Enhanced Photo-Cross-Linking of Thymines in DNA Holliday Junction-Templated Squaraine Dimers

Basu, Shibani; Roy, Simon K.; Barcenas, German; Li, Lan; Yurke, Bernard; Knowlton, William B.; Lee, Jeunghoon

doi:10.1021/acs.biochem.3c00471

Title: Enhanced Photo-Cross-Linking of Thymines in DNA Holliday Junction-Templated Squaraine Dimers

Journal Article · 30 October 2023 · Biochemistry

DOI: https://doi.org/10.1021/acs.biochem.3c00471 · OSTI ID:2234021

^[1];

^[2];

^[2]

Boise State University, ID (United States); Boise State University
Boise State University, ID (United States)

Programmable self-assembly of dyes using DNA templates to promote exciton delocalization in dye aggregates is gaining considerable interest. New methods to improve the rigidity of the DNA scaffold and thus the stability of the molecular dye aggregates to encourage exciton delocalization are desired. In these dye–DNA constructs, one potential way to increase the stability of the aggregates is to create an additional covalent bond via photo-cross-linking reactions between thymines in the DNA scaffold. Specifically, we report an approach to increase the yield of photo-cross-linking reaction between thymines in the core of a DNA Holliday junction while limiting the damage from UV irradiation to DNA. We investigated the effect of the distance between thymines on the photo-cross-linking reaction yields by using linkers with different lengths to tether the dyes to the DNA templates. By comprehensively evaluating the photo-cross-linking reaction yields of dye–DNA aggregates using linkers with different lengths, we conclude that interstrand thymines tend to photo-cross-link more efficiently with short linkers. A higher cross-linking yield was achieved due to the shorter intermolecular distance between thymines influenced by strong dye–dye interactions. Furthermore, our method establishes the possibility of improving the stability of DNA-scaffolded dye aggregates, thereby expanding their use in exciton-based applications such as light harvesting, nanoscale computing, quantum computing, and optoelectronics.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Boise State University, ID (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division (MSE)

Grant/Contract Number:: SC0020089

OSTI ID:: 2234021

Journal Information:: Biochemistry, Journal Name: Biochemistry Journal Issue: 22 Vol. 62; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (70)

Optical Properties of Vibronically Coupled Cy3 Dimers on DNA Scaffolds Cunningham, Paul D.; Kim, Young C.; Díaz, Sebastián A. The Journal of Physical Chemistry B, Vol. 122, Issue 19 https://doi.org/10.1021/acs.jpcb.8b02134	journal	April 2018
Unraveling the Molecular Pathway from Sunlight to Skin Cancer Taylor, John Stephen Accounts of Chemical Research, Vol. 27, Issue 3 https://doi.org/10.1021/ar00039a003	journal	March 1994
Molecular Aggregate Photophysics beyond the Kasha Model: Novel Design Principles for Organic Materials Hestand, Nicholas J.; Spano, Frank C. Accounts of Chemical Research, Vol. 50, Issue 2 https://doi.org/10.1021/acs.accounts.6b00576	journal	January 2017
Sequence-programmable covalent bonding of designed DNA assemblies Gerling, Thomas; Kube, Massimo; Kick, Benjamin Science Advances, Vol. 4, Issue 8 https://doi.org/10.1126/sciadv.aau1157	journal	August 2018
Engineering couplings for exciton transport using synthetic DNA scaffolds Hart, Stephanie M.; Chen, Wei Jia; Banal, James L. Chem, Vol. 7, Issue 3 https://doi.org/10.1016/j.chempr.2020.12.020	journal	March 2021
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Coherent interactions of dyes assembled on DNA Asanuma, Hiroyuki; Fujii, Taiga; Kato, Tomohiro Journal of Photochemistry and Photobiology C: Photochemistry Reviews, Vol. 13, Issue 2 https://doi.org/10.1016/j.jphotochemrev.2012.04.002	journal	June 2012
Coherent Multidimensional Optical Spectroscopy of Excitons in Molecular Aggregates; Quasiparticle versus Supermolecule Perspectives Abramavicius, Darius; Palmieri, Benoit; Voronine, Dmitri V. Chemical Reviews, Vol. 109, Issue 6 https://doi.org/10.1021/cr800268n	journal	June 2009
DNA single-strand breaks during repair of UV damage in human fibroblasts and abnormalities of repair in xeroderma pigmentosum. Fornace, A. J.; Kohn, K. W.; Kann, H. E. Proceedings of the National Academy of Sciences, Vol. 73, Issue 1 https://doi.org/10.1073/pnas.73.1.39	journal	January 1976
Exciton Delocalization in Indolenine Squaraine Aggregates Templated by DNA Holliday Junction Scaffolds Mass, Olga A.; Wilson, Christopher K.; Roy, Simon K. The Journal of Physical Chemistry B, Vol. 124, Issue 43 https://doi.org/10.1021/acs.jpcb.0c06480	journal	October 2020
Analysis of Coherent Heteroclustering of Different Dyes by Use of Threoninol Nucleotides for Comparison with the Molecular Exciton Theory Fujii, Taiga; Kashida, Hiromu; Asanuma, Hiroyuki Chemistry - A European Journal, Vol. 15, Issue 39 https://doi.org/10.1002/chem.200900962	journal	October 2009
Photochemical modifications for DNA/RNA oligonucleotides Tavakoli, Amirrasoul; Min, Jung-Hyun RSC Advances, Vol. 12, Issue 11 https://doi.org/10.1039/D1RA05951C	journal	January 2022
Hybridization-Sensitive On–Off DNA Probe: Application of the Exciton Coupling Effect to Effective Fluorescence Quenching Ikeda, Shuji; Okamoto, Akimitsu Chemistry – An Asian Journal, Vol. 3, Issue 6 https://doi.org/10.1002/asia.200800014	journal	June 2008
Extended dipole model for aggregates of dye molecules Czikklely, V.; Forsterling, H. D.; Kuhn, H. Chemical Physics Letters, Vol. 6, Issue 3 https://doi.org/10.1016/0009-2614(70)80220-2	journal	August 1970
Effects of combinations of ROS scavengers on oxidative DNA damage caused by visible‐light‐activated camphorquinone/N,N‐dimethyl‐p‐toluidine Lee, Seungbum; Pagoria, Dustin; Raigrodski, Ariel Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 83B, Issue 2 https://doi.org/10.1002/jbm.b.30808	journal	April 2007
Influence of Hydrophobicity on Excitonic Coupling in DNA-Templated Indolenine Squaraine Dye Aggregates Mass, Olga A.; Wilson, Christopher K.; Barcenas, German The Journal of Physical Chemistry C, Vol. 126, Issue 7 https://doi.org/10.1021/acs.jpcc.1c08981	journal	February 2022
Studies of polaron motion Holstein, T. Annals of Physics, Vol. 8, Issue 3 https://doi.org/10.1016/0003-4916(59)90002-8	journal	November 1959
Triplex-directed covalent cross-linking of a DNA nanostructure Rusling, David A.; Nandhakumar, Iris S.; Brown, Tom Chemical Communications, Vol. 48, Issue 77 https://doi.org/10.1039/c2cc35407a	journal	January 2012
DNA Photo-Cross-Linking Using 3-Cyanovinylcarbazole Modified Oligonucleotide with Threoninol Linker Sakamoto, Takashi; Tanaka, Yuya; Fujimoto, Kenzo Organic Letters, Vol. 17, Issue 4 https://doi.org/10.1021/acs.orglett.5b00035	journal	February 2015
Exciton Delocalization and Scaffold Stability in Bridged Nucleotide-Substituted, DNA Duplex-Templated Cyanine Aggregates Roy, Simon K.; Mass, Olga A.; Kellis, Donald L. The Journal of Physical Chemistry B, Vol. 125, Issue 50 https://doi.org/10.1021/acs.jpcb.1c07602	journal	December 2021
Molecular Mechanisms of Ultraviolet Radiation-Induced DNA Damage and Repair Rastogi, Rajesh P.; Kumar, Ashok Journal of Nucleic Acids, Vol. 2010 https://doi.org/10.4061/2010/592980	journal	January 2010
Organic Optoelectronic Materials: Mechanisms and Applications Ostroverkhova, Oksana Chemical Reviews, Vol. 116, Issue 22 https://doi.org/10.1021/acs.chemrev.6b00127	journal	October 2016
Differential biologic effects of CPD and 6-4PP UV-induced DNA damage on the induction of apoptosis and cell-cycle arrest Lo, Hsin-Lung; Nakajima, Satoshi; Ma, Lisa BMC Cancer, Vol. 5, Issue 1 https://doi.org/10.1186/1471-2407-5-135	journal	October 2005
Oxygen Toxicity and Reactive Oxygen Species: The Devil Is in the Details Auten, Richard L.; Davis, Jonathan M. Pediatric Research, Vol. 66, Issue 2 https://doi.org/10.1203/PDR.0b013e3181a9eafb	journal	August 2009
Squaraine as a bright, stable and environment-sensitive far-red label for receptor-specific cellular imaging Karpenko, I. A.; Klymchenko, A. S.; Gioria, S. Chemical Communications, Vol. 51, Issue 14 https://doi.org/10.1039/C4CC09113B	journal	January 2015
On the design of molecular excitonic circuits for quantum computing: the universal quantum gates Castellanos, Maria A.; Dodin, Amro; Willard, Adam P. Physical Chemistry Chemical Physics, Vol. 22, Issue 5 https://doi.org/10.1039/C9CP05625D	journal	January 2020
Perspective: Detecting and measuring exciton delocalization in photosynthetic light harvesting Scholes, Gregory D.; Smyth, Cathal The Journal of Chemical Physics, Vol. 140, Issue 11 https://doi.org/10.1063/1.4869329	journal	March 2014
Unsymmetrical Squaraines Incorporating Quinoline for Near Infrared Responsive Dye-Sensitized Solar Cells Li, Jheng-Ying; Chen, Chia-Yuan; Ho, Wen-Chein Organic Letters, Vol. 14, Issue 21 https://doi.org/10.1021/ol302481k	journal	October 2012
Organic photoconductive materials: recent trends and developments Law, Kock Yee. Chemical Reviews, Vol. 93, Issue 1 https://doi.org/10.1021/cr00017a020	journal	January 1993
DNA−Dye Conjugates for Controllable H* Aggregation ¹ Asanuma, Hiroyuki; Shirasuka, Kenji; Takarada, Tohru Journal of the American Chemical Society, Vol. 125, Issue 8 https://doi.org/10.1021/ja021153k	journal	February 2003
A DNA-Based Light-Harvesting Antenna Garo, Florian; Häner, Robert Angewandte Chemie International Edition, Vol. 51, Issue 4 https://doi.org/10.1002/anie.201103295	journal	December 2011
DNA Assembly of Dye Aggregates—A Possible Path to Quantum Computing Yurke, Bernard Natural Computing Series https://doi.org/10.1007/978-981-19-9891-1_9	book	January 2023
Arylamine-Based Squaraine Donors for Use in Organic Solar Cells Wei, Guodan; Xiao, Xin; Wang, Siyi Nano Letters, Vol. 11, Issue 10 https://doi.org/10.1021/nl2022515	journal	October 2011
Near-Infrared Squaraine Dye Encapsulated Micelles for in Vivo Fluorescence and Photoacoustic Bimodal Imaging Sreejith, Sivaramapanicker; Joseph, James; Lin, Manjing ACS Nano, Vol. 9, Issue 6 https://doi.org/10.1021/acsnano.5b02172	journal	May 2015
Application of electronic circular dichroism in configurational and conformational analysis of organic compounds Berova, Nina; Bari, Lorenzo Di; Pescitelli, Gennaro Chemical Society Reviews, Vol. 36, Issue 6 https://doi.org/10.1039/b515476f	journal	January 2007
Exciton Delocalization in a DNA-Templated Organic Semiconductor Dimer Assembly Wang, Xiao; Sha, Ruojie; Knowlton, William B. ACS Nano, Vol. 16, Issue 1 https://doi.org/10.1021/acsnano.1c09143	journal	January 2022
Coherent Exciton Delocalization in a Two-State DNA-Templated Dye Aggregate System Cannon, Brittany L.; Kellis, Donald L.; Patten, Lance K. The Journal of Physical Chemistry A, Vol. 121, Issue 37 https://doi.org/10.1021/acs.jpca.7b04344	journal	September 2017
Oxidative Stress: Harms and Benefits for Human Health Pizzino, Gabriele; Irrera, Natasha; Cucinotta, Mariapaola Oxidative Medicine and Cellular Longevity, Vol. 2017 https://doi.org/10.1155/2017/8416763	journal	January 2017
Complete Photochemical Regulation of 8–17 DNAzyme Activity by Using Reversible DNA Photo‐crosslinking Watanabe, Yasuha; Fujimoto, Kenzo ChemBioChem, Vol. 21, Issue 22 https://doi.org/10.1002/cbic.202000227	journal	July 2020
Recent Advances in the Synthesis of Cyclobutanes by Olefin [2 + 2] Photocycloaddition Reactions Poplata, Saner; Tröster, Andreas; Zou, You-Quan Chemical Reviews, Vol. 116, Issue 17 https://doi.org/10.1021/acs.chemrev.5b00723	journal	March 2016
Preparation of interstrand cross-linked DNA oligonucleotide duplexes Noll, David, M. Frontiers in Bioscience, Vol. 9, Issue 1-3 https://doi.org/10.2741/1246	journal	January 2004
Theory of exciton-vibrational dynamics in molecular dimers Kühn, Oliver; Renger, Thomas; May, Volkhard Chemical Physics, Vol. 204, Issue 1 https://doi.org/10.1016/0301-0104(95)00448-3	journal	March 1996
Extracting single and two-exciton couplings in photosynthetic complexes by coherent two-dimensional electronic spectra Abramavicius, Darius; Palmieri, Benoit; Mukamel, Shaul Chemical Physics, Vol. 357, Issue 1-3 https://doi.org/10.1016/j.chemphys.2008.10.010	journal	February 2009
Squaraine‐Doped Functional Nanoprobes: Lipophilically Protected Near‐Infrared Fluorescence for Bioimaging Lee, Yong‐Deok; Lim, Chang‐Keun; Kim, Sehoon Advanced Functional Materials, Vol. 20, Issue 17 https://doi.org/10.1002/adfm.201000650	journal	September 2010
Squaraine Dyes: Molecular Design for Different Applications and Remaining Challenges Ilina, Kristina; MacCuaig, William M.; Laramie, Matthew Bioconjugate Chemistry, Vol. 31, Issue 2 https://doi.org/10.1021/acs.bioconjchem.9b00482	journal	July 2019
Resonance Energy Transfer in DNA Duplexes Labeled with Localized Dyes Cunningham, Paul D.; Khachatrian, Ani; Buckhout-White, Susan The Journal of Physical Chemistry B, Vol. 118, Issue 50 https://doi.org/10.1021/jp5065006	journal	December 2014
Exciton Chirality Inversion in Dye Dimers Templated by DNA Holliday Junction Mass, Olga A.; Basu, Shibani; Patten, Lance K. The Journal of Physical Chemistry Letters, Vol. 13, Issue 46 https://doi.org/10.1021/acs.jpclett.2c02721	journal	November 2022
Beneficial and Detrimental Effects of Reactive Oxygen Species on Lifespan: A Comprehensive Review of Comparative and Experimental Studies Shields, Hazel J.; Traa, Annika; Van Raamsdonk, Jeremy M. Frontiers in Cell and Developmental Biology, Vol. 9 https://doi.org/10.3389/fcell.2021.628157	journal	February 2021
Large Davydov Splitting and Strong Fluorescence Suppression: An Investigation of Exciton Delocalization in DNA-Templated Holliday Junction Dye Aggregates Cannon, Brittany L.; Patten, Lance K.; Kellis, Donald L. The Journal of Physical Chemistry A, Vol. 122, Issue 8 https://doi.org/10.1021/acs.jpca.7b12668	journal	February 2018
Photoswitchable Formation of a DNA Interstrand Cross‐Link by a Coumarin‐Modified Nucleotide Haque, Mohammad Mojibul; Sun, Huabing; Liu, Shuo Angewandte Chemie International Edition, Vol. 53, Issue 27 https://doi.org/10.1002/anie.201310609	journal	May 2014
Nanoscale Resonance Energy Transfer-Based Devices for Probabilistic Computing Wang, Siyang; Lebeck, Alvin R.; Dwyer, Chris IEEE Micro, Vol. 35, Issue 5 https://doi.org/10.1109/MM.2015.124	journal	September 2015
DNA-Assisted Self-Assembly of Pyrene Foldamers Häner, Robert; Samain, Florent; Malinovskii, Vladimir L. Chemistry - A European Journal, Vol. 15, Issue 23 https://doi.org/10.1002/chem.200900369	journal	June 2009
Efficient Far Red Sensitization of Nanocrystalline TiO ₂ Films by an Unsymmetrical Squaraine Dye Yum, Jun-Ho; Walter, Pablo; Huber, Simon Journal of the American Chemical Society, Vol. 129, Issue 34 https://doi.org/10.1021/ja0731470	journal	August 2007
Photocrosslinking Probes Proximity of Thymine Modifiers Tethering Excitonically Coupled Dye Aggregates to DNA Holliday Junction Basu, Shibani; Cervantes-Salguero, Keitel; Yurke, Bernard Molecules, Vol. 27, Issue 13 https://doi.org/10.3390/molecules27134006	journal	June 2022
The Cartography of UV‐induced DNA Damage Formation and DNA Repair Hu, Jinchuan; Adar, Sheera Photochemistry and Photobiology, Vol. 93, Issue 1 https://doi.org/10.1111/php.12668	journal	January 2017
Exciton delocalization, charge transfer, and electronic coupling for singlet excitation energy transfer between stacked nucleobases in DNA: An MS-CASPT2 study Blancafort, Lluís; Voityuk, Alexander A. The Journal of Chemical Physics, Vol. 140, Issue 9 https://doi.org/10.1063/1.4867118	journal	March 2014
Synthesis and properties of squaraine-modified DNA Markova, Larysa I.; Malinovskii, Vladimir L.; Patsenker, Leonid D. Organic & Biomolecular Chemistry, Vol. 10, Issue 45 https://doi.org/10.1039/c2ob26787j	journal	January 2012
Programmable materials and the nature of the DNA bond Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Science, Vol. 347, Issue 6224 https://doi.org/10.1126/science.1260901	journal	February 2015
Fluorescent Labeling of Biomolecules with Organic Probes Gonçalves, M. Sameiro T. Chemical Reviews, Vol. 109, Issue 1 https://doi.org/10.1021/cr0783840	journal	January 2009
Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems Monshouwer, René; Abrahamsson, Malin; van Mourik, Frank The Journal of Physical Chemistry B, Vol. 101, Issue 37 https://doi.org/10.1021/jp963377t	journal	September 1997
Squaraine dyes: The hierarchical synthesis and its application in optical detection Xia, Guomin; Wang, Hongming Journal of Photochemistry and Photobiology C: Photochemistry Reviews, Vol. 31 https://doi.org/10.1016/j.jphotochemrev.2017.03.001	journal	June 2017
Nanomaterials Based on DNA Seeman, Nadrian C. Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev-biochem-060308-102244	journal	June 2010
5-Methylcytosine Selective Photoligation Using Photoresponsive Oligonucleotides Containing Various 5-Vinyl-2′-deoxyuridines Having an Aromatic Group Sakamoto, Takashi; Ami, Takehiro; Fujimoto, Kenzo Chemistry Letters, Vol. 41, Issue 1 https://doi.org/10.1246/cl.2012.47	journal	January 2012
DNA Self-Assembly of Single Molecules with Deterministic Position and Orientation Adamczyk, Aleksandra K.; Huijben, Teun A. P. M.; Sison, Miguel ACS Nano, Vol. 16, Issue 10 https://doi.org/10.1021/acsnano.2c06936	journal	September 2022
Molecular Dynamic Studies of Dye–Dye and Dye–DNA Interactions Governing Excitonic Coupling in Squaraine Aggregates Templated by DNA Holliday Junctions Barcenas, German; Biaggne, Austin; Mass, Olga A. International Journal of Molecular Sciences, Vol. 24, Issue 4 https://doi.org/10.3390/ijms24044059	journal	February 2023
Photo-Cross-Linking-Assisted Thermal Stability of DNA Origami Structures and Its Application for Higher-Temperature Self-Assembly Rajendran, Arivazhagan; Endo, Masayuki; Katsuda, Yousuke Journal of the American Chemical Society, Vol. 133, Issue 37 https://doi.org/10.1021/ja204546h	journal	September 2011
The DNA three-way junction as a mould for tripartite chromophore assembly Probst, Markus; Wenger, Daniel; Biner, Sarah M. Org. Biomol. Chem., Vol. 10, Issue 4 https://doi.org/10.1039/C1OB06400B	journal	January 2012
Alkyne–Alkene [2 + 2] cycloaddition based on visible light photocatalysis Ha, Sujin; Lee, Yeji; Kwak, Yoonna Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16283-9	journal	May 2020
Directional Photonic Wire Mediated by Homo-Förster Resonance Energy Transfer on a DNA Origami Platform Nicoli, Francesca; Barth, Anders; Bae, Wooli ACS Nano, Vol. 11, Issue 11 https://doi.org/10.1021/acsnano.7b05631	journal	September 2017
DNA Damage and Interstrand Cross-Link Formation upon Irradiation of Aryl Iodide C-Nucleotide Analogues Ding, Hui; Greenberg, Marc M. The Journal of Organic Chemistry, Vol. 75, Issue 3 https://doi.org/10.1021/jo902071y	journal	January 2010

Similar Records

Photocrosslinking Probes Proximity of Thymine Modifiers Tethering Excitonically Coupled Dye Aggregates to DNA Holliday Junction

Journal Article · 2022 · Molecules · OSTI ID:1873523

Basu, Shibani; Cervantes-Salguero, Keitel; Yurke, Bernard; +3 more

Exciton Delocalization in Indolenine Squaraine Aggregates Templated by DNA Holliday Junction Scaffolds

Journal Article · 2020 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1670511

Mass, Olga A.; Wilson, Christopher Kimo; Roy, Simon K.; +7 more

Effect of Hydrophilicity-Imparting Substituents on Exciton Delocalization in Squaraine Dye Aggregates Covalently Templated to DNA Holliday Junctions

Journal Article · 2023 · Nanoscale · OSTI ID:2234233

Pascual, Gissela; Roy, Simon K.; Barcenas, German; +12 more

Related Subjects

59
37
Adjacent thymines
Interstrand photo−crosslinking
Short linker length
Squaraine dye
Dye−dye interactions
Dyes and pigments
Genetics
Nucleic acid structure
Oligomers
Thymine

Title: Enhanced Photo-Cross-Linking of Thymines in DNA Holliday Junction-Templated Squaraine Dimers

Citation Formats

References (70)

Similar Records

Related Subjects