Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine
Abstract
5-Hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC) form during active demethylation of 5-methylcytosine (5mC) and are implicated in epigenetic regulation of the genome. They are differentially processed by thymine DNA glycosylase (TDG), an enzyme involved in active demethylation of 5mC. Three modified Dickerson–Drew dodecamer (DDD) sequences, amenable to crystallographic and spectroscopic analyses and containing the 5'-CG-3' sequence associated with genomic cytosine methylation, containing 5hmC, 5fC, or 5caC placed site-specifically into the 5'-T8X9G10-3' sequence of the DDD, were compared. The presence of 5caC at the X9 base increased the stability of the DDD, whereas 5hmC or 5fC did not. Both 5hmC and 5fC increased imino proton exchange rates and calculated rate constants for base pair opening at the neighboring base pair A5:T8, whereas 5caC did not. At the oxidized base pair G4:X9, 5fC exhibited an increase in the imino proton exchange rate and the calculated kop. In all cases, minimal effects to imino proton exchange rates occurred at the neighboring base pair C3:G10. No evidence was observed for imino tautomerization, accompanied by wobble base pairing, for 5hmC, 5fC, or 5caC when positioned at base pair G4:X9; each favored Watson–Crick base pairing. However, both 5fC and 5caC exhibited intranucleobase hydrogen bonding betweenmore »
- Authors:
-
- Department of Chemistry, Vanderbilt Institute of Chemical Biology, Vanderbilt Ingram Cancer Center, and Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37235, United States
- Department of Biochemistry, Vanderbilt Institute of Chemical Biology, Vanderbilt Ingram Cancer Center, and Center for Structural Biology, School of Medicine, Vanderbilt University, Nashville, Tennessee 37232, United States
- Bioscience Division, Argonne National Laboratory, Argonne, Illinois 60439, United States
- Northeastern Collaborative Access Team and Department of Chemistry and Chemical Biology, Cornell University, Argonne National Laboratory, Argonne, Illinois 60439, United States
- Department of Biological Sciences, Vanderbilt Institute of Chemical Biology, and Center for Structural Biology, Vanderbilt University, Nashville, Tennessee 37235, United States
- Publication Date:
- Research Org.:
- Vanderbilt Univ., Nashville, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1168972
- Alternate Identifier(s):
- OSTI ID: 1345617
- Grant/Contract Number:
- AC02-06CH11357; S10 RR- 05805; S10 RR-025677; DBI 0922862; P41 GM103403; R01 ES-019625; R01 CA-55678
- Resource Type:
- Published Article
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Name: Biochemistry Journal Volume: 54 Journal Issue: 5; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Szulik, Marta W., Pallan, Pradeep S., Nocek, Boguslaw, Voehler, Markus, Banerjee, Surajit, Brooks, Sonja, Joachimiak, Andrzej, Egli, Martin, Eichman, Brandt F., and Stone, Michael P. Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine. United States: N. p., 2015.
Web. doi:10.1021/bi501534x.
Szulik, Marta W., Pallan, Pradeep S., Nocek, Boguslaw, Voehler, Markus, Banerjee, Surajit, Brooks, Sonja, Joachimiak, Andrzej, Egli, Martin, Eichman, Brandt F., & Stone, Michael P. Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine. United States. https://doi.org/10.1021/bi501534x
Szulik, Marta W., Pallan, Pradeep S., Nocek, Boguslaw, Voehler, Markus, Banerjee, Surajit, Brooks, Sonja, Joachimiak, Andrzej, Egli, Martin, Eichman, Brandt F., and Stone, Michael P. Thu .
"Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine". United States. https://doi.org/10.1021/bi501534x.
@article{osti_1168972,
title = {Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine},
author = {Szulik, Marta W. and Pallan, Pradeep S. and Nocek, Boguslaw and Voehler, Markus and Banerjee, Surajit and Brooks, Sonja and Joachimiak, Andrzej and Egli, Martin and Eichman, Brandt F. and Stone, Michael P.},
abstractNote = {5-Hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC) form during active demethylation of 5-methylcytosine (5mC) and are implicated in epigenetic regulation of the genome. They are differentially processed by thymine DNA glycosylase (TDG), an enzyme involved in active demethylation of 5mC. Three modified Dickerson–Drew dodecamer (DDD) sequences, amenable to crystallographic and spectroscopic analyses and containing the 5'-CG-3' sequence associated with genomic cytosine methylation, containing 5hmC, 5fC, or 5caC placed site-specifically into the 5'-T8X9G10-3' sequence of the DDD, were compared. The presence of 5caC at the X9 base increased the stability of the DDD, whereas 5hmC or 5fC did not. Both 5hmC and 5fC increased imino proton exchange rates and calculated rate constants for base pair opening at the neighboring base pair A5:T8, whereas 5caC did not. At the oxidized base pair G4:X9, 5fC exhibited an increase in the imino proton exchange rate and the calculated kop. In all cases, minimal effects to imino proton exchange rates occurred at the neighboring base pair C3:G10. No evidence was observed for imino tautomerization, accompanied by wobble base pairing, for 5hmC, 5fC, or 5caC when positioned at base pair G4:X9; each favored Watson–Crick base pairing. However, both 5fC and 5caC exhibited intranucleobase hydrogen bonding between their formyl or carboxyl oxygens, respectively, and the adjacent cytosine N4 exocyclic amines. The lesion-specific differences observed in the DDD may be implicated in recognition of 5hmC, 5fC, or 5caC in DNA by TDG. Furthermore, they do not correlate with differential excision of 5hmC, 5fC, or 5caC by TDG, which may be mediated by differences in transition states of the enzyme-bound complexes.},
doi = {10.1021/bi501534x},
journal = {Biochemistry},
number = 5,
volume = 54,
place = {United States},
year = {Thu Jan 29 00:00:00 EST 2015},
month = {Thu Jan 29 00:00:00 EST 2015}
}
https://doi.org/10.1021/bi501534x
Web of Science
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