Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines

Julie Van Coillie; Tamas Pongracz; Tonći Šuštić; Wenjun Wang; Jan Nouta; Mathieu Le Gars; Sofie Keijzer; Federica Linty; Olvi Cristianawati; Jim B.D. Keijser; Remco Visser; Lonneke A. van Vught; Marleen A. Slim; Niels van Mourik; Merel J. Smit; Adam Sander; David E. Schmidt; Maurice Steenhuis; Theo Rispens; Morten A. Nielsen; Benjamin G. Mordmüller; Alexander P.J. Vlaar; C. Ellen van der Schoot; Ramon Roozendaal; Manfred Wuhrer; Gestur Vidarsson; Brent Appelman; Diederik van de Beek; Marije K. Bomers; Justin de Brabander; Matthijs C. Brouwer; David T.P. Buis; Nora Chekrouni; Marit J. van Gils; Menno D. de Jong; Ayesha H.A. Lavell; Sabine E. Olie; Edgar J.G. Peters; Tom D.Y. Reijnders; Michiel Schinkel; Alex R. Schuurman; Jonne J. Sikkens; Yvo M. Smulders; Joost W. Wiersinga; Antinori Spinello; Cinzia Bassoli; Giovanna Bestetti; Mario Corbellino; Ali Salanti; Thor G. Theander; in collaboration with the UMC COVID-19 S3/HCW study group

doi:10.1016/j.isci.2023.107619

Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines

Julie Van Coillie, Tamas Pongracz, Tonći Šuštić, Wenjun Wang, Jan Nouta, Mathieu Le Gars, Sofie Keijzer, Federica Linty, Olvi Cristianawati, Jim B.D. Keijser, Remco Visser, Lonneke A. van Vught, Marleen A. Slim, Niels van Mourik, Merel J. Smit, Adam Sander, David E. Schmidt, Maurice Steenhuis, Theo Rispens, Morten A. NielsenBenjamin G. Mordmüller, Alexander P.J. Vlaar, C. Ellen van der Schoot, Ramon Roozendaal, Manfred Wuhrer, Gestur Vidarsson^*, Brent Appelman, Diederik van de Beek, Marije K. Bomers, Justin de Brabander, Matthijs C. Brouwer, David T.P. Buis, Nora Chekrouni, Marit J. van Gils, Menno D. de Jong, Ayesha H.A. Lavell, Sabine E. Olie, Edgar J.G. Peters, Tom D.Y. Reijnders, Michiel Schinkel, Alex R. Schuurman, Jonne J. Sikkens, Yvo M. Smulders, Joost W. Wiersinga, Antinori Spinello, Cinzia Bassoli, Giovanna Bestetti, Mario Corbellino, Ali Salanti, Thor G. Theander, in collaboration with the UMC COVID-19 S3/HCW study group

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

6 Citations (Scopus)

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Abstract

IgG antibodies are important mediators of vaccine-induced immunity through complement- and Fc receptor-dependent effector functions. Both are influenced by the composition of the conserved N-linked glycan located in the IgG Fc domain. Here, we compared the anti-Spike (S) IgG1 Fc glycosylation profiles in response to mRNA, adenoviral, and protein-based COVID-19 vaccines by mass spectrometry (MS). All vaccines induced a transient increase of antigen-specific IgG1 Fc galactosylation and sialylation. An initial, transient increase of afucosylated IgG was induced by membrane-encoding S protein formulations. A fucose-sensitive ELISA for antigen-specific IgG (FEASI) exploiting FcγRIIIa affinity for afucosylated IgG was used as an orthogonal method to confirm the LC-MS-based afucosylation readout. Our data suggest that vaccine-induced anti-S IgG glycosylation is dynamic, and although variation is seen between different vaccine platforms and individuals, the evolution of glycosylation patterns display marked overlaps.

Original language	English
Article number	107619
Journal	iScience
Volume	26
Issue number	9
Pages (from-to)	1-15
ISSN	2589-0042
DOIs	https://doi.org/10.1016/j.isci.2023.107619
Publication status	Published - 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s)

Keywords

Glycomics
Immune response
Immunology
Microbiology

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Cite this

Van Coillie, J., Pongracz, T., Šuštić, T., Wang, W., Nouta, J., Le Gars, M., Keijzer, S., Linty, F., Cristianawati, O., Keijser, J. B. D., Visser, R., van Vught, L. A., Slim, M. A., van Mourik, N., Smit, M. J., Sander, A., Schmidt, D. E., Steenhuis, M., Rispens, T., ... in collaboration with the UMC COVID-19 S3/HCW study group (2023). Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines. iScience, 26(9), 1-15. [107619]. https://doi.org/10.1016/j.isci.2023.107619

Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines. / Van Coillie, Julie; Pongracz, Tamas; Šuštić, Tonći; Wang, Wenjun; Nouta, Jan; Le Gars, Mathieu; Keijzer, Sofie; Linty, Federica; Cristianawati, Olvi; Keijser, Jim B.D.; Visser, Remco; van Vught, Lonneke A.; Slim, Marleen A.; van Mourik, Niels; Smit, Merel J.; Sander, Adam; Schmidt, David E.; Steenhuis, Maurice; Rispens, Theo; Nielsen, Morten A.; Mordmüller, Benjamin G.; Vlaar, Alexander P.J.; Ellen van der Schoot, C.; Roozendaal, Ramon; Wuhrer, Manfred; Vidarsson, Gestur; Appelman, Brent; van de Beek, Diederik; Bomers, Marije K.; de Brabander, Justin; Brouwer, Matthijs C.; Buis, David T.P.; Chekrouni, Nora; van Gils, Marit J.; de Jong, Menno D.; Lavell, Ayesha H.A.; Olie, Sabine E.; Peters, Edgar J.G.; Reijnders, Tom D.Y.; Schinkel, Michiel; Schuurman, Alex R.; Sikkens, Jonne J.; Smulders, Yvo M.; Wiersinga, Joost W.; Spinello, Antinori; Bassoli, Cinzia; Bestetti, Giovanna; Corbellino, Mario; Salanti, Ali ; Theander, Thor G.; in collaboration with the UMC COVID-19 S3/HCW study group.

In: iScience, Vol. 26, No. 9, 107619, 2023, p. 1-15.

Research output: Contribution to journal › Journal article › Research › peer-review

Van Coillie, J, Pongracz, T, Šuštić, T, Wang, W, Nouta, J, Le Gars, M, Keijzer, S, Linty, F, Cristianawati, O, Keijser, JBD, Visser, R, van Vught, LA, Slim, MA, van Mourik, N, Smit, MJ, Sander, A, Schmidt, DE, Steenhuis, M, Rispens, T, Nielsen, MA, Mordmüller, BG, Vlaar, APJ, Ellen van der Schoot, C, Roozendaal, R, Wuhrer, M, Vidarsson, G, Appelman, B, van de Beek, D, Bomers, MK, de Brabander, J, Brouwer, MC, Buis, DTP, Chekrouni, N, van Gils, MJ, de Jong, MD, Lavell, AHA, Olie, SE, Peters, EJG, Reijnders, TDY, Schinkel, M, Schuurman, AR, Sikkens, JJ, Smulders, YM, Wiersinga, JW, Spinello, A, Bassoli, C, Bestetti, G, Corbellino, M, Salanti, A , Theander, TG & in collaboration with the UMC COVID-19 S3/HCW study group 2023, 'Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines', iScience, vol. 26, no. 9, 107619, pp. 1-15. https://doi.org/10.1016/j.isci.2023.107619

Van Coillie, Julie ; Pongracz, Tamas ; Šuštić, Tonći ; Wang, Wenjun ; Nouta, Jan ; Le Gars, Mathieu ; Keijzer, Sofie ; Linty, Federica ; Cristianawati, Olvi ; Keijser, Jim B.D. ; Visser, Remco ; van Vught, Lonneke A. ; Slim, Marleen A. ; van Mourik, Niels ; Smit, Merel J. ; Sander, Adam ; Schmidt, David E. ; Steenhuis, Maurice ; Rispens, Theo ; Nielsen, Morten A. ; Mordmüller, Benjamin G. ; Vlaar, Alexander P.J. ; Ellen van der Schoot, C. ; Roozendaal, Ramon ; Wuhrer, Manfred ; Vidarsson, Gestur ; Appelman, Brent ; van de Beek, Diederik ; Bomers, Marije K. ; de Brabander, Justin ; Brouwer, Matthijs C. ; Buis, David T.P. ; Chekrouni, Nora ; van Gils, Marit J. ; de Jong, Menno D. ; Lavell, Ayesha H.A. ; Olie, Sabine E. ; Peters, Edgar J.G. ; Reijnders, Tom D.Y. ; Schinkel, Michiel ; Schuurman, Alex R. ; Sikkens, Jonne J. ; Smulders, Yvo M. ; Wiersinga, Joost W. ; Spinello, Antinori ; Bassoli, Cinzia ; Bestetti, Giovanna ; Corbellino, Mario ; Salanti, Ali ; Theander, Thor G. ; in collaboration with the UMC COVID-19 S3/HCW study group. / Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines. In: iScience. 2023 ; Vol. 26, No. 9. pp. 1-15.

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title = "Comparative analysis of spike-specific IgG Fc glycoprofiles elicited by adenoviral, mRNA, and protein-based SARS-CoV-2 vaccines",

abstract = "IgG antibodies are important mediators of vaccine-induced immunity through complement- and Fc receptor-dependent effector functions. Both are influenced by the composition of the conserved N-linked glycan located in the IgG Fc domain. Here, we compared the anti-Spike (S) IgG1 Fc glycosylation profiles in response to mRNA, adenoviral, and protein-based COVID-19 vaccines by mass spectrometry (MS). All vaccines induced a transient increase of antigen-specific IgG1 Fc galactosylation and sialylation. An initial, transient increase of afucosylated IgG was induced by membrane-encoding S protein formulations. A fucose-sensitive ELISA for antigen-specific IgG (FEASI) exploiting FcγRIIIa affinity for afucosylated IgG was used as an orthogonal method to confirm the LC-MS-based afucosylation readout. Our data suggest that vaccine-induced anti-S IgG glycosylation is dynamic, and although variation is seen between different vaccine platforms and individuals, the evolution of glycosylation patterns display marked overlaps.",

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author = "{Van Coillie}, Julie and Tamas Pongracz and Ton{\'c}i {\v S}u{\v s}ti{\'c} and Wenjun Wang and Jan Nouta and {Le Gars}, Mathieu and Sofie Keijzer and Federica Linty and Olvi Cristianawati and Keijser, {Jim B.D.} and Remco Visser and {van Vught}, {Lonneke A.} and Slim, {Marleen A.} and {van Mourik}, Niels and Smit, {Merel J.} and Adam Sander and Schmidt, {David E.} and Maurice Steenhuis and Theo Rispens and Nielsen, {Morten A.} and Mordm{\"u}ller, {Benjamin G.} and Vlaar, {Alexander P.J.} and {Ellen van der Schoot}, C. and Ramon Roozendaal and Manfred Wuhrer and Gestur Vidarsson and Brent Appelman and {van de Beek}, Diederik and Bomers, {Marije K.} and {de Brabander}, Justin and Brouwer, {Matthijs C.} and Buis, {David T.P.} and Nora Chekrouni and {van Gils}, {Marit J.} and {de Jong}, {Menno D.} and Lavell, {Ayesha H.A.} and Olie, {Sabine E.} and Peters, {Edgar J.G.} and Reijnders, {Tom D.Y.} and Michiel Schinkel and Schuurman, {Alex R.} and Sikkens, {Jonne J.} and Smulders, {Yvo M.} and Wiersinga, {Joost W.} and Antinori Spinello and Cinzia Bassoli and Giovanna Bestetti and Mario Corbellino and Ali Salanti and Theander, {Thor G.} and {in collaboration with the UMC COVID-19 S3/HCW study group}",

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year = "2023",

doi = "10.1016/j.isci.2023.107619",

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AU - Van Coillie, Julie

AU - Pongracz, Tamas

AU - Šuštić, Tonći

AU - Wang, Wenjun

AU - Nouta, Jan

AU - Le Gars, Mathieu

AU - Keijzer, Sofie

AU - Linty, Federica

AU - Cristianawati, Olvi

AU - Keijser, Jim B.D.

AU - Visser, Remco

AU - van Vught, Lonneke A.

AU - Slim, Marleen A.

AU - van Mourik, Niels

AU - Smit, Merel J.

AU - Sander, Adam

AU - Schmidt, David E.

AU - Steenhuis, Maurice

AU - Rispens, Theo

AU - Nielsen, Morten A.

AU - Mordmüller, Benjamin G.

AU - Vlaar, Alexander P.J.

AU - Ellen van der Schoot, C.

AU - Roozendaal, Ramon

AU - Wuhrer, Manfred

AU - Vidarsson, Gestur

AU - Appelman, Brent

AU - van de Beek, Diederik

AU - Bomers, Marije K.

AU - de Brabander, Justin

AU - Brouwer, Matthijs C.

AU - Buis, David T.P.

AU - Chekrouni, Nora

AU - van Gils, Marit J.

AU - de Jong, Menno D.

AU - Lavell, Ayesha H.A.

AU - Olie, Sabine E.

AU - Peters, Edgar J.G.

AU - Reijnders, Tom D.Y.

AU - Schinkel, Michiel

AU - Schuurman, Alex R.

AU - Sikkens, Jonne J.

AU - Smulders, Yvo M.

AU - Wiersinga, Joost W.

AU - Spinello, Antinori

AU - Bassoli, Cinzia

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AU - Theander, Thor G.

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N2 - IgG antibodies are important mediators of vaccine-induced immunity through complement- and Fc receptor-dependent effector functions. Both are influenced by the composition of the conserved N-linked glycan located in the IgG Fc domain. Here, we compared the anti-Spike (S) IgG1 Fc glycosylation profiles in response to mRNA, adenoviral, and protein-based COVID-19 vaccines by mass spectrometry (MS). All vaccines induced a transient increase of antigen-specific IgG1 Fc galactosylation and sialylation. An initial, transient increase of afucosylated IgG was induced by membrane-encoding S protein formulations. A fucose-sensitive ELISA for antigen-specific IgG (FEASI) exploiting FcγRIIIa affinity for afucosylated IgG was used as an orthogonal method to confirm the LC-MS-based afucosylation readout. Our data suggest that vaccine-induced anti-S IgG glycosylation is dynamic, and although variation is seen between different vaccine platforms and individuals, the evolution of glycosylation patterns display marked overlaps.

AB - IgG antibodies are important mediators of vaccine-induced immunity through complement- and Fc receptor-dependent effector functions. Both are influenced by the composition of the conserved N-linked glycan located in the IgG Fc domain. Here, we compared the anti-Spike (S) IgG1 Fc glycosylation profiles in response to mRNA, adenoviral, and protein-based COVID-19 vaccines by mass spectrometry (MS). All vaccines induced a transient increase of antigen-specific IgG1 Fc galactosylation and sialylation. An initial, transient increase of afucosylated IgG was induced by membrane-encoding S protein formulations. A fucose-sensitive ELISA for antigen-specific IgG (FEASI) exploiting FcγRIIIa affinity for afucosylated IgG was used as an orthogonal method to confirm the LC-MS-based afucosylation readout. Our data suggest that vaccine-induced anti-S IgG glycosylation is dynamic, and although variation is seen between different vaccine platforms and individuals, the evolution of glycosylation patterns display marked overlaps.

KW - Glycomics

KW - Immune response

KW - Immunology

KW - Microbiology

U2 - 10.1016/j.isci.2023.107619

DO - 10.1016/j.isci.2023.107619

M3 - Journal article

C2 - 37670790

AN - SCOPUS:85169841393

VL - 26

SP - 1

EP - 15

JO - iScience

JF - iScience

SN - 2589-0042

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