Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination

Carlos A. Sariol; Petraleigh Pantoja; Crisanta Serrano‐collazo; Tiffany Rosa‐arocho; Albersy Armina‐rodríguez; Lorna Cruz; E. Taylor Stone; Teresa Arana; Consuelo Climent; Gerardo Latoni; Dianne Atehortua; Christina Pabon‐carrero; Amelia K. Pinto; James D. Brien; Ana M. Espino

doi:10.3390/v13101972

Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination

Carlos A. Sariol, Petraleigh Pantoja, Crisanta Serrano‐collazo, Tiffany Rosa‐arocho, Albersy Armina‐rodríguez, Lorna Cruz, E. Taylor Stone, Teresa Arana, Consuelo Climent, Gerardo Latoni, Dianne Atehortua, Christina Pabon‐carrero, Amelia K. Pinto, James D. Brien, Ana M. Espino

Microbiology, Immunology, and Molecular Genetics

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

12 Scopus citations

Abstract

Both the SARS‐CoV‐2 pandemic and emergence of variants of concern have highlighted the need for functional antibody assays to monitor the humoral response over time. Antibodies directed against the spike (S) protein of SARS‐CoV‐2 are an important component of the neutralizing antibody response. In this work, we report that in a subset of patients—despite a decline in total S‐specific antibodies—neutralizing antibody titers remain at a similar level for an average of 98 days in longitudinal sampling of a cohort of 59 Hispanic/Latino patients exposed to SARS‐CoV‐2. Our data suggest that 100% of seroconverting patients make detectable neutralizing antibody responses which can be quantified by a surrogate viral neutralization test. Examination of sera from ten out of the 59 subjects which received mRNA‐based vaccination revealed that both IgG titers and neutralizing activity of sera were higher after vaccination compared to a cohort of 21 SARS‐CoV‐2 naïve subjects. One dose was sufficient for the induction of a neutralizing antibody, but two doses were necessary to reach 100% surrogate virus neutralization in subjects irrespective of previous SARS‐ CoV‐2 natural infection status. Like the pattern observed after natural infection, the total anti‐S antibodies titers declined after the second vaccine dose; however, neutralizing activity remained relatively constant for more than 80 days after the first vaccine dose. Furthermore, our data indicates that—compared with mRNA vaccination—natural infection induces a more robust humoral immune response in unexposed subjects. This work is an important contribution to understanding the natural immune response to the novel coronavirus in a population severely impacted by SARS‐ CoV‐2. Furthermore, by comparing the dynamics of the immune response after the natural infection vs. the vaccination, these findings suggest that functional neutralizing antibody tests are more relevant indicators than the presence or absence of binding antibodies.

Original language	English
Article number	1972
Journal	Viruses
Volume	13
Issue number	10
DOIs	https://doi.org/10.3390/v13101972
State	Published - Oct 2021

Bibliographical note

Funding Information:
Funding: This research was funded by the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB.

Funding Information:
Acknowledgments: Authors want to thank the volunteers that were willing to participate and to contribute to science. To Ilia Toledo: MT, Francheska Rivera, MT and Ivelisse Martin for their con‐ tribution and diligent efforts to provide access to the samples from some presumptive‐positive sub‐ jects exposed to SARS‐CoV‐2. Authors recognize the support provided by Elmer Rodriguez, PhD reviewing the statistics. Particular acknowledgement is deserved for all administrative and support‐ ive staff at the Medical Sciences Campus, University of Puerto Rico, Laboratorio Clinico Toledo, Laboratorio, Clinico Martin, Banco de Sangre Centro Médico and Banco de Sangre Servicios Mutuos for their availability and commitment during the curfew imposed by the quarantine period. Thanks also to the Latin clinical Trial Center staff for their dedication providing excellent care to the partic‐ ipants. The Puerto Rico Science: Technology and Research Trust supported research reported in this work under agreement number 2020‐00272 to A.M.E. and C.A.S. Also, the University of Puerto Rico contributed with the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB.

Publisher Copyright:
© 2021 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

COVID‐19 vaccine
Neutralization
Protection
SARS‐CoV‐2
Serology

ASJC Scopus subject areas

Infectious Diseases
Virology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.3390/v13101972

Cite this

Sariol, C. A., Pantoja, P., Serrano‐collazo, C., Rosa‐arocho, T., Armina‐rodríguez, A., Cruz, L., Stone, E. T., Arana, T., Climent, C., Latoni, G., Atehortua, D., Pabon‐carrero, C., Pinto, A. K., Brien, J. D., & Espino, A. M. (2021). Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination. Viruses, 13(10), Article 1972. https://doi.org/10.3390/v13101972

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title = "Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination",

abstract = "Both the SARS‐CoV‐2 pandemic and emergence of variants of concern have highlighted the need for functional antibody assays to monitor the humoral response over time. Antibodies directed against the spike (S) protein of SARS‐CoV‐2 are an important component of the neutralizing antibody response. In this work, we report that in a subset of patients—despite a decline in total S‐specific antibodies—neutralizing antibody titers remain at a similar level for an average of 98 days in longitudinal sampling of a cohort of 59 Hispanic/Latino patients exposed to SARS‐CoV‐2. Our data suggest that 100% of seroconverting patients make detectable neutralizing antibody responses which can be quantified by a surrogate viral neutralization test. Examination of sera from ten out of the 59 subjects which received mRNA‐based vaccination revealed that both IgG titers and neutralizing activity of sera were higher after vaccination compared to a cohort of 21 SARS‐CoV‐2 na{\"i}ve subjects. One dose was sufficient for the induction of a neutralizing antibody, but two doses were necessary to reach 100% surrogate virus neutralization in subjects irrespective of previous SARS‐ CoV‐2 natural infection status. Like the pattern observed after natural infection, the total anti‐S antibodies titers declined after the second vaccine dose; however, neutralizing activity remained relatively constant for more than 80 days after the first vaccine dose. Furthermore, our data indicates that—compared with mRNA vaccination—natural infection induces a more robust humoral immune response in unexposed subjects. This work is an important contribution to understanding the natural immune response to the novel coronavirus in a population severely impacted by SARS‐ CoV‐2. Furthermore, by comparing the dynamics of the immune response after the natural infection vs. the vaccination, these findings suggest that functional neutralizing antibody tests are more relevant indicators than the presence or absence of binding antibodies.",

keywords = "COVID‐19 vaccine, Neutralization, Protection, SARS‐CoV‐2, Serology",

author = "Sariol, {Carlos A.} and Petraleigh Pantoja and Crisanta Serrano‐collazo and Tiffany Rosa‐arocho and Albersy Armina‐rodr{\'i}guez and Lorna Cruz and Stone, {E. Taylor} and Teresa Arana and Consuelo Climent and Gerardo Latoni and Dianne Atehortua and Christina Pabon‐carrero and Pinto, {Amelia K.} and Brien, {James D.} and Espino, {Ana M.}",

note = "Funding Information: Funding: This research was funded by the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB. Funding Information: Acknowledgments: Authors want to thank the volunteers that were willing to participate and to contribute to science. To Ilia Toledo: MT, Francheska Rivera, MT and Ivelisse Martin for their con‐ tribution and diligent efforts to provide access to the samples from some presumptive‐positive sub‐ jects exposed to SARS‐CoV‐2. Authors recognize the support provided by Elmer Rodriguez, PhD reviewing the statistics. Particular acknowledgement is deserved for all administrative and support‐ ive staff at the Medical Sciences Campus, University of Puerto Rico, Laboratorio Clinico Toledo, Laboratorio, Clinico Martin, Banco de Sangre Centro M{\'e}dico and Banco de Sangre Servicios Mutuos for their availability and commitment during the curfew imposed by the quarantine period. Thanks also to the Latin clinical Trial Center staff for their dedication providing excellent care to the partic‐ ipants. The Puerto Rico Science: Technology and Research Trust supported research reported in this work under agreement number 2020‐00272 to A.M.E. and C.A.S. Also, the University of Puerto Rico contributed with the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB. Publisher Copyright: {\textcopyright} 2021 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2021",

month = oct,

doi = "10.3390/v13101972",

language = "English",

volume = "13",

number = "10",

}

Sariol, CA, Pantoja, P, Serrano‐collazo, C, Rosa‐arocho, T, Armina‐rodríguez, A, Cruz, L, Stone, ET, Arana, T, Climent, C, Latoni, G, Atehortua, D, Pabon‐carrero, C, Pinto, AK , Brien, JD & Espino, AM 2021, 'Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination', Viruses, vol. 13, no. 10, 1972. https://doi.org/10.3390/v13101972

Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination. / Sariol, Carlos A.; Pantoja, Petraleigh; Serrano‐collazo, Crisanta et al.
In: Viruses, Vol. 13, No. 10, 1972, 10.2021.

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

TY - JOUR

T1 - Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination

AU - Sariol, Carlos A.

AU - Pantoja, Petraleigh

AU - Serrano‐collazo, Crisanta

AU - Rosa‐arocho, Tiffany

AU - Armina‐rodríguez, Albersy

AU - Cruz, Lorna

AU - Stone, E. Taylor

AU - Arana, Teresa

AU - Climent, Consuelo

AU - Latoni, Gerardo

AU - Atehortua, Dianne

AU - Pabon‐carrero, Christina

AU - Pinto, Amelia K.

AU - Brien, James D.

AU - Espino, Ana M.

N1 - Funding Information: Funding: This research was funded by the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB. Funding Information: Acknowledgments: Authors want to thank the volunteers that were willing to participate and to contribute to science. To Ilia Toledo: MT, Francheska Rivera, MT and Ivelisse Martin for their con‐ tribution and diligent efforts to provide access to the samples from some presumptive‐positive sub‐ jects exposed to SARS‐CoV‐2. Authors recognize the support provided by Elmer Rodriguez, PhD reviewing the statistics. Particular acknowledgement is deserved for all administrative and support‐ ive staff at the Medical Sciences Campus, University of Puerto Rico, Laboratorio Clinico Toledo, Laboratorio, Clinico Martin, Banco de Sangre Centro Médico and Banco de Sangre Servicios Mutuos for their availability and commitment during the curfew imposed by the quarantine period. Thanks also to the Latin clinical Trial Center staff for their dedication providing excellent care to the partic‐ ipants. The Puerto Rico Science: Technology and Research Trust supported research reported in this work under agreement number 2020‐00272 to A.M.E. and C.A.S. Also, the University of Puerto Rico contributed with the UPR‐COVID‐19 Grant to C.A.S. and A.M.E. This work was also supported by 1 U01 CA260541‐01 to C.A.S. (NCI/NIAID). This work was also partially funded by Saint Louis University COVID‐19 research Seed Funding to awarded to AKP and awarded to JDB. Publisher Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2021/10

Y1 - 2021/10

N2 - Both the SARS‐CoV‐2 pandemic and emergence of variants of concern have highlighted the need for functional antibody assays to monitor the humoral response over time. Antibodies directed against the spike (S) protein of SARS‐CoV‐2 are an important component of the neutralizing antibody response. In this work, we report that in a subset of patients—despite a decline in total S‐specific antibodies—neutralizing antibody titers remain at a similar level for an average of 98 days in longitudinal sampling of a cohort of 59 Hispanic/Latino patients exposed to SARS‐CoV‐2. Our data suggest that 100% of seroconverting patients make detectable neutralizing antibody responses which can be quantified by a surrogate viral neutralization test. Examination of sera from ten out of the 59 subjects which received mRNA‐based vaccination revealed that both IgG titers and neutralizing activity of sera were higher after vaccination compared to a cohort of 21 SARS‐CoV‐2 naïve subjects. One dose was sufficient for the induction of a neutralizing antibody, but two doses were necessary to reach 100% surrogate virus neutralization in subjects irrespective of previous SARS‐ CoV‐2 natural infection status. Like the pattern observed after natural infection, the total anti‐S antibodies titers declined after the second vaccine dose; however, neutralizing activity remained relatively constant for more than 80 days after the first vaccine dose. Furthermore, our data indicates that—compared with mRNA vaccination—natural infection induces a more robust humoral immune response in unexposed subjects. This work is an important contribution to understanding the natural immune response to the novel coronavirus in a population severely impacted by SARS‐ CoV‐2. Furthermore, by comparing the dynamics of the immune response after the natural infection vs. the vaccination, these findings suggest that functional neutralizing antibody tests are more relevant indicators than the presence or absence of binding antibodies.

AB - Both the SARS‐CoV‐2 pandemic and emergence of variants of concern have highlighted the need for functional antibody assays to monitor the humoral response over time. Antibodies directed against the spike (S) protein of SARS‐CoV‐2 are an important component of the neutralizing antibody response. In this work, we report that in a subset of patients—despite a decline in total S‐specific antibodies—neutralizing antibody titers remain at a similar level for an average of 98 days in longitudinal sampling of a cohort of 59 Hispanic/Latino patients exposed to SARS‐CoV‐2. Our data suggest that 100% of seroconverting patients make detectable neutralizing antibody responses which can be quantified by a surrogate viral neutralization test. Examination of sera from ten out of the 59 subjects which received mRNA‐based vaccination revealed that both IgG titers and neutralizing activity of sera were higher after vaccination compared to a cohort of 21 SARS‐CoV‐2 naïve subjects. One dose was sufficient for the induction of a neutralizing antibody, but two doses were necessary to reach 100% surrogate virus neutralization in subjects irrespective of previous SARS‐ CoV‐2 natural infection status. Like the pattern observed after natural infection, the total anti‐S antibodies titers declined after the second vaccine dose; however, neutralizing activity remained relatively constant for more than 80 days after the first vaccine dose. Furthermore, our data indicates that—compared with mRNA vaccination—natural infection induces a more robust humoral immune response in unexposed subjects. This work is an important contribution to understanding the natural immune response to the novel coronavirus in a population severely impacted by SARS‐ CoV‐2. Furthermore, by comparing the dynamics of the immune response after the natural infection vs. the vaccination, these findings suggest that functional neutralizing antibody tests are more relevant indicators than the presence or absence of binding antibodies.

KW - COVID‐19 vaccine

KW - Neutralization

KW - Protection

KW - SARS‐CoV‐2

KW - Serology

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AN - SCOPUS:85116478634

SN - 1999-4915

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JO - Viruses

JF - Viruses

IS - 10

M1 - 1972

ER -

Function is more reliable than quantity to follow up the humoral response to the receptor‐binding domain of sars‐cov‐2‐spike protein after natural infection or covid‐19 vaccination

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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Cite this