Lysozyme's lectin-like characteristics facilitates its immune defense function

Ruiyan Zhang; Lisha Wu; Thomas Eckert; Monika Burg-Roderfeld; Miguel A. Rojas-Macias; Thomas Lütteke; Vadim B. Krylov; Dmitry A. Argunov; Aritreyee Datta; Philipp Markart; Andreas Guenther; Bengt Norden; Roland Schauer; Anirban Bhunia; Mushira Abdelaziz Enani; Martin Billeter; Axel J. Scheidig; Nikolay E. Nifantiev; Hans-Christian Siebert

doi:10.1017/s0033583517000075

Lysozyme's lectin-like characteristics facilitates its immune defense function

Ruiyan Zhang, Lisha Wu, Thomas Eckert, Monika Burg-Roderfeld, Miguel A. Rojas-Macias, Thomas Lütteke, Vadim B. Krylov, Dmitry A. Argunov, Aritreyee Datta, Philipp Markart, Andreas Guenther, Bengt Norden, Roland Schauer, Anirban Bhunia, Mushira Abdelaziz Enani, Martin Billeter, Axel J. Scheidig, Nikolay E. Nifantiev, Hans-Christian Siebert

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34 Scopus citations

Abstract

Interactions between human lysozyme (HL) and the lipopolysaccharide (LPS) of Klebsiella pneumoniae O1, a causative agent of lung infection, were identified by surface plasmon resonance. To characterize the molecular mechanism of this interaction, HL binding to synthetic disaccharides and tetrasaccharides representing one and two repeating units, respectively, of the O-chain of this LPS were studied. pH-dependent structural rearrangements of HL after interaction with the disaccharide were observed through nuclear magnetic resonance. The crystal structure of the HL-tetrasaccharide complex revealed carbohydrate chain packing into the A, B, C, and D binding sites of HL, which primarily occurred through residue-specific, direct or water-mediated hydrogen bonds and hydrophobic contacts. Overall, these results support a crucial role of the Glu35/Asp53/Trp63/Asp102 residues in HL binding to the tetrasaccharide. These observations suggest an unknown glycan-guided mechanism that underlies recognition of the bacterial cell wall by lysozyme and may complement the HL immune defense function.

Original language	English (US)
Journal	Quarterly Reviews of Biophysics
Volume	50
DOIs	https://doi.org/10.1017/s0033583517000075
State	Published - May 30 2017
Externally published	Yes

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Zhang, R., Wu, L., Eckert, T., Burg-Roderfeld, M., Rojas-Macias, M. A., Lütteke, T., Krylov, V. B., Argunov, D. A., Datta, A., Markart, P., Guenther, A., Norden, B., Schauer, R., Bhunia, A., Enani, M. A., Billeter, M., Scheidig, A. J., Nifantiev, N. E., & Siebert, H.-C. (2017). Lysozyme's lectin-like characteristics facilitates its immune defense function. Quarterly Reviews of Biophysics, 50. https://doi.org/10.1017/s0033583517000075

@article{69d68f90add54dad9f3e6d0099ec9bbb,

title = "Lysozyme's lectin-like characteristics facilitates its immune defense function",

abstract = "Interactions between human lysozyme (HL) and the lipopolysaccharide (LPS) of Klebsiella pneumoniae O1, a causative agent of lung infection, were identified by surface plasmon resonance. To characterize the molecular mechanism of this interaction, HL binding to synthetic disaccharides and tetrasaccharides representing one and two repeating units, respectively, of the O-chain of this LPS were studied. pH-dependent structural rearrangements of HL after interaction with the disaccharide were observed through nuclear magnetic resonance. The crystal structure of the HL-tetrasaccharide complex revealed carbohydrate chain packing into the A, B, C, and D binding sites of HL, which primarily occurred through residue-specific, direct or water-mediated hydrogen bonds and hydrophobic contacts. Overall, these results support a crucial role of the Glu35/Asp53/Trp63/Asp102 residues in HL binding to the tetrasaccharide. These observations suggest an unknown glycan-guided mechanism that underlies recognition of the bacterial cell wall by lysozyme and may complement the HL immune defense function.",

author = "Ruiyan Zhang and Lisha Wu and Thomas Eckert and Monika Burg-Roderfeld and Rojas-Macias, {Miguel A.} and Thomas L{\"u}tteke and Krylov, {Vadim B.} and Argunov, {Dmitry A.} and Aritreyee Datta and Philipp Markart and Andreas Guenther and Bengt Norden and Roland Schauer and Anirban Bhunia and Enani, {Mushira Abdelaziz} and Martin Billeter and Scheidig, {Axel J.} and Nifantiev, {Nikolay E.} and Hans-Christian Siebert",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): KUK-11-008-23 Acknowledgements: The Swedish NMR Centre is acknowledged for supplying instrument time and support. Diffraction data were collected on a P14 operated by EMBL at the PETRAIII storage ring (Hamburg, Germany). We are grateful to the beamline staff for providing assistance in using the beamline. We thank Dr Timothy Weaver (Cincinnati Children's Hospital Medical Center, Cincinnati, USA) for the provision of human recombinant lysozyme. This work was supported by the King Abdullah University of Science and Technology (grant KUK-11-008-23 awarded to B.N. with a Ph.D. position for L.W.) and the European Research Council (ERC-2008-AdG 227700 to B.N.). Beamtime on the P14 at the EMBL outstation in Hamburg was funded by a BioStruct-X grant. We thank the Sialic Acids Society for financial support. The synthetic portion of the work was supported by the RSF (grant 14-23-00199 to N.E.N.). A.D. would like to thank CSIR, Govt. of India for senior research fellowship. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

year = "2017",

month = may,

day = "30",

doi = "10.1017/s0033583517000075",

language = "English (US)",

volume = "50",

journal = "Quarterly Reviews of Biophysics",

issn = "0033-5835",

publisher = "Cambridge University Press",

}

Zhang, R, Wu, L, Eckert, T, Burg-Roderfeld, M, Rojas-Macias, MA, Lütteke, T, Krylov, VB, Argunov, DA, Datta, A, Markart, P, Guenther, A, Norden, B, Schauer, R, Bhunia, A, Enani, MA, Billeter, M, Scheidig, AJ, Nifantiev, NE & Siebert, H-C 2017, 'Lysozyme's lectin-like characteristics facilitates its immune defense function', Quarterly Reviews of Biophysics, vol. 50. https://doi.org/10.1017/s0033583517000075

TY - JOUR

T1 - Lysozyme's lectin-like characteristics facilitates its immune defense function

AU - Zhang, Ruiyan

AU - Wu, Lisha

AU - Eckert, Thomas

AU - Burg-Roderfeld, Monika

AU - Rojas-Macias, Miguel A.

AU - Lütteke, Thomas

AU - Krylov, Vadim B.

AU - Argunov, Dmitry A.

AU - Datta, Aritreyee

AU - Markart, Philipp

AU - Guenther, Andreas

AU - Norden, Bengt

AU - Schauer, Roland

AU - Bhunia, Anirban

AU - Enani, Mushira Abdelaziz

AU - Billeter, Martin

AU - Scheidig, Axel J.

AU - Nifantiev, Nikolay E.

AU - Siebert, Hans-Christian

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): KUK-11-008-23 Acknowledgements: The Swedish NMR Centre is acknowledged for supplying instrument time and support. Diffraction data were collected on a P14 operated by EMBL at the PETRAIII storage ring (Hamburg, Germany). We are grateful to the beamline staff for providing assistance in using the beamline. We thank Dr Timothy Weaver (Cincinnati Children's Hospital Medical Center, Cincinnati, USA) for the provision of human recombinant lysozyme. This work was supported by the King Abdullah University of Science and Technology (grant KUK-11-008-23 awarded to B.N. with a Ph.D. position for L.W.) and the European Research Council (ERC-2008-AdG 227700 to B.N.). Beamtime on the P14 at the EMBL outstation in Hamburg was funded by a BioStruct-X grant. We thank the Sialic Acids Society for financial support. The synthetic portion of the work was supported by the RSF (grant 14-23-00199 to N.E.N.). A.D. would like to thank CSIR, Govt. of India for senior research fellowship. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2017/5/30

Y1 - 2017/5/30

N2 - Interactions between human lysozyme (HL) and the lipopolysaccharide (LPS) of Klebsiella pneumoniae O1, a causative agent of lung infection, were identified by surface plasmon resonance. To characterize the molecular mechanism of this interaction, HL binding to synthetic disaccharides and tetrasaccharides representing one and two repeating units, respectively, of the O-chain of this LPS were studied. pH-dependent structural rearrangements of HL after interaction with the disaccharide were observed through nuclear magnetic resonance. The crystal structure of the HL-tetrasaccharide complex revealed carbohydrate chain packing into the A, B, C, and D binding sites of HL, which primarily occurred through residue-specific, direct or water-mediated hydrogen bonds and hydrophobic contacts. Overall, these results support a crucial role of the Glu35/Asp53/Trp63/Asp102 residues in HL binding to the tetrasaccharide. These observations suggest an unknown glycan-guided mechanism that underlies recognition of the bacterial cell wall by lysozyme and may complement the HL immune defense function.

AB - Interactions between human lysozyme (HL) and the lipopolysaccharide (LPS) of Klebsiella pneumoniae O1, a causative agent of lung infection, were identified by surface plasmon resonance. To characterize the molecular mechanism of this interaction, HL binding to synthetic disaccharides and tetrasaccharides representing one and two repeating units, respectively, of the O-chain of this LPS were studied. pH-dependent structural rearrangements of HL after interaction with the disaccharide were observed through nuclear magnetic resonance. The crystal structure of the HL-tetrasaccharide complex revealed carbohydrate chain packing into the A, B, C, and D binding sites of HL, which primarily occurred through residue-specific, direct or water-mediated hydrogen bonds and hydrophobic contacts. Overall, these results support a crucial role of the Glu35/Asp53/Trp63/Asp102 residues in HL binding to the tetrasaccharide. These observations suggest an unknown glycan-guided mechanism that underlies recognition of the bacterial cell wall by lysozyme and may complement the HL immune defense function.

UR - http://hdl.handle.net/10754/624958

UR - https://www.cambridge.org/core/product/identifier/S0033583517000075/type/journal_article

UR - http://www.scopus.com/inward/record.url?scp=85041004776&partnerID=8YFLogxK

U2 - 10.1017/s0033583517000075

DO - 10.1017/s0033583517000075

M3 - Article

SN - 0033-5835

VL - 50

JO - Quarterly Reviews of Biophysics

JF - Quarterly Reviews of Biophysics

ER -

Lysozyme's lectin-like characteristics facilitates its immune defense function

Abstract

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