Observation of α-Helical Hydrogen-Bond Cooperativity in an Intact Protein

Overview

Journal J Am Chem Soc

Publisher American Chemical Society

Specialty Chemistry

Date 2016 Feb 9

PMID 26853186

Citations 7

Authors

Jingwen Li

Yefei Wang

Jingfei Chen

Zhijun Liu

Ad Bax

Lishan Yao

Affiliations

Soon will be listed here.

Abstract

The presence and extent of hydrogen-bonding (H-bonding) cooperativity in proteins remains a fundamental question, which in the past has been studied extensively, mostly by infrared and fluorescence measurements on model peptides. We demonstrate that such cooperativity can be studied in an intact protein by hydrogen/deuterium exchange NMR spectroscopy. The method is based on the fact that substitution of NH by ND in a backbone amide group slightly weakens the N-H···O═C hydrogen bond. Our results show that such substitution at position i in an α-helix impacts the (1)H and (15)N chemical shifts of the amide sites of residues i - 3 to i + 3. Quantum mechanical calculations indicate that the upfield shifts of (1)H and (15)N resonances at site i, observed upon H/D exchanges at sites i - 3, i + 1, i + 2, and i + 3, correspond to a decrease of the ith backbone amide electric dipole moment, which weakens its H-bonding and long-range electrostatic interactions with other backbone amides in the α-helix. These results provide new quantitative insights into the cooperativity of H-bonding in protein α-helices.

Citing Articles

Detecting the Hydrogen Bond Cooperativity in a Protein β-Sheet by H/D Exchange.

Li J, Chen J, Wang Y, Yao L Int J Mol Sci. 2022; 23(23).

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Anticooperativity of Multiple Halogen Bonds and Its Effect on Stoichiometry of Cocrystals of Perfluorinated Iodobenzenes.

Bedekovic N, Pitesa T, Erakovic M, Stilinovic V, Cincic D Cryst Growth Des. 2022; 22(4):2644-2653.

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Halogen bonding organocatalysis enhanced through intramolecular hydrogen bonds.

Riel A, Decato D, Sun J, Berryman O Chem Commun (Camb). 2022; 58(9):1378-1381.

PMID: 34989732 PMC: 8919959. DOI: 10.1039/d1cc05475a.

Polyol and sugar osmolytes can shorten protein hydrogen bonds to modulate function.

Li J, Chen J, An L, Yuan X, Yao L Commun Biol. 2020; 3(1):528.

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Remarkable Rigidity of the Single α-Helical Domain of Myosin-VI As Revealed by NMR Spectroscopy.

Barnes C, Shen Y, Ying J, Takagi Y, Torchia D, Sellers J J Am Chem Soc. 2019; 141(22):9004-9017.

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References

Rossmeisl J, Norskov J, Jacobsen K . Elastic effects behind cooperative bonding in beta-sheets. J Am Chem Soc. 2004; 126(40):13140-3. DOI: 10.1021/ja0490626. View

Williams S, Causgrove T, Gilmanshin R, Fang K, Callender R, Woodruff W . Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry. 1996; 35(3):691-7. DOI: 10.1021/bi952217p. View

Manalo M, Perez L, LiWang A . Hydrogen-bonding and pi-pi base-stacking interactions are coupled in DNA, as suggested by calculated and experimental trans-Hbond deuterium isotope shifts. J Am Chem Soc. 2007; 129(37):11298-9. DOI: 10.1021/ja0692940. View

Engler N, Ostermann A, Niimura N, Parak F . Hydrogen atoms in proteins: positions and dynamics. Proc Natl Acad Sci U S A. 2003; 100(18):10243-8. PMC: 193546. DOI: 10.1073/pnas.1834279100. View

Wieczorek R, Dannenberg J . Hydrogen-bond cooperativity, vibrational coupling, and dependence of helix stability on changes in amino acid sequence in small 3 10-helical peptides. A density functional theory study. J Am Chem Soc. 2003; 125(46):14065-71. DOI: 10.1021/ja034034t. View

Krantz B, Srivastava A, Nauli S, Baker D, Sauer R, Sosnick T . Understanding protein hydrogen bond formation with kinetic H/D amide isotope effects. Nat Struct Biol. 2002; 9(6):458-63. DOI: 10.1038/nsb794. View

Thompson P, Eaton W, Hofrichter J . Laser temperature jump study of the helix<==>coil kinetics of an alanine peptide interpreted with a 'kinetic zipper' model. Biochemistry. 1997; 36(30):9200-10. DOI: 10.1021/bi9704764. View

Kachalova G, Popov A, Bartunik H . A steric mechanism for inhibition of CO binding to heme proteins. Science. 1999; 284(5413):473-6. DOI: 10.1126/science.284.5413.473. View

Dellarole M, Caro J, Roche J, Fossat M, Barthe P, Garcia-Moreno E B . Evolutionarily Conserved Pattern of Interactions in a Protein Revealed by Local Thermal Expansion Properties. J Am Chem Soc. 2015; 137(29):9354-62. DOI: 10.1021/jacs.5b04320. View

10.

Zeko T, Hannigan S, Jacisin T, Guberman-Pfeffer M, Falcone E, Guildford M . FT-IR spectroscopy and density functional theory calculations of 13C isotopologues of the helical peptide Z-Aib6-OtBu. J Phys Chem B. 2013; 118(1):58-68. DOI: 10.1021/jp408818g. View

11.

Kanematsu Y, Tachikawa M . Theoretical analysis of geometry and NMR isotope shift in hydrogen-bonding center of photoactive yellow protein by combination of multicomponent quantum mechanics and ONIOM scheme. J Chem Phys. 2014; 141(18):185101. DOI: 10.1063/1.4900987. View

12.

Li F, Grishaev A, Ying J, Bax A . Side Chain Conformational Distributions of a Small Protein Derived from Model-Free Analysis of a Large Set of Residual Dipolar Couplings. J Am Chem Soc. 2015; 137(46):14798-811. PMC: 4665082. DOI: 10.1021/jacs.5b10072. View

13.

Vakonakis I, Salazar M, Kang M, Dunbar K, LiWang A . Deuterium isotope effects and fractionation factors of hydrogen-bonded A:T base pairs of DNA. J Biomol NMR. 2003; 25(2):105-12. DOI: 10.1023/a:1022211927051. View

14.

Lakhani A, Roy A, De Poli M, Nakaema M, Formaggio F, Toniolo C . Experimental and theoretical spectroscopic study of 3(10)-helical peptides using isotopic labeling to evaluate vibrational coupling. J Phys Chem B. 2011; 115(19):6252-64. DOI: 10.1021/jp2003134. View

15.

Jaravine V, Cordier F, Grzesiek S . Quantification of H/D isotope effects on protein hydrogen-bonds by h3JNC' and 1JNC' couplings and peptide group 15N and 13C' chemical shifts. J Biomol NMR. 2004; 29(3):309-18. DOI: 10.1023/B:JNMR.0000032516.87434.35. View

16.

Kobko N, Paraskevas L, Del Rio E, Dannenberg J . Cooperativity in amide hydrogen bonding chains: implications for protein-folding models. J Am Chem Soc. 2001; 123(18):4348-9. DOI: 10.1021/ja004271l. View

17.

Davis C, Cooper A, Dyer R . Fast helix formation in the B domain of protein A revealed by site-specific infrared probes. Biochemistry. 2015; 54(9):1758-66. PMC: 4356530. DOI: 10.1021/acs.biochem.5b00037. View

18.

Vakonakis I, LiWang A . N1...N3 hydrogen bonds of A:U base pairs of RNA are stronger than those of A:T base pairs of DNA. J Am Chem Soc. 2004; 126(18):5688-9. DOI: 10.1021/ja048981t. View

19.

Markwick P, Bouvignies G, Blackledge M . Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy. J Am Chem Soc. 2007; 129(15):4724-30. DOI: 10.1021/ja0687668. View

20.

Nisius L, Grzesiek S . Key stabilizing elements of protein structure identified through pressure and temperature perturbation of its hydrogen bond network. Nat Chem. 2012; 4(9):711-7. DOI: 10.1038/nchem.1396. View