Direct enzymatic sequencing of 5-methylcytosine at single-base resolution

5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here we present direct methylation sequencing (DM-Seq), a...

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Published inNature chemical biology Vol. 19; no. 8; pp. 1004 - 1012
Main Authors Wang, Tong, Fowler, Johanna M., Liu, Laura, Loo, Christian E., Luo, Meiqi, Schutsky, Emily K., Berríos, Kiara N., DeNizio, Jamie E., Dvorak, Ashley, Downey, Nick, Montermoso, Saira, Pingul, Bianca Y., Nasrallah, MacLean, Gosal, Walraj S., Wu, Hao, Kohli, Rahul M.
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.08.2023
Nature Publishing Group
Subjects
5-Methylcytosine
631/208
631/92/147
Animals
Biochemical Engineering
Biochemistry
Bioorganic Chemistry
Bisulfite
Cell Biology
Chemistry
Chemistry and Materials Science
Chemistry/Food Science
Cytosine
Deamination
Deoxyribonucleic acid
DNA
DNA - genetics
DNA Methylation
DNA methyltransferase
Genetic testing
Genomes
Localization
Mammals - genetics
Nondestructive testing
Nucleotide sequence
Sequence Analysis, DNA - methods
Substrates
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Abstract 5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here we present direct methylation sequencing (DM-Seq), a bisulfite-free method for profiling 5mC at single-base resolution using nanogram quantities of DNA. DM-Seq employs two key DNA-modifying enzymes: a neomorphic DNA methyltransferase and a DNA deaminase capable of precise discrimination between cytosine modification states. Coupling these activities with deaminase-resistant adapters enables accurate detection of only 5mC via a C-to-T transition in sequencing. By comparison, we uncover a PCR-related underdetection bias with the hybrid enzymatic-chemical TET-assisted pyridine borane sequencing approach. Importantly, we show that DM-Seq, unlike bisulfite sequencing, unmasks prognostically important CpGs in a clinical tumor sample by not confounding 5mC with 5-hydroxymethylcytosine. DM-Seq thus offers an all-enzymatic, nondestructive, faithful and direct method for the reading of 5mC alone. Wang et al. developed a bisulfite-free method termed DM-Seq that leverages an unnatural enzyme–substrate pair coupled with a DNA deaminase to sequence 5-methylcytosine at base resolution in sparse DNA samples, circumventing the limitations of chemical deamination methods.
AbstractList 5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here we present direct methylation sequencing (DM-Seq), a bisulfite-free method for profiling 5mC at single-base resolution using nanogram quantities of DNA. DM-Seq employs two key DNA-modifying enzymes: a neomorphic DNA methyltransferase and a DNA deaminase capable of precise discrimination between cytosine modification states. Coupling these activities with deaminase-resistant adapters enables accurate detection of only 5mC via a C-to-T transition in sequencing. By comparison, we uncover a PCR-related underdetection bias with the hybrid enzymatic-chemical TET-assisted pyridine borane sequencing approach. Importantly, we show that DM-Seq, unlike bisulfite sequencing, unmasks prognostically important CpGs in a clinical tumor sample by not confounding 5mC with 5-hydroxymethylcytosine. DM-Seq thus offers an all-enzymatic, nondestructive, faithful and direct method for the reading of 5mC alone. Wang et al. developed a bisulfite-free method termed DM-Seq that leverages an unnatural enzyme–substrate pair coupled with a DNA deaminase to sequence 5-methylcytosine at base resolution in sparse DNA samples, circumventing the limitations of chemical deamination methods.
5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here we present direct methylation sequencing (DM-Seq), a bisulfite-free method for profiling 5mC at single-base resolution using nanogram quantities of DNA. DM-Seq employs two key DNA-modifying enzymes: a neomorphic DNA methyltransferase and a DNA deaminase capable of precise discrimination between cytosine modification states. Coupling these activities with deaminase-resistant adapters enables accurate detection of only 5mC via a C-to-T transition in sequencing. By comparison, we uncover a PCR-related underdetection bias with the hybrid enzymatic-chemical TET-assisted pyridine borane sequencing approach. Importantly, we show that DM-Seq, unlike bisulfite sequencing, unmasks prognostically important CpGs in a clinical tumor sample by not confounding 5mC with 5-hydroxymethylcytosine. DM-Seq thus offers an all-enzymatic, nondestructive, faithful and direct method for the reading of 5mC alone.
5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both non-destructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here, we present Direct Methylation Sequencing (DM-Seq), a bisulfite-free method for profiling 5mC at single-base resolution using nanogram quantities of DNA. DM-Seq employs two key DNA modifying enzymes: a neomorphic DNA methyltransferase and a DNA deaminase capable of precise discrimination between cytosine modification states. Coupling these activities with novel deaminase-resistant adapters enables accurate detection of only 5mC via a C-to-T transition in sequencing. By comparison, we uncover a PCR-related underdetection bias with the hybrid enzymatic-chemical TAPS approach. Importantly, we show that DM-Seq, unlike bisulfite-sequencing, unmasks prognostically important CpGs in a clinical tumor sample by not confounding 5mC with 5-hydroxymethylcytosine. DM-Seq thus offers an all-enzymatic, non-destructive, faithful, and direct method for the reading of 5-methylcytosine alone.
5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA and direct, without requiring inference based on detection of unmodified cytosines. Here we present direct methylation sequencing (DM-Seq), a bisulfite-free method for profiling 5mC at single-base resolution using nanogram quantities of DNA. DM-Seq employs two key DNA-modifying enzymes: a neomorphic DNA methyltransferase and a DNA deaminase capable of precise discrimination between cytosine modification states. Coupling these activities with deaminase-resistant adapters enables accurate detection of only 5mC via a C-to-T transition in sequencing. By comparison, we uncover a PCR-related underdetection bias with the hybrid enzymatic-chemical TET-assisted pyridine borane sequencing approach. Importantly, we show that DM-Seq, unlike bisulfite sequencing, unmasks prognostically important CpGs in a clinical tumor sample by not confounding 5mC with 5-hydroxymethylcytosine. DM-Seq thus offers an all-enzymatic, nondestructive, faithful and direct method for the reading of 5mC alone.Wang et al. developed a bisulfite-free method termed DM-Seq that leverages an unnatural enzyme–substrate pair coupled with a DNA deaminase to sequence 5-methylcytosine at base resolution in sparse DNA samples, circumventing the limitations of chemical deamination methods.
Author DeNizio, Jamie E.
Wu, Hao
Schutsky, Emily K.
Downey, Nick
Pingul, Bianca Y.
Gosal, Walraj S.
Wang, Tong
Liu, Laura
Fowler, Johanna M.
Montermoso, Saira
Kohli, Rahul M.
Nasrallah, MacLean
Dvorak, Ashley
Loo, Christian E.
Berríos, Kiara N.
Luo, Meiqi
AuthorAffiliation 7 Epigenetics Institute, University of Pennsylvania, Philadelphia, PA, USA
8 Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, PA, USA
1 Graduate Group in Biochemistry and Molecular Biophysics, University of Pennsylvania, Philadelphia, PA, USA
4 Department of Pathology, University of Pennsylvania, Philadelphia, PA, USA
2 Department of Medicine, University of Pennsylvania, Philadelphia, PA, USA
3 Integrated DNA Technologies, Inc., Coralville, IA, USA
6 Department of Genetics, University of Pennsylvania, Philadelphia, PA, USA
5 Cambridge Epigenetix, Saffron Walden, United Kingdom
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content type line 23
T.W., E.K.S., and R.M.K. conceived of the approach with input from W.G. and H.W. T.W. conducted experiments with assistance from J.M.F, L.L., C.E.L., M.L., E.K.S., K.N.B., J.E.D., S.M., and B.P. A.D. and N.D. supervised synthesis of 5pyC-adapters and M.N. contributed GBM gDNA. T.W., J.M.F., and H.W. performed computational analysis and analyzed the results. T.W. and R.M.K. wrote the manuscript, with contributions from all authors.
AUTHOR CONTRIBUTIONS
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PublicationDate 2023-08-01
PublicationDateYYYYMMDD 2023-08-01
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  year: 2023
  text: 2023-08-01
  day: 01
PublicationDecade 2020
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PublicationTitle Nature chemical biology
PublicationTitleAbbrev Nat Chem Biol
PublicationTitleAlternate Nat Chem Biol
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Publisher Nature Publishing Group US
Nature Publishing Group
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Snippet 5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both nondestructive of DNA...
5-methylcytosine (5mC) is the most important DNA modification in mammalian genomes. The ideal method for 5mC localization would be both non-destructive of DNA...
SourceID pubmedcentral
proquest
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springer
SourceType Open Access Repository
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Index Database
Publisher
StartPage 1004
SubjectTerms 5-Methylcytosine
631/208
631/92/147
Animals
Biochemical Engineering
Biochemistry
Bioorganic Chemistry
Bisulfite
Cell Biology
Chemistry
Chemistry and Materials Science
Chemistry/Food Science
Cytosine
Deamination
Deoxyribonucleic acid
DNA
DNA - genetics
DNA Methylation
DNA methyltransferase
Genetic testing
Genomes
Localization
Mammals - genetics
Nondestructive testing
Nucleotide sequence
Sequence Analysis, DNA - methods
Substrates
Title Direct enzymatic sequencing of 5-methylcytosine at single-base resolution
URI https://link.springer.com/article/10.1038/s41589-023-01318-1
https://www.ncbi.nlm.nih.gov/pubmed/37322153
https://www.proquest.com/docview/2842728244
https://search.proquest.com/docview/2827252666
https://pubmed.ncbi.nlm.nih.gov/PMC10763687
Volume 19
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