Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2
Abstract
Immunoglobulin G (IgG) glycosylation critically modulates antibody effector functions. Streptococcus pyogenes secretes a unique endo-β-N-acetylglucosaminidase, EndoS2, which deglycosylates the conserved N-linked glycan at Asn297 on IgG Fc to eliminate its effector functions and evade the immune system. EndoS2 and specific point mutants have been used to chemoenzymatically synthesize antibodies with customizable glycosylation for gain of functions. EndoS2 is useful in these schemes because it accommodates a broad range of N-glycans, including high-mannose, complex, and hybrid types; however, its mechanism of substrate recognition is poorly understood. We present crystal structures of EndoS2 alone and bound to complex and high-mannose glycans; the broad N-glycan specificity is governed by critical loops that shape the binding site of EndoS2. Furthermore, hydrolytic experiments, domain-swap chimeras, and hydrogen–deuterium exchange mass spectrometry reveal the importance of the carbohydrate-binding module in the mechanism of IgG recognition by EndoS2, providing insights into engineering enzymes to catalyze customizable glycosylation reactions.
- Authors:
-
[1];
;
;
[4];
[5];
[1]
- Univ. of Maryland School of Medicine, Baltimore, MD (United States)
- Univ. of Maryland School of Medicine, Baltimore, MD (United States); Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
- Univ. of Maryland School of Pharmacy, Baltimore, MD (United States)
- Univ. of Maryland, College Park, MD (United States)
- CIC bioGUNE, Derio (Spain); Basque Foundation for Science, Bilbao (Spain)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); Ministry of Economic Affairs and Digital Transformation of Spain (MINECO); Federación Española de Enfermedades Raras (FEDER)
- OSTI Identifier:
- 1557279
- Grant/Contract Number:
- AC02-06CH11357; AC02-76SF00515; BFU2016-7427-C2-2-R; IJCI-2014-19206
- Resource Type:
- Accepted Manuscript
- Journal Name:
- ACS Central Science
- Additional Journal Information:
- Journal Volume: 5; Journal Issue: 3; Journal ID: ISSN 2374-7943
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Antennas; Peptides and proteins; Carbohydrates; Crystal structure; Chemical biology
Citation Formats
Klontz, Erik H., Trastoy, Beatriz, Deredge, Daniel, Fields, James K., Li, Chao, Orwenyo, Jared, Marina, Alberto, Beadenkopf, Robert, Günther, Sebastian, Flores, Jair, Wintrode, Patrick L., Wang, Lai-Xi, Guerin, Marcelo E., and Sundberg, Eric J. Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2. United States: N. p., 2019.
Web. doi:10.1021/acscentsci.8b00917.
Klontz, Erik H., Trastoy, Beatriz, Deredge, Daniel, Fields, James K., Li, Chao, Orwenyo, Jared, Marina, Alberto, Beadenkopf, Robert, Günther, Sebastian, Flores, Jair, Wintrode, Patrick L., Wang, Lai-Xi, Guerin, Marcelo E., & Sundberg, Eric J. Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2. United States. https://doi.org/10.1021/acscentsci.8b00917
Klontz, Erik H., Trastoy, Beatriz, Deredge, Daniel, Fields, James K., Li, Chao, Orwenyo, Jared, Marina, Alberto, Beadenkopf, Robert, Günther, Sebastian, Flores, Jair, Wintrode, Patrick L., Wang, Lai-Xi, Guerin, Marcelo E., and Sundberg, Eric J. Wed .
"Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2". United States. https://doi.org/10.1021/acscentsci.8b00917. https://www.osti.gov/servlets/purl/1557279.
@article{osti_1557279,
title = {Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2},
author = {Klontz, Erik H. and Trastoy, Beatriz and Deredge, Daniel and Fields, James K. and Li, Chao and Orwenyo, Jared and Marina, Alberto and Beadenkopf, Robert and Günther, Sebastian and Flores, Jair and Wintrode, Patrick L. and Wang, Lai-Xi and Guerin, Marcelo E. and Sundberg, Eric J.},
abstractNote = {Immunoglobulin G (IgG) glycosylation critically modulates antibody effector functions. Streptococcus pyogenes secretes a unique endo-β-N-acetylglucosaminidase, EndoS2, which deglycosylates the conserved N-linked glycan at Asn297 on IgG Fc to eliminate its effector functions and evade the immune system. EndoS2 and specific point mutants have been used to chemoenzymatically synthesize antibodies with customizable glycosylation for gain of functions. EndoS2 is useful in these schemes because it accommodates a broad range of N-glycans, including high-mannose, complex, and hybrid types; however, its mechanism of substrate recognition is poorly understood. We present crystal structures of EndoS2 alone and bound to complex and high-mannose glycans; the broad N-glycan specificity is governed by critical loops that shape the binding site of EndoS2. Furthermore, hydrolytic experiments, domain-swap chimeras, and hydrogen–deuterium exchange mass spectrometry reveal the importance of the carbohydrate-binding module in the mechanism of IgG recognition by EndoS2, providing insights into engineering enzymes to catalyze customizable glycosylation reactions.},
doi = {10.1021/acscentsci.8b00917},
journal = {ACS Central Science},
number = 3,
volume = 5,
place = {United States},
year = {Wed Feb 06 00:00:00 EST 2019},
month = {Wed Feb 06 00:00:00 EST 2019}
}
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- Glycobiology, Vol. 30, Issue 4