1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biomedical Engineering
  4. Volume 25, 2023
  5. Article

Annual Review of Biomedical Engineering

Volume 25, 2023

Epitranscriptional Regulation: From the Perspectives of Cardiovascular Bioengineering

Abstract

The central dogma of gene expression involves DNA transcription to RNA and RNA translation into protein. As key intermediaries and modifiers, RNAs undergo various forms of modifications such as methylation, pseudouridylation, deamination, and hydroxylation. These modifications, termed epitranscriptional regulations, lead to functional changes in RNAs. Recent studies have demonstrated crucial roles for RNA modifications in gene translation, DNA damage response, and cell fate regulation. Epitranscriptional modifications play an essential role in development, mechanosensing, atherogenesis, and regeneration in the cardiovascular (CV) system, and their elucidation is critically important to understanding the molecular mechanisms underlying CV physiology and pathophysiology. This review aims at providing biomedical engineers with an overview of the epitranscriptome landscape, related key concepts, recent findings in epitranscriptional regulations, and tools for epitranscriptome analysis. The potential applications of this important field in biomedical engineering research are discussed.

Keyword(s): cardiovascular, epitranscriptome, gene regulation, RNA
Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-081922-021233
2023-06-08
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/25/1/annurev-bioeng-081922-021233.html?itemId=/content/journals/10.1146/annurev-bioeng-081922-021233&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Boccaletto P, Stefaniak F, Ray A, Cappannini A, Mukherjee S et al. 2022. MODOMICS: a database of RNA modification pathways. 2021 update. Nucleic Acids Res. 50:D231–35
     [Google Scholar]
  2. 2.
    Roundtree IA, Evans ME, Pan T, He C. 2017. Dynamic RNA modifications in gene expression regulation. Cell 169:1187–200
     [Google Scholar]
  3. 3.
    Wiener D, Schwartz S. 2021. The epitranscriptome beyond m6A. Nat. Rev. Genet. 22:119–31
     [Google Scholar]
  4. 4.
    Barbieri I, Kouzarides T. 2020. Role of RNA modifications in cancer. Nat. Rev. Cancer 20:303–22
     [Google Scholar]
  5. 5.
    Haruehanroengra P, Zheng YY, Zhou Y, Huang Y, Sheng J. 2020. RNA modifications and cancer. RNA Biol. 17:1560–75
     [Google Scholar]
  6. 6.
    Wei CM, Gershowitz A, Moss B. 1976. 5′-Terminal and internal methylated nucleotide sequences in HeLa cell mRNA. Biochemistry 15:397–401
     [Google Scholar]
  7. 7.
    Wei CM, Moss B. 1977. Nucleotide sequences at the N6-methyladenosine sites of HeLa cell messenger ribonucleic acid. Biochemistry 16:1672–6
     [Google Scholar]
  8. 8.
    Srinivasan PR, Borek E. 1966. Enzymatic alteration of macromolecular structure. Prog. Nucleic Acid Res. Mol. Biol. 5:157–89
     [Google Scholar]
  9. 9.
    Starr JL, Sells BH. 1969. Methylated ribonucleic acids. Physiol. Rev. 49:623–69
     [Google Scholar]
  10. 10.
    Desrosiers R, Friderici K, Rottman F. 1974. Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells. PNAS 71:3971–75
     [Google Scholar]
  11. 11.
    Perry RP, Kelley DK. 1974. Existence of methylated messenger RNA in mouse L cells. Cell 1:37–42
     [Google Scholar]
  12. 12.
    Sommer S, Lavi U, Darnell JE Jr. 1978. The absolute frequency of labeled N-6-methyladenosine in HeLa cell messenger RNA decreases with label time. J. Mol. Biol. 124:487–99
     [Google Scholar]
  13. 13.
    Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L et al. 2012. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201–6
     [Google Scholar]
  14. 14.
    Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. 2012. Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149:1635–46
     [Google Scholar]
  15. 15.
    Lavi U, Fernandez-Munoz R, Darnell JE Jr. 1977. Content of N-6 methyl adenylic acid in heterogeneous nuclear and messenger RNA of HeLa cells. Nucleic Acids Res. 4:63–69
     [Google Scholar]
  16. 16.
    Perry RP, Kelley DE, Friderici K, Rottman F. 1975. The methylated constituents of L cell messenger RNA: evidence for an unusual cluster at the 5′ terminus. Cell 4:387–94
     [Google Scholar]
  17. 17.
    Wei CM, Gershowitz A, Moss B. 1975. Methylated nucleotides block 5′ terminus of HeLa cell messenger RNA. Cell 4:379–86
     [Google Scholar]
  18. 18.
    Covelo-Molares H, Bartosovic M, Vanacova S. 2018. RNA methylation in nuclear pre-mRNA processing. Wiley Interdiscip. Rev. RNA 9:e1489
     [Google Scholar]
  19. 19.
    Wang X, Lu Z, Gomez A, Hon GC, Yue Y et al. 2014. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505:117–20
     [Google Scholar]
  20. 20.
    Wang X, Zhao BS, Roundtree IA, Lu Z, Han D et al. 2015. N6-methyladenosine modulates messenger RNA translation efficiency. Cell 161:1388–99
     [Google Scholar]
  21. 21.
    Alarcon CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF. 2015. N6-methyladenosine marks primary microRNAs for processing. Nature 519:482–85
     [Google Scholar]
  22. 22.
    Lee JH, Wang R, Xiong F, Krakowiak J, Liao Z et al. 2021. Enhancer RNA m6A methylation facilitates transcriptional condensate formation and gene activation. Mol. Cell 81:3368–85.e9
     [Google Scholar]
  23. 23.
    Clancy MJ, Shambaugh ME, Timpte CS, Bokar JA. 2002. Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6-methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucleic Acids Res. 30:4509–18
     [Google Scholar]
  24. 24.
    Zhong S, Li H, Bodi Z, Button J, Vespa L et al. 2008. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell 20:1278–88
     [Google Scholar]
  25. 25.
    Geula S, Moshitch-Moshkovitz S, Dominissini D, Mansour AA, Kol N et al. 2015. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science 347:1002–6
     [Google Scholar]
  26. 26.
    Ping XL, Sun BF, Wang L, Xiao W, Yang X et al. 2014. Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 24:177–89
     [Google Scholar]
  27. 27.
    Xiao W, Adhikari S, Dahal U, Chen YS, Hao YJ et al. 2016. Nuclear m6A reader YTHDC1 regulates mRNA splicing. Mol. Cell 61:507–19
     [Google Scholar]
  28. 28.
    Zaccara S, Ries RJ, Jaffrey SR. 2019. Reading, writing and erasing mRNA methylation. Nat. Rev. Mol. Cell Biol. 20:608–24
     [Google Scholar]
  29. 29.
    Darnell RB, Ke S, Darnell JE Jr. 2018. Pre-mRNA processing includes N6 methylation of adenosine residues that are retained in mRNA exons and the fallacy of “RNA epigenetics.”. RNA 24:262–67
     [Google Scholar]
  30. 30.
    Jia G, Fu Y, Zhao X, Dai Q, Zheng G et al. 2011. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 7:12885–87
     [Google Scholar]
  31. 31.
    Dina C, Meyre D, Gallina S, Durand E, Korner A et al. 2007. Variation in FTO contributes to childhood obesity and severe adult obesity. Nat. Genet. 39:724–26
     [Google Scholar]
  32. 32.
    Fischer J, Koch L, Emmerling C, Vierkotten J, Peters T et al. 2009. Inactivation of the Fto gene protects from obesity. Nature 458:894–98
     [Google Scholar]
  33. 33.
    Mauer J, Luo X, Blanjoie A, Jiao X, Grozhik AV et al. 2017. Reversible methylation of m6Am in the 5′ cap controls mRNA stability. Nature 541:371–75
     [Google Scholar]
  34. 34.
    Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM et al. 2013. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell 49:18–29
     [Google Scholar]
  35. 35.
    Mathiyalagan P, Adamiak M, Mayourian J, Sassi Y, Liang Y et al. 2019. FTO-dependent N6-methyladenosine regulates cardiac function during remodeling and repair. Circulation 139:518–32
     [Google Scholar]
  36. 36.
    Berulava T, Buchholz E, Elerdashvili V, Pena T, Islam MR et al. 2020. Changes in m6A RNA methylation contribute to heart failure progression by modulating translation. Eur. J. Heart Fail. 22:54–66
     [Google Scholar]
  37. 37.
    Dorn LE, Lasman L, Chen J, Xu X, Hund TJ et al. 2019. The N6-methyladenosine mRNA methylase METTL3 controls cardiac homeostasis and hypertrophy. Circulation 139:533–45
     [Google Scholar]
  38. 38.
    Horiuchi K, Umetani M, Minami T, Okayama H, Takada S et al. 2006. Wilms' tumor 1-associating protein regulates G2/M transition through stabilization of cyclin A2 mRNA. PNAS 103:17278–83
     [Google Scholar]
  39. 39.
    Zhang C, Chen Y, Sun B, Wang L, Yang Y et al. 2017. m6A modulates haematopoietic stem and progenitor cell specification. Nature 549:273–76
     [Google Scholar]
  40. 40.
    Kruger N, Biwer LA, Good ME, Ruddiman CA, Wolpe AG et al. 2020. Loss of endothelial FTO antagonizes obesity-induced metabolic and vascular dysfunction. Circ. Res. 126:232–42
     [Google Scholar]
  41. 41.
    Chien CS, Li JY, Chien Y, Wang ML, Yarmishyn AA et al. 2021. METTL3-dependent N6-methyladenosine RNA modification mediates the atherogenic inflammatory cascades in vascular endothelium. PNAS 118:e2025070118
     [Google Scholar]
  42. 42.
    Dong G, Yu J, Shan G, Su L, Yu N, Yang S 2021. N6-Methyladenosine methyltransferase METTL3 promotes angiogenesis and atherosclerosis by upregulating the JAK2/STAT3 pathway via m6A reader IGF2BP1. Front. Cell Dev. Biol. 9:731810
     [Google Scholar]
  43. 43.
    Li B, Zhang T, Liu M, Cui Z, Zhang Y et al. 2022. RNA N6-methyladenosine modulates endothelial atherogenic responses to disturbed flow in mice. eLife 11:e69906
     [Google Scholar]
  44. 44.
    Jian D, Wang Y, Jian L, Tang H, Rao L et al. 2020. METTL14 aggravates endothelial inflammation and atherosclerosis by increasing FOXO1 N6-methyladeosine modifications. Theranostics 10:8939–56
     [Google Scholar]
  45. 45.
    Chien CS, Li JYS, Chiou SH, Chien S. 2022. Comment on: RNA N6-methyladenosine modulates endothelial atherogenic responses to disturbed flow in mice. eLife 11:e69906
     [Google Scholar]
  46. 46.
    Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR. 2015. Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat. Methods 12:767–72
     [Google Scholar]
  47. 47.
    Garcia-Campos MA, Edelheit S, Toth U, Safra M, Shachar R et al. 2019. Deciphering the “m6A Code” via antibody-independent quantitative profiling. Cell 178:3731–47
     [Google Scholar]
  48. 48.
    Zhang Z, Chen LQ, Zhao YL, Yang CG, Roundtree IA et al. 2019. Single-base mapping of m6A by an antibody-independent method. Sci. Adv. 5:eaax0250
     [Google Scholar]
  49. 49.
    Meyer KD. 2019. DART-seq: an antibody-free method for global m6A detection. Nat. Methods 16:1275–80
     [Google Scholar]
  50. 50.
    Liu H, Begik O, Lucas MC, Ramirez JM, Mason CE et al. 2019. Accurate detection of m6A RNA modifications in native RNA sequences. Nat. Commun. 10:4079
     [Google Scholar]
  51. 51.
    Dunin-Horkawicz S, Czerwoniec A, Gajda MJ, Feder M, Grosjean H, Bujnicki JM. 2006. MODOMICS: a database of RNA modification pathways. Nucleic Acids Res. 34:D145–49
     [Google Scholar]
  52. 52.
    Amort T, Rieder D, Wille A, Khokhlova-Cubberley D, Riml C et al. 2017. Distinct 5-methylcytosine profiles in poly(A) RNA from mouse embryonic stem cells and brain. Genome Biol. 18:1
     [Google Scholar]
  53. 53.
    Huang T, Chen W, Liu J, Gu N, Zhang R. 2019. Genome-wide identification of mRNA 5-methylcytosine in mammals. Nat. Struct. Mol. Biol. 26:380–88
     [Google Scholar]
  54. 54.
    Liu Y, Zhao Y, Wu R, Chen Y, Chen W et al. 2021. mRNA m5C controls adipogenesis by promoting CDKN1A mRNA export and translation. RNA Biol. 18:711–21
     [Google Scholar]
  55. 55.
    Yang X, Yang Y, Sun BF, Chen YS, Xu JW et al. 2017. 5-methylcytosine promotes mRNA export—NSUN2 as the methyltransferase and ALYREF as an m5C reader. Cell Res. 27:606–25
     [Google Scholar]
  56. 56.
    Zhang X, Liu Z, Yi J, Tang H, Xing J et al. 2012. The tRNA methyltransferase NSun2 stabilizes p16INK4 mRNA by methylating the 3′-untranslated region of p16. Nat. Commun. 3:712
     [Google Scholar]
  57. 57.
    Bohnsack KE, Hobartner C, Bohnsack MT. 2019. Eukaryotic 5-methylcytosine (m5C) RNA methyltransferases: mechanisms, cellular functions, and links to disease. Genes 10:102
     [Google Scholar]
  58. 58.
    Liu RJ, Long T, Li J, Li H, Wang ED. 2017. Structural basis for substrate binding and catalytic mechanism of a human RNA:m5C methyltransferase NSun6. Nucleic Acids Res. 45:6684–97
     [Google Scholar]
  59. 59.
    Gigova A, Duggimpudi S, Pollex T, Schaefer M, Kos M. 2014. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability. RNA 20:1632–44
     [Google Scholar]
  60. 60.
    Schosserer M, Minois N, Angerer TB, Amring M, Dellago H et al. 2015. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nat. Commun. 6:6158
     [Google Scholar]
  61. 61.
    Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S et al. 2012. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat. Struct. Mol. Biol. 19:900–5
     [Google Scholar]
  62. 62.
    Haag S, Sloan KE, Ranjan N, Warda AS, Kretschmer J et al. 2016. NSUN3 and ABH1 modify the wobble position of mt-tRNAMet to expand codon recognition in mitochondrial translation. EMBO J. 35:2104–19
     [Google Scholar]
  63. 63.
    Van Haute L, Dietmann S, Kremer L, Hussain S, Pearce SF et al. 2016. Deficient methylation and formylation of mt-tRNAMet wobble cytosine in a patient carrying mutations in NSUN3. Nat. Commun. 7:12039
     [Google Scholar]
  64. 64.
    Scott DD, Aguilar LC, Kramar M, Oeffinger M. 2019. It's not the destination, it's the journey: heterogeneity in mRNA export mechanisms. Adv. Exp. Med. Biol. 1203:33–81
     [Google Scholar]
  65. 65.
    Chen L, Wang P, Bahal R, Manautou JE, Zhong XB. 2019. Ontogenic mRNA expression of RNA modification writers, erasers, and readers in mouse liver. PLOS ONE 14:e0227102
     [Google Scholar]
  66. 66.
    Wang L, Zhang J, Su Y, Maimaitiyiming Y, Yang S et al. 2022. Distinct roles of m5C RNA methyltransferase NSUN2 in major gynecologic cancers. Front. Oncol. 12:786266
     [Google Scholar]
  67. 67.
    Dai X, Gonzalez G, Li L, Li J, You C et al. 2020. YTHDF2 binds to 5-methylcytosine in RNA and modulates the maturation of ribosomal RNA. Anal. Chem. 92:1346–54
     [Google Scholar]
  68. 68.
    Shen H, Ontiveros RJ, Owens MC, Liu MY, Ghanty U et al. 2021. TET-mediated 5-methylcytosine oxidation in tRNA promotes translation. J. Biol. Chem. 296:100087
     [Google Scholar]
  69. 69.
    Shen Q, Zhang Q, Shi Y, Shi Q, Jiang Y et al. 2018. Tet2 promotes pathogen infection-induced myelopoiesis through mRNA oxidation. Nature 554:123–27
     [Google Scholar]
  70. 70.
    Kawarada L, Suzuki T, Ohira T, Hirata S, Miyauchi K, Suzuki T. 2017. ALKBH1 is an RNA dioxygenase responsible for cytoplasmic and mitochondrial tRNA modifications. Nucleic Acids Res. 45:7401–15
     [Google Scholar]
  71. 71.
    Zhang Q, Liu F, Chen W, Miao H, Liang H et al. 2021. The role of RNA m5C modification in cancer metastasis. Int. J. Biol. Sci. 17:3369–80
     [Google Scholar]
  72. 72.
    He Y, Zhang H, Yin F, Guo P, Wang S et al. 2021. Novel insights into the role of 5-methylcytosine RNA methylation in human abdominal aortic aneurysm. Front. Biosci. 26:1147–65
     [Google Scholar]
  73. 73.
    Luo Y, Feng J, Xu Q, Wang W, Wang X 2016. NSun2 deficiency protects endothelium from inflammation via mRNA methylation of ICAM-1. Circ. Res. 118:944–56
     [Google Scholar]
  74. 74.
    Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. 2013. Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLOS Genet. 9:e1003602
     [Google Scholar]
  75. 75.
    Huber SM, van Delft P, Mendil L, Bachman M, Smollett K et al. 2015. Formation and abundance of 5-hydroxymethylcytosine in RNA. ChemBioChem 16:752–55
     [Google Scholar]
  76. 76.
    De Borre M, Branco MR. 2021. Oxidative bisulfite sequencing: an experimental and computational protocol. Methods Mol. Biol. 2198:333–48
     [Google Scholar]
  77. 77.
    Yuan F, Bi Y, Siejka-Zielinska P, Zhou YL, Zhang XX, Song CX. 2019. Bisulfite-free and base-resolution analysis of 5-methylcytidine and 5-hydroxymethylcytidine in RNA with peroxotungstate. Chem. Commun. 55:2328–31
     [Google Scholar]
  78. 78.
    Khoddami V, Cairns BR. 2013. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat. Biotechnol. 31:458–64
     [Google Scholar]
  79. 79.
    Khoddami V, Cairns BR. 2014. Transcriptome-wide target profiling of RNA cytosine methyltransferases using the mechanism-based enrichment procedure Aza-IP. Nat. Protoc. 9:337–61
     [Google Scholar]
  80. 80.
    Cohn WE. 1960. Pseudouridine, a carbon-carbon linked ribonucleoside in ribonucleic acids: isolation, structure, and chemical characteristics. J. Biol. Chem. 235:1488–98
     [Google Scholar]
  81. 81.
    Davis FF, Allen FW. 1957. Ribonucleic acids from yeast which contain a fifth nucleotide. J. Biol. Chem. 227:907–15
     [Google Scholar]
  82. 82.
    Cohn WE, Volkin E. 1951. Nucleoside-5′-phosphates from ribonucleic acid. Nature 167:483–84
     [Google Scholar]
  83. 83.
    Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. 2014. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515:143–46
     [Google Scholar]
  84. 84.
    Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH et al. 2014. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 159:148–62
     [Google Scholar]
  85. 85.
    Cerneckis J, Cui Q, He C, Yi C, Shi Y 2022. Decoding pseudouridine: an emerging target for therapeutic development. Trends Pharmacol. Sci. 43:522–35
     [Google Scholar]
  86. 86.
    Borchardt EK, Martinez NM, Gilbert WV. 2020. Regulation and function of RNA pseudouridylation in human cells. Annu. Rev. Genet. 54:309–36
     [Google Scholar]
  87. 87.
    Hoernes TP, Clementi N, Faserl K, Glasner H, Breuker K et al. 2016. Nucleotide modifications within bacterial messenger RNAs regulate their translation and are able to rewire the genetic code. Nucleic Acids Res. 44:852–62
     [Google Scholar]
  88. 88.
    Kariko K, Muramatsu H, Welsh FA, Ludwig J, Kato H et al. 2008. Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability. Mol. Ther. 16:1833–40
     [Google Scholar]
  89. 89.
    Karijolich J, Yu YT. 2011. Converting nonsense codons into sense codons by targeted pseudouridylation. Nature 474:395–98
     [Google Scholar]
  90. 90.
    Parisien M, Yi C, Pan T 2012. Rationalization and prediction of selective decoding of pseudouridine-modified nonsense and sense codons. RNA 18:355–67
     [Google Scholar]
  91. 91.
    Davis DR. 1995. Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 23:5020–26
     [Google Scholar]
  92. 92.
    Liang XH, Liu Q, Fournier MJ. 2007. rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol. Cell 28:965–77
     [Google Scholar]
  93. 93.
    Liang XH, Liu Q, Fournier MJ. 2009. Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. RNA 15:1716–28
     [Google Scholar]
  94. 94.
    Donmez G, Hartmuth K, Luhrmann R. 2004. Modified nucleotides at the 5′ end of human U2 snRNA are required for spliceosomal E-complex formation. RNA 10:1925–33
     [Google Scholar]
  95. 95.
    Hamma T, Ferre-D'Amare AR. 2006. Pseudouridine synthases. Chem. Biol. 13:1125–35
     [Google Scholar]
  96. 96.
    Garus A, Autexier C. 2021. Dyskerin: an essential pseudouridine synthase with multifaceted roles in ribosome biogenesis, splicing, and telomere maintenance. RNA 27:1441–58
     [Google Scholar]
  97. 97.
    Angrisani A, Vicidomini R, Turano M, Furia M. 2014. Human dyskerin: beyond telomeres. Biol. Chem. 395:593–610
     [Google Scholar]
  98. 98.
    Fernandez-Vizarra E, Berardinelli A, Valente L, Tiranti V, Zeviani M. 2007. Nonsense mutation in pseudouridylate synthase 1 (PUS1) in two brothers affected by myopathy, lactic acidosis and sideroblastic anaemia (MLASA). J. Med. Genet. 44:173–80
     [Google Scholar]
  99. 99.
    Kasapkara CS, Tumer L, Zanetti N, Ezgu F, Lamantea E, Zeviani M. 2017. A myopathy, lactic acidosis, sideroblastic anemia (MLASA) case due to a novel PUS1 mutation. Turk. J. Haematol. 34:376–77
     [Google Scholar]
  100. 100.
    Oncul U, Unal-Ince E, Kuloglu Z, Teber-Tiras S, Kaygusuz G, Eminoglu FT. 2021. A novel PUS1 mutation in 2 siblings with MLASA syndrome: a review of the literature. J. Pediatr. Hematol. Oncol. 43:e592–95
     [Google Scholar]
  101. 101.
    Woods J, Cederbaum S. 2019. Myopathy, lactic acidosis and sideroblastic anemia 1 (MLASA1): a 25-year follow-up. Mol. Genet. Metab. Rep. 21:100517
     [Google Scholar]
  102. 102.
    Zeharia A, Fischel-Ghodsian N, Casas K, Bykhocskaya Y, Tamari H et al. 2005. Mitochondrial myopathy, sideroblastic anemia, and lactic acidosis: an autosomal recessive syndrome in Persian Jews caused by a mutation in the PUS1 gene. J. Child Neurol. 20:449–52
     [Google Scholar]
  103. 103.
    Shaheen R, Han L, Faqeih E, Ewida N, Alobeid E et al. 2016. A homozygous truncating mutation in PUS3 expands the role of tRNA modification in normal cognition. Hum. Genet. 135:707–13
     [Google Scholar]
  104. 104.
    Shaheen R, Tasak M, Maddirevula S, Abdel-Salam GMH, Sayed ISM et al. 2019. PUS7 mutations impair pseudouridylation in humans and cause intellectual disability and microcephaly. Hum. Genet. 138:231–39
     [Google Scholar]
  105. 105.
    Stockert JA, Weil R, Yadav KK, Kyprianou N, Tewari AK. 2021. Pseudouridine as a novel biomarker in prostate cancer. Urol. Oncol. 39:63–71
     [Google Scholar]
  106. 106.
    Motyl T, Traczyk Z, Ciesluk S, Daniewska-Michalska D, Kukulska W et al. 1993. Blood plasma pseudouridine in patients with malignant proliferative diseases. Eur. J. Clin. Chem. Clin. Biochem. 31:765–71
     [Google Scholar]
  107. 107.
    Hocher B, Adamski J. 2017. Metabolomics for clinical use and research in chronic kidney disease. Nat. Rev. Nephrol. 13:269–84
     [Google Scholar]
  108. 108.
    Dunn WB, Broadhurst DI, Deepak SM, Buch MH, McDowell G et al. 2007. Serum metabolomics reveals many novel metabolic markers of heart failure, including pseudouridine and 2-oxoglutarate. Metabolomics 3:413–26
     [Google Scholar]
  109. 109.
    Razavi AC, Bazzano LA, He J, Li S, Fernandez C et al. 2020. Pseudouridine and N-formylmethionine associate with left ventricular mass index: metabolome-wide association analysis of cardiac remodeling. J. Mol. Cell. Cardiol. 140:22–29
     [Google Scholar]
  110. 110.
    Bakin AV, Ofengand J. 1998. Mapping of pseudouridine residues in RNA to nucleotide resolution. Methods Mol. Biol. 77:297–309
     [Google Scholar]
  111. 111.
    Lovejoy AF, Riordan DP, Brown PO. 2014. Transcriptome-wide mapping of pseudouridines: pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLOS ONE 9:e110799
     [Google Scholar]
  112. 112.
    Li X, Zhu P, Ma S, Song J, Bai J et al. 2015. Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nat. Chem. Biol. 11:592–97
     [Google Scholar]
  113. 113.
    Khoddami V, Yerra A, Mosbruger TL, Fleming AM, Burrows CJ, Cairns BR. 2019. Transcriptome-wide profiling of multiple RNA modifications simultaneously at single-base resolution. PNAS 116:146784–89
     [Google Scholar]
  114. 114.
    Song B, Tang Y, Wei Z, Liu G, Su J et al. 2020. PIANO: a web server for pseudouridine-site (Ψ) identification and functional annotation. Front. Genet. 11:88
     [Google Scholar]
  115. 115.
    Wagner RW, Smith JE, Cooperman BS, Nishikura K. 1989. A double-stranded RNA unwinding activity introduces structural alterations by means of adenosine to inosine conversions in mammalian cells and Xenopus eggs. PNAS 86:2647–51
     [Google Scholar]
  116. 116.
    Bazak L, Haviv A, Barak M, Jacob-Hirsch J, Deng P et al. 2014. A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res. 24:365–76
     [Google Scholar]
  117. 117.
    Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M et al. 2004. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol. 22:1001–5
     [Google Scholar]
  118. 118.
    Schaub M, Keller W. 2002. RNA editing by adenosine deaminases generates RNA and protein diversity. Biochimie 84:791–803
     [Google Scholar]
  119. 119.
    Sommer B, Köhler M, Sprengel R, Seeburg PH. 1991. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:111–19
     [Google Scholar]
  120. 120.
    Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H et al. 1997. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303–8
     [Google Scholar]
  121. 121.
    Lomeli H, Mosbacher J, Melcher T, Hoger T, Geiger JR et al. 1994. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266:1709–13
     [Google Scholar]
  122. 122.
    Stellos K, Gatsiou A, Stamatelopoulos K, Perisic Matic L, John D et al. 2016. Adenosine-to-inosine RNA editing controls cathepsin S expression in atherosclerosis by enabling HuR-mediated post-transcriptional regulation. Nat. Med. 22:1140–50
     [Google Scholar]
  123. 123.
    Palladino MJ, Keegan LP, O'Connell MA, Reenan RA. 2000. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102:437–49
     [Google Scholar]
  124. 124.
    Quin J, Sedmik J, Vukic D, Khan A, Keegan LP, O'Connell MA. 2021. ADAR RNA modifications, the epitranscriptome and innate immunity. Trends Biochem. Sci. 46:758–71
     [Google Scholar]
  125. 125.
    Savva YA, Rieder LE, Reenan RA. 2012. The ADAR protein family. Genome Biol. 13:252
     [Google Scholar]
  126. 126.
    Kim U, Wang Y, Sanford T, Zeng Y, Nishikura K. 1994. Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. PNAS 91:11457–61
     [Google Scholar]
  127. 127.
    Wang Q, Miyakoda M, Yang W, Khillan J, Stachura DL et al. 2004. Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J. Biol. Chem. 279:4952–61
     [Google Scholar]
  128. 128.
    Mannion NM, Greenwood SM, Young R, Cox S, Brindle J et al. 2014. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep. 9:1482–94
     [Google Scholar]
  129. 129.
    Melcher T, Maas S, Herb A, Sprengel R, Seeburg PH, Higuchi M. 1996. A mammalian RNA editing enzyme. Nature 379:460–64
     [Google Scholar]
  130. 130.
    Higuchi M, Maas S, Single FN, Hartner J, Rozov A et al. 2000. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406:78–81
     [Google Scholar]
  131. 131.
    Chen CX, Cho DS, Wang Q, Lai F, Carter KC, Nishikura K. 2000. A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. RNA 6:755–67
     [Google Scholar]
  132. 132.
    Melcher T, Maas S, Herb A, Sprengel R, Higuchi M, Seeburg PH. 1996. RED2, a brain-specific member of the RNA-specific adenosine deaminase family. J. Biol. Chem. 271:31795–98
     [Google Scholar]
  133. 133.
    Wang Y, Chung DH, Monteleone LR, Li J, Chiang Y et al. 2019. RNA binding candidates for human ADAR3 from substrates of a gain of function mutant expressed in neuronal cells. Nucleic Acids Res. 47:10801–14
     [Google Scholar]
  134. 134.
    Patterson JB, Samuel CE. 1995. Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase. Mol. Cell. Biol. 15:5376–88
     [Google Scholar]
  135. 135.
    Vlachogiannis NI, Sachse M, Georgiopoulos G, Zormpas E, Bampatsias D et al. 2021. Adenosine-to-inosine Alu RNA editing controls the stability of the pro-inflammatory long noncoding RNA NEAT1 in atherosclerotic cardiovascular disease. J. Mol. Cell. Cardiol. 160:111–20
     [Google Scholar]
  136. 136.
    Fei J, Cui XB, Wang JN, Dong K, Chen SY 2016. ADAR1-mediated RNA editing, a novel mechanism controlling phenotypic modulation of vascular smooth muscle cells. Circ. Res. 119:463–69
     [Google Scholar]
  137. 137.
    Eggington JM, Greene T, Bass BL. 2011. Predicting sites of ADAR editing in double-stranded RNA. Nat. Commun. 2:319
     [Google Scholar]
  138. 138.
    Li JB, Levanon EY, Yoon JK, Aach J, Xie B et al. 2009. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324:1210–13
     [Google Scholar]
  139. 139.
    Maki H, Sekiguchi M. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355:273–75
     [Google Scholar]
  140. 140.
    Taddei F, Hayakawa H, Bouton M, Cirinesi A, Matic I et al. 1997. Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science 278:128–30
     [Google Scholar]
  141. 141.
    Tanaka M, Chock PB, Stadtman ER. 2007. Oxidized messenger RNA induces translation errors. PNAS 104:66–71
     [Google Scholar]
  142. 142.
    Kong Q, Lin CL. 2010. Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell. Mol. Life Sci. 67:1817–29
     [Google Scholar]
  143. 143.
    Poulsen HE, Specht E, Broedbaek K, Henriksen T, Ellervik C et al. 2012. RNA modifications by oxidation: a novel disease mechanism? Free Radic. . Biol. Med. 52:1353–61
     [Google Scholar]
  144. 144.
    Wang JX, Gao J, Ding SL, Wang K, Jiao JQ et al. 2015. Oxidative modification of miR-184 enables it to target Bcl-xL and Bcl-w. Mol. Cell 59:50–61
     [Google Scholar]
  145. 145.
    Seok H, Lee H, Lee S, Ahn SH, Lee HS et al. 2020. Position-specific oxidation of miR-1 encodes cardiac hypertrophy. Nature 584:279–85
     [Google Scholar]
  146. 146.
    Thapa B, Hebert SP, Munk BH, Burrows CJ, Schlegel HB. 2019. Computational study of the formation of C8, C5, and C4 guanine:lysine adducts via oxidation of guanine by sulfate radical anion. J. Phys. Chem. A 123:5150–63
     [Google Scholar]
  147. 147.
    Shyu AB, Wilkinson MF, van Hoof A. 2008. Messenger RNA regulation: to translate or to degrade. EMBO J. 27:471–81
     [Google Scholar]
  148. 148.
    Wu J, Li Z. 2008. Human polynucleotide phosphorylase reduces oxidative RNA damage and protects HeLa cell against oxidative stress. Biochem. Biophys. Res. Commun. 372:288–92
     [Google Scholar]
  149. 149.
    Hayakawa H, Uchiumi T, Fukuda T, Ashizuka M, Kohno K et al. 2002. Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry 41:12739–44
     [Google Scholar]
  150. 150.
    Martinet W, de Meyer GR, Herman AG, Kockx MM. 2004. Reactive oxygen species induce RNA damage in human atherosclerosis. Eur. J. Clin. Investig. 34:323–27
     [Google Scholar]
  151. 151.
    Shan X, Tashiro H, Lin CL. 2003. The identification and characterization of oxidized RNAs in Alzheimer's disease. J. Neurosci. 23:4913–21
     [Google Scholar]
  152. 152.
    Ding Q, Markesbery WR, Cecarini V, Keller JN. 2006. Decreased RNA, and increased RNA oxidation, in ribosomes from early Alzheimer's disease. Neurochem. Res. 31:705–10
     [Google Scholar]
  153. 153.
    Abe T, Isobe C, Murata T, Sato C, Tohgi H. 2003. Alteration of 8-hydroxyguanosine concentrations in the cerebrospinal fluid and serum from patients with Parkinson's disease. Neurosci. Lett. 336:105–8
     [Google Scholar]
  154. 154.
    Abe T, Tohgi H, Isobe C, Murata T, Sato C. 2002. Remarkable increase in the concentration of 8-hydroxyguanosine in cerebrospinal fluid from patients with Alzheimer's disease. J. Neurosci. Res. 70:447–50
     [Google Scholar]
  155. 155.
    Hofer T, Seo AY, Prudencio M, Leeuwenburgh C. 2006. A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol. Chem. 387:103–11
     [Google Scholar]
  156. 156.
    Chen Q, Hu Y, Fang Z, Ye M, Li J et al. 2020. Elevated levels of oxidative nucleic acid modification markers in urine from gastric cancer patients: quantitative analysis by ultra performance liquid chromatography-tandem mass spectrometry. Front. Chem. 8:606495
     [Google Scholar]
  157. 157.
    Gonzalez-Rivera JC, Sherman MW, Wang DS, Chuvalo-Abraham JCL, Hildebrandt Ruiz L, Contreras LM 2020. RNA oxidation in chromatin modification and DNA-damage response following exposure to formaldehyde. Sci. Rep. 10:16545
     [Google Scholar]
  158. 158.
    Zhao Y, Kong L, Pei Z, Li F, Li C et al. 2021. m7G methyltransferase METTL1 promotes post-ischemic angiogenesis via promoting VEGFA mRNA translation. Front. Cell Dev. Biol. 9:642080
     [Google Scholar]
  159. 159.
    Wu Y, Jiang D, Zhang H, Yin F, Guo P et al. 2022. N1-methyladenosine (m1A) regulation associated with the pathogenesis of abdominal aortic aneurysm through YTHDF3 modulating macrophage polarization. Front. Cardiovasc. Med. 9:883155
     [Google Scholar]
  160. 160.
    Wu Y, Zhan S, Xu Y, Gao X. 2021. RNA modifications in cardiovascular diseases, the potential therapeutic targets. Life Sci. 278:119565
     [Google Scholar]
  161. 161.
    Huang H, Weng H, Zhou K, Wu T, Zhao BS et al. 2019. Histone H3 trimethylation at lysine 36 guides m6A RNA modification co-transcriptionally. Nature 567:414–19
     [Google Scholar]
  162. 162.
    Fazi F, Fatica A. 2019. Interplay between N6-methyladenosine (m6A) and non-coding RNAs in cell development and cancer. Front. Cell Dev. Biol. 7:116
     [Google Scholar]
  163. 163.
    Duenas-Gonzalez A, Medina-Franco JL, Chavez-Blanco A, Dominguez-Gomez G, Fernandez-de Gortari E. 2016. Developmental DNA methyltransferase inhibitors in the treatment of gynecologic cancers. Expert Opin. Pharmacother. 17:323–38
     [Google Scholar]
  164. 164.
    Hu C, Liu X, Zeng Y, Liu J, Wu F. 2021. DNA methyltransferase inhibitors combination therapy for the treatment of solid tumor: mechanism and clinical application. Clin. Epigenetics 13:166
     [Google Scholar]
  165. 165.
    Yankova E, Blackaby W, Albertella M, Rak J, De Braekeleer E et al. 2021. Small-molecule inhibition of METTL3 as a strategy against myeloid leukaemia. Nature 593:597–601
     [Google Scholar]
  166. 166.
    Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW et al. 2019. Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149–57
     [Google Scholar]
  167. 167.
    Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ et al. 2017. RNA editing with CRISPR-Cas13. Science 358:1019–27
     [Google Scholar]
  168. 168.
    Marina RJ, Brannan KW, Dong KD, Yee BA, Yeo GW. 2020. Evaluation of engineered CRISPR-Cas-mediated systems for site-specific RNA editing. Cell Rep. 33:108350
     [Google Scholar]
  169. 169.
    Liu XM, Zhou J, Mao Y, Ji Q, Qian SB 2019. Programmable RNA N6-methyladenosine editing by CRISPR-Cas9 conjugates. Nat. Chem. Biol. 15:865–71
     [Google Scholar]
  170. 170.
    Rau K, Rosner L, Rentmeister A. 2019. Sequence-specific m6A demethylation in RNA by FTO fused to RCas9. RNA 25:1311–23
     [Google Scholar]
  171. 171.
    Wilson C, Chen PJ, Miao Z, Liu DR. 2020. Programmable m6A modification of cellular RNAs with a Cas13-directed methyltransferase. Nat. Biotechnol. 38:1431–40
     [Google Scholar]
  172. 172.
    Xia Z, Tang M, Ma J, Zhang H, Gimple RC et al. 2021. Epitranscriptomic editing of the RNA N6-methyladenosine modification by dCasRx conjugated methyltransferase and demethylase. Nucleic Acids Res. 49:7361–74
     [Google Scholar]
  173. 173.
    Li Z, Xu Q, Huangfu N, Chen X, Zhu J 2022. Mettl3 promotes oxLDL-mediated inflammation through activating STAT1 signaling. J. Clin. Lab. Anal. 36:e24019
     [Google Scholar]
  174. 174.
    Liu Y, Luo G, Tang Q, Song Y, Liu D et al. 2022. Methyltransferase-like 14 silencing relieves the development of atherosclerosis via m6A modification of p65 mRNA. Bioengineered 13:11832–43
     [Google Scholar]
  175. 175.
    Chamorro-Jorganes A, Sweaad WK, Katare R, Besnier M, Anwar M et al. 2021. METTL3 regulates angiogenesis by modulating let-7e-5p and miRNA-18a-5p expression in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 41:e325–37
     [Google Scholar]
  176. 176.
    Yao MD, Jiang Q, Ma Y, Liu C, Zhu CY et al. 2020. Role of METTL3-dependent N6-methyladenosine mRNA modification in the promotion of angiogenesis. Mol. Ther. 28:2191–202
     [Google Scholar]
  177. 177.
    Qin Y, Qiao Y, Li L, Luo E, Wang D et al. 2021. The m6A methyltransferase METTL3 promotes hypoxic pulmonary arterial hypertension. Life Sci. 274:119366
     [Google Scholar]
  178. 178.
    Chen J, Lai K, Yong X, Yin H, Chen Z et al. 2022. Silencing METTL3 stabilizes atherosclerotic plaques by regulating the phenotypic transformation of vascular smooth muscle cells via the miR-375-3p/PDK1 axis. Cardiovasc Drugs Ther. https://doi.org/10.1007/s10557-022-07348-6
    [Google Scholar]
  179. 179.
    Guo X, Lin Y, Lin Y, Zhong Y, Yu H et al. 2022. PM2.5 induces pulmonary microvascular injury in COPD via METTL16-mediated m6A modification. Environ. Pollut. 303:119115
     [Google Scholar]
  180. 180.
    Han Y, Du T, Guo S, Wang L, Dai G et al. 2022. Loss of m6A methyltransferase METTL5 promotes cardiac hypertrophy through epitranscriptomic control of SUZ12 expression. Front. Cardiovasc. Med. 9:852775
     [Google Scholar]
  181. 181.
    Fan T, Du Y, Zhang M, Zhu AR, Zhang J. 2022. Senolytics cocktail dasatinib and quercetin alleviate human umbilical vein endothelial cell senescence via the TRAF6-MAPK-NF-κB axis in a YTHDF2-dependent manner. Gerontology 68:920–34
     [Google Scholar]
  182. 182.
    He Y, Xing J, Wang S, Xin S, Han Y, Zhang J. 2019. Increased m6A methylation level is associated with the progression of human abdominal aortic aneurysm. Ann. Transl. Med. 7:797
     [Google Scholar]
  183. 183.
    Liang D, Lin WJ, Ren M, Qiu J, Yang C et al. 2022. m6A reader YTHDC1 modulates autophagy by targeting SQSTM1 in diabetic skin. Autophagy 18:1318–37
     [Google Scholar]
  184. 184.
    Tanabe A, Tanikawa K, Tsunetomi M, Takai K, Ikeda H et al. 2016. RNA helicase YTHDC2 promotes cancer metastasis via the enhancement of the efficiency by which HIF-1α mRNA is translated. Cancer Lett. 376:34–42
     [Google Scholar]
  185. 185.
    Sjogren M, Lyssenko V, Jonsson A, Berglund G, Nilsson P et al. 2008. The search for putative unifying genetic factors for components of the metabolic syndrome. Diabetologia 51:2242–51
     [Google Scholar]
  186. 186.
    Kumari R, Dutta R, Ranjan P, Suleiman ZG, Goswami SK et al. 2021. ALKBH5 regulates SPHK1-dependent endothelial cell angiogenesis following ischemic stress. Front. Cardiovasc. Med. 8:817304
     [Google Scholar]
  187. 187.
    Zhao Y, Hu J, Sun X, Yang K, Yang L et al. 2021. Loss of m6A demethylase ALKBH5 promotes post-ischemic angiogenesis via post-transcriptional stabilization of WNT5A. Clin. Transl. Med. 11:e402
     [Google Scholar]
  188. 188.
    Li J, Chen J, Zhao M, Li Z, Liu N et al. 2022. Downregulated ALKBH5 contributes to myocardial ischemia/reperfusion injury by increasing m6A modification of Trio mRNA. Ann. Transl. Med. 10:417
     [Google Scholar]
  189. 189.
    Liu C, Mou S, Pan C. 2013. The FTO gene rs9939609 polymorphism predicts risk of cardiovascular disease: a systematic review and meta-analysis. PLOS ONE 8:e71901
     [Google Scholar]
  190. 190.
    Miao Y, Zhao Y, Han L, Ma X, Deng J et al. 2021. NSun2 regulates aneurysm formation by promoting autotaxin expression and T cell recruitment. Cell. Mol. Life Sci. 78:1709–27
     [Google Scholar]
  191. 191.
    Chi L, Delgado-Olguin P. 2013. Expression of NOL1/NOP2/sun domain (Nsun) RNA methyltransferase family genes in early mouse embryogenesis. Gene Expr. Patterns 13:319–27
     [Google Scholar]
  192. 192.
    Wang Y, Jiang T, Xu J, Gu Y, Zhou Y et al. 2021. Mutations in RNA methyltransferase gene NSUN5 confer high risk of outflow tract malformation. Front. Cell Dev. Biol. 9:623394
     [Google Scholar]
  193. 193.
    Ghanbarian H, Wagner N, Polo B, Baudouy D, Kiani J et al. 2016. Dnmt2/Trdmt1 as mediator of RNA polymerase II transcriptional activity in cardiac growth. PLOS ONE 11:e0156953
     [Google Scholar]
  194. 194.
    Garcia-Martin R, Wang G, Brandao BB, Zanotto TM, Shah S et al. 2022. MicroRNA sequence codes for small extracellular vesicle release and cellular retention. Nature 601:446–51
     [Google Scholar]
  195. 195.
    Peng J, Yang Q, Li AF, Li RQ, Wang Z et al. 2016. Tet methylcytosine dioxygenase 2 inhibits atherosclerosis via upregulation of autophagy in ApoE−/− mice. Oncotarget 7:76423–36
     [Google Scholar]
  196. 196.
    Pan X, Chen S, Chen X, Ren Q, Yue L et al. 2022. UTP14A, DKC1, DDX10, PinX1, and ESF1 modulate cardiac angiogenesis leading to obesity-induced cardiac injury. J. Diabetes Res. 2022:2923291
     [Google Scholar]
  197. 197.
    Liu S, Zhu A, He C, Chen M. 2020. REPIC: a database for exploring the N6-methyladenosine methylome. Genome Biol. 21:100
     [Google Scholar]
  198. 198.
    Chen K, Song B, Tang Y, Wei Z, Xu Q et al. 2021. RMDisease: a database of genetic variants that affect RNA modifications, with implications for epitranscriptome pathogenesis. Nucleic Acids Res. 49:D1396–404
     [Google Scholar]
  199. 199.
    Ma J, Song B, Wei Z, Huang D, Zhang Y et al. 2022. m5C-Atlas: a comprehensive database for decoding and annotating the 5-methylcytosine (m5C) epitranscriptome. Nucleic Acids Res. 50:D196–203
     [Google Scholar]
  200. 200.
    Tang Y, Chen K, Song B, Ma J, Wu X et al. 2021. m6A-Atlas: a comprehensive knowledgebase for unraveling the N6-methyladenosine (m6A) epitranscriptome. Nucleic Acids Res. 49:D134–43
     [Google Scholar]
  201. 201.
    Xuan JJ, Sun WJ, Lin PH, Zhou KR, Liu S et al. 2018. RMBase v2.0: deciphering the map of RNA modifications from epitranscriptome sequencing data. Nucleic Acids Res. 46:D327–34
     [Google Scholar]
/content/journals/10.1146/annurev-bioeng-081922-021233
Loading
Epitranscriptional Regulation: From the Perspectives of Cardiovascular Bioengineering
Annual Review of Biomedical Engineering 25, 157 (2023); https://doi.org/10.1146/annurev-bioeng-081922-021233
/content/journals/10.1146/annurev-bioeng-081922-021233
/content/journals/10.1146/annurev-bioeng-081922-021233
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error