Skip to main content
SpringerLink
Log in

G-Quadruplexes as Sensors of Intracellular Na+/K+ Ratio: Potential Role in Regulation of Transcription and Translation

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Data on the structure of G-quadruplexes, noncanonical nucleic acid forms, supporting an idea of their potential participation in regulation of gene expression in response to the change in intracellular Na+i/K+i ratio are considered in the review. Structural variety of G-quadruplexes, role of monovalent cations in formation of this structure, and thermodynamic stability of G-quadruplexes are described. Data on the methods of their identification in the cells and biological functions of these structures are presented. Analysis of information about specific interactions of G-quadruplexes with some proteins was conducted, and their potential participation in the development of some pathological conditions, in particular, cancer and neurodegenerative diseases, is considered. Special attention is given to the plausible role of G-quadruplexes as sensors of intracellular Na+i/K+i ratio, because alteration of this parameter affects folding of G-quadruplexes changing their stability and, thereby, organization of the regulatory elements of nucleic acids. The data presented in the conclusion section demonstrate significant change in the expression of some early response genes under certain physiological conditions of cells and tissues depending on the intracellular Na+i/K+i ratio.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

References

  1. Bacolla, A., and Wells, R. D. (2004) Non-B DNA conformations, genomic rearrangements, and human disease, J. Biol. Chem., 279, 47411-47414, https://doi.org/10.1074/jbc.R400028200.

    Article  CAS  PubMed  Google Scholar 

  2. Bochman, M. L., Paeschke, K., and Zakian, V. A. (2012) DNA secondary structures: stability and function of G-quadruplex structures, Nat. Rev. Genet., 13, 770-780, https://doi.org/10.1038/nrg3296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Phan, A. T. (2010) Human telomeric G-quadruplex: structures of DNA and RNA sequences, FEBS J., 277, 1107-1117, https://doi.org/10.1111/j.1742-4658.2009.07464.x.

    Article  CAS  PubMed  Google Scholar 

  4. Davis, J. T. (2004) G-quartets 40 years later: from 5′-GMP to molecular biology and supramolecular chemistry, Angew. Chem. Int. Ed., 43, 668-698, https://doi.org/10.1002/anie.200300589.

    Article  CAS  Google Scholar 

  5. Williamson, J. R., Raghuraman, M. K., and Cech, T. R. (1989) Monovalent cation-induced structure of telomeric DNA: the G-quartet model, Cell, 59, 871-880, https://doi.org/10.1016/0092-8674(89)90610-7.

    Article  CAS  PubMed  Google Scholar 

  6. Zahn, M., Berthold, N., Kieslich, B., Knappe, D., Hoffmann, R., and Sträter, N. (2013) Structural studies on the forward and reverse binding modes of peptides to the chaperone DnaK, J. Mol. Biol., 425, 2463-2479, https://doi.org/10.1016/j.jmb.2013.03.041.

    Article  CAS  PubMed  Google Scholar 

  7. Webba da Silva, M. (2007) Geometric formalism for DNA quadruplex folding, Chem. Weinh. Bergstr. Ger., 13, 9738-9745, https://doi.org/10.1002/chem.200701255.

    Article  CAS  Google Scholar 

  8. Lech, C. J., Heddi, B., and Phan, A. T. (2013) Guanine base stacking in G-quadruplex nucleic acids, Nucleic Acids Res., 41, 2034-2046, https://doi.org/10.1093/nar/gks1110.

    Article  CAS  PubMed  Google Scholar 

  9. Li, X., Zheng, K., Zhang, J., Liu, H., He, Y., Yuan, B., Hao, Y., and Tan, Z. (2015) Guanine-vacancy-bearing G-quadruplexes responsive to guanine derivatives, Proc. Natl. Acad. Sci. USA, 112, 14581-14586, https://doi.org/10.1073/pnas.1516925112.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  10. Marsico, G., Chambers, V. S., Sahakyan, A. B., McCauley, P., Boutell, J. M., Antonio, M. D., and Balasubramanian, S. (2019) Whole genome experimental maps of DNA G-quadruplexes in multiple species, Nucleic Acids Res., 47, 3862-3874, https://doi.org/10.1093/nar/gkz179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rachwal, P. A., Brown, T., and Fox, K. R. (2007) Effect of G-tract length on the topology and stability of intramolecular DNA quadruplexes, Biochemistry, 46, 3036-3044, https://doi.org/10.1021/bi062118j.

    Article  CAS  PubMed  Google Scholar 

  12. Harkness, R. W., and Mittermaier, A. K. (2017) G-quadruplex dynamics, Biochim. Biophys. Acta Proteins Proteomics, 1865, 1544-1554, https://doi.org/10.1016/j.bbapap.2017.06.012.

    Article  CAS  PubMed  Google Scholar 

  13. Ida, R., and Wu, G. (2008) Direct NMR detection of alkali metal ions bound to G-quadruplex DNA, J. Am. Chem. Soc., 130, 3590-3602, https://doi.org/10.1021/ja709975z.

    Article  CAS  PubMed  Google Scholar 

  14. Balaratnam, S., and Basu, S. (2015) Divalent cation-aided identification of physico-chemical properties of metal ions that stabilize RNA g-quadruplexes, Biopolymers, 103, 376-386, https://doi.org/10.1002/bip.22628.

    Article  CAS  PubMed  Google Scholar 

  15. Venczel, E. A., and Sen, D. (1993) Parallel and antiparallel G-DNA structures from a complex telomeric sequence, Biochemistry, 32, 6220-6228, https://doi.org/10.1021/bi00075a015.

    Article  CAS  PubMed  Google Scholar 

  16. Burge, S., Parkinson, G. N., Hazel, P., Todd, A. K., and Neidle, S. (2006) Quadruplex DNA: sequence, topology and structure, Nucleic Acids Res., 34, 5402-5415, https://doi.org/10.1093/nar/gkl655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chung, W. J., Heddi, B., Schmitt, E., Lim, K. W., Mechulam, Y., and Phan, A. T. (2015) Structure of a left-handed DNA G-quadruplex, Proc. Natl. Acad. Sci. USA, 112, 2729-2733, https://doi.org/10.1073/pnas.1418718112.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  18. del Villar-Guerra, R., Trent, J. O., and Chaires, J. B. (2018) G-quadruplex secondary structure obtained from circular dichroism spectroscopy, Angew. Chem. Int. Ed., 57, 7171-7175, https://doi.org/10.1002/anie.201709184.

    Article  CAS  Google Scholar 

  19. Kumari, S., Bugaut, A., Huppert, J. L., and Balasubramanian, S. (2007) An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation, Nat. Chem. Biol., 3, 218-221, https://doi.org/10.1038/nchembio864.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Vorlíčková, M., Kejnovská, I., Sagi, J., Renčiuk, D., Bednářová, K., Motlová, J., and Kypr, J. (2012) Circular dichroism and guanine quadruplexes, Methods San Diego Calif., 57, 64-75, https://doi.org/10.1016/j.ymeth.2012.03.011.

    Article  CAS  PubMed  Google Scholar 

  21. Joachimi, A., Benz, A., and Hartig, J. S. (2009) A comparison of DNA and RNA quadruplex structures and stabilities, Bioorg. Med. Chem., 17, 6811-6815, https://doi.org/10.1016/j.bmc.2009.08.043.

    Article  CAS  PubMed  Google Scholar 

  22. Bang, I. (1910) Studies on guanylic acid [in German], Biochem. Zeitschrift, 26, 293-311.

    CAS  Google Scholar 

  23. Gellert, M., Lipsett, M. N., and Davies, D. R. (1962) Helix formation by guanylic acid, Proc. Natl. Acad. Sci. USA, 48, 2013-2018, https://doi.org/10.1073/pnas.48.12.2013.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  24. Sen, D., and Gilbert, W. (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis, Nature, 334, 364-366, https://doi.org/10.1038/334364a0.

    Article  CAS  PubMed  ADS  Google Scholar 

  25. Mergny, J.-L., and Lacroix, L. (2009) UV melting of G-quadruplexes, Curr. Protoc. Nucleic Acid Chem., 37, 17.1.1-17.1.15, https://doi.org/10.1002/0471142700.nc1701s37.

    Article  Google Scholar 

  26. Huppert, J. L., and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome, Nucleic Acids Res., 33, 2908-2916, https://doi.org/10.1093/nar/gki609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Teng, F.-Y., Jiang, Z.-Z., Guo, M., Tan, X.-Z., Chen, F., Xi, X.-G., and Xu, Y. (2021) G-quadruplex DNA: a novel target for drug design, Cell. Mol. Life Sci. CMLS, 78, 6557-6583, https://doi.org/10.1007/s00018-021-03921-8.

    Article  CAS  PubMed  Google Scholar 

  28. Chambers, V. S., Marsico, G., Boutell, J. M., Di Antonio, M., Smith, G. P., and Balasubramanian, S. (2015) High-throughput sequencing of DNA G-quadruplex structures in the human genome, Nat. Biotechnol., 33, 877-881, https://doi.org/10.1038/nbt.3295.

    Article  CAS  PubMed  Google Scholar 

  29. Schaffitzel, C., Berger, I., Postberg, J., Hanes, J., Lipps, H. J., and Plückthun, A. (2001) In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei, Proc. Natl. Acad. Sci. USA, 98, 8572-8577, https://doi.org/10.1073/pnas.141229498.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  30. Biffi, G., Tannahill, D., McCafferty, J., and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells, Nat. Chem., 5, 182-186, https://doi.org/10.1038/nchem.1548.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Biffi, G., Di Antonio, M., Tannahill, D., and Balasubramanian, S. (2014) Visualization and selective chemical targeting of RNA G-quadruplex structures in the cytoplasm of human cells, Nat. Chem., 6, 75-80, https://doi.org/10.1038/nchem.1805.

    Article  CAS  PubMed  Google Scholar 

  32. Zafferani, M., and Hargrove, A. E. (2021) Small molecule targeting of biologically relevant RNA tertiary and quaternary structures, Cell Chem. Biol., 28, 594-609, https://doi.org/10.1016/j.chembiol.2021.03.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Monchaud, D., and Teulade-Fichou, M.-P. (2008) A Hitchhiker’s guide to G-quadruplex ligands, Org. Biomol. Chem., 6, 627-636, https://doi.org/10.1039/B714772B.

    Article  CAS  PubMed  Google Scholar 

  34. Yang, D., and Okamoto, K. (2010) Structural insights into G-quadruplexes: towards new anticancer drugs, Fut. Med. Chem., 2, 619-646, https://doi.org/10.4155/fmc.09.172.

    Article  CAS  Google Scholar 

  35. Neidle, S. (2010) Human telomeric G-quadruplex: the current status of telomeric G-quadruplexes as therapeutic targets in human cancer, FEBS J., 277, 1118-1125, https://doi.org/10.1111/j.1742-4658.2009.07463.x.

    Article  CAS  PubMed  Google Scholar 

  36. Kim, M.-Y., Vankayalapati, H., Shin-Ya, K., Wierzba, K., and Hurley, L. H. (2002) Telomestatin, a potent telomerase inhibitor that interacts quite specifically with the human telomeric intramolecular G-quadruplex, J. Am. Chem. Soc., 124, 2098-2099, https://doi.org/10.1021/ja017308q.

    Article  CAS  PubMed  Google Scholar 

  37. Sun, D., Thompson, B., Cathers, B. E., Salazar, M., Kerwin, S. M., Trent, J. O., Jenkins, T. C., Neidle, S., and Hurley, L. H. (1997) Inhibition of human telomerase by a G-quadruplex-interactive compound, J. Med. Chem., 40, 2113-2116, https://doi.org/10.1021/jm970199z.

    Article  CAS  PubMed  Google Scholar 

  38. Moore, M. J. B., Schultes, C. M., Cuesta, J., Cuenca, F., Gunaratnam, M., Tanious, F. A., Wilson, W. D., and Neidle, S. (2006) Trisubstituted acridines as G-quadruplex telomere targeting agents. Effects of extensions of the 3,6- and 9-side chains on quadruplex binding, telomerase activity, and cell proliferation, J. Med. Chem., 49, 582-599, https://doi.org/10.1021/jm050555a.

    Article  CAS  PubMed  Google Scholar 

  39. Kern, J. T., Thomas, P. W., and Kerwin, S. M. (2002) The relationship between ligand aggregation and G-quadruplex DNA selectivity in a series of 3,4,9,10-perylenetetracarboxylic acid diimides, Biochemistry, 41, 11379-11389, https://doi.org/10.1021/bi0263107.

    Article  CAS  PubMed  Google Scholar 

  40. De Cian, A., DeLemos, E., Mergny, J.-L., Teulade-Fichou, M.-P., and Monchaud, D. (2007) Highly efficient g-quadruplex recognition by bisquinolinium compounds, J. Am. Chem. Soc., 129, 1856-1857, https://doi.org/10.1021/ja067352b.

    Article  CAS  PubMed  Google Scholar 

  41. Balasubramanian, S., Hurley, L. H., and Neidle, S. (2011) Targeting G-quadruplexes in gene promoters: a novel anticancer strategy? Nat. Rev. Drug Discov., 10, 261-275, https://doi.org/10.1038/nrd3428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Neidle, S. (2016) Quadruplex nucleic acids as novel therapeutic targets, J. Med. Chem., 59, 5987-6011, https://doi.org/10.1021/acs.jmedchem.5b01835.

    Article  CAS  PubMed  Google Scholar 

  43. Wu, S., Wang, L., Zhang, N., Liu, Y., Zheng, W., Chang, A., Wang, F., Li, S., and Shangguan, D. (2016) A Bis(methylpiperazinylstyryl)phenanthroline as a fluorescent ligand for G-quadruplexes, Chem. Eur. J., 22, 6037-6047, https://doi.org/10.1002/chem.201505170.

    Article  CAS  PubMed  Google Scholar 

  44. Umar, M. I., Ji, D., Chan, C.-Y., and Kwok, C. K. (2019) G-quadruplex-based fluorescent turn-on ligands and aptamers: from development to applications, Molecules, 24, 2416, https://doi.org/10.3390/molecules24132416.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Di Antonio, M., Ponjavic, A., Radzevičius, A., Ranasinghe, R. T., Catalano, M., Zhang, X., Shen, J., Needham, L.-M., Lee, S. F., Klenerman, D., and Balasubramanian, S. (2020) Single-molecule visualization of DNA G-quadruplex formation in live cells, Nat. Chem., 12, 832-837, https://doi.org/10.1038/s41557-020-0506-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hänsel-Hertsch, R., Di Antonio, M., and Balasubramanian, S. (2017) DNA G-quadruplexes in the human genome: detection, functions and therapeutic potential, Nat. Rev. Mol. Cell Biol., 18, 279-284, https://doi.org/10.1038/nrm.2017.3.

    Article  CAS  PubMed  Google Scholar 

  47. Rigo, R., Palumbo, M., and Sissi, C. (2017) G-quadruplexes in human promoters: A challenge for therapeutic applications, Biochim. Biophys. Acta BBA Gen. Subj., 1861, 1399-1413, https://doi.org/10.1016/j.bbagen.2016.12.024.

    Article  CAS  Google Scholar 

  48. Huppert, J. L., and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome, Nucleic Acids Res., 35, 406-413, https://doi.org/10.1093/nar/gkl1057.

    Article  CAS  PubMed  Google Scholar 

  49. Eddy, J., and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes, Nucleic Acids Res., 36, 1321-1333, https://doi.org/10.1093/nar/gkm1138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Dolinnaya, N. G., Ogloblina, A. M., and Yakubovskaya, M. G. (2016) Structure, properties, and biological relevance of the DNA and RNA G-quadruplexes: Overview 50 years after their discovery, Biochemistry (Moscow), 81, 1602-1649, https://doi.org/10.1134/S0006297916130034.

    Article  CAS  PubMed  Google Scholar 

  51. González, V., Guo, K., Hurley, L., and Sun, D. (2009) Identification and characterization of nucleolin as a c-myc G-quadruplex-binding protein, J. Biol. Chem., 284, 23622-23635, https://doi.org/10.1074/jbc.M109.018028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Soemedi, R., Cygan, K. J., Rhine, C. L., Glidden, D. T., Taggart, A. J., Lin, C.-L., Fredericks, A. M., and Fairbrother, W. G. (2017) The effects of structure on pre-mRNA processing and stability, Methods San Diego Calif., 125, 36-44, https://doi.org/10.1016/j.ymeth.2017.06.001.

    Article  CAS  PubMed  Google Scholar 

  53. Bugaut, A., and Balasubramanian, S. (2012) 5′-UTR RNA G-quadruplexes: translation regulation and targeting, Nucleic Acids Res., 40, 4727-4741, https://doi.org/10.1093/nar/gks068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Beaudoin, J.-D., and Perreault, J.-P. (2013) Exploring mRNA 3′-UTR G-quadruplexes: evidence of roles in both alternative polyadenylation and mRNA shortening, Nucleic Acids Res., 41, 5898-5911, https://doi.org/10.1093/nar/gkt265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Brázda, V., Hároníková, L., Liao, J. C. C., and Fojta, M. (2014) DNA and RNA quadruplex-binding proteins, Int. J. Mol. Sci., 15, 17493-17517, https://doi.org/10.3390/ijms151017493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kosiol, N., Juranek, S., Brossart, P., Heine, A., and Paeschke, K. (2021) G-quadruplexes: a promising target for cancer therapy, Mol. Cancer, 20, 40, https://doi.org/10.1186/s12943-021-01328-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Meier-Stephenson, V. (2022) G4-quadruplex-binding proteins: review and insights into selectivity, Biophys. Rev., 14, 635-654, https://doi.org/10.1007/s12551-022-00952-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Grasso, N., Graziano, R., Marzano, S., D’Aria, F., Merlino, F., Grieco, P., Randazzo, A., Pagano, B., and Amato, J. (2023) Unveiling the interaction between DNA G-quadruplexes and RG-rich peptides, Int. J. Biol. Macromol., 253, 126749, https://doi.org/10.1016/j.ijbiomac.2023.126749.

    Article  CAS  PubMed  Google Scholar 

  59. Sun, H., Karow, J. K., Hickson, I. D., and Maizels, N. (1998) The Bloom’s syndrome helicase unwinds G4 DNA, J. Biol. Chem., 273, 27587-27592, https://doi.org/10.1074/jbc.273.42.27587.

    Article  CAS  PubMed  Google Scholar 

  60. Crabbe, L., Verdun, R. E., Haggblom, C. I., and Karlseder, J. (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity, Science, 306, 1951-1953, https://doi.org/10.1126/science.1103619.

    Article  CAS  PubMed  ADS  Google Scholar 

  61. Sarkies, P., Reams, C., Simpson, L. J., and Sale, J. E. (2010) Epigenetic instability due to defective replication of structured DNA, Mol. Cell, 40, 703-713, https://doi.org/10.1016/j.molcel.2010.11.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wu, Y., Shin-ya, K., and Brosh, R. M. (2008) FANCJ helicase defective in Fanconia anemia and breast cancer unwinds G-quadruplex DNA to defend genomic stability, Mol. Cell. Biol., 28, 4116-4128, https://doi.org/10.1128/MCB.02210-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Li, Y., Syed, J., Suzuki, Y., Asamitsu, S., Shioda, N., Wada, T., and Sugiyama, H. (2016) Effect of ATRX and G-quadruplex formation by the VNTR sequence on α-globin gene expression, ChemBioChem, 17, 928-935, https://doi.org/10.1002/cbic.201500655.

    Article  CAS  PubMed  Google Scholar 

  64. Valle-Orero, J., Rieu, M., Tran, P. L. T., Joubert, A., Raj, S., Allemand, J.-F., Croquette, V., and Boulé, J.-B. (2022) Strand switching mechanism of Pif1 helicase induced by its collision with a G-quadruplex embedded in dsDNA, Nucleic Acids Res., 50, 8767-8778, https://doi.org/10.1093/nar/gkac667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Ling, X., Yao, Y., Ding, L., and Ma, J. (2023) The mechanism of UP1 binding and unfolding of human telomeric DNA G-quadruplex, Biochim. Biophys. Acta BBA Gene Regul. Mech., 1866, 194985, https://doi.org/10.1016/j.bbagrm.2023.194985.

    Article  CAS  Google Scholar 

  66. Calcaterra, N. B., Armas, P., Weiner, A. M. J., and Borgognone, M. (2010) CNBP: a multifunctional nucleic acid chaperone involved in cell death and proliferation control, IUBMB Life, 62, 707-714, https://doi.org/10.1002/iub.379.

    Article  CAS  PubMed  Google Scholar 

  67. David, A. P., Pipier, A., Pascutti, F., Binolfi, A., Weiner, A. M. J., Challier, E., Heckel, S., Calsou, P., Gomez, D., Calcaterra, N. B., and Armas, P. (2019) CNBP controls transcription by unfolding DNA G-quadruplex structures, Nucleic Acids Res., 47, 7901-7913, https://doi.org/10.1093/nar/gkz527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Borgognone, M., Armas, P., and Calcaterra, N. B. (2010) Cellular nucleic-acid-binding protein, a transcriptional enhancer of c-Myc, promotes the formation of parallel G-quadruplexes, Biochem. J., 428, 491-498, https://doi.org/10.1042/BJ20100038.

    Article  CAS  PubMed  Google Scholar 

  69. Takasugi, T., Gu, P., Liang, F., Staco, I., and Chang, S. (2023) Pot1b–/– tumors activate G-quadruplex-induced DNA damage to promote telomere hyper-elongation, Nucleic Acids Res., 51, 9227-9247, https://doi.org/10.1093/nar/gkad648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Olson, C. L., Barbour, A. T., Wieser, T. A., and Wuttke, D. S. (2023) RPA engages telomeric G-quadruplexes more effectively than CST, Nucleic Acids Res., 51, 5073-5086, https://doi.org/10.1093/nar/gkad315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Niu, K., Zhang, X., Song, Q., and Feng, Q. (2022) G-quadruplex regulation of VEGFA mRNA translation by RBM4, Int. J. Mol. Sci., 23, 743, https://doi.org/10.3390/ijms23020743.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ginisty, H., Sicard, H., Roger, B., and Bouvet, P. (1999) Structure and functions of nucleolin, J. Cell Sci., 112, 761-772, https://doi.org/10.1242/jcs.112.6.761.

    Article  CAS  PubMed  Google Scholar 

  73. Angelov, D., Bondarenko, V. A., Almagro, S., Menoni, H., Mongélard, F., Hans, F., Mietton, F., Studitsky, V. M., Hamiche, A., Dimitrov, S., and Bouvet, P. (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes, EMBO J., 25, 1669-1679, https://doi.org/10.1038/sj.emboj.7601046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. He, T.-C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998) Identification of c-MYC as a target of the APC pathway, Science, 281, 1509-1512, https://doi.org/10.1126/science.281.5382.1509.

    Article  CAS  PubMed  ADS  Google Scholar 

  75. Verdun, R. E., and Karlseder, J. (2007) Replication and protection of telomeres, Nature, 447, 924-931, https://doi.org/10.1038/nature05976.

    Article  CAS  PubMed  ADS  Google Scholar 

  76. Fernando, H., Rodriguez, R., and Balasubramanian, S. (2008) Selective recognition of a DNA G-quadruplex by an engineered antibody, Biochemistry, 47, 9365-9371, https://doi.org/10.1021/bi800983u.

    Article  CAS  PubMed  Google Scholar 

  77. Wang, F., Podell, E. R., Zaug, A. J., Yang, Y., Baciu, P., Cech, T. R., and Lei, M. (2007) The POT1-TPP1 telomere complex is a telomerase processivity factor, Nature, 445, 506-510, https://doi.org/10.1038/nature05454.

    Article  CAS  PubMed  ADS  Google Scholar 

  78. Ye, J. Z.-S., Hockemeyer, D., Krutchinsky, A. N., Loayza, D., Hooper, S. M., Chait, B. T., and de Lange, T. (2004) POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex, Genes Dev., 18, 1649-1654, https://doi.org/10.1101/gad.1215404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Mao, S.-Q., Ghanbarian, A. T., Spiegel, J., Martínez Cuesta, S., Beraldi, D., Di Antonio, M., Marsico, G., Hänsel-Hertsch, R., Tannahill, D., and Balasubramanian, S. (2018) DNA G-quadruplex structures mold the DNA methylome, Nat. Struct. Mol. Biol., 25, 951-957, https://doi.org/10.1038/s41594-018-0131-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Cree, S. L., Fredericks, R., Miller, A., Pearce, F. G., Filichev, V., Fee, C., and Kennedy, M. A. (2016) DNA G-quadruplexes show strong interaction with DNA methyltransferases in vitro, FEBS Lett., 590, 2870-2883, https://doi.org/10.1002/1873-3468.12331.

    Article  CAS  PubMed  Google Scholar 

  81. Nakanishi, C., and Seimiya, H. (2020) G-quadruplex in cancer biology and drug discovery, Biochem. Biophys. Res. Commun., 531, 45-50, https://doi.org/10.1016/j.bbrc.2020.03.178.

    Article  CAS  PubMed  Google Scholar 

  82. Wang, E., Thombre, R., Shah, Y., Latanich, R., and Wang, J. (2021) G-Quadruplexes as pathogenic drivers in neurodegenerative disorders, Nucleic Acids Res., 49, 4816-4830, https://doi.org/10.1093/nar/gkab164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ruggiero, E., and Richter, S. N. (2020) Chapter Four - Viral G-quadruplexes: new frontiers in virus pathogenesis and antiviral therap, Annu. Rep. Med. Chem., 54, 101-131, https://doi.org/10.1016/bs.armc.2020.04.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Hänsel-Hertsch, R., Beraldi, D., Lensing, S. V., Marsico, G., Zyner, K., Parry, A., Di Antonio, M., Pike, J., Kimura, H., Narita, M., Tannahill, D., and Balasubramanian, S. (2016) G-quadruplex structures mark human regulatory chromatin, Nat. Genet., 48, 1267-1272, https://doi.org/10.1038/ng.3662.

    Article  CAS  PubMed  Google Scholar 

  85. Biffi, G., Tannahill, D., Miller, J., Howat, W. J., and Balasubramanian, S. (2014) Elevated levels of G-quadruplex formation in human stomach and liver cancer tissues, PLoS One, 9, e102711, https://doi.org/10.1371/journal.pone.0102711.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  86. Hänsel-Hertsch, R., Spiegel, J., Marsico, G., Tannahill, D., and Balasubramanian, S. (2018) Genome-wide mapping of endogenous G-quadruplex DNA structures by chromatin immunoprecipitation and high-throughput sequencing, Nat. Protoc., 13, 551-564, https://doi.org/10.1038/nprot.2017.150.

    Article  CAS  PubMed  Google Scholar 

  87. Ruggiero, E., and Richter, S. N. (2018) G-quadruplexes and G-quadruplex ligands: targets and tools in antiviral therapy, Nucleic Acids Res., 46, 3270-3283, https://doi.org/10.1093/nar/gky187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Carvalho, J., Mergny, J.-L., Salgado, G. F., Queiroz, J. A., and Cruz, C. (2020) G-quadruplex, friend or foe: the role of the G-quartet in anticancer strategies, Trends Mol. Med., 26, 848-861, https://doi.org/10.1016/j.molmed.2020.05.002.

    Article  CAS  PubMed  Google Scholar 

  89. Cimino-Reale, G., Zaffaroni, N., and Folini, M. (2016) Emerging role of G-quadruplex DNA as target in anticancer therapy, Curr. Pharm. Des., 22, 6612-6624, https://doi.org/10.2174/1381612822666160831101031.

    Article  CAS  PubMed  Google Scholar 

  90. Kim, N. W., Piatyszek, M. A., Prowse, K. R., Harley, C. B., West, M. D., Ho, P. L., Coviello, G. M., Wright, W. E., Weinrich, S. L., and Shay, J. W. (1994) Specific association of human telomerase activity with immortal cells and cancer, Science, 266, 2011-2015, https://doi.org/10.1126/science.7605428.

    Article  CAS  PubMed  ADS  Google Scholar 

  91. Zahler, A. M., Williamson, J. R., Cech, T. R., and Prescott, D. M. (1991) Inhibition of telomerase by G-quartet DMA structures, Nature, 350, 718-720, https://doi.org/10.1038/350718a0.

    Article  CAS  PubMed  ADS  Google Scholar 

  92. Moye, A. L., Porter, K. C., Cohen, S. B., Phan, T., Zyner, K. G., Sasaki, N., Lovrecz, G. O., Beck, J. L., and Bryan, T. M. (2015) Telomeric G-quadruplexes are a substrate and site of localization for human telomerase, Nat. Commun., 6, 7643, https://doi.org/10.1038/ncomms8643.

    Article  PubMed  ADS  Google Scholar 

  93. Paeschke, K., Simonsson, T., Postberg, J., Rhodes, D., and Lipps, H. J. (2005) Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo, Nat. Struct. Mol. Biol., 12, 847-854, https://doi.org/10.1038/nsmb982.

    Article  CAS  PubMed  Google Scholar 

  94. Paudel, B. P., Moye, A. L., Abou Assi, H., El-Khoury, R., Cohen, S. B., Holien, J. K., Birrento, M. L., Samosorn, S., Intharapichai, K., Tomlinson, C. G., Teulade-Fichou, M.-P., González, C., Beck, J. L., Damha, M. J., van Oijen, A. M., and Bryan, T. M. (2020) A mechanism for the extension and unfolding of parallel telomeric G-quadruplexes by human telomerase at single-molecule resolution, eLife, 9, e56428, https://doi.org/10.7554/eLife.56428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Tan, J., and Lan, L. (2020) The DNA secondary structures at telomeres and genome instability, Cell Biosci., 10, 47, https://doi.org/10.1186/s13578-020-00409-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Zyner, K. G., Mulhearn, D. S., Adhikari, S., Martínez Cuesta, S., Di Antonio, M., Erard, N., Hannon, G. J., Tannahill, D., and Balasubramanian, S. (2019) Genetic interactions of G-quadruplexes in humans, eLife, 8, e46793, https://doi.org/10.7554/eLife.46793.

    Article  PubMed  PubMed Central  Google Scholar 

  97. De, S., and Michor, F. (2011) DNA secondary structures and epigenetic determinants of cancer genome evolution, Nat. Struct. Mol. Biol., 18, 950-955, https://doi.org/10.1038/nsmb.2089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription, Proc. Natl. Acad. Sci. USA, 99, 11593-11598, https://doi.org/10.1073/pnas.182256799.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  99. Rankin, S., Reszka, A. P., Huppert, J., Zloh, M., Parkinson, G. N., Todd, A. K., Ladame, S., Balasubramanian, S., and Neidle, S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene, J. Am. Chem. Soc., 127, 10584-10589, https://doi.org/10.1021/ja050823u.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Sun, D., Guo, K., Rusche, J. J., and Hurley, L. H. (2005) Facilitation of a structural transition in the polypurine/polypyrimidine tract within the proximal promoter region of the human VEGF gene by the presence of potassium and G-quadruplex-interactive agents, Nucleic Acids Res., 33, 6070-6080, https://doi.org/10.1093/nar/gki917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Dexheimer, T. S., Sun, D., and Hurley, L. H. (2006) Deconvoluting the structural and drug-recognition complexity of the G-quadruplex-forming region upstream of the bcl-2 P1 promoter, J. Am. Chem. Soc., 128, 5404-5415, https://doi.org/10.1021/ja0563861.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Cogoi, S., and Xodo, L. E. (2006) G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription, Nucleic Acids Res., 34, 2536-2549, https://doi.org/10.1093/nar/gkl286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Yang, D., and Hurley, L. H. (2006) Structure of the biologically relevant G-quadruplex in the c-MYC promoter, Nucleosides Nucleotides Nucleic Acids, 25, 951-968, https://doi.org/10.1080/15257770600809913.

    Article  CAS  PubMed  Google Scholar 

  104. Dang, C. V. (2012) MYC on the path to cancer, Cell, 149, 22-35, https://doi.org/10.1016/j.cell.2012.03.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Lin, C. Y., Lovén, J., Rahl, P. B., Paranal, R. M., Burge, C. B., Bradner, J. E., Lee, T. I., and Young, R. A. (2012) Transcriptional amplification in tumor cells with elevated c-Myc, Cell, 151, 56-67, https://doi.org/10.1016/j.cell.2012.08.026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Whitfield, J. R., Beaulieu, M.-E., and Soucek, L. (2017) Strategies to inhibit Myc and their clinical applicability, Front. Cell Dev. Biol., 5, 10, https://doi.org/10.3389/fcell.2017.00010.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Felsenstein, K. M., Saunders, L. B., Simmons, J. K., Leon, E., Calabrese, D. R., Zhang, S., Michalowski, A., Gareiss, P., Mock, B. A., and Schneekloth, J. S., Jr. (2016) Small molecule microarrays enable the identification of a selective, quadruplex-binding inhibitor of MYC expression, ACS Chem. Biol., 11, 139-148, https://doi.org/10.1021/acschembio.5b00577.

    Article  CAS  PubMed  Google Scholar 

  108. Boddupally, P. V. L., Hahn, S., Beman, C., De, B., Brooks, T. A., Gokhale, V., and Hurley, L. H. (2012) Anticancer activity and cellular repression of c-MYC by the G-quadruplex-stabilizing 11-piperazinylquindoline is not dependent on Direct targeting of the G-quadruplex in the c-MYC promoter, J. Med. Chem., 55, 6076-6086, https://doi.org/10.1021/jm300282c.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Varshney, D., Spiegel, J., Zyner, K., Tannahill, D., and Balasubramanian, S. (2020) The regulation and functions of DNA and RNA G-quadruplexes, Nat. Rev. Mol. Cell Biol., 21, 459-474, https://doi.org/10.1038/s41580-020-0236-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Sato, K., and Knipscheer, P. (2023) G-quadruplex resolution: from molecular mechanisms to physiological relevance, DNA Rep., 130, 103552, https://doi.org/10.1016/j.dnarep.2023.103552.

    Article  CAS  Google Scholar 

  111. Lerner, L. K., and Sale, J. E. (2019) Replication of G quadruplex DNA, Genes., 10, 95, https://doi.org/10.3390/genes10020095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Bryan, T. M. (2019) Mechanisms of DNA Replication and Repair: Insights from the Study of G-Quadruplexes, Molecules, 24, 3439, https://doi.org/10.3390/molecules24193439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. De Magis, A., Manzo, S. G., Russo, M., Marinello, J., Morigi, R., Sordet, O., and Capranico, G. (2019) DNA damage and genome instability by G-quadruplex ligands are mediated by R loops in human cancer cells, Proc. Natl. Acad. Sci. USA, 116, 816-825, https://doi.org/10.1073/pnas.1810409116.

    Article  CAS  PubMed  ADS  Google Scholar 

  114. Rodriguez, R., Miller, K. M., Forment, J. V., Bradshaw, C. R., Nikan, M., Britton, S., Oelschlaegel, T., Xhemalce, B., Balasubramanian, S., and Jackson, S. P. (2012) Small-molecule-induced DNA damage identifies alternative DNA structures in human genes, Nat. Chem. Biol., 8, 301-310, https://doi.org/10.1038/nchembio.780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Salvati, E., Leonetti, C., Rizzo, A., Scarsella, M., Mottolese, M., Galati, R., Sperduti, I., Stevens, M. F. G., D’Incalci, M., Blasco, M., Chiorino, G., Bauwens, S., Horard, B., Gilson, E., Stoppacciaro, A., Zupi, G., and Biroccio, A. (2007) Telomere damage induced by the G-quadruplex ligand RHPS4 has an antitumor effect, J. Clin. Invest., 117, 3236-3247, https://doi.org/10.1172/JCI32461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Rodriguez, R., Müller, S., Yeoman, J. A., Trentesaux, C., Riou, J.-F., and Balasubramanian, S. (2008) A novel small molecule that alters shelterin integrity and triggers a DNA-damage response at telomeres, J. Am. Chem. Soc., 130, 15758-15759, https://doi.org/10.1021/ja805615w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Paeschke, K., Capra, J. A., and Zakian, V. A. (2011) DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase, Cell, 145, 678-691, https://doi.org/10.1016/j.cell.2011.04.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Wang, Y., Yang, J., Wild, A. T., Wu, W. H., Shah, R., Danussi, C., Riggins, G. J., Kannan, K., Sulman, E. P., Chan, T. A., and Huse, J. T. (2019) G-quadruplex DNA drives genomic instability and represents a targetable molecular abnormality in ATRX-deficient malignant glioma, Nat. Commun., 10, 943, https://doi.org/10.1038/s41467-019-08905-8.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  119. Lomen-Hoerth, C., Anderson, T., and Miller, B. (2002) The overlap of amyotrophic lateral sclerosis and frontotemporal dementia, Neurology, 59, 1077-1079, https://doi.org/10.1212/wnl.59.7.1077.

    Article  PubMed  Google Scholar 

  120. Umoh, M. E., Dammer, E. B., Dai, J., Duong, D. M., Lah, J. J., Levey, A. I., Gearing, M., Glass, J. D., and Seyfried, N. T. (2018) A proteomic network approach across the ALS-FTD disease spectrum resolves clinical phenotypes and genetic vulnerability in human brain, EMBO Mol. Med., 10, 48-62, https://doi.org/10.15252/emmm.201708202.

    Article  CAS  PubMed  Google Scholar 

  121. Renton, A. E., Majounie, E., Waite, A., Simón-Sánchez, J., Rollinson, S., Gibbs, J. R., Schymick, J. C., Laaksovirta, H., van Swieten, J. C., Myllykangas, L., Kalimo, H., Paetau, A., Abramzon, Y., Remes, A. M., Kaganovich, A., Scholz, S. W., Duckworth, J., Ding, J., Harmer, D. W., Hernandez, D. G., Johnson, J. O., Mok, K., Ryten, M., Trabzuni, D., Guerreiro, R. J., Orrell, R. W., Neal, J., Murray, A., Pearson, J., Jansen, I. E., Sondervan, D., Seelaar, H., Blake, D., Young, K., Halliwell, N., Callister, J. B., Toulson, G., Richardson, A., Gerhard, A., Snowden, J., Mann, D., Neary, D., Nalls, M. A., Peuralinna, T., Jansson, L., Isoviita, V.-M., Kaivorinne, A.-L., Hölttä-Vuori, M., Ikonen, E., Sulkava, R., Benatar, M., Wuu, J., Chiò, A., Restagno, G., Borghero, G., Sabatelli, M., ITALSGEN Consortium, Heckerman, D., Rogaeva, E., Zinman, L., Rothstein, J. D., Sendtner, M., Drepper, C., Eichler, E. E., Alkan, C., Abdullaev, Z., Pack, S. D., Dutra, A., Pak, E., Hardy, J., Singleton, A., Williams, N. M., Heutink, P., Pickering-Brown, S., Morris, H. R., Tienari, P. J., and Traynor, B. J. (2011) A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD, Neuron, 72, 257-268, https://doi.org/10.1016/j.neuron.2011.09.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Fratta, P., Mizielinska, S., Nicoll, A. J., Zloh, M., Fisher, E. M. C., Parkinson, G., and Isaacs, A. M. (2012) C9orf72 hexanucleotide repeat associated with amyotrophic lateral sclerosis and frontotemporal dementia forms RNA G-quadruplexes, Sci. Rep., 2, 1016, https://doi.org/10.1038/srep01016.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  123. Haeusler, A. R., Donnelly, C. J., Periz, G., Simko, E. A. J., Shaw, P. G., Kim, M.-S., Maragakis, N. J., Troncoso, J. C., Pandey, A., Sattler, R., Rothstein, J. D., and Wang, J. (2014) C9orf72 nucleotide repeat structures initiate molecular cascades of disease, Nature, 507, 195-200, https://doi.org/10.1038/nature13124.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  124. Gitler, A. D., and Tsuiji, H. (2016) There has been an awakening: emerging mechanisms of C9orf72 mutations in FTD/ALS, Brain Res., 1647, 19-29, https://doi.org/10.1016/j.brainres.2016.04.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. An, H., and Shelkovnikova, T. A. (2019) Stress granules regulate paraspeckles: RNP granule continuum at work, Cell Stress, 3, 385-387, https://doi.org/10.15698/cst2019.12.207.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Boeynaems, S., Alberti, S., Fawzi, N. L., Mittag, T., Polymenidou, M., Rousseau, F., Schymkowitz, J., Shorter, J., Wolozin, B., Van Den Bosch, L., Tompa, P., and Fuxreiter, M. (2018) Protein phase separation: a new phase in cell biology, Trends Cell Biol., 28, 420-435, https://doi.org/10.1016/j.tcb.2018.02.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Mackenzie, I. R., Rademakers, R., and Neumann, M. (2010) TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia, Lancet Neurol., 9, 995-1007, https://doi.org/10.1016/S1474-4422(10)70195-2.

    Article  CAS  PubMed  Google Scholar 

  128. Ishiguro, A., Kimura, N., Watanabe, Y., Watanabe, S., and Ishihama, A. (2016) TDP-43 binds and transports G-quadruplex-containing mRNAs into neurites for local translation, Genes Cells, 21, 466-481, https://doi.org/10.1111/gtc.12352.

    Article  CAS  PubMed  Google Scholar 

  129. Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T., and Darnell, R. B. (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function, Cell, 107, 489-499, https://doi.org/10.1016/s0092-8674(01)00566-9.

    Article  CAS  PubMed  Google Scholar 

  130. Dictenberg, J. B., Swanger, S. A., Antar, L. N., Singer, R. H., and Bassell, G. J. (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome, Dev. Cell, 14, 926-939, https://doi.org/10.1016/j.devcel.2008.04.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Muddashetty, R. S., Kelić, S., Gross, C., Xu, M., and Bassell, G. J. (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of Fragile X Syndrome, J. Neurosci., 27, 5338-5348, https://doi.org/10.1523/JNEUROSCI.0937-07.2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Zalfa, F., Eleuteri, B., Dickson, K. S., Mercaldo, V., De Rubeis, S., di Penta, A., Tabolacci, E., Chiurazzi, P., Neri, G., Grant, S. G. N., and Bagni, C. (2007) A new function for the fragile X mental retardation protein in regulation of PSD-95 mRNA stability, Nat. Neurosci., 10, 578-587, https://doi.org/10.1038/nn1893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Goering, R., Hudish, L. I., Guzman, B. B., Raj, N., Bassell, G. J., Russ, H. A., Dominguez, D., and Taliaferro, J. M. (2020) FMRP promotes RNA localization to neuronal projections through interactions between its RGG domain and G-quadruplex RNA sequences, eLife, 9, e52621, https://doi.org/10.7554/eLife.52621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Costa-Mattioli, M., Sossin, W. S., Klann, E., and Sonenberg, N. (2009) Translational control of long-lasting synaptic plasticity and memory, Neuron, 61, 10-26, https://doi.org/10.1016/j.neuron.2008.10.055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y. S., Mele, A., Fraser, C. E., Stone, E. F., Chen, C., Fak, J. J., Chi, S. W., Licatalosi, D. D., Richter, J. D., and Darnell, R. B. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism, Cell, 146, 247-261, https://doi.org/10.1016/j.cell.2011.06.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Didiot, M.-C., Subramanian, M., Flatter, E., Mandel, J.-L., and Moine, H. (2009) Cells lacking the fragile X mental retardation protein (FMRP) have normal RISC activity but exhibit altered stress granule assembly, Mol. Biol. Cell, 20, 428-437, https://doi.org/10.1091/mbc.e08-07-0737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Zhang, Y., Gaetano, C. M., Williams, K. R., Bassell, G. J., and Mihailescu, M. R. (2014) FMRP interacts with G-quadruplex structures in the 3′-UTR of its dendritic target Shank1 mRNA, RNA Biol., 11, 1364-1374, https://doi.org/10.1080/15476286.2014.996464.

    Article  PubMed  Google Scholar 

  138. Verkhratsky, A., Parpura, V., Vardjan, N., and Zorec, R. (2019) Physiology of Astroglia in Neuroglia in Neurodegenerative Diseases, Springer, Singapore, pp. 45-91, https://doi.org/10.1007/978-981-13-9913-8_3.

  139. Bhattacharyya, D., Mirihana Arachchilage, G., and Basu, S. (2016) Metal cations in G-quadruplex folding and stability, Front. Chem., 4, 38, https://doi.org/10.3389/fchem.2016.00038.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  140. Taurin, S., Dulin, N. O., Pchejetski, D., Grygorczyk, R., Tremblay, J., Hamet, P., and Orlov, S. N. (2002) c-Fos expression in ouabain-treated vascular smooth muscle cells from rat aorta: evidence for an intracellular-sodium-mediated, calcium-independent mechanism, J. Physiol., 543, 835-847, https://doi.org/10.1113/jphysiol.2002.023259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Koltsova, S. V., Trushina, Y., Haloui, M., Akimova, O. A., Tremblay, J., Hamet, P., and Orlov, S. N. (2012) Ubiquitous Na+i/K+i-sensitive transcriptome in mammalian cells: evidence for Ca2+i-independent excitation-transcription coupling, PLoS One, 7, e38032, https://doi.org/10.1371/journal.pone.0038032.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  142. Klimanova, E. A., Sidorenko, S. V., Tverskoi, A. M., Shiyan, A. A., Smolyaninova, L. V., Kapilevich, L. V., Gusakova, S. V., Maksimov, G. V., Lopina, O. D., and Orlov, S. N. (2019) Search for intracellular sensors involved in the functioning of monovalent cations as secondary messengers, Biochemistry (Moscow), 84, 1280-1295, https://doi.org/10.1134/S0006297919110063.

    Article  CAS  PubMed  Google Scholar 

  143. Klimanova, E. A., Sidorenko, S. V., Abramicheva, P. A., Tverskoi, A. M., Orlov, S. N., and Lopina, O. D. (2020) Transcriptomic changes in endothelial cells triggered by Na,K-ATPase inhibition: a search for upstream Na+i/K+i sensitive genes, Int. J. Mol. Sci., 21, 7992, https://doi.org/10.3390/ijms21217992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Skou, J. C. (1965) Enzymatic basis for active transport of Na+ and K+ across cell membrane, Physiol. Rev., 45, 596-618, https://doi.org/10.1152/physrev.1965.45.3.596.

    Article  CAS  PubMed  Google Scholar 

  145. Rose, C. R., and Konnerth, A. (2001) NMDA receptor-mediated Na+ signals in spines and dendrites, J. Neurosci., 21, 4207-4214, https://doi.org/10.1523/JNEUROSCI.21-12-04207.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Zhu, Y., Li, D., and Huang, H. (2020) Activity and cytosolic Na+ regulate synaptic vesicle endocytosis, J. Neurosci., 40, 6112-6120, https://doi.org/10.1523/JNEUROSCI.0119-20.2020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Kapilevich, L. V., Kironenko, T. A., Zaharova, A. N., Kotelevtsev, Y. V., Dulin, N. O., and Orlov, S. N. (2015) Skeletal muscle as an endocrine organ: role of Na+i/K+i-mediated excitation-transcription coupling, Genes Dis., 2, 328-336, https://doi.org/10.1016/j.gendis.2015.10.001.

    Article  PubMed  PubMed Central  Google Scholar 

  148. Kironenko, T. A., Milovanova, K. G., Zakharova, A. N., Sidorenko, S. V., Klimanova, E. A., Dyakova, E. Yu., Orlova, A. A., Negodenko, E. S., Kalinnikova, Y. G., Orlov, S. N., and Kapilevich, L. V. (2021) Effect of dynamic and static load on the concentration of myokines in the blood plasma and content of sodium and potassium in mouse skeletal muscles, Biochemistry (Moscow), 86, 370-381, https://doi.org/10.1134/S0006297921030123.

    Article  CAS  PubMed  Google Scholar 

  149. Despa, S., Islam, M. A., Weber, C. R., Pogwizd, S. M., and Bers, D. M. (2002) Intracellular Na+ concentration is elevated in heart failure but Na/K pump function is unchanged, Circulation, 105, 2543-2548, https://doi.org/10.1161/01.CIR.0000016701.85760.97.

    Article  CAS  PubMed  Google Scholar 

  150. Pogwizd, S. M., Sipido, K. R., Verdonck, F., and Bers, D. M. (2003) Intracellular Na in animal models of hypertrophy and heart failure: contractile function and arrhythmogenesis, Cardiovasc. Res., 57, 887-896, https://doi.org/10.1016/S0008-6363(02)00735-6.

    Article  CAS  PubMed  Google Scholar 

  151. Pieske, B., Maier, L. S., Piacentino, V., Weisser, J., Hasenfuss, G., and Houser, S. (2002) Rate dependence of Na+i and contractility in nonfailing and failing human myocardium, Circulation, 106, 447-453, https://doi.org/10.1161/01.CIR.0000023042.50192.F4.

    Article  CAS  PubMed  Google Scholar 

  152. Petrushanko, I. Y., Yakushev, S., Mitkevich, V. A., Kamanina, Y. V., Ziganshin, R. H., Meng, X., Anashkina, A. A., Makhro, A., Lopina, O. D., Gassmann, M., Makarov, A. A., and Bogdanova, A. (2012) S-glutathionylation of the Na,K-ATPase catalytic α subunit is a determinant of the enzyme redox sensitivity, J. Biol. Chem., 287, 32195-32205, https://doi.org/10.1074/jbc.M112.391094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Koltsova, S. V., Shilov, B., Birulina, J. G., Akimova, O. A., Haloui, M., Kapilevich, L. V., Gusakova, S. V., Tremblay, J., Hamet, P., and Orlov, S. N. (2014) Transcriptomic changes triggered by hypoxia: evidence for HIF-1α-independent, Na+i/K+i-mediated, excitation-transcription coupling, PLoS One, 9, e110597, https://doi.org/10.1371/journal.pone.0110597.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  154. Weisburger, J. H. (1994) Vitamins and minerals in the prevention and treatment of cancer, J. Am. Coll. Nutr., 13, 211-212, https://doi.org/10.1080/07315724.1994.10738223.

    Article  Google Scholar 

  155. Reshkin, S. J., Cardone, R. A., and Harguindey, S. (2013) Na+-H+ exchanger, pH regulation and cancer, Recent Pat. Anticancer Drug Discov., 8, 85-99, https://doi.org/10.2174/15748928130108.

    Article  CAS  PubMed  Google Scholar 

  156. Boardman, L., Huett, M., Lamb, J. F., Newton, J. P., and Polson, J. M. (1974) Evidence for the genetic control of the sodium pump density in HeLa cells, J. Physiol., 241, 771-794, https://doi.org/10.1113/jphysiol.1974.sp010684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Shiyan, A. A., Sidorenko, S. V., Fedorov, D., Klimanova, E. A., Smolyaninova, L. V., Kapilevich, L. V., Grygorczyk, R., and Orlov, S. N. (2019) Elevation of intracellular Na+ contributes to expression of early response genes triggered by endothelial cell shrinkage, Cell. Physiol. Biochem., 53, 638-647, https://doi.org/10.33594/000000162.

    Article  CAS  PubMed  Google Scholar 

  158. Fedorov, D. A., Sidorenko, S. V., Yusipovich, A. I., Parshina, E. Y., Tverskoi, A. M., Abramicheva, P. A., Maksimov, G. V., Orlov, S. N., Lopina, O. D., and Klimanova, E. A. (2021) Na+i/K+i imbalance contributes to gene expression in endothelial cells exposed to elevated NaCl, Heliyon, 7, e08088, https://doi.org/10.1016/j.heliyon.2021.e08088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.

Author information

Authors and Affiliations

  1. Faculty of Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    Olga D. Lopina, Svetlana V. Sidorenko, Dmitry A. Fedorov & Elizaveta A. Klimanova

Authors
  1. Olga D. Lopina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana V. Sidorenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dmitry A. Fedorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizaveta A. Klimanova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

O.D.L. and E.A.K. wrote the original text of the manuscript; S.V.S. and D.A.F. preparing illustrations; all authors reviewed the manuscript.

Corresponding authors

Correspondence to Olga D. Lopina or Elizaveta A. Klimanova.

Ethics declarations

This work does not contain any studies involving human and animal subjects. The authors of this work declare that they have no conflicts of interest.

Additional information

Translated from Uspekhi Biologicheskoi Khimii, 2024, Vol. 64, pp. 503-532.

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lopina, O.D., Sidorenko, S.V., Fedorov, D.A. et al. G-Quadruplexes as Sensors of Intracellular Na+/K+ Ratio: Potential Role in Regulation of Transcription and Translation. Biochemistry Moscow 89 (Suppl 1), S262–S277 (2024). https://doi.org/10.1134/S0006297924140153

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297924140153

Keywords

Search

Navigation