Cyclic dipeptide peroxosolvates: First direct evidence for hydrogen bonding between hydrogen peroxide and a peptide backbone

Andrei V. Churakov; Dmitry A. Grishanov; Alexander G. Medvedev; Alexey A. Mikhaylov; Tatiana A. Tripol'Skaya; Mikhail V. Vener; Mger A. Navasardyan; Ovadia Lev; Petr V. Prikhodchenko

doi:10.1039/c9ce00892f

Cyclic dipeptide peroxosolvates: First direct evidence for hydrogen bonding between hydrogen peroxide and a peptide backbone

Andrei V. Churakov, Dmitry A. Grishanov, Alexander G. Medvedev, Alexey A. Mikhaylov, Tatiana A. Tripol'Skaya, Mikhail V. Vener, Mger A. Navasardyan, Ovadia Lev, Petr V. Prikhodchenko^*

^*Corresponding author for this work

Institute of Chemistry

Research output: Contribution to journal › Article › peer-review

12 Scopus citations

Abstract

Herein, peroxosolvates of the cyclic dipeptides disarcosine (C₆H₁₀N₂O₂·H₂O₂), dialanine (C₆H₁₀N₂O₂·2(H₂O₂)), diglycine (C₄H₆N₂O₂·2(H₂O₂) and C₄H₆N₂O₂·1.786(H₂O₂)·0.214(H₂O)) were synthesized and studied by single crystal X-ray analysis and periodic DFT calculations. The hydrogen bonding networks of cyclic diglycine peroxosolvate and isomorphous hydrate were characterized using Bader analysis of periodic electron density and empirical correlations between enthalpy and metric and spectroscopic parameters of the H-bond. The obtained data for the peroxosolvate of cyclic dipeptides provided a molecular-level insight into the non-redox interaction of hydrogen peroxide with the peptide backbone in aqueous systems. In all structures, H₂O₂ acts as a proton donor in two hydrogen bonds. The carbonyl oxygen atom of the peptide (-CO-NH-) forms a relatively stronger hydrogen bond with the hydrogen peroxide molecule (32-34 kJ mol^-1) as compared to that with water in the isomorphous hydrate of cyclic diglycine (26-28 kJ mol^-1). The hydrogen atom of the peptide group (-CO-NH-) can form a moderate H-bond with hydrogen peroxide (25 kJ mol^-1). The total hydrogen bonding energy of the peroxosolvate is higher than that of the corresponding hydrate (91 vs. 82 kJ mol^-1). The stronger hydrogen bonding in peroxosolvates as compared to that in the hydrate and the fact that the intermolecular H-bonds C(O)NH⋯OCNH between cyclic dipeptides are not found in peroxosolvates, despite being prevalent in the structure of nonsolvated dipeptides, imply that hydrogen peroxide can interfere with the secondary structure of proteins via a mechanism that can lead to reversible inhibition or signaling in living systems.

Original language	American English
Pages (from-to)	4961-4968
Number of pages	8
Journal	CrystEngComm
Volume	21
Issue number	33
DOIs	https://doi.org/10.1039/c9ce00892f
State	Published - 2019

Bibliographical note

Funding Information:
X-ray diffraction studies were performed at the JRC PMR IGIC RAS. The authors acknowledge the Russian Foundation for Basic Research for providing the financial support (grants 17-03-00762, 18-03-00973, 18-33-20211, 18-29-19119). The publication was carried out within the State Assignment on Fundamental Research to the Kurnakov Institute of General and Inorganic Chemistry. O. L. thanks partial support of the Israel Science Foundation (grant No 1215/19). M. V. V. and A. G. M. thank Prof. G. L. Perlovich for a possibility to conduct computations using Crystal17.

Publisher Copyright:
© The Royal Society of Chemistry.

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@article{8c38ac11b50242048680e496f17bb3f1,

title = "Cyclic dipeptide peroxosolvates: First direct evidence for hydrogen bonding between hydrogen peroxide and a peptide backbone",

abstract = "Herein, peroxosolvates of the cyclic dipeptides disarcosine (C6H10N2O2·H2O2), dialanine (C6H10N2O2·2(H2O2)), diglycine (C4H6N2O2·2(H2O2) and C4H6N2O2·1.786(H2O2)·0.214(H2O)) were synthesized and studied by single crystal X-ray analysis and periodic DFT calculations. The hydrogen bonding networks of cyclic diglycine peroxosolvate and isomorphous hydrate were characterized using Bader analysis of periodic electron density and empirical correlations between enthalpy and metric and spectroscopic parameters of the H-bond. The obtained data for the peroxosolvate of cyclic dipeptides provided a molecular-level insight into the non-redox interaction of hydrogen peroxide with the peptide backbone in aqueous systems. In all structures, H2O2 acts as a proton donor in two hydrogen bonds. The carbonyl oxygen atom of the peptide (-CO-NH-) forms a relatively stronger hydrogen bond with the hydrogen peroxide molecule (32-34 kJ mol-1) as compared to that with water in the isomorphous hydrate of cyclic diglycine (26-28 kJ mol-1). The hydrogen atom of the peptide group (-CO-NH-) can form a moderate H-bond with hydrogen peroxide (25 kJ mol-1). The total hydrogen bonding energy of the peroxosolvate is higher than that of the corresponding hydrate (91 vs. 82 kJ mol-1). The stronger hydrogen bonding in peroxosolvates as compared to that in the hydrate and the fact that the intermolecular H-bonds C(O)NH⋯OCNH between cyclic dipeptides are not found in peroxosolvates, despite being prevalent in the structure of nonsolvated dipeptides, imply that hydrogen peroxide can interfere with the secondary structure of proteins via a mechanism that can lead to reversible inhibition or signaling in living systems.",

author = "Churakov, {Andrei V.} and Grishanov, {Dmitry A.} and Medvedev, {Alexander G.} and Mikhaylov, {Alexey A.} and Tripol'Skaya, {Tatiana A.} and Vener, {Mikhail V.} and Navasardyan, {Mger A.} and Ovadia Lev and Prikhodchenko, {Petr V.}",

note = "Funding Information: X-ray diffraction studies were performed at the JRC PMR IGIC RAS. The authors acknowledge the Russian Foundation for Basic Research for providing the financial support (grants 17-03-00762, 18-03-00973, 18-33-20211, 18-29-19119). The publication was carried out within the State Assignment on Fundamental Research to the Kurnakov Institute of General and Inorganic Chemistry. O. L. thanks partial support of the Israel Science Foundation (grant No 1215/19). M. V. V. and A. G. M. thank Prof. G. L. Perlovich for a possibility to conduct computations using Crystal17. Publisher Copyright: {\textcopyright} The Royal Society of Chemistry.",

year = "2019",

doi = "10.1039/c9ce00892f",

language = "American English",

volume = "21",

pages = "4961--4968",

journal = "CrystEngComm",

issn = "1466-8033",

publisher = "Royal Society of Chemistry",

number = "33",

}

TY - JOUR

T1 - Cyclic dipeptide peroxosolvates

T2 - First direct evidence for hydrogen bonding between hydrogen peroxide and a peptide backbone

AU - Churakov, Andrei V.

AU - Grishanov, Dmitry A.

AU - Medvedev, Alexander G.

AU - Mikhaylov, Alexey A.

AU - Tripol'Skaya, Tatiana A.

AU - Vener, Mikhail V.

AU - Navasardyan, Mger A.

AU - Lev, Ovadia

AU - Prikhodchenko, Petr V.

N1 - Funding Information: X-ray diffraction studies were performed at the JRC PMR IGIC RAS. The authors acknowledge the Russian Foundation for Basic Research for providing the financial support (grants 17-03-00762, 18-03-00973, 18-33-20211, 18-29-19119). The publication was carried out within the State Assignment on Fundamental Research to the Kurnakov Institute of General and Inorganic Chemistry. O. L. thanks partial support of the Israel Science Foundation (grant No 1215/19). M. V. V. and A. G. M. thank Prof. G. L. Perlovich for a possibility to conduct computations using Crystal17. Publisher Copyright: © The Royal Society of Chemistry.

PY - 2019

Y1 - 2019

N2 - Herein, peroxosolvates of the cyclic dipeptides disarcosine (C6H10N2O2·H2O2), dialanine (C6H10N2O2·2(H2O2)), diglycine (C4H6N2O2·2(H2O2) and C4H6N2O2·1.786(H2O2)·0.214(H2O)) were synthesized and studied by single crystal X-ray analysis and periodic DFT calculations. The hydrogen bonding networks of cyclic diglycine peroxosolvate and isomorphous hydrate were characterized using Bader analysis of periodic electron density and empirical correlations between enthalpy and metric and spectroscopic parameters of the H-bond. The obtained data for the peroxosolvate of cyclic dipeptides provided a molecular-level insight into the non-redox interaction of hydrogen peroxide with the peptide backbone in aqueous systems. In all structures, H2O2 acts as a proton donor in two hydrogen bonds. The carbonyl oxygen atom of the peptide (-CO-NH-) forms a relatively stronger hydrogen bond with the hydrogen peroxide molecule (32-34 kJ mol-1) as compared to that with water in the isomorphous hydrate of cyclic diglycine (26-28 kJ mol-1). The hydrogen atom of the peptide group (-CO-NH-) can form a moderate H-bond with hydrogen peroxide (25 kJ mol-1). The total hydrogen bonding energy of the peroxosolvate is higher than that of the corresponding hydrate (91 vs. 82 kJ mol-1). The stronger hydrogen bonding in peroxosolvates as compared to that in the hydrate and the fact that the intermolecular H-bonds C(O)NH⋯OCNH between cyclic dipeptides are not found in peroxosolvates, despite being prevalent in the structure of nonsolvated dipeptides, imply that hydrogen peroxide can interfere with the secondary structure of proteins via a mechanism that can lead to reversible inhibition or signaling in living systems.

AB - Herein, peroxosolvates of the cyclic dipeptides disarcosine (C6H10N2O2·H2O2), dialanine (C6H10N2O2·2(H2O2)), diglycine (C4H6N2O2·2(H2O2) and C4H6N2O2·1.786(H2O2)·0.214(H2O)) were synthesized and studied by single crystal X-ray analysis and periodic DFT calculations. The hydrogen bonding networks of cyclic diglycine peroxosolvate and isomorphous hydrate were characterized using Bader analysis of periodic electron density and empirical correlations between enthalpy and metric and spectroscopic parameters of the H-bond. The obtained data for the peroxosolvate of cyclic dipeptides provided a molecular-level insight into the non-redox interaction of hydrogen peroxide with the peptide backbone in aqueous systems. In all structures, H2O2 acts as a proton donor in two hydrogen bonds. The carbonyl oxygen atom of the peptide (-CO-NH-) forms a relatively stronger hydrogen bond with the hydrogen peroxide molecule (32-34 kJ mol-1) as compared to that with water in the isomorphous hydrate of cyclic diglycine (26-28 kJ mol-1). The hydrogen atom of the peptide group (-CO-NH-) can form a moderate H-bond with hydrogen peroxide (25 kJ mol-1). The total hydrogen bonding energy of the peroxosolvate is higher than that of the corresponding hydrate (91 vs. 82 kJ mol-1). The stronger hydrogen bonding in peroxosolvates as compared to that in the hydrate and the fact that the intermolecular H-bonds C(O)NH⋯OCNH between cyclic dipeptides are not found in peroxosolvates, despite being prevalent in the structure of nonsolvated dipeptides, imply that hydrogen peroxide can interfere with the secondary structure of proteins via a mechanism that can lead to reversible inhibition or signaling in living systems.

UR - http://www.scopus.com/inward/record.url?scp=85070960885&partnerID=8YFLogxK

U2 - 10.1039/c9ce00892f

DO - 10.1039/c9ce00892f

M3 - Article

AN - SCOPUS:85070960885

SN - 1466-8033

VL - 21

SP - 4961

EP - 4968

JO - CrystEngComm

JF - CrystEngComm

IS - 33

ER -

Cyclic dipeptide peroxosolvates: First direct evidence for hydrogen bonding between hydrogen peroxide and a peptide backbone

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