A GTP-dependent switch that controls G-quadruplex multimer formation

Sofia Kolesnikova1,2, Pavel Srb1, Lukáš Vrzal1, Michael S. Lawrence3, Václav Veverka1,4, Edward A. Curtis1

1Institute of Organic Chemistry and Biochemistry ASCR, Prague 166 10, Czech Republic, curtis@uochb.cas.cz

2Department of Biochemistry and Microbiology, University of Chemistry and Technology, Prague 166 28, Czech Republic

3Cancer Center and Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA

4Department of Cell Biology, Charles University in Prague, Faculty of Science, Prague 128 44, Czech Republic

G-quadruplexes are four-stranded nucleic acid structures typically made up of stacked GGGG tetrads connected by short loops [1].  Although most studies investigating potential biological roles of G-quadruplexes have focused on monomeric structures, recent work suggests that multimeric G-quadruplexes could also be important.  We recently identified mutations in the central tetrad of a monomeric G-quadruplex that induce formation of higher-order structures [2-4].  Here we show that both DNA-DNA and DNA-RNA G-quadruplexes containing a guanosine to adenosine mutation at a specific position in this tetrad behave like molecular switches in which the equilibrium between monomeric and multimeric G-quadruplex is controlled by GTP concentration.  Analysis of the nucleotide specificity of inhibition and characterization of the mechanism of binding by NMR suggest that GTP stabilizes the monomeric form of the G-quadruplex by becoming incorporated into one of the tetrads.  Hundreds of sequences with the potential to form such GTP-dependent switches are present in the human genome, including some that are evolutionarily conserved.  Our experiments provide new insights into the small molecule-mediated control of G-quadruplex multimerization, and raise the possibility that a GTP-dependent switch controls G-quadruplex multimer formation in cells.

1. Davis, J.T., Angew. Chem. Int. Ed. Engl., 2004, 43, 668-698. 

2. Švehlová, K., Lawrence, M.S., Bednárová, L. and Curtis, E.A., Nucleic Acids Res., 2016, 44, 10789-10803.

3. Kolesnikova, S., Hubálek, M., Bednárová, L., Cvačka, J. and Curtis, E.A., Nucleic Acids Res., 2017, 45, 8684-8696.

4. Majerová, T., Streckerová, T., Bednárová, L. and Curtis, E.A., Biochemistry, 2018, 57, 4052-4062.