Skip to main content
SpringerLink
Log in

Modificaomics: deciphering the functions of biomolecule modifications

  • Reviews
  • Published:
Science China Chemistry Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Cantone I, Fisher AG. Nat Struct Mol Biol, 2013, 20: 282–289

    Article  PubMed  CAS  Google Scholar 

  2. Smith ZD, Meissner A. Nat Rev Genet, 2013, 14: 204–220

    Article  PubMed  CAS  Google Scholar 

  3. Chen K, Zhao BS, He C. Cell Chem Biol, 2016, 23: 74–85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Zhao Y, Garcia BA. Cold Spring Harb Perspect Biol, 2015, 7: a025064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Fu Y, Dominissini D, Rechavi G, He C. Nat Rev Genet, 2014, 15: 293–306

    Article  PubMed  CAS  Google Scholar 

  6. Kriaucionis S, Heintz N. Science, 2009, 324: 929–930

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. Science, 2011, 333: 1300–1303

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  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. Nucleic Acids Res, 2013, 41: D262–D267

    Article  PubMed  CAS  Google Scholar 

  11. Lothrop AP, Torres MP, Fuchs SM. FEBS Lett, 2013, 587: 1247–1257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Chuang HY, Hofree M, Ideker T. Annu Rev Cell Dev Biol, 2010, 26: 721–744

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Feng S, Jacobsen SE, Reik W. Science, 2010, 330: 622–627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Yuan BF, Feng YQ. TrAC Trends Anal Chem, 2014, 54: 24–35

    Article  CAS  Google Scholar 

  15. Jones PA. Nat Rev Genet, 2012, 13: 484–492

    Article  PubMed  CAS  Google Scholar 

  16. Robertson KD. Nat Rev Genet, 2005, 6: 597–610

    Article  PubMed  CAS  Google Scholar 

  17. Huang W, Qi CB, Lv SW, Xie M, Feng YQ, Huang WH, Yuan BF. Anal Chem, 2016, 88: 1378–1384

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  19. Kellinger MW, Song CX, Chong J, Lu XY, He C, Wang D. Nat Struct Mol Biol, 2012, 19: 831–833

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  Google Scholar 

  21. Tang Y, Zheng SJ, Qi CB, Feng YQ, Yuan BF. Anal Chem, 2015, 87: 3445–3452

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Janulaitis A, Klimašauskas S, Petrušyte M, Butkus V. FEBS Lett, 1983, 161: 131–134

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  25. Yu M, Ji L, Neumann DA, Chung DH, Groom J, Westpheling J, He C, Schmitz RJ. Nucleic Acids Res, 2015, 43: e148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Reisenauer A, Shapiro L. EMBO J, 2002, 21: 4969–4977

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Heyn H, Esteller M. Cell, 2015, 161: 710–713

    Article  PubMed  CAS  Google Scholar 

  28. Ratel D, Ravanat JL, Berger F, Wion D. Bioessays, 2006, 28: 309–315

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Koziol MJ, Bradshaw CR, Allen GE, Costa ASH, Frezza C, Gurdon JB. Nat Struct Mol Biol, 2016, 23: 24–30

    Article  PubMed  CAS  Google Scholar 

  35. Huang W, Xiong J, Yang Y, Liu SM, Yuan BF, Feng YQ. RSC Adv, 2015, 5: 64046–64054

    Article  CAS  Google Scholar 

  36. Schiffers S, Ebert C, Rahimoff R, Kosmatchev O, Steinbacher J, Bohne AV, Spada F, Michalakis S, Nickelsen J, Müller M, Carell T. Angew Chem Int Ed, 2017, 56: 11268–11271

    Article  CAS  Google Scholar 

  37. He C. Nat Chem Biol, 2010, 6: 863–865

    Article  PubMed  CAS  Google Scholar 

  38. Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, Yi C. Nat Chem Biol, 2016, 12: 311–316

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Huang W, Lan MD, Qi CB, Zheng SJ, Wei SZ, Yuan BF, Feng YQ. Chem Sci, 2016, 7: 5495–5502

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Li X, Xiong X, Yi C. Nat Meth, 2016, 14: 23–31

    Article  CAS  Google Scholar 

  46. Wang Y, Jia G. Genomics Proteomics Bioinf, 2016, 14: 172–175

    Article  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  Google Scholar 

  49. Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. Cell, 2012, 149: 1635–1646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR. Nat Meth, 2015, 12: 767–772

    Article  CAS  Google Scholar 

  51. Zhao BS, Roundtree IA, He C. Nat Rev Mol Cell Biol, 2016, 18: 31–42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Haussmann IU, Bodi Z, Sanchez-Moran E, Mongan NP, Archer N, Fray RG, Soller M. Nature, 2016, 540: 301–304

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Deng X, Su R, Feng X, Wei M, Chen J. Curr Opin Genet Dev, 2017, 48: 1–7

    Article  PubMed  CAS  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 Metab, 2015, 100: E148–E154

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  Google Scholar 

  66. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T. Nucleic Acids Res, 2012, 40: 5023–5033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Li B, Luo X, Dong Y. Bioconjugate Chem, 2016, 27: 849–853

    Article  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  Google Scholar 

  71. Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. Nature, 2014, 515: 143–146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C. Nat Chem Biol, 2015, 11: 592–597

    Article  PubMed  CAS  Google Scholar 

  73. Sun WJ, Li JH, Liu S, Wu J, Zhou H, Qu LH, Yang JH. Nucleic Acids Res, 2016, 44: D259–D265

    Article  PubMed  CAS  Google Scholar 

  74. Vaidyanathan PP, AlSadhan I, Merriman DK, Al-Hashimi HM, Herschlag D. RNA, 2017, 23: 611–618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. deLorimier E, Hinman MN, Copperman J, Datta K, Guenza M, Berglund JA. J Biol Chem, 2017, 292: 4350–4357

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Kumar S, Mapa K, Maiti S. Biochemistry, 2014, 53: 1607–1615

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  79. Sergiev PV, Golovina AY, Prokhorova IV, Sergeeva OV, Osterman IA, Nesterchuk MV, Burakovsky DE, Bogdanov AB, Dontsova OA. Ribosomes: Struct, Funct, Dyn, 2011: 97–110

    Book  Google Scholar 

  80. Sloan KE, Warda AS, Sharma S, Entian KD, Lafontaine DLJ, Bohnsack MT. RNA Biol, 2017, 14: 1138–1152

    Article  PubMed  Google Scholar 

  81. Decatur WA, Fournier MJ. Trends Biochem Sci, 2002, 27: 344–351

    Article  PubMed  CAS  Google Scholar 

  82. Jiang J, Seo H, Chow CS. Acc Chem Res, 2016, 49: 893–901

    Article  PubMed  CAS  Google Scholar 

  83. Helm M. Nucleic Acids Res, 2006, 34: 721–733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Ge J, Yu YT. Trends Biochem Sci, 2013, 38: 210–218

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Chow CS, Lamichhane TN, Mahto SK. ACS Chem Biol, 2007, 2: 610–619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV. Nat Rev Micro, 2015, 13: 42–51

    Article  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Brown JWS, Echeverria M, Qu LH. Trends Plant Sci, 2003, 8: 42–49

    Article  PubMed  CAS  Google Scholar 

  90. Lorenz C, Lünse CE, Mörl M. Biomolecules, 2017, 7: 35

    Article  PubMed Central  CAS  Google Scholar 

  91. Duechler M, Leszczyńska G, Sochacka E, Nawrot B. Cell Mol Life Sci, 2016, 73: 3075–3095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Wilusz JE. Wiley Interdiscip Rev RNA, 2015, 6: 453–470

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Björk GR, Hagervall TG. EcoSal Plus, 2014,: doi: 10.1128/ecosalplus. ESP-0007-2013

    Google Scholar 

  94. Manickam N, Joshi K, Bhatt MJ, Farabaugh PJ. Nucleic Acids Res, 2016, 44: 1871–1881

    Article  PubMed  Google Scholar 

  95. Hori H. Front Genet, 2014, 5: 144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Agris PF. EMBO Rep, 2008, 9: 629–635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Machnicka MA, Olchowik A, Grosjean H, Bujnicki JM. RNA Biol, 2014, 11: 1619–1629

    Article  PubMed  Google Scholar 

  98. Agris PF. Prog Nucleic Acid Res Mol Biol, 1996, 53: 79–129

    Article  PubMed  CAS  Google Scholar 

  99. Torres AG, Batlle E, Ribas de Pouplana L. Trends Mol Med, 2014, 20: 306–314

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  101. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, Lyko F. Genes Dev, 2010, 24: 1590–1595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Anderson P, Ivanov P. FEBS Lett, 2014, 588: 4297–4304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Lee YS, Shibata Y, Malhotra A, Dutta A. Genes Dev, 2009, 23: 2639–2649

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Klassen R, Paluszynski JP, Wemhoff S, Pfeiffer A, Fricke J, Meinhardt F. Mol Microbiol, 2008, 69: 681–697

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Preston MA, D’Silva S, Kon Y, Phizicky EM. RNA, 2013, 19: 243–256

    Article  PubMed  PubMed Central  Google Scholar 

  108. Han L, Kon Y, Phizicky EM. RNA, 2015, 21: 188–201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Chan CTY, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, Begley TJ. PLoS Genet, 2010, 6: e1001247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Tuorto F, Lyko F. Open Biol, 2016, 6: 160287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Suzuki T, Suzuki T. Nucleic Acids Res, 2014, 42: 7346–7357

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Miyauchi K, Kimura S, Suzuki T. Nat Chem Biol, 2013, 9: 105–111

    Article  PubMed  CAS  Google Scholar 

  113. Matuszewski M, Sochacka E. Bioorg Med Chem Lett, 2014, 24: 2703–2706

    Article  PubMed  CAS  Google Scholar 

  114. Zhang X, Cozen AE, Liu Y, Chen Q, Lowe TM. Trends Mol Med, 2016, 22: 1025–1034

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X. Science, 2005, 307: 932–935

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Ji L, Chen X. Cell Res, 2012, 22: 624–636

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  119. Breker M, Schuldiner M. Nat Rev Mol Cell Biol, 2014, 15: 453–464

    Article  PubMed  CAS  Google Scholar 

  120. Lawrence M, Daujat S, Schneider R. Trends Genets, 2016, 32: 42–56

    Article  CAS  Google Scholar 

  121. Kouzarides T. Cell, 2007, 128: 693–705

    Article  PubMed  CAS  Google Scholar 

  122. Bannister AJ, Kouzarides T. Cell Res, 2011, 21: 381–395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Rose NR, Klose RJ. Biochim Biophys Acta, 2014, 1839: 1362–1372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Silva AMN, Vitorino R, Domingues MRM, Spickett CM, Domingues P. Free Radical Biol Med, 2013, 65: 925–941

    Article  CAS  Google Scholar 

  125. Prabakaran S, Lippens G, Steen H, Gunawardena J. WIREs Syst Biol Med, 2012, 4: 565–583

    Article  CAS  Google Scholar 

  126. Salovska B, Tichy A, Rezacova M, Vavrova J, Novotna E. Rev Anal Chem, 2012, 31: 29–41

    Article  CAS  Google Scholar 

  127. Ubersax JA, Ferrell Jr JE. Nat Rev Mol Cell Biol, 2007, 8: 530–541

    Article  PubMed  CAS  Google Scholar 

  128. Sacco F, Perfetto L, Castagnoli L, Cesareni G. FEBS Lett, 2012, 586: 2732–2739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. Moremen KW, Tiemeyer M, Nairn AV. Nat Rev Mol Cell Biol, 2012, 13: 448–462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  130. Resh MD. Curr Biol, 2013, 23: R431–R435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Braakman I, Bulleid NJ. Annu Rev Biochem, 2011, 80: 71–99

    Article  PubMed  CAS  Google Scholar 

  132. Reimand J, Wagih O, Bader GD. PLoS Genet, 2015, 11: e1004919

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Cedar H, Bergman Y. Nat Rev Genet, 2009, 10: 295–304

    Article  PubMed  CAS  Google Scholar 

  134. Walport LJ, Hopkinson RJ, Schofield CJ. Curr Opin Chem Biol, 2012, 16: 525–534

    Article  PubMed  CAS  Google Scholar 

  135. Falnes PØ, Johansen RF, Seeberg E. Nature, 2002, 419: 178–182

    Article  PubMed  CAS  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

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Kawarada L, Suzuki T, Ohira T, Hirata S, Miyauchi K, Suzuki T. Nucleic Acids Res, 2017, 45: 7401–7415

    Article  PubMed  PubMed Central  CAS  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  140. van den Born E, Vagbo CB, Songe-Moller L, Leihne V, Lien GF, Leszczynska G, Malkiewicz A, Krokan HE, Kirpekar F, Klungland A, Falnes PO. Nat Commun, 2011, 2: 172

    Article  PubMed  CAS  Google Scholar 

  141. Jia G, Yang CG, Yang S, Jian X, Yi C, Zhou Z, He C. FEBS Lett, 2008, 582: 3313–3319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Landgraf BJ, McCarthy EL, Booker SJ. Annu Rev Biochem, 2016, 85: 485–514

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The work was supported by the National Key R&D Program of China (2017YFC0906800) and the National Natural Science Foundation of China (21522507, 21672166, 21635006, 21721005).

Author information

Authors and Affiliations

  1. Key Laboratory of Analytical Chemistry for Biology and Medicine (Ministry of Education), Department of Chemistry, Wuhan University, Wuhan, 430072, China

    Ting Liu, Cheng-Jie Ma, Bi-Feng Yuan & Yu-Qi Feng

Authors
  1. Ting Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Jie Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bi-Feng Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Qi Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bi-Feng Yuan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, T., Ma, CJ., Yuan, BF. et al. Modificaomics: deciphering the functions of biomolecule modifications. Sci. China Chem. 61, 381–392 (2018). https://doi.org/10.1007/s11426-017-9186-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11426-017-9186-y

Keywords

Search

Navigation