Cited by 223DNA and Nucleic Acid ChemistryAdvanced biosensing and bioanalysis techniquesTelomeres, Telomerase, and Senescence

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Elevated Levels of G-Quadruplex Formation in Human Stomach and Liver Cancer Tissues

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Biffi, Giulia, Tannahill, David, Miller, Jodi, Howat, William J., Balasubramanian, Shankar·2014·PLoS ONE

DOI 10.1371/journal.pone.0102711PMC PMC4102534

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Abstract

Four-stranded G-quadruplex DNA secondary structures have recently been visualized in the nuclei of human cultured cells. Here, we show that BG4, a G-quadruplex-specific antibody, can be used to stain DNA G-quadruplex structures in patient-derived tissues using immunohistochemistry. We observe a significantly elevated number of G-quadruplex-positive nuclei in human cancers of the liver and stomach as compared to background non-neoplastic tissue. Our results suggest that G-quadruplex formation can be detected and measured in patient-derived material and that elevated G-quadruplex formation may be a characteristic of some cancers.

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Figure 1 Validation of G-quadruplex nuclear staining by immunohistochemistry. A. Human MDA-MB-231 breast adenocarcinoma cell pellets were fixed, paraffin embedded and processed for IHC using the G-quadruplex-specific antibody BG4. No staining is observed in the absence of epitope retrieval. Scale bar corresponds to 20 µm. Nuclei are counterstained with haematoxylin (blue). B. Strong BG4 staining (brown) is readily apparent in cell nuclei following antigen retrieval with citrate-based buffer pH 6.0. C. No staining is observed in the absence of the BG4 primary antibody. D. No staining is seen following DNase treatment prior to BG4 staining. These results show that BG4 can be employed for DNA G-quadruplex detection by IHC staining.CC BY · PubMed Central

Figure 2 Increased incidence of DNA G-quadruplex structures in human liver cancer relative to matched non-neoplastic tissue. Background non-neoplastic and cancer liver tissues were stained by IHC using the G-quadruplex-specific antibody BG4. A. The nuclei of non-neoplastic liver tissue from a hepatocellular carcinoma patient are mostly BG4-negative, with haematoxylin counterstaining (blue) evident. Scale bar corresponds to 50 µm. Note that the cytoplasmic granules are variable and likely to be heme-based artifacts sometimes observed in liver IHC. B. Neoplastic tissue from the same patient in A shows the extensive presence of BG4-positive nuclei (brown). C. The nuclei of non-neoplastic liver tissue for an intrahepatic cholangiocarcinoma patient are mostly BG4-negative. D. Neoplastic tissue from the same patient in C shows many BG4-positive nuclei. E. The nuclei of non-neoplastic liver tissue from a metastatic large cell undifferentiated lung carcinoma patient are mostly BG4-negative. F. Metastatic liver tissue isolated from the same patient in E shows many BG4-positive nuclei. G. Quantification of the number of BG4-positive nuclei in liver cancer and corresponding matched non-neoplastic tissues from nine patients. Error bars represent the standard error of the mean (s.e.m.) calculated when duplicate TMA cores were available. Overall, these results indicate that there are a greater number of G-quadruplex structures in liver cancer compared to background non-neoplastic tissue from the same individual.CC BY · PubMed Central

Figure 3 Increased incidence of G-quadruplex-positive cell nuclei across human liver cancers. A. Quantification of the number of BG4-positive nuclei in individual liver tissues including unmatched TMA cores. Non-neoplastic liver shows less BG4-positive nuclei compared to hepatocellular carcinoma or intrahepatic cholangiocarcinoma. Each column corresponds to a single tissue sample and error bars represent the s.e.m. calculated when duplicate tissue samples were available. B. Overall quantification of the number of BG4-positive nuclei in all non-neoplastic and cancer liver tissues. Error bars represent the s.e.m. **P<0.001, n = 19 and 32 for non-neoplastic and cancer cores, respectively. These results confirm the generality of more extensive G-quadruplex formation in the liver cancers compared to non-neoplastic tissues.CC BY · PubMed Central

Figure 4 Increased incidence of DNA G-quadruplex structures in human stomach cancer relative to matched non-neoplastic tissue. Gastric adenocarcinoma and signet ring cell carcinoma and matched background non-neoplastic tissues taken from the same patient were stained with the G-quadruplex-specific antibody BG4 by IHC. A. The nuclei of non-neoplastic stomach tissue from a gastric adenocarcinoma patient are mostly BG4-negative, with haematoxylin counterstaining (blue) readily apparent. Scale bar corresponds to 50 µm. B. Adenocarcinoma tissue from the same patient in A shows extensive numbers of BG4-positive nuclei (brown). C. The nuclei of non-neoplastic stomach tissue from a signet ring cell carcinoma patient are mostly BG4-negative. D. Signet ring cell carcinoma tissue from the same patient in C shows many BG4-positive nuclei. E. Quantification of the number of BG4-positive nuclei in the matched stomach cancers and background non-neoplastic tissues from two different patients. Error bars represent the s.e.m. calculated when duplicate TMA cores were available. These results indicate that there are more G-quadruplex structures in the nuclei of stomach cancer tissue than in non-neoplastic tissue from the same individual.CC BY · PubMed Central

Figure 5 Increased incidence of G-quadruplex-positive cell nuclei across human stomach cancers. Confirmation of the increased presence of BG4-positive nuclei in a range of stomach cancer tissues compared to background non-neoplastic tissues including unmatched cases. A. The nuclei of non-neoplastic stomach tissues are largely BG4-negative. Cell nuclei were counterstained with haematoxylin (blue). Scale bar corresponds to 50 µm. B. Gastric adenocarcinoma tissue shows the extensive presence of BG4-positive nuclei (brown). C. Signet ring cell carcinoma shows many BG4-positive nuclei. D. Gastrointestinal stromal tumors (GIST) are largely BG4-positive (for the survey of stomach cancer only unmatched GIST tissues were available). E. Quantification of the number of BG4-positive nuclei in individual stomach tissues including unmatched TMA cores. Non-neoplastic stomach tissue shows less BG4-positive nuclei compared to adenocarcinoma, signet ring carcinoma or GIST. Each column corresponds to a single tissue sample and error bars represent the s.e.m. calculated when duplicate tissue samples were available. F. Overall quantification of the number of BG4-positive nuclei in all non-neoplastic and stomach liver tissues. Error bars represent the s.e.m. **P<0.001, n = 10 and 34 for non-neoplastic and cancer cores, respectively. These results confirm the generality of more extensive G-quadruplex formation in the stomach cancers compared to non-neoplastic tissues.CC BY · PubMed Central

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BackgroundMethodResultInfluential
Probing the Binding Pathway of BRACO19 to a Parallel-Stranded Human Telomeric G-Quadruplex Using Molecular Dynamics Binding Simulation with AMBER DNA OL15 and Ligand GAFF2 Force Fields
Machireddy, B., Kalra, G., Jonnalagadda, S. C., Ramanujachary, K. V., & Wu, C. F. (2017) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.7b00287 · Cited by 53
Disentangling the Structure–Activity Relationships of Naphthalene Diimides as Anticancer G-Quadruplex-Targeting Drugs
Platella, C., Napolitano, E., Riccardi, C., Musumeci, D., & Montesarchio, D. (2021) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c00125 · Cited by 47
Ligands stimulating antitumour immunity as the next G-quadruplex challenge
Miglietta, G., Marinello, J., Russo, M., & Capranico, G. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01649-y · Cited by 44
On the binding of naphthalene diimides to a human telomeric G-quadruplex multimer model.
Pirota, V., Platella, C., Musumeci, D., Benassi, A., Amato, J., Pagano, B., Colombo, G., Freccero, M., Doria, F., & Montesarchio, D. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.11.013 · Cited by 43
Gallic Acid: A Natural Phenolic Compound Exerting Antitumoral Activities in Colorectal Cancer via Interaction with G-Quadruplexes
Sánchez-Martín, V., Plaza‐Calonge, M. D. C., Soriano‐Lerma, A., Ortiz-González, M., Linde-Rodríguez, Á., Pérez‐Carrasco, V., Ramírez-Macías, I., Cuadros, M., Fernández, J. G., Murciano‐Calles, J., et al. (2022) · Cancers · doi:10.3390/cancers14112648 · Cited by 43
Cancer-associated noncoding mutations affect RNA G-quadruplex-mediated regulation of gene expression
Zeraati, M., Moye, A. L., Wong, J. W. H., Perera, D. S., Cowley, M. J., Christ, D., Bryan, T. M., & Dinger, M. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-00739-y · Cited by 42
Copper–Alkyne Complexation Responsible for the Nucleolar Localization of Quadruplex Nucleic Acid Drugs Labeled by Click Reactions
Lefebvre, J., Guetta, C., Poyer, F., Mahuteau‐Betzer, F., & Teulade‐Fichou, M. (2017) · Angewandte Chemie International Edition · doi:10.1002/anie.201703783 · Cited by 58
PARP3 is a promoter of chromosomal rearrangements and limits G4 DNA
Day, T. A., Layer, J. V., Cleary, J. P., Guha, S., Stevenson, K. E., Tivey, T. R., Kim, S. S., Schinzel, A. C., Izzo, F., Doench, J. G., et al. (2017) · Nature Communications · doi:10.1038/ncomms15110 · Cited by 43
“Certain malignancies, including those of the stomach and liver, have abundant G4 DNA relative to the surrounding stromal tissue 69 and may therefore be ideal targets for G4 DNA ligands.”
Loop flexibility in human telomeric quadruplex small-molecule complexes
Collie, G. W., Campbell, N. H., & Neidle, S. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv427 · Cited by 45
Small molecule targeting of biologically relevant RNA tertiary and quaternary structures
Zafferani, M., & Hargrove, A. E. (2021) · Cell chemical biology · doi:10.1016/j.chembiol.2021.03.003 · Cited by 56
“Accordingly, small molecule targeting has the potential to lead to selective regulation of the genes associated with riboswitches and yield novel antibacterial and antifungal agents (Blount and Breaker, 2006; Machtel et al., 2016; Panchal and Brenk, 2021).”
Background
Single-molecule fluorescence studies on cotranscriptional G-quadruplex formation coupled with R-loop formation
Lim, G., & Hohng, S. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa695 · Cited by 51
“Consistently, GQ was reported to be formed more abundantly in cancer cells than normal cells (14).”
Background
Binding of Telomestatin, TMPyP4, BSU6037, and BRACO19 to a Telomeric G-Quadruplex–Duplex Hybrid Probed by All-Atom Molecular Dynamics Simulations with Explicit Solvent
Sullivan, H.-J., Readmond, C., Radicella, C., Persad, V., Fasano, T. J., & Wu, C. F. (2018) · ACS Omega · doi:10.1021/acsomega.8b01574 · Cited by 43
Pif1 helicase unfolding of G-quadruplex DNA is highly dependent on sequence and reaction conditions
Byrd, A. K., Bell, M. R., & Raney, K. D. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004499 · Cited by 46
From R-Loops to G-Quadruplexes: Emerging New Threats for the Replication Fork
Maffia, A., Ranise, C., & Sabbioneda, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041506 · Cited by 40
A newly identified berberine derivative induces cancer cell senescence by stabilizing endogenous G-quadruplexes and sparking a DNA damage response at the telomere region
Xiong, Y., Su, H.-F., Lv, P., Ma, Y., Wang, S., Miao, H., Liu, H., Tan, J., Ou, T., Gu, L., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5521 · Cited by 40
“The availability of a new G-quadruplex antibody, BG4, for quantitatively visualizing G-quadruplexes in both cancer cells and tissues has enhanced the attractiveness of this strategy [1, 2].”
Rotaxanes as cages to control DNA binding, cytotoxicity and cellular uptake of a small molecule.
Kench, T., Summers, P. A., Kuimova, M., Lewis, J. E., & Vilar, R. (2020) · Angewandte Chemie · doi:10.26434/chemrxiv.13249643.v1 · Cited by 34
Binding of Telomestatin to a Telomeric G-Quadruplex DNA Probed by All-Atom Molecular Dynamics Simulations with Explicit Solvent
Mulholland, K., & Wu, C. (2016) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.6b00473 · Cited by 34
A sodium/potassium switch for G4-prone G/C-rich sequences
Luo, Y., Živković, M. L., Wang, J.-W., Ryneš, J., Foldynová-Trantírková, S., Trantírek, L., Verga, D., & Mergny, J. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1073 · Cited by 33
“This result is surprising, given that cancer cells seem to exhibit more G4s, as shown by BG4 antibody immunostaining experiments ( 10 ) .”
Background
The G-quadruplex fluorescent probe 3,6-bis(1-methyl-2-vinyl-pyridinium) carbazole diiodide as a biosensor for human cancers
Tseng, T., Chen, W., Chu, I.-T., Wang, C., Chang, C., Lin, M., Lou, P., & Chang, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-34378-8 · Cited by 47
The dual role and mutual dependence of heme/HO-1/Bach1 axis in the carcinogenic and anti-carcinogenic intersection
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“Compared to normal cells, cancer cells can tolerate the accumulation of labile heme in the nucleus (Biffi et al. 2014) and exhibit a higher activity of heme-containing proteins and a more significant concentration of heme (Fiorito et al.”
Background
The Cellular Functions and Molecular Mechanisms of G-Quadruplex Unwinding Helicases in Humans
Liu, Y., Zhu, X., Wang, K., Zhang, B., & Qiu, S. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.783889 · Cited by 28
“In addition, different cell states can influence the formation of G4s; for example, the levels of G4 structures are higher in cancer cells compared to healthy cells (Biffi et al., 2014; Hänsel-Hertsch et al., 2016).”
Background
Spotlight on G-Quadruplexes: From Structure and Modulation to Physiological and Pathological Roles
dell’Oca, M. C., Quadri, R., Bernini, G. M., Menin, L., Grasso, L., Rondelli, D., Yazici, O., Sertic, S., Marini, F., Pellicioli, A., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063162 · Cited by 35
“Remarkably, global G-quadruplex levels are generally higher in tumor or immortalized cells than in normal ones [85,339].”
Background
On the interaction of an anticancer trisubstituted naphthalene diimide with G-quadruplexes of different topologies: a structural insight
Platella, C., Trajkovski, M., Doria, F., Freccero, M., Plavec, J., & Montesarchio, D. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1001 · Cited by 29
Crossroads of telomere biology and anticancer drug discovery
Seimiya, H. (2020) · Cancer Science · doi:10.1111/cas.14540 · Cited by 38
Novel splicing in IGFN1 intron 15 and role of stable G-quadruplex in the regulation of splicing in renal cell carcinoma
Verma, S. P., & Das, P. K. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205660 · Cited by 31
A Cyanine Dye for Highly Specific Recognition of Parallel G-Quadruplex Topology and Its Application in Clinical RNA Detection for Cancer Diagnosis.
Sun, H.-X., Sun, R., Yang, D., Li, Q., Jiang, W.-N., Zhou, T.-X., Bai, R.-Y., Zhong, F., Zhang, B., Xiang, J.-F., et al. (2024) · Journal of the American Chemical Society · doi:10.1021/jacs.4c07698 · Cited by 26
Differential responses of neurons, astrocytes, and microglia to G-quadruplex stabilization
Tabor, N., Ngwa, C., Mitteaux, J., Meyer, M. D., Moruno-Manchon, J. F., Zhu, L., Liu, F., Monchaud, D., McCullough, L. D., & Tsvetkov, A. S. (2021) · Aging · doi:10.18632/aging.203222 · Cited by 25
“10,000 QFS) and varied between cancerous and non-cancerous tissues and between cancer cell lines, demonstrating a cell type–specific G4-DNA landscape [9, 10].”
Background
Trifunctionalized Naphthalene Diimides and Dimeric Analogues as G-Quadruplex-Targeting Anticancer Agents Selected by Affinity Chromatography
Platella, C., Pirota, V., Musumeci, D., Rizzi, F., Iachettini, S., Zizza, P., Biroccio, A., Freccero, M., Montesarchio, D., & Doria, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21061964 · Cited by 25
Binding modes and pathway of RHPS4 to human telomeric G-quadruplex and duplex DNA probed by all-atom molecular dynamics simulations with explicit solvent
Mulholland, K. A., Farzana, S., & Wu, C. F. (2017) · Physical Chemistry Chemical Physics · doi:10.1039/c7cp03313c · Cited by 33
UV-induced G4 DNA structures recruit ZRF1 which prevents UV-induced senescence
Magis, A. D., Limmer, M., Mudiyam, V., Monchaud, D., Juranek, S., & Paeschke, K. (2023) · Nature Communications · doi:10.1038/s41467-023-42494-x · Cited by 25
G-Quadruplex Structures Are Key Modulators of Somatic Structural Variants in Cancers
Zhang, R., Shu, H., Wang, Y., Tao, T., Tu, J., Wang, C., Mergny, J., & Sun, X. S. (2023) · Cancer Research · doi:10.1158/0008-5472.can-22-3089 · Cited by 31
“Notably, a previous study has con ﬁ rmed the presence of G4 structures in cancer cells using BG4 antibody – staining techniques (57), and the authors speculated that these G4s may be associated with genomic instability.”
Fanconi Anemia Pathway in Colorectal Cancer: A Novel Opportunity for Diagnosis, Prognosis and Therapy
Parsa, F. G., Nobili, S., Karimpour, M., Aghdaei, H. A., Mojarad, E. N., & Mini, E. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12030396 · Cited by 21
“The increased level of G-quadruplex structures has been diagnosed in various cancers that underlie genomic instability [57,58].”
Background
Molecular Dynamics Study on the Binding of an Anticancer DNA G‑Quadruplex Stabilizer, CX-5461, to Human Telomeric, c‑KIT1, and c‑Myc G-Quadruplexes and a DNA Duplex
Sullivan, H.-J., Chen, B., & Wu, C. F. (2020) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.0c00632 · Cited by 28
Stable bulged G-quadruplexes in the human genome: identification, experimental validation and functionalization
Papp, C., Mukundan, V. T., Jenjaroenpun, P., Winnerdy, F. R., Ow, G. S., Phan, A. T., & Kuznetsov, V. A. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad252 · Cited by 23
“These pG4-BS are co-localized with experimentally-defined G4 signals (G4-seq (14,51,75), RLFS clusters (14,51,75), CpG islands, and ENCODE promoter-like elements (TF binding sites).”
Background
A label-free fluorescent probe for accurate mitochondrial G-quadruplex structures tracking via assembly hindered rotation induced emission
Yu, K.-K., Li, K., He, H.-Z., Liu, Y.-H., Bao, J.-K., & Yu, X.-Q. (2020) · doi:10.1016/j.snb.2020.128479 · Cited by 23
A triple stranded G-quadruplex formation in the promoter region of human myosin β(Myh7)gene
Singh, A., & Kukreti, S. (2017) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2017.1374211 · Cited by 27
Identification of G-Quadruplex-Binding Inhibitors of Myc Expression through Affinity Selection–Mass Spectrometry
Flusberg, D. A., Rizvi, N. F., Kutilek, V. D., Andrews, C. L., Saradjian, P., Chamberlin, C., Curran, P., Swalm, B. M., Kattar, S. D., Smith, G. F., et al. (2018) · SLAS DISCOVERY · doi:10.1177/2472555218796656 · Cited by 27
G-quadruplex-mediated genomic instability drives SNVs in cancer
Richl, T., Kuper, J., & Kisker, C. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae098 · Cited by 20
“Additionally, G-rich sequences, like G4 motifs, are prone to oxidative DNA damage, which can lead to mutations if not repaired properly ( 76 ).”
BackgroundInfluential
Development of a near-infrared fluorescent ligand that visualizes and stabilizes G-quadruplexes by decorating the triphenylamine scaffold
Wang, X., Yu, B.-Y., Lin, J.-H., Yan, Y., & Hu, M.-H. (2021) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2020.129391 · Cited by 27
Flexible RuII Schiff Base Complexes: G‐Quadruplex DNA Binding and Photo‐Induced Cancer Cell Death
Gillard, M., Weynand, J., Bonnet, H., Loiseau, F., Decottignies, A., Dejeu, J., Defrancq, É., & Elias, B. (2020) · Chemistry - A European Journal · doi:10.1002/chem.202001409 · Cited by 28
G-quadruplex structures regulate long-range transcriptional reprogramming to promote drug resistance in ovarian cancer cells
Robinson, J., Flint, G., Garner, I., Galli, S., Maher, T. E., Kuimova, M. K., Vilar, R., McNeish, I. A., Brown, R. E., Keun, H. C., et al. (2025) · Genome biology · doi:10.1186/s13059-025-03654-y · Cited by 22
Frontiers in G‐Quadruplex therapeutics in cancer: Selection of small molecules, peptides and aptamers
Banerjee, N., Panda, S., & Chatterjee, S. (2021) · Chemical Biology & Drug Design · doi:10.1111/cbdd.13910 · Cited by 26
Fundamentals of G-quadruplex biology
Johnson, F. B. (2020) · Annual reports in medicinal chemistry · doi:10.1016/bs.armc.2020.06.004 · Cited by 29
“Furthermore, studies with the BG4 antibody suggests that G4 levels may be higher in some types of cancer cells.(46,202) Although more evi-”
Binding of anticancer drug daunomycin to a TGGGGT G-quadruplex DNA probed by all-atom molecular dynamics simulations: additional pure groove binding mode and implications on designing more selective G-quadruplex ligands
Shen, Z., Mulholland, K. A., Zheng, Y. G., & Wu, C. F. (2017) · Journal of Molecular Modeling · doi:10.1007/s00894-017-3417-6 · Cited by 24
Discovery of Small Molecules for Repressing Cap-Independent Translation of Human Vascular Endothelial Growth Factor (hVEGF) as Novel Antitumor Agents
Wang, S., Wu, Y., Wang, X., Kuang, G., Zhang, Q., Lin, S., Liu, H., Tan, J., Huang, Z., & Ou, T. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b01444 · Cited by 19
G-quadruplexes as pivotal components of cis-regulatory elements in the human genome
Zhang, R., Wang, Y., Wang, C., Sun, X. S., & Mergny, J. (2024) · BMC Biology · doi:10.1186/s12915-024-01971-5 · Cited by 21
“We then investigated whether G4-associated cCREs are more inclined to be activated in cancer cells, given the higher levels of G4s in cancer tissues compared to non-malignant tissues [7, 37].”
Background
Side-by-side comparison of G-quadruplex (G4) capture efficiency of the antibody BG4 versus the small-molecule ligands TASQs
Feng, Y., He, Z., Luo, Z., Sperti, F. R., Valverde, I. E., Zhang, W., & Monchaud, D. (2023) · iScience · doi:10.1016/j.isci.2023.106846 · Cited by 22
Activation-induced cytidine deaminase localizes to G-quadruplex motifs at mutation hotspots in lymphoma
Xu, Y.-Z., Jenjaroenpun, P., Wongsurawat, T., Byrum, S. D., Shponka, V., Tannahill, D., Chavez, E. A., Hung, S. S., Steidl, C., Balasubramanian, S., et al. (2020) · NAR Cancer · doi:10.1093/narcan/zcaa029 · Cited by 22
“the single-chain Fv BG4 antibody (38,54) to develop a semiautomated colorimetric IHC protocol.”
BackgroundMethodSelf-citation
Enrichment of G4DNA and a Large Inverted Repeat Coincide in the Mitochondrial Genomes of Termitomyces
Nieuwenhuis, M., van de Peppel, L. V. D., Bakker, F., Zwaan, B., & Aanen, D. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz122 · Cited by 17
Alternative paths to telomere elongation
Lee, J., Lee, J., & Lee, H. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.11.003 · Cited by 18
Predicting G-Quadruplexes from DNA Sequences Using Multi-Kernel Convolutional Neural Networks
Barshai, M., & Orenstein, Y. (2019) · ACM International Conference on Bioinformatics, Computational Biology and Biomedicine · doi:10.1145/3307339.3342133 · Cited by 16
“Recent studies using immunofluorescence to visualize G4s revealed their active formation in human cells and tissues and highlighted potential functional implications of these structures in diseases such as cancer [3, 4, 16].”
Background
Naphthalene diimide-polyamine hybrids as antiproliferative agents: Focus on the architecture of the polyamine chains.
Milelli, A., Marchetti, C., Greco, M., Moraca, F., Costa, G., Turrini, E., Catanzaro, E., Betari, N., Calcabrini, C., Sissi, C., et al. (2017) · European journal of medicinal chemistry · doi:10.1016/j.ejmech.2017.01.025 · Cited by 16
Multi-faceted attributes of salivary cell-free DNA as liquid biopsy biomarkers for gastric cancer detection
Swarup, N., Cheng, J. C., Choi, I. F., Heo, Y. J., Kordi, M., Aziz, M. A., Arora, A., Li, F., Chia, D., Fang, W., et al. (2023) · Biomarker Research · doi:10.1186/s40364-023-00524-2 · Cited by 18
“[30] It has been noted that there is an increased retention of G-quadruplex structures in cancer cells, especially GC cells, [52, 53] while plasma cfDNA demonstrates reduced G-quadruplex structures in cancers [17].”
Background
Pirh2-dependent DNA damage in neurons induced by the G-quadruplex ligand pyridostatin
Escarcega, R. D., Patil, A. A., Moruno-Manchon, J. F., Urayama, A., Marrelli, S. P., Kim, N., Monchaud, D., McCullough, L. D., & Tsvetkov, A. S. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105157 · Cited by 20
“Analyses of “ active ” G4-DNA structures revealed that G4 landscapes differ between cell types (13, 14), and these G4 landscapes are regulated by G4-DNA-binding proteins and G4-DNA helicases (3, 4).”
Background
G-quadruplex ligands as potent regulators of lysosomes
Ferret, L., Alvarez-Valadez, K., Rivière, J., Müller, A., Bohálová, N., Luo, Y., Guittat, L., Brázda, V., Kroemer, G., Mergny, J., et al. (2023) · Autophagy · doi:10.1080/15548627.2023.2170071 · Cited by 17
“The number of G4 actually formed within the genome at a given time is probably much lower and may depend on DNA sequence [17], the phase of the cell cycle or on malignant transformation [18].”
Background

Authors: Biffi, G., Tannahill, D., Miller, J., Howat, W. J., & Balasubramanian, S.
Affiliations: University of Cambridge (GB)
Corresponding author: Balasubramanian, Shankar
ORCID: Biffi, Giulia
Tannahill, David
Miller, Jodi
Howat, William J.
Balasubramanian, Shankar
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-07-17
Volume: 9
Issue: 7
Pages: e102711
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0102711
PMC: PMC4102534
OpenAlex: W2100966371
Cited by: 223
References: 34
Citations by year: 2026: 8 · 2025: 17 · 2024: 27 · 2023: 31 · 2022: 20 · 2021: 30 · 2020: 25 · 2019: 15 · 2018: 14 · 2017: 17 · 2016: 7 · 2015: 10 · 2014: 2
FWCI: 4.92
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Figshare (submittedVersion, cc-by)
Funders: Cancer Research UK (11961, A11961, 12488, 22310, C9681/A11961)
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
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Keywords: G-quadruplex, G-quadruplex formation, immunohistochemistry, gastric cancer, liver cancer, tumor markers, DNA secondary structure, patient-derived tissue
MeSH terms: DNA, Gastric Mucosa, Humans, Immunohistochemistry, Liver, Liver Neoplasms, Stomach Neoplasms, Cell Line, Tumor, G-Quadruplexes

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Elevated Levels of G-Quadruplex Formation in Human Stomach and Liver Cancer Tissues

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