The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing

Molecular Psychiatry

Volumn 19, Issue 4, 2014, Pages 486-494

  Barry, G ^a   Briggs, J A ^a   Vanichkina, D P ^a   Poth, E M ^b   Beveridge, N J ^c,d   Ratnu, V S ^a   Nayler, S P ^a   Nones, K ^a   Hu, J ^e   Bredy, T W ^a   Nakagawa, S ^f   Rigo, F ^g   Taft, R J ^a   Cairns, M J ^c,d   Blackshaw, S ^b   Wolvetang, E J ^a   Mattick, J S ^a,h,i  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF NEWCASTLE   (Australia)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f RIKEN   (Japan)

^g ISIS PHARMACEUTICALS   (United States)

^h GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

ⁱ UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Alternative splicing; Gomafu; Neuronal activation; Quaking homolog; Schizophrenia

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; LONG UNTRANSLATED RNA; SERINE ARGININE RICH PROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL ACTIVATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; EMBRYO; GRAY MATTER; MOUSE; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RETINA DEVELOPMENT; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; TRANSCRIPTOMICS;

ALTERNATIVE SPLICING; ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPRECIPITATION; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; PROTEOME; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, LONG NONCODING; RNA-BINDING PROTEINS; SCHIZOPHRENIA;

EID: 84897108067     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2013.45     Document Type: Article

References (71)

1. Rossler W, Salize HJ, van Os J, Riecher-Rossler A. Size of burden of schizophrenia and psychotic disorders. Eur Neuropsychopharmacol 2005; 15: 399-409
2. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011; 12: 585-601
3. Sullivan PF, Kendler KS, Neale MC. Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 2003; 60: 1187-1192
4. Girard SL, Gauthier J, Noreau A, Xiong L, Zhou S, Jouan L et al. Increased exonic de novo mutation rate in individuals with schizophrenia. Nat Genet 2011; 43: 860-863
5. 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
6. Morikawa T, Manabe T. Aberrant regulation of alternative pre-mRNA splicing in schizophrenia. Neurochem Int 2010; 57: 691-704
7. Nakata K, Lipska BK, Hyde TM, Ye T, Newburn EN, Morita Y et al. DISC1 splice variants are upregulated in schizophrenia and associated with risk polymorphisms. Proc Natl Acad Sci USA 2009; 106: 15873-15878
8. Law AJ, Kleinman JE, Weinberger DR, Weickert CS. Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum Mol Genet 2007; 16: 129-141
9. Tsuiji H, Yoshimoto R, Hasegawa Y, Furuno M, Yoshida M, Nakagawa S. Competition between a noncoding exon and introns: Gomafu contains tandem UACUAAC repeats and associates with splicing factor-1. Genes Cells 2011; 16: 479-490
10. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007; 316: 1484-1488
11. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012; 22: 1775-1789
12. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A et al. Landscape of transcription in human cells. Nature 2012; 489: 101-108
13. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F et al. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489: 57-74
14. Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature 2012; 482: 339-346
15. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43: 904-914
16. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011; 477: 295-300
17. Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol 2011; 21: 354-361
18. Chen LL, Carmichael GG. Decoding the function of nuclear long non-coding RNAs. Curr Opin Cell Biol 2010; 22: 357-364
19. Ishii N, Ozaki K, Sato H, Mizuno H, Saito S, Takahashi A et al. Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. J Hum Genet 2006; 51: 1087-1099
20. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, Kuo WP et al. Genomic analysis of mouse retinal development. PLoS Biol 2004; 2: E247
21. Rapicavoli NA, Blackshaw S. New meaning in the message: noncoding RNAs and their role in retinal development. Dev Dyn 2009; 238: 2103-2114
22. Rapicavoli NA, Poth EM, Blackshaw S. The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev Biol 2010; 10: 49
23. Mercer TR, Qureshi IA, Gokhan S, Dinger ME, Li G, Mattick JS et al. Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci 2010; 11: 14
24. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 2008; 105: 716-721
25. Sone M, Hayashi T, Tarui H, Agata K, Takeichi M, Nakagawa S. The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J Cell Sci 2007; 120: 2498-2506
26. Albertson DN, Schmidt CJ, Kapatos G, Bannon MJ. Distinctive profiles of gene expression in the human nucleus accumbens associated with cocaine and heroin abuse. Neuropsychopharmacology 2006; 31: 2304-2312
27. Michelhaugh SK, Lipovich L, Blythe J, Jia H, Kapatos G, Bannon MJ. Mining Affymetrix microarray data for long non-coding RNAs: altered expression in the nucleus accumbens of heroin abusers. J Neurochem 2011; 116: 459-466
28. Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C et al. Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 2004; 47(Suppl 1): 227-241
29. Takahashi S, Ohtsuki T, Yu SY, Tanabe E, Yara K, Kamioka M et al. Significant linkage to chromosome 22q for exploratory eye movement dysfunction in schizophrenia. Am J Med Genet B Neuropsychiatr Genet 2003; 123B: 27-32
30. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003; 302: 890-893
31. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article 3
32. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007; 23: 2700-2707
33. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003; 31: 265-273
34. Clark MB, Johnston RL, Inostroza-Ponta M, Fox AH, Fortini E, Moscato P et al. Genome-wide analysis of long noncoding RNA stability. Genome Res 2012; 22: 885-898
35. Medina I, Carbonell J, Pulido L, Madeira SC, Goetz S, Conesa A et al. Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res 2010; 38: W210-W213
36. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer: New York, 2009
37. Chen H, Boutros PC. VennDiagram: a package for the generation of highlycustomizable Venn and Euler diagrams in R. BMC Bioinformatics 2011; 12: 35
38. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005; 2: 185-190
39. Vetter I. Development and Optimization of FLIPR high throughput calcium assays for ion channels and GPCRs. Adv Exp Med Biol 2012; 740: 45-82
40. Jeong JS, Jiang L, Albino E, Marrero J, Rho HS, Hu J et al. Rapid identification of monospecific monoclonal antibodies using a human proteome microarray. Mol Cell Proteomics 2012; 11: O111. 016253
41. Fok V, Mitton-Fry RM, Grech A, Steitz JA. Multiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22. RNA 2006; 12: 872-882
42. 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
43. 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
44. Lyons MR, West AE. Mechanisms of specificity in neuronal activity-regulated gene transcription. Prog Neurobiol 2011; 94: 259-295
45. Bredy TW, Lin Q, Wei W, Baker-Andresen D, Mattick JS. MicroRNA regulation of neural plasticity and memory. Neurobiol Learn Mem 2011; 96: 89-94
46. Siemen H, Colas D, Heller HC, Brustle O, Pera RA. Pumilio-2 function in the mouse nervous system. PLoS ONE 2011; 6: e25932
47. Lahmann I, Fabienke M, Henneberg B, Pabst O, Vauti F, Minge D et al. The hnRNP and cytoskeletal protein raver1 contributes to synaptic plasticity. Exp Cell Res 2008; 314: 1048-1060
48. Kundel M, Jones KJ, Shin CY, Wells DG. Cytoplasmic polyadenylation element-binding protein regulates neurotrophin-3-dependent beta-catenin mRNA translation in developing hippocampal neurons. J Neurosci 2009; 29: 13630-13639
49. Zearfoss NR, Alarcon JM, Trifilieff P, Kandel E, Richter JD. A molecular circuit composed of CPEB-1 and c-Jun controls growth hormone-mediated synaptic plasticity in the mouse hippocampus. J Neurosci 2008; 28: 8502-8509
50. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011; 25: 1915-1927
51. Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 2005; 25: 247-251
52. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z et al. A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J 2010; 29: 3082-3093
53. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 2010; 39: 925-938
54. Aberg K, Saetre P, Jareborg N, Jazin E. Human QKI, a potential regulator of mRNA expression of human oligodendrocyte-related genes involved in schizophrenia. Proc Natl Acad Sci USA 2006; 103: 7482-7487
55. Aberg K, Saetre P, Lindholm E, Ekholm B, Pettersson U, Adolfsson R et al. Human QKI, a new candidate gene for schizophrenia involved in myelination. Am J Med Genet B Neuropsychiatr Genet 2006; 141B: 84-90
56. Haroutunian V, Katsel P, Dracheva S, Davis KL. The human homolog of the QKI gene affected in the severe dysmyelination 'quaking' mouse phenotype: downregulated in multiple brain regions in schizophrenia. Am J Psychiatry 2006; 163: 1834-1837
57. McCullumsmith RE, Gupta D, Beneyto M, Kreger E, Haroutunian V, Davis KL et al. Expression of transcripts for myelination-related genes in the anterior cingulate cortex in schizophrenia. Schizophr Res 2007; 90: 15-27
58. Hashimoto R, Straub RE, Weickert CS, Hyde TM, Kleinman JE, Weinberger DR. Expression analysis of neuregulin-1 in the dorsolateral prefrontal cortex in schizophrenia. Mol Psychiatry 2004; 9: 299-307
59. Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci 2011; 12: 707-722
60. Ishizuka K, Kamiya A, Oh EC, Kanki H, Seshadri S, Robinson JF et al. DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature 2011; 473: 92-96
61. Wang Q, Charych EI, Pulito VL, Lee JB, Graziane NM, Crozier RA et al. The psychiatric disease risk factors DISC1 and TNIK interact to regulate synapse composition and function. Mol Psychiatry 2011; 16: 1006-1023
62. Hayashi-Takagi A, Takaki M, Graziane N, Seshadri S, Murdoch H, Dunlop AJ et al. Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat Neurosci 2010; 13: 327-332
63. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ et al. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci 2012; 32: 2988-2997
64. Veikkolainen V, Vaparanta K, Halkilahti K, Iljin K, Sundvall M, Elenius K. Function of ERBB4 is determined by alternative splicing. Cell Cycle 2011; 10: 2647-2657
65. Beveridge NJ, Cairns MJ. MicroRNA dysregulation in schizophrenia. Neurobiol Dis 2012; 46: 263-271
66. 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
67. Gardiner E, Beveridge NJ, Wu JQ, Carr V, Scott RJ, Tooney PA et al. Imprinted DLK1-DIO3 region of 14q32 defines a schizophrenia-associated miRNA signature in peripheral blood mononuclear cells. Mol Psychiatry 2012; 17: 827-840
68. 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
69. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009; 10: 155-159
70. Day JJ, Sweatt JD. Epigenetic mechanisms in cognition. Neuron 2011; 70: 813-829
71. Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD et al. ncRNA-and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 2011; 147: 773-788.