G-quadruplex formation of oligonucleotides containing ALS and FTD related GGGGCC repeat

doi:10.1007/s11705-016-1556-4

Front. Chem. Sci. Eng.

2016, Vol. 10

Issue (2) : 222-237 https://doi.org/10.1007/s11705-016-1556-4

RESEARCH ARTICLE

G-quadruplex formation of oligonucleotides containing ALS and FTD related GGGGCC repeat

Jasna Brčić¹,Janez Plavec^1,^2,^3,^*(

)

¹. Slovenian NMR Center, National Institute of Chemistry, Hajdrihova 19, SI-1000, Ljubljana, Slovenia
². Faculty of Chemistry and Chemical Technology, University of Ljubljana, SI-1000, Ljubljana, Slovenia
³. EN-FIST Center of Excellence, SI-1000, Ljubljana, Slovenia

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Abstract

A largely increased number of GGGGCC repeats located in the non-coding region of C9orf72 gene have been identified as the leading cause of two related neurological disorders, familial amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD). We examined G-quadruplex forming ability of GGGGCC-repeat containing oligonucleotides with four guanine tracts chosen as the smallest possible model to form a unimolecular G-quadruplex. These oligonucleotides are readily to folded into G-quadruplexes in the presence of K⁺ ions. However, the formation of multiple structures makes structural analysis challenging and time consuming. We observed that flanking sequences on 5'- and 3'-ends as well as mutations of loop residues have a profound effect on folding. Sequence d[(G₄C₂)₃G₄] was chosen for further scrutiny and optimization of nuclear magnetic resonance (NMR) spectroscopic properties with dG to 8Br-dG substitutions at specific positions in the sequence under different folding conditions. Expectedly, folding into desired predominant topology is facilitated when substituted residue adopted a syn conformation in the naturally-occurring structure. Single dG to 8Br-dG substitution at position 21 and fine tuning of folding conditions facilitate folding of d[(G₄C₂)₃GG^BrGG] into (mostly) a single G-quadruplex, and thus enable determination of its high-resolution structure by high-field NMR.

Keywords G-quadruplex GGGGCC NMR ALS/FTD polymorphism

Corresponding Author(s): Janez Plavec

Online First Date: 01 February 2016 Issue Date: 19 May 2016

Cite this article:

Jasna Brčić,Janez Plavec. G-quadruplex formation of oligonucleotides containing ALS and FTD related GGGGCC repeat[J]. Front. Chem. Sci. Eng., 2016, 10(2): 222-237.

URL:

https://academic.hep.com.cn/fcse/EN/10.1007/s11705-016-1556-4
https://academic.hep.com.cn/fcse/EN/Y2016/V10/I2/222

Fig.1 Sequences and extended imino regions of ¹H NMR spectra of S1, S2 and S3. (A) Sequences of S1, S2 and S3 oligonucleotides. Sequences represent DNA oligonucleotides written in 5′ to 3′ direction; (B) Imino regions of ¹H NMR spectra of S1, S2 and S3; (C) Imino regions of ¹H NMR spectra of S1 recorded at different times after the addition of KCl. Time after the addition of K⁺ ions is indicated on the left side of individual spectrum. Spectra were recorded at 25 °C, pH around 6 and oligonucleotide concentration between 0.9 and 1.9 mmol/L per strand in the presence of 30 mmol/L (S1 and S2) and 100 mmol/L KCl (S3)

Fig.2 G-quadruplex formation of 5′-phosphorylated oligonucleotides S4, S5, S6, S7 and S8. (A) Sequences of oligonucleotides. Sequences represent DNA oligonucleotides with added 5′-phosphate group and written in 5′ to 3′ direction; (B) CD spectra recorded at 25 °C, pH around 6 and 30 µmol/L oligonucleotide concentration per strand in the presence of 30 mmol/L KCl; (C) Imino region of ¹H NMR spectra recorded at 25 °C, pH around 6 and oligonucleotide concentration between 0.9 and 2.1 mmol/L per strand in the presence of 30 mmol/L KCl

Fig.3 G-quadruplex formation of oligonucleotides with one dC to T substitution. (A) Sequences of oligonucleotides with dC to T substitution. Sequences represent DNA oligonucleotides with added 5′-phosphate group and written in 5′ to 3′ direction; (B) Imino regions of ¹H NMR spectra of oligonucleotides after approximately 2 months of folding in the presence of KCl. Spectra were recorded at 25 °C, pH around 6 and oligonucleotide concentration between 0.9 and 1.1 mmol/L per strand in the presence of 30 mmol/L KCl

Fig.4 G-quadruplex formation of oligonucleotides with dC to 5Me-dC substitutions. (A) Sequences of S4A, S4B, S4C and S4D oligonucleotides. Sequences represent DNA oligonucleotides with added 5′-phosphate group and written in 5′ to 3′ direction. ^mC indicates 5Me-dC residue and is depicted in orange; (B) CD spectra of S4A, S4B, S4C and S4D after between two weeks and one month of folding in the presence of KCl. Spectra were recorded at 25 °C, pH around 6 and 30 μmol/L oligonucleotide concentration per strand in the presence of 30 mmol/L KCl; (C) Structure of 5Me-dC residue

Fig.5 Imino and aromatic regions of ¹H NMR spectra of 5Me-dC substituted oligonucleotides between two weeks and one month after folding in the presence of KCl. Resolved doublets of H6 of dC (star) and singlet of H6 of 5Me-dC (letter X) are indicated in the spectra of S4B and S4C to highlight their similarities. Spectra were recorded at 40 °C, pH around 6 and oligonucleotide concentration between 0.7 and 0.9 mmol/L per strand in the presence of 30 mmol/L KCl

Fig.6 Methyl regions of ¹H NMR spectra of 5Me-dC substituted oligonucleotides between two weeks and one month of folding in the presence of KCl. Signals corresponding to methyl protons of 5Me-dC residues are indicated with a star. Presented spectra were recorded at 40 °C, pH around 6 and oligonucleotide concentration between 0.7 and 0.9 mmol/L per strand in the presence of 30 mmol/L KCl

Fig.7 Expanded imino regions of ¹H NMR spectra of S4 after five days of folding in the presence of different salts. Spectra were recorded at 25 °C, pH around 6 and oligonucleotide concentration between 0.7 and 1.4 mmol/L per strand in the presence of 30 mmol/L KCl, NaCl or ¹⁵NH₄Cl

Fig.8 Influence of concentration of K⁺ ions and time on folding for (A) S4 and (B) S4B. Spectra were recorded at 25 °C, pH around 6, 1.4 (S4) and 0.9 mmol/L (S4B) oligonucleotide concentration per strand in the presence of 30 or 120 mmol/L KCl

Fig.9 H1′-H6/H8 region of NOESY and TOCSY spectra of S4B recorded after four months of folding in the presence of KCl. (A) NOESY spectrum with 300 ms mixing time; (B) NOESY spectrum with 150 ms mixing time; (C) TOCSY spectrum with 40 ms mixing time. Spectra were recorded at 25 °C, pH around 6 and 0.9 mmol/L oligonucleotide per strand in the presence of 30 mmol/L KCl

Fig.10 Proposed topologies of predominant G-quadruplex structures adopted by S4 and sequences of oligonucleotides with a single dG to 8Br-dG substitution. (A) Two proposed topologies of a G-quadruplex adopted by S4 named L (only lateral loops) and P (one propeller loops); (B) Structures of dG in anti conformation around the glycosidic bond and its brominated 8Br-dG analogue adopting a syn conformation and sequences of oligonucleotides with dG to 8Br-dG substitution. Sequences represent DNA oligonucleotides with added 5′-phosphate group and written in 5′ to 3′ direction. ^BrG indicates 8Br-dG residue depicted in magenta

Fig.11 Comparison of imino and aromatic regions of ¹H NMR spectra of wild type (S4) and oligonucleotides with dG to 8Br-dG substitutions at different positions recorded between two days and one month of folding in the presence of KCl. Spectra were recorded at 25 °C, pH around 6 and oligonucleotide concentration between 0.2 and 0.5 mmol/L per strand in the presence of 30 mmol/L KCl

Fig.12 Comparison of imino and aromatic regions of ¹H NMR spectra of wild type (S4) and oligonucleotides with dG to 8Br-dG substitutions at positions that resulted in folding into the same predominant G-quadruplex structures recorded between 10 days and 1 month of folding in the presence of KCl. Spectra were recorded at 25 °C, pH around 6 and between 0.3 and 0.5 mmol/L oligonucleotide per strand in the presence of 30 mmol/L KCl

Fig.13 Comparison of imino and aromatic regions of ¹H NMR spectra of (A) SL21 and (B) S1 folded in solutions with two different pH values indicated on the left side of each spectrum. Spectra were recorded at 25 °C in the presence of 120 mmol/L KCl and 20 mmol/L phosphate buffer with different pH values. Oligonucleotide concentrations were 0.5 mmol/L (SL21) and 0.6 mmol/L (S1) per strand. Sequences represent DNA oligonucleotides written in 5′ to 3′ direction

Fig.14 Representative structure of the major G-quadruplex adopted by SL21 at pH 7.2 in the presence of 120 mmol/L KCl. Side views in A and B are rotated with respect to one another to allow a better overview of the structures. Guanine residues are shown in dark green, cytosine in dark yellow and ^BrG21 in magenta

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