Demonstration of ligand decoration, and ligand-induced perturbation, of G-quadruplexes in a plasmid using atomic force microscopy

Biochemistry

Volumn 51, Issue 2, 2012, Pages 578-585

  Mela, Ioanna ^a   Kranaster, Ramon ^a,b   Henderson, Robert M ^a   Balasubramanian, Shankar ^a,b,c   Edwardson, J Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE; DNA FRAGMENT; FUNCTIONAL SYSTEMS; G-QUADRUPLEXES; GENE PROMOTER; INDIRECT METHODS; NUCLEAR PROTEINS; SECONDARY STRUCTURES; SINGLE MOLECULE LEVEL; SINGLE-CHAIN ANTIBODIES; SMALL MOLECULES; STRUCTURAL EVIDENCE; TELOMERES; THERAPEUTIC POTENTIALS;

ATOMIC FORCE MICROSCOPY; DNA; GENE THERAPY; LIGANDS; MOLECULES; TRANSCRIPTION;

DNA SEQUENCES;

DNA FRAGMENT; GUANINE QUADRUPLEX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PLASMID DNA; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; DNA BINDING; DNA STRUCTURE; DNA TRANSCRIPTION; ENZYME ACTIVATION; HUMAN; IN VITRO STUDY; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TELOMERE;

AMINOQUINOLINES; ANIMALS; BASE SEQUENCE; G-QUADRUPLEXES; HUMANS; LIGANDS; MICE; MICROSCOPY, ATOMIC FORCE; PICOLINIC ACIDS; PLASMIDS; POLY(ADP-RIBOSE) POLYMERASES; SINGLE-CHAIN ANTIBODIES; TRANSCRIPTION, GENETIC;

EID: 84855948076     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201600g     Document Type: Article

References (44)

1. Sannohe, Y. and Sugiyama, H. (2010) Overview of formation of G-quadruplex structures. Current Protocols in Nucleic Acid Chemistry, Chapter 17, Unit 17.2.1-17.2.17, Wiley, New York.
2. Balasubramanian, S., Hurley, L. H., and Neidle, S. (2011) Targeting G-quadruplexes in gene promoters: A novel anticancer strategy? Nat. Rev. Drug Discovery 10, 261-275
3. Huppert, J. L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome Nucleic Acids Res. 33, 2908-2916 (Pubitemid 41511230)
4. Oganesian, L. and Bryan, T. M. (2007) Physiological relevance of telomeric G-quadruplex formation: A potential drug target BioEssays 29, 155-165 (Pubitemid 46340250)
5. Smith, J. S., Chen, Q., Yatsunyk, L. A., Nicoludis, J. M., Garcia, M. S., Kranaster, R., Balasubramanian, S., Monchaud, D., Teulade-Fichou, M. P., Abramowitz, L., Schultz, D. C., and Johnson, F. B. (2011) Rudimentary G-quadruplex-based telomere capping in Saccharomyces cerevisiae Nat. Struct. Mol. Biol. 18, 478-485
6. 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. U.S.A. 99, 11593-11598 (Pubitemid 34994444)
7. Huppert, J. L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome Nucleic Acids Res. 35, 406-413 (Pubitemid 46232058)
8. Eddy, J., Vallur, A. C., Varma, S., Liu, H., Reinhold, W. C., Pommier, Y., and Maizels, N. (2011) G4 motifs correlate with promoter-proximal transcriptional pausing in human genes Nucleic Acids Res. 39, 4975-4983
9. Law, M. J., Lower, K. M., Voon, H. P., Hughes, J. R., Garrick, D., Viprakasit, V., Mitson, M., De Gobbi, M., Marra, M., Morris, A., Abbott, A., Wilder, S. P., Taylor, S., Santos, G. M., Cross, J., Ayyub, H., Jones, S., Ragoussis, J., Rhodes, D., Dunham, I., Higgs, D. R., and Gibbons, R. J. (2010) ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner Cell 143, 367-378
10. 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
11. De, S. and Michor, F. (2011) DNA secondary structures and epigenetic determinants of cancer genome evolution Nat. Struct. Mol. Biol. 18, 950-955
12. Balasubramanian, S. and Neidle, S. (2009) G-quadruplex nucleic acids as therapeutic targets Curr. Opin. Chem. Biol. 13, 345-353
13. Uribe, D. J., Guo, K., Shin, Y. J., and Sun, D. (2011) Heterogeneous nuclear ribonucleoprotein K and nucleolin as transcriptional activators of the vascular endothelial growth factor promoter through interaction with secondary DNA structures Biochemistry 50, 3796-3806
14. 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
15. Schaffitzel, C., Postberg, J., Paeschke, K., and Lipps, H. J. (2010) Probing telomeric G-quadruplex DNA structures in cells with in vitro generated single-chain antibody fragments Methods Mol. Biol. 608, 159-181
16. Monchaud, D. and Teulade-Fichou, M. P. (2008) A hitchhiker's guide to G-quadruplex ligands Org. Biomol. Chem. 6, 627-636 (Pubitemid 351972601)
17. Fernando, H., Sewitz, S., Darot, J., Tavar, S., Huppert, J. L., and Balasubramanian, S. (2009) Genome-wide analysis of a G-quadruplex-specific single-chain antibody that regulates gene expression Nucleic Acids Res. 37, 6716-6722
18. Soldatenkov, V. A., Vetcher, A. A., Duka, T., and Ladame, S. (2008) First evidence of a functional interaction between DNA quadruplexes and poly(ADP-ribose) polymerase-1 ACS Chem. Biol. 3, 214-219
19. 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
20. Bugaut, A., Rodriguez, R., Kumari, S., Hsu, S.-T. D., and Balasubramanian, S. (2010) Small molecule-mediated inhibition of translation by targeting a native RNA G-quadruplex Org. Biomol. Chem. 8, 2771-2776
21. Waller, Z. A. E., Sewitz, S. A., Hsu, S.-T. D., and Balasubramanian, S. (2009) A small molecule that disrupts G-quadruplex DNA structure and enhances gene expression J. Am. Chem. Soc. 131, 12628-12633
22. Müller, S., Kumari, S., Rodriquez, R., and Balasubramanian, S. (2010) Small-molecule-mediated G-quadruplex isolation from human cells Nat. Chem. 2, 1095-1098
23. Fernando, H., Rodriguez, R., and Balasubramanian, S. (2008) Selective recognition of a DNA G-quadruplex by an engineered antibody Biochemistry 47, 9365-9371
24. Rangan, A., Fedoroff, O. Y., and Hurley, L. H. (2001) Induction of duplex to G-quadruplex transition in the c-myc promoter region by a small molecule J. Biol. Chem. 276, 4640-4646
25. Hounsou, C., Guittat, L., Monchaud, D., Jourdan, M., Saettel, N., Mergny, J. L., and Teulade-Fichou, M. P. (2007) G-quadruplex recognition by quinacridines: A SAR, NMR, and biological study ChemMedChem 2, 655-666
26. Campbell, N. H., Patel, M., Tofa, A. B., Ghosh, R., Parkinson, G. N., and Neidle, S. (2009) Selectivity in ligand recognition of G-quadruplex loops Biochemistry 48, 1675-1680
27. Tran, P. L., Largy, E., Hamon, F., Teulade-Fichou, M. P., and Mergny, J. L. (2011) Fluorescence intercalator displacement assay for screening G4 ligands towards a variety of G-quadruplex structures Biochimie 93, 1288-1296
28. Crampton, N., Roes, S., Dryden, D. T. F., Rao, D. N., Edwardson, J. M., and Henderson, R. M. (2007) DNA looping and translocation provide an optimal cleavage mechanism for the type III restriction enzymes EMBO J. 26, 3815-3825 (Pubitemid 47295874)
29. Crampton, N., Yokokawa, M., Dryden, D. T. F., Edwardson, J. M., Rao, D. N., Takeyasu, K., Yoshimura, S. H., and Henderson, R. M. (2007) Fast-scan atomic force microscopy reveals that the type III restriction enzyme EcoP15I is capable of DNA translocation and looping Proc. Natl. Acad. Sci. U.S.A. 104, 12755-12760 (Pubitemid 47255227)
30. Neaves, K. J., Cooper, L. P., White, J. H., Carnally, S. M., Dryden, D. T. F., Edwardson, J. M., and Henderson, R. M. (2009) Atomic force microscopy of the EcoKI type I DNA restriction enzyme bound to DNA shows enzyme dimerisation and DNA looping Nucleic Acids Res. 37, 2053-2063
31. Neaves, K. J., Huppert, J. L., Henderson, R. M., and Edwardson, J. M. (2009) Direct visualization of G-quadruplexes in DNA using atomic force microscopy Nucleic Acids Res. 37, 6269-6275
32. Duquette, M. L., Handa, P., Vincent, J. A., Taylor, A. F., and Maizels, N. (2007) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA Genes Dev. 18, 1618-1629 (Pubitemid 38868912)
33. Bardin, C. and Leroy, J. L. (2008) The formation pathway of tetramolecular G-quadruplexes Nucleic Acids Res. 36, 477-488 (Pubitemid 351258862)
34. Scott, D. W. (1979) On optimal and data-based histograms Biometrika 66, 605-610 (Pubitemid 10218411)
35. Welch, B. L. (1947) The generalization of 'Student's' problem when several different population variances are involved Biometrika 34, 28-35
36. Schneider, S. W., Lärmer, J., Henderson, R. M., and Oberleithner, H. (1998) Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy Pfluegers Arch. 435, 362-367 (Pubitemid 28066227)
37. Cantor, C. R. and Schimmel, P. R. (1980) Biophysical Chemistry. Part II. Techniques for the Study of Biological Structure and Function, W. H. Freeman and Co., New York.
38. Edstrom, R. D., Meinke, M. H., Yang, X., Yang, R., Elings, V., and Evans, D. F. (1990) Direct visualization of phosphorylase-phosphorylase kinase complexes by scanning tunneling and atomic force microsopy Biophys. J. 58, 1437-1448
39. Oncley, J. L., Scatchard, G., and Brown, A. (1947) Physical-chemical characteristics of certain of the proteins of normal human plasma J. Phys. Colloid Chem. 51, 184-198
40. Durschchlag, H. and Zipper, P. (1997) Calculation of partial specific volumes and other volumetric properties of small molecules and polymers J. Appl. Crystallogr. 30, 803-807 (Pubitemid 127820730)
41. Grant, E. H. (1957) The dielectric method of estimating protein hydration Phys. Med. Biol. 2, 17-28
42. Hori, K., Takahashi, T., and Okada, T. (1998) The measurement of exonuclease activities by atomic force microscopy Eur. Biophys. J. 27, 63-68 (Pubitemid 28105806)
43. Kikin, O., D'Antonio, L., and Bagga, P. S. (2006) QGRS Mapper: A web-based server for predicting G-quadruplexes in nucleotide sequences Nucleic Acids Res. 34, W676-W682
44. Rolli, V., Ruf, A., Augustin, A., Schulz, G. E., Mnissier-de Murcia, J., and de Murcia, G. (2000) Poly(ADP-ribose) polymerase: Structure and function. In From DNA Damage and Stress Signalling to Cell Death: Poly ADP-Ribosylation Reactions (de Murcia, G., and Shall, S., Eds.) pp 35-79. Oxford University Press, New York.