Short Hydrogen Bonds Enhance Nonaromatic Protein-related Fluorescence

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2021 May 18

PMID 34001606

Citations 7

Authors

Amberley D Stephens

Muhammad Nawaz Qaisrani

Michael T Ruggiero

Gonzalo Diaz Miron

Uriel N Morzan

Mariano C Gonzalez Lebrero

Saul T E Jones

Emiliano Poli

Andrew D Bond

Philippa J Woodhams

Elyse M Kleist

Luca Grisanti

Ralph Gebauer

J Axel Zeitler

Dan Credgington

Ali Hassanali

Gabriele S Kaminski Schierle

Affiliations

Soon will be listed here.

Abstract

Fluorescence in biological systems is usually associated with the presence of aromatic groups. Here, by employing a combined experimental and computational approach, we show that specific hydrogen bond networks can significantly affect fluorescence. In particular, we reveal that the single amino acid L-glutamine, by undergoing a chemical transformation leading to the formation of a short hydrogen bond, displays optical properties that are significantly enhanced compared with L-glutamine itself. Ab initio molecular dynamics simulations highlight that these short hydrogen bonds prevent the appearance of a conical intersection between the excited and the ground states and thereby significantly decrease nonradiative transition probabilities. Our findings open the door to the design of new photoactive materials with biophotonic applications.

Citing Articles

The carbonyl-lock mechanism underlying non-aromatic fluorescence in biological matter.

Diaz Miron G, Semelak J, Grisanti L, Rodriguez A, Conti I, Stella M Nat Commun. 2023; 14(1):7325.

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A Comprehensive Analysis of the Intrinsic Visible Fluorescence Emitted by Peptide/Protein Amyloid-like Assemblies.

Balasco N, Diaferia C, Rosa E, Monti A, Ruvo M, Doti N Int J Mol Sci. 2023; 24(9).

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Intrinsic fluorescence of nucleobase crystals.

Aizen R, Arnon Z, Berger O, Ruggiero A, Zaguri D, Brown N Nanoscale Adv. 2023; 5(2):344-348.

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Unveiling the Metal-Dependent Aggregation Properties of the C-terminal Region of Amyloidogenic Intrinsically Disordered Protein Isoforms DPF3b and DPF3a.

Leyder T, Mignon J, Mottet D, Michaux C Int J Mol Sci. 2022; 23(23).

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One- and Two-Photon Excited Autofluorescence of Lysozyme Amyloids.

Grelich-Mucha M, Lipok M, Rozycka M, Samoc M, Olesiak-Banska J J Phys Chem Lett. 2022; 13(21):4673-4681.

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References

Morzan U, Ramirez F, Oviedo M, Sanchez C, Scherlis D, Gonzalez Lebrero M . Electron dynamics in complex environments with real-time time dependent density functional theory in a QM-MM framework. J Chem Phys. 2014; 140(16):164105. DOI: 10.1063/1.4871688. View

Zhang X, Chen S, Li J . Hydrogen-bond potential for ice VIII-X phase transition. Sci Rep. 2016; 6:37161. PMC: 5107924. DOI: 10.1038/srep37161. View

Geissler P, Dellago C, Chandler D, Hutter J, Parrinello M . Autoionization in liquid water. Science. 2001; 291(5511):2121-4. DOI: 10.1126/science.1056991. View

Law Y, Hassanali A . Role of Quantum Vibrations on the Structural, Electronic, and Optical Properties of 9-Methylguanine. J Phys Chem A. 2015; 119(44):10816-27. DOI: 10.1021/acs.jpca.5b07022. View

Chan F, Kaminski Schierle G, Kumita J, Bertoncini C, Dobson C, Kaminski C . Protein amyloids develop an intrinsic fluorescence signature during aggregation. Analyst. 2013; 138(7):2156-62. PMC: 5360231. DOI: 10.1039/c3an36798c. View

Forneris F, Heuts D, Delvecchio M, Rovida S, Fraaije M, Mattevi A . Structural analysis of the catalytic mechanism and stereoselectivity in Streptomyces coelicolor alditol oxidase. Biochemistry. 2007; 47(3):978-85. DOI: 10.1021/bi701886t. View

Law Y, Hassanali A . The importance of nuclear quantum effects in spectral line broadening of optical spectra and electrostatic properties in aromatic chromophores. J Chem Phys. 2018; 148(10):102331. DOI: 10.1063/1.5005056. View

Tapavicza E, Tavernelli I, Rothlisberger U . Trajectory surface hopping within linear response time-dependent density-functional theory. Phys Rev Lett. 2007; 98(2):023001. DOI: 10.1103/PhysRevLett.98.023001. View

Andresen J, Gayan J, Djousse L, Roberts S, Brocklebank D, Cherny S . The relationship between CAG repeat length and age of onset differs for Huntington's disease patients with juvenile onset or adult onset. Ann Hum Genet. 2006; 71(Pt 3):295-301. DOI: 10.1111/j.1469-1809.2006.00335.x. View

10.

Cuny J, Hassanali A . Ab initio molecular dynamics study of the mechanism of proton recombination with a weak base. J Phys Chem B. 2014; 118(48):13903-12. DOI: 10.1021/jp507246e. View

11.

Goedecker , Teter , HUTTER . Separable dual-space Gaussian pseudopotentials. Phys Rev B Condens Matter. 1996; 54(3):1703-1710. DOI: 10.1103/physrevb.54.1703. View

12.

Zhou S, Wang L . Unraveling the structural and chemical features of biological short hydrogen bonds. Chem Sci. 2019; 10(33):7734-7745. PMC: 6764281. DOI: 10.1039/c9sc01496a. View

13.

Chai J, Head-Gordon M . Long-range corrected hybrid density functionals with damped atom-atom dispersion corrections. Phys Chem Chem Phys. 2008; 10(44):6615-20. DOI: 10.1039/b810189b. View

14.

Shukla A, Mukherjee S, Sharma S, Agrawal V, Radha Kishan K, Guptasarma P . A novel UV laser-induced visible blue radiation from protein crystals and aggregates: scattering artifacts or fluorescence transitions of peptide electrons delocalized through hydrogen bonding?. Arch Biochem Biophys. 2004; 428(2):144-53. DOI: 10.1016/j.abb.2004.05.007. View

15.

Fandrich M, Dobson C . The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation. EMBO J. 2002; 21(21):5682-90. PMC: 131070. DOI: 10.1093/emboj/cdf573. View

16.

Amdursky N, Molotskii M, Aronov D, Adler-Abramovich L, Gazit E, Rosenman G . Blue luminescence based on quantum confinement at peptide nanotubes. Nano Lett. 2009; 9(9):3111-5. DOI: 10.1021/nl9008265. View

17.

Hassanali A, Cuny J, Ceriotti M, Pickard C, Parrinello M . The fuzzy quantum proton in the hydrogen chloride hydrates. J Am Chem Soc. 2012; 134(20):8557-69. DOI: 10.1021/ja3014727. View

18.

Handelman A, Kuritz N, Natan A, Rosenman G . Reconstructive Phase Transition in Ultrashort Peptide Nanostructures and Induced Visible Photoluminescence. Langmuir. 2015; 32(12):2847-62. DOI: 10.1021/acs.langmuir.5b02784. View

19.

Stavrinides A, Tatsis E, Caputi L, Foureau E, Stevenson C, Lawson D . Structural investigation of heteroyohimbine alkaloid synthesis reveals active site elements that control stereoselectivity. Nat Commun. 2016; 7:12116. PMC: 4947188. DOI: 10.1038/ncomms12116. View

20.

Grimme S, Antony J, Ehrlich S, Krieg H . A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu. J Chem Phys. 2010; 132(15):154104. DOI: 10.1063/1.3382344. View