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SCIENTIA SINICA Chimica, Volume 48, Issue 5: 477-490(2018) https://doi.org/10.1007/s11426-017-9186-y

Modificaomics: deciphering the functions of biomolecule modifications

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  • ReceivedJan 30, 2018
  • AcceptedFeb 5, 2018
  • PublishedApr 28, 2018

Abstract

The spatiotemporal expression of genes is sophisticatedly controlled through three main layers: transcriptional, translational and post-translational. Now increasing chemical modifications are discovered on genomic DNA, RNA and proteins. These modifications are recognized as additional layer of regulatory mechanisms in controlling gene expression that defines cell status. So far, more than 150 chemical modifications are identified in nucleic acids, and more than 400 discrete types of modifications are identified in proteins. How these modifications are interpreted are fundamental questions to our understanding of living organisms. The omics sciences of systems biology, including genomics, transcriptomics, proteomics, and metabolomics, have been in existence for decades. Due to the large numbers of modifications occurring in DNA, RNA and proteins with regulatory roles, we propose the modificaomics from the words of modification and omics. Modificaomics mainly refers to the comprehensive study of the modifications on DNA, RNA and proteins. In this review, we conceive modificaomics by introducing the discovered modifications in DNA, RNA and proteins as well as summarizing their biological functions. We hope the proposed modificaomics can provide a whole picture of modifications of these biopolymers and simulate the study of the functions of the modifications on DNA, RNA and proteins.


Funded by

国家重点研发项目(2017YFC0906800)

国家自然科学基金(21522507,21672166,21635006,21721005)


Acknowledgment

感谢武汉大学化学与分子科学学院的丁姜慧、张玉樊、游雪娇硕士研究生在本文写作过程中给予的帮助.


Interest statement

The authors declare that they have no conflict of interests.


References

[1] Cantone I, Fisher AG. Nat Struct Mol Biol, 2013, 20: 282-289 CrossRef PubMed Google Scholar

[2] Smith ZD, Meissner A. Nat Rev Genet, 2013, 14: 204-220 CrossRef PubMed Google Scholar

[3] Chen K, Zhao BS, He C. Cell Chem Biol, 2016, 23: 74-85 CrossRef PubMed Google Scholar

[4] Zhao Y, Garcia BA. Cold Spring Harb Perspect Biol, 2015, 7: a025064 CrossRef PubMed Google Scholar

[5] Fu Y, Dominissini D, Rechavi G, He C. Nat Rev Genet, 2014, 15: 293-306 CrossRef PubMed Google Scholar

[6] Kriaucionis S, Heintz N. Science, 2009, 324: 929-930 CrossRef PubMed ADS Google Scholar

[7] Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Science, 2009, 324: 930-935 CrossRef PubMed ADS Google Scholar

[8] Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. Science, 2011, 333: 1300-1303 CrossRef PubMed ADS Google Scholar

[9] He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, Sun Y, Li X, Dai Q, Song CX, Zhang K, He C, Xu GL. Science, 2011, 333: 1303-1307 CrossRef PubMed ADS Google Scholar

[10] Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin-Horkawicz S, Rother KM, Helm M, Bujnicki JM, Grosjean H. Nucl Acids Res, 2013, 41: D262-D267 CrossRef PubMed Google Scholar

[11] Lothrop AP, Torres MP, Fuchs SM. FEBS Lett, 2013, 587: 1247-1257 CrossRef PubMed Google Scholar

[12] Chuang HY, Hofree M, Ideker T. Annu Rev Cell Dev Biol, 2010, 26: 721-744 CrossRef PubMed Google Scholar

[13] Feng S, Jacobsen SE, Reik W. Science, 2010, 330: 622-627 CrossRef PubMed ADS Google Scholar

[14] Yuan BF, Feng YQ. TrAC Trends Anal Chem, 2014, 54: 24-35 CrossRef Google Scholar

[15] Jones PA. Nat Rev Genet, 2012, 13: 484-492 CrossRef PubMed Google Scholar

[16] Robertson KD. Nat Rev Genet, 2005, 6: 597-610 CrossRef PubMed Google Scholar

[17] Huang W, Qi CB, Lv SW, Xie M, Feng YQ, Huang WH, Yuan BF. Anal Chem, 2016, 88: 1378-1384 CrossRef PubMed Google Scholar

[18] Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Nature, 2011, 473: 398-402 CrossRef PubMed ADS Google Scholar

[19] Kellinger MW, Song CX, Chong J, Lu XY, He C, Wang D. Nat Struct Mol Biol, 2012, 19: 831-833 CrossRef PubMed Google Scholar

[20] Tang Y, Chu JM, Huang W, Xiong J, Xing XW, Zhou X, Feng YQ, Yuan BF. Anal Chem, 2013, 85: 6129-6135 CrossRef PubMed Google Scholar

[21] Tang Y, Zheng SJ, Qi CB, Feng YQ, Yuan BF. Anal Chem, 2015, 87: 3445-3452 CrossRef PubMed Google Scholar

[22] Chen ML, Shen F, Huang W, Qi JH, Wang Y, Feng YQ, Liu SM, Yuan BF. Clin Chem, 2013, 59: 824-832 CrossRef Google Scholar

[23] Janulaitis A, Klimašauskas S, Petrušyte M, Butkus V. FEBS Lett, 1983, 161: 131-134 CrossRef Google Scholar

[24] Ehrlich M, Gama-Sosa MA, Carreira LH, Ljungdahl LG, Kuo KC, Gehrke CW. Nucl Acids Res, 1985, 13: 1399-1412 CrossRef Google Scholar

[25] Yu M, Ji L, Neumann DA, Chung DH, Groom J, Westpheling J, He C, Schmitz RJ. Nucl Acids Res, 2015, 44: gkv738 CrossRef PubMed Google Scholar

[26] Reisenauer A, Shapiro L. EMBO J, 2002, 21: 4969-4977 CrossRef Google Scholar

[27] Heyn H, Esteller M. Cell, 2015, 161: 710-713 CrossRef PubMed Google Scholar

[28] Ratel D, Ravanat JL, Berger F, Wion D. Bioessays, 2006, 28: 309-315 CrossRef PubMed Google Scholar

[29] Zhang G, Huang H, Liu D, Cheng Y, Liu X, Zhang W, Yin R, Zhang D, Zhang P, Liu J, Li C, Liu B, Luo Y, Zhu Y, Zhang N, He S, He C, Wang H, Chen D. Cell, 2015, 161: 893-906 CrossRef PubMed Google Scholar

[30] Greer EL, Blanco MA, Gu L, Sendinc E, Liu J, Aristizábal-Corrales D, Hsu CH, Aravind L, He C, Shi Y. Cell, 2015, 161: 868-878 CrossRef PubMed Google Scholar

[31] Fu Y, Luo GZ, Chen K, Deng X, Yu M, Han D, Hao Z, Liu J, Lu X, Dore LC, Weng X, Ji Q, Mets L, He C. Cell, 2015, 161: 879-892 CrossRef PubMed Google Scholar

[32] Wu TP, Wang T, Seetin MG, Lai Y, Zhu S, Lin K, Liu Y, Byrum SD, Mackintosh SG, Zhong M, Tackett A, Wang G, Hon LS, Fang G, Swenberg JA, Xiao AZ. Nature, 2016, 532: 329-333 CrossRef PubMed ADS Google Scholar

[33] Liu J, Zhu Y, Luo GZ, Wang X, Yue Y, Wang X, Zong X, Chen K, Yin H, Fu Y, Han D, Wang Y, Chen D, He C. Nat Commun, 2016, 7: 13052 CrossRef PubMed ADS Google Scholar

[34] Koziol MJ, Bradshaw CR, Allen GE, Costa ASH, Frezza C, Gurdon JB. Nat Struct Mol Biol, 2016, 23: 24-30 CrossRef PubMed Google Scholar

[35] Huang W, Xiong J, Yang Y, Liu SM, Yuan BF, Feng YQ. RSC Adv, 2015, 5: 64046-64054 CrossRef Google Scholar

[36] Schiffers S, Ebert C, Rahimoff R, Kosmatchev O, Steinbacher J, Bohne AV, Spada F, Michalakis S, Nickelsen J, Muller M, Carell T. Angew Chem Int Ed Engl, 2017, 56: 11268--11271. Google Scholar

[37] He C. Nat Chem Biol, 2010, 6: 863-865 CrossRef PubMed Google Scholar

[38] Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, Yi C. Nat Chem Biol, 2016, 12: 311-316 CrossRef PubMed Google Scholar

[39] Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC, Zheng G, Pan T, Solomon O, Eyal E, Hershkovitz V, Han D, Doré LC, Amariglio N, Rechavi G, He C. Nature, 2016, 530: 441-446 CrossRef PubMed ADS Google Scholar

[40] Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, León-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES, Fink G, Regev A. Cell, 2014, 159: 148-162 CrossRef PubMed Google Scholar

[41] Delatte B, Wang F, Ngoc LV, Collignon E, Bonvin E, Deplus R, Calonne E, Hassabi B, Putmans P, Awe S, Wetzel C, Kreher J, Soin R, Creppe C, Limbach PA, Gueydan C, Kruys V, Brehm A, Minakhina S, Defrance M, Steward R, Fuks F. Science, 2016, 351: 282-285 CrossRef PubMed ADS Google Scholar

[42] Huber SM, van Delft P, Mendil L, Bachman M, Smollett K, Werner F, Miska EA, Balasubramanian S. ChemBioChem, 2015, 16: 752-755 CrossRef PubMed Google Scholar

[43] Huang W, Lan MD, Qi CB, Zheng SJ, Wei SZ, Yuan BF, Feng YQ. Chem Sci, 2016, 7: 5495-5502 CrossRef Google Scholar

[44] Xu L, Liu X, Sheng N, Oo KS, Liang J, Chionh YH, Xu J, Ye F, Gao YG, Dedon PC, Fu XY. J Biol Chem, 2017, 292: 14695--14703. Google Scholar

[45] Li X, Xiong X, Yi C. Nat Methods, 2016, 14: 23-31 CrossRef PubMed Google Scholar

[46] Wang Y, Jia G. Genom Proteom Bioinf, 2016, 14: 172-175 CrossRef PubMed Google Scholar

[47] Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang YG, He C. Nat Chem Biol, 2011, 7: 885-887 CrossRef PubMed Google Scholar

[48] Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, Sorek R, Rechavi G. Nature, 2012, 485: 201-206 CrossRef PubMed ADS Google Scholar

[49] Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. Cell, 2012, 149: 1635-1646 CrossRef PubMed Google Scholar

[50] Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR. Nat Methods, 2015, 12: 767-772 CrossRef PubMed Google Scholar

[51] Zhao BS, Roundtree IA, He C. Nat Rev Mol Cell Biol, 2016, 18: 31--42. Google Scholar

[52] Haussmann IU, Bodi Z, Sanchez-Moran E, Mongan NP, Archer N, Fray RG, Soller M. Nature, 2016, 540: 301-304 CrossRef PubMed ADS Google Scholar

[53] Ke S, Alemu EA, Mertens C, Gantman EC, Fak JJ, Mele A, Haripal B, Zucker-Scharff I, Moore MJ, Park CY, Vågbø CB, Kusśnierczyk A, Klungland A, Darnell Jr. JE, Darnell RB. Genes Dev, 2015, 29: 2037-2053 CrossRef PubMed Google Scholar

[54] Fustin JM, Doi M, Yamaguchi Y, Hida H, Nishimura S, Yoshida M, Isagawa T, Morioka MS, Kakeya H, Manabe I, Okamura H. Cell, 2013, 155: 793-806 CrossRef PubMed Google Scholar

[55] Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM, Li CJ, Vågbø CB, Shi Y, Wang WL, Song SH, Lu Z, Bosmans RPG, Dai Q, Hao YJ, Yang X, Zhao WM, Tong WM, Wang XJ, Bogdan F, Furu K, Fu Y, Jia G, Zhao X, Liu J, Krokan HE, Klungland A, Yang YG, He C. Mol Cell, 2013, 49: 18-29 CrossRef PubMed Google Scholar

[56] Batista PJ, Molinie B, Wang J, Qu K, Zhang J, Li L, Bouley DM, Lujan E, Haddad B, Daneshvar K, Carter AC, Flynn RA, Zhou C, Lim KS, Dedon P, Wernig M, Mullen AC, Xing Y, Giallourakis CC, Chang HY. Cell Stem Cell, 2014, 15: 707-719 CrossRef PubMed Google Scholar

[57] Deng X, Su R, Feng X, Wei M, Chen J. Curr Opin Genets Dev, 2017, 48: 1-7 CrossRef PubMed Google Scholar

[58] Shen F, Huang W, Huang JT, Xiong J, Yang Y, Wu K, Jia GF, Chen J, Feng YQ, Yuan BF, Liu SM. J Clin Endocrinol Metabol, 2015, 100: E148-E154 CrossRef PubMed Google Scholar

[59] Cui Q, Shi H, Ye P, Li L, Qu Q, Sun G, Sun G, Lu Z, Huang Y, Yang CG, Riggs AD, He C, Shi Y. Cell Rep, 2017, 18: 2622-2634 CrossRef PubMed Google Scholar

[60] Li Z, Weng H, Su R, Weng X, Zuo Z, Li C, Huang H, Nachtergaele S, Dong L, Hu C, Qin X, Tang L, Wang Y, Hong GM, Huang H, Wang X, Chen P, Gurbuxani S, Arnovitz S, Li Y, Li S, Strong J, Neilly MB, Larson RA, Jiang X, Zhang P, Jin J, He C, Chen J. Cancer Cell, 2017, 31: 127-141 CrossRef PubMed Google Scholar

[61] Zhang S, Zhao BS, Zhou A, Lin K, Zheng S, Lu Z, Chen Y, Sulman EP, Xie K, Bögler O, Majumder S, He C, Huang S. Cancer Cell, 2017, 31: 591-606.e6 CrossRef PubMed Google Scholar

[62] Zhang C, Samanta D, Lu H, Bullen JW, Zhang H, Chen I, He X, Semenza GL. Proc Natl Acad Sci USA, 2016, 113: E2047-E2056 CrossRef PubMed ADS Google Scholar

[63] Feillet C, van der Horst GTJ, Levi F, Rand DA, Delaunay F. Front Neurol, 2015, 6: 96 CrossRef Google Scholar

[64] Aguilo F, Zhang F, Sancho A, Fidalgo M, Di Cecilia S, Vashisht A, Lee DF, Chen CH, Rengasamy M, Andino B, Jahouh F, Roman A, Krig SR, Wang R, Zhang W, Wohlschlegel JA, Wang J, Walsh MJ. Cell Stem Cell, 2015, 17: 689-704 CrossRef PubMed Google Scholar

[65] Mauer J, Luo X, Blanjoie A, Jiao X, Grozhik AV, Patil DP, Linder B, Pickering BF, Vasseur JJ, Chen Q, Gross SS, Elemento O, Debart F, Kiledjian M, Jaffrey SR. Nature, 2017, 541: 371-375 CrossRef PubMed ADS Google Scholar

[66] Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T. Nucl Acids Res, 2012, 40: 5023-5033 CrossRef PubMed Google Scholar

[67] Li B, Luo X, Dong Y. Bioconjugate Chem, 2016, 27: 849-853 CrossRef PubMed Google Scholar

[68] Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ. Cell Stem Cell, 2010, 7: 618-630 CrossRef PubMed Google Scholar

[69] Fu L, Guerrero CR, Zhong N, Amato NJ, Liu Y, Liu S, Cai Q, Ji D, Jin SG, Niedernhofer LJ, Pfeifer GP, Xu GL, Wang Y. J Am Chem Soc, 2014, 136: 11582-11585 CrossRef PubMed Google Scholar

[70] Basanta-Sanchez M, Wang R, Liu Z, Ye X, Li M, Shi X, Agris PF, Zhou Y, Huang Y, Sheng J. ChemBioChem, 2017, 18: 72-76 CrossRef PubMed Google Scholar

[71] Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. Nature, 2014, 515: 143-146 CrossRef PubMed ADS Google Scholar

[72] Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C. Nat Chem Biol, 2015, 11: 592-597 CrossRef PubMed Google Scholar

[73] Sun WJ, Li JH, Liu S, Wu J, Zhou H, Qu LH, Yang JH. Nucl Acids Res, 2015, 11: 592--597. Google Scholar

[74] Vaidyanathan PP, AlSadhan I, Merriman DK, Al-Hashimi HM, Herschlag D. RNA, 2017, 23: 611-618 CrossRef PubMed Google Scholar

[75] deLorimier E, Hinman MN, Copperman J, Datta K, Guenza M, Berglund JA. J Biol Chem, 2017, 292: 4350-4357 CrossRef PubMed Google Scholar

[76] Daffis S, Szretter KJ, Schriewer J, Li J, Youn S, Errett J, Lin TY, Schneller S, Zust R, Dong H, Thiel V, Sen GC, Fensterl V, Klimstra WB, Pierson TC, Buller RM, Gale Jr. M, Shi PY, Diamond MS. Nature, 2010, 468: 452-456 CrossRef PubMed ADS Google Scholar

[77] Kumar S, Mapa K, Maiti S. Biochemistry, 2014, 53: 1607-1615 CrossRef PubMed Google Scholar

[78] Dai Q, Moshitch-Moshkovitz S, Han D, Kol N, Amariglio N, Rechavi G, Dominissini D, He C. Nat Meth, 2017, 14: 695-698 CrossRef PubMed Google Scholar

[79] Sergiev PV, Golovina AY, Prokhorova IV, Sergeeva OV, Osterman IA, Nesterchuk MV, Burakovsky DE, Bogdanov AA, Dontsova OA. In: Ribosomes: Structure, Function, and Dynamics. 2011. 97--110. Google Scholar

[80] Sloan KE, Warda AS, Sharma S, Entian KD, Lafontaine DLJ, Bohnsack MT. RNA Biol, 2017, 14: 1138-1152 CrossRef PubMed Google Scholar

[81] Decatur WA, Fournier MJ. Trends Biochem Sci, 2002, 27: 344-351 CrossRef Google Scholar

[82] Jiang J, Seo H, Chow CS. Acc Chem Res, 2016, 49: 893-901 CrossRef PubMed Google Scholar

[83] Helm M. Nucl Acids Res, 2006, 34: 721-733 CrossRef PubMed Google Scholar

[84] Ge J, Yu YT. Trends Biochem Sci, 2013, 38: 210-218 CrossRef PubMed Google Scholar

[85] Behrmann E, Loerke J, Budkevich TV, Yamamoto K, Schmidt A, Penczek PA, Vos MR, Bürger J, Mielke T, Scheerer P, Spahn CMT. Cell, 2015, 161: 845-857 CrossRef PubMed Google Scholar

[86] Chow CS, Lamichhane TN, Mahto SK. ACS Chem Biol, 2007, 2: 610-619 CrossRef PubMed Google Scholar

[87] Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV. Nat Rev Micro, 2015, 13: 42-51 CrossRef PubMed Google Scholar

[88] Jack K, Bellodi C, Landry DM, Niederer RO, Meskauskas A, Musalgaonkar S, Kopmar N, Krasnykh O, Dean AM, Thompson SR, Ruggero D, Dinman JD. Mol Cell, 2011, 44: 660-666 CrossRef PubMed Google Scholar

[89] Brown JWS, Echeverria M, Qu LH. Trends Plant Sci, 2003, 8: 42-49 CrossRef Google Scholar

[90] Lorenz C, Lünse CE, Mörl M. Biomolecules, 2017, 7: 35 CrossRef PubMed Google Scholar

[91] Duechler M, Leszczyńska G, Sochacka E, Nawrot B. Cell Mol Life Sci, 2016, 73: 3075-3095 CrossRef PubMed Google Scholar

[92] Wilusz JE. WIREs RNA, 2015, 6: 453-470 CrossRef PubMed Google Scholar

[93] Björk GR, Hagervall TG. EcoSal Plus, 2014, 6: 1 CrossRef Google Scholar

[94] Manickam N, Joshi K, Bhatt MJ, Farabaugh PJ. Nucl Acids Res, 2016, 44: 1871-1881 CrossRef PubMed Google Scholar

[95] Hori H. Front Genet, 2014, 5: 144 CrossRef Google Scholar

[96] Agris PF. EMBO Rep, 2008, 9: 629-635 CrossRef PubMed Google Scholar

[97] Machnicka MA, Olchowik A, Grosjean H, Bujnicki JM. RNA Biol, 2014, 11: 1619-1629 CrossRef PubMed Google Scholar

[98] Agris PF. Prog Nucl Acid Res Mol Biol, 1996, 53: 79--129. Google Scholar

[99] Torres AG, Batlle E, Ribas de Pouplana L. Trends Mol Med, 2014, 20: 306-314 CrossRef PubMed Google Scholar

[100] Guy MP, Shaw M, Weiner CL, Hobson L, Stark Z, Rose K, Kalscheuer VM, Gecz J, Phizicky EM. Human Mutat, 2015, 36: 1176-1187 CrossRef PubMed Google Scholar

[101] Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, Lyko F. Genes Dev, 2010, 24: 1590-1595 CrossRef PubMed Google Scholar

[102] Anderson P, Ivanov P. FEBS Lett, 2014, 588: 4297-4304 CrossRef PubMed Google Scholar

[103] Lee YS, Shibata Y, Malhotra A, Dutta A. Genes Dev, 2009, 23: 2639-2649 CrossRef PubMed Google Scholar

[104] Klassen R, Paluszynski JP, Wemhoff S, Pfeiffer A, Fricke J, Meinhardt F. Mol Microbiol, 2008, 69: 681-697 CrossRef PubMed Google Scholar

[105] Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C, Humphreys P, Lukk M, Lombard P, Treps L, Popis M, Kellner S, Hölter SM, Garrett L, Wurst W, Becker L, Klopstock T, Fuchs H, Gailus-Durner V, Hrabĕ de Angelis M, Káradóttir RT, Helm M, Ule J, Gleeson JG, Odom DT, Frye M. EMBO J, 2014, 33: 2020-2039 CrossRef PubMed Google Scholar

[106] Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu G, Anderson P, Pan T, Hatzoglou M. J Biol Chem, 2012, 287: 42708-42725 CrossRef PubMed Google Scholar

[107] Preston MA, D'Silva S, Kon Y, Phizicky EM. RNA, 2013, 19: 243-256 CrossRef PubMed Google Scholar

[108] Han L, Kon Y, Phizicky EM. RNA, 2015, 21: 188-201 CrossRef PubMed Google Scholar

[109] Chan CTY, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, Begley TJ. PLoS Genet, 2010, 6: e1001247 CrossRef PubMed Google Scholar

[110] Tuorto F, Lyko F. Open Biol, 2016, 6: 160287 CrossRef PubMed Google Scholar

[111] Suzuki T, Suzuki T. Nucl Acids Res, 2014, 42: 7346-7357 CrossRef PubMed Google Scholar

[112] Miyauchi K, Kimura S, Suzuki T. Nat Chem Biol, 2013, 9: 105-111 CrossRef PubMed Google Scholar

[113] Matuszewski M, Sochacka E. Bioorg Med Chem Lett, 2014, 24: 2703-2706 CrossRef PubMed Google Scholar

[114] Zhang X, Cozen AE, Liu Y, Chen Q, Lowe TM. Trends Mol Med, 2016, 22: 1025-1034 CrossRef PubMed Google Scholar

[115] Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X. Science, 2005, 307: 932-935 CrossRef PubMed ADS Google Scholar

[116] Ji L, Chen X. Cell Res, 2012, 22: 624-636 CrossRef PubMed Google Scholar

[117] Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, Feng G, Peng H, Zhang X, Zhang Y, Qian J, Duan E, Zhai Q, Zhou Q. Science, 2016, 351: 397-400 CrossRef PubMed ADS Google Scholar

[118] Yan M, Wang Y, Hu Y, Feng Y, Dai C, Wu J, Wu D, Zhang F, Zhai Q. Anal Chem, 2013, 85: 12173-12181 CrossRef PubMed Google Scholar

[119] Breker M, Schuldiner M. Nat Rev Mol Cell Biol, 2014, 15: 453-464 CrossRef PubMed Google Scholar

[120] Lawrence M, Daujat S, Schneider R. Trends Genets, 2016, 32: 42-56 CrossRef PubMed Google Scholar

[121] Kouzarides T. Cell, 2007, 128: 693-705 CrossRef PubMed Google Scholar

[122] Bannister AJ, Kouzarides T. Cell Res, 2011, 21: 381-395 CrossRef PubMed Google Scholar

[123] Rose NR, Klose RJ. Biochim Biophys Acta, 2014, 1839: 1362-1372 CrossRef PubMed Google Scholar

[124] Silva AMN, Vitorino R, Domingues MRM, Spickett CM, Domingues P. Free Radical Biol Med, 2013, 65: 925-941 CrossRef PubMed Google Scholar

[125] Prabakaran S, Lippens G, Steen H, Gunawardena J. WIREs Syst Biol Med, 2012, 4: 565-583 CrossRef PubMed Google Scholar

[126] Salovska B, Tichy A, Rezacova M, Vavrova J, Novotna E. Rev Anal Chem, 2012, 31: 29-41 CrossRef Google Scholar

[127] Ubersax JA, Ferrell Jr JE. Nat Rev Mol Cell Biol, 2007, 8: 530-541 CrossRef PubMed Google Scholar

[128] Sacco F, Perfetto L, Castagnoli L, Cesareni G. FEBS Lett, 2012, 586: 2732-2739 CrossRef PubMed Google Scholar

[129] Moremen KW, Tiemeyer M, Nairn AV. Nat Rev Mol Cell Biol, 2012, 13: 448-462 CrossRef PubMed Google Scholar

[130] Resh MD. Curr Biol, 2013, 23: R431-R435 CrossRef PubMed Google Scholar

[131] Braakman I, Bulleid NJ. Annu Rev Biochem, 2011, 80: 71-99 CrossRef PubMed Google Scholar

[132] Reimand J, Wagih O, Bader GD. PLoS Genet, 2015, 11: e1004919 CrossRef PubMed Google Scholar

[133] Cedar H, Bergman Y. Nat Rev Genet, 2009, 10: 295-304 CrossRef PubMed Google Scholar

[134] Walport LJ, Hopkinson RJ, Schofield CJ. Curr Opin Chem Biol, 2012, 16: 525-534 CrossRef PubMed Google Scholar

[135] Falnes PØ, Johansen RF, Seeberg E. Nature, 2002, 419: 178-182 CrossRef PubMed Google Scholar

[136] Liu F, Clark W, Luo G, Wang X, Fu Y, Wei J, Wang X, Hao Z, Dai Q, Zheng G, Ma H, Han D, Evans M, Klungland A, Pan T, He C. Cell, 2016, 167: 816-828.e16 CrossRef PubMed Google Scholar

[137] Haag S, Sloan KE, Ranjan N, Warda AS, Kretschmer J, Blessing C, Hübner B, Seikowski J, Dennerlein S, Rehling P, Rodnina MV, Höbartner C, Bohnsack MT. EMBO J, 2016, 35: 2104-2119 CrossRef PubMed Google Scholar

[138] Kawarada L, Suzuki T, Ohira T, Hirata S, Miyauchi K, Suzuki T. Nucl Acids Res, 2017, 45: 7401-7415 CrossRef PubMed Google Scholar

[139] Westbye MP, Feyzi E, Aas PA, Vågbø CB, Talstad VA, Kavli B, Hagen L, Sundheim O, Akbari M, Liabakk NB, Slupphaug G, Otterlei M, Krokan HE. J Biol Chem, 2008, 283: 25046-25056 CrossRef PubMed Google Scholar

[140] van den Born E, Vågbø CB, Songe-Møller L, Leihne V, Lien GF, Leszczynska G, Malkiewicz A, Krokan HE, Kirpekar F, Klungland A, Falnes PØ. Nat Commun, 2011, 2: 172 CrossRef PubMed ADS Google Scholar

[141] Jia G, Yang CG, Yang S, Jian X, Yi C, Zhou Z, He C. FEBS Lett, 2008, 582: 3313-3319 CrossRef PubMed Google Scholar

[142] Landgraf BJ, McCarthy EL, Booker SJ. Annu Rev Biochem, 2016, 85: 485-514 CrossRef PubMed Google Scholar

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