell Neurosci. 2014; 8: 175. doi: 10.3389/fncel.2014.00175 PMID: 25009466
10. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009; 136: 215-233. doi: 10.1016/j.cell.2009.01.002 PMID: 19167326
11. Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006; 11: 441-450. doi: 10.1016/j.devcel.2006.09.009 PMID: 17011485
12. Chitwood DH, Timmermans MC. Small RNAs are on the move. Nature. 2010; 467: 415-419. doi: 10.1038/nature09351 PMID: 20864994
13. Slezak-Prochazka I, Durmus S, Kroesen BJ, van den Berg A. MicroRNAs, macrocontrol: Regulation of miRNA processing. RNA. 2010; 16: 1087-1095. doi: 10.1261/rna.1804410 PMID: 20423980
14. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014; 15: 509-524. doi: 10.1038/nrm3838 PMID: 25027649
15. Stappert L, Roese-Koerner B, Brustle O. The role of microRNAs in human neural stem cells, neuronal differentiation and subtype specification. Cell Tissue Res. 2015; 359: 47-64. doi: 10.1007/s00441-014-1981-y PMID: 25172833
16. Schizophrenia Psychiatric Genome-Wide Association Study (GWAS) Consortium. Genome-wide association study identifies five new schizophrenia loci. Nat Genet. 2011; 43: 969-976. doi: 10.1038/ng.940 PMID: 21926974
17. Lett TA, Chakavarty MM, Felsky D, Brandl EJ, Tiwari AK, Goncalves VF, et al. The genome-wide supported microRNA-137 variant predicts phenotypic heterogeneity within schizophrenia. Mol Psychiatry. 2013. doi: 10.1038/mp.2013.17
18. Green MJ, Cairns MJ, Wu J, Dragovic M, Jablensky A, Tooney PA, et al. Genome-wide supported variant MIR137 and severe negative symptoms predict membership of an impaired cognitive subtype of schizophrenia. Mol Psychiatry. 2012. doi: 10.1038/mp.2012.84
19. Das S, Chang C. Regulation of early xenopus embryogenesis by smad ubiquitination regulatory factor 2. Dev Dyn. 2012; 241: 1260-1273. doi: 10.1002/dvdy.23811 PMID: 22674516
20. Kwon E, Wang W, Tsai LH. Validation of schizophrenia-associated genes CSMD1, C10orf26, CAC-NA1C and TCF4 as miR-137 targets. Mol Psychiatry. 2013; 18: 11-12. doi: 10.1038/mp.2011.170 PMID: 22182936
21. Kim AH, Parker EK, Williamson V, McMichael GO, Fanous AH, Vladimirov VI. Experimental validation of candidate schizophrenia gene ZNF804A as target for hsa-miR-137. Schizophr Res. 2012; 141: 60-64. doi: 10.1016/j.schres.2012.06.038 PMID: 22883350
22. 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. doi: 10.1016/j.biopsych.2010.09.030 PMID: 21111402
23. 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. doi: 10.1016/j.biopsych.2010.09.039 PMID: 21183010
24. Beveridge NJ, Santarelli DM, Wang X, Tooney PA, Webster MJ, Weickert CS, et al. Maturation of the human dorsolateral prefrontal cortex coincides with a dynamic shift in MicroRNA expression. Schizophr Bull. 2013. doi: 10.1093/schbul/sbs198
25. Scambler PJ, Kelly D, Lindsay E, Williamson R, Goldberg R, Shprintzen R, et al. Velo-cardio-facial syndrome associated with chromosome 22 deletions encompassing the DiGeorge locus. Lancet. 1992; 339: 1138-1139. PMID: 1349369
26. Carlson C, Papolos D, Pandita RK, Faedda GL, Veit S, Goldberg R, et al. Molecular analysis of velocardio-facial syndrome patients with psychiatric disorders. Am J Hum Genet. 1997; 60: 851-859. PMID: 9106531
27. Carlson C, Sirotkin H, Pandita R, Goldberg R, McKie J, Wadey R, et al. Molecular definition of 22q11 deletions in 151 velo-cardio-facial syndrome patients. Am J Hum Genet. 1997; 61: 620-629. doi: 10.1086/515508 PMID: 9326327
28. Driscoll DA, Spinner NB, Budarf ML, McDonald-McGinn DM, Zackai EH, Goldberg RB, et al. Deletions and microdeletions of 22q11.2 in velo-cardio-facial syndrome. Am J Med Genet. 1992; 44: 261-268. doi: 10.1002/ajmg.1320440237 PMID: 1360769
29. Edelmann L, Pandita RK, Spiteri E, Funke B, Goldberg R, Palanisamy N, et al. A common molecular basis for rearrangement disorders on chromosome 22q11. Hum Mol Genet. 1999; 8: 1157-1167. PMID: 10369860
30. Brzustowicz LM, Bassett AS. miRNA-mediated risk for schizophrenia in 22q11.2 deletion syndrome. Front Genet. 2012; 3: 291. doi: 10.3389/fgene.2012.00291 PMID: 23248646
31. Stark KL, Xu B, Bagchi A, Lai WS, Liu H, Hsu R, et al. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat Genet. 2008; 40: 751-760. doi: 10.1038/ng.138 PMID: 18469815
32. Shprintzen RJ, Goldberg RB, Lewin ML, Sidoti EJ, Berkman MD, Argamaso RV, et al. A new syndrome involving cleft palate, cardiac anomalies, typical facies, and learning disabilities: Velo-cardiofacial syndrome. Cleft Palate J. 1978; 15: 56-62. PMID: 272242
33. Papolos DF, Veit S, Faedda GL, Saito T, Lachman HM. Ultra-ultra rapid cycling bipolar disorder is associated with the low activity catecholamine-O-methyltransferase allele. Mol Psychiatry. 1998; 3: 346-349. PMID: 9702745
34. Lachman HM, Morrow B, Shprintzen R, Veit S, Parsia SS, Faedda G, et al. Association of codon 108/158 catechol-O-methyltransferase gene polymorphism with the psychiatric manifestations of velo-cardio-facial syndrome. Am J Med Genet. 1996; 67: 468-472. doi: 2-G. PMID: 8886163
35. Murphy KC, Owen MJ. Velo-cardio-facial syndrome: A model for understanding the genetics and pathogenesis of schizophrenia. Br J Psychiatry. 2001; 179: 397-402. PMID: 11689394
36. Aneja A, Fremont WP, Antshel KM, Faraone SV, AbdulSabur N, Higgins AM, et al. Manic symptoms and behavioral dysregulation in youth with velocardiofacial syndrome (22q11.2 deletion syndrome). J Child Adolesc Psychopharmacol. 2007; 17: 105-114. doi: 10.1089/cap.2006.0023 PMID: 17343558
37. Kates WR, Antshel KM, Fremont WP, Shprintzen RJ, Strunge LA, Burnette CP, et al. Comparing phenotypes in patients with idiopathic autism to patients with velocardiofacial syndrome (22q11 DS) with and without autism. Am J Med Genet A. 2007; 143A: 2642-2650. doi: 10.1002/ajmg.a.32012 PMID: 17937445
38. Ivanov D, Kirov G, Norton N, Williams HJ, Williams NM, Nikolov I, et al. Chromosome 22q11 deletions, velo-cardio-facial syndrome and early-onset psychosis. molecular genetic study. Br J Psychiatry. 2003; 183: 409-413. PMID: 14594915
39. Schneider M, Debbane M, Bassett AS, Chow EW, Fung WL, van den Bree M, et al. Psychiatric disorders from childhood to adulthood in 22q11.2 deletion syndrome: Results from the international consortium on brain and behavior in 22q11.2 deletion syndrome. Am J Psychiatry. 2014; 171: 627-639. doi: 1838527 [pii]. PMID: 24577245
40. Gothelf D, Schneider M, Green T, Debbane M, Frisch A, Glaser B, et al. Risk factors and the evolution of psychosis in 22q11.2 deletion syndrome: A longitudinal 2-site study. J Am Acad Child Adolesc Psychiatry. 2013; 52: 1192-1203.e3. doi: 10.1016/j.jaac.2013.08.008 PMID: 24157393
41. Bassett AS, Chow EW. Schizophrenia and 22q11.2 deletion syndrome. Curr Psychiatry Rep. 2008; 10: 148-157. PMID: 18474208
42. Ahn K, Gotay N, Andersen TM, Anvari AA, Gochman P, Lee Y, et al. High rate of disease-related copy number variations in childhood onset schizophrenia. Mol Psychiatry. 2014; 19: 568-572. doi: 10.1038/mp.2013.59 PMID: 23689535
43. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM, et al. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell. 2001; 104: 619-629. PMID: 11239417
44. Hiramoto T, Kang G, Suzuki G, Satoh Y, Kucherlapati R, Watanabe Y, et al. Tbx1: Identification of a 22q11.2 gene as a risk factor for autism spectrum disorder in a mouse model. Hum Mol Genet. 2011; 20: 4775-4785. doi: 10.1093/hmg/ddr404 PMID: 21908517
45. Xu B, Roos JL, Dexheimer P, Boone B, Plummer B, Levy S, et al. Exome sequencing supports a de novo mutational paradigm for schizophrenia. Nat Genet. 2011; 43: 864-868. doi: 10.1038/ng.902 PMID: 21822266
46. Li T, Ma X, Hu X, Wang Y, Yan C, Meng H, et al. PRODH gene is associated with executive function in schizophrenic families. Am J Med Genet B Neuropsychiatr Genet. 2007. doi: 10.1002/ajmg.b.30648
47. Karayiorgou M, Gogos JA. The molecular genetics of the 22q11-associated schizophrenia. Brain Res Mol Brain Res. 2004; 132: 95-104. doi: 10.1016/j.molbrainres.2004.09.029 PMID: 15582150
48. Schofield CM, Hsu R, Barker AJ, Gertz CC, Blelloch R, Ullian EM. Monoallelic deletion of the micro-RNA biogenesis gene Dgcr8 produces deficits in the development of excitatory synaptic transmission in the prefrontal cortex. Neural Dev. 2011; 6: 11-8104-6-11. doi: 10.1186/1749-8104-6-11
49. Forstner AJ, Basmanav FB, Mattheisen M, Bohmer AC, Hollegaard MV, Janson E, et al. Investigation of the involvement of MIR185 and its target genes in the development of schizophrenia. J Psychiatry Neurosci. 2014; 39: 386-396. doi: 10.1503/jpn.130189 [pii]. PMID: 24936775
50. Xu B, Hsu PK, Stark KL, Karayiorgou M, Gogos JA. Derepression of a neuronal inhibitor due to miRNA dysregulation in a schizophrenia-related microdeletion. Cell. 2013; 152: 262-275. doi: 10.1016/j.cell.2012.11.052 PMID: 23332760
51. Earls LR, Fricke RG, Yu J, Berry RB, Baldwin LT, Zakharenko SS. Age-dependent microRNA control of synaptic plasticity in 22q11 deletion syndrome and schizophrenia. J Neurosci. 2012; 32: 14132-14144. doi: 10.1523/JNEUROSCI.1312-12.2012 PMID: 23055483
52. Belkaya S, Murray SE, Eitson JL, de la Morena MT, Forman JA, van Oers NS. Transgenic expression of microRNA-185 causes a developmental arrest of T cells by targeting multiple genes including Mzb1. J Biol Chem. 2013; 288: 30752-30762. doi: 10.1074/jbc.M113.503532 PMID: 24014023
53. de la Morena MT, Eitson JL, Dozmorov IM, Belkaya S, Hoover AR, Anguiano E, et al. Signature Micro-RNA expression patterns identified in humans with 22q11.2 deletion/DiGeorge syndrome. Clin Immunol. 2013; 147: 11-22. doi: 10.1016/j.clim.2013.01.011 PMID: 23454892
54. Irish Schizophrenia Genomics Consortium and the Wellcome Trust Case Control Consortium 2. Genome-wide association study implicates HLA-C&z.ast;01:02 as a risk factor at the major histocompatibility complex locus in schizophrenia. Biol Psychiatry. 2012; 72: 620-628. doi: 10.1016/j.biopsych.2012.05.035 PMID: 22883433
55. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014; 511: 421-427. doi: 10.1038/nature13595
56. Sheridan SD, Theriault KM, Reis SA, Zhou F, Madison JM, Daheron L, et al. Epigenetic characterization of the FMR1 gene and aberrant neurodevelopment in human induced pluripotent stem cell models of fragile X syndrome. PLoS One. 2011; 6: e26203. doi: 10.1371/journal.pone.0026203 PMID: 22022567
57. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature. 2011. doi: 10.1038/nature09915
58. Chamberlain SJ, Chen PF, Ng KY, Bourgois-Rocha F, Lemtiri-Chlieh F, Levine ES, et al. Induced pluripotent stem cell models of the genomic imprinting disorders angelman and prader-willi syndromes. Proc Natl Acad Sci U S A. 2010; 107: 17668-17673. doi: 10.1073/pnas.1004487107 PMID: 20876107
59. Chiang CH, Su Y, Wen Z, Yoritomo N, Ross CA, Margolis RL, et al. Integration-free induced pluripotent stem cells derived from schizophrenia patients with a DISC1 mutation. Mol Psychiatry. 2011. doi: 10.1038/mp.2011.13
60. DeRosa BA, Van Baaren JM, Dubey GK, Lee JM, Cuccaro ML, Vance JM, et al. Derivation of autism spectrum disorder-specific induced pluripotent stem cells from peripheral blood mononuclear cells. Neurosci Lett. 2012; 516: 9-14. doi: 10.1016/j.neulet.2012.02.086 PMID: 22405972
61. Farra N, Zhang WB, Pasceri P, Eubanks JH, Salter MW, Ellis J. Rett syndrome induced pluripotent stem cell-derived neurons reveal novel neurophysiological alterations. Mol Psychiatry. 2012. doi: 10.1038/mp.2011.180
62. Kim KY, Jung YW, Sullivan GJ, Chung L, Park IH. Cellular reprogramming: A novel tool for investigating autism spectrum disorders. Trends Mol Med. 2012. doi: 10.1016/j.molmed.2012.06.002
63. Lin M, Hrabovsky A, Pedrosa E, Wang T, Zheng D, Lachman HM. Allele-biased expression in differentiating human neurons: Implications for neuropsychiatric disorders. PLoS One. 2012; 7: e44017. doi: 10.1371/journal.pone.0044017 PMID: 22952857
64. Lin M, Pedrosa E, Shah A, Hrabovsky A, Maqbool S, Zheng D, et al. RNA-seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatric disorders. PLoS One. 2011; 6: e23356. doi: 10.1371/journal.pone.0023356 PMID: 21915259
65. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, et al. A model for neural development and treatment of rett syndrome using human induced pluripotent stem cells. Cell. 2010; 143: 527-539. doi: 10.1016/j.cell.2010.10.016 PMID: 21074045
66. Tian Y, Voineagu I, Pasca SP, Won H, Chandran V, Horvath S, et al. Alteration in basal and depolarization induced transcriptional network in iPSC derived neurons from timothy syndrome. Genome Med. 2014; 6: 75-014-0075-5. eCollection 2014. doi: 10.1186/s13073-014-0075-5
67. Zhao WN, Cheng C, Theriault KM, Sheridan SD, Tsai LH, Haggarty SJ. A high-throughput screen for Wnt/beta-catenin signaling pathway modulators in human iPSC-derived neural progenitors. J Biomol Screen. 2012; 17: 1252-1263. doi: 10.1177/1087057112456876 PMID: 22923789
68. Wen Z, Nguyen HN, Guo Z, Lalli MA, Wang X, Su Y, et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature. 2014; 515: 414-418. doi: 10.1038/nature13716 PMID: 25132547
69. Okita K, Matsumura Y, Sato Y, Okada A, Morizane A, Okamoto S, et al. A more efficient method to generate integration-free human iPS cells. Nat Methods. 2011; 8: 409-412. doi: 10.1038/nmeth.1591 PMID: 21460823
70. Muenthaisong S, Ujhelly O, Polgar Z, Varga E, Ivics Z, Pirity MK, et al. Generation of mouse induced pluripotent stem cells from different genetic backgrounds using sleeping beauty transposon mediated gene transfer. Exp Cell Res. 2012; 318: 2482-2489. doi: 10.1016/j.yexcr.2012.07.014 PMID: 22846649
71. Pal R, Mamidi MK, Das AK, Bhonde R. Comparative analysis of cardiomyocyte differentiation from human embryonic stem cells under 3-D and 2-D culture conditions. J Biosci Bioeng. 2012. doi: 10.1016/j.jbiosc.2012.08.018
72. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126: 663-676. doi: 10.1016/j.cell.2006.07.024 PMID: 16904174
73. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131: 861-872. doi: 10.1016/j.cell.2007.11.019 PMID: 18035408
74. Pantano L, Estivill X, Marti E. SeqBuster, a bioinformatic tool for the processing and analysis of small RNAs datasets, reveals ubiquitous miRNA modifications in human embryonic cells. Nucleic Acids Res. 2010; 38: e34. doi: 10.1093/nar/gkp1127 PMID: 20008100
75. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10: R25. doi: 10.1186/gb-2009-10-3-r25 PMID: 19261174
76. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, et al. GENCODE: The reference human genome annotation for the ENCODE project. Genome Res. 2012; 22: 1760-1774. doi: 10.1101/gr.135350.111 PMID: 22955987
77. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15: 550. doi: s13059-014-0550-8 [pii]. PMID: 25516281
78. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990; 9: 811-818. PMID: 2218183
79. Green GH, Diggle PJ. On the operational characteristics of the benjamini and hochberg false discovery rate procedure. Stat Appl Genet Mol Biol. 2007; 6: Article27. doi: 10.2202/1544-6115.1302
80. Vlachos IS, Paraskevopoulou MD, Karagkouni D, Georgakilas G, Vergoulis T, Kanellos I, et al. DIANA-TarBase v7.0: Indexing more than half a million experimentally supported miRNA:MRNA interactions. Nucleic Acids Res. 2015; 43: D153-9. doi: 10.1093/nar/gku1215 PMID: 25416803
81. Vergoulis T, Kanellos I, Kostoulas N, Georgakilas G, Sellis T, Hatzigeorgiou A, et al. mirPub: A database for searching microRNA publications. Bioinformatics. 2014. doi: btu819 [pii].
82. Xiao F, Zuo Z, Cai G, Kang S, Gao X, Li T. miRecords: An integrated resource for microRNA-target interactions. Nucleic Acids Res. 2009; 37: D105-10. doi: 10.1093/nar/gkn851 PMID: 18996891
83. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009; 19: 92-105. doi: 10.1101/gr.082701.108 PMID: 18955434
84. Lin M, Zhao D, Hrabovsky A, Pedrosa E, Zheng D, Lachman HM. Heat shock alters the expression of schizophrenia and autism candidate genes in an induced pluripotent stem cell model of the human telencephalon. PLoS One. 2014; 9: e94968. doi: 10.1371/journal.pone.0094968 PMID: 24736721
85. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4: 44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956
86. Isserlin R, Merico D, Voisin V, Bader GD. Enrichment map-a cytoscape app to visualize and explore OMICs pathway enrichment results. F1000Res. 2014; 3: 141. doi: 10.12688/f1000research.4536.1 PMID: 25075306
87. Binns D, Dimmer E, Huntley R, Barrell D, O'Donovan C, Apweiler R. QuickGO: A web-based tool for gene ontology searching. Bioinformatics. 2009; 25: 3045-3046. doi: 10.1093/bioinformatics/btp536 PMID: 19744993
88. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, et al. A travel guide to cytoscape plugins. Nat Methods. 2012; 9: 1069-1076. doi: 10.1038/nmeth.2212 PMID: 23132118
89. Wang L, Yu J, Xu J, Zheng C, Li X, Du J. The analysis of microRNA-34 family expression in human cancer studies comparing cancer tissues with corresponding pericarcinous tissues. Gene. 2014; 554: 1-8. doi: S0378-1119(14)01192-5 [pii]. doi: 10.1016/j.gene.2014.10.032 PMID: 25452192
90. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell. 2007; 26: 731-743. doi: S1097-2765(07)00318-8 [pii]. PMID: 17540598
91. Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, Eramo A, et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res. 2008; 68: 10128-10136. doi: 10.1158/0008-5472.CAN-08-2148 PMID: 19074879
92. Lai CY, Yu SL, Hsieh MH, Chen CH, Chen HY, Wen CC, et al. MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS One. 2011; 6: e21635. doi: 10.1371/journal.pone.0021635 PMID: 21738743
93. Morgado AL, Xavier JM, Dionisio PA, Ribeiro MF, Dias RB, Sebastiao AM, et al. MicroRNA-34a modulates neural stem cell differentiation by regulating expression of synaptic and autophagic proteins. Mol Neurobiol. 2014. doi: 10.1007/s12035-014-8794-6
94. 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. doi: 10.1016/j.schres.2010.07.002 PMID: 20675101
95. Smalheiser NR, Lugli G, Zhang H, Rizavi H, Cook EH, Dwivedi Y. Expression of microRNAs and other small RNAs in prefrontal cortex in schizophrenia, bipolar disorder and depressed subjects. PLoS One. 2014; 9: e86469. doi: 10.1371/journal.pone.0086469 PMID: 24475125
96. Vaishnavi V, Manikandan M, Tiwary BK, Munirajan AK. Insights on the functional impact of micro-RNAs present in autism-associated copy number variants. PLoS One. 2013; 8: e56781. doi: 10.1371/journal.pone.0056781 PMID: 23451085
97. Maekawa M, Yamada K, Toyoshima M, Ohnishi T, Iwayama Y, Shimamoto C, et al. Utility of scalp hair follicles as a novel source of biomarker genes for psychiatric illnesses. Biol Psychiatry. 2014. doi: S0006-3223(14)00570-8 [pii].
98. van Spronsen M, van Battum EY, Kuijpers M, Vangoor VR, Rietman ML, Pothof J, et al. Developmental and activity-dependent miRNA expression profiling in primary hippocampal neuron cultures. PLoS One. 2013; 8: e74907. doi: 10.1371/journal.pone.0074907 PMID: 24098357
99. Sarachana T, Hu VW. Genome-wide identification of transcriptional targets of RORA reveals direct regulation of multiple genes associated with autism spectrum disorder. Mol Autism. 2013; 4: 14-2392-4-14. doi: 10.1186/2040-2392-4-14
100. Abu-Elneel K, Liu T, Gazzaniga FS, Nishimura Y, Wall DP, Geschwind DH, et al. Heterogeneous dysregulation of microRNAs across the autism spectrum. Neurogenetics. 2008; 9: 153-161. doi: 10.1007/s10048-008-0133-5 PMID: 18563458
101. 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. doi: 10.1038/mp.2009.84 PMID: 19721432
102. Henshall DC. MicroRNA and epilepsy: Profiling, functions and potential clinical applications. Curr Opin Neurol. 2014; 27: 199-205. doi: 10.1097/WCO.0000000000000079 PMID: 24553459
103. Na KS, Jung HY, Kim YK. The role of pro-inflammatory cytokines in the neuroinflammation and neurogenesis of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2014; 48: 277-286. doi: 10.1016/j.pnpbp.2012.10.022 PMID: 23123365
104. Wei H, Chadman KK, McCloskey DP, Sheikh AM, Malik M, Brown WT, et al. Brain IL-6 elevation causes neuronal circuitry imbalances and mediates autism-like behaviors. Biochim Biophys Acta. 2012; 1822: 831-842. doi: 10.1016/j.bbadis.2012.01.011 PMID: 22326556
105. Garbett KA, Hsiao EY, Kalman S, Patterson PH, Mirnics K. Effects of maternal immune activation on gene expression patterns in the fetal brain. Transl Psychiatry. 2012; 2: e98. doi: 10.1038/tp.2012.24 PMID: 22832908
106. Schulte LN, Westermann AJ, Vogel J. Differential activation and functional specialization of miR-146 and miR-155 in innate immune sensing. Nucleic Acids Res. 2013; 41: 542-553. doi: 10.1093/nar/gks1030 PMID: 23143100
107. Sheedy FJ, O'Neill LA. Adding fuel to fire: MicroRNAs as a new class of mediators of inflammation. Ann Rheum Dis. 2008; 67 Suppl 3: iii50-5. doi: 10.1136/ard.2008.100289 PMID: 19022814
108. Sonkoly E, Stahle M, Pivarcsi A. MicroRNAs and immunity: Novel players in the regulation of normal immune function and inflammation. Semin Cancer Biol. 2008; 18: 131-140. doi: 10.1016/j.semcancer.2008.01.005 PMID: 18291670
109. Clarke RA, Fang ZM, Diwan AD, Gilbert DL. Tourette syndrome and klippel-feil anomaly in a child with chromosome 22q11 duplication. Case Rep Med. 2009; 2009: 361518. doi: 10.1155/2009/361518 PMID: 20069037
110. Robertson MM, Shelley BP, Dalwai S, Brewer C, Critchley HD. A patient with both gilles de la tourette's syndrome and chromosome 22q11 deletion syndrome: Clue to the genetics of gilles de la tourette's syndrome? J Psychosom Res. 2006; 61: 365-368. doi: S0022-3999(06)00299-6 [pii]. PMID: 16938515
111. Liu Y, Li Z, Zhang M, Deng Y, Yi Z, Shi T. Exploring the pathogenetic association between schizophrenia and type 2 diabetes mellitus diseases based on pathway analysis. BMC Med Genomics. 2013; 6 Suppl 1: S17-8794-6-S1-S17. Epub 2013 Jan 23. doi: 10.1186/1755-8794-6-S1-S17
112. Zhang Y, Chen M, Wu Z, Chen J, Yu S, Fang Y, et al. Association study of Val66Met polymorphism in brain-derived neurotrophic factor gene with clozapine-induced metabolic syndrome: Preliminary results. PLoS One. 2013; 8: e72652. doi: 10.1371/journal.pone.0072652 PMID: 23967328
113. Zerbo O, Iosif AM, Walker C, Ozonoff S, Hansen RL, Hertz-Picciotto I. Is maternal influenza or fever during pregnancy associated with autism or developmental delays? results from the CHARGE (CHildhood autism risks from genetics and environment) study. J Autism Dev Disord. 2012. doi: 10.1007/s10803-012-1540-x
114. Parker-Athill EC, Tan J. Maternal immune activation and autism spectrum disorder: Interleukin-6 signaling as a key mechanistic pathway. Neurosignals. 2010; 18: 113-128. doi: 10.1159/000319828 PMID: 20924155
115. Hsiao EY, McBride SW, Chow J, Mazmanian SK, Patterson PH. Modeling an autism risk factor in mice leads to permanent immune dysregulation. Proc Natl Acad Sci U S A. 2012; 109: 12776-12781. doi: 10.1073/pnas.1202556109 PMID: 22802640
116. Ghanizadeh A. Could fever and neuroinflammation play a role in the neurobiology of autism? A subject worthy of more research. Int J Hyperthermia. 2011; 27: 737-738. doi: 10.3109/02656736.2011.604665 PMID: 21967199
117. Merico D, Costain G, Butcher NJ, Warnica W, Ogura L, Alfred SE, et al. MicroRNA dysregulation, gene networks, and risk for schizophrenia in 22q11.2 deletion syndrome. Front Neurol. 2014; 5: 238. doi: 10.3389/fneur.2014.00238 PMID: 25484875
118. Isshiki M, Tanaka S, Kuriu T, Tabuchi K, Takumi T, Okabe S. Enhanced synapse remodelling as a common phenotype in mouse models of autism. Nat Commun. 2014; 5: 4742. doi: 10.1038/ncomms5742 PMID: 25144834
119. Hall J, Trent S, Thomas KL, O'Donovan MC, Owen MJ. Genetic risk for schizophrenia: Convergence on synaptic pathways involved in plasticity. Biol Psychiatry. 2014. doi: S0006-3223(14)00519-8 [pii].
120. Leblond CS, Nava C, Polge A, Gauthier J, Huguet G, Lumbroso S, et al. Meta-analysis of SHANK mutations in autism spectrum disorders: A gradient of severity in cognitive impairments. PLoS Genet. 2014; 10: e1004580. doi: 10.1371/journal.pgen.1004580 PMID: 25188300
121. Penzes P, Buonanno A, Passafaro M, Sala C, Sweet RA. Developmental vulnerability of synapses and circuits associated with neuropsychiatric disorders. J Neurochem. 2013; 126: 165-182. doi: 10.1111/jnc.12261 PMID: 23574039
122. Tsai NP, Wilkerson JR, Guo W, Maksimova MA, DeMartino GN, Cowan CW, et al. Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell. 2012; 151: 1581-1594. doi: 10.1016/j.cell.2012.11.040 PMID: 23260144
123. Lepagnol-Bestel AM, Kvajo M, Karayiorgou M, Simonneau M, Gogos JA. A Disc1 mutation differentially affects neurites and spines in hippocampal and cortical neurons. Mol Cell Neurosci. 2013; 54: 84-92. doi: 10.1016/j.mcn.2013.01.006 PMID: 23396153
124. Aoto J, Martinelli DC, Malenka RC, Tabuchi K, Sudhof TC. Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell. 2013; 154: 75-88. doi: 10.1016/j.cell.2013.05.060 PMID: 23827676
125. Missler M, Sudhof TC, Biederer T. Synaptic cell adhesion. Cold Spring Harb Perspect Biol. 2012; 4: a005694. doi: 10.1101/cshperspect.a005694 PMID: 22278667
126. Guo R, Wang Y, Shi WY, Liu B, Hou SQ, Liu L. MicroRNA miR-491-5p targeting both TP53 and bcl-XL induces cell apoptosis in SW1990 pancreatic cancer cells through mitochondria mediated pathway. Molecules. 2012; 17: 14733-14747. doi: 10.3390/molecules171214733 PMID: 23519249
127. Kumarasinghe N, Beveridge NJ, Gardiner E, Scott RJ, Yasawardene S, Perera A, et al. Gene expression profiling in treatment-naive schizophrenia patients identifies abnormalities in biological pathways involving AKT1 that are corrected by antipsychotic medication. Int J Neuropsychopharmacol. 2013: 1-21. doi: 10.1017/S1461145713000035
128. Yao JJ, Sun J, Zhao QR, Wang CY, Mei YA. Neuregulin-1/ErbB4 signaling regulates Kv4.2-mediated transient outward K+ current through the Akt/mTOR pathway. Am J Physiol Cell Physiol. 2013; 305: C197-206. doi: 10.1152/ajpcell.00041.2013 PMID: 23703525
129. Porteous D, Millar K. How DISC1 regulates postnatal brain development: Girdin gets in on the AKT. Neuron. 2009; 63: 711-713. doi: 10.1016/j.neuron.2009.09.017 PMID: 19778497
130. Gasso P, Mas S, Molina O, Lafuente A, Bernardo M, Parellada E. Increased susceptibility to apoptosis in cultured fibroblasts from antipsychotic-naive first-episode schizophrenia patients. J Psychiatr Res. 2014; 48: 94-101. doi: 10.1016/j.jpsychires.2013.09.017 PMID: 24128664
131. Drerup CM, Wiora HM, Topczewski J, Morris JA. Disc1 regulates foxd3 and sox10 expression, affecting neural crest migration and differentiation. Development. 2009; 136: 2623-2632. doi: 10.1242/dev.030577 PMID: 19570850
132. Ghahramani Seno MM, Hu P, Gwadry FG, Pinto D, Marshall CR, Casallo G, et al. Gene and miRNA expression profiles in autism spectrum disorders. Brain Res. 2011; 1380: 85-97. doi: 10.1016/j.brainres.2010.09.046 PMID: 20868653
133. Clipperton-Allen AE, Page DT. Pten haploinsufficient mice show broad brain overgrowth but selective impairments in autism-relevant behavioral tests. Hum Mol Genet. 2014. doi: 10.1093/hmg/ddu057
134. Lv JW, Cheng TL, Qiu ZL, Zhou WH. Role of the PTEN signaling pathway in autism spectrum disorder. Neurosci Bull. 2013; 29: 773-778. doi: 10.1007/s12264-013-1382-3 PMID: 24136242
135. Shaham L, Vendramini E, Ge Y, Goren Y, Birger Y, Tijssen MR, et al. MicroRNA-486-5p is an erythroid oncomiR of the myeloid leukemias of down syndrome. Blood. 2014. doi: blood-2014-06-581892 [pii].
136. Pietrzykowski AZ, Spijker S. Impulsivity and comorbid traits: A multi-step approach for finding putative responsible microRNAs in the amygdala. Front Neurosci. 2014; 8: 389. doi: 10.3389/fnins.2014.00389 PMID: 25561905
137. Antshel KM, Aneja A, Strunge L, Peebles J, Fremont WP, Stallone K, et al. Autistic spectrum disorders in velo-cardio facial syndrome (22q11.2 deletion). J Autism Dev Disord. 2007; 37: 1776-1786. doi: 10.1007/s10803-006-0308-6 PMID: 17180713
138. Kates WR, Miller AM, Abdulsabur N, Antshel KM, Conchelos J, Fremont W, et al. Temporal lobe anatomy and psychiatric symptoms in velocardiofacial syndrome (22q11.2 deletion syndrome). J Am Acad Child Adolesc Psychiatry. 2006; 45: 587-595. doi: 10.1097/01.chi.0000205704.33077.4a PMID: 16670653
139. Montojo CA, Jalbrzikowski M, Congdon E, Domicoli S, Chow C, Dawson C, et al. Neural substrates of inhibitory control deficits in 22q11.2 deletion syndrome. Cereb Cortex. 2013. doi: bht304 [pii].
140. Liu T, Wan RP, Tang LJ, Liu SJ, Li HJ, Zhao QH, et al. A MicroRNA profile in Fmr1 knockout mice reveals MicroRNA expression alterations with possible roles in fragile X syndrome. Mol Neurobiol. 2014. doi: 10.1007/s12035-014-8770-1
141. Urdinguio RG, Fernandez AF, Lopez-Nieva P, Rossi S, Huertas D, Kulis M, et al. Disrupted microRNA expression caused by Mecp2 loss in a mouse model of rett syndrome. Epigenetics. 2010; 5: 656-663. doi: 10.4161/epi.5.7.13055 PMID: 20716963
142. Simao I, Lourenco T, Lopes L, Ramos MP. First seizure as late presentation of velo-cardio-facial syndrome. J Pediatr Endocrinol Metab. 2013; 26: 381-383. doi: 10.1515/jpem-2012-0348 PMID: 23327824
143. Cheung EN, George SR, Andrade DM, Chow EW, Silversides CK, Bassett AS. Neonatal hypocalcemia, neonatal seizures, and intellectual disability in 22q11.2 deletion syndrome. Genet Med. 2014; 16: 40-44. doi: 10.1038/gim.2013.71 PMID: 23765047
144. Lionel AC, Vaags AK, Sato D, Gazzellone MJ, Mitchell EB, Chen HY, et al. Rare exonic deletions implicate the synaptic organizer gephyrin (GPHN) in risk for autism, schizophrenia and seizures. Hum Mol Genet. 2013; 22: 2055-2066. doi: 10.1093/hmg/ddt056 PMID: 23393157
145. Clarke MC, Tanskanen A, Huttunen MO, Clancy M, Cotter DR, Cannon M. Evidence for shared susceptibility to epilepsy and psychosis: A population-based family study. Biol Psychiatry. 2012; 71: 836-839. doi: 10.1016/j.biopsych.2012.01.011 PMID: 22365727
146. Murdoch JD, State MW. Recent developments in the genetics of autism spectrum disorders. Curr Opin Genet Dev. 2013; 23: 310-315. doi: 10.1016/j.gde.2013.02.003 PMID: 23537858
147. Doherty JL, O'Donovan MC, Owen MJ. Recent genomic advances in schizophrenia. Clin Genet. 2012; 81: 103-109. doi: 10.1111/j.1399-0004.2011.01773.x PMID: 21895634