Ontogenic mRNA expression of RNA modification writers, erasers, and readers in mouse liver

Autoři: Liming Chen aff001;  Pei Wang aff002;  Raman Bahal aff001;  José E. Manautou aff001;  Xiao-bo Zhong aff001
Působiště autorů: Department of Pharmaceutic Sciences, School of Pharmacy, University of Connecticut, Storrs, Connecticut, United States of America aff001;  Department of Pharmacology, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, China aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227102


RNA modifications are recently emerged epigenetic modifications. These diverse RNA modifications have been shown to regulate multiple biological processes, including development. RNA modifications are dynamically controlled by the “writers, erasers, and readers”, where RNA modifying proteins are able to add, remove, and recognize specific chemical modification groups on RNAs. However, little is known about the ontogenic expression of these RNA modifying proteins in various organs, such as liver. In the present study, the hepatic mRNA expression of selected RNA modifying proteins involve in m6A, m1A, m5C, hm5C, m7G, and Ψ modifications was analyzed using the RNA-seq technique. Liver samples were collected from male C57BL/6 mice at several ages from prenatal through neonatal, infant, child to young adult. Results showed that most of the RNA modifying proteins were highly expressed in prenatal mouse liver with a dramatic drop at birth. After birth, most of the RNA modifying proteins showed a downregulation trend during liver maturation. Moreover, the RNA modifying proteins that belong to the same enzyme family were expressed at different abundances at the same ages in mouse liver. In conclusion, this study unveils that the mRNA expression of RNA modifying proteins follows specific ontogenic expression patterns in mice liver during maturation. These data indicated that the changes in expression of RNA modifying proteins might have a potential role to regulate gene expression in liver through alteration of RNA modification status.

Klíčová slova:

Epigenetics – Gene expression – Messenger RNA – Methyltransferases – Protein translation – Ribosomal RNA – RNA sequencing – Transfer RNA


1. Dupont C, Armant DR, Brenner CA. Epigenetics: definition, mechanisms and clinical perspective. Seminars in reproductive medicine. 2009;27(5):351–7. doi: 10.1055/s-0029-1237423 19711245.

2. Shakya K, O’Connell MJ, Ruskin HJ. The landscape for epigenetic/epigenomic biomedical resources. Epigenetics. 2012;7(9):982–6. doi: 10.4161/epi.21493 22874136.

3. Kim JK, Samaranayake M, Pradhan S. Epigenetic mechanisms in mammals. Cellular and molecular life sciences: CMLS. 2009;66(4):596–612. doi: 10.1007/s00018-008-8432-4 18985277.

4. Skvortsova K, Iovino N, Bogdanovic O. Functions and mechanisms of epigenetic inheritance in animals. Nature reviews Molecular cell biology. 2018;19(12):774–90. doi: 10.1038/s41580-018-0074-2 30425324.

5. Krishnakumar R, Blelloch RH. Epigenetics of cellular reprogramming. Current opinion in genetics & development. 2013;23(5):548–55. doi: 10.1016/j.gde.2013.06.005 23948105.

6. Soubry A. Epigenetics as a driver of developmental origins of health and disease: did we forget the fathers? Bioessays. 2018;40(1):1700113.

7. Cheng Z, Zheng L, Almeida FA. Epigenetic reprogramming in metabolic disorders: nutritional factors and beyond. The Journal of nutritional biochemistry. 2018;54:1–10. doi: 10.1016/j.jnutbio.2017.10.004 29154162.

8. Saletore Y, Chen-Kiang S, Mason CE. Novel RNA regulatory mechanisms revealed in the epitranscriptome. RNA biology. 2013;10(3):342–6. doi: 10.4161/rna.23812 23434792.

9. Roundtree IA, Evans ME, Pan T, He C. Dynamic RNA Modifications in Gene Expression Regulation. Cell. 2017;169(7):1187–200. doi: 10.1016/j.cell.2017.05.045 28622506.

10. Jaffrey SR. An expanding universe of mRNA modifications. Nature structural & molecular biology. 2014;21(11):945–6. doi: 10.1038/nsmb.2911 25372308.

11. Incarnato D, Oliviero S. The RNA Epistructurome: Uncovering RNA Function by Studying Structure and Post-Transcriptional Modifications. Trends in biotechnology. 2017;35(4):318–33. doi: 10.1016/j.tibtech.2016.11.002 27988057.

12. Jonkhout N, Tran J, Smith MA, Schonrock N, Mattick JS, Novoa EM. The RNA modification landscape in human disease. Rna. 2017;23(12):1754–69. doi: 10.1261/rna.063503.117 28855326.

13. Klungland A, Dahl JA. Dynamic RNA modifications in disease. Current opinion in genetics & development. 2014;26:47–52. doi: 10.1016/j.gde.2014.05.006 25005745.

14. Lambert MC, Johnson LE. Ontogenetic Development. In: Goldstein S, Naglieri JA, editors. Encyclopedia of Child Behavior and Development. Boston, MA: Springer US; 2011. p. 1037-.

15. Lee JS, Ward WO, Knapp G, Ren H, Vallanat B, Abbott B, et al. Transcriptional ontogeny of the developing liver. BMC genomics. 2012;13:33. doi: 10.1186/1471-2164-13-33 22260730.

16. Lu H, Gunewardena S, Cui JY, Yoo B, Zhong XB, Klaassen CD. RNA-sequencing quantification of hepatic ontogeny and tissue distribution of mRNAs of phase II enzymes in mice. Drug metabolism and disposition: the biological fate of chemicals. 2013;41(4):844–57. doi: 10.1124/dmd.112.050211 23382457.

17. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature genetics. 2003;33 Suppl:245–54. doi: 10.1038/ng1089 12610534.

18. Kiefer JC. Epigenetics in development. Developmental dynamics: an official publication of the American Association of Anatomists. 2007;236(4):1144–56. doi: 10.1002/dvdy.21094 17304537.

19. Lu H, Cui JY, Gunewardena S, Yoo B, Zhong XB, Klaassen CD. Hepatic ontogeny and tissue distribution of mRNAs of epigenetic modifiers in mice using RNA-sequencing. Epigenetics. 2012;7(8):914–29. doi: 10.4161/epi.21113 22772165.

20. Gunewardena SS, Yoo B, Peng L, Lu H, Zhong X, Klaassen CD, et al. Deciphering the Developmental Dynamics of the Mouse Liver Transcriptome. PLoS One. 2015;10(10):e0141220. doi: 10.1371/journal.pone.0141220 26496202.

21. Molinie B, Giallourakis CC. Genome-Wide Location Analyses of N6-Methyladenosine Modifications (m(6)A-Seq). Methods in molecular biology. 2017;1562:45–53. doi: 10.1007/978-1-4939-6807-7_4 28349453.

22. Dominissini D, Moshitch-Moshkovitz S, Salmon-Divon M, Amariglio N, Rechavi G. Transcriptome-wide mapping of N 6-methyladenosine by m 6 A-seq based on immunocapturing and massively parallel sequencing. Nature protocols. 2013;8(1):176. doi: 10.1038/nprot.2012.148 23288318

23. Zhao BS, Roundtree IA, He C. Post-transcriptional gene regulation by mRNA modifications. Nature reviews Molecular cell biology. 2017;18(1):31–42. doi: 10.1038/nrm.2016.132 27808276.

24. Fustin JM, Doi M, Yamaguchi Y, Hida H, Nishimura S, Yoshida M, et al. RNA-methylation-dependent RNA processing controls the speed of the circadian clock. Cell. 2013;155(4):793–806. doi: 10.1016/j.cell.2013.10.026 24209618.

25. Merkestein M, Laber S, McMurray F, Andrew D, Sachse G, Sanderson J, et al. FTO influences adipogenesis by regulating mitotic clonal expansion. Nature communications. 2015;6:6792. doi: 10.1038/ncomms7792 25881961.

26. Xiao W, Adhikari S, Dahal U, Chen YS, Hao YJ, Sun BF, et al. Nuclear m(6)A Reader YTHDC1 Regulates mRNA Splicing. Molecular cell. 2016;61(4):507–19. doi: 10.1016/j.molcel.2016.01.012 26876937.

27. Zhou J, Wan J, Gao X, Zhang X, Jaffrey SR, Qian SB. Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature. 2015;526(7574):591–4. doi: 10.1038/nature15377 26458103.

28. Wickramasinghe VO, Laskey RA. Control of mammalian gene expression by selective mRNA export. Nature reviews Molecular cell biology. 2015;16(7):431–42. doi: 10.1038/nrm4010 26081607.

29. Bokar JA, Shambaugh ME, Polayes D, Matera AG, Rottman FM. Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase. Rna. 1997;3(11):1233–47. 9409616.

30. Liu J, Yue Y, Han D, Wang X, Fu Y, Zhang L, et al. A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nature chemical biology. 2014;10(2):93–5. doi: 10.1038/nchembio.1432 24316715.

31. Agarwala SD, Blitzblau HG, Hochwagen A, Fink GR. RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLoS genetics. 2012;8(6):e1002732. doi: 10.1371/journal.pgen.1002732 22685417.

32. Schwartz S, Mumbach MR, Jovanovic M, Wang T, Maciag K, Bushkin GG, et al. Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell reports. 2014;8(1):284–96. doi: 10.1016/j.celrep.2014.05.048 24981863

33. Patil DP, Chen CK, Pickering BF, Chow A, Jackson C, Guttman M, et al. m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature. 2016;537(7620):369–73. doi: 10.1038/nature19342 27602518.

34. Wen J, Lv R, Ma H, Shen H, He C, Wang J, et al. Zc3h13 Regulates Nuclear RNA m(6)A Methylation and Mouse Embryonic Stem Cell Self-Renewal. Molecular cell. 2018;69(6):1028–38 e6. doi: 10.1016/j.molcel.2018.02.015 29547716.

35. Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang C-M, Li CJ, et al. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular cell. 2013;49(1):18–29. doi: 10.1016/j.molcel.2012.10.015 23177736

36. Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nature chemical biology. 2011;7(12):885–7. doi: 10.1038/nchembio.687 22002720.

37. Zhao X, Yang Y, Sun B-F, Shi Y, Yang X, Xiao W, et al. FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell research. 2014;24(12):1403. doi: 10.1038/cr.2014.151 25412662

38. Luo S, Tong L. Molecular basis for the recognition of methylated adenines in RNA by the eukaryotic YTH domain. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(38):13834–9. doi: 10.1073/pnas.1412742111 25201973.

39. Theler D, Dominguez C, Blatter M, Boudet J, Allain FH. Solution structure of the YTH domain in complex with N6-methyladenosine RNA: a reader of methylated RNA. Nucleic acids research. 2014;42(22):13911–9. doi: 10.1093/nar/gku1116 25389274.

40. Liu N, Dai Q, Zheng G, He C, Parisien M, Pan T. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature. 2015;518(7540):560–4. doi: 10.1038/nature14234 25719671.

41. Edupuganti RR, Geiger S, Lindeboom RGH, Shi H, Hsu PJ, Lu Z, et al. N(6)-methyladenosine (m(6)A) recruits and repels proteins to regulate mRNA homeostasis. Nature structural & molecular biology. 2017;24(10):870–8. doi: 10.1038/nsmb.3462 28869609.

42. Hsu PJ, Zhu Y, Ma H, Guo Y, Shi X, Liu Y, et al. Ythdc2 is an N(6)-methyladenosine binding protein that regulates mammalian spermatogenesis. Cell research. 2017;27(9):1115–27. doi: 10.1038/cr.2017.99 28809393.

43. Wojtas MN, Pandey RR, Mendel M, Homolka D, Sachidanandam R, Pillai RS. Regulation of m(6)A Transcripts by the 3'—>5' RNA Helicase YTHDC2 Is Essential for a Successful Meiotic Program in the Mammalian Germline. Molecular cell. 2017;68(2):374–87 e12. doi: 10.1016/j.molcel.2017.09.021 29033321.

44. Kretschmer J, Rao H, Hackert P, Sloan KE, Hobartner C, Bohnsack MT. The m(6)A reader protein YTHDC2 interacts with the small ribosomal subunit and the 5'-3' exoribonuclease XRN1. Rna. 2018;24(10):1339–50. doi: 10.1261/rna.064238.117 29970596.

45. Wu R, Li A, Sun B, Sun JG, Zhang J, Zhang T, et al. A novel m(6)A reader Prrc2a controls oligodendroglial specification and myelination. Cell research. 2019;29(1):23–41. doi: 10.1038/s41422-018-0113-8 30514900.

46. Dunn DB. The occurrence of 1-methyladenine in ribonucleic acid. Biochimica et biophysica acta. 1961;46:198–200. doi: 10.1016/0006-3002(61)90668-0 13725042.

47. Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, et al. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA. Nature. 2016;530(7591):441–6. doi: 10.1038/nature16998 26863196.

48. Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, et al. Transcriptome-wide mapping reveals reversible and dynamic N 1-methyladenosine methylome. Nature chemical biology. 2016;12(5):311. doi: 10.1038/nchembio.2040 26863410

49. Voigts-Hoffmann F, Hengesbach M, Kobitski AY, van Aerschot A, Herdewijn P, Nienhaus GU, et al. A methyl group controls conformational equilibrium in human mitochondrial tRNA(Lys). Journal of the American Chemical Society. 2007;129(44):13382–3. doi: 10.1021/ja075520+ 17941640.

50. Basavappa R, Sigler PB. The 3 A crystal structure of yeast initiator tRNA: functional implications in initiator/elongator discrimination. The EMBO journal. 1991;10(10):3105–11. 1915284.

51. Anderson JT, Droogmans L. Biosynthesis and function of 1-methyladenosine in transfer RNA. Fine-Tuning of RNA Functions by Modification and Editing: Springer; 2005. p. 121–39.

52. Oerum S, Degut C, Barraud P, Tisne C. m1A Post-Transcriptional Modification in tRNAs. Biomolecules. 2017;7(1). doi: 10.3390/biom7010020 28230814.

53. Sergiev PV, Aleksashin NA, Chugunova AA, Polikanov YS, Dontsova OA. Structural and evolutionary insights into ribosomal RNA methylation. Nature chemical biology. 2018;14(3):226. doi: 10.1038/nchembio.2569 29443970

54. Sharma S, Hartmann JD, Watzinger P, Klepper A, Peifer C, Kotter P, et al. A single N(1)-methyladenosine on the large ribosomal subunit rRNA impacts locally its structure and the translation of key metabolic enzymes. Scientific reports. 2018;8(1):11904. doi: 10.1038/s41598-018-30383-z 30093689.

55. Ozanick S, KRECIC A, Andersland J, Anderson JT. The bipartite structure of the tRNA m1A58 methyltransferase from S. cerevisiae is conserved in humans. Rna. 2005;11(8):1281–90. doi: 10.1261/rna.5040605 16043508

56. Waku T, Nakajima Y, Yokoyama W, Nomura N, Kako K, Kobayashi A, et al. NML-mediated rRNA base methylation links ribosomal subunit formation to cell proliferation in a p53-dependent manner. Journal of cell science. 2016;129(12):2382–93. doi: 10.1242/jcs.183723 27149924.

57. Liu F, Clark W, Luo G, Wang X, Fu Y, Wei J, et al. ALKBH1-Mediated tRNA Demethylation Regulates Translation. Cell. 2016;167(7):1897. doi: 10.1016/j.cell.2016.11.045 27984735.

58. Dai X, Wang T, Gonzalez G, Wang Y. Identification of YTH Domain-containing proteins as the readers for N 1-Methyladenosine in RNA. Analytical chemistry. 2018;90(11):6380–4. doi: 10.1021/acs.analchem.8b01703 29791134

59. Wyatt G. Occurrence of 5-methyl-cytosine in nucleic acids. Nature. 1950;166(4214):237.

60. Amos H, Korn M. 5-Methyl cytosine in the RNA of Escherichia coli. Biochimica et biophysica acta. 1958;29(2):444–5. doi: 10.1016/0006-3002(58)90214-2 13572373

61. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, et al. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic acids research. 2012;40(11):5023–33. doi: 10.1093/nar/gks144 22344696.

62. Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLoS genetics. 2013;9(6):e1003602. doi: 10.1371/journal.pgen.1003602 23825970

63. Haag S, Sloan KE, Ranjan N, Warda AS, Kretschmer J, Blessing C, et al. NSUN3 and ABH1 modify the wobble position of mt-tRNAMet to expand codon recognition in mitochondrial translation. The EMBO journal. 2016;35(19):2104–19. doi: 10.15252/embj.201694885 27497299.

64. Nakano S, Suzuki T, Kawarada L, Iwata H, Asano K, Suzuki T. NSUN3 methylase initiates 5-formylcytidine biogenesis in human mitochondrial tRNA(Met). Nature chemical biology. 2016;12(7):546–51. doi: 10.1038/nchembio.2099 27214402.

65. Yang X, Yang Y, Sun B-F, Chen Y-S, Xu J-W, Lai W-Y, et al. 5-methylcytosine promotes mRNA export—NSUN2 as the methyltransferase and ALYREF as an m 5 C reader. Cell research. 2017;27(5):606. doi: 10.1038/cr.2017.55 28418038

66. Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S, Kellner S, et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nature structural & molecular biology. 2012;19(9):900–5. doi: 10.1038/nsmb.2357 22885326.

67. Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic acids research. 2010;38(5):1415–30. doi: 10.1093/nar/gkp1117 20007150.

68. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, Frye M. The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS genetics. 2011;7(12):e1002403. doi: 10.1371/journal.pgen.1002403 22144916.

69. Flores JV, Cordero-Espinoza L, Oeztuerk-Winder F, Andersson-Rolf A, Selmi T, Blanco S, et al. Cytosine-5 RNA Methylation Regulates Neural Stem Cell Differentiation and Motility. Stem cell reports. 2017;8(1):112–24. doi: 10.1016/j.stemcr.2016.11.014 28041877.

70. Van Haute L, Lee SY, McCann BJ, Powell CA, Bansal D, Vasiliauskaite L, et al. NSUN2 introduces 5-methylcytosines in mammalian mitochondrial tRNAs. Nucleic acids research. 2019;47(16):8720–33. doi: 10.1093/nar/gkz559 31276587.

71. Cheng JX, Chen L, Li Y, Cloe A, Yue M, Wei J, et al. RNA cytosine methylation and methyltransferases mediate chromatin organization and 5-azacytidine response and resistance in leukaemia. Nature communications. 2018;9(1):1163. doi: 10.1038/s41467-018-03513-4 29563491.

72. Bourgeois G, Ney M, Gaspar I, Aigueperse C, Schaefer M, Kellner S, et al. Eukaryotic rRNA Modification by Yeast 5-Methylcytosine-Methyltransferases and Human Proliferation-Associated Antigen p120. PLoS One. 2015;10(7):e0133321. doi: 10.1371/journal.pone.0133321 26196125.

73. Metodiev MD, Spahr H, Loguercio Polosa P, Meharg C, Becker C, Altmueller J, et al. NSUN4 is a dual function mitochondrial protein required for both methylation of 12S rRNA and coordination of mitoribosomal assembly. PLoS genetics. 2014;10(2):e1004110. doi: 10.1371/journal.pgen.1004110 24516400.

74. Schosserer M, Minois N, Angerer TB, Amring M, Dellago H, Harreither E, et al. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nature communications. 2015;6:6158. doi: 10.1038/ncomms7158 25635753.

75. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science. 2006;311(5759):395–8. doi: 10.1126/science.1120976 16424344.

76. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, et al. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes & development. 2010;24(15):1590–5. doi: 10.1101/gad.586710 20679393.

77. Ito S, D’Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466(7310):1129–33. doi: 10.1038/nature09303 20639862.

78. Chen X, Li A, Sun BF, Yang Y, Han YN, Yuan X, et al. 5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs. Nature cell biology. 2019;21(8):978–90. doi: 10.1038/s41556-019-0361-y 31358969.

79. Fu L, Guerrero CR, Zhong N, Amato NJ, Liu Y, Liu S, et al. Tet-mediated formation of 5-hydroxymethylcytosine in RNA. Journal of the American Chemical Society. 2014;136(33):11582–5. doi: 10.1021/ja505305z 25073028.

80. Lewis CJ, Pan T, Kalsotra A. RNA modifications and structures cooperate to guide RNA-protein interactions. Nature reviews Molecular cell biology. 2017;18(3):202–10. doi: 10.1038/nrm.2016.163 28144031.

81. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, Bauer C, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell. 2013;152(5):1146–59. doi: 10.1016/j.cell.2013.02.004 23434322.

82. Zhou T, Xiong J, Wang M, Yang N, Wong J, Zhu B, et al. Structural basis for hydroxymethylcytosine recognition by the SRA domain of UHRF2. Molecular cell. 2014;54(5):879–86. doi: 10.1016/j.molcel.2014.04.003 24813944.

83. Shatkin AJ. Capping of eucaryotic mRNAs. Cell. 1976;9(4 PT 2):645–53. doi: 10.1016/0092-8674(76)90128-8 1017010.

84. Lin S, Liu Q, Lelyveld VS, Choe J, Szostak JW, Gregory RI. Mettl1/Wdr4-Mediated m(7)G tRNA Methylome Is Required for Normal mRNA Translation and Embryonic Stem Cell Self-Renewal and Differentiation. Molecular cell. 2018;71(2):244–55 e5. doi: 10.1016/j.molcel.2018.06.001 29983320.

85. Zhang LS, Liu C, Ma H, Dai Q, Sun HL, Luo G, et al. Transcriptome-wide Mapping of Internal N(7)-Methylguanosine Methylome in Mammalian mRNA. Molecular cell. 2019;74(6):1304–16 e8. doi: 10.1016/j.molcel.2019.03.036 31031084.

86. Malbec L, Zhang T, Chen YS, Zhang Y, Sun BF, Shi BY, et al. Dynamic methylome of internal mRNA N(7)-methylguanosine and its regulatory role in translation. Cell research. 2019. doi: 10.1038/s41422-019-0230-z 31520064.

87. Oliva R, Cavallo L, Tramontano A. Accurate energies of hydrogen bonded nucleic acid base pairs and triplets in tRNA tertiary interactions. Nucleic acids research. 2006;34(3):865–79. doi: 10.1093/nar/gkj491 16461956.

88. Alexandrov A, Grayhack EJ, Phizicky EM. tRNA m7G methyltransferase Trm8p/Trm82p: evidence linking activity to a growth phenotype and implicating Trm82p in maintaining levels of active Trm8p. Rna. 2005;11(5):821–30. doi: 10.1261/rna.2030705 15811913.

89. Shaheen R, Abdel-Salam GM, Guy MP, Alomar R, Abdel-Hamid MS, Afifi HH, et al. Mutation in WDR4 impairs tRNA m(7)G46 methylation and causes a distinct form of microcephalic primordial dwarfism. Genome biology. 2015;16:210. doi: 10.1186/s13059-015-0779-x 26416026.

90. Figaro S, Wacheul L, Schillewaert S, Graille M, Huvelle E, Mongeard R, et al. Trm112 is required for Bud23-mediated methylation of the 18S rRNA at position G1575. Molecular and cellular biology. 2012;32(12):2254–67. doi: 10.1128/MCB.06623-11 22493060.

91. Haag S, Kretschmer J, Bohnsack MT. WBSCR22/Merm1 is required for late nuclear pre-ribosomal RNA processing and mediates N7-methylation of G1639 in human 18S rRNA. Rna. 2015;21(2):180–7. doi: 10.1261/rna.047910.114 25525153.

92. Mandal SS, Chu C, Wada T, Handa H, Shatkin AJ, Reinberg D. Functional interactions of RNA-capping enzyme with factors that positively and negatively regulate promoter escape by RNA polymerase II. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(20):7572–7. doi: 10.1073/pnas.0401493101 15136722.

93. Furuichi Y, LaFiandra A, Shatkin AJ. 5'-Terminal structure and mRNA stability. Nature. 1977;266(5599):235–9. doi: 10.1038/266235a0 557727.

94. Muthukrishnan S, Both GW, Furuichi Y, Shatkin AJ. 5'-Terminal 7-methylguanosine in eukaryotic mRNA is required for translation. Nature. 1975;255(5503):33–7. doi: 10.1038/255033a0 165427.

95. Gonatopoulos-Pournatzis T, Cowling VH. Cap-binding complex (CBC). The Biochemical journal. 2014;457(2):231–42. doi: 10.1042/BJ20131214 24354960.

96. Spenkuch F, Motorin Y, Helm M. Pseudouridine: still mysterious, but never a fake (uridine)! RNA biology. 2014;11(12):1540–54. doi: 10.4161/15476286.2014.992278 25616362.

97. Boccaletto P, Machnicka MA, Purta E, Piatkowski P, Baginski B, Wirecki TK, et al. MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic acids research. 2018;46(D1):D303–D7. doi: 10.1093/nar/gkx1030 29106616.

98. Xuan JJ, Sun WJ, Lin PH, Zhou KR, Liu S, Zheng LL, et al. RMBase v2.0: deciphering the map of RNA modifications from epitranscriptome sequencing data. Nucleic acids research. 2018;46(D1):D327–D34. doi: 10.1093/nar/gkx934 29040692.

99. Li X, Zhu P, Ma S, Song J, Bai J, Sun F, et al. Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nature chemical biology. 2015;11(8):592–7. doi: 10.1038/nchembio.1836 26075521.

100. Davis DR. Stabilization of RNA stacking by pseudouridine. Nucleic acids research. 1995;23(24):5020–6. doi: 10.1093/nar/23.24.5020 8559660.

101. Liang XH, Liu Q, Fournier MJ. Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. Rna. 2009;15(9):1716–28. doi: 10.1261/rna.1724409 19628622.

102. Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, Leon-Ricardo BX, et al. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell. 2014;159(1):148–62. doi: 10.1016/j.cell.2014.08.028 25219674.

103. Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature. 2014;515(7525):143–6. doi: 10.1038/nature13802 25192136.

104. Geula S, Moshitch-Moshkovitz S, Dominissini D, Mansour AA, Kol N, Salmon-Divon M, et al. Stem cells. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science. 2015;347(6225):1002–6. 25569111.

105. Frye M, Harada BT, Behm M, He C. RNA modifications modulate gene expression during development. Science. 2018;361(6409):1346–9. doi: 10.1126/science.aau1646 30262497.

106. Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C, Humphreys P, et al. Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. The EMBO journal. 2014;33(18):2020–39. doi: 10.15252/embj.201489282 25063673.

107. Tuorto F, Herbst F, Alerasool N, Bender S, Popp O, Federico G, et al. The tRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis. The EMBO journal. 2015;34(18):2350–62. doi: 10.15252/embj.201591382 26271101

108. Sadler NC, Nandhikonda P, Webb-Robertson BJ, Ansong C, Anderson LN, Smith JN, et al. Hepatic Cytochrome P450 Activity, Abundance, and Expression Throughout Human Development. Drug metabolism and disposition: the biological fate of chemicals. 2016;44(7):984–91. doi: 10.1124/dmd.115.068593 27084891.

109. Ohtsuki S, Schaefer O, Kawakami H, Inoue T, Liehner S, Saito A, et al. Simultaneous absolute protein quantification of transporters, cytochromes P450, and UDP-glucuronosyltransferases as a novel approach for the characterization of individual human liver: comparison with mRNA levels and activities. Drug metabolism and disposition: the biological fate of chemicals. 2012;40(1):83–92. doi: 10.1124/dmd.111.042259 21994437.

110. Rodriguez-Antona C, Donato MT, Pareja E, Gomez-Lechon MJ, Castell JV. Cytochrome P-450 mRNA expression in human liver and its relationship with enzyme activity. Archives of biochemistry and biophysics. 2001;393(2):308–15. doi: 10.1006/abbi.2001.2499 11556818.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden