Long Non-Coding RNA and Alternative Splicing Modulations in Parkinson's Leukocytes Identified by RNA Sequencing

PLoS Computational Biology

Volumn 10, Issue 3, 2014, Pages

  Soreq, Lilach ^a   Guffanti, Alessandro ^b,c   Salomonis, Nathan ^d   Simchovitz, Alon ^c   Israel, Zvi ^e   Bergman, Hagai ^a,b   Soreq, Hermona ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c Genomnia   (Italy)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^e HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; BRAIN; DIAGNOSIS; NEURODEGENERATIVE DISEASES; POLYMERASE CHAIN REACTION;

ALTERNATIVE SPLICING; DEEP BRAIN STIMULATION; DISEASE INCIDENCE; LEUCOCYTES; LIFESPANS; PARKINSON'S DISEASE; RNA SPLICING; RNA-SEQ DATUM; TRANSCRIPTOMES; WORK-FLOWS;

RNA;

LONG UNTRANSLATED RNA; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; AMYGDALOID NUCLEUS; ARTICLE; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GENETIC IDENTIFICATION; GENETIC REGULATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKOCYTE; MALE; PARKINSON DISEASE; PROMOTER REGION; PROTEIN DOMAIN; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA BINDING; RNA SEQUENCE; SEQUENCE ANALYSIS; SPLICEOSOME; SUBSTANTIA NIGRA;

ALTERNATIVE SPLICING; AMYGDALA; BRAIN MAPPING; DEEP BRAIN STIMULATION; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LEUKOCYTES; MALE; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARKINSON DISEASE; RNA, LONG NONCODING; SEQUENCE ANALYSIS, RNA; SUBSTANTIA NIGRA;

EID: 84897431152     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003517     Document Type: Article

References (134)

1. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
2. Guenzl PM, Barlow DP, (2012) Macro lncRNAs: a new layer of cis-regulatory information in the mammalian genome. RNA biology 9: 731-741.
3. Wang KC, Chang HY, (2011) Molecular mechanisms of long noncoding RNAs. Molecular cell 43: 904-914.
4. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, et al. (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome research 22: 1760-1774.
5. Guttman M, Rinn JL, (2012) Modular regulatory principles of large non-coding RNAs. Nature 482: 339-346.
6. Qureshi IA, Mehler MF, (2012) Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nature reviews Neuroscience 13: 528-541.
7. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH, (2006) Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29: 77-103.
8. Li M, Wen S, Guo X, Bai B, Gong Z, et al. (2012) The novel long non-coding RNA CRG regulates Drosophila locomotor behavior. Nucleic Acids Res 40: 11714-11727.
9. Lin M, Pedrosa E, Shah A, Hrabovsky A, Maqbool S, et al. (2011) RNA-Seq of human neurons derived from iPS cells reveals candidate long non-coding RNAs involved in neurogenesis and neuropsychiatric disorders. PLoS One 6: e23356.
10. Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, et al. (2007) The H19 non-coding RNA is essential for human tumor growth. PLoS One 2: e845.
11. Ziats MN, Rennert OM, (2013) Aberrant expression of long noncoding RNAs in autistic brain. Journal of molecular neuroscience: MN 49: 589-593.
12. Johnson R, (2012) Long non-coding RNAs in Huntington's disease neurodegeneration. Neurobiol Dis 46: 245-254.
13. Holden T, Nguyen A, Lin E, Cheung E, Dehipawala S, et al. (2013) Exploratory bioinformatics study of lncRNAs in Alzheimer's disease mRNA sequences with application to drug development. Comput Math Methods Med 2013: 579136.
14. Nussbaum RL, Ellis CE, (2003) Alzheimer's disease and Parkinson's disease. N Engl J Med 348: 1356-1364.
15. Dorsey ER, Thompson JP, Noyes K, Dick AW, Holloway RG, et al. (2007) Quantifying the risks and benefits of natalizumab in relapsing multiple sclerosis. Neurology 68: 1524-1528.
16. Allain H, Bentue-Ferrer D, Akwa Y, (2008) Disease-modifying drugs and Parkinson's disease. Prog Neurobiol 84: 25-39.
17. Benmoyal-Segal L, Soreq H, (2006) Gene-environment interactions in sporadic Parkinson's disease. J Neurochem 97: 1740-1755.
18. Douglas MR, Lewthwaite AJ, Nicholl DJ, (2007) Genetics of Parkinson's disease and parkinsonism. Expert Rev Neurother 7: 657-666.
19. Hoehn MM, Yahr MD, (1967) Parkinsonism: onset, progression and mortality. Neurology 17: 427-442.
20. Fahn S, (2003) Description of Parkinson's disease as a clinical syndrome. Ann N Y Acad Sci 991: 1-14.
21. Kringelbach ML, Jenkinson N, Owen SL, Aziz TZ, (2007) Translational principles of deep brain stimulation. Nat Rev Neurosci 8: 623-635.
22. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, et al. (1997) Mutation in the-synuclein gene identified in families with Parkinson's disease. Science 276: 2045.
23. Baba M, Nakajo S, Tu PH, Tomita T, Nakaya K, et al. (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 152: 879-884.
24. Gibb WR, Lees AJ, (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry 51: 745-752.
25. Um JW, Im E, Lee HJ, Min B, Yoo L, et al. (2010) Parkin directly modulates 26S proteasome activity. J Neurosci 30: 11805-11814.
26. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, et al. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608.
27. Mullett SJ, Di Maio R, Greenamyre JT, Hinkle DA, (2013) DJ-1 expression modulates astrocyte-mediated protection against neuronal oxidative stress. J Mol Neurosci 49: 507-511.
28. Shendelman S, Jonason A, Martinat C, Leete T, Abeliovich A, (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2: e362.
29. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, et al. (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468: 696-700.
30. Cooper O, Seo H, Andrabi S, Guardia-Laguarta C, Graziotto J, et al. (2012) Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci Transl Med 4: 141ra190.
31. Hatano Y, Li Y, Sato K, Asakawa S, Yamamura Y, et al. (2004) Novel PINK1 mutations in early-onset parkinsonism. Ann Neurol 56: 424-427.
32. Grenier K, McLelland GL, Fon EA, (2013) Parkin- and PINK1-Dependent Mitophagy in Neurons: Will the Real Pathway Please Stand Up? Front Neurol 4: 100.
33. Soreq L, Bergman H, Goll Y, Greenberg DS, Israel Z, et al. (2012) Deep brain stimulation induces rapidly reversible transcript changes in Parkinson's leucocytes. J Cell Mol Med 16: 1496-1507.
34. Nickles D, Chen HP, Li MM, Khankhanian P, Madireddy L, et al. (2013) Blood RNA profiling in a large cohort of multiple sclerosis patients and healthy controls. Human molecular genetics 22: 4194-4205.
35. Harris LW, Pietsch S, Cheng TM, Schwarz E, Guest PC, et al. (2012) Comparison of peripheral and central schizophrenia biomarker profiles. PloS one 7: e46368.
36. Fehlbaum-Beurdeley P, Sol O, Desire L, Touchon J, Dantoine T, et al. (2012) Validation of AclarusDx, a blood-based transcriptomic signature for the diagnosis of Alzheimer's disease. Journal of Alzheimer's disease: JAD 32: 169-181.
37. Soreq L, Salomonis N, Bronstein M, Greenberg DS, Israel Z, et al. (2013) Small RNA sequencing-microarray analyses in Parkinson leukocytes reveal deep brain stimulation-induced splicing changes that classify brain region transcriptomes. Front Mol Neurosci 6: 10.
38. Soreq L, Israel Z, Bergman H, Soreq H, (2008) Advanced microarray analysis highlights modified neuro-immune signaling in nucleated blood cells from Parkinson's disease patients. J Neuroimmunol 201-202: 227-236.
39. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, et al. (2007) A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317: 1220-1224.
40. Mouradian MM, (2012) MicroRNAs in Parkinson's disease. Neurobiol Dis 46: 279-284.
41. Junn E, Mouradian MM, (2012) MicroRNAs in neurodegenerative diseases and their therapeutic potential. Pharmacol Ther 133: 142-150.
42. Harraz MM, Dawson TM, Dawson VL, (2011) MicroRNAs in Parkinson's disease. J Chem Neuroanat 42: 127-130.
43. Gascon E, Gao FB, (2012) Cause or Effect: Misregulation of microRNA Pathways in Neurodegeneration. Front Neurosci 6: 48.
44. Minones-Moyano E, Porta S, Escaramis G, Rabionet R, Iraola S, et al. (2011) MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum Mol Genet 20: 3067-3078.
45. de Mena L, Coto E, Cardo LF, Diaz M, Blazquez M, et al. (2010) Analysis of the Micro-RNA-133 and PITX3 genes in Parkinson's disease. Am J Med Genet B Neuropsychiatr Genet 153B: 1234-1239.
46. Doxakis E, (2010) Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153. J Biol Chem 285: 12726-12734.
47. Soreq L, Bergman H, Israel Z, Soreq H, (2013) Deep brain stimulation modulates nonsense-mediated RNA decay in Parkinson's patients leukocytes. BMC Genomics 14: 478.
48. Soreq L, Bergman H, Israel Z, Soreq H, (2012) Exon arrays reveal alternative splicing aberrations in Parkinson's disease leukocytes. Neurodegener Dis 10: 203-206.
49. Kim VN, (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
50. Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, et al. (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495: 467-473.
51. Salomonis N, Schlieve CR, Pereira L, Wahlquist C, Colas A, et al. (2010) Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proceedings of the National Academy of Sciences of the United States of America 107: 10514-10519.
52. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
53. Hubbard T, Barker D, Birney E, Cameron G, Chen Y, et al. (2002) The Ensembl genome database project. Nucleic acids research 30: 38-41.
54. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome research 12: 996-1006.
55. Ilott NE, Ponting CP, (2013) Predicting long non-coding RNAs using RNA sequencing. Methods 63: 50-59.
56. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, et al. (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome research 22: 1775-1789.
57. Howald C, Tanzer A, Chrast J, Kokocinski F, Derrien T, et al. (2012) Combining RT-PCR-seq and RNA-seq to catalog all genic elements encoded in the human genome. Genome research 22: 1698-1710.
58. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, et al. (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nature biotechnology 28: 503-510.
59. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
60. Robinson MD, Oshlack A, (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome biology 11: R25.
61. Seal RL, Gordon SM, Lush MJ, Wright MW, Bruford EA, (2011) genenames.org: the HGNC resources in 2011. Nucleic acids research 39: D514-519.
62. Pruitt KD, Tatusova T, Brown GR, Maglott DR, (2012) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic acids research 40: D130-135.
63. Volders PJ, Helsens K, Wang X, Menten B, Martens L, et al. (2013) LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic acids research 41: D246-251.
64. Ziats MN, Rennert OM, (2013) Aberrant expression of long noncoding RNAs in autistic brain. J Mol Neurosci 49: 589-593.
65. Rhinn H, Qiang L, Yamashita T, Rhee D, Zolin A, et al. (2012) Alternative alpha-synuclein transcript usage as a convergent mechanism in Parkinson's disease pathology. Nature communications 3: 1084.
66. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, et al. (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33: D121-124.
67. Andronescu M, Bereg V, Hoos HH, Condon A, (2008) RNA STRAND: the RNA secondary structure and statistical analysis database. BMC Bioinformatics 9: 340.
68. Hamada M, Sato K, Asai K, (2010) Prediction of RNA secondary structure by maximizing pseudo-expected accuracy. BMC Bioinformatics 11: 586.
69. Sato K, Hamada M, Asai K, Mituyama T, (2009) CENTROIDFOLD: a web server for RNA secondary structure prediction. Nucleic acids research 37: W277-280.
70. Lee K, Kim JH, Kwon OB, An K, Ryu J, et al. (2012) An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2. J Neurosci 32: 5678-5687.
71. Le MT, Xie H, Zhou B, Chia PH, Rizk P, et al. (2009) MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol Cell Biol 29: 5290-5305.
72. Salomonis N, Schlieve CR, Pereira L, Wahlquist C, Colas A, et al. (2010) Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc Natl Acad Sci U S A 107: 10514-10519.
73. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
74. Dimon MT, Sorber K, DeRisi JL, (2010) HMMSplicer: a tool for efficient and sensitive discovery of known and novel splice junctions in RNA-Seq data. PloS one 5: e13875.
75. Au KF, Jiang H, Lin L, Xing Y, Wong WH, (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic acids research 38: 4570-4578.
76. Srinivasan K, Shiue L, Hayes JD, Centers R, Fitzwater S, et al. (2005) Detection and measurement of alternative splicing using splicing-sensitive microarrays. Methods 37: 345-359.
77. Gardina PJ, Clark TA, Shimada B, Staples MK, Yang Q, et al. (2006) Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. Bmc Genomics 7: 325.
78. Soreq L, Bergman H, Israel Z, Soreq H, (2012) Exon arrays reveal alternative splicing aberrations in Parkinson's disease leukocytes. Neuro-degenerative diseases 10: 203-206.
79. Berson A, Barbash S, Shaltiel G, Goll Y, Hanin G, et al. (2012) Cholinergic-associated loss of hnRNP-A/B in Alzheimer's disease impairs cortical splicing and cognitive function in mice. EMBO molecular medicine 4: 730-742.
80. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, et al. (2010) iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17: 909-915.
81. Charlesworth G, Mohire MD, Schneider SA, Stamelou M, Wood NW, et al. (2013) Ataxia telangiectasia presenting as dopa-responsive cervical dystonia. Neurology.
82. Ule J, Ule A, Spencer J, Williams A, Hu JS, et al. (2005) Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37: 844-852.
83. Pauls E, Nanda SK, Smith H, Toth R, Arthur JS, et al. (2013) Two Phases of Inflammatory Mediator Production Defined by the Study of IRAK2 and IRAK1 Knock-in Mice. Journal of immunology 191 (5) (): 2717-30.
84. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics 25: 25-29.
85. Brown K, Xie S, Qiu X, Mohrin M, Shin J, et al. (2013) SIRT3 Reverses Aging-Associated Degeneration. Cell Rep 3: 319-327.
86. An Q, Wright SL, Moorman AV, Parker H, Griffiths M, et al. (2009) Heterogeneous breakpoints in patients with acute lymphoblastic leukemia and the dic(9;20)(p 11-13;q11) show recurrent involvement of genes at 20q11.21. Haematologica 94: 1164-1169.
87. Guo D, Liu J, Wang W, Hao F, Sun X, et al. (2013) Alteration in abundance and compartmentalization of inflammation-related miRNAs in plasma after intracerebral hemorrhage. Stroke; a journal of cerebral circulation 44: 1739-1742.
88. Kim HJ, Kim NC, Wang YD, Scarborough EA, Moore J, et al. (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495: 467-73.
89. Ishigaki S, Masuda A, Fujioka Y, Iguchi Y, Katsuno M, et al. (2012) Position-dependent FUS-RNA interactions regulate alternative splicing events and transcriptions. Sci Rep 2: 529.
90. Carter CJ, (2007) eIF2B and oligodendrocyte survival: where nature and nurture meet in bipolar disorder and schizophrenia? Schizophr Bull 33: 1343-1353.
91. Fan X, Li D, Lichti CF, Green TA, (2013) Dynamic proteomics of nucleus accumbens in response to acute psychological stress in environmentally enriched and isolated rats. PLoS One 8: e73689.
92. Mitsui S, Watanabe Y, Yamaguchi T, Yamaguchi N, (2008) Mosaic serine proteases in the mammalian central nervous system. Front Biosci 13: 1991-2000.
93. Cha Y, Kim DK, Hyun J, Kim SJ, Park KS, (2013) TCEA3 binds to TGF-beta receptor I and induces Smad-independent, JNK-dependent apoptosis in ovarian cancer cells. Cell Signal 25: 1245-1251.
94. Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, et al. (2012) Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 1: 167-178.
95. Gao L, Gao H, Zhou H, Xu Y, (2013) Gene expression profiling analysis of the putamen for the investigation of compensatory mechanisms in Parkinson's disease. BMC Neurol 13: 181.
96. Ben Abdelali R, Asnafi V, Petit A, Micol JB, Callens C, et al. (2013) The prognosis of CALM-AF10-positive adult T-cell acute lymphoblastic leukemias depends on the stage of maturation arrest. Haematologica 98: 1711-1717.
97. Gerstner JR, Landry CF, (2007) The zinc-binding protein chordc1 undergoes complex diurnal changes in mRNA expression during mouse brain development. Neurochem Res 32: 241-250.
98. Costa LG, de Laat R, Dao K, Pellacani C, Cole TB, et al. (2013) Paraoxonase-2 (PON2) in brain and its potential role in neuroprotection. Neurotoxicology.
99. Thompson JW, Bruick RK, (2012) Protein degradation and iron homeostasis. Biochim Biophys Acta 1823: 1484-1490.
100. Tyagarajan SK, Ghosh H, Harvey K, Fritschy JM, (2011) Collybistin splice variants differentially interact with gephyrin and Cdc42 to regulate gephyrin clustering at GABAergic synapses. J Cell Sci 124: 2786-2796.
101. Tybulewicz VL, Henderson RB, (2009) Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 9: 630-644.
102. Zhao W, Manley JL, (1996) Complex alternative RNA processing generates an unexpected diversity of poly(A) polymerase isoforms. Molecular and cellular biology 16: 2378-2386.
103. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, et al. (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212-1215.
104. Purdom E, Simpson KM, Robinson MD, Conboy JG, Lapuk AV, et al. (2008) FIRMA: a method for detection of alternative splicing from exon array data. Bioinformatics 24: 1707-1714.
105. Young RS, Ponting CP, (2013) Identification and function of long non-coding RNAs. Essays Biochem 54: 113-126.
106. Wapinski O, Chang HY, (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21: 354-361.
107. Soreq L, Salomonis N, Bronstein M, Greenberg DS, Israel Z, et al. (2013) Small RNA sequencing-microarray analyses in Parkinson leukocytes reveal deep brain stimulation-induced splicing changes that classify brain region transcriptomes. Frontiers in molecular neuroscience 6: 10.
108. Zambon AC, Gaj S, Ho I, Hanspers K, Vranizan K, et al. (2012) GO-Elite: a flexible solution for pathway and ontology over-representation. Bioinformatics 28: 2209-2210.
109. Wilusz JE, Sunwoo H, Spector DL, (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23: 1494-1504.
110. Beckedorff FC, Amaral MS, Deocesano-Pereira C, Verjovski-Almeida S, (2013) Long noncoding RNAs and their implications in cancer epigenetics. Biosci Rep 33: pii: e00061.
111. Lee JT, (2012) Epigenetic regulation by long noncoding RNAs. Science 338: 1435-1439.
112. Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, et al. (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149: 819-831.
113. Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V, (2013) Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS One 8: e53823.
114. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP, (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353-358.
115. Moran VA, Perera RJ, Khalil AM, (2012) Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 40: 6391-6400.
116. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, et al. (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39: 925-938.
117. Sanford JR, Wang X, Mort M, Vanduyn N, Cooper DN, et al. (2009) Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res 19: 381-394.
118. Rands CM, Darling A, Fujita M, Kong L, Webster MT, et al. (2013) Insights into the evolution of Darwin's finches from comparative analysis of the Geospiza magnirostris genome sequence. Bmc Genomics 14: 95.
119. Young RS, Ponting CP, (2013) Identification and function of long non-coding RNAs. Essays in biochemistry 54: 113-126.
120. Schapira AH, Tolosa E, (2010) Molecular and clinical prodrome of Parkinson disease: implications for treatment. Nat Rev Neurol 6: 309-317.
121. Narendra DP, Youle RJ, (2012) Neurodegeneration: Trouble in the cell's powerhouse. Nature 483: 418-419.
122. Heeramun-Aubeeluck A, Lu Z, (2013) Neurosurgery for mental disorders: a review. African journal of psychiatry 16: 177-181.
123. Fahn S MotUDC (1987) Unified Parkinson's Disease Rating Scale.
124. Ewing B, Green P, (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
125. Au KF, Jiang H, Lin L, Xing Y, Wong WH, (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res 38: 4570-4578.
126. Zhang H, Hu J, Recce M, Tian B, (2005) PolyA_DB: a database for mammalian mRNA polyadenylation. Nucleic acids research 33: D116-120.
127. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome biology 4: P3.
128. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, et al. (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25: 1091-1093.
129. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research 13: 2498-2504.
130. Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, et al. (2005) BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21: 3439-3440.
131. Harrow J, Denoeud F, Frankish A, Reymond A, Chen CK, et al. (2006) GENCODE: producing a reference annotation for ENCODE. Genome biology 7 Suppl 1: S4 1-9.
132. Wang X, El Naqa IM, (2008) Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24: 325-332.
133. Langmead B (2010) Aligning short sequencing reads with Bowtie. Current protocols in bioinformatics/editoral board, Andreas D Baxevanis [et al] Chapter 11: Unit 11 17.
134. Rustici G, Kolesnikov N, Brandizi M, Burdett T, Dylag M, et al. (2013) ArrayExpress update-trends in database growth and links to data analysis tools. Nucleic acids research 41: D987-990.