In-cell optical imaging of exogenous G-quadruplex DNA by fluorogenic ligands

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10605-10618

  Tseng, Ting Yuan ^a,b   Wang, Zi Fu ^b,c   Chien, Cheng Hao ^a,b   Chang, Ta Chau ^a,b,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF ATOMIC AND MOLECULAR SCIENCES   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3,6 BIS(1 METHYL 4 VINYLPYRIDINIUM)CARBAZOLE DIIODIDE; ANTINEOPLASTIC AGENT; APTAMER; FLUORESCENT DYE; GUANINE RICH OLIGONUCLEOTIDE; THROMBIN BINDING APTAMER; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA STRUCTURE; DRUG LABELING; DRUG TRANSPORT; DRUG UPTAKE; FLUORESCENCE ANALYSIS; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; INCUBATION TIME; INTRACELLULAR TRANSPORT; LUNG CANCER; LYSOSOME; MITOCHONDRION; PRIORITY JOURNAL; TELOMERE;

CARBAZOLES; CELL LINE, TUMOR; DNA; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; G-QUADRUPLEXES; GUANINE; HUMANS; LIGANDS; MICROSCOPY, CONFOCAL; OLIGODEOXYRIBONUCLEOTIDES; OPTICAL IMAGING; PYRIDINIUM COMPOUNDS;

EID: 84890345112     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt814     Document Type: Article

References (58)

1. Todd, A.K., Johnston, M. and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motufs in human DNA. Nucleic Acids Res., 33, 2901-2907.
2. Huppert, J.L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2908-2916.
3. Eddy, J. and Maizels, N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res., 34, 3887-3896.
4. Qin, Y. and Hurley, L.H. (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie, 90, 1149-1171.
5. Balasubramanian, S. and Neidle, S. (2009) G-quadruplex nucleic acids as therapeutic targets. Curr. Opin. Chem. Biol., 13, 345-353.
6. Xu, Y. (2011) Chemistry in human telomere biology: structure, function and targeting of telomere DNA/RNA. Chem. Soc. Rev., 40, 2719-2740.
7. Patel, D.J., Phan, A.T. and Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 50-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res., 35, 7429-7455.
8. 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.
9. Bates, P.J., Kahlon, J.B., Thomas, S.D., Trent, J.O. and Miller, D.M. (1999) Antiproliferative activity of G-rich oligonucleotides correlates with protein binding. J. Biol. Chem., 274, 26369-26377.
10. Jing, N., Li, Y., Xiong, W., Sha, W., Jing, L. and Tweardy, D.J. (2004) G-quartet oligonucleotides: A new class of signal transducer and activator of transcription 3 inhibitors that suppresses growth of prostate and breast tumors through induction of apoptosis. Cancer Res., 64, 6603-6609.
11. Qi, H., Lin, C.P., Fu, X., Wood, L.M., Liu, A.A., Tsai, Y.C., Chen, Y., Barbieri, C.M., Pilch, D.S. and Liu, L.F. (2006) Gquadruplexes induces apoptosis in tumor cells. Cancer Res., 66, 11808-11816.
12. Sedoris, K.C., Thomas, S.D., Clarkson, C.R., Muench, D., Islam, A., Singh, R. and Miller, D.M. (2012) Genomic c-Myc quadruplex DNA selectively kills leukemia. Mol. Cancer Ther., 11, 66-76.
13. 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.
14. Wittrup, A., Sandgren, S., Lilja, J., Bratt, C., Gustavsson, N., Morgelin, M. and Belting, M. (2007) Identification of proteins released by mammalian cells that mediate DNA internalization through proteoglycan-dependent macropinocytosis. J. Biol. Chem., 282, 27897-27904.
15. Fumoto, S., Nishi, J., Ishii, H., Wang, X., Miyamoto, H., Yoshikawa, N., Nakashima, M., Nakamura, J. and Nishida, K. (2009) Rac-mediated macropinocytosis is a critical route for naked plasmid DNA transfer in mice. Mol. Pharm., 6, 1170-1179.
16. Reyes-R., E.M., Teng, Y. and Bates, P.J. (2010) A new paradigm for aptamer therapeutic AS1411 action: uptake by macropinocytosis and its stimulation by a nucleolin-dependent mechanism. Cancer Res., 70, 8617-8629.
17. Siddiqui-J., A., Grand, C.L., Bearss, D.L. 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.
18. Dailey, M.M., Miller, M.C., Bates, P.J., Lane, A.N. and Trent, J.O. (2010) Resolution and characterization of the structural polymorphism of a single quadruplex-forming sequence. Nucleic Acids Res., 38, 4877-4888.
19. Ambrus, A., Chen, D., Dai, J., Bialis, T., Jones, R.A. and Yang, D. (2006) Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res., 34, 2723-2735.
20. Rujan, I.N., Meleney, J.C. and Bolton, P.H. (2005) Vertebrate telomere repeat DNAs favor external loop propeller quadruplex structures in the presence of high concentrations of potassium. Nucleic Acids Res., 33, 2022-2031.
21. Li, J., Correia, J.J., Wang, L., Trent, J.O. and Chaires, J.B. (2005) Not so crystal clear: the structure of the human telomere G-quadruplex in solution differs from that present in a crystal. Nucleic Acids Res., 33, 4649-4659.
22. Redon, S., Bombard, S., Elizondo-Riojas, M.A. and Chottard, J.C. (2003) Platinum cross-linking of adenines and guanines on the quadruplex structure of the AG3(T2AG3)3 and (T2AG3)4 human telomere structure in Na+ and K+ solutions. Nucleic Acids Res., 31, 1605-1613.
23. Chang, C.C., Chien, C.W., Lin, Y.H., Kang, C.C. and Chang, T.C. (2007) Investigation of spectral conversion of d(TTAGGG)4 and d(TTAGGG)13 upon potassium titration by a G-quadruplex recognizer BMVC molecule. Nucleic Acids Res., 35, 2846-2860.
24. Luu, K.N., Phan, A.T., Kuryavyi, V., Lacroix, L. and Patel, D.J. (2006) Structure of the human telomere in K+ solution: an intramolecular (3+1) G-quadruplex scaffold. J. Am. Chem. Soc., 128, 9963-9970.
25. Lim, K.W., Amrane, S., Bouaziz, S., Xu, W., Mu, Y., Patel, D.J., Luu, K.N. and Phan, A.T. (2009) Structure of the human telomere in K+ solution: a stable basket-type G-quadruplex with only two G-tetrad layers. J. Am. Chem. Soc., 131, 4301-4309.
26. Heddi, B. and Phan, A.T. (2011) Structure of human telomeric DNA in crowded solution. J. Am. Chem. Soc., 133, 9824-9833.
27. Chang, C.C., Kuo, I.C., Ling, I.F., Chen, C.T., Chen, H.C., Lou, P.J., Lin, J.J. and Chang, T.C. (2004) Detection of quadruplex DNA structures in human telomeres by a fluorescent carbazole derivative. Anal. Chem., 76, 4490-4494.
28. Chang, C.C., Chu, J.F., Kao, F.J., Chiu, Y.C., Lou, P.J., Chen, H.C. and Chang, T.C. (2006) Verification of anti-parallel G-quadruplex structure in human telomeres by using two photon-excitation fluorescence lifetime imaging microscopy of the 3, 6-bis(1-methyl-4-vinylpyridinium)carbazole diiodide molecule. Anal. Chem., 78, 2810-2815.
29. Kang, C.C., Chang, C.C., Chang, T.C., Liao, L.J., Lou, P.J., Xie, W. and Yeung, E.S. (2007) A handheld device for potential point-ofcare screening of cancer. Analyst, 132, 745-749.
30. Stafford, W.F. and Sherwood, P.J. (2004) Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys. Chem., 108, 231-243.
31. Yang, P.C., Luh, K.T., Wu, R. and Wu, C.W. (1992) Characterization of the mucin differentiation in human lung adenocarcinoma cell lines. Am. J. Respir. Cell Mol. Biol., 7, 161-171.
32. Balagurumoorthy, P., Brahmachari, S.K., Mohanty, D., Bansal, M. and Sasisekharan, V. (1992) Hairpin and parallel quartet structures for telomeric sequences. Nucleic Acids Res., 20, 4061-4067.
33. Gray, D.M., Wen, J.D., Gray, C.W., Repges, R., Repges, C., Raabe, G. and Fleischhauer, J. (2008) Measured and calculated CD spectra of G-quartets stacked with the same or opposite polarities. Chirality, 20, 431-440.
34. Kypr, J., Kejnovska, I., Renciuk, D. and Vorlickova, M. (2009) Circular dichroism and conformational polymorphism of DNA. Nucleic Acids Res., 37, 1713-1725.
35. Masiero, S., Trotta, R., Pieraccini, S., De T., S., Perone, R., Randazzo, A. and Spada, G.P. (2010) A non-empirical chromophoric interpretation of CD spectra of DNA G-quadruplex structures. Org. Biomol. Chem., 8, 2683-2692.
36. Bock, L.C., Griffin, L.C., Latham, J.A., Vermaas, E.H. and Toole, J.J. (1992) Selection of single-stranded DNA molecules that bind and inhibit human thrombin. Nature, 355, 564-566.
37. Macaya, R.F., Schultze, P., Smith, F.W., Roe, J.A. and Feigon, J. (1993) Thrombin-binding DNA aptamer forms a unimolecular quadruplex structure in solution. Proc Natl Acad. Sci USA, 90, 3745-3749.
38. Do, N.Q., Lim, K.W., Teo, M.H., Heddi, B. and Phan, A.T. (2011) Stacking of G-quadruplexes: NMR structure of a G-rich oligonucleotides with potential anti-HIV and anticancer activity. Nucleic Acids Res., 39, 9448-9457.
39. Phan, A.T., Modi, Y.S. and Patel, D.J. (2004) Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J. Am. Chem. Soc., 126, 8710-8716.
40. Tsai, Y.L., Wang, Z.F., Chen, W.W. and Chang, T.C. (2011) Emulsified BMVC derivative induced filtration for G-quadruplex DNA structural separation. Nucleic Acids Res., 39, e114.
41. Chaires, J.B. (2001) Analysis and interpretation of ligand-DNA binding isotherms. Methods Enzymol., 340, 3-22.
42. Uchimoto, T., Nohara, H., Kamehara, R., Iwamura, M., Watanabe, N. and Kobayashi, Y. (1999) Mechanism of apoptosis induced by a lysosomotropic agent, L-Leucyl-L-Leucine methyl ester. Apoptosis, 4, 357-362.
43. Wang, Z.F. and Chang, T.C. (2012) Molecular engineering of G-quadruplex ligands based on solvent effect of polyethylene glycol. Nucleic Acids Res., 40, 8711-8720.
44. Lin, C.T., Tseng, T.Y., Wang, Z.F. and Chang, T.C. (2011) Structural conversion of intramolecular and intermolecular G-quadruplexes of bcl2mid: the effect of potassium concentration and ion exchange. J. Phys. Chem. B, 115, 2360-2370.
45. Kang, C.C., Huang, W.C., Kouh, C.W., Wang, Z.F., Cho, C.C., Chang, C.C., Wang, C.L., Chang, T.C., Seemann, J. and Huang, L.J. (2013) Chemical principles for the design of a novel fluorescent probe with high cancer-targeting selectivity and sensitivity. Integr. Biol., 5, 1217-1228.
46. Scaria, P.V., Shire, S.J. and Shafer, R.H. (1992) Quadruplex structure of d(G3T4G3) stabilized by K+or Na+is an asymmetric hairpin dimer. Proc. Natl Acad. Sci. USA, 89, 10336-10340.
47. Rachwal, P.A., Brown, T. and Fox, K.R. (2007) Sequence effects of single base loops in intramolecular quadruplex DNA. FEBS Lett., 581, 1657-1660.
48. Smargiasso, N., Rosu, F., Hsia, W., Colson, P., Baker, E.S., Bowers, M.T., De Pauw, E. and Gabelica, V. (2008) G-quadruplex DNA assemblies: Loop length, cation identity, and multimer formation. J. Am. Chem. Soc., 130, 10208-10216.
49. Bugaut, A. and Balasubramanian, S. (2008) A sequenceindependent study of the influence of short loop lengths on the stability and topology of intramolecular DNA G-quadruplexes. Biochemistry, 47, 689-697.
50. Martadinata, H. and Phan, A.T. (2009) Structure of Propeller-Type Parallel-Stranded RNA G-Quadruplexes, Formed by Human Telomeric RNA Sequences in K+ Solution. J. Am. Chem. Soc., 131, 2570-2578.
51. Azzalin, C.M., Reichenbach, P., Khoriauli, L., Giulotto, E. and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science, 318, 798-801.
52. Schoeftner, S. and Blasco, M.A. (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol., 10, 228-236.
53. Jing, N., Xiong, W., Guan, Y., Pallansch, L. and Wang, S. (2002) Potassium-dependent folding: A key to intracellular delivery of G-quartet oligonucleotides as HIV inhibitors. Biochemistry, 41, 5397-5403.
54. Boussif, O., Lezoualc'h, F., Zanta, M.A., Mergny, M.D., Scherman, D., Demeneix, B. and Behr, J.P. (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl Acad. Sci. USA, 92, 7297-7301.
55. Bates, P.J., Laber, D.A., Miller, D.M., Thomas, S.D. and Trent, J.O. (2009) Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp. Mol. Pathol., 86, 151-164.
56. Lapetre, B., Bourbon, H. and Amalric, F. (1987) Nucleolin, the major nucleolar protein of growing eukaryotic cells: An unusual protein structure revealed by the nucleotide sequence. Proc. Natl Acad. Sci. USA, 84, 1472-1476.
57. Srivastava, M. and Pollard, H.B. (1999) Molecular dissection of nucleolin's role in growth and cell proliferation: New insights. FASEB J., 13, 1911-1922.
58. Gonzalez, V., Guo, K., Hurley, L. and Sun, D. (2009) Identification and characterization of nucleolin as a c-myc G-quadruplexbinding protein. J. Biol. Chem., 284, 23622-23635.