Resonance Energy Transfer in a Genetically Engineered Polypeptide Results in Unanticipated Fluorescence Intensity

Seeley, Jason P.; Cotlet, Mircea; Eagleton, Aileen M.; Higashiya, Seiichiro; Welch, John T.

doi:10.1002/chem.201804470

Title: Resonance Energy Transfer in a Genetically Engineered Polypeptide Results in Unanticipated Fluorescence Intensity

Journal Article · 08 November 2018 · Chemistry - A European Journal

DOI: https://doi.org/10.1002/chem.201804470 · OSTI ID:1504878

Seeley, Jason P. ^[1];

^[2]; Eagleton, Aileen M. ^[1]; Higashiya, Seiichiro ^[1];

^[1]

Univ. at Albany, SUNY, Albany, NY (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)

The fluorescence intensity of a C-terminal acceptor chromophore, N-(7-dimethylamino-4-methyl coumarin (DACM), increased proportionally with 280 nm irradiation of an increasing number of donor tryptophan residues located on a β-sheet forming polypeptide. The fluorescence intensity of the acceptor chromophore increased even as the length of the β-sheet edge approached 256 Å, well beyond the Förster radius for the tryptophan–acceptor chromophore pair. Here the folding of the peptides under investigation was verified by circular dichroism (CD) and deep UV resonance Raman experiments. Control experiments showed that the enhancement of DACM fluorescence occurred concomitantly with peptide folding. In other control experiments, the DACM fluorescence intensity of the solutions of tryptophan and DACM did not show any enhancement of DACM fluorescence with increasing tryptophan concentrations. Formation of fibrillar aggregates of the substrate peptides prepared for the fluorescence studies was undetectable by thioflavin T (ThT) fluorescence.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0012704

OSTI ID:: 1504878

Report Number(s):: BNL--211501-2019-JAAM

Journal Information:: Chemistry - A European Journal, Journal Name: Chemistry - A European Journal Journal Issue: 4 Vol. 25; ISSN 0947-6539

Publisher:: ChemPubSoc EuropeCopyright Statement

Country of Publication:: United States

Language:: English

References (54)

Dendritisch eingeschlossene aktive Zentren: Anwendung des Isolationsprinzips der Natur in der Biomimetik und den Materialwissenschaften Hecht, Stefan; Fréchet, Jean M. J. Angewandte Chemie, Vol. 113, Issue 1 https://doi.org/10.1002/1521-3757(20010105)113:1<76::AID-ANGE76>3.0.CO;2-F	journal	January 2001
Dendritic Encapsulation of Function: Applying Nature's Site Isolation Principle from Biomimetics to Materials Science Hecht, Stefan; Fréchet, Jean M. J. Angewandte Chemie International Edition, Vol. 40, Issue 1 https://doi.org/10.1002/1521-3773(20010105)40:1<74::AID-ANIE74>3.0.CO;2-C	journal	January 2001
Molecular Materials by Self-Assembly of Porphyrins, Phthalocyanines, and Perylenes Elemans, J. A. A. W.; van Hameren, R.; Nolte, R. J. M. Advanced Materials, Vol. 18, Issue 10 https://doi.org/10.1002/adma.200502498	journal	May 2006
Macromolecular Scaffolding: The Relationship Between Nanoscale Architecture and Function in Multichromophoric Arrays for Organic Electronics Palermo, Vincenzo; Schwartz, Erik; Finlayson, Chris E. Advanced Materials, Vol. 22, Issue 8 https://doi.org/10.1002/adma.200903672	journal	February 2010
Peptide-Modulated Self-Assembly of Chromophores toward Biomimetic Light-Harvesting Nanoarchitectonics Zou, Qianli; Liu, Kai; Abbas, Manzar Advanced Materials, Vol. 28, Issue 6 https://doi.org/10.1002/adma.201502454	journal	August 2015
Elektronischer Energietransfer über lange Distanzen in lichtsammelnden supramolekularen Polymeren Winiger, Christian B.; Li, Shaoguang; Kumar, Ganesh R. Angewandte Chemie, Vol. 126, Issue 49 https://doi.org/10.1002/ange.201407968	journal	October 2014
Templated Chromophore Assembly by Dynamic Covalent Bonds Rocard, Lou; Berezin, Andrey; De Leo, Federica Angewandte Chemie, Vol. 127, Issue 52 https://doi.org/10.1002/ange.201507186	journal	December 2015
Long-Distance Electronic Energy Transfer in Light-Harvesting Supramolecular Polymers Winiger, Christian B.; Li, Shaoguang; Kumar, Ganesh R. Angewandte Chemie International Edition, Vol. 53, Issue 49 https://doi.org/10.1002/anie.201407968	journal	October 2014
Templated Chromophore Assembly by Dynamic Covalent Bonds Rocard, Lou; Berezin, Andrey; De Leo, Federica Angewandte Chemie International Edition, Vol. 54, Issue 52 https://doi.org/10.1002/anie.201507186	journal	December 2015
β-sheet folding of 11-kDa fibrillogenic polypeptide is completely aggregation driven Topilina, Natalya I.; Ermolenkov, Vladimir V.; Higashiya, Seiichiro Biopolymers, Vol. 86, Issue 4 https://doi.org/10.1002/bip.20730	journal	January 2007
Aggregation-Controlled Excimer Emission from Anthracene-Containing Polyamidoamine Dendrimers Lekha, P. K.; Prasad, Edamana Chemistry - A European Journal, Vol. 16, Issue 12 https://doi.org/10.1002/chem.200902391	journal	March 2010
Optical Antenna for Photofunctional Molecular Systems Ikeda, Katsuyoshi; Uosaki, Kohei Chemistry - A European Journal, Vol. 18, Issue 6 https://doi.org/10.1002/chem.201102013	journal	January 2012
Light-Harvesting Hybrid Assemblies Rao, K. Venkata; Datta, K. K. R.; Eswaramoorthy, Muthusamy Chemistry - A European Journal, Vol. 18, Issue 8 https://doi.org/10.1002/chem.201103601	journal	January 2012
Designing Dye–Nanochannel Antenna Hybrid Materials for Light Harvesting, Transport and Trapping Calzaferri, Gion; Méallet‐Renault, Rachel; Brühwiler, Dominik ChemPhysChem, Vol. 12, Issue 3 https://doi.org/10.1002/cphc.201000947	journal	February 2011
Dendrimers and other dendritic macromolecules: From building blocks to functional assemblies in nanoscience and nanotechnology: Highlight Fréchet, Jean M. J. Journal of Polymer Science Part A: Polymer Chemistry, Vol. 41, Issue 23 https://doi.org/10.1002/pola.10952	journal	October 2003
Fluorescence Lifetimes of Tryptophan: Structural Origin and Relation with So → 1Lb and So → 1La Transitions René Albani, Jihad Journal of Fluorescence, Vol. 19, Issue 6 https://doi.org/10.1007/s10895-009-0506-7	journal	June 2009
Light Harvesting Dendrimers Nantalaksakul, Arpornrat; Reddy, D. Raghunath; Bardeen, Christopher J. Photosynthesis Research, Vol. 87, Issue 1 https://doi.org/10.1007/s11120-005-8387-3	journal	January 2006
Versatile design of biohybrid light-harvesting architectures to tune location, density, and spectral coverage of attached synthetic chromophores for enhanced energy capture Harris, Michelle A.; Jiang, Jianbing; Niedzwiedzki, Dariusz M. Photosynthesis Research, Vol. 121, Issue 1 https://doi.org/10.1007/s11120-014-9993-8	journal	March 2014
Fluorescence resonance energy transfer Clegg, Robert M. Current Opinion in Biotechnology, Vol. 6, Issue 1 https://doi.org/10.1016/0958-1669(95)80016-6	journal	January 1995
Rnq1 Sondheimer, Neal; Lindquist, Susan Molecular Cell, Vol. 5, Issue 1 https://doi.org/10.1016/S1097-2765(00)80412-8	journal	January 2000
Chameleonic, Light Harvesting Photonic Gels Based on Orthogonal Molecular Fibrillization Felip-León, Carles; Díaz-Oltra, Santiago; Galindo, Francisco Chemistry of Materials, Vol. 28, Issue 21 https://doi.org/10.1021/acs.chemmater.6b03137	journal	October 2016
Nanoscale Strategies for Light Harvesting Kundu, Simanta; Patra, Amitava Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00036	journal	March 2016
Role of Macromolecular Structure in the Ultrafast Energy and Electron Transfer Dynamics of a Light-Harvesting Polymer Morseth, Zachary A.; Pho, Toan V.; Gilligan, Alexander T. The Journal of Physical Chemistry B, Vol. 120, Issue 32 https://doi.org/10.1021/acs.jpcb.6b05589	journal	August 2016
Persistent Charge-Separated States in Self-Assembled Twisted Nonsymmetric Donor–Acceptor Triads Mallia, Ajith R.; Philip, Abbey M.; Bhat, Vinayak The Journal of Physical Chemistry C, Vol. 121, Issue 9 https://doi.org/10.1021/acs.jpcc.6b11153	journal	February 2017
FRET from Multiple Pathways in Fluorophore-Labeled DNA Melinger, Joseph S.; Khachatrian, Ani; Ancona, Mario G. ACS Photonics, Vol. 3, Issue 4 https://doi.org/10.1021/acsphotonics.6b00006	journal	March 2016
One-Dimensional Self-Assembly of Planar π-Conjugated Molecules: Adaptable Building Blocks for Organic Nanodevices Zang, Ling; Che, Yanke; Moore, Jeffrey S. Accounts of Chemical Research, Vol. 41, Issue 12 https://doi.org/10.1021/ar800030w	journal	December 2008
Spectroscopic Determination of Tryptophan and Tyrosine in Proteins ^* Edelhoch, Harold Biochemistry, Vol. 6, Issue 7 https://doi.org/10.1021/bi00859a010	journal	July 1967
Bilayer Fibril Formation by Genetically Engineered Polypeptides: Preparation and Characterization Topilina, Natalya I.; Higashiya, Seiichiro; Rana, Narender Biomacromolecules, Vol. 7, Issue 4 https://doi.org/10.1021/bm0509016	journal	April 2006
Design and Preparation of β-Sheet Forming Repetitive and Block-Copolymerized Polypeptides Higashiya, Seiichiro; Topilina, Natalya I.; Ngo, Silvana C. Biomacromolecules, Vol. 8, Issue 5 https://doi.org/10.1021/bm061098y	journal	May 2007
Fibrillation Mechanism of a Model Intrinsically Disordered Protein Revealed by 2D Correlation Deep UV Resonance Raman Spectroscopy Sikirzhytski, Vitali; Topilina, Natalya I.; Takor, Gaius A. Biomacromolecules, Vol. 13, Issue 5 https://doi.org/10.1021/bm300193f	journal	April 2012
Charge Distribution and Amyloid Fibril Formation: Insights from Genetically Engineered Model Systems Topilina, Natalya I.; Sikirzhytsky, Vitali; Higashiya, Seiichiro Biomacromolecules, Vol. 11, Issue 7 https://doi.org/10.1021/bm901467a	journal	July 2010
Self-Assembled Lanthanide-Cored Dendrimer Complexes: Enhancement of the Luminescence Properties of Lanthanide Ions through Site-Isolation and Antenna Effects Kawa, Manabu; Fréchet, Jean M. J. Chemistry of Materials, Vol. 10, Issue 1 https://doi.org/10.1021/cm970441q	journal	January 1998
Biological Applications of Supramolecular Assemblies Designed for Excitation Energy Transfer Peng, Hui-Qing; Niu, Li-Ya; Chen, Yu-Zhe Chemical Reviews, Vol. 115, Issue 15 https://doi.org/10.1021/cr5007057	journal	June 2015
Electronic excitation transfer in organized molecular assemblies Yamazaki, Iwao.; Tamai, Naoto.; Yamazaki, Tomoko. The Journal of Physical Chemistry, Vol. 94, Issue 2 https://doi.org/10.1021/j100365a007	journal	January 1990
Formation of Mixed Fibrils Demonstrates the Generic Nature and Potential Utility of Amyloid Nanostructures MacPhee, Cait E.; Dobson, Christopher M. Journal of the American Chemical Society, Vol. 122, Issue 51 https://doi.org/10.1021/ja0029580	journal	December 2000
Self-Assembling Light-Harvesting Systems from Synthetically Modified Tobacco Mosaic Virus Coat Proteins Miller, Rebekah A.; Presley, Andrew D.; Francis, Matthew B. Journal of the American Chemical Society, Vol. 129, Issue 11 https://doi.org/10.1021/ja063887t	journal	March 2007
DNA-Directed Artificial Light-Harvesting Antenna Dutta, Palash K.; Varghese, Reji; Nangreave, Jeanette Journal of the American Chemical Society, Vol. 133, Issue 31 https://doi.org/10.1021/ja1115138	journal	August 2011
Genetic Engineering Combined with Deep UV Resonance Raman Spectroscopy for Structural Characterization of Amyloid-like Fibrils Sikirzhytski, Vitali; Topilina, Natalya I.; Higashiya, Seiichiro Journal of the American Chemical Society, Vol. 130, Issue 18 https://doi.org/10.1021/ja8006275	journal	May 2008
Giant Multiporphyrin Arrays as Artificial Light-Harvesting Antennas Imahori, Hiroshi The Journal of Physical Chemistry B, Vol. 108, Issue 20 https://doi.org/10.1021/jp038036b	journal	May 2004
Structural Tuning of Optical Antenna Properties for Plasmonic Enhancement of Photocurrent Generation on a Molecular Monolayer System Ikeda, Katsuyoshi; Takahashi, Kenji; Masuda, Takuya The Journal of Physical Chemistry C, Vol. 116, Issue 39 https://doi.org/10.1021/jp308290v	journal	September 2012
Direct Measurement of Energy Migration in Supramolecular Carbocyanine Dye Nanotubes Clark, Katie A.; Krueger, Emma L.; Vanden Bout, David A. The Journal of Physical Chemistry Letters, Vol. 5, Issue 13 https://doi.org/10.1021/jz500634f	journal	June 2014
Enhancing Long-Range Exciton Guiding in Molecular Nanowires by H-Aggregation Lifetime Engineering Chaudhuri, Debangshu; Li, Dongbo; Che, Yanke Nano Letters, Vol. 11, Issue 2 https://doi.org/10.1021/nl1033039	journal	February 2011
Long-range energy transport in single supramolecular nanofibres at room temperature Haedler, Andreas T.; Kreger, Klaus; Issac, Abey Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14570	journal	July 2015
Two-dimensional artificial light-harvesting antennae with predesigned high-order structure and robust photosensitising activity Feng, Xiao; Ding, Xuesong; Chen, Long Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32944	journal	September 2016
Cascade energy transfer in a conformationally mobile multichromophoric dendrimer Serin, Jason M.; Brousmiche, Darryl W.; Fréchet, Jean M. J. Chem. Commun., Issue 22 https://doi.org/10.1039/B207905D	journal	January 2002
Organogels as scaffolds for excitation energy transfer and light harvesting Ajayaghosh, Ayyappanpillai; Praveen, Vakayil K.; Vijayakumar, Chakkooth Chem. Soc. Rev., Vol. 37, Issue 1 https://doi.org/10.1039/B704456A	journal	January 2008
Mixed non-covalent assemblies of ethynyl nile red and ethynyl pyrene along oligonucleotide templates Ensslen, Philipp; Fritz, Yannic; Wagenknecht, Hans-Achim Organic & Biomolecular Chemistry, Vol. 13, Issue 2 https://doi.org/10.1039/C4OB01860E	journal	January 2015
Supramolecular dendrimers with a [Ru(bpy)3]2+ core and naphthyl peripheral units Plevoets, Marcus; Vögtle, Fritz; De Cola, Luisa New Journal of Chemistry, Vol. 23, Issue 1 https://doi.org/10.1039/a807619g	journal	January 1999
Relative fluorescence quantum yields using a computer-controlled luminescence spectrometer Williams, Alun T. Rhys; Winfield, Stephen A.; Miller, James N. The Analyst, Vol. 108, Issue 1290 https://doi.org/10.1039/an9830801067	journal	January 1983
Possibilities for ‘smart’ materials exploiting the self-assembly of polypeptides into fibrils Channon, Kevin; MacPhee, Cait E. Soft Matter, Vol. 4, Issue 4 https://doi.org/10.1039/b713013a	journal	January 2008
Discovery of energy transfer nanostructures using gelation-driven dynamic combinatorial libraries Nalluri, Siva Krishna Mohan; Ulijn, Rein V. Chemical Science, Vol. 4, Issue 9 https://doi.org/10.1039/c3sc51036k	journal	January 2013
Photosynthetic light harvesting: excitons and coherence Fassioli, Francesca; Dinshaw, Rayomond; Arpin, Paul C. Journal of The Royal Society Interface, Vol. 11, Issue 92 https://doi.org/10.1098/rsif.2013.0901	journal	March 2014
Thioflavin T as an amyloid dye: fibril quantification, optimal concentration and effect on aggregation Xue, Christine; Lin, Tiffany Yuwen; Chang, Dennis Royal Society Open Science, Vol. 4, Issue 1 https://doi.org/10.1098/rsos.160696	journal	January 2017
Fretting about FRET: Correlation between κ and R VanBeek, Darren B.; Zwier, Matthew C.; Shorb, Justin M. Biophysical Journal, Vol. 92, Issue 12 https://doi.org/10.1529/biophysj.106.092650	journal	June 2007

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Related Subjects

77 NANOSCIENCE AND NANOTECHNOLOGY
energy transfer
fluorescence
peptides
photophysics
protein folding

Title: Resonance Energy Transfer in a Genetically Engineered Polypeptide Results in Unanticipated Fluorescence Intensity

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