Volume 63, Issue 14 e202319516

Research Article

Site-Selective Photo-Crosslinking of Stilbene Pairs in a DNA Duplex Mediated by Ruthenium Photocatalyst

Corresponding Author

Dr. Hiromu Kashida

[email protected]

orcid.org/0000-0002-0946-0113

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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Hidenori Azuma,

Hidenori Azuma

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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Dr. Hikaru Sotome,

Dr. Hikaru Sotome

Division of Frontier Materials Science and, Center for Advanced Interdisciplinary Research, Graduate School of Engineering Science, Osaka University 1-3 Machikaneyama, Toyonaka, Osaka, 560-8531 Japan

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Prof. Dr. Hiroshi Miyasaka,

Prof. Dr. Hiroshi Miyasaka

Division of Frontier Materials Science and, Center for Advanced Interdisciplinary Research, Graduate School of Engineering Science, Osaka University 1-3 Machikaneyama, Toyonaka, Osaka, 560-8531 Japan

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Prof. Dr. Hiroyuki Asanuma,

Corresponding Author

Prof. Dr. Hiroyuki Asanuma

[email protected]

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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Dr. Hiromu Kashida,

Corresponding Author

Dr. Hiromu Kashida

[email protected]

orcid.org/0000-0002-0946-0113

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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Hidenori Azuma,

Hidenori Azuma

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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Dr. Hikaru Sotome,

Dr. Hikaru Sotome

Division of Frontier Materials Science and, Center for Advanced Interdisciplinary Research, Graduate School of Engineering Science, Osaka University 1-3 Machikaneyama, Toyonaka, Osaka, 560-8531 Japan

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Prof. Dr. Hiroshi Miyasaka,

Prof. Dr. Hiroshi Miyasaka

Division of Frontier Materials Science and, Center for Advanced Interdisciplinary Research, Graduate School of Engineering Science, Osaka University 1-3 Machikaneyama, Toyonaka, Osaka, 560-8531 Japan

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Prof. Dr. Hiroyuki Asanuma,

Corresponding Author

Prof. Dr. Hiroyuki Asanuma

[email protected]

Department of Biomolecular Engineering, Graduate School of Engineering, Nagoya University Furo-cho, Chikusa-ku, Nagoya, 464-8603 Japan

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First published: 28 January 2024

https://doi.org/10.1002/anie.202319516

Citations: 1

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Graphical Abstract

A novel method to site-specifically crosslink DNA duplex upon visible light irradiation. Ru complex on the third strand catalyzed [2+2] photocycloaddition of stilbene moieties via triplet-triplet energy transfer. Site specificity is realized owing to steep distance dependence of the energy transfer. This method will be useful in construction of complex photoresponsive DNA circuits, nanodevices and biological tools.

Abstract

We herein report a method for site-selective photo-crosslinking of a DNA duplex. A stilbene pair was introduced into a DNA duplex and a ruthenium complex was conjugated with a triplex-forming oligonucleotide. We demonstrated that [2+2] photocycloaddition of the stilbene pair occurred upon irradiation with visible light when the ruthenium complex was in close proximity due to triplex formation. No reaction occurred when the ruthenium complex was not in proximity to the stilbene pair. The wavelength of visible light used was of lower energy than the wavelength of UV light necessary for direct excitation of stilbene. Quantum chemical calculation indicated that ruthenium complex catalyzed the photocycloaddition via triplet-triplet energy transfer. Site selectivity of this photo-crosslinking system was evaluated using a DNA duplex bearing two stilbene pairs as a substrate; we showed that the site of crosslinking was precisely regulated by the sequence of the oligonucleotide linked to the ruthenium complex. Since this method does not require orthogonal photoresponsive molecules, it will be useful in construction of complex photoresponsive DNA circuits, nanodevices and biological tools.

Conflict of interests

The authors declare no conflict of interest.

Open Research

Data Availability Statement

The data that support the findings of this study are available in the supplementary material of this article.

Supporting Information

References

1
1aM. J. Hansen, W. A. Velema, M. M. Lerch, W. Szymanski, B. L. Feringa, Chem. Soc. Rev. 2015, 44, 3358–3377;
10.1039/C5CS00118H
CAS PubMed Web of Science® Google Scholar
1bM. M. Lerch, M. J. Hansen, W. A. Velema, W. Szymanski, B. L. Feringa, Nat. Commun. 2016, 7, 12054;
10.1038/ncomms12054
CAS PubMed Web of Science® Google Scholar
1cN. Ankenbruck, T. Courtney, Y. Naro, A. Deiters, Angew. Chem. Int. Ed. 2018, 57, 2768–2798;
10.1002/anie.201700171
CAS PubMed Web of Science® Google Scholar
1dM. Jeong, J. Park, S. Kwon, Eur. J. Org. Chem. 2020, 2020, 7254–7283;
10.1002/ejoc.202001179
CAS Web of Science® Google Scholar
1eM. Regehly, Y. Garmshausen, M. Reuter, N. F. König, E. Israel, D. P. Kelly, C.-Y. Chou, K. Koch, B. Asfari, S. Hecht, Nature 2020, 588, 620–624;
10.1038/s41586-020-3029-7
CAS PubMed Web of Science® Google Scholar
1fP. Lu, D. Ahn, R. Yunis, L. Delafresnaye, N. Corrigan, C. Boyer, C. Barner-Kowollik, Z. A. Page, Matter 2021, 4, 2172–2229;
10.1016/j.matt.2021.03.021
CAS Web of Science® Google Scholar
1gV. M. Lechner, M. Nappi, P. J. Deneny, S. Folliet, J. C. K. Chu, M. J. Gaunt, Chem. Rev. 2022, 122, 1752–1829;
10.1021/acs.chemrev.1c00357
CAS PubMed Web of Science® Google Scholar
1hS. L. Walden, L. L. Rodrigues, J. Alves, J. P. Blinco, V. X. Truong, C. Barner-Kowollik, Nat. Commun. 2022, 13, 2943.
10.1038/s41467-022-30002-6
CAS PubMed Web of Science® Google Scholar
2
2aY. Kamiya, H. Asanuma, Acc. Chem. Res. 2014, 47, 1663–1672;
10.1021/ar400308f
CAS PubMed Web of Science® Google Scholar
2bA. S. Lubbe, W. Szymanski, B. L. Feringa, Chem. Soc. Rev. 2017, 46, 1052–1079;
10.1039/C6CS00461J
CAS PubMed Web of Science® Google Scholar
2cC. Wang, M. P. O'Hagan, Z. Li, J. Zhang, X. Ma, H. Tian, I. Willner, Chem. Soc. Rev. 2022, 51, 720–760.
10.1039/D1CS00688F
CAS PubMed Web of Science® Google Scholar
3
3aM. Singer, A. Jäschke, J. Am. Chem. Soc. 2010, 132, 8372–8377;
10.1021/ja1024782
CAS PubMed Web of Science® Google Scholar
3bM. W. Haydell, M. Centola, V. Adam, J. Valero, M. Famulok, J. Am. Chem. Soc. 2018, 140, 16868–16872;
10.1021/jacs.8b08738
CAS PubMed Web of Science® Google Scholar
3cI. Elamri, C. Abdellaoui, J. K. Bains, K. F. Hohmann, S. L. Gande, E. Stirnal, J. Wachtveitl, H. Schwalbe, J. Am. Chem. Soc. 2021, 143, 10596–10603.
10.1021/jacs.1c02817
CAS PubMed Web of Science® Google Scholar
4A. Rodrigues-Correia, D. Knapp-Bühle, J. W. Engels, A. Heckel, Org. Lett. 2014, 16, 5128–5131.
10.1021/ol502478g
CAS PubMed Web of Science® Google Scholar
5
5aK. Fujimoto, A. Yamada, Y. Yoshimura, T. Tsukaguchi, T. Sakamoto, J. Am. Chem. Soc. 2013, 135, 16161–16167;
10.1021/ja406965f
CAS PubMed Web of Science® Google Scholar
5bK. Fujimoto, S. Sasago, J. Mihara, S. Nakamura, Org. Lett. 2018, 20, 2802–2805.
10.1021/acs.orglett.8b00593
CAS PubMed Web of Science® Google Scholar
6R. T. Michenfelder, L. Delafresnaye, V. X. Truong, C. Barner-Kowollik, H.-A. Wagenknecht, Chem. Commun. 2023, 59, 4012–4015.
10.1039/D3CC00817G
CAS PubMed Web of Science® Google Scholar
7
7aH. Nishioka, X. Liang, T. Kato, H. Asanuma, Angew. Chem. Int. Ed. 2012, 51, 1165–1168;
10.1002/anie.201106093
CAS PubMed Web of Science® Google Scholar
7bY. Yamano, K. Murayama, H. Asanuma, Chem. Eur. J. 2021, 27, 4599–4604.
10.1002/chem.202003528
CAS PubMed Web of Science® Google Scholar
8
8aC. J. Murphy, M. R. Arkin, Y. Jenkins, N. D. Ghatlia, S. H. Bossmann, N. J. Turro, J. K. Barton, Science 1993, 262, 1025–1029;
10.1126/science.7802858
CAS PubMed Web of Science® Google Scholar
8bM. R. Arkin, E. D. A. Stemp, S. Coates Pulver, J. K. Barton, Chem. Biol. 1997, 4, 389–400;
10.1016/S1074-5521(97)90129-0
CAS PubMed Web of Science® Google Scholar
8cP. K. Bhattacharya, J. K. Barton, J. Am. Chem. Soc. 2001, 123, 8649–8656.
10.1021/ja010996t
CAS PubMed Web of Science® Google Scholar
9
9aY. Jenkins, J. K. Barton, J. Am. Chem. Soc. 1992, 114, 8736–8738;
10.1021/ja00048a077
CAS Web of Science® Google Scholar
9bD. J. Hurley, Y. Tor, J. Am. Chem. Soc. 1998, 120, 2194–2195;
10.1021/ja9739998
CAS Web of Science® Google Scholar
9cD. J. Hurley, Y. Tor, J. Am. Chem. Soc. 2002, 124, 13231–13241.
10.1021/ja020172r
CAS PubMed Web of Science® Google Scholar
10
10aI. Vargas-Baca, D. Mitra, H. J. Zulyniak, J. Banerjee, H. F. Sleiman, Angew. Chem. Int. Ed. 2001, 40, 4629–4632;
10.1002/1521-3773(20011217)40:24<4629::AID-ANIE4629>3.0.CO;2-S
CAS PubMed Web of Science® Google Scholar
10bK. M. Stewart, J. Rojo, L. W. McLaughlin, Angew. Chem. Int. Ed. 2004, 43, 5808–5811.
10.1002/anie.200460399
CAS PubMed Web of Science® Google Scholar
11
11aG. N. Grimm, A. S. Boutorine, P. Lincoln, B. Norden, C. Helene, ChemBioChem 2002, 3, 324–331;
10.1002/1439-7633(20020402)3:4<324::AID-CBIC324>3.0.CO;2-7
CAS PubMed Web of Science® Google Scholar
11bS. Le Gac, S. Rickling, P. Gerbaux, E. Defrancq, C. Moucheron, A. Kirsch-De Mesmaeker, Angew. Chem. Int. Ed. 2009, 48, 1122–1125.
10.1002/anie.200804503
CAS PubMed Web of Science® Google Scholar
12
12aM. A. Ischay, M. E. Anzovino, J. Du, T. P. Yoon, J. Am. Chem. Soc. 2008, 130, 12886–12887;
10.1021/ja805387f
CAS PubMed Web of Science® Google Scholar
12bC. K. Prier, D. A. Rankic, D. W. C. MacMillan, Chem. Rev. 2013, 113, 5322–5363.
10.1021/cr300503r
CAS PubMed Web of Science® Google Scholar
13
13aH. Kashida, T. Doi, T. Sakakibara, T. Hayashi, H. Asanuma, J. Am. Chem. Soc. 2013, 135, 7960–7966;
10.1021/ja401835j
CAS PubMed Web of Science® Google Scholar
13bT. Doi, H. Kashida, H. Asanuma, Org. Biomol. Chem. 2015, 13, 4430–4437.
10.1039/C4OB02520B
CAS PubMed Web of Science® Google Scholar
14
14aT. W. Welch, H. H. Thorp, J. Phys. Chem. 1996, 100, 13829–13836;
10.1021/jp960251n
CAS Web of Science® Google Scholar
14bL. Jacquet, R. J. H. Davies, A. Kirsch-De Mesmaeker, J. M. Kelly, J. Am. Chem. Soc. 1997, 119, 11763–11768.
10.1021/ja971163z
CAS Web of Science® Google Scholar
15M. Oppermann, B. Bauer, T. Rossi, F. Zinna, J. Helbing, J. Lacour, M. Chergui, Optica 2019, 6, 56–60.
10.1364/OPTICA.6.000056
CAS Web of Science® Google Scholar
16F. Bosca, V. Lhiaubet-Vallet, M. C. Cuquerella, J. V. Castell, M. A. Miranda, J. Am. Chem. Soc. 2006, 128, 6318–6319.
10.1021/ja060651g
CAS PubMed Web of Science® Google Scholar
17
17aM. Wrighton, J. Markham, J. Phys. Chem. 1973, 77, 3042–3044;
10.1021/j100644a002
CAS Web of Science® Google Scholar
17bR. R. Islangulov, F. N. Castellano, Angew. Chem. Int. Ed. 2006, 45, 5957–5959.
10.1002/anie.200601615
CAS PubMed Web of Science® Google Scholar
18
18aD. L. Dexter, J. Chem. Phys. 1953, 21, 836–850;
10.1063/1.1699044
CAS Web of Science® Google Scholar
18bN. J. Turro, Modern molecular photochemistry, University Science books, 1991.
Google Scholar
19
19aR. E. Holmlin, R. T. Tong, J. K. Barton, J. Am. Chem. Soc. 1998, 120, 9724–9725;
10.1021/ja982187o
CAS Web of Science® Google Scholar
19bL. Antusch, N. Gaß, H.-A. Wagenknecht, Angew. Chem. Int. Ed. 2017, 56, 1385–1389;
10.1002/anie.201610065
CAS PubMed Web of Science® Google Scholar
19cS. Häcker, M. Schrödter, A. Kuhlmann, H.-A. Wagenknecht, JACS Au 2023, 3, 1843–1850.
10.1021/jacsau.3c00167
PubMed Web of Science® Google Scholar
20
20aF. Strieth-Kalthoff, F. Glorius, Chem 2020, 6, 1888–1903;
10.1016/j.chempr.2020.07.010
CAS Web of Science® Google Scholar
20bJ. Diekmann, J. Gontcharov, S. Fröbel, C. Torres Ziegenbein, W. Zinth, P. Gilch, J. Am. Chem. Soc. 2019, 141, 13643–13653.
10.1021/jacs.9b06521
CAS PubMed Web of Science® Google Scholar
21
21aB. P. Sullivan, D. J. Salmon, T. J. Meyer, Inorg. Chem. 1978, 17, 3334–3341;
10.1021/ic50190a006
CAS Web of Science® Google Scholar
21bM. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, G. Scalmani, V. Barone, G. A. Petersson, H. Nakatsuji, X. Li, M. Caricato, A. V. Marenich, J. Bloino, B. G. Janesko, R. Gomperts, B. Mennucci, H. P. Hratchian, J. V. Ortiz, A. F. Izmaylov, J. L. Sonnenberg, Williams, F. Ding, F. Lipparini, F. Egidi, J. Goings, B. Peng, A. Petrone, T. Henderson, D. Ranasinghe, V. G. Zakrzewski, J. Gao, N. Rega, G. Zheng, W. Liang, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, K. Throssell, J. A. Montgomery Jr., J. E. Peralta, F. Ogliaro, M. J. Bearpark, J. J. Heyd, E. N. Brothers, K. N. Kudin, V. N. Staroverov, T. A. Keith, R. Kobayashi, J. Normand, K. Raghavachari, A. P. Rendell, J. C. Burant, S. S. Iyengar, J. Tomasi, M. Cossi, J. M. Millam, M. Klene, C. Adamo, R. Cammi, J. W. Ochterski, R. L. Martin, K. Morokuma, O. Farkas, J. B. Foresman, D. J. Fox, Gaussian 16 Rev. C.01, Wallingford, CT, 2016;
Google Scholar
21cK. Makino, Y. Hattori, H. Kashida, H. Asanuma, Current Protocols 2021, 1, e106;
10.1002/cpz1.106
CAS PubMed Web of Science® Google Scholar
21dJ. D. Vasta, R. T. Raines, Biochemistry 2016, 55, 3224–3233.
10.1021/acs.biochem.6b00251
CAS PubMed Web of Science® Google Scholar

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Volume63, Issue14

April 2, 2024

e202319516

Site-Selective Photo-Crosslinking of Stilbene Pairs in a DNA Duplex Mediated by Ruthenium Photocatalyst

Graphical Abstract

Abstract

Conflict of interests

Open Research

Data Availability Statement

Supporting Information

References

Citing Literature

References

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Site-Selective Photo-Crosslinking of Stilbene Pairs in a DNA Duplex Mediated by Ruthenium Photocatalyst

Graphical Abstract

Abstract

Conflict of interests

Open Research

Data Availability Statement

Supporting Information

References

Citing Literature

References

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