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Cross-reactive serum and memory B cell responses to spike protein in SARS-CoV-2 and endemic coronavirus infection
Open accessPreprint — published as 10.1038/s41467-021-23074-3
Abstract
Pre-existing immune responses to seasonal endemic coronaviruses could have profound consequences for antibody responses to SARS-CoV-2, either induced in natural infection or through vaccination. Such consequences are well established in the influenza and flavivirus fields. A first step to establish whether pre-existing responses can impact SARS-CoV-2 infection is to understand the nature and extent of cross-reactivity in humans to coronaviruses. We compared serum antibody and memory B cell responses to coronavirus spike (S) proteins from pre-pandemic and SARS-CoV-2 convalescent donors using a series of binding and functional assays. We found weak evidence of pre-existing SARS-CoV-2 cross-reactive serum antibodies in pre-pandemic donors. However, we found stronger evidence of pre-existing cross-reactive memory B cells that were activated on SARS-CoV-2 infection. Monoclonal antibodies (mAbs) isolated from the donors showed varying degrees of cross-reactivity with betacoronaviruses, including SARS and endemic coronaviruses. None of the cross-reactive mAbs were neutralizing except for one that targeted the S2 subunit of the S protein. The results suggest that pre-existing immunity to endemic coronaviruses should be considered in evaluating antibody responses to SARS-CoV-2.
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“Neutralizing mAbs that bind regions of the viral spike have also been identified (24, 33, 38–42).”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [41]
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“Nonetheless, cross-reactive HCoV antibodies targeting conserved regionswere reported to be boosted in some hospitalized patients (Anderson et al., 2021; Guo et al., 2021; Song et al., 2021) and have been associatedwith the development of neutralizing antibodies (Dispinseri et al., 2021).”
Amanat, F., Thapa, M., Lei, T., Ahmed, S. M. S., Adelsberg, D. C., Carreño, J. M., Strohmeier, S., Schmitz, A. J., Zafar, S., Zhou, J. Q., et al. (2021) · medRxiv · doi:10.1101/2021.03.07.21253098 · Cited by 41
“This phenomenon resembles the immune imprinting described in influenza virus immunology and has already been described for natural infection with SARS-CoV-2 (Aydillo et al., 2020; Song et al., 2020).”
COVID-19 Neutralizing Antibodies Predict Disease Severity and Survival
García-Beltrán, W. F., Lam, E. C., Astudillo, M. G., Yang, D., Miller, T. E., Feldman, J. E., Hauser, B. M., Caradonna, T. M., Clayton, K., Nitido, A. D., et al. (2020) · Cell · doi:10.1016/j.cell.2020.12.015 · Cited by 708
“The diverse and atypical kinetics of antibody production—in particular, early rise of IgG and in some cases IgA—suggests the possibility of a contribution from class-switched (IgG or IgA) memory B cells early in the humoral immune response rather than solely from the naive (IgM) B cell pool, as has been recently postu…”
COVID ‐19 and plasma cells: Is there long‐lived protection?*
Nguyen, D. C., Lamothe, P. A., Woodruff, M. C., Saini, A. S., Faliti, C. E., Sanz, I., & Lee, F. E.-H. (2022) · Immunological Reviews · doi:10.1111/imr.13115 · Cited by 48
Abela, I. A., Pasin, C., Schwarzmüller, M., Epp, S., Sickmann, M., Schanz, M., Rusert, P., Weber, J., Schmutz, S., Audigé, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27040-x · Cited by 45
Cagigi, A., Yu, M., Österberg, B., Svensson, J., Falck‐Jones, S., Vangeti, S., Åhlberg, E., Azizmohammadi, L., Warnqvist, A., Falck‐Jones, R., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.151463 · Cited by 48
“have shown that cross-reactivity between coronaviruses exists (53, 54).”
Adli, A., Rahimi, M., Khodaie, R., Hashemzaei, N., & Hosseini, S. M. (2022) · Journal of Medical Virology · doi:10.1002/jmv.27615 · Cited by 46
“The immunological deregulation, in particular, is mediated by IL‐6 rather than interleukin‐ 1 (IL‐1) beta.176 Increased generation of pro‐inflammatory cytokines through lymphocyte and monocytes dysfunction with CD4 lymphopenia are two critical characteristics of this immune dysregulation.176 Increased expression of th…”
BackgroundInfluentialLu, L., Chu, A. W., Zhang, R., Chan, W.-M., Ip, J. D., Tsoi, H., Chen, L., Cai, J., Lung, D. C., Tam, A. R., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103544 · Cited by 39
“Indeed, neutralizing antibodies targeting the S2 region have been found [36].”
Borrega, R., Nelson, D. K. S., Koval, A. P., Bond, N. G., Heinrich, M. L., Rowland, M. M., Lathigra, R. B., Bush, D. J., Aimukanova, I., Phinney, W. N., et al. (2021) · Viruses · doi:10.3390/v13112325 · Cited by 37
“Pre-existing memory B cells that are cross-reactive with other coronaviruses are activated on SARS-CoV-2 infection [45].”
BackgroundShroff, R., Chalasani, P., Wei, R., et al. (2021) · medRxiv · doi:10.1101/2021.05.13.21257129 · Cited by 33
Huang, Y., Nguyen, A. W., Hsieh, C., et al. (2021) · bioRxiv · doi:10.1101/2021.01.31.428824 · Cited by 33
Meyer‐Arndt, L., Braun, J., Fauchère, F., Vanshylla, K., Loyal, L., Henze, L., Kruse, B., Dingeldey, M., Jürchott, K., Mangold, M., et al. (2022) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2022-329395 · Cited by 33
The immune response to COVID ‐19: Does sex matter?
Ho, J. Q., Sepand, M. R., Bigdelou, B., Shekarian, T., Esfandyarpour, R., Chauhan, P. S., Serpooshan, V., Beura, L. K., Hütter, G., & Zanganeh, S. (2022) · Immunology · doi:10.1111/imm.13487 · Cited by 45
“detected in SARS-CoV-2 unexposed individuals, the disease outcome is largely thought to be shaped by initial innate immune responses.(51,52) Pattern recognition receptors (PRRs) such as toll-like receptor 7 (TLR7) that sense single-stranded RNA may play a major role in the initial innate immune response against RNA vi…”
BackgroundGeanes, E. S., LeMaster, C., Fraley, E., Khanal, S., McLennan, R., Grundberg, E., Selvarangan, R., & Bradley, T. (2022) · Scientific Reports · doi:10.1038/s41598-022-10230-y · Cited by 33
Wu, W.-L., Chiang, C.-Y., Lai, S.-C., Yu, C.-Y., Huang, Y., Liao, H., Liao, C., Chen, H., & Liu, S. (2022) · JCI Insight · doi:10.1172/jci.insight.157597 · Cited by 41
Laing, E. D., Epsi, N. J., Richard, S. A., Samuels, E. C., Wang, W., Vassell, R. A., Ewing, D. F., Herrup, R., Sterling, S. L., Lindholm, D. A., et al. (2021) · medRxiv · doi:10.1101/2021.04.27.21256207 · Cited by 20
Olukitibi, T. A., Ao, Z., Warner, B. M., Unat, R., Kobasa, D., & Yao, X. (2023) · Vaccines · doi:10.3390/vaccines11030545 · Cited by 38
mRNA COVID-19 Vaccines and Long-Lived Plasma Cells: A Complicated Relationship
Giannotta, G., & Giannotta, N. (2021) · Vaccines · doi:10.3390/vaccines9121503 · Cited by 33
“However, there is strong evidence of pre-existing cross-reactive MBCs that were activated on SARS-CoV-2 infection [65].”
BackgroundRapid Development of Analytical Methods for Evaluating Pandemic Vaccines: A Covid-19 Perspective
Baldwin, J., Piplani, S., Sakala, I. G., Honda‐Okubo, Y., Li, L., & Petrovsky, N. (2021) · Bioanalysis · doi:10.4155/bio-2021-0096 · Cited by 33
“Variations of SARS-CoV-2 Spike protein based CELISA assays reported in literature make use of alternative transfected cell lines (namely HEK293 cells) and analyze samples via flow cytometry, representing antibody binding [72].”
BackgroundMalherbe, D. C., Kurup, D., Wirblich, C., Ronk, A. J., Mire, C. E., Kuzmina, N. A., Shaik, N. F., Periasamy, S., Hyde, M. A., Williams, J. M., et al. (2021) · npj Vaccines · doi:10.1038/s41541-021-00352-1 · Cited by 31
Poston, D., Weisblum, Y., Wise, H., et al. (2020) · medRxiv · doi:10.1101/2020.10.08.20209650 · Cited by 30
Korenkov, M., Zehner, M., Cohen‐Dvashi, H., Borenstein-Katz, A., Kottege, L., Janicki, H., Vanshylla, K., Weber, T., Gruell, H., Koch, M., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.11.004 · Cited by 36
Broadly neutralizing antibodies to SARS-related viruses can be readily induced in rhesus macaques
He, W., Yuan, M., Callaghan, S., Musharrafieh, R. G., Song, G., Silva, M., Beutler, N., Lee, W.-H., Yong, P., Torres, J. L., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abl9605 · Cited by 31
Self-citationHumoral Immunity against SARS-CoV-2 and the Impact on COVID-19 Pathogenesis
Lee, E.-J., & Oh, J. E. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0075 · Cited by 30
“In contrast, other studies have reported limited pre-existing cross-reactive antibodies against SARS-CoV-2 in unexposed individuals (Nguyen-Contant et al., 2020; Poston et al., 2020; Song et al., 2020).”
BackgroundResultFocosi, D., Genoni, A., Lucenteforte, E., et al. (2021) · Life · doi:10.3390/life11040298 · Cited by 28
“There is weak evidence of pre-existing SARS CoV-2 cross-reactive serum antibodies and limited crossreactive memory B cells in pre-pandemic donors [14], and cross-reactivity to NL63 and 229E was more common in sub-Saharan Africa than in the USA [15].”
BackgroundScharf, L., Axelsson, H., Emmanouilidi, A., Mathew, N. R., Sheward, D. J., Leach, S., Isakson, P., Smirnov, I. V., Marklund, E., Miron, N., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.165299 · Cited by 28
Li, T., Kan, Q., Ge, J., Wan, Z., Yuan, M., Huang, Y., Xie, Q., Yang, Y., Shao, H., Li, X., et al. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00778-6 · Cited by 27
Sealy, R. E., & Hurwitz, J. L. (2021) · Microorganisms · doi:10.3390/microorganisms9081643 · Cited by 30
Seasonal respiratory virus circulation was diminished during the COVID‐19 pandemic
Heiskanen, A., Galipeau, Y., Little, J., Mortimer, L., Ramotar, K., Langlois, M., & Cooper, C. (2022) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.13065 · Cited by 30
Ng, K. T., Mohd-Ismail, N. K., & Tan, Y. (2021) · Vaccines · doi:10.3390/vaccines9020178 · Cited by 28
“Thus far, there are two anti-S2 neutralizing monoclonal antibodies that have been isolated from COVID-19 patients and reported in preprints, of which one demonstrated the ability of an S2 monoclonal antibody in neutralizing the emerging variant [42,43].”
BackgroundRecent Infection With HCoV-OC43 Is Associated With Protection Against Sars-Cov-2 Infection
Lavell, A. H. A., Sikkens, J. J., Edridge, A. W. D., van der Straten, K., Sechan, F., Oomen, M., Buis, D. T. P., Schinkel, M., Burger, J. A., Poniman, M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105105 · Cited by 25
“…elicited by previous infections with seasonal human coronaviruses (HCoVs) is therefore of great interest, but studies have yielded conflicting results (Anderson et al., 2021; Dugas et al., 2021; Ladner et al., 2021; Lin et al., 2022a; Ortega et al., 2021; Sagar et al., 2021; Song et al., 2021).”
InfluentialPedersen, J., Koumakpayi, I. H., Babuadze, G. G., Baz, M., Ndiaye, O., Faye, O., Diagne, C. T., Dia, N., Naghibosadat, M., McGeer, A., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-17241-9 · Cited by 31
Lawrenz, J., Xie, Q., Zech, F., Weil, T., Seidel, A., Krnavek, D., van der Hoek, L., Münch, J., Müller, J. A., & Kirchhoff, F. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac057 · Cited by 25
“Thus, our results add to the evidence that increased neutralizing activity against seasonal coronaviruses observed after SARS-CoV-2 vaccination may be due to reactivation of memory hCoV B cells rather than cross-neutralizing activity of SARS-CoV-2 antibodies [23,40,41].”
ResultAdaptive immunity to human coronaviruses is widespread but low in magnitude
Tan, H., Lee, W. S., Wragg, K. M., Nelson, C., Esterbauer, R., Kelly, H. G., Amarasena, T. H., Jones, R. M., Starkey, G., Wang, B. Z., et al. (2021) · Clinical & Translational Immunology · doi:10.1002/cti2.1264 · Cited by 18
Grant, M. D., Bentley, K., Fielding, C. A., Hatfield, K. M., Ings, D. P., Harnum, D. O. A., Wang, E. C. Y., Stanton, R. J., & Holder, K. A. (2023) · JCI Insight · doi:10.1172/jci.insight.170681 · Cited by 29
Innate and adaptive immunity to SARS-CoV-2 and predisposing factors
Shen, J., Fan, J., Zhao, Y., Jiang, D., Niu, Z., Zhang, Z., & Cao, G. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1159326 · Cited by 38
SARS-CoV-2 infection and immune responses
Harne, R., Williams, B., Abdelaal, H. F. M., Baldwin, S. L., & Coler, R. N. (2023) · AIMS Microbiology · doi:10.3934/microbiol.2023015 · Cited by 21
“Antibodies developed from previous infections to coronaviruses conferring pre-existing immunity may cross-react and contribute to SARS-CoV-2-specific neutralizing antibodies including rapid EF IgG immune responses in primary SARS-CoV-2 infection [113,114].”
BackgroundAntibody-mediated immunity to SARS-CoV-2 spike
Errico, J. M., Adams, L. J., & Fremont, D. H. (2022) · Advances in immunology · doi:10.1016/bs.ai.2022.07.001 · Cited by 22
“8 were both able to neutralize SARS-CoV and SARS-CoV-2 and bind to hCoV-OC43 and hCoV-HKU1 spike, but displayed no cross-reactivity to MERS (Song et al., 2021).”
InfluentialHeterologous humoral immunity to human and zoonotic coronaviruses: Aiming for the achilles heel
Ng, K. W., Faulkner, N., Wrobel, A. G., Gamblin, S. J., & Kassiotis, G. (2021) · Seminars in Immunology · doi:10.1016/j.smim.2021.101507 · Cited by 19
Rabaan, A. A., Al-Ahmed, S. H., Albayat, H., Alwarthan, S. M., Alhajri, M. M., Najim, M. A., Alshehail, B. M., Al-Adsani, W., Alghadeer, A., Abduljabbar, W. A., et al. (2023) · Medicina · doi:10.3390/medicina59030507 · Cited by 25
SARS-CoV-2 spike conformation determines plasma neutralizing activityPreprint
Bowen, J. E., Walls, A. C., Joshi, A., Sprouse, K. R., Stewart, C., Tortorici, M. A., Franko, N., Logue, J. K., Mazzitelli, I. G., Tilles, S. W., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.19.473391 · Cited by 21
“Targeting of the prefusion S 2 subunit conformation, as opposed to the postfusion state, makes only a small contribution to overall neutralizing activity due to the low frequency and potency of fusion machinery-specific neutralizing antibodies ( 24 , 28 , 70 ).”
Decay of Fc-dependent antibody functions after mild to moderate COVID-19
Lee, W. S., Selva, K. J., Davis, S. K., Wines, B. D., Reynaldi, A., Esterbauer, R., Kelly, H. G., Haycroft, E. R., Tan, H.-X., Juno, J. A., et al. (2020) · doi:10.1101/2020.12.13.20248143 · Cited by 80
Singh, G., Abbad, A., Kleiner, G., Srivastava, K., Gleason, C., PARIS Study Group, Carreño, J. M., Simon, V. R., Krammer, F., Andre, D., et al. (2023) · mBio · doi:10.1128/mbio.02250-23 · Cited by 17
“Such antibodies have been 129 isolated with some of them having neutralizing activity although at low potency [9, 11-13].”
BackgroundAmanat, F., Clark, J. J., Carreño, J. M., Strohmeier, S., Yellin, T., Meade, P. S., Bhavsar, D., Muramatsu, H., Sun, W., Coughlan, L., et al. (2023) · Journal of Virology · doi:10.1128/jvi.01664-22 · Cited by 21
“more conserved S2 subunit, have been shown to cross-react to seasonal β-CoV spike proteins as well 126 (19-24).”
BackgroundElko, E. A., Nelson, G. A., Mead, H., Kelley, E., Carvalho, S. T., Sarbo, N., Harms, C. E., Verche, V. L., Cardoso, A. A., Ely, J. L., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111022 · Cited by 21
Tanunliong, G., Liu, A. C., Kaweski, S. E., Irvine, M. A., Reyes, R. C., Purych, D., Krajden, M., Morshed, M. G., Sekirov, I., Gantt, S. M., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.836449 · Cited by 17
Vo, H. T. M., Maestri, A., Auerswald, H., Sorn, S., Lay, S., Seng, H., Sann, S., Ya, N., Pean, P., Dussart, P., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.817905 · Cited by 18
“Consequently, anti-N IgG rather than anti-S1 IgG can be found in individuals not exposed to SARS-CoV-2 (68, 71, 72).”
BackgroundVanderheijden, N., Stevaert, A., Xie, J., Ren, X., Barbezange, C., Noppen, S., Desombere, I., Verhasselt, B., Geldhof, P., Vereecke, N., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.790415 · Cited by 12
“This might involve a recall of pre-existing anti-HCoVOC43 memory B cells (47).”
BackgroundThe S2 subunit of spike encodes diverse targets for functional antibody responses to SARS-CoV-2
Guenthoer, J., Garrett, M. E., Lilly, M., Depierreux, D., Ruiz, F., Chi, M., Stoddard, C. I., Chohan, V., Yaffe, Z. A., Sung, K., et al. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012383 · Cited by 25
“To date, most S2-specific neutralizing mAbs that have been identified target the FP (816–833) or SH regions (1141–1160) [28,42,43,45,51,98].”
Boland, B. S., Goodwin, B., Zhang, Z., Bloom, N. I., Kato, Y., Neill, J., Le, H., Tysl, T., Collins, A. E., Dulai, P. S., et al. (2022) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000484 · Cited by 14
“Furthermore, it is unclear why IFX monotherapy patients had comparable spike IgG titers, but this may be due to pre-existing endemic coronavirus spike-specific memory B cells because there was no difference in the frequency of spike-specific memory B cells (14).”
Background
Metadata
- Authors
- Song, G., He, W.-T., Callaghan, S., Anzanello, F., Huang, D., Ricketts, J., Torres, J. L., Beutler, N., Peng, L., Vargas, S., Cassell, J., Parren, M., Yang, L., Ignacio, C., Smith, D. M., Voss, J. E., Nemazee, D., Ward, A. B., Rogers, T., Burton, D. R., & Andrabi, R.
- Affiliations
- Scripps Research Institute (US)
- University of California San Diego (US)
- Corresponding author
- Burton, Dennis R.
- Andrabi, Raiees
- ORCID
- Venue
- Nature Communications
- Publisher
- openRxiv
- Published
- 2020-09-23
- Volume
- 12
- Issue
- 1
- Pages
- 2938-2938
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC7523096
- OpenAlex
- W3161511556
- Cited by
- 285
- References
- 40
- Citations by year
- 2026: 15 · 2025: 17 · 2024: 30 · 2023: 53 · 2022: 78 · 2021: 85 · 2020: 7
- FWCI
- 19.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Bill and Melinda Gates Foundation (OPP1170236, UM1 AI44462)
- International AIDS Vaccine Initiative
- National Institutes of Health (UM1 AI44462, COVID-19)
- National Institute of Allergy and Infectious Diseases (R01AI132317, R01AI073148, R56AI073148)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
- Keywords
- SARS-CoV-2, cross-reactive antibodies, memory B cells, spike protein, endemic coronaviruses, pre-existing immunity, SARS-CoV-1, betacoronaviruses, neutralizing antibodies, S2 subunit, monoclonal antibodies, antibody cross-reactivity, convalescent donors
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