Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect
ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

A Small Molecule That Represses Translation of G-Quadruplex-Containing mRNA

View Author Information
† ‡ Institute for Integrated Cell-Material Sciences (WPI-iCeMS) and Institute for Chemical Research, Kyoto University, Uji, Kyoto 611-0011, Japan
§Center for the Promotion of Excellence in Higher Education and Department of Chemistry, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan
Graduate School of Science and Technology, Hirosaki University, Hirosaki, Aomori 036-8561, Japan
Cite this: J. Am. Chem. Soc. 2016, 138, 29, 9037–9040
Publication Date (Web):July 13, 2016
https://doi.org/10.1021/jacs.6b04506
Copyright © 2016 American Chemical Society

    Article Views

    5560

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (1)»

    Abstract

    Abstract Image

    The G-quadruplexes form highly stable nucleic acid structures, which are implicated in various biological processes in both DNA and RNA. Although DNA G-quadruplexes have been studied in great detail, biological roles of RNA G-quadruplexes have received less attention. Here, a screening of a chemical library permitted identification of a small-molecule tool that binds selectively to RNA G-quadruplex structures. The polyaromatic molecule, RGB-1, stabilizes RNA G-quadruplex, but not DNA versions or other RNA structures. RGB-1 intensified the G-quadruplex-mediated inhibition of RNA translation in mammalian cells, decreased expression of the NRAS proto-oncogene in breast cancer cells, and permitted identification of a novel sequence that forms G-quadruplex in NRAS mRNA. RGB-1 may serve as a unique tool for understanding cellular roles of RNA G-quadruplex structures.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/jacs.6b04506.

    • Experimental details and data (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 78 publications.

    1. Jaskirat Kaur, Akanksha Sharma, Poonam Mundlia, Vikas Sood, Ankur Pandey, Gurpal Singh, Ravi Pratap Barnwal. RNA–Small-Molecule Interaction: Challenging the “Undruggable” Tag. Journal of Medicinal Chemistry 2024, 67 (6) , 4259-4297. https://doi.org/10.1021/acs.jmedchem.3c01354
    2. Rajesh Kumar Patidar, Khushboo Tiwari, Ratnesh Tiwari, Nihar Ranjan. Promoter G-Quadruplex Binding Styryl Benzothiazolium Derivative for Applications in Ligand Affinity Ranking and as Ethidium Bromide Substitute in Gel Staining. ACS Applied Bio Materials 2023, 6 (6) , 2196-2210. https://doi.org/10.1021/acsabm.3c00060
    3. Soma Roy, Bappa Maiti, Nilanjan Banerjee, Mangesh H. Kaulage, Kalappa Muniyappa, Subhrangsu Chatterjee, Santanu Bhattacharya. New Xanthone Derivatives as Potent G-Quadruplex Binders for Developing Anti-Cancer Therapeutics. ACS Pharmacology & Translational Science 2023, 6 (4) , 546-566. https://doi.org/10.1021/acsptsci.2c00205
    4. Xiu-Cai Chen, Gui-Xue Tang, Jing Dai, Le-Tian Dai, Tian-Ying Wu, Wen-Wei Li, Tian-Miao Ou, Zhi-Shu Huang, Jia-Heng Tan, Shuo-Bin Chen. Discovery of Clinically Used Octenidine as NRAS Repressor That Effectively Inhibits NRAS-Mutant Melanoma. Journal of Medicinal Chemistry 2023, 66 (7) , 5171-5184. https://doi.org/10.1021/acs.jmedchem.3c00094
    5. Farzad Zamani, Takayoshi Suzuki. Synthetic RNA Modulators in Drug Discovery. Journal of Medicinal Chemistry 2021, 64 (11) , 7110-7155. https://doi.org/10.1021/acs.jmedchem.1c00154
    6. Soma Roy, Asfa Ali, Santanu Bhattacharya. Theoretical Insight into the Library Screening Approach for Binding of Intermolecular G-Quadruplex RNA and Small Molecules through Docking and Molecular Dynamics Simulation Studies. The Journal of Physical Chemistry B 2021, 125 (21) , 5489-5501. https://doi.org/10.1021/acs.jpcb.0c10991
    7. Yi-de He, Ke-wei Zheng, Cui-jiao Wen, Xin-min Li, Jia-yuan Gong, Yu-hua Hao, Yong Zhao, Zheng Tan. Selective Targeting of Guanine-Vacancy-Bearing G-Quadruplexes by G-Quartet Complementation and Stabilization with a Guanine–Peptide Conjugate. Journal of the American Chemical Society 2020, 142 (26) , 11394-11403. https://doi.org/10.1021/jacs.0c00774
    8. Shinzi Ogasawara. Transcription Driven by Reversible Photocontrol of Hyperstable G-Quadruplexes. ACS Synthetic Biology 2018, 7 (11) , 2507-2513. https://doi.org/10.1021/acssynbio.8b00216
    9. Giulia Miglietta, Susanna Cogoi, Jessica Marinello, Giovanni Capranico, Alexander S. Tikhomirov, Andrey Shchekotikhin, and Luigi E. Xodo . RNA G-Quadruplexes in Kirsten Ras (KRAS) Oncogene as Targets for Small Molecules Inhibiting Translation. Journal of Medicinal Chemistry 2017, 60 (23) , 9448-9461. https://doi.org/10.1021/acs.jmedchem.7b00622
    10. Amine Garci, Katherine J. Castor, Johans Fakhoury, Jean-Louis Do, Justin Di Trani, Pongphak Chidchob, Robin S. Stein, Anthony K. Mittermaier, Tomislav Friščić, and Hanadi Sleiman . Efficient and Rapid Mechanochemical Assembly of Platinum(II) Squares for Guanine Quadruplex Targeting. Journal of the American Chemical Society 2017, 139 (46) , 16913-16922. https://doi.org/10.1021/jacs.7b09819
    11. Meng Xu, Dulmi Senanayaka, Rongwei Zhao, Tafadzwa Chigumira, Astha Tripathi, Jason Tones, Rachel M. Lackner, Anne R. Wondisford, Laurel N. Moneysmith, Alexander Hirschi, Sara Craig, Sahar Alishiri, Roderick J. O’Sullivan, David M. Chenoweth, Nicholas J. Reiter, Huaiying Zhang. TERRA-LSD1 phase separation promotes R-loop formation for telomere maintenance in ALT cancer cells. Nature Communications 2024, 15 (1) https://doi.org/10.1038/s41467-024-46509-z
    12. Xiao-Dong Wang, Yong-Si Liu, Ming-Hao Hu. Discovery of an indolium-based, turn-on fluorescent ligand that represses the Neuroblastoma RAS expression by targeting the 5′-UTR G-quadruplex structure. Sensors and Actuators B: Chemical 2024, 408 , 135506. https://doi.org/10.1016/j.snb.2024.135506
    13. Aakriti Singh, Neha Jain, Uma Shankar, Tarun Kumar Sharma, Amit Kumar. Characterization of G-quadruplex structures in genes involved in survival and pathogenesis of Acinetobacter baumannii as a potential drug target. International Journal of Biological Macromolecules 2024, 269 , 131806. https://doi.org/10.1016/j.ijbiomac.2024.131806
    14. Jia-Wei Sun, Jing Zou, Ying Zheng, Hao Yuan, Yuan-Ze-Yu Xie, Xiao-Na Wang, Tian-Miao Ou. Design, synthesis, and evaluation of novel quindoline derivatives with fork-shaped side chains as RNA G-quadruplex stabilizers for repressing oncogene NRAS translation. European Journal of Medicinal Chemistry 2024, 271 , 116406. https://doi.org/10.1016/j.ejmech.2024.116406
    15. Vinodh J. Sahayasheela, Hiroshi Sugiyama. RNA G-quadruplex in functional regulation of noncoding RNA: Challenges and emerging opportunities. Cell Chemical Biology 2024, 31 (1) , 53-70. https://doi.org/10.1016/j.chembiol.2023.08.010
    16. Ritwika Bose, Irfana Saleem, Anthony M. Mustoe. Causes, functions, and therapeutic possibilities of RNA secondary structure ensembles and alternative states. Cell Chemical Biology 2024, 31 (1) , 17-35. https://doi.org/10.1016/j.chembiol.2023.12.010
    17. Francesca Romano, Anna Di Porzio, Nunzia Iaccarino, Gelsomina Riccardi, Ritamaria Di Lorenzo, Sonia Laneri, Bruno Pagano, Jussara Amato, Antonio Randazzo. G-quadruplexes in cancer-related gene promoters: from identification to therapeutic targeting. Expert Opinion on Therapeutic Patents 2023, 33 (11) , 745-773. https://doi.org/10.1080/13543776.2023.2271168
    18. Václav Brázda, Jean-Louis Mergny. Quadruplexes and aging: G4-binding proteins regulate the presence of miRNA in small extracellular vesicles (sEVs). Biochimie 2023, 214 , 69-72. https://doi.org/10.1016/j.biochi.2023.01.014
    19. Yicong Dai, Xucong Teng, Qiushuang Zhang, Hongwei Hou, Jinghong Li. Advances and challenges in identifying and characterizing G-quadruplex–protein interactions. Trends in Biochemical Sciences 2023, 48 (10) , 894-909. https://doi.org/10.1016/j.tibs.2023.06.007
    20. Akanksha Pandey, Sarupa Roy, Seergazhi G. Srivatsan. Probing the Competition between Duplex, G‐Quadruplex and i‐Motif Structures of the Oncogenic c‐Myc DNA Promoter Region. Chemistry – An Asian Journal 2023, 18 (17) https://doi.org/10.1002/asia.202300510
    21. Maria Razzaq, Ji Ho Han, Subramaniyam Ravichandran, Jaehyun Kim, Joon-Yong Bae, Man-Seong Park, Shrute Kannappan, Woo-Chang Chung, Jin-Hyun Ahn, Moon Jung Song, Kyeong Kyu Kim. Stabilization of RNA G-quadruplexes in the SARS-CoV-2 genome inhibits viral infection via translational suppression. Archives of Pharmacal Research 2023, 46 (7) , 598-615. https://doi.org/10.1007/s12272-023-01458-x
    22. Sefan Asamitsu, Yasushi Yabuki, Kazuya Matsuo, Moe Kawasaki, Yuki Hirose, Gengo Kashiwazaki, Anandhakumar Chandran, Toshikazu Bando, Dan Ohtan Wang, Hiroshi Sugiyama, Norifumi Shioda. RNA G-quadruplex organizes stress granule assembly through DNAPTP6 in neurons. Science Advances 2023, 9 (8) https://doi.org/10.1126/sciadv.ade2035
    23. Helen L. Lightfoot, Graham F. Smith. Targeting RNA with small molecules—A safety perspective. British Journal of Pharmacology 2023, https://doi.org/10.1111/bph.16027
    24. Prakash Kharel, Pavel Ivanov. Structure and Functions of RNA G-quadruplexes. 2023, 183-203. https://doi.org/10.1007/978-3-031-36390-0_9
    25. Shuqi Chen, Daniel L. Priebbenow, Julie Somkhit, Carmen V. Scullino, Keli Agama, Yves Pommier, Bernard L. Flynn. Alkyne Activation in the Diversity Oriented Synthesis of sp 2 ‐Rich Scaffolds: A Biased Library Approach for Targeting Polynucleotides (DNA/RNA). Chemistry – A European Journal 2022, 28 (71) https://doi.org/10.1002/chem.202201925
    26. Payal Gupta, Rushikesh M. Khadake, Shounok Panja, Krushna Shinde, Ambadas B. Rode. Alternative RNA Conformations: Companion or Combatant. Genes 2022, 13 (11) , 1930. https://doi.org/10.3390/genes13111930
    27. Loukiani Savva, Mathieu Fossépré, Odysseas Keramidas, Alexandros Themistokleous, Natalia Rizeq, Nikos Panagiotou, Maxime Leclercq, Eliana Nicolaidou, Mathieu Surin, Sophia C. Hayes, Savvas N. Georgiades. Gaining Insights on the Interactions of a Class of Decorated (2‐([2,2′‐Bipyridin]‐6‐yl)phenyl)platinum Compounds with c‐Myc Oncogene Promoter G‐Quadruplex and Other DNA Structures. Chemistry – A European Journal 2022, 28 (54) https://doi.org/10.1002/chem.202201497
    28. Yousuke Katsuda, Shin-ichi Sato, Maimi Inoue, Hisashi Tsugawa, Takuto Kamura, Tomoki Kida, Rio Matsumoto, Sefan Asamitsu, Norifumi Shioda, Shuhei Shiroto, Yoshiki Oosawatsu, Kenji Yatsuzuka, Yusuke Kitamura, Masaki Hagihara, Toshihiro Ihara, Motonari Uesugi. Small molecule-based detection of non-canonical RNA G-quadruplex structures that modulate protein translation. Nucleic Acids Research 2022, 50 (14) , 8143-8153. https://doi.org/10.1093/nar/gkac580
    29. Martina Zafferani, Dhanasheel Muralidharan, Nadeska I. Montalvan, Amanda E. Hargrove. RT-qPCR as a screening platform for mutational and small molecule impacts on structural stability of RNA tertiary structures. RSC Chemical Biology 2022, 3 (7) , 905-915. https://doi.org/10.1039/D2CB00015F
    30. Lei Liu, Wei Zhang, Ming-Qing Zhong, Meng-Hao Jia, Fei Jiang, Yan Zhang, Chao-Da Xiao, Xin Xiao, Xiang-Chun Shen. Tetraphenylethene derivative that discriminates parallel G-quadruplexes. RSC Advances 2022, 12 (23) , 14765-14775. https://doi.org/10.1039/D2RA01433E
    31. Jia-Hong Lin, Xiao Chen, Ming-Hao Hu. Detection of G-quadruplex structures with a minimalistic crescent-shaped carbazole-indolium ligand. Sensors and Actuators B: Chemical 2022, 358 , 131498. https://doi.org/10.1016/j.snb.2022.131498
    32. Joanna R Kovalski, Duygu Kuzuoglu‐Ozturk, Davide Ruggero. Protein synthesis control in cancer: selectivity and therapeutic targeting. The EMBO Journal 2022, 41 (8) https://doi.org/10.15252/embj.2021109823
    33. Xucong Teng, Yicong Dai, Jinghong Li. Methodological advances of bioanalysis and biochemical targeting of intracellular G‐quadruplexes. Exploration 2022, 2 (2) https://doi.org/10.1002/EXP.20210214
    34. Alessio Cantara, Yu Luo, Michaela Dobrovolná, Natalia Bohalova, Miroslav Fojta, Daniela Verga, Lionel Guittat, Anne Cucchiarini, Solène Savrimoutou, Cécile Häberli, Jean Guillon, Jennifer Keiser, Václav Brázda, Jean Louis Mergny. G-quadruplexes in helminth parasites. Nucleic Acids Research 2022, 50 (5) , 2719-2735. https://doi.org/10.1093/nar/gkac129
    35. Eduarda Mendes, Israa M. Aljnadi, Bárbara Bahls, Bruno L. Victor, Alexandra Paulo. Major Achievements in the Design of Quadruplex-Interactive Small Molecules. Pharmaceuticals 2022, 15 (3) , 300. https://doi.org/10.3390/ph15030300
    36. Zhiguo Wang, Baofeng Yang. Polypharmacology in Drug Design and Discovery—Basis for Rational Design of Multitarget Drugs. 2022, 397-533. https://doi.org/10.1007/978-3-031-04998-9_12
    37. Xiao-Xia Hu, Sheng-Quan Wang, Shi-Quan Gan, Lei Liu, Ming-Qing Zhong, Meng-Hao Jia, Fei Jiang, Yan Xu, Chao-Da Xiao, Xiang-Chun Shen. A Small Ligand That Selectively Binds to the G-quadruplex at the Human Vascular Endothelial Growth Factor Internal Ribosomal Entry Site and Represses the Translation. Frontiers in Chemistry 2021, 9 https://doi.org/10.3389/fchem.2021.781198
    38. Tiago Santos, Gilmar F. Salgado, Eurico J. Cabrita, Carla Cruz. G-Quadruplexes and Their Ligands: Biophysical Methods to Unravel G-Quadruplex/Ligand Interactions. Pharmaceuticals 2021, 14 (8) , 769. https://doi.org/10.3390/ph14080769
    39. Sefan Asamitsu, Norifumi Shioda. Potential roles of G-quadruplex structures in RNA granules for physiological and pathological phase separation. The Journal of Biochemistry 2021, 169 (5) , 527-533. https://doi.org/10.1093/jb/mvab018
    40. Victoria Sanchez-Martin, Miguel Soriano, Jose Antonio Garcia-Salcedo. Quadruplex Ligands in Cancer Therapy. Cancers 2021, 13 (13) , 3156. https://doi.org/10.3390/cancers13133156
    41. Jared T. Baisden, Jessica L. Childs-Disney, Lucas S. Ryan, Matthew D. Disney. Affecting RNA biology genome-wide by binding small molecules and chemically induced proximity. Current Opinion in Chemical Biology 2021, 62 , 119-129. https://doi.org/10.1016/j.cbpa.2021.03.006
    42. Martina Zafferani, Amanda E. Hargrove. Small molecule targeting of biologically relevant RNA tertiary and quaternary structures. Cell Chemical Biology 2021, 28 (5) , 594-609. https://doi.org/10.1016/j.chembiol.2021.03.003
    43. Kazumitsu Onizuka, Erchissaran Ganbold, Yue Ma, Shogo Sasaki, Madoka E. Hazemi, Yutong Chen, Norihiro Sato, Mamiko Ozawa, Kazuo Nagasawa, Fumi Nagatsugi. Selective alkylation of parallel G-quadruplex structure. Organic & Biomolecular Chemistry 2021, 19 (13) , 2891-2894. https://doi.org/10.1039/D0OB02365E
    44. Pauline Lejault, Jérémie Mitteaux, Francesco Rota Sperti, David Monchaud. How to untie G-quadruplex knots and why?. Cell Chemical Biology 2021, 28 (4) , 436-455. https://doi.org/10.1016/j.chembiol.2021.01.015
    45. Loukiani Savva, Savvas N. Georgiades. Recent Developments in Small-Molecule Ligands of Medicinal Relevance for Harnessing the Anticancer Potential of G-Quadruplexes. Molecules 2021, 26 (4) , 841. https://doi.org/10.3390/molecules26040841
    46. Dorota Gudanis, Damian Kaniowski, Katarzyna Kulik, Daniel Baranowski, Zofia Gdaniec, Barbara Nawrot. Formation of an RNA Quadruplex-Duplex Hybrid in Living Cells between mRNA of the Epidermal Growth Factor Receptor (EGFR) and a G-Rich Antisense Oligoribonucleotide. Cells 2020, 9 (11) , 2375. https://doi.org/10.3390/cells9112375
    47. Ai-Ming Yu, Young Hee Choi, Mei-Juan Tu, . RNA Drugs and RNA Targets for Small Molecules: Principles, Progress, and Challenges. Pharmacological Reviews 2020, 72 (4) , 862-898. https://doi.org/10.1124/pr.120.019554
    48. Josué Carvalho, Jean-Louis Mergny, Gilmar F. Salgado, João A. Queiroz, Carla Cruz. G-quadruplex, Friend or Foe: The Role of the G-quartet in Anticancer Strategies. Trends in Molecular Medicine 2020, 26 (9) , 848-861. https://doi.org/10.1016/j.molmed.2020.05.002
    49. Vyankat A. Sontakke, Seergazhi G. Srivatsan. A dual-app nucleoside probe reports G-quadruplex formation and ligand binding in the long terminal repeat of HIV-1 proviral genome. Bioorganic & Medicinal Chemistry Letters 2020, 30 (16) , 127345. https://doi.org/10.1016/j.bmcl.2020.127345
    50. Lukasz Ciszewski, Ngoc Lu-Nguyen, Alex Slater, Andrew Brennan, Huw E L Williams, George Dickson, Mark S Searle, Linda Popplewell. G-quadruplex ligands mediate downregulation of DUX4 expression. Nucleic Acids Research 2020, 48 (8) , 4179-4194. https://doi.org/10.1093/nar/gkaa146
    51. Takuto Kamura, Yousuke Katsuda, Yusuke Kitamura, Toshihiro Ihara. G-quadruplexes in mRNA: A key structure for biological function. Biochemical and Biophysical Research Communications 2020, 526 (1) , 261-266. https://doi.org/10.1016/j.bbrc.2020.02.168
    52. Ken-ichi Fujita, Takaki Ishizuka, Mizuki Mitsukawa, Masashi Kurata, Seiji Masuda. Regulating Divergent Transcriptomes through mRNA Splicing and Its Modulation Using Various Small Compounds. International Journal of Molecular Sciences 2020, 21 (6) , 2026. https://doi.org/10.3390/ijms21062026
    53. Prakash Kharel, Sumirtha Balaratnam, Nathan Beals, Soumitra Basu. The role of RNA G‐quadruplexes in human diseases and therapeutic strategies. WIREs RNA 2020, 11 (1) https://doi.org/10.1002/wrna.1568
    54. Sefan Asamitsu. Introduction. 2020, 1-44. https://doi.org/10.1007/978-981-15-7716-1_1
    55. Luigi E. Xodo. Quadruplex nucleic acids in KRAS targeted-cancer therapy. 2020, 325-359. https://doi.org/10.1016/bs.armc.2020.04.004
    56. Valentina Pirota, Michele Stasi, Alessandra Benassi, Filippo Doria. An overview of quadruplex ligands: Their common features and chemotype diversity. 2020, 163-196. https://doi.org/10.1016/bs.armc.2020.04.008
    57. F. Brad Johnson. Fundamentals of G-quadruplex biology. 2020, 3-44. https://doi.org/10.1016/bs.armc.2020.06.004
    58. Jingqi Chen, Yingying Chen, Lijuan Zhao, Lingyan Feng, Feifei Xing, Chuanqi Zhao, Lianzhe Hu, Jinsong Ren, Xiaogang Qu. G-quadruplex DNA regulates invertible circularly polarized luminescence. Journal of Materials Chemistry C 2019, 7 (44) , 13947-13952. https://doi.org/10.1039/C9TC04508B
    59. Miss Sui-Qi Cheng, Miss Xiao-Xuan Su, Miss Xiao-Na Wang, Miss Zhi-Yin Sun, Tian-Miao Ou. Probes and drugs that interfere with protein translation via targeting to the RNAs or RNA-protein interactions. Methods 2019, 167 , 124-133. https://doi.org/10.1016/j.ymeth.2019.06.004
    60. Yanfang Song, Qing Lin, Zhaolian Cai, Taisen Hao, Yaohan Zhang, Xianjin Zhu. Cysteine‐rich protein 61 regulates the chemosensitivity of chronic myeloid leukemia to imatinib mesylate through the nuclear factor kappa B/Bcl‐2 pathway. Cancer Science 2019, 110 (8) , 2421-2430. https://doi.org/10.1111/cas.14083
    61. Ashok Nuthanakanti, Ishtiyaq Ahmed, Saddam Y Khatik, Kayarat Saikrishnan, Seergazhi G Srivatsan. Probing G-quadruplex topologies and recognition concurrently in real time and 3D using a dual-app nucleoside probe. Nucleic Acids Research 2019, 47 (12) , 6059-6072. https://doi.org/10.1093/nar/gkz419
    62. Jing Zhang, Samuel E Harvey, Chonghui Cheng. A high-throughput screen identifies small molecule modulators of alternative splicing by targeting RNA G-quadruplexes. Nucleic Acids Research 2019, 47 (7) , 3667-3679. https://doi.org/10.1093/nar/gkz036
    63. Sefan Asamitsu, Toshikazu Bando, Hiroshi Sugiyama. Ligand Design to Acquire Specificity to Intended G‐Quadruplex Structures. Chemistry – A European Journal 2019, 25 (2) , 417-430. https://doi.org/10.1002/chem.201802691
    64. Xuedong Li, Bo Chen, Ling Lan, Ruili Wang, Duqiang Luo, Li Liu, Liang Cheng. Selective recognition of HIV RNA by dinuclear metallic ligands. Chinese Chemical Letters 2018, 29 (11) , 1637-1640. https://doi.org/10.1016/j.cclet.2018.06.003
    65. Brittany S Morgan, Jordan E Forte, Amanda E Hargrove. Insights into the development of chemical probes for RNA. Nucleic Acids Research 2018, 46 (16) , 8025-8037. https://doi.org/10.1093/nar/gky718
    66. Anita Donlic, Amanda E. Hargrove. Targeting RNA in mammalian systems with small molecules. WIREs RNA 2018, 9 (4) https://doi.org/10.1002/wrna.1477
    67. Tian Tian, Yu-Qi Chen, Shao-Ru Wang, Xiang Zhou. G-Quadruplex: A Regulator of Gene Expression and Its Chemical Targeting. Chem 2018, 4 (6) , 1314-1344. https://doi.org/10.1016/j.chempr.2018.02.014
    68. David R Calabrese, Katherine Zlotkowski, Stephanie Alden, William M Hewitt, Colleen M Connelly, Robert M Wilson, Snehal Gaikwad, Lu Chen, Rajarshi Guha, Craig J Thomas, Beverly A Mock, John S Schneekloth. Characterization of clinically used oral antiseptics as quadruplex-binding ligands. Nucleic Acids Research 2018, 46 (6) , 2722-2732. https://doi.org/10.1093/nar/gky084
    69. Robert W. Harkness, Anthony K. Mittermaier. G-quadruplex dynamics. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2017, 1865 (11) , 1544-1554. https://doi.org/10.1016/j.bbapap.2017.06.012
    70. Tamaki Endoh, Naoki Sugimoto. Conformational Dynamics of mRNA in Gene Expression as New Pharmaceutical Target. The Chemical Record 2017, 17 (9) , 817-832. https://doi.org/10.1002/tcr.201700016
    71. Hong‐Liang Bao, Takumi Ishizuka, Ayaka Iwanami, Takanori Oyoshi, Yan Xu. A Simple and Sensitive 19 F NMR Approach for Studying the Interaction of RNA G‐Quadruplex with Ligand Molecule and Protein. ChemistrySelect 2017, 2 (15) , 4170-4175. https://doi.org/10.1002/slct.201700711
    72. Satyaprakash Pandey, Prachi Agarwala, Souvik Maiti. Targeting RNA G-Quadruplexes for Potential Therapeutic Applications. 2017, 177-206. https://doi.org/10.1007/7355_2016_22
    73. Edward R. Biehl. Five-Membered Ring Systems. 2017, 147-182. https://doi.org/10.1016/B978-0-08-102310-5.00005-9
    74. Zhize Ou, Moheng Xu, Yunyan Gao, Rui Hu, Qingqing Li, Wenjiao Cai, Ziji Wang, Yimeng Qian, Guoqiang Yang. Synthesis, G-quadruplex binding properties and cytotoxicity of naphthalimide–thiourea conjugates. New Journal of Chemistry 2017, 41 (17) , 9397-9405. https://doi.org/10.1039/C7NJ02366A
    75. Zi-Qi Li, Ting-Cong Liao, Cheng Dong, Jian-Wei Yang, Xiao-Jie Chen, Lihong Liu, Yuan Luo, Yuan-Yuan Liang, Wen-Hua Chen, Chun-Qiong Zhou. Specifically targeting mixed-type dimeric G-quadruplexes using berberine dimers. Organic & Biomolecular Chemistry 2017, 15 (48) , 10221-10229. https://doi.org/10.1039/C7OB02326J
    76. Arpita Tawani, Ayeman Amanullah, Amit Mishra, Amit Kumar. Evidences for Piperine inhibiting cancer by targeting human G-quadruplex DNA sequences. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep39239
    77. Anne Cammas, Stefania Millevoi. RNA G-quadruplexes: emerging mechanisms in disease. Nucleic Acids Research 2016, 9 , gkw1280. https://doi.org/10.1093/nar/gkw1280
    78. Jingwen Song, Jean-Pierre Perreault, Ivan Topisirovic, Stéphane Richard. RNA G-quadruplexes and their potential regulatory roles in translation. Translation 2016, 4 (2) , e1244031. https://doi.org/10.1080/21690731.2016.1244031