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Article

B Cells Isolated from Individuals Who Do Not Respond to the HBV Vaccine Are Characterized by Higher DNA Methylation-Estimated Aging Compared to Responders

by
Katarzyna Malgorzata Kwiatkowska
1,*,†,
Simona Anticoli
2,†,
Stefano Salvioli
1,3,
Luciano Calzari
4,
Davide Gentilini
4,5,
Christian Albano
6,
Reparata Rosa Di Prinzio
7,
Salvatore Zaffina
7,
Rita Carsetti
6,
Anna Ruggieri
2,‡ and
Paolo Garagnani
1,3,*,‡
1
Department of Medical and Surgical Sciences (DIMEC), University of Bologna, 40126 Bologna, Italy
2
Istituto Superiore di Sanità, Center for Gender Specific Medicine, 00161 Rome, Italy
3
IRCCS Azienda Ospedaliero, Universitaria di Bologna, 40138 Bologna, Italy
4
Bioinformatics and Statistical Genomics Unit, Istituto Auxologico Italiano IRCCS, 20095 Cusano Milanino, Italy
5
Department of Brain and Behavioral Sciences, Università di Pavia, 27100 Pavia, Italy
6
Immunology Research Area, B Cell Unit, Ospedale Pediatrico Bambino Gesù IRCCS, 00146 Rome, Italy
7
Occupational Medicine/Health Technology Assessment and Safety Research Unit, Clinical-Technological Innovations Research Area, Ospedale Pediatrico Bambino Gesù IRCCS, 00146 Rome, Italy
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
These authors also contributed equally to this work.
Vaccines 2024, 12(8), 880; https://doi.org/10.3390/vaccines12080880
Submission received: 21 June 2024 / Revised: 25 July 2024 / Accepted: 27 July 2024 / Published: 2 August 2024

Abstract

Healthcare workers (HCWs) are a high-risk group for hepatitis B virus (HBV) infection. Notably, about 5–10% of the general population does not respond to the HBV vaccination. In this study, we aimed to investigate DNA methylation (DNAm) in order to estimate the biological age of B cells from HCW of both sexes, either responder (R) or non-responder (NR), to HBV vaccination. We used genome-wide DNA methylation data to calculate a set of biomarkers in B cells collected from 41 Rs and 30 NRs between 22 and 62 years old. Unresponsiveness to HBV vaccination was associated with accelerated epigenetic aging (DNAmAge, AltumAge, DunedinPoAm) and was accompanied by epigenetic drift. Female non-responders had higher estimates of telomere length and lower CRP inflammation risk score when compared to responders. Overall, epigenetic differences between responders and non-responders were more evident in females than males. In this study we demonstrated that several methylation DNAm-based clocks and biomarkers are associated with an increased risk of non-response to HBV vaccination, particularly in females. Based on these results, we propose that accelerated epigenetic age could contribute to vaccine unresponsiveness. These insights may help improve the evaluation of the effectiveness of vaccination strategies, especially among HCWs and vulnerable patients.
Keywords: hepatitis B; vaccine; health care workers; sex; immune response; B lymphocytes; DNA methylation clock; epigenetic clock; epigenetic age; aging hepatitis B; vaccine; health care workers; sex; immune response; B lymphocytes; DNA methylation clock; epigenetic clock; epigenetic age; aging

Share and Cite

MDPI and ACS Style

Kwiatkowska, K.M.; Anticoli, S.; Salvioli, S.; Calzari, L.; Gentilini, D.; Albano, C.; Di Prinzio, R.R.; Zaffina, S.; Carsetti, R.; Ruggieri, A.; et al. B Cells Isolated from Individuals Who Do Not Respond to the HBV Vaccine Are Characterized by Higher DNA Methylation-Estimated Aging Compared to Responders. Vaccines 2024, 12, 880. https://doi.org/10.3390/vaccines12080880

AMA Style

Kwiatkowska KM, Anticoli S, Salvioli S, Calzari L, Gentilini D, Albano C, Di Prinzio RR, Zaffina S, Carsetti R, Ruggieri A, et al. B Cells Isolated from Individuals Who Do Not Respond to the HBV Vaccine Are Characterized by Higher DNA Methylation-Estimated Aging Compared to Responders. Vaccines. 2024; 12(8):880. https://doi.org/10.3390/vaccines12080880

Chicago/Turabian Style

Kwiatkowska, Katarzyna Malgorzata, Simona Anticoli, Stefano Salvioli, Luciano Calzari, Davide Gentilini, Christian Albano, Reparata Rosa Di Prinzio, Salvatore Zaffina, Rita Carsetti, Anna Ruggieri, and et al. 2024. "B Cells Isolated from Individuals Who Do Not Respond to the HBV Vaccine Are Characterized by Higher DNA Methylation-Estimated Aging Compared to Responders" Vaccines 12, no. 8: 880. https://doi.org/10.3390/vaccines12080880

APA Style

Kwiatkowska, K. M., Anticoli, S., Salvioli, S., Calzari, L., Gentilini, D., Albano, C., Di Prinzio, R. R., Zaffina, S., Carsetti, R., Ruggieri, A., & Garagnani, P. (2024). B Cells Isolated from Individuals Who Do Not Respond to the HBV Vaccine Are Characterized by Higher DNA Methylation-Estimated Aging Compared to Responders. Vaccines, 12(8), 880. https://doi.org/10.3390/vaccines12080880

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