Influence of a GC base pair on excitation energy transfer in DNA-assembled phenanthrene π-stacks

Bioconjugate Chemistry

Volumn 23, Issue 10, 2012, Pages 2105-2113

  Garo, Florian ^a   Häner, Robert ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOPHORES; DNA; ENERGY TRANSFER; EXCITATION ENERGY; FLUORESCENCE; LIGHT; PYRENE; QUENCHING;

% REDUCTIONS; AROMATIC RESIDUES; BASE PAIRS; BUILDING BLOCKES; DNA BASE PAIRS; EXCIPLEXES; EXCITATION ENERGY TRANSFER; FLUORESCENCE INTENSITIES; LIGHT-HARVESTING; PYRENE CHROMOPHORES;

ANTHRACENE;

AROMATIC COMPOUND; PHENANTHRENE DERIVATIVE;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; DNA BASE COMPOSITION; ENERGY TRANSFER; FLUORESCENCE; LIGHT ABSORPTION; PHOTOCHEMICAL QUENCHING;

EID: 84867542309     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc300302v     Document Type: Article

References (100)

1. Hagfeldt, A. and Graetzel, M. (2000) Molecular photovoltaics Acc. Chem. Res. 33, 269-277
2. Lewis, N. S. and Nocera, D. G. (2006) Powering the planet: chemical challenges in solar energy utilization Proc. Natl. Acad. Sci. U.S.A. 103, 15729-15735 (Pubitemid 44657536)
3. Balzani, V., Credi, A., and Venturi, M. (2008) Photochemical conversion of solar energy ChemSusChem 1, 26-58
4. Magnuson, A., Anderlund, M., Johansson, O., Lindblad, P., Lomoth, R., Polivka, T., Ott, S., Stensjo, K., Styring, S., Sundstrom, V., and Hammarstrom, L. (2009) Biomimetic and microbial approaches to solar fuel generation Acc. Chem. Res. 42, 1899-1909
5. Green, B. R. and Parson, W. W. (2003) Light-Harvesting Antennas in Photosynthesis, Kluwer Academic Publishers, Dordrecht.
6. Nelson, N. and Yocum, C. F. (2006) Structure and function of photosystems I and II Annu. Rev. Plant. Biol. 57, 521-565 (Pubitemid 44061036)
7. Renger, T. (2009) Theory of excitation energy transfer: from structure to function Photosynth. Res. 102, 471-485
8. McConnell, I., Li, G. H., and Brudvig, G. W. (2010) Energy conversion in natural and artificial photosynthesis Chem. Biol. 17, 434-447
9. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krauss, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution Nature 411, 909-917 (Pubitemid 32601481)
10. Engel, G. S., Calhoun, T. R., Read, E. L., Ahn, T. K., Mancal, T., Cheng, Y. C., Blankenship, R. E., and Fleming, G. R. (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems Nature 446, 782-786 (Pubitemid 46582029)
11. Panitchayangkoon, G., Hayes, D., Fransted, K. A., Caram, J. R., Harel, E., Wen, J., Blankenship, R. E., and Engel, G. S. (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature Proc. Natl. Acad. Sci. U.S.A. 107, 12766-12770
12. Kouril, R., Oostergetel, G. T., and Boekema, E. J. (2011) Fine structure of granal thylakoid membrane organization using cryo electron tomography Biochim. Biophys. Acta Bioenerg. 1807, 368-374
13. Huang, L., Ponomarenko, N., Wiederrecht, G. P., and Tiede, D. M. (2012) Cofactor-specific photochemical function resolved by ultrafast spectroscopy in photosynthetic reaction center crystals Proc. Natl. Acad. Sci. U.S.A. 109, 4851-4856
14. Psencik, J., Ikonen, T. P., Laurinmaki, P., Merckel, M. C., Butcher, S. J., Serimaa, R. E., and Tuma, R. (2004) Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria Biophys. J. 87, 1165-1172 (Pubitemid 39095093)
15. Oostergetel, G. T., Reus, M., Chew, A. G. M., Bryant, D. A., Boekema, E. J., and Holzwarth, A. R. (2007) Long-range organization of bacteriochlorophyll in chlorosomes of chlorobium tepidum investigated by cryo-electron microscopy FEBS Lett. 581, 5435-5439 (Pubitemid 350101525)
16. Ganapathy, S., Oostergetel, G. T., Wawrzyniak, P. K., Reus, M., Chew, A. G. M., Buda, F., Boekema, E. J., Bryant, D. A., Holzwarth, A. R., and de Groot, H. J. (2009) Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes Proc. Natl. Acad. Sci. U.S.A. 106, 8525-8530
17. Oostergetel, G. T., van Amerongen, H., and Boekema, E. J. (2010) The chlorosome: a prototype for efficient light harvesting in photosynthesis Photosynth. Res. 104, 245-255
18. Adronov, A. and Frechet, J. M. J. (2000) Light-harvesting dendrimers Chem. Commun. 1701-1710
19. Gust, D., Moore, T. A., and Moore, A. L. (2001) Mimicking photosynthetic solar energy transduction Acc. Chem. Res. 34, 40-48 (Pubitemid 32066588)
20. Choi, M. S., Yamazaki, T., Yamazaki, I., and Aida, T. (2004) Bioinspired molecular design of light-harvesting multiporphyrin arrays Angew. Chem., Int. Ed. 43, 150-158 (Pubitemid 38082098)
21. Hoeben, F. J. M., Jonkheijm, P., Meijer, E. W., and Schenning, A. P. H. J. (2005) About supramolecular assemblies of pi-conjugated systems Chem. Rev. 105, 1491-1546
22. Wasielewski, M. R. (2009) Self-assembly strategies for integrating light harvesting and charge separation in artificial photosynthetic systems Acc. Chem. Res. 42, 1910-1921
23. Barber, J. (2009) Photosynthetic energy conversion: natural and artificial Chem. Soc. Rev. 38, 185-196
24. Scholes, G. D., Fleming, G. R., Olaya-Castro, A., and van Grondelle, R. (2011) Lessons from nature about solar light harvesting Nat. Chem. 3, 763-774
25. Nocera, D. G. (2012) The artificial leaf Acc. Chem. Res. 45, 767-776
26. Ganapathy, S., Sengupta, S., Wawrzyniak, P. K., Huber, V., Buda, F., Baumeister, U., Wuerthner, F., and de Groot, H. J. (2009) Zinc chlorins for artificial light-harvesting self-assemble into antiparallel stacks forming a microcrystalline solid-state material Proc. Natl. Acad. Sci. U.S.A. 106, 11472-11477
27. Mass, O., Taniguchi, M., Ptaszek, M., Springer, J. W., Faries, K. M., Diers, J. R., Bocian, D. F., Holten, D., and Lindsey, J. S. (2011) Structural characteristics that make chlorophylls green: interplay of hydrocarbon skeleton and substituents New J. Chem. 35, 76-88
28. Calzaferri, G., Meallet-Renault, R., Brühwiler, D., Pansu, R., Dolamic, I., Dienel, T., Adler, P., Li, H. R., and Kunzmann, A. (2011) Designing dye-nanochannel antenna hybrid materials for light harvesting, transport and trapping ChemPhysChem 12, 580-594
29. Sun, K., Jing, Y., Li, C., Zhang, X., Aguinaldo, R., Kargar, A., Madsen, K., Banu, K., Zhou, Y., Bando, Y., Liu, Z., and Wang, D. (2012) 3D branched nanowire heterojunction photoelectrodes for high-efficiency solar water splitting and H-2 generation Nanoscale 4, 1515-1521
30. Peng, H. Q., Chen, Y. Z., Zhao, Y., Yang, Q. Z., Wu, L. Z., Tung, C. H., Zhang, L. P., and Tong, Q. X. (2012) Artificial light-harvesting system based on multifunctional surface-cross-linked micelles Angew. Chem., Int. Ed. 51, 2088-2092
31. Kameta, N., Ishikawa, K., Masuda, M., Asakawa, M., and Shimizu, T. (2012) Soft nanotubes acting as a light-harvesting antenna system Chem. Mater. 24, 209-214
32. Iehl, J., Nierengarten, J. F., Harriman, A., Bura, T., and Ziessel, R. (2012) Artificial light-harvesting arrays: electronic energy migration and trapping on a sphere and between spheres J. Am. Chem. Soc. 134, 988-998
33. Katz, E. and Willner, I. (2004) Integrated nanoparticle-biomolecule hybrid systems: synthesis, properties, and applications Angew. Chem., Int. Ed. 43, 6042-6108 (Pubitemid 39611873)
34. Liu, J., Cao, Z., and Lu, Y. (2009) Functional nucleic acid sensors Chem. Rev. 109, 1948-1998
35. Singh, Y., Murat, P., and Defrancq, E. (2010) Recent developments in oligonucleotide conjugation Chem. Soc. Rev. 39, 2054-2070
36. Yang, H., Metera, K. L., and Sleiman, H. F. (2010) DNA modified with metal complexes: applications in the construction of higher order metal-DNA nanostructures Coord. Chem. Rev. 254, 2403-2415
37. Tan, S. J., Campolongo, M. J., Luo, D., and Cheng, W. (2011) Building plasmonic nanostructures with DNA Nat. Nanotech. 6, 268-276
38. Diezmann, F. and Seitz, O. (2011) DNA-guided display of proteins and protein ligands for the interrogation of biology Chem. Soc. Rev. 40, 5789-5801
39. Seeman, N. C. (2003) DNA in a material world Nature 421, 427-431 (Pubitemid 36157949)
40. Rosi, N. L. and Mirkin, C. A. (2005) Nanostructures in biodiagnostics Chem. Rev. 105, 1547-1562 (Pubitemid 40596871)
41. Endo, M. and Sugiyama, H. (2009) Chemical approaches to DNA nanotechnology ChemBioChem 10, 2420-2443
42. Silverman, S. K. (2010) DNA as a versatile chemical component for catalysis, encoding, and stereocontrol Angew. Chem., Int. Ed. 49, 7180-7201
43. Genereux, J. C., Boal, A. K., and Barton, J. K. (2010) DNA-mediated charge transport in redox sensing and signaling J. Am. Chem. Soc. 132, 891-905
44. Khakshoor, O. and Kool, E. T. (2011) Chemistry of nucleic acids: impacts in multiple fields Chem. Commun. 47, 7018-7024
45. Dohno, C. and Nakatani, K. (2011) Control of DNA hybridization by photoswitchable molecular glue Chem. Soc. Rev. 40, 5718-5729
46. Sacca, B. and Niemeyer, C. M. (2012) DNA origami: the art of folding DNA Angew. Chem., Int. Ed. 51, 58-66
47. Kawahara, S., Uchimaru, T., and Murata, S. (1999) Sequential multistep energy transfer: enhancement of efficiency of long-range fluorescence resonance energy transfer Chem. Commun. 563-564 (Pubitemid 29141858)
48. Ohya, Y., Yabuki, K., Hashimoto, M., Nakajima, A., and Ouchi, T. (2003) Multistep fluorescence resonance energy transfer in sequential chromophore array constructed on oligo-DNA assemblies Bioconjugate Chem. 14, 1057-1066 (Pubitemid 37449032)
49. Heilemann, M., Tinnefeld, P., Mosteiro, G. S., Garcia-Parajo, M., Van Hulst, N. F., and Sauer, M. (2004) Multistep energy transfer in single molecular photonic wires J. Am. Chem. Soc. 126, 6514-6515 (Pubitemid 38697327)
50. Vyawahare, S., Eyal, S., Mathews, K. D., and Quake, S. R. (2004) Nanometer-scale fluorescence resonance optical waveguides Nano Lett. 4, 1035-1039 (Pubitemid 38859976)
51. Hannestad, J. K., Sandin, P., and Albinsson, B. (2008) Self-assembled DNA photonic wire for long-range energy transfer J. Am. Chem. Soc. 130, 15889-15895
52. Dutta, P. K., Varghese, R., Nangreave, J., Lin, S., Yan, H., and Liu, Y. (2011) DNA-directed artificial light-harvesting antenna J. Am. Chem. Soc. 133, 11985-11993
53. Su, W., Bonnard, V., and Burley, G. A. (2011) DNA-templated photonic arrays and assemblies: design principles and future opportunities Chem. Eur. J. 17, 7982-7991
54. Stein, I. H., Steinhauer, C., and Tinnefeld, P. (2011) Single-molecule four-color FRET visualizes energy-transfer paths on DNA origami J. Am. Chem. Soc. 133, 4193-4195
55. Tikhomirov, G., Hoogland, S., Lee, P., Fischer, A., Sargent, E. H., and Kelley, S. O. (2011) DNA-based programming of quantum dot valency, self-assembly and luminescence Nat. Nanotech. 6, 485-490
56. Hannestad, J. K., Gerrard, S. R., Brown, T., and Albinsson, B. (2011) Self-assembled DNA-based fluorescence waveguide with selectable output Small 7, 3178-3185
57. Graugnard, E., Kellis, D. L., Bui, H., Barnes, S., Kuang, W., Lee, J., Hughes, W. L., Knowlton, W. B., and Yurke, B. (2012) DNA-controlled excitonic switches Nano Lett. 12, 2117-2122
58. Kool, E. T. (2002) Replacing the nucleohases in DNA with designer molecules Acc. Chem. Res. 35, 936-943
59. Varghese, R. and Wagenknecht, H. A. (2009) DNA as a supramolecular framework for the helical arrangements of chromophores: towards photoactive DNA-based nanomaterials Chem. Commun. 2615-2624
60. Kashida, H., Liang, X., and Asanuma, H. (2009) Rational design of functional DNA with a non-ribose acyclic scaffold Curr. Org. Chem. 13, 1065-1084
61. Malinovskii, V. L., Wenger, D., and Häner, R. (2010) Nucleic acid-guided assembly of aromatic chromophores Chem. Soc. Rev. 39, 410-422
62. Stulz, E. (2012) DNA architectonics: towards the next generation of bio-inspired materials Chem. Eur. J. 18, 4456-4469
63. Ostergaard, M. E. and Hrdlicka, P. J. (2011) Pyrene-functionalized oligonucleotides and locked nucleic acids (LNAs): tools for fundamental research, diagnostics, and nanotechnology Chem. Soc. Rev. 40, 5771-5788
64. Teo, Y. N. and Kool, E. T. (2012) DNA-multichromophore systems Chem. Rev. 112, 4221-4245
65. Langenegger, S. M. and Häner, R. (2005) A DNA mimic made of non-nucleosidic phenanthrene building blocks ChemBioChem 6, 2149-2152
66. Malinovskii, V. L., Samain, F., and Häner, R. (2007) Helical arrangement of interstrand stacked pyrenes in a DNA framework Angew. Chem., Int. Ed. 46, 4464-4467 (Pubitemid 46954595)
67. Hariharan, M., Zheng, Y., Long, H., Zeidan, T. A., Schatz, G. C., Vura-Weis, J., Wasielewski, M. R., Zuo, X. B., Tiede, D. M., and Lewis, F. D. (2009) Hydrophobic dimerization and thermal dissociation of perylenediimide- linked DNA hairpins J. Am. Chem. Soc. 131, 5920-5929
68. Häner, R., Garo, F., Wenger, D., and Malinovskii, V. L. (2010) Oligopyrenotides: abiotic, polyanionic oligomers with nucleic acid-like structural properties J. Am. Chem. Soc. 132, 7466-7471
69. Nussbaumer, A. L., Studer, D., Malinovskii, V. L., and Häner, R. (2011) Amplification of chirality by supramolecular polymerization of pyrene oligomers Angew. Chem., Int. Ed. 50, 5490-5494
70. Wenger, D., Malinovskii, V. L., and Häner, R. (2011) Modulation of chiroptical properties by DNA-guided assembly of fluorenes Chem. Commun. 47, 3168-3170
71. Biner, S. M. and Häner, R. (2011) A two-color, self-controlled molecular beacon ChemBioChem 12, 2733-2736
72. Probst, M., Wenger, D., Biner, S. M., and Häner, R. (2012) The DNA three-way junction as a mould for tripartite chromophore assembly Org. Biomol. Chem. 10, 755-759
73. Malinovskii, V. L., Nussbaumer, A. L., and Häner, R. (2012) Oligopyrenotides: chiral nanoscale templates for chromophore assembly Angew. Chem., Int. Ed. 51, 4905-4908
74. Garo, F. and Häner, R. (2012) 2,1,3-Benzothiadiazole-modified DNA Eur. J. Org. Chem. 2012, 2801-2808
75. Asanuma, H., Osawa, T., Kashida, H., Fujii, T., Liang, X., Niwa, K., Yoshida, Y., Shimadad, N., and Maruyama, A. (2012) A polycation-chaperoned in-stem molecular beacon system Chem. Commun. 48, 1760-1762
76. Garo, F. and Häner, R. (2012) A DNA-based light-harvesting antenna Angew. Chem., Int. Ed. 51, 916-919
77. Rehm, D. and Weller, A. (1970) Kinetics of fluorescence quenching by electron and H-atom transfer Isr. J. Chem. 8, 259-271
78. Lewis, F. D., Letsinger, R. L., and Wasielewski, M. R. (2001) Dynamics of photoinduced charge transfer and hole transport in synthetic DNA hairpins Acc. Chem. Res. 34, 159-170 (Pubitemid 32167865)
79. Doose, S., Neuweiler, H., and Sauer, M. (2009) Fluorescence quenching by photoinduced electron transfer: a reporter for conformational dynamics of macromolecules ChemPhysChem 10, 1389-1398
80. Cummings, T. E. and Elving, P. J. (1979) Electrochemical reduction of thymine in dimethyl-sulfoxide auto-protonation of the radical-anion and reduced free-radical J. Electroanal. Chem. 102, 237-248
81. Seidel, C. A. M., Schulz, A., and Sauer, M. H. M. (1996) Nucleobase-specific quenching of fluorescent dyes 0.1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies J. Phys. Chem. 100, 5541-5553 (Pubitemid 126790528)
82. Boussicault, F. and Robert, M. (2008) Electron transfer in DNA and in DNA-related biological processes. electrochemical insights Chem. Rev. 108, 2622-2645
83. Langenegger, S. M. and Häner, R. (2002) The effect of a non-nucleosidic phenanthrene building block on DNA duplex stability Helv. Chim. Acta 85, 3414-3421 (Pubitemid 35340168)
84. Langenegger, S. M. and Häner, R. (2004) Excimer formation by interstrand stacked pyrenes Chem. Commun. 2792-2793 (Pubitemid 40064790)
85. Langenegger, S. M. and Häner, R. (2005) Remarkable stabilization of duplex DNA containing an abasic site by non-nucleosidic phenanthroline and pyrene building blocks ChemBioChem 6, 848-851 (Pubitemid 40873745)
86. Matray, T. J. and Kool, E. T. (1998) Selective and stable DNA base pairing without hydrogen bonds J. Am. Chem. Soc. 120, 6191-6192 (Pubitemid 28307018)
87. Langenegger, S. M. and Häner, R. (2004) A simple, non-nucleosidic base surrogate increases the duplex stability of DNA containing an abasic site Chem. Biodiv. 1, 259-264
88. Yamana, K., Iwase, R., Furutani, S., Tsuchida, H., Zako, H., Yamaoka, T., and Murakami, A. (1999) 2′-Pyrene modified oligonucleotide provides a highly sensitive fluorescent probe of RNA Nucleic Acids Res. 27, 2387-2392 (Pubitemid 29245659)
89. Kawai, T., Ikegami, M., and Arai, T. (2004) Exciplex formation between pyrene and guanine in highly polar solvents Chem. Commun. 824-825 (Pubitemid 38530254)
90. Trkulja, I. and Häner, R. (2007) Triple-helix mediated excimer and exciplex formation Bioconjugate Chem. 18, 289-292 (Pubitemid 46493496)
91. Trkulja, I. and Häner, R. (2007) Monomeric and heterodimeric triple helical DNA mimics J. Am. Chem. Soc. 129, 7982-7989 (Pubitemid 46998197)
92. Nakamura, Y., Fujii, T., and Nishimura, J. (2001) Synthesis and fluorescence emission behavior of anti-[2.3](3,10)phenanthrenophane: overlap between phenanthrene rings required for excimer formation Chem. Lett. 970-971
93. Nakamura, Y., Yamazaki, T., and Nishimura, J. (2005) Synthesis and fluorescence spectra of oxa[3.n]phenanthrenophanes Org. Lett. 7, 3259-3262 (Pubitemid 41059120)
94. Lewis, F. D. and Burch, E. L. (1996) Excimer fluorescence from phenanthrene-9-carboxylate derivatives J. Photochem. Photobiol. A: Chem. 96, 19-23 (Pubitemid 126171142)
95. Chandross, E. A. and Thomas, H. T. (1972) Excited dimer luminescence of pairs of phenanthrene molecules J. Am. Chem. Soc. 94, 2421-2424
96. Lewis, F. D., Wu, T. F., Zhang, Y. F., Letsinger, R. L., Greenfield, S. R., and Wasielewski, M. R. (1997) Distance-dependent electron transfer in DNA hairpins Science 277, 673-676 (Pubitemid 27373910)
97. Conron, S. M., Thazhathveetil, A. K., Wasielewski, M. R., Burin, A. L., and Lewis, F. D. (2010) Direct measurement of the dynamics of hole hopping in extended DNA G-tracts. an unbiased random walk J. Am. Chem. Soc. 132, 14388-14390
98. Wilson, J. N., Cho, Y. J., Tan, S., Cuppoletti, A., and Kool, E. T. (2008) Quenching of fluorescent nucleobases by neighboring DNA: the "insulator" concept ChemBioChem 9, 279-285 (Pubitemid 351196796)
99. Kashida, H., Sekiguchi, K., Higashiyama, N., Kato, T., and Asanuma, H. (2011) Cyclohexyl "base pairs" stabilize duplexes and intensify pyrene fluorescence by shielding it from natural base pairs Org. Biomol. Chem. 9, 8313-8320
100. HyperChem, release 8.0.8, Hypercube, Inc., 1115 NW 4th Street, Gainesville, Florida 32601, USA.