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Role of intramolecular hydrogen bonds in promoting electron flow through amino acid and oligopeptide conjugates

Orłowski, Rafał and Clark, John A. and Derr, James B. and Espinoza, Eli M. and Mayther, Maximilian F. and Staszewska-Krajewska, Olga and Winkler, Jay R. and Jędrzejewska, Hanna and Szumna, Agnieszka and Gray, Harry B. and Vullev, Valentine I. and Gryko, Daniel T. (2021) Role of intramolecular hydrogen bonds in promoting electron flow through amino acid and oligopeptide conjugates. Proceedings of the National Academy of Sciences of the United States of America, 118 (11). Art. No. e2026462118. ISSN 0027-8424. PMCID PMC7980400. doi:10.1073/pnas.2026462118.

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Elucidating the factors that control charge transfer rates in relatively flexible conjugates is of importance for understanding energy flows in biology as well as assisting the design and construction of electronic devices. Here, we report ultrafast electron transfer (ET) and hole transfer (HT) between a corrole (Cor) donor linked to a perylene-diimide (PDI) acceptor by a tetrameric alanine (Ala)4. Selective photoexcitation of the donor and acceptor triggers subpicosecond and picosecond ET and HT. Replacement of the (Ala)4 linker with either a single alanine or phenylalanine does not substantially affect the ET and HT kinetics. We infer that electronic coupling in these reactions is not mediated by tetrapeptide backbone nor by direct donor–acceptor interactions. Employing a combination of NMR, circular dichroism, and computational studies, we show that intramolecular hydrogen bonding brings the donor and the acceptor into proximity in a “scorpion-shaped” molecular architecture, thereby accounting for the unusually high ET and HT rates. Photoinduced charge transfer relies on a (Cor)NH…O=C–NH…O=C(PDI) electronic-coupling pathway involving two pivotal hydrogen bonds and a central amide group as a mediator. Our work provides guidelines for construction of effective donor–acceptor assemblies linked by long flexible bridges as well as insights into structural motifs for mediating ET and HT in proteins.

Item Type:Article
Related URLs:
URLURL TypeDescription CentralArticle Information
Orłowski, Rafał0000-0002-6250-1914
Derr, James B.0000-0003-1309-9102
Espinoza, Eli M.0000-0002-0134-2833
Mayther, Maximilian F.0000-0003-0749-9046
Winkler, Jay R.0000-0002-4453-9716
Jędrzejewska, Hanna0000-0002-4789-1571
Szumna, Agnieszka0000-0003-3869-1321
Gray, Harry B.0000-0002-7937-7876
Vullev, Valentine I.0000-0002-3416-9686
Gryko, Daniel T.0000-0002-2146-1282
Additional Information:© 2021 National Academy of Sciences. Published under the PNAS license. Contributed by Harry B. Gray, January 17, 2021 (sent for review December 28, 2020; reviewed by David N. Beratan and David I. Schuster). This work was supported by the National Science Centre, Poland (Grants HARMONIA 2016/22/M/ST5/00431 and PRELUDIUM 2016/23/N/ST5/00052), and the NSF (Grants CHE 1800602 and MPS AGEP-GRS to J.A.C.). A.S. and H.J. were supported by National Science Centre Grant 2017/25/B/ST5/01011 and Wroclaw Centre for Networking and Supercomputing Grant 299. Research at the California Institute of Technology was supported by the National Institute of Diabetes and Digestive and Kidney Diseases of the NIH under Award R01DK019038. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Data Availability: All study data are included in the article and/or supporting information. R.O. and J.A.C. contributed equally to this work. Author contributions: R.O., V.I.V., and D.T.G. designed research; R.O., J.A.C., J.B.D., E.M.E., M.F.M., O.S.-K., and H.J. performed research; J.R.W., A.S., H.B.G., V.I.V., and D.T.G. analyzed data; and R.O., J.A.C., J.R.W., H.B.G., V.I.V., and D.T.G. wrote the paper. Reviewers: D.N.B., Duke University; and D.I.S., New York University. The authors declare no competing interest.
Funding AgencyGrant Number
National Science Centre (Poland)HARMONIA 2016/22/M/ST5/00431
National Science Centre (Poland)PRELUDIUM 2016/23/N/ST5/00052
National Science Centre (Poland)2017/25/B/ST5/01011
Wroclaw Centre for Networking and Supercomputing Grant299
Subject Keywords:charge transfer; hydrogen bonding; corrole; folding; perylene diimide
Issue or Number:11
PubMed Central ID:PMC7980400
Record Number:CaltechAUTHORS:20210312-131517680
Persistent URL:
Official Citation:Role of intramolecular hydrogen bonds in promoting electron flow through amino acid and oligopeptide conjugates. Rafał Orłowski, John A. Clark, James B. Derr, Eli M. Espinoza, Maximilian F. Mayther, Olga Staszewska-Krajewska, Jay R. Winkler, Hanna Jędrzejewska, Agnieszka Szumna, Harry B. Gray, Valentine I. Vullev, Daniel T. Gryko. Proceedings of the National Academy of Sciences Mar 2021, 118 (11) e2026462118; DOI: 10.1073/pnas.2026462118
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108414
Deposited By: Tony Diaz
Deposited On:12 Mar 2021 21:35
Last Modified:09 Feb 2022 00:36

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