Composite 5-methylations of cytosines modulate i-motif
stability in a sequence-specific manner: Implications for DNA
nanotechnology and epigenetic regulation of plant telomeric DNA

J 2020

Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA

ŠKOLÁKOVÁ, Petra; Zahra BADRI; Silvie TRANTÍRKOVÁ; Jan RYNEŠ; Jiří ŠPONER et al.

Basic information

Original name

Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA

Authors

Edition

BBA - General Subjects, Elsevier B.V. 2020, 0304-4165

Other information

Language

English

Type of outcome

Article in a journal

Field of Study

10610 Biophysics

Country of publisher

Netherlands

Confidentiality degree

is not subject to a state or trade secret

References:

DOI: 10.1016/j.bbagen.2020.129651

Impact factor

Impact factor: 3.770

Marked to be transferred to RIV

Yes

RIV identification code

RIV/00216224:14740/20:00115829

Organization unit

Central European Institute of Technology

Keywords in English

i-motif;DNA;Epigenetic modification;DNA nanotechnology;Plant telomeric DNA;Cytosine methylation

Abstract

In the original language

Background: The i-motif is a tetrameric DNA structure based on the formation of hemiprotonated cytosinecytosine (C+.C) base pairs. i-motifs are widely used in nanotechnology. In biological systems, i-motifs are involved in gene regulation and in control of genome integrity. In vivo, the i-motif forming sequences are subjects of epigenetic modifications, particularly 5-cytosine methylation. In plants, natively occurring methylation patterns lead to a complex network of C+.C, 5mC+.C and 5mC+.5mC base-pairs in the i-motif stem. The impact of complex methylation patterns (CMPs) on i-motif formation propensity is currently unknown. Methods: We employed CD and UV-absorption spectroscopies, native PAGE, thermal denaturation and quantumchemical calculations to analyse the effects of native, native-like, and non-native CMPs in the i-motif stem on the i-motif stability and pKa. Results: CMPs have strong influence on i-motif stability and pKa and influence these parameters in sequencespecific manner. In contrast to a general belief, i) CMPs do not invariably stabilize the i-motif, and ii) when the CMPs do stabilize the i-motif, the extent of the stabilization depends (in a complex manner) on the number and pattern of symmetric 5mC+.5mC or asymmetric 5mC+.C base pairs in the i-motif stem. Conclusions: CMPs can be effectively used to fine-tune i-motif properties. Our data support the notion of epigenetic modifications as a plausible control mechanism of i-motif formation in vivo. General Significance: Our results have implications in epigenetic regulation of telomeric DNA in plants and highlight the potential and limitations of engineered patterning of cytosine methylations on the i-motif scaffold in nanotechnological applications.

Links

LQ1601, research and development project

Name: CEITEC 2020 (Acronym: CEITEC2020)

Investor: Ministry of Education, Youth and Sports of the CR

NV19-08-00450, research and development project

Name: Atomárně rozlišená NMR spektroskopie in vivo jako nástroj pro biologické testování terapeuticky významných cílů v genomové ne-kanonické DNA a jejich interakcí s léčivy ve fenotypově diverzifikovaných nádorových buňkách.

Investor: Ministry of Health of the CR

90127, large research infrastructures

Name: CIISB II

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Cite

ŠKOLÁKOVÁ, Petra; Zahra BADRI; Silvie TRANTÍRKOVÁ; Jan RYNEŠ; Jiří ŠPONER; Miloslava FOJTOVÁ; Jiří FAJKUS; Radek MAREK; Michaela VORLÍČKOVÁ; Jean-Louis MERGNY and Lukáš TRANTÍREK. Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA. BBA - General Subjects. Elsevier B.V., 2020, vol. 1864, No 9, p. 129651-129659. ISSN 0304-4165. Available from: https://doi.org/10.1016/j.bbagen.2020.129651.

@article{1663196,
   author = {Školáková, Petra and Badri, Zahra and Trantírková, Silvie and Ryneš, Jan and Šponer, Jiří and Fojtová, Miloslava and Fajkus, Jiří and Marek, Radek and Vorlíčková, Michaela and Mergny, JeanandLouis and Trantírek, Lukáš},
   article_number = {9},
   doi = {https://doi.org/10.1016/j.bbagen.2020.129651},
   keywords = {i-motif;DNA;Epigenetic modification;DNA nanotechnology;Plant telomeric DNA;Cytosine methylation},
   language = {eng},
   issn = {0304-4165},
   journal = {BBA - General Subjects},
   title = {Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA},
   url = {http://dx.doi.org/10.1016/j.bbagen.2020.129651},
   volume = {1864},
   year = {2020}
}

TY  - JOUR
ID  - 1663196
AU  - Školáková, Petra - Badri, Zahra - Trantírková, Silvie - Ryneš, Jan - Šponer, Jiří - Fojtová, Miloslava - Fajkus, Jiří - Marek, Radek - Vorlíčková, Michaela - Mergny, Jean-Louis - Trantírek, Lukáš
PY  - 2020
TI  - Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA
JF  - BBA - General Subjects
VL  - 1864
IS  - 9
SP  - 129651
EP  - 129651
PB  - Elsevier B.V.
SN  - 03044165
KW  - i-motif;DNA;Epigenetic modification;DNA nanotechnology;Plant telomeric DNA;Cytosine methylation
UR  - http://dx.doi.org/10.1016/j.bbagen.2020.129651
L2  - http://dx.doi.org/10.1016/j.bbagen.2020.129651
N2  - Background: The i-motif is a tetrameric DNA structure based on the formation of hemiprotonated cytosinecytosine (C+.C) base pairs. i-motifs are widely used in nanotechnology. In biological systems, i-motifs are involved in gene regulation and in control of genome integrity. In vivo, the i-motif forming sequences are subjects of epigenetic modifications, particularly 5-cytosine methylation. In plants, natively occurring methylation patterns lead to a complex network of C+.C, 5mC+.C and 5mC+.5mC base-pairs in the i-motif stem. The impact of complex methylation patterns (CMPs) on i-motif formation propensity is currently unknown. Methods: We employed CD and UV-absorption spectroscopies, native PAGE, thermal denaturation and quantumchemical calculations to analyse the effects of native, native-like, and non-native CMPs in the i-motif stem on the i-motif stability and pKa. Results: CMPs have strong influence on i-motif stability and pKa and influence these parameters in sequencespecific manner. In contrast to a general belief, i) CMPs do not invariably stabilize the i-motif, and ii) when the CMPs do stabilize the i-motif, the extent of the stabilization depends (in a complex manner) on the number and pattern of symmetric 5mC+.5mC or asymmetric 5mC+.C base pairs in the i-motif stem. Conclusions: CMPs can be effectively used to fine-tune i-motif properties. Our data support the notion of epigenetic modifications as a plausible control mechanism of i-motif formation in vivo. General Significance: Our results have implications in epigenetic regulation of telomeric DNA in plants and highlight the potential and limitations of engineered patterning of cytosine methylations on the i-motif scaffold in nanotechnological applications.
ER  -

ŠKOLÁKOVÁ, Petra; Zahra BADRI; Silvie TRANTÍRKOVÁ; Jan RYNEŠ; Jiří ŠPONER; Miloslava FOJTOVÁ; Jiří FAJKUS; Radek MAREK; Michaela VORLÍČKOVÁ; Jean-Louis MERGNY and Lukáš TRANTÍREK. Composite 5-methylations of cytosines modulate i-motif stability in a sequence-specific manner: Implications for DNA nanotechnology and epigenetic regulation of plant telomeric DNA. \textit{BBA - General Subjects}. Elsevier B.V., 2020, vol.~1864, No~9, p.~129651-129659. ISSN~0304-4165. Available from: https://doi.org/10.1016/j.bbagen.2020.129651.

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