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The Adaptive Immunity in COVID-19

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (30 December 2022) | Viewed by 29727

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Prof. Dr. Vincenzo Barnaba

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1. Department of Internal Clinical Sciences, Anaesthesiology and Cardiovascular Sciences, Sapienza Università di Roma, 00161 Rome, Italy
2. Laboratory Affiliated to Istituto Pasteur Italia-Fondazione Cenci Bolognetti, 00161 Rome, Italy
Interests: tumor immunology; pathogenesis of immune-mediated diseases (infections and autoimmunity)
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Prof. Dr. Manlio Ferrarini

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Department of Experimental Medicine, University of Genoa, 16132 Genoa, Italy
Interests: B cells; B cell subpopulations; lymphokines; lymphomas; oncogenes; immunoglobulin genes
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Prof. Dr. Jeffrey L. Platt

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Collection Editor

1. Department of Surgery, University of Michigan, Ann Arbor, MI 48109, USA
2. Department of Microbiology & Immunology, University of Michigan, Ann Arbor, MI 48109, USA
3. The Transplantation Biology Program, University of Michigan, Ann Arbor, MI 48109, USA
Interests: the immunology and cell biology of transplantation; cancer and related fields
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

In this Collection, we will consider the latest research on the immunology of SARS-CoV-2 and the associated disease COVID-19, in order to deeply understand the difference between protective and immunopathological B and T cell responses in patients with severe, moderated, or asymptomatic COVID-19, as well as in recovered or vaccinated individuals. In this context, this Topical Collection will enclose reports discussing the kinetics of immunological memory against SARS-CoV-2, its heterogeneity, and capacity to provide, or not, durable immunity against new emerging variants.

The scope of this Topical Collection is, therefore, to provide insight into: (i) the different facets of immunopathology supporting the phenomena associated with severe COVID-19, such as lymphopenia, impaired response to interferon, and “cytokine storm”; (ii) the immunoregulatory mechanisms addressed to control excessive inflammatory responses without excessively limiting the anti-viral immune responses; (iii) the differences in adaptive immune responses between infected patients and vaccinated individuals, deciphering both immunopathology and protection signatures. This research will provide useful information to set up new therapeutic strategies and to develop new vaccines that prevent viral immune escape and the selection of new variants.

Prof. Dr. Vincenzo Barnaba
Prof. Dr. Manlio Ferrarini
Prof. Dr. Jeffrey L. Platt
Collection Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

COVID-19
immunity
immune escape
immunopathology
immunoregulatory mechanisms
immunotherapy

Related Special Issue

Innate and Adaptive Immunity in COVID-19 in International Journal of Molecular Sciences (1 article)

Published Papers (11 papers)

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Research

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12 pages, 942 KiB

Open AccessArticle

Coronavirus-Specific Antibody and T Cell Responses Developed after Sputnik V Vaccination in Patients with Chronic Lymphocytic Leukemia

by Alexey A. Komissarov, Maria Kislova, Ivan A. Molodtsov, Andrei A. Petrenko, Elena Dmitrieva, Maria Okuneva, Iuliia O. Peshkova, Naina T. Shakirova, Daria M. Potashnikova, Anna V. Tvorogova, Vadim V. Ptushkin, Grigory A. Efimov, Eugene A. Nikitin and Elena Vasilieva

Int. J. Mol. Sci. 2023, 24(1), 416; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24010416 - 27 Dec 2022

Cited by 1 | Viewed by 1840

Abstract

The clinical course of the new coronavirus disease 2019 (COVID-19) has shown that patients with chronic lymphocytic leukemia (CLL) are characterized by a high mortality rate, poor response to standard treatment, and low virus-specific antibody response after recovery and/or vaccination. To date, there are no data on the safety and efficacy of the combined vector vaccine Sputnik V in patients with CLL. Here, we analyzed and compared the magnitudes of the antibody and T cell responses after vaccination with the Sputnik V vaccine among healthy donors and individuals with CLL with different statuses of preexposure to coronavirus. We found that vaccination of the COVID-19–recovered individuals resulted in the boosting of pre-existing immune responses in both healthy donors and CLL patients. However, the COVID-19–naïve CLL patients demonstrated a considerably lower antibody response than the healthy donors, although they developed a robust T cell response. Regardless of the previous infection, the individuals over 70 years old demonstrated a decreased response to vaccination, as did those receiving anti-CD20 therapy. In summary, we showed that Sputnik V, like other vaccines, did not induce a robust antibody response in individuals with CLL; however, it provided for the development of a significant anti-COVID-19 T cell response. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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19 pages, 18738 KiB

Open AccessArticle

Comparative Analysis of Antibody Titers against the Spike Protein of SARS-CoV-2 Variants in Infected Patient Cohorts and Diverse Vaccination Regimes

by Alexandru Odainic, Jasper Spitzer, Jennifer Barbara Szlapa, Simon Schade, Tim Jonas Krämer, Jakob Neuberger, Christian Bode, Folkert Steinhagen, Ricarda Maria Schmithausen, Gero Wilbring, Esther Sib, Nico Tom Mutters, Frederik Rabenschlag, Lisa Kettel, Maike Woznitza, Kathrin van Bremen, Tina Peers, Gez Medinger, Anushka Kudaliyanage, Maike Kreutzenbeck, Ulrike Strube, Joseph M. Johnson, Dawn Mattoon, Andrew J. Ball, Stefan Scory, Richard McGuire, Christian Putensen, Zeinab Abdullah, Catharina Latz and Susanne Viktoria Schmidt Show full author list Hide full author list

Int. J. Mol. Sci. 2022, 23(20), 12231; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232012231 - 13 Oct 2022

Cited by 4 | Viewed by 2118

Abstract

The presence of neutralizing antibodies against SARS-CoV-2 correlates with protection against infection and severe COVID-19 disease courses. Understanding the dynamics of antibody development against the SARS-CoV-2 virus is important for recommendations on vaccination strategies and on control of the COVID-19 pandemic. This study investigates the dynamics and extent of α-Spike-Ab development by different vaccines manufactured by Johnson & Johnson, AstraZeneca, Pfizer-BioNTech and Moderna. On day 1 after vaccination, we observed a temporal low-grade inflammatory response. α-Spike-Ab titers were reduced after six months of vaccination with mRNA vaccines and increased 14 days after booster vaccinations to a maximum that exceeded titers from mild and critical COVID-19 and Long-COVID patients. Within the group of critical COVID-19 patients, we observed a trend for lower α-Spike-Ab titers in the group of patients who survived COVID-19. This trend accompanied higher numbers of pro-B cells, fewer mature B cells and a higher frequency of T follicular helper cells. Finally, we present data demonstrating that past infection with mild COVID-19 does not lead to long-term increased Ab titers and that even the group of previously infected SARS-CoV-2 patients benefit from a vaccination six months after the infection. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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15 pages, 1554 KiB

Open AccessArticle

Patients Recovering from Severe COVID-19 Develop a Polyfunctional Antigen-Specific CD4+ T Cell Response

by Annamaria Paolini, Rebecca Borella, Anita Neroni, Domenico Lo Tartaro, Marco Mattioli, Lucia Fidanza, Alessia Di Nella, Elena Santacroce, Licia Gozzi, Stefano Busani, Tommaso Trenti, Marianna Meschiari, Giovanni Guaraldi, Massimo Girardis, Cristina Mussini, Lara Gibellini, Sara De Biasi and Andrea Cossarizza

Int. J. Mol. Sci. 2022, 23(14), 8004; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23148004 - 20 Jul 2022

Cited by 7 | Viewed by 2110

Abstract

Specific T cells are crucial to control SARS-CoV-2 infection, avoid reinfection and confer protection after vaccination. We have studied patients with severe or moderate COVID-19 pneumonia, compared to patients who recovered from a severe or moderate infection that had occurred about 4 months before the analyses. In all these subjects, we assessed the polyfunctionality of virus-specific CD4+ and CD8+ T cells by quantifying cytokine production after in vitro stimulation with different SARS-CoV-2 peptide pools covering different proteins (M, N and S). In particular, we quantified the percentage of CD4+ and CD8+ T cells simultaneously producing interferon-γ, tumor necrosis factor, interleukin (IL)-2, IL-17, granzyme B, and expressing CD107a. Recovered patients who experienced a severe disease display high proportions of antigen-specific CD4+ T cells producing Th1 and Th17 cytokines and are characterized by polyfunctional SARS-CoV-2-specific CD4+ T cells. A similar profile was found in patients experiencing a moderate form of COVID-19 pneumonia. No main differences in polyfunctionality were observed among the CD8+ T cell compartments, even if the proportion of responding cells was higher during the infection. The identification of those functional cell subsets that might influence protection can thus help in better understanding the complexity of immune response to SARS-CoV-2. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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26 pages, 3693 KiB

Open AccessArticle

Comprehensive Cytokine Profiling of Patients with COVID-19 Receiving Tocilizumab Therapy

by Anna Lebedeva, Ivan Molodtsov, Alexandra Anisimova, Anastasia Berestovskaya, Oleg Dukhin, Antonina Elizarova, Wendy Fitzgerald, Darya Fomina, Kseniya Glebova, Oxana Ivanova, Anna Kalinskaya, Anastasia Lebedeva, Maryana Lysenko, Elena Maryukhnich, Elena Misyurina, Denis Protsenko, Alexander Rosin, Olga Sapozhnikova, Denis Sokorev, Alexander Shpektor, Daria Vorobyeva, Elena Vasilieva and Leonid Margolis Show full author list Hide full author list

Int. J. Mol. Sci. 2022, 23(14), 7937; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23147937 - 19 Jul 2022

Cited by 1 | Viewed by 2370

Abstract

Coronavirus disease 2019 (COVID-19) is characterized by immune activation in response to viral spread, in severe cases leading to the development of cytokine storm syndrome (CSS) and increased mortality. Despite its importance in prognosis, the pathophysiological mechanisms of CSS in COVID-19 remain to be defined. Towards this goal, we analyzed cytokine profiles and their interrelation in regard to anti-cytokine treatment with tocilizumab in 98 hospitalized patients with COVID-19. We performed a multiplex measurement of 41 circulating cytokines in the plasma of patients on admission and 3–5 days after, during the follow-up. Then we analyzed the patient groups separated in two ways: according to the clusterization of their blood cytokines and based on the administration of tocilizumab therapy. Patients with and without CSS formed distinct clusters according to their cytokine concentration changes. However, the tocilizumab therapy, administered based on the standard clinical and laboratory criteria, did not fully correspond to those clusters of CSS. Furthermore, among all cytokines, IL-6, IL-1RA, IL-10, and G-CSF demonstrated the most prominent differences between patients with and without clinical endpoints, while only IL-1RA was prognostically significant in both groups of patients with and without tocilizumab therapy, decreasing in the former and increasing in the latter during the follow-up period. Thus, CSS in COVID-19, characterized by a correlated release of multiple cytokines, does not fully correspond to the standard parameters of disease severity. Analysis of the cytokine signature, including the IL-1RA level in addition to standard clinical and laboratory parameters may be useful to define the onset of a cytokine storm in COVID-19 as well as the indications for anti-cytokine therapy. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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15 pages, 1835 KiB

Open AccessArticle

T Cells in Multisystem Inflammatory Syndrome in Children (MIS-C) Have a Predominant CD4+ T Helper Response to SARS-CoV-2 Peptides and Numerous Virus-Specific CD4− CD8− Double-Negative T Cells

by Li-En Hsieh, Jaeyoon Song, Alba Grifoni, Chisato Shimizu, Adriana H. Tremoulet, Kirsten B. Dummer, Jane C. Burns, Alessandro Sette and Alessandra Franco

Int. J. Mol. Sci. 2022, 23(13), 7219; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23137219 - 29 Jun 2022

Cited by 10 | Viewed by 1785

Abstract

We studied SARS-CoV-2-specific T cell responses in 22 subacute MIS-C children enrolled in 2021 and 2022 using peptide pools derived from SARS-CoV-2 spike or nonspike proteins. CD4+ and CD8+ SARS-CoV-2-specific T cells were detected in 5 subjects, CD4+ T helper (Th) responses alone were detected in 12 subjects, and CD8+ cytotoxic T cell (CTL) responses alone were documented in 1 subject. Notably, a sizeable subpopulation of CD4− CD8− double-negative (DN) T cells out of total CD3+ T cells was observed in MIS-C (median: 14.5%; IQR 8.65–25.3) and recognized SARS-CoV-2 peptides. T cells bearing the Vβ21.3 T cell receptor (TcRs), previously reported as pathogenic in the context of MIS-C, were detected in high frequencies, namely, in 2.8% and 3.9% of the CD4+ and CD8+ T cells, respectively. However, Vβ21.3 CD8+ T cells that responded to SARS-CoV-2 peptides were detected in only a single subject, suggesting recognition of nonviral antigens in the majority of subjects. Subjects studied 6–14 months after MIS-C showed T cell epitope spreading, meaning the activation of T cells that recognize more SARS-CoV-2 peptides following the initial expansion of T cells that see immunodominant epitopes. For example, subjects that did not recognize nonspike proteins in the subacute phase of MIS-C showed good Th response to nonspike peptides, and/or CD8+ T cell responses not appreciable before arose over time and could be detected in the 6–14 months’ follow-up. The magnitude of the Th and CTL responses also increased over time. In summary, patients with MIS-C associated with acute lymphopenia, a classical feature of MIS-C, showed a physiological response to the virus with a prominent role for virus-specific DN T cells. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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13 pages, 1771 KiB

Open AccessArticle

Early and Polyantigenic CD4 T Cell Responses Correlate with Mild Disease in Acute COVID-19 Donors

by Alison Tarke, Marina Potesta, Stefania Varchetta, Daniela Fenoglio, Marco Iannetta, Loredana Sarmati, Dalila Mele, Chiara Dentone, Matteo Bassetti, Carla Montesano, Mario U. Mondelli, Gilberto Filaci, Alba Grifoni and Alessandro Sette

Int. J. Mol. Sci. 2022, 23(13), 7155; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23137155 - 28 Jun 2022

Cited by 28 | Viewed by 3870

Abstract

We assessed SARS-CoV-2-specific CD4+ and CD8+ T cell responses in samples from 89 acute COVID-19 patients, utilizing blood samples collected during the first wave of COVID-19 in Italy. The goal of the study was to examine correlations between SARS-CoV-2-specific T cell responses in the early phase comparing mild, moderate, or severe COVID-19 disease outcomes. T cell responses to the spike (S) and non-S proteins were measured in a combined activation-induced marker (AIM) and intracellular cytokine staining (ICS) assay. Early CD4+ T cell responses to SARS-CoV-2 S correlated with milder disease by both AIM and IFNγ ICS readouts. The correlation of S-specific CD4+ T cell responses with milder disease severity was most striking within the first two weeks of symptom onset compared to later time points. Furthermore, donors with milder disease were associated with polyantigenic CD4+ T cell responses that recognized more prominently non-S proteins in addition to S, while severe acute COVID-19 was characterized by lower magnitudes of CD4+ T cell responses and a narrower repertoire. In conclusion, this study highlights that both the magnitude and breadth of early SARS-CoV-2-specific CD4+ T cell responses correlated with milder disease outcomes in acute COVID-19 patients. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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16 pages, 651 KiB

Open AccessReview

Immunology of Multisystem Inflammatory Syndrome after COVID-19 in Children: A Review of the Current Evidence

by Filippos Filippatos, Elizabeth-Barbara Tatsi and Athanasios Michos

Int. J. Mol. Sci. 2023, 24(6), 5711; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24065711 - 16 Mar 2023

Cited by 5 | Viewed by 2553

Abstract

Immune responses following severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in children are still under investigation. Even though coronavirus disease 2019 (COVID-19) is usually mild in the pediatric population, some children exhibit severe clinical manifestations, require hospitalization, or develop the most severe condition: a multisystem inflammatory syndrome in children (MIS-C) associated with SARS-CoV-2 infection. The activated innate, humoral and T-cell-mediated immunological pathways that lead certain pediatric populations to present with MIS-C or remain asymptomatic after SARS-CoV-2 infection are yet to be established. This review focuses on the immunological aspects of MIS-C with respect to innate, humoral, and cellular immunity. In addition, presents the role of the SARS-CoV-2 Spike protein as a superantigen in the pathophysiological mechanisms, discusses the great heterogeneity among the immunological studies in the pediatric population, and highlights possible reasons why some children with a certain genetic background present with MIS-C. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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14 pages, 621 KiB

Open AccessReview

Can T Cells Abort SARS-CoV-2 and Other Viral Infections?

by Leo Swadling and Mala K. Maini

Int. J. Mol. Sci. 2023, 24(5), 4371; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24054371 - 22 Feb 2023

Cited by 4 | Viewed by 2330

Abstract

Despite the highly infectious nature of the SARS-CoV-2 virus, it is clear that some individuals with potential exposure, or even experimental challenge with the virus, resist developing a detectable infection. While a proportion of seronegative individuals will have completely avoided exposure to the virus, a growing body of evidence suggests a subset of individuals are exposed, but mediate rapid viral clearance before the infection is detected by PCR or seroconversion. This type of “abortive” infection likely represents a dead-end in transmission and precludes the possibility for development of disease. It is, therefore, a desirable outcome on exposure and a setting in which highly effective immunity can be studied. Here, we describe how early sampling of a new pandemic virus using sensitive immunoassays and a novel transcriptomic signature can identify abortive infections. Despite the challenges in identifying abortive infections, we highlight diverse lines of evidence supporting their occurrence. In particular, expansion of virus-specific T cells in seronegative individuals suggests abortive infections occur not only after exposure to SARS-CoV-2, but for other coronaviridae, and diverse viral infections of global health importance (e.g., HIV, HCV, HBV). We discuss unanswered questions related to abortive infection, such as: ‘Are we just missing antibodies? Are T cells an epiphenomenon? What is the influence of the dose of viral inoculum?’ Finally, we argue for a refinement of the current paradigm that T cells are only involved in clearing established infection; instead, we emphasise the importance of considering their role in terminating early viral replication by studying abortive infections. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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20 pages, 1073 KiB

Open AccessReview

Durable CD8 T Cell Memory against SARS-CoV-2 by Prime/Boost and Multi-Dose Vaccination: Considerations on Inter-Dose Time Intervals

by Ambra Natalini, Sonia Simonetti, Carmel Sher, Ugo D’Oro, Adrian C. Hayday and Francesca Di Rosa

Int. J. Mol. Sci. 2022, 23(22), 14367; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232214367 - 19 Nov 2022

Cited by 4 | Viewed by 2308

Abstract

Facing the COVID-19 pandemic, anti-SARS-CoV-2 vaccines were developed at unprecedented pace, productively exploiting contemporary fundamental research and prior art. Large-scale use of anti-SARS-CoV-2 vaccines has greatly limited severe morbidity and mortality. Protection has been correlated with high serum titres of neutralizing antibodies capable of blocking the interaction between the viral surface protein spike and the host SARS-CoV-2 receptor, ACE-2. Yet, vaccine-induced protection subsides over time, and breakthrough infections are commonly observed, mostly reflecting the decay of neutralizing antibodies and the emergence of variant viruses with mutant spike proteins. Memory CD8 T cells are a potent weapon against viruses, as they are against tumour cells. Anti-SARS-CoV-2 memory CD8 T cells are induced by either natural infection or vaccination and can be potentially exploited against spike-mutated viruses. We offer here an overview of current research about the induction of anti-SARS-CoV-2 memory CD8 T cells by vaccination, in the context of prior knowledge on vaccines and on fundamental mechanisms of immunological memory. We focus particularly on how vaccination by two doses (prime/boost) or more (boosters) promotes differentiation of memory CD8 T cells, and on how the time-length of inter-dose intervals may influence the magnitude and persistence of CD8 T cell memory. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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13 pages, 610 KiB

Open AccessReview

Act Early and at the Right Location: SARS-CoV-2 T Cell Kinetics and Tissue Localization

by Antonio Bertoletti, Nina Le Bert and Anthony T. Tan

Int. J. Mol. Sci. 2022, 23(18), 10679; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231810679 - 14 Sep 2022

Cited by 4 | Viewed by 2230

Abstract

The emergence of new SARS-CoV-2 lineages able to escape antibodies elicited by infection or vaccination based on the Spike protein of the Wuhan isolates has reduced the ability of Spike-specific antibodies to protect previously infected or vaccinated individuals from infection. Therefore, the role played by T cells in the containment of viral replication and spread after infection has taken a more central stage. In this brief review, we will discuss the role played by T cells in the protection from COVID-19, with a particular emphasis on the kinetics of the T cell response and its localization at the site of primary infection. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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18 pages, 2878 KiB

Open AccessReview

Evolution of Anti-SARS-CoV-2 Therapeutic Antibodies

by Juan C. Almagro, Gabriela Mellado-Sánchez, Martha Pedraza-Escalona and Sonia M. Pérez-Tapia

Int. J. Mol. Sci. 2022, 23(17), 9763; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23179763 - 28 Aug 2022

Cited by 17 | Viewed by 4516

Abstract

Since the first COVID-19 reports back in December of 2019, this viral infection caused by SARS-CoV-2 has claimed millions of lives. To control the COVID-19 pandemic, the Food and Drug Administration (FDA) and/or European Agency of Medicines (EMA) have granted Emergency Use Authorization (EUA) to nine therapeutic antibodies. Nonetheless, the natural evolution of SARS-CoV-2 has generated numerous variants of concern (VOCs) that have challenged the efficacy of the EUA antibodies. Here, we review the most relevant characteristics of these therapeutic antibodies, including timeline of approval, neutralization profile against the VOCs, selection methods of their variable regions, somatic mutations, HCDR3 and LCDR3 features, isotype, Fc modifications used in the therapeutic format, and epitope recognized on the receptor-binding domain (RBD) of SARS-CoV-2. One of the conclusions of the review is that the EUA therapeutic antibodies that still retain efficacy against new VOCs bind an epitope formed by conserved residues that seem to be evolutionarily conserved as thus, critical for the RBD:hACE-2 interaction. The information reviewed here should help to design new and more efficacious antibodies to prevent and/or treat COVID-19, as well as other infectious diseases. Full article

(This article belongs to the Special Issue The Adaptive Immunity in COVID-19)

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