DOI QR코드

DOI QR Code

Detecting DNA hydroxymethylation: exploring its role in genome regulation

  • Sun-Min Lee (Department of Physics, Konkuk Univeristy)
  • 투고 : 2023.12.15
  • 심사 : 2024.02.01
  • 발행 : 2024.03.31

초록

DNA methylation is one of the most extensively studied epigenetic regulatory mechanisms, known to play crucial roles in various organisms. It has been implicated in the regulation of gene expression and chromatin changes, ranging from global alterations during cell state transitions to locus-specific modifications. 5-hydroxymethylcytosine (5hmC) is produced by a major oxidation, from 5-methylcytosine (5mC), catalyzed by the ten-eleven translocation (TET) enzymes, and is gradually being recognized for its significant role in genome regulation. With the development of state-of-the-art experimental techniques, it has become possible to detect and distinguish 5mC and 5hmC at base resolution. Various techniques have evolved, encompassing chemical and enzymatic approaches, as well as third-generation sequencing techniques. These advancements have paved the way for a thorough exploration of the role of 5hmC across a diverse array of cell types, from embryonic stem cells (ESCs) to various differentiated cells. This review aims to comprehensively report on recent techniques and discuss the emerging roles of 5hmC.

키워드

과제정보

Sun-Min Lee is supported by the Brain Pool programme funded by the Ministry of Science and ICT through the National Research Foundation of Korea (2022H1D3A2A02063272).

참고문헌

  1. Hotchkiss RD (1948) The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J Biol Chem 175, 315-332  https://doi.org/10.1016/S0021-9258(18)57261-6
  2. Yokochi T and Robertson KD (2002) Preferential methylation of unmethylated DNA by Mammalian de novo DNA methyltransferase Dnmt3a. J Biol Chem 277, 11735-11745  https://doi.org/10.1074/jbc.M106590200
  3. Guo F, Li X, Liang D et al (2014) Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell 15, 447-459  https://doi.org/10.1016/j.stem.2014.08.003
  4. Tahiliani M, Koh KP, Shen Y et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935  https://doi.org/10.1126/science.1170116
  5. He YF, Li BZ, Li Z et al (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307  https://doi.org/10.1126/science.1210944
  6. Nabel CS, Jia H, Ye Y et al (2012) AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol 8, 751-758  https://doi.org/10.1038/nchembio.1042
  7. Frommer M, McDonald LE, Millar DS et al (1992) A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci U S A 89, 1827-1831  https://doi.org/10.1073/pnas.89.5.1827
  8. Pastor WA, Aravind L and Rao A (2013) TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat Rev Mol Cell Biol 14, 341-356  https://doi.org/10.1038/nrm3589
  9. Hu LL, Lu JY, Cheng JD et al (2015) Structural insight into substrate preference for TET- mediated oxidation. Nature 527, 118-122  https://doi.org/10.1038/nature15713
  10. Hu LL, Li Z, Cheng JD et al (2013) Crystal structure of TET2-DNA complex: insight into TET-mediated 5mC oxidation. Cell 155, 1545-1555  https://doi.org/10.1016/j.cell.2013.11.020
  11. Dunican DS, Pennings S and Meehan RR (2013) The CXXC-TET bridge - mind the methylation gap! Cell Res 23, 973-974  https://doi.org/10.1038/cr.2013.71
  12. Yu M, Hon GC, Szulwach KE et al (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149, 1368-1380  https://doi.org/10.1016/j.cell.2012.04.027
  13. Szulwach KE, Li XK, Li YJ et al (2011) Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet 7, e1002154 
  14. Ficz G, Branco MR, Seisenberger S et al (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402  https://doi.org/10.1038/nature10008
  15. Schutsky EK, DeNizio JE, Hu P et al (2018) Nondestructive, base-resolution sequencing of 5-hydroxymethylcytosine using a DNA deaminase. Nat Biotechnol 36, 1083-1090  https://doi.org/10.1038/nbt.4204
  16. Fabyanic EB, Hu P, Qiu Q et al (2023) Joint single-cell profiling resolves 5mC and 5hmC and reveals their distinct gene regulatory effects. Nat Biotechnol 41, 1-15  https://doi.org/10.1038/s41587-022-01655-x
  17. Hahn MA, Qiu R, Wu X et al (2013) Dynamics of 5-hydroxymethylcytosine and chromatin marks in mammalian neurogenesis. Cell Rep 3, 291-300  https://doi.org/10.1016/j.celrep.2013.01.011
  18. Li J, Wu X, Zhou Y et al (2018) Decoding the dynamic DNA methylation and hydroxymethylation landscapes in endodermal lineage intermediates during pancreatic differentiation of hESC. Nucleic Acids Res 46, 2883-2900  https://doi.org/10.1093/nar/gky063
  19. Tsagaratou A, Aijo T, Lio CW et al (2014) Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc Natl Acad Sci U S A 111, E3306-E3315  https://doi.org/10.1073/pnas.1412327111
  20. Cui XL, Nie J, Ku J et al (2020) A human tissue map of 5-hydroxymethylcytosines exhibits tissue specificity through gene and enhancer modulation. Nat Commun 11, 6161 
  21. Tang WW, Dietmann S, Irie N et al (2015) A unique gene regulatory network resets the human germline epigenome for development. Cell 161, 1453-1467  https://doi.org/10.1016/j.cell.2015.04.053
  22. Irie N, Lee SM, Lorenzi V et al (2023) DMRT1 regulates human germline commitment. Nat Cell Biol 25, 1439-1452  https://doi.org/10.1038/s41556-023-01224-7
  23. Frauer C, Hoffmann T, Bultmann S et al (2011) Recognition of 5-hydroxymethylcytosine by the Uhrf1 SRA domain. PLoS One 6, e21306 
  24. Hashimoto H, Liu Y, Upadhyay AK et al (2012) Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res 40, 4841-4849  https://doi.org/10.1093/nar/gks155
  25. Mayer W, Niveleau A, Walter J, Fundele R and Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403, 501-502  https://doi.org/10.1038/35000656
  26. Shen L, Inoue A, He J, Liu Y, Lu F and Zhang Y (2014) Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell 15, 459-471  https://doi.org/10.1016/j.stem.2014.09.002
  27. Yan R, Cheng X, Gu C et al (2023) Dynamics of DNA hydroxymethylation and methylation during mouse embryonic and germline development. Nat Genet 55, 130-143  https://doi.org/10.1038/s41588-022-01258-x
  28. Dawlaty MM, Breiling A, Le T et al (2013) Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24, 310-323  https://doi.org/10.1016/j.devcel.2012.12.015
  29. Hon GC, Song CX, Du T et al (2014) 5mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol Cell 56, 286-297  https://doi.org/10.1016/j.molcel.2014.08.026
  30. Huang Y, Chavez L, Chang X et al (2014) Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells. Proc Natl Acad Sci U S A 111, 1361-1366  https://doi.org/10.1073/pnas.1322921111
  31. Song CX, Szulwach KE, Fu Y et al (2011) Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 29, 68-72  https://doi.org/10.1038/nbt.1732
  32. Miura F, Enomoto Y, Dairiki R and Ito T (2012) Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 40, e136 
  33. Booth MJ, Branco MR, Ficz G et al (2012) Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336, 934-937  https://doi.org/10.1126/science.1220671
  34. Liu Y, Siejka-Zielinska P, Velikova G et al (2019) Bisulfite-free direct detection of 5-methylcytosine and 5-hydroxymethylcytosine at base resolution. Nat Biotechnol 37, 424-429  https://doi.org/10.1038/s41587-019-0041-2
  35. Liu YB, Hu ZY, Cheng JF et al (2021) Subtraction-free and bisulfite-free specific sequencing of 5-methylcytosine and its oxidized derivatives at base resolution. Nat Commun 12, 618 
  36. Xu HQ, Chen JF, Cheng JF et al (2023) Modular oxidation of cytosine modifications and their application in direct and quantitative sequencing of 5-hydroxymethylcytosine. JACS 145, 7095-7100  https://doi.org/10.1021/jacs.3c01663
  37. Vaisvila R, Ponnaluri VKC, Sun ZY et al (2021) Enzymatic methyl sequencing detects DNA methylation at single-base resolution from picograms of DNA. Genome Res 31, 1280-1289  https://doi.org/10.1101/gr.266551.120
  38. Wang T, Fowler JM, Liu L et al (2023) Direct enzymatic sequencing of 5-methylcytosine at single-base resolution. Nat Chem Biol 19, 1004-1012  https://doi.org/10.1038/s41589-023-01318-1
  39. Smallwood SA, Lee HJ, Angermueller C et al (2014) Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods 11, 817-820  https://doi.org/10.1038/nmeth.3035
  40. Clark SJ, Argelaguet R, Kapourani CA et al (2018) scNMT-seq enables joint profiling of chromatin accessibility DNA methylation and transcription in single cells. Nat Commun 9, 781 
  41. Lee DS, Luo C, Zhou J et al (2019) Simultaneous profiling of 3D genome structure and DNA methylation in single human cells. Nat Methods 16, 999-1006  https://doi.org/10.1038/s41592-019-0547-z
  42. Flusberg BA, Webster DR, Lee JH et al (2010) Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 7, 461-465  https://doi.org/10.1038/nmeth.1459
  43. Laszlo AH, Derrington IM, Brinkerhoff H et al (2013) Detection and mapping of 5-methylcytosine and 5-hydroxymethylcytosine with nanopore MspA. Proc Natl Acad Sci U S A 110, 18904-18909  https://doi.org/10.1073/pnas.1310240110
  44. Clark TA, Lu X, Luong K et al (2013) Enhanced 5-methylcytosine detection in single-molecule, real-time sequencing via Tet1 oxidation. BMC Biol 11, 4 
  45. Tse OYO, Jiang P, Cheng SH et al (2021) Genome-wide detection of cytosine methylation by single molecule real-time sequencing. Proc Natl Acad Sci U S A 118, e2019768118 
  46. Liu Q, Fang L, Yu G, Wang D, Xiao CL and Wang K (2019) Detection of DNA base modifications by deep recurrent neural network on Oxford Nanopore sequencing data. Nat Commun 10, 2449 
  47. Kingan SB, Heaton H, Cudini J et al (2019) A high-quality de novo genome assembly from a single mosquito using PacBio sequencing. Genes (Basel) 10, 62 
  48. Xu L and Seki M (2020) Recent advances in the detection of base modifications using the Nanopore sequencer. J Hum Genet 65, 25-33 https://doi.org/10.1038/s10038-019-0679-0