Cited by 920DNA and Nucleic Acid ChemistryAdvanced biosensing and bioanalysis techniquesMetal complexes synthesis and properties

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The Structure and Function of DNA G-Quadruplexes

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Spiegel, Jochen, Adhikari, Santosh, Balasubramanian, Shankar·2020·Trends in Chemistry

DOI 10.1016/j.trechm.2019.07.002PMC PMC7472594

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Abstract

Guanine-rich DNA sequences can fold into four-stranded, noncanonical secondary structures called G-quadruplexes (G4s). G4s were initially considered a structural curiosity, but recent evidence suggests their involvement in key genome functions such as transcription, replication, genome stability, and epigenetic regulation, together with numerous connections to cancer biology. Collectively, these advances have stimulated research probing G4 mechanisms and consequent opportunities for therapeutic intervention. Here, we provide a perspective on the structure and function of G4s with an emphasis on key molecules and methodological advances that enable the study of G4 structures in human cells. We also critically examine recent mechanistic insights into G4 biology and protein interaction partners and highlight opportunities for drug discovery.

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Figure 1 G-Quadruplex (G4) Structures. (A) Structure of a G-quartet formed by the Hoogsteen hydrogen-bonded guanines and central cation (coloured green) coordinated to oxygen atoms. Crystal structure of human telomeric G4s (Protein Data Bank: 1KF1): (B) top view and (C) side view; backbone is represented by grey tube and the structures are colour-coded by atoms. Schematic representation of unimolecular G4s based on the strand direction: (D) parallel, (E) anti-parallel, and (F) hybrid with a bulge.CC BY-NC-ND · PubMed Central

Figure 2 G-Quadruplex (G4) Ligands. (A) Crystal structure of a naphthalene diimide, MM41 bound to an intramolecular human telomeric DNA G4, colour-coded by atoms; water molecules are shown as red spheres, MM41 carbon atoms are coloured green, surface of the G4 is coloured light grey (Protein Data Bank: 3UYH). (B) Structures of selected widely used G4 ligands.CC BY-NC-ND · PubMed Central

Figure 3 Detection and Mapping of DNA G-Quadruplexes (G4s). (A) Visualisation of G4s in fixed or live cells using structure-specific antibodies as well as labelled or intrinsically fluorescent G4 ligands. The number of detected G4 foci can be increased by small molecule treatment or helicase depletion. (B) High-throughput sequencing of G4s in human genomic DNA (G4-Seq). Two consecutive sequencing runs, under normal and G4 stabilising conditions, provide a reference map and detect G4-dependent polymerase stalling, respectively. (C) Chromatin immunoprecipitation employing antibodies against endogenous G4-binding proteins followed by next-generation sequencing (ChIP-seq). Genomic occupancy of endogenous proteins is used to infer putative G4 sites. (D) Treatment with G4 ligands induces G4-dependent DNA damage. ChIP-seq of DNA damage markers in combination with deep sequencing detects G4-associated regions. (E) Permanganate oxidation of nucleotides in transiently unwound regions traps the unpaired state, resulting in sensitivity to a single-strand specific nuclease. Computational prediction is then used to infer the type of underlying non-B-DNA structures based on sequence context. (F) G4-specific chromatin immunoprecipitation and next-generation sequencing (G4 ChIP-seq). A G4-specific antibody (e.g., BG4) is used to precipitate G4 structures directly from native chromatin and is identified by deep sequencing.CC BY-NC-ND · PubMed Central

Figure 4 Crystal Structure of DHX36 Bound to the c-Myc G4 (Protein Data Bank: 5VHE). Overall structure is shown in cartoon representation with the domain organisation of DHX36 colour-coded (top). The α-helical DHX36-specific motif (DSM) stacks on the 5′-quartet. The residues Ile65, Tyr69, and Ala70 form a nonpolar surface similar to the proposed binding mode of most small molecule G-quadruplex (G4) ligands (bottom).CC BY-NC-ND · PubMed Central

Figure 5 G-Quadruplex (G4) Can Induce Epigenetic Reprogramming. Unresolved G4 structures (e.g., G4 ligand treatment, impaired helicases) on the leading strand may promote uncoupling of DNA synthesis from opening of the replication fork and disrupt histone recycling. Original histone modifications (blue) are lost and replaced with new histones (brown), resulting in epigenetic reprogramming upstream of G4 sites.CC BY-NC-ND · PubMed Central

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“Telomeric regions consist of non-coding tandem DNA repeats, TTAGGG, which form a lariat-like molecular Tloop structure and act as a protective cap to prevent chromosome degradation, inter-chromosomal fusion, and preserve genetic integrity (Shammas 2011; Spiegel, Adhikari, and Balasubramanian 2020).”
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“G-quadruplexes (G4s) and R-loops are non-canonical nucleic acid structures involved in cellular processes such as DNA replication, transcription, and translation [ 1–4 ] with implications for diseases including cancer [ 5–7 ] and neurological disorders [ 8 , 9 ].”
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“It is believed that G4s play significant regulatory roles in a variety of diseases, mainly cancers and neurodegenerative disorders (22, 23).”
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“Among those mentioned above, G4s stand out as the most broadly studied alternative structures of DNA ( 5 ).”
Background
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Development of a multi-targeted chemotherapeutic approach based on G-quadruplex stabilisation and carbonic anhydrase inhibition
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BackgroundMethodInfluential
Small molecule telomerase inhibitors are also potent inhibitors of telomeric C-strand synthesis
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“…DNA sequences, including the repeating human telomeric sequence (TTAGGG) n , are capable of forming G-quadruplexes (GQs), structures in which four guanines interact to form a tetrad or “ G-quartet, ” and several such quartets stack to form a quadruplex (Williamson et al. 1989; Spiegel et al. 2020).”
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Influence of the Charge Ratio of Guanine-Quadruplex Structure-Based CpG Oligodeoxynucleotides and Cationic DOTAP Liposomes on Cytokine Induction Profiles
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Peptides and Peptide Derivatives as G‐Quadruplex Targeting Ligands: A Brief Review
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Prospecting the cancer therapeutic edge of chitosan-based gold nanoparticles through conformation selective binding to the parallel G-quadruplex formed by short telomeric DNA sequence: A multi-spectroscopic approach
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Development of Fluorescent Aptasensors Based on G-Quadruplex Quenching Ability for Ochratoxin A and Potassium Ions Detection
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“The G-quadruplex is a unique secondary structure of DNA folding from a single-strand or several strands of DNA sequences rich in guanine with a highly ordered and diverse structure [4,5].”
Background
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Selective Binding and Redox-Activity on Parallel G-Quadruplexes by Pegylated Naphthalene Diimide-Copper Complexes
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Identifying and validating the presence of Guanine-Quadruplexes (G4) within the blood fluke parasite Schistosoma mansoni
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Enhancing G‐Quadruplex Binding: Rational Design and Biophysical Evaluation of Dimeric Ligands
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Degradation of G‐Quadruplex‐Binding Proteins by G4L‐PROTAC via Quaternary Complex Formation
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Molecular Tools for Precision Targeting and Detection of G-Quadruplex Structures
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“However, the dynamic environment that surrounds the nucleic acid and that builds up the genomic machinery is responsible for variations in the coiling and its conformation, making possible the observation of different secondary structures [3].”
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Functional and Structural Analyses of Diverse G‐Quadruplex and Non‐G‐Quadruplex Structures Formed by Guanine‐Rich Nucleic Acids: A Study on the Insulin Aptamer
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“…vitro , G4s have been shown to serve as structural motifs of aptamers—nucleic acid-based functional analogs of formation of G4s has been suggested to have a regulatory role in vivo in telomere maintenance, DNA replication, gene expression, and translation [5,6]. a The deox-yribozyme a [11,13–19].”
APE1 promotes lung adenocarcinoma through G4-mediated transcriptional reprogramming of urea cycle metabolism
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“48,49 It remains possible that the discrepancy between these results may arise from the diverse regulation of KRAS in different tumor models.”
Interactions between heme and G-quadruplex DNA involve the oxygen of guanine
Chiura, T., Pham, M. N., Baum, D. A., & Mak, P. J. (2025) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2025.112843 · Cited by 6
Asymmetric distribution of G-quadruplex forming sequences in genomes of retroviruses
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G-Quadruplex Recognition by Tetraalkylammonium Ions: A New Paradigm for Discrimination between Parallel and Antiparallel G-Quadruplexes.
Li, X., Dubins, D., Völker, J., & Chalikian, T. (2024) · Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.4c06355 · Cited by 5
Interlocking G-Quadruplexes Using a G-Triad•G Connection: Implications for G-Wire Assembly.
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Quantitative Effects of the Loop Region on Topology, Thermodynamics, and Cation Binding of DNA G-quadruplexes
Nakata, M., Kosaka, N., Kawauchi, K., & Miyoshi, D. (2024) · ACS Omega · doi:10.1021/acsomega.4c05008 · Cited by 5
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TMPRSS2 isoform 1 downregulation by G-quadruplex stabilization induces SARS-CoV-2 replication arrest
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Background
Predicting the Three-Dimensional Structure of the c-KIT Proto-Oncogene Promoter and the Dynamics of Its Strongly Coupled Guanine Quadruplexes
Bignon, E., Spinello, A., Miclot, T., D’Anna, L., Ducani, C., Grandemange, S., Barone, G., Monari, A., & Terenzi, A. (2023) · The Journal of Physical Chemistry Letters · doi:10.1021/acs.jpclett.3c00765 · Cited by 8
Mapping and characterization of G‐quadruplexes in monkeypox genomes
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“G‐quadruplexes (G4s) are noncanonical DNA and RNA structures formed by guanine‐rich sequences that fold into two or more consecutive quartets.(10) A G‐quartet refers to four planar guanines”
Background
Exploring the Binding of Natural Compounds to Cancer-Related G-Quadruplex Structures: From 9,10-Dihydrophenanthrenes to Their Dimeric and Glucoside Derivatives
Platella, C., Criscuolo, A., Riccardi, C., Gaglione, R., Arciello, A., Musumeci, D., DellaGreca, M., & Montesarchio, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24097765 · Cited by 5
“DNA secondary structures, such as G-quadruplexes, are promising targets for anticancer strategies in the context of targeted therapies [1,2].”
Background
G-quadruplex landscape and its regulation revealed by a new antibody capture method
Datta, S., Patel, M., Sathyaseelan, C., Ghosh, C., Mudgal, A., Patel, D., Rathinavelan, T., & Singh, U. (2023) · bioRxiv · doi:10.18632/oncotarget.28564 · Cited by 5
“More recently, regulatory functions have been attributed to quadruplex structures [8, 18–20].”
Nanopore Liberates G-Quadruplexes from Biochemical Buffers for Accurate Mass Spectrometric Examination
Lei, W., Hu, J. J., Chen, H., & Xu, J. (2022) · Analytical Chemistry · doi:10.1021/acs.analchem.2c04099 · Cited by 5
Functional Downregulation of PD-L1 and PD-L2 by CpG and non-CpG Oligonucleotides in Melanoma Cells
Kleemann, J., Steinhorst, K., König, V., Zöller, N., Cinatl, J., Ozistanbullu, D., Kaufmann, R., Meissner, M., & Kippenberger, S. (2022) · Cancers · doi:10.3390/cancers14194698 · Cited by 5
“In particular, the formation of successive G-tetrads (G4) of Hoogsteen hydrogen-bonded guanine bases has been shown to have an impact on genome functions such as transcription, replication and epigenetic regulation [42].”
Background
Telomere G-triplex lights up Thioflavin T for RNA detection: new wine in an old bottle
Qin, S., Chen, X., Xu, Z., Li, T., Zhao, S., Hu, R., Zhu, J., Li, Y., Yang, Y.-H., & Liu, M. (2022) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-022-04180-7 · Cited by 5

Authors: Spiegel, J., Adhikari, S., & Balasubramanian, S.
Affiliations: Cancer Research UK (GB)
University of Cambridge (GB)
Corresponding author: Balasubramanian, Shankar
ORCID: Spiegel, Jochen
Adhikari, Santosh
Balasubramanian, Shankar
Venue: Trends in Chemistry
Publisher: Elsevier BV
Published: 2020-02
Volume: 2
Issue: 2
Pages: 123-136
ISSN: 2589-5974 (ISSN-L)
DOI: 10.1016/j.trechm.2019.07.002
PMC: PMC7472594
OpenAlex: W2966334511
Cited by: 920
References: 121
Citations by year: 2026: 111 · 2025: 157 · 2024: 158 · 2023: 144 · 2022: 151 · 2021: 122 · 2020: 74
FWCI: 7.73
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Trends in Chemistry (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
Apollo
Funders: Wellcome Trust
Cancer Research UK
Horizon 2020 Framework Programme
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Advanced biosensing and bioanalysis techniques
Health Sciences › Medicine › Oncology › Metal complexes synthesis and properties
Keywords: G-quadruplex, guanine-rich DNA, genome stability, transcription, DNA replication, epigenetic regulation, cancer, G-quadruplex-binding proteins

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The Structure and Function of DNA G-Quadruplexes

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