Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine

Ivan Odak; Lennart Riemann; Inga Sandrock; Anne Cossmann; Gema Morillas Ramos; Swantje I Hammerschmidt; Christiane Ritter; Michaela Friedrichsen; Ahmed Hassan; Alexandra Dopfer-Jablonka; Metodi V Stankov; Leonie M Weskamm; Marylyn M Addo; Inga Ravens; Stefanie Willenzon; Anja Schimrock; Jasmin Ristenpart; Anika Janssen; Joana Barros-Martins; Gesine Hansen; Christine Falk; Georg M N Behrens; Reinhold Förster

doi:10.1016/j.ebiom.2023.104947

Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine

Standard

Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine. / Odak, Ivan; Riemann, Lennart; Sandrock, Inga; Cossmann, Anne; Ramos, Gema Morillas; Hammerschmidt, Swantje I; Ritter, Christiane; Friedrichsen, Michaela; Hassan, Ahmed; Dopfer-Jablonka, Alexandra; Stankov, Metodi V; Weskamm, Leonie M ; Addo, Marylyn M; Ravens, Inga; Willenzon, Stefanie; Schimrock, Anja; Ristenpart, Jasmin; Janssen, Anika; Barros-Martins, Joana; Hansen, Gesine; Falk, Christine; Behrens, Georg M N; Förster, Reinhold.

In: EBIOMEDICINE, Vol. 99, 104947, 01.2024.

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

Harvard

Odak, I, Riemann, L, Sandrock, I, Cossmann, A, Ramos, GM, Hammerschmidt, SI, Ritter, C, Friedrichsen, M, Hassan, A, Dopfer-Jablonka, A, Stankov, MV, Weskamm, LM , Addo, MM, Ravens, I, Willenzon, S, Schimrock, A, Ristenpart, J, Janssen, A, Barros-Martins, J, Hansen, G, Falk, C, Behrens, GMN & Förster, R 2024, 'Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine', EBIOMEDICINE, vol. 99, 104947. https://doi.org/10.1016/j.ebiom.2023.104947

APA

Odak, I., Riemann, L., Sandrock, I., Cossmann, A., Ramos, G. M., Hammerschmidt, S. I., Ritter, C., Friedrichsen, M., Hassan, A., Dopfer-Jablonka, A., Stankov, M. V., Weskamm, L. M., Addo, M. M., Ravens, I., Willenzon, S., Schimrock, A., Ristenpart, J., Janssen, A., Barros-Martins, J., ... Förster, R. (2024). Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine. EBIOMEDICINE, 99, [104947]. https://doi.org/10.1016/j.ebiom.2023.104947

Vancouver

Odak I, Riemann L, Sandrock I, Cossmann A, Ramos GM, Hammerschmidt SI et al. Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine. EBIOMEDICINE. 2024 Jan;99. 104947. https://doi.org/10.1016/j.ebiom.2023.104947

Bibtex

@article{4fb91010b846470fbe5dcfde7245d6f6,

title = "Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine",

abstract = "BACKGROUND: Human immune responses to COVID-19 vaccines display a large heterogeneity of induced immunity and the underlying immune mechanisms for this remain largely unknown.METHODS: Using a systems biology approach, we longitudinally profiled a unique cohort of female high and low responders to the BNT162b vaccine, who were known from previous COVID-19 vaccinations to develop maximum and minimum immune responses to the vaccine. We utilized high dimensional flow cytometry, bulk and single cell mRNA sequencing and 48-plex serum cytokine analyses.FINDINGS: We revealed early, transient immunological and molecular signatures that distinguished high from low responders and correlated with B and T cell responses measured 14 days later. High responders featured a distinct transcriptional activity of interferon-driven genes and genes connected to enhanced antigen presentation. This was accompanied by a robust cytokine response related to Th1 differentiation. Both transcriptome and serum cytokine signatures were confirmed in two independent confirmatory cohorts.INTERPRETATION: Collectively, our data contribute to a better understanding of the immunogenicity of mRNA-based COVID-19 vaccines, which might lead to the optimization of vaccine designs for individuals with poor vaccine responses.FUNDING: German Center for Infection Research, German Center for Lung Research, German Research Foundation, Excellence Strategy EXC 2155 {"}RESIST{"} and European Regional Development Fund.",

author = "Ivan Odak and Lennart Riemann and Inga Sandrock and Anne Cossmann and Ramos, {Gema Morillas} and Hammerschmidt, {Swantje I} and Christiane Ritter and Michaela Friedrichsen and Ahmed Hassan and Alexandra Dopfer-Jablonka and Stankov, {Metodi V} and Weskamm, {Leonie M} and Addo, {Marylyn M} and Inga Ravens and Stefanie Willenzon and Anja Schimrock and Jasmin Ristenpart and Anika Janssen and Joana Barros-Martins and Gesine Hansen and Christine Falk and Behrens, {Georg M N} and Reinhold F{\"o}rster",

year = "2024",

month = jan,

doi = "10.1016/j.ebiom.2023.104947",

language = "English",

volume = "99",

journal = "EBIOMEDICINE",

issn = "2352-3964",

publisher = "Elsevier BV",

}

RIS

TY - JOUR

T1 - Systems biology analysis reveals distinct molecular signatures associated with immune responsiveness to the BNT162b COVID-19 vaccine

AU - Odak, Ivan

AU - Riemann, Lennart

AU - Sandrock, Inga

AU - Cossmann, Anne

AU - Ramos, Gema Morillas

AU - Hammerschmidt, Swantje I

AU - Ritter, Christiane

AU - Friedrichsen, Michaela

AU - Hassan, Ahmed

AU - Dopfer-Jablonka, Alexandra

AU - Stankov, Metodi V

AU - Weskamm, Leonie M

AU - Addo, Marylyn M

AU - Ravens, Inga

AU - Willenzon, Stefanie

AU - Schimrock, Anja

AU - Ristenpart, Jasmin

AU - Janssen, Anika

AU - Barros-Martins, Joana

AU - Hansen, Gesine

AU - Falk, Christine

AU - Behrens, Georg M N

AU - Förster, Reinhold

PY - 2024/1

Y1 - 2024/1

N2 - BACKGROUND: Human immune responses to COVID-19 vaccines display a large heterogeneity of induced immunity and the underlying immune mechanisms for this remain largely unknown.METHODS: Using a systems biology approach, we longitudinally profiled a unique cohort of female high and low responders to the BNT162b vaccine, who were known from previous COVID-19 vaccinations to develop maximum and minimum immune responses to the vaccine. We utilized high dimensional flow cytometry, bulk and single cell mRNA sequencing and 48-plex serum cytokine analyses.FINDINGS: We revealed early, transient immunological and molecular signatures that distinguished high from low responders and correlated with B and T cell responses measured 14 days later. High responders featured a distinct transcriptional activity of interferon-driven genes and genes connected to enhanced antigen presentation. This was accompanied by a robust cytokine response related to Th1 differentiation. Both transcriptome and serum cytokine signatures were confirmed in two independent confirmatory cohorts.INTERPRETATION: Collectively, our data contribute to a better understanding of the immunogenicity of mRNA-based COVID-19 vaccines, which might lead to the optimization of vaccine designs for individuals with poor vaccine responses.FUNDING: German Center for Infection Research, German Center for Lung Research, German Research Foundation, Excellence Strategy EXC 2155 "RESIST" and European Regional Development Fund.

AB - BACKGROUND: Human immune responses to COVID-19 vaccines display a large heterogeneity of induced immunity and the underlying immune mechanisms for this remain largely unknown.METHODS: Using a systems biology approach, we longitudinally profiled a unique cohort of female high and low responders to the BNT162b vaccine, who were known from previous COVID-19 vaccinations to develop maximum and minimum immune responses to the vaccine. We utilized high dimensional flow cytometry, bulk and single cell mRNA sequencing and 48-plex serum cytokine analyses.FINDINGS: We revealed early, transient immunological and molecular signatures that distinguished high from low responders and correlated with B and T cell responses measured 14 days later. High responders featured a distinct transcriptional activity of interferon-driven genes and genes connected to enhanced antigen presentation. This was accompanied by a robust cytokine response related to Th1 differentiation. Both transcriptome and serum cytokine signatures were confirmed in two independent confirmatory cohorts.INTERPRETATION: Collectively, our data contribute to a better understanding of the immunogenicity of mRNA-based COVID-19 vaccines, which might lead to the optimization of vaccine designs for individuals with poor vaccine responses.FUNDING: German Center for Infection Research, German Center for Lung Research, German Research Foundation, Excellence Strategy EXC 2155 "RESIST" and European Regional Development Fund.

U2 - 10.1016/j.ebiom.2023.104947

DO - 10.1016/j.ebiom.2023.104947

M3 - SCORING: Journal article

C2 - 38160529

VL - 99

JO - EBIOMEDICINE

JF - EBIOMEDICINE

SN - 2352-3964

M1 - 104947

ER -