Dynamic landscape and regulation of RNA editing in mammals

Nature

Volumn 550, Issue 7675, 2017, Pages 249-254

  Tan, Meng How ^a,b,c   Li, Qin ^a,r   Shanmugam, Raghuvaran ^b,c   Piskol, Robert ^a   Kohler, Jennefer ^a   Young, Amy N ^a   Liu, Kaiwen Ivy ^c   Zhang, Rui ^a,r   Ramaswami, Gokul ^a   Ariyoshi, Kentaro ^d   Gupte, Ankita ^e   Keegan, Liam P ^f,g   George, Cyril X ^h   Ramu, Avinash ⁱ   Huang, Ni ⁱ   Pollina, Elizabeth A ^a   Leeman, Dena S ^a   Rustighi, Alessandra ^j,k   Goh, Y P Sharon ^l   Aguet, François ⁿ   Ardlie, Kristin G ⁿ   Cummings, Beryl B ^n,o   Gelfand, Ellen T ⁿ   Getz, Gad ^a,p   Hadley, Kane ⁿ   Handsaker, Robert E ^n,q   Huang, Katherine H ⁿ   Kashin, Seva ^n,q   Karczewski, Konrad J ^n,o   Lek, Monkol ^n,o   Li, Xiao ^n,r   MacArthur, Daniel G ^n,o   Nedzel, Jared L ⁿ   Nguyen, Duyen T ⁿ   Noble, Michael S ⁿ   Segrè, Ayellet V ⁿ   Trowbridge, Casandra A ⁿ   Tukiainen, Taru ^n,o   Abell, Nathan S ^a,r   Balliu, Brunilda ^a   Barshir, Ruth ^s   Basha, Omer ^s   Battle, Alexis ^t   Bogu, Gireesh K ^u,v   Brown, Andrew ^w,x,y   Brown, Christopher D ^z   Castel, Stephane E ^aa,ab   Chen, Lin S ^ac   Chiang, Colby ⁱ   Conrad, Donald F ⁱ   Cox, Nancy J ^ad   Damani, Farhan N ^t   Davis, Joe R ^a,r   Delaneau, Olivier ^w,x,y   Dermitzakis, Emmanouil T ^w,x,y   Engelhardt, Barbara E ^ae   Eskin, Eleazar ^af,ag   Ferreira, Pedro G ^ah,ai   Frésard, Laure ^a,r   Gamazon, Eric R ^ad,aj   Garrido Martín, Diego ^u,v   Gewirtz, Ariel D H ^ak   Gliner, Genna ^ae   Gloudemans, Michael J ^a,r   Guigo, Roderic ^u,v,al   Hall, Ira M ⁱ   Han, Buhm ^am   He, Yuan ^an   Hormozdiari, Farhad ^af   Howald, Cedric ^w,x,y   Im, Hae Kyung ^ac   Jo, Brian ^ak   Kang, Eun Yong ^af   Kim, Yungil ^t   Kim Hellmuth, Sarah ^aa,ab   Lappalainen, Tuuli ^aa,ab   Li, Gen ^ao   Li, Xin ^a   Liu, Boxiang ^a,r   Mangul, Serghei ^af   McCarthy, Mark I ^ap,aq,ar   McDowell, Ian C ^as   Mohammadi, Pejman ^aa,ab   Monlong, Jean ^u,v,at   Montgomery, Stephen B ^a,r   Muñoz Aguirre, Manuel ^u,v,au   Ndungu, Anne W ^ap   Nicolae, Dan L ^ac   Nobel, Andrew B ^av,aw   Oliva, Meritxell ^ac,ax   Ongen, Halit ^w,x,y   Palowitch, John J ^av   Panousis, Nikolaos ^w,x,y   Papasaikas, Panagiotis ^u,v   Park, Yoson ^z   Parsana, Princy ^t   Payne, Anthony J ^ap   Peterson, Christine B ^ay   Quan, Jie ^az   Reverter, Ferran ^u,v,ba   Sabatti, Chiara ^r   Saha, Ashis ^t   Sammeth, Michael ^bb   Scott, Alexandra J ⁱ   Shabalin, Andrey A ^bc   Sodaei, Reza ^u,v   Stephens, Matthew ^ac   Stranger, Barbara E ^ac,ax   Strober, Benjamin J ^an   Sul, Jae Hoon ^bd   Tsang, Emily K ^a,r,ac   Urbut, Sarah ^ac   Van De Bunt, Martijn ^ap,aq   Wang, Gao ^ac   Wen, Xiaoquan ^be   Wright, Fred A ^bf   Xi, Hualin S ^az   Yeger Lotem, Esti ^s   Zappala, Zachary ^a,r   Zaugg, Judith B ^bg   Zhou, Yi Hui ^bf   Akey, Joshua M ^ak   Bates, Daniel ^bh   Chan, Joanne ^r   Claussnitzer, Melina ^n,q,bi   Demanelis, Kathryn ^ac   Diegel, Morgan ^bh   Doherty, Jennifer A ^bj   Feinberg, Andrew P ^an,bk,bl   Fernando, Marian S ^ac,ax   Halow, Jessica ^bh   Hansen, Kasper D ^bk,bm   Haugen, Eric ^bh   Hickey, Peter F ^bm   Hou, Lei ^n,bn   Jasmine, Farzana ^ac   Jian, Ruiqi ^r   Jiang, Lihua ^r   Johnson, Audra ^bh   Kaul, Rajinder ^bh   Kellis, Manolis ^n,bn   Kibriya, Muhammad G ^ac   Lee, Kristen ^bh   Lin, Jessica ^r,bo   Lin, Shin ^r,bp   Linder, Sandra ^a,r   Linke, Caroline ^ac,ax   Liu, Yaping ^n,bn   Maurano, Matthew T ^bq   Molinie, Benoit ⁿ   Nelson, Jemma ^bh   Neri, Fidencio J ^bh   Park, Yongjin ^n,bn   Pierce, Brandon L ^ac   Rinaldi, Nicola J ^n,bn   Rizzardi, Lindsay F ^bk   Sandstrom, Richard ^bh   Skol, Andrew ^ac,ax   Smith, Kevin S ^a,r   Snyder, Michael P ^r   Stamatoyannopoulos, John ^bh,bo   Tang, Hua ^r   Wang, Li ⁿ   Wang, Meng ^r   Van Wittenberghe, Nicholas ⁿ   Wu, Fan ^ac,ax   Nierras, Concepcion R ^br   Branton, Philip A ^bs   Carithers, Latarsha J ^bs,bt   Guan, Ping ^bs   Moore, Helen M ^bs   Rao, Abhi ^bs   Vaught, Jimmie B ^bs   Gould, Sarah E ^bu   Lockart, Nicole C ^bu   Martin, Casey ^bu   Struewing, Jeffery P ^bu   Volpi, Simona ^bu   Addington, Anjene M ^bv   Koester, Susan E ^bv   Little, A Roger ^bw   Brigham, Lori E ^bx   Hasz, Richard ^by   Hunter, Marcus ^bz   Johns, Christopher ^ca   Johnson, Mark ^cb   Kopen, Gene ^cc   Leinweber, William F ^cc   Lonsdale, John T ^cc   McDonald, Alisa ^cc   Mestichelli, Bernadette ^cc   Myer, Kevin ^bz   Roe, Brian ^bz   Salvatore, Michael ^cc   Shad, Saboor ^cc   Thomas, Jeffrey A ^cc   Walters, Gary ^cb   Washington, Michael ^cb   Wheeler, Joseph ^ca   Bridge, Jason ^cd   Foster, Barbara A ^ce   Gillard, Bryan M ^ce   Karasik, Ellen ^ce   Kumar, Rachna ^ce   Miklos, Mark ^cd   Moser, Michael T ^ce   Jewell, Scott D ^cf   Montroy, Robert G ^cf   Rohrer, Daniel C ^cf   Valley, Dana R ^cf   Davis, David A ^cg   Mash, Deborah C ^cg   Undale, Anita H ^ch   Smith, Anna M ^ci   Tabor, David E ^ci   Roche, Nancy V ^ci   McLean, Jeffrey A ^ci   Vatanian, Negin ^ci   Robinson, Karna L ^ci   Sobin, Leslie ^ci   Barcus, Mary E ^ci   Valentino, Kimberly M ^ci   Qi, Liqun ^ci   Hunter, Steven ^ci   Hariharan, Pushpa ^ci   Singh, Shilpi ^ci   Um, Ki Sung ^ci   Matose, Takunda ^ci   Tomaszewski, Maria M ^ci   Barker, Laura K ^cj   Mosavel, Maghboeba ^ck   Siminoff, Laura A ^cj   Traino, Heather M ^cj   Flicek, Paul ^cl   Juettemann, Thomas ^cl   Ruffier, Magali ^cl   Sheppard, Dan ^cl   Taylor, Kieron ^cl   Trevanion, Stephen J ^cl   Zerbino, Daniel R ^cl   Craft, Brian ^cm   Goldman, Mary ^cm   Haeussler, Maximilian ^cm   Kent, W James ^cm   Lee, Christopher M ^cm   Paten, Benedict ^cm   Rosenbloom, Kate R ^cm   Vivian, John ^cm   Zhu, Jingchun ^cm   Chawla, Ajay ^l   Del Sal, Giannino ^j,k   Peltz, Gary ^a   Brunet, Anne ^a   Samuel, Charles E ^h   O'Connell, Mary A ^f,g   Walkley, Carl R ^e,m   Nishikura, Kazuko ^d   Li, Jin Billy ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Nanyang Technological University   (Singapore)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d WISTAR INSTITUTE   (United States)

^e ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g MASARYK UNIVERSITY   (Czech Republic)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j UNIVERSITY OF TRIESTE   (Italy)

^k CIB   (Italy)

^l UNIVERSITY OF CALIFORNIA   (United States)

^m UNIVERSITY OF MELBOURNE   (Australia)

ⁿ HARVARD UNIVERSITY   (United States)

^o MASSACHUSETTS GENERAL HOSPITAL   (United States)

^p MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^q HARVARD MEDICAL SCHOOL   (United States)

^r STANFORD UNIVERSITY   (United States)

^s BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^t Johns Hopkins University   (United States)

^u BARCELONA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Spain)

^v UNIVERSITAT POMPEU FABRA   (Spain)

^w UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^x UNIVERSITY OF GENEVA   (Switzerland)

^y SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^z UNIVERSITY OF PENNSYLVANIA   (United States)

^aa NEW YORK GENOME CENTER   (United States)

^ab NewYork Presbyterian Hospital   (United States)

^ac UNIVERSITY OF CHICAGO   (United States)

^ad VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^ae Princeton University   (United States)

^af University of California   (United States)

^ag UNIVERSITY OF CALIFORNIA   (United States)

^ah UNIVERSITY OF PORTO   (Portugal)

^ai UNIVERSITY OF PORTO   (Portugal)

^aj UNIVERSITY OF AMSTERDAM   (Netherlands)

^ak PRINCETON UNIVERSITY   (United States)

^al HOSPITAL DEL MAR   (Spain)

^am University of Ulsan College of Medicine   (South Korea)

^an Johns Hopkins University   (United States)

^ao McGill University ^*  (United States)

^ap UNIVERSITY OF OXFORD   (United Kingdom)

^aq UNIVERSITY OF OXFORD   (United Kingdom)

^ar CHURCHILL HOSPITAL   (United Kingdom)

^as DUKE UNIVERSITY   (United States)

^at MCGILL UNIVERSITY   (Canada)

^au UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^av University of North Carolina at Chapel Hill   (United States)

^aw IL   (United States)

^ax UNIVERSITY OF CHICAGO   (United States)

^ay UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^az PFIZER INC   (United States)

^ba UNIVERSITY OF BARCELONA   (Spain)

^bb FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^bc UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^bd UNIVERSITY OF CALIFORNIA   (United States)

^be UNIVERSITY OF MICHIGAN   (United States)

^bf NORTH CAROLINA STATE UNIVERSITY   (United States)

^bg EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^bh Altius Institute for Biomedical Sciences   (United States)

^bi UNIVERSITY OF HOHENHEIM   (Germany)

^bj UNIVERSITY OF UTAH   (United States)

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

^bl JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^bm JOHNS HOPKINS UNIVERSITY   (United States)

^bn MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^bo UNIVERSITY OF WASHINGTON   (United States)

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

^bq NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^br NATIONAL INSTITUTES OF HEALTH   (United States)

^bs NATIONAL CANCER INSTITUTE   (United States)

^bt NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^bu NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^bv NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^bw NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^bx Washington Regional Transplant Community   (United States)

^by Gift of Life Donor Program   (United States)

^bz LifeGift   (United States)

^ca Center for Organ Recovery and Education   (United States)

^cb LifeNet Health   (United States)

^cc National Disease Research Interchange   (United States)

^cd UNYTS   (United States)

^ce ROSWELL PARK CANCER INSTITUTE   (United States)

^cf VAN ANDEL RESEARCH INSTITUTE   (United States)

^cg UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^ch NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^ci FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^cj TEMPLE UNIVERSITY   (United States)

^ck VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^cl EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^cm University of California Santa Cruz   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAR1 PROTEIN; ADAR2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ADAR1 PROTEIN, HUMAN; ADAR1 PROTEIN, MOUSE; ADAR2 PROTEIN, MOUSE; ADARB1 PROTEIN, HUMAN; ADENOSINE DEAMINASE; AIMP2 PROTEIN, HUMAN; NUCLEAR PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTOME;

ENZYME; GENETIC ENGINEERING; INHIBITOR; MAMMAL; RNA; SPATIOTEMPORAL ANALYSIS;

ADULT; ANIMAL TISSUE; ARTICLE; CODING; CONTROLLED STUDY; ENZYME REGULATION; FETUS; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EDITING; ANIMAL; ANTIBODY SPECIFICITY; FEMALE; GENETICS; GENOTYPE; HEK293 CELL LINE; MALE; METABOLISM; MUSCLE; PRIMATE; PROTEIN DEGRADATION; SPATIOTEMPORAL ANALYSIS; SPECIES DIFFERENCE;

MAMMALIA; PRIMATES;

ADENOSINE DEAMINASE; ANIMALS; FEMALE; GENOTYPE; HEK293 CELLS; HUMANS; MALE; MICE; MUSCLES; NUCLEAR PROTEINS; ORGAN SPECIFICITY; PRIMATES; PROTEOLYSIS; RNA EDITING; RNA-BINDING PROTEINS; SPATIO-TEMPORAL ANALYSIS; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 85031298074     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature24041     Document Type: Article

References (34)

1. Nishikura, K. Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem. 79, 321-349 (2010).
2. Bahn, J. H. et al. Accurate identification of A-to-I RNA editing in human by transcriptome sequencing. Genome Res. 22, 142-150 (2012).
3. Danecek, P. et al. High levels of RNA-editing site conservation amongst 15 laboratory mouse strains. Genome Biol. 13, R26 (2012).
4. Li, J. B. et al. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324, 1210-1213 (2009).
5. Peng, Z. et al. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat. Biotechnol. 30, 253-260 (2012).
6. Ramaswami, G. et al. Accurate identification of human Alu and non-Alu RNA editing sites. Nat. Methods 9, 579-581 (2012).
7. Ramaswami, G. et al. Identifying RNA editing sites using RNA sequencing data alone. Nat. Methods 10, 128-132 (2013).
8. Behm, M. & Öhman, M. RNA editing: A contributor to neuronal dynamics in the mammalian brain. Trends Genet. 32, 165-175 (2016).
9. Rosenthal, J. J. C. & Seeburg, P. H. A-to-I RNA editing: effects on proteins key to neural excitability. Neuron 74, 432-439 (2012).
10. Li, J. B. & Church, G. M. Deciphering the functions and regulation of brain-enriched A-to-I RNA editing. Nat. Neurosci. 16, 1518-1522 (2013).
11. Ramaswami, G. & Li, J. B. RADAR: A rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res. 42, D109-D113 (2014).
12. Ramaswami, G. & Li, J. B. Identification of human RNA editing sites: A historical perspective. Methods 107, 42-47 (2016).
13. Wahlstedt, H., Daniel, C., Ensterö, M. & Öhman, M. Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res. 19, 978-986 (2009).
14. Stulić, M. & Jantsch, M. F. Spatio-temporal profiling of Filamin A RNA-editing reveals ADAR preferences and high editing levels outside neuronal tissues. RNA Biol. 10, 1611-1617 (2013).
15. Zhang, Q. & Xiao, X. Genome sequence-independent identification of RNA editing sites. Nat. Methods 12, 347-350 (2015).
16. Picardi, E. et al. Profiling RNA editing in human tissues: Towards the inosinome Atlas. Sci. Rep. 5, 14941 (2015).
17. Hwang, T. et al. Dynamic regulation of RNA editing in human brain development and disease. Nat. Neurosci. 19, 1093-1099 (2016).
18. Stellos, K. et al. Adenosine-to-inosine RNA editing controls cathepsin S expression in atherosclerosis by enabling HuR-mediated post-transcriptional regulation. Nat. Med. 22, 1140-1150 (2016).
19. Zhang, R. et al. Quantifying RNA allelic ratios by microfluidic multiplex PCR and sequencing. Nat. Methods 11, 51-54 (2014).
20. Oakes, E., Anderson, A., Cohen-Gadol, A. & Hundley, H. A. Adenosine deaminase that acts on RNA 3 (ADAR3) binding to glutamate receptor subunit b pre-mRNA inhibits RNA editing in glioblastoma. J. Biol. Chem. 292, 4326-4335 (2017).
21. Liddicoat, B. J. et al. RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science 349, 1115-1120 (2015).
22. Daniel, C., Silberberg, G., Behm, M. & Öhman, M. Alu elements shape the primate transcriptome by cis-regulation of RNA editing. Genome Biol. 15, R28 (2014).
23. Pinto, Y., Cohen, H. Y. & Levanon, E. Y. Mammalian conserved ADAR targets comprise only a small fragment of the human editosome. Genome Biol. 15, R5 (2014).
24. Sapiro, A. L., Deng, P., Zhang, R. & Li, J. B. Cis regulatory effects on A-to-I RNA editing in related Drosophila species. Cell Reports 11, 697-703 (2015).
25. Ramaswami, G. et al. Genetic mapping uncovers cis-regulatory landscape of RNA editing. Nat. Commun. 6, 8194 (2015).
26. Barbosa-Morais, N. L. et al. The evolutionary landscape of alternative splicing in vertebrate species. Science 338, 1587-1593 (2012).
27. Merkin, J., Russell, C., Chen, P. & Burge, C. B. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science 338, 1593-1599 (2012).
28. Bhogal, B. et al. Modulation of dADAR-dependent RNA editing by the Drosophila fragile X mental retardation protein. Nat. Neurosci. 14, 1517-1524 (2011).
29. Marcucci, R. et al. Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J. 30, 4211-4222 (2011).
30. Kim, M. J. et al. Downregulation of FUSE-binding protein and c-myc by tRNA synthetase cofactor p38 is required for lung cell differentiation. Nat. Genet. 34, 330-336 (2003).
31. Hsieh, C.-L. et al. ADAR1 deaminase contributes to scheduled skeletal myogenesis progression via stage-specific functions. Cell Death Differ. 21, 707-719 (2014).
32. Tariq, A. et al. RNA-interacting proteins act as site-specific repressors of ADAR2-mediated RNA editing and fluctuate upon neuronal stimulation. Nucleic Acids Res. 41, 2581-2593 (2013).
33. Garncarz, W., Tariq, A., Handl, C., Pusch, O. & Jantsch, M. F. A high-throughput screen to identify enhancers of ADAR-mediated RNA-editing. RNA Biol. 10, 192-204 (2013).
34. Pipes, L. et al. The non-human primate reference transcriptome resource (NHPRTR) for comparative functional genomics. Nucleic Acids Res. 41, D906-D914 (2013).