Transcriptome-wide analysis of TDP-43 binding small RNAs identifies miR-NID1 (miR-8485), a novel miRNA that represses NRXN1 expression

Genomics

Volumn 103, Issue 1, 2014, Pages 76-82

  Fan, Zhen ^a,b   Chen, Xiaowei ^a,b   Chen, Runsheng ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

CA repeat; Novel intronic miRNA; NRXN1; TDP 43

Indexed keywords

MICRORNA; MICRORNA 8485; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; INTRON; MOUSE; NEUREXIN 1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA BINDING; SYNAPSE; TRANSCRIPTOMICS;

CA REPEAT; NOVEL INTRONIC MIRNA; NRXN1; TDP-43;

ANIMALS; BASE SEQUENCE; CELL ADHESION MOLECULES, NEURONAL; CELL LINE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84895895949     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2013.06.006     Document Type: Article

References (48)

1. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
2. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
3. Du T., Zamore P.D. microPrimer: the biogenesis and function of microRNA. Development 2005, 132:4645-4652.
4. Rodriguez A., Griffiths-Jones S., Ashurst J.L., Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 2004, 14:1902-1910.
5. Baskerville S., Bartel D.P. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11:241-247.
6. Bosia C., Osella M., Baroudi M.E., Cora D., Caselle M. Gene autoregulation via intronic microRNAs and its functions. BMC Syst. Biol. 2012, 6:131.
7. Gangaraju V.K., Lin H. MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 2009, 10:116-125.
8. Ishizu H., Siomi H., Siomi M.C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012, 26:2361-2373.
9. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 2003, 5:R1.
10. Kertesz M., Iovino N., Unnerstall U., Gaul U., Segal E. The role of site accessibility in microRNA target recognition. Nat. Genet. 2007, 39:1278-1284.
11. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
12. Friedlander M.R., Chen W., Adamidi C., Maaskola J., Einspanier R., Knespel S., Rajewsky N. Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 2008, 26:407-415.
13. Hackenberg M., Sturm M., Langenberger D., Falcón-Pérez J.M., Aransay A.M. miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Res. 2009, 37:W68-W76.
14. Lee E.B., Lee V.M.Y., Trojanowski J.Q. Gains or losses: molecular mechanisms of TDP-43-mediated neurodegeneration. Nat. Rev. Neurosci. 2012, 13:38-50.
15. Lagier-Tourenne C., Polymenidou M., Cleveland D.W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 2010, 19:R46-R64.
16. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
17. Wang H.-Y., Wang I.F., Bose J., Shen C.K.J. Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 2004, 83:130-139.
18. Kuo P.H., Doudeva L.G., Wang Y.T., Shen C.K.J., Yuan H.S. Structural insights into TDP-43 in nucleic-acid binding and domain interactions. Nucleic Acids Res. 2009, 37:1799-1808.
19. Abhyankar M.M., Urekar C., Reddi P.P. A novel CpG-free vertebrate insulator silences the testis-specific SP-10 gene in somatic tissues. J. Biol. Chem. 2007, 282:36143-36154.
20. Ayala Y.M., Misteli T., Baralle F.E. TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3785-3789.
21. Ou S.H., Wu F., Harrich D., García-Martínez L.F., Gaynor R.B. Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol. 1995, 69:3584-3596.
22. Tollervey J.R., Curk T., Rogelj B., Briese M., Cereda M., Kayikci M., Koenig J., Hortobagyi T., Nishimura A.L., Zupunski V., Patani R., Chandran S., Rot G., Zupan B., Shaw C.E., Ule J. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 2011, 14:452-458.
23. Polymenidou M., Lagier-Tourenne C., Hutt K.R., Huelga S.C., Moran J., Liang T.Y., Ling S.-C., Sun E., Wancewicz E., Mazur C., Kordasiewicz H., Sedaghat Y., Donohue J.P., Shiue L., Bennett C.F., Yeo G.W., Cleveland D.W. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 2011, 14:459-468.
24. Kawahara Y., Mieda-Sato A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3347-3352.
25. Buratti E., De Conti L., Stuani C., Romano M., Baralle M., Baralle F. Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 2010, 277:2268-2281.
26. Gregory R.I., Yan K.-p., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., Shiekhattar R. The microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
27. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
28. Jiang Q., Wang Y., Hao Y., Juan L., Teng M., Zhang X., Li M., Wang G., Liu Y. miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res. 2009, 37:D98-D104.
29. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
30. Flicek P., Amode M.R., Barrell D., Beal K., Brent S., Carvalho-Silva D., Clapham P., Coates G., Fairley S., Fitzgerald S., Gil L., Gordon L., Hendrix M., Hourlier T., Johnson N., Kahari A.K., Keefe D., Keenan S., Kinsella R., Komorowska M., Koscielny G., Kulesha E., Larsson P., Longden I., McLaren W., Muffato M., Overduin B., Pignatelli M., Pritchard B., Riat H.S., Ritchie G.R., Ruffier M., Schuster M., Sobral D., Tang Y.A., Taylor K., Trevanion S., Vandrovcova J., White S., Wilson M., Wilder S.P., Aken B.L., Birney E., Cunningham F., Dunham I., Durbin R., Fernandez-Suarez X.M., Harrow J., Herrero J., Hubbard T.J., Parker A., Proctor G., Spudich G., Vogel J., Yates A., Zadissa A., Searle S.M. Ensembl 2012. Nucleic Acids Res. 2012, 40:D84-D90.
31. Ayala Y.M., De Conti L., Avendaño-Vázquez S.E., Dhir A., Romano M., D'Ambrogio A., Tollervey J., Ule J., Baralle M., Buratti E., Baralle F.E. TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 2010, 30:277-288.
32. Hui J., Reither G., Bindereif A. Novel functional role of CA repeats and hnRNP L in RNA stability. RNA 2003, 9:931-936.
33. Hui J., Hung L.H., Heiner M., Schreiner S., Neumuller N., Reither G., Haas S.A., Bindereif A. Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J. 2005, 24:1988-1998.
34. Huang V., Li L.-C. miRNA goes nuclear. RNA Biol. 2012, 9:269-273.
35. Pesiridis G.S., Lee V.M., Trojanowski J.Q. Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis. Hum. Mol. Genet. 2009, 18:R156-R162.
36. Dharap A., Nakka V.P., Vemuganti R. Altered expression of PIWI RNA in the rat brain after transient focal ischemia. Stroke 2011, 42:1105-1109.
37. Craig A.M., Kang Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 2007, 17:43-52.
38. Bottos A., Rissone A., Bussolino F., Arese M. Neurexins and neuroligins: synapses look out of the nervous system. Cell. Mol. Life Sci. 2011, 68:2655-2666.
39. Tabuchi K., Südhof T.C. Structure and evolution of neurexin genes: insight into the mechanism of alternative splicing. Genomics 2002, 79:849-859.
40. Reichelt A.C., Rodgers R.J., Clapcote S.J. The role of neurexins in schizophrenia and autistic spectrum disorder. Neuropharmacology 2012, 62:1519-1526.
41. Etherton M.R., Blaiss C.A., Powell C.M., Sudhof T.C. Mouse neurexin-1 deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17998-18003.
42. Li Z.D., Lu Y.B., Xu X.L., Gao F.B. The FTD/ALS-associated RNA-binding protein TDP-43 regulates the robustness of neuronal specification through microRNA-9a in Drosophila. Hum. Mol. Genet. 2013, 22:218-225.
43. Parkinson H., Kapushesky M., Kolesnikov N., Rustici G., Shojatalab M., Abeygunawardena N., Berube H., Dylag M., Emam I., Farne A., Holloway E., Lukk M., Malone J., Mani R., Pilicheva E., Rayner T.F., Rezwan F., Sharma A., Williams E., Bradley X.Z., Adamusiak T., Brandizi M., Burdett T., Coulson R., Krestyaninova M., Kurnosov P., Maguire E., Neogi S.G., Rocca-Serra P., Sansone S.A., Sklyar N., Zhao M., Sarkans U., Brazma A. ArrayExpress update-from an archive of functional genomics experiments to the atlas of gene expression. Nucleic Acids Res. 2009, 37:D868-D872.
44. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:D152-D157.
45. Rosenkranz D., Zischler H. proTRAC-a software for probabilistic piRNA cluster detection, visualization and analysis. BMC Bioinforma. 2012, 13:5.
46. Guo W., Chen Y., Zhou X., Kar A., Ray P., Chen X., Rao E.J., Yang M., Ye H., Zhu L., Liu J., Xu M., Yang Y., Wang C., Zhang D., Bigio E.H., Mesulam M., Shen Y., Xu Q., Fushimi K., Wu J.Y. An ALS-associated mutation affecting TDP-43 enhances protein aggregation, fibril formation and neurotoxicity. Nat. Struct. Mol. Biol. 2011, 18:822-830.
47. Chen C., Ridzon D.A., Broomer A.J., Zhou Z., Lee D.H., Nguyen J.T., Barbisin M., Xu N.L., Mahuvakar V.R., Andersen M.R., Lao K.Q., Livak K.J., Guegler K.J. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005, 33:e179.
48. Yan D., He D., He S., Chen X., Fan Z., Chen R. Identification and analysis of intermediate size noncoding RNAs in the human fetal brain. PLoS One 2011, 6:e21652.