Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history

Wei Wang; Sabrina Lusvarghi; Rahul Subramanian; Nusrat J. Epsi; Richard Wang; Emilie Goguet; Anthony C. Fries; Fernando Echegaray; Russell Vassell; Si'Ana A. Coggins; Stephanie A. Richard; David A. Lindholm; Katrin Mende; Evan C. Ewers; Derek T. Larson; Rhonda E. Colombo; Christopher J. Colombo; Janet O. Joseph; Julia S. Rozman; Alfred Smith; Tahaniyat Lalani; Catherine M. Berjohn; Ryan C. Maves; Milissa U. Jones; Rupal Mody; Nikhil Huprikar; Jeffrey Livezey; David Saunders; Monique Hollis-Perry; Gregory Wang; Anuradha Ganesan; Mark P. Simons; Christopher C. Broder; David R. Tribble; Eric D. Laing; Brian K. Agan; Timothy H. Burgess; Edward Mitre; Simon D. Pollett; Leah C. Katzelnick; Carol D. Weiss

doi:10.1016/j.chom.2022.10.012

Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history

Wei Wang, Sabrina Lusvarghi, Rahul Subramanian, Nusrat J. Epsi, Richard Wang, Emilie Goguet, Anthony C. Fries, Fernando Echegaray, Russell Vassell, Si'Ana A. Coggins, Stephanie A. Richard, David A. Lindholm, Katrin Mende, Evan C. Ewers, Derek T. Larson, Rhonda E. Colombo, Christopher J. Colombo, Janet O. Joseph, Julia S. Rozman, Alfred SmithTahaniyat Lalani, Catherine M. Berjohn, Ryan C. Maves, Milissa U. Jones, Rupal Mody, Nikhil Huprikar, Jeffrey Livezey, David Saunders, Monique Hollis-Perry, Gregory Wang, Anuradha Ganesan, Mark P. Simons, Christopher C. Broder, David R. Tribble, Eric D. Laing, Brian K. Agan, Timothy H. Burgess, Edward Mitre, Simon D. Pollett^*, Leah C. Katzelnick^*, Carol D. Weiss^*

^*Corresponding author for this work

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

34 Scopus citations

Abstract

The rapid emergence of SARS-CoV-2 variants challenges vaccination strategies. Here, we collected 201 serum samples from persons with a single infection or multiple vaccine exposures, or both. We measured their neutralization titers against 15 natural variants and 7 variants with engineered spike mutations and analyzed antigenic diversity. Antigenic maps of primary infection sera showed that Omicron sublineages BA.2, BA.4/BA.5, and BA.2.12.1 are distinct from BA.1 and more similar to Beta/Gamma/Mu variants. Three mRNA COVID-19 vaccinations increased neutralization of BA.1 more than BA.4/BA.5 or BA.2.12.1. BA.1 post-vaccination infection elicited higher neutralization titers to all variants than three vaccinations alone, although with less neutralization to BA.2.12.1 and BA.4/BA.5. Those with BA.1 infection after two or three vaccinations had similar neutralization titer magnitude and antigenic recognition. Accounting for antigenic differences among variants when interpreting neutralization titers can aid the understanding of complex patterns in humoral immunity that informs the selection of future COVID-19 vaccine strains.

Original language	English
Pages (from-to)	1745-1758.e7
Journal	Cell Host and Microbe
Volume	30
Issue number	12
DOIs	https://doi.org/10.1016/j.chom.2022.10.012
State	Published - 14 Dec 2022
Externally published	Yes

Keywords

COVID-19 vaccine
Omicron
SARS-CoV-2
SARS-CoV-2 variants
antigenic cartography
antigenic landscape
cartography
hybrid immunity
mRNA vaccine
spike

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10.1016/j.chom.2022.10.012

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Wang, W., Lusvarghi, S., Subramanian, R., Epsi, N. J., Wang, R., Goguet, E., Fries, A. C., Echegaray, F., Vassell, R., Coggins, SA. A., Richard, S. A., Lindholm, D. A., Mende, K., Ewers, E. C., Larson, D. T., Colombo, R. E., Colombo, C. J., Joseph, J. O., Rozman, J. S., ... Weiss, C. D. (2022). Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history. Cell Host and Microbe, 30(12), 1745-1758.e7. https://doi.org/10.1016/j.chom.2022.10.012

@article{d41727d79e2c40db94465dbba5b82421,

title = "Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history",

abstract = "The rapid emergence of SARS-CoV-2 variants challenges vaccination strategies. Here, we collected 201 serum samples from persons with a single infection or multiple vaccine exposures, or both. We measured their neutralization titers against 15 natural variants and 7 variants with engineered spike mutations and analyzed antigenic diversity. Antigenic maps of primary infection sera showed that Omicron sublineages BA.2, BA.4/BA.5, and BA.2.12.1 are distinct from BA.1 and more similar to Beta/Gamma/Mu variants. Three mRNA COVID-19 vaccinations increased neutralization of BA.1 more than BA.4/BA.5 or BA.2.12.1. BA.1 post-vaccination infection elicited higher neutralization titers to all variants than three vaccinations alone, although with less neutralization to BA.2.12.1 and BA.4/BA.5. Those with BA.1 infection after two or three vaccinations had similar neutralization titer magnitude and antigenic recognition. Accounting for antigenic differences among variants when interpreting neutralization titers can aid the understanding of complex patterns in humoral immunity that informs the selection of future COVID-19 vaccine strains.",

keywords = "COVID-19 vaccine, Omicron, SARS-CoV-2, SARS-CoV-2 variants, antigenic cartography, antigenic landscape, cartography, hybrid immunity, mRNA vaccine, spike",

author = "Wei Wang and Sabrina Lusvarghi and Rahul Subramanian and Epsi, {Nusrat J.} and Richard Wang and Emilie Goguet and Fries, {Anthony C.} and Fernando Echegaray and Russell Vassell and Coggins, {Si'Ana A.} and Richard, {Stephanie A.} and Lindholm, {David A.} and Katrin Mende and Ewers, {Evan C.} and Larson, {Derek T.} and Colombo, {Rhonda E.} and Colombo, {Christopher J.} and Joseph, {Janet O.} and Rozman, {Julia S.} and Alfred Smith and Tahaniyat Lalani and Berjohn, {Catherine M.} and Maves, {Ryan C.} and Jones, {Milissa U.} and Rupal Mody and Nikhil Huprikar and Jeffrey Livezey and David Saunders and Monique Hollis-Perry and Gregory Wang and Anuradha Ganesan and Simons, {Mark P.} and Broder, {Christopher C.} and Tribble, {David R.} and Laing, {Eric D.} and Agan, {Brian K.} and Burgess, {Timothy H.} and Edward Mitre and Pollett, {Simon D.} and Katzelnick, {Leah C.} and Weiss, {Carol D.}",

note = "Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = dec,

day = "14",

doi = "10.1016/j.chom.2022.10.012",

language = "English",

volume = "30",

pages = "1745--1758.e7",

journal = "Cell Host and Microbe",

issn = "1931-3128",

number = "12",

}

Wang, W, Lusvarghi, S, Subramanian, R, Epsi, NJ, Wang, R, Goguet, E, Fries, AC, Echegaray, F, Vassell, R, Coggins, SAA, Richard, SA , Lindholm, DA , Mende, K, Ewers, EC, Larson, DT, Colombo, RE , Colombo, CJ, Joseph, JO, Rozman, JS, Smith, A, Lalani, T , Berjohn, CM, Maves, RC, Jones, MU, Mody, R, Huprikar, N, Livezey, J, Saunders, D, Hollis-Perry, M, Wang, G, Ganesan, A , Simons, MP, Broder, CC, Tribble, DR, Laing, ED, Agan, BK , Burgess, TH, Mitre, E, Pollett, SD, Katzelnick, LC & Weiss, CD 2022, 'Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history', Cell Host and Microbe, vol. 30, no. 12, pp. 1745-1758.e7. https://doi.org/10.1016/j.chom.2022.10.012

TY - JOUR

T1 - Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history

AU - Wang, Wei

AU - Lusvarghi, Sabrina

AU - Subramanian, Rahul

AU - Epsi, Nusrat J.

AU - Wang, Richard

AU - Goguet, Emilie

AU - Fries, Anthony C.

AU - Echegaray, Fernando

AU - Vassell, Russell

AU - Coggins, Si'Ana A.

AU - Richard, Stephanie A.

AU - Lindholm, David A.

AU - Mende, Katrin

AU - Ewers, Evan C.

AU - Larson, Derek T.

AU - Colombo, Rhonda E.

AU - Colombo, Christopher J.

AU - Joseph, Janet O.

AU - Rozman, Julia S.

AU - Smith, Alfred

AU - Lalani, Tahaniyat

AU - Berjohn, Catherine M.

AU - Maves, Ryan C.

AU - Jones, Milissa U.

AU - Mody, Rupal

AU - Huprikar, Nikhil

AU - Livezey, Jeffrey

AU - Saunders, David

AU - Hollis-Perry, Monique

AU - Wang, Gregory

AU - Ganesan, Anuradha

AU - Simons, Mark P.

AU - Broder, Christopher C.

AU - Tribble, David R.

AU - Laing, Eric D.

AU - Agan, Brian K.

AU - Burgess, Timothy H.

AU - Mitre, Edward

AU - Pollett, Simon D.

AU - Katzelnick, Leah C.

AU - Weiss, Carol D.

PY - 2022/12/14

Y1 - 2022/12/14

N2 - The rapid emergence of SARS-CoV-2 variants challenges vaccination strategies. Here, we collected 201 serum samples from persons with a single infection or multiple vaccine exposures, or both. We measured their neutralization titers against 15 natural variants and 7 variants with engineered spike mutations and analyzed antigenic diversity. Antigenic maps of primary infection sera showed that Omicron sublineages BA.2, BA.4/BA.5, and BA.2.12.1 are distinct from BA.1 and more similar to Beta/Gamma/Mu variants. Three mRNA COVID-19 vaccinations increased neutralization of BA.1 more than BA.4/BA.5 or BA.2.12.1. BA.1 post-vaccination infection elicited higher neutralization titers to all variants than three vaccinations alone, although with less neutralization to BA.2.12.1 and BA.4/BA.5. Those with BA.1 infection after two or three vaccinations had similar neutralization titer magnitude and antigenic recognition. Accounting for antigenic differences among variants when interpreting neutralization titers can aid the understanding of complex patterns in humoral immunity that informs the selection of future COVID-19 vaccine strains.

AB - The rapid emergence of SARS-CoV-2 variants challenges vaccination strategies. Here, we collected 201 serum samples from persons with a single infection or multiple vaccine exposures, or both. We measured their neutralization titers against 15 natural variants and 7 variants with engineered spike mutations and analyzed antigenic diversity. Antigenic maps of primary infection sera showed that Omicron sublineages BA.2, BA.4/BA.5, and BA.2.12.1 are distinct from BA.1 and more similar to Beta/Gamma/Mu variants. Three mRNA COVID-19 vaccinations increased neutralization of BA.1 more than BA.4/BA.5 or BA.2.12.1. BA.1 post-vaccination infection elicited higher neutralization titers to all variants than three vaccinations alone, although with less neutralization to BA.2.12.1 and BA.4/BA.5. Those with BA.1 infection after two or three vaccinations had similar neutralization titer magnitude and antigenic recognition. Accounting for antigenic differences among variants when interpreting neutralization titers can aid the understanding of complex patterns in humoral immunity that informs the selection of future COVID-19 vaccine strains.

KW - COVID-19 vaccine

KW - Omicron

KW - SARS-CoV-2

KW - SARS-CoV-2 variants

KW - antigenic cartography

KW - antigenic landscape

KW - cartography

KW - hybrid immunity

KW - mRNA vaccine

KW - spike

UR - http://www.scopus.com/inward/record.url?scp=85141496873&partnerID=8YFLogxK

U2 - 10.1016/j.chom.2022.10.012

DO - 10.1016/j.chom.2022.10.012

M3 - Article

C2 - 36356586

AN - SCOPUS:85141496873

SN - 1931-3128

VL - 30

SP - 1745-1758.e7

JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 12

ER -

Antigenic cartography of well-characterized human sera shows SARS-CoV-2 neutralization differences based on infection and vaccination history

Abstract

Keywords

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