Cellular and humoral immunogenicity against SARS-CoV-2 vaccination or infection is associated with the memory phenotype of T- and B-lymphocytes in adult allogeneic hematopoietic cell transplant recipients.

Allogeneic hematopoietic cell transplantation Coronavirus disease 2019 (COVID-19) Memory B cells Memory T cells Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)

Journal

International journal of hematology
ISSN: 1865-3774
Titre abrégé: Int J Hematol
Pays: Japan
ID NLM: 9111627

Informations de publication

Date de publication:
06 Jun 2024
Historique:
received: 06 10 2023
accepted: 22 05 2024
revised: 10 05 2024
medline: 6 6 2024
pubmed: 6 6 2024
entrez: 6 6 2024
Statut: aheadofprint

Résumé

We conducted a cross-sectional study to evaluate cellular and humoral immunogenicity against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination or infection and examine how lymphocyte subpopulations in peripheral blood correlate with cellular and humoral immunogenicity in adult allogeneic hematopoietic cell transplantation (HCT) recipients. The median period from SARS-CoV-2 vaccination or infection to sample collection was 110.5 days (range, 6-345 days). The median SARS-CoV-2 spike-specific antibody level was 1761 binding antibody units (BAU)/ml (range, 0 to > 11,360 BAU/ml). Enzyme-linked immunosorbent spot (ELISpot) assay of T cells stimulated with SARS-CoV-2 spike antigens showed that interferon-gamma (IFN-γ)-, interleukin-2 (IL-2)-, and IFN-γ + IL-2-producing T cells were present in 68.9%, 62.0%, and 56.8% of patients, respectively. The antibody level was significantly correlated with frequency of IL-2-producing T cells (P = 0.001) and IFN-γ + IL-2-producing T cells (P = 0.006) but not IFN-γ-producing T cells (P = 0.970). Absolute counts of CD8+ and CD4+ central memory T cells were higher in both IL-2- and IFN-γ + IL-2-producing cellular responders compared with non-responders. These data suggest that cellular and humoral immunogenicity against SARS-CoV-2 vaccination or infection is associated with the memory phenotype of T cells and B cells in adult allogeneic HCT recipients.

Identifiants

pubmed: 38842630
doi: 10.1007/s12185-024-03802-3
pii: 10.1007/s12185-024-03802-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Wiersinga WJ, Rhodes A, Cheng AC, Peacock SJ, Prescott HC. Pathophysiology, transmission, diagnosis, and treatment of coronavirus disease 2019 (COVID-19): a review. JAMA. 2020;324:782–93.
pubmed: 32648899 doi: 10.1001/jama.2020.12839
Hu B, Guo H, Zhou P, Shi ZL. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 2021;19:141–54.
pubmed: 33024307 doi: 10.1038/s41579-020-00459-7
Sahin U, Muik A, Vogler I, Derhovanessian E, Kranz LM, Vormehr M, et al. BNT162b2 vaccine induces neutralizing antibodies and poly-specific T cells in humans. Nature. 2021;595:572–7.
pubmed: 34044428 doi: 10.1038/s41586-021-03653-6
El Sahly HM, Baden LR, Essink B, Doblecki-Lewis S, Martin JM, Anderson EJ, et al. Efficacy of the mRNA-1273 SARS-CoV-2 vaccine at completion of blinded phase. N Engl J Med. 2021;385:1774–85.
pubmed: 34551225 doi: 10.1056/NEJMoa2113017
Vijenthira A, Gong IY, Fox TA, Booth S, Cook G, Fattizzo B, et al. Outcomes of patients with hematologic malignancies and COVID-19: a systematic review and meta-analysis of 3377 patients. Blood. 2020;136:2881–92.
pubmed: 33113551 pmcid: 7746126 doi: 10.1182/blood.2020008824
Langerbeins P, Hallek M. COVID-19 in patients with hematologic malignancy. Blood. 2022;140:236–52.
pubmed: 35544585 pmcid: 9098396 doi: 10.1182/blood.2021012251
Sharma A, Bhatt NS, St Martin A, Abid MB, Bloomquist J, Chemaly RF, et al. Clinical characteristics and outcomes of COVID-19 in haematopoietic stem-cell transplantation recipients: an observational cohort study. Lancet Haematol. 2021;8:e185–93.
pubmed: 33482113 pmcid: 7816949 doi: 10.1016/S2352-3026(20)30429-4
Ljungman P, de la Camara R, Mikulska M, Tridello G, Aguado B, Zahrani MA, et al. COVID-19 and stem cell transplantation; results from an EBMT and GETH multicenter prospective survey. Leukemia. 2021;35:2885–94.
pubmed: 34079042 pmcid: 8171362 doi: 10.1038/s41375-021-01302-5
Schaffrath J, Brummer C, Wolff D, Holtick U, Kröger N, Bornhäuser M, et al. High mortality of COVID-19 early after allogeneic stem cell transplantation: a retrospective multicenter analysis on behalf of the German Cooperative Transplant Study Group. Transplant Cell Ther. 2022;28:337.e1-337.e10.
pubmed: 35296445 doi: 10.1016/j.jtct.2022.03.010
Piechotta V, Mellinghoff SC, Hirsch C, Brinkmann A, Iannizzi C, Kreuzberger N, et al. Effectiveness, immunogenicity, and safety of COVID-19 vaccines for individuals with hematological malignancies: a systematic review. Blood Cancer J. 2022;12:86.
pubmed: 35641489 pmcid: 9152308 doi: 10.1038/s41408-022-00684-8
Sette A, Crotty S. Adaptive immunity to SARS-CoV-2 and COVID-19. Cell. 2021;184:861–80.
pubmed: 33497610 pmcid: 7803150 doi: 10.1016/j.cell.2021.01.007
Kedzierska K, Thomas PG. Count on us: T cells in SARS-CoV-2 infection and vaccination. Cell Rep Med. 2022;3: 100562.
pubmed: 35474748 pmcid: 8872824 doi: 10.1016/j.xcrm.2022.100562
Bertoletti A, Le Bert N, Tan AT. SARS-CoV-2-specific T cells in the changing landscape of the COVID-19 pandemic. Immunity. 2022;55:1764–78.
pubmed: 36049482 pmcid: 9385766 doi: 10.1016/j.immuni.2022.08.008
Almendro-Vázquez P, Laguna-Goya R, Paz-Artal E. Defending against SARS-CoV-2: the T cell perspective. Front Immunol. 2023;14:1107803.
pubmed: 36776863 pmcid: 9911802 doi: 10.3389/fimmu.2023.1107803
Redjoul R, Le Bouter A, Beckerich F, Fourati S, Maury S. Antibody response after second BNT162b2 dose in allogeneic HSCT recipients. Lancet. 2021;398:298–9.
pubmed: 34270933 pmcid: 8277189 doi: 10.1016/S0140-6736(21)01594-4
Maneikis K, Šablauskas K, Ringelevičiūtė U, Vaitekėnaitė V, Čekauskienė R, Kryžauskaitė L, et al. Immunogenicity of the BNT162b2 COVID-19 mRNA vaccine and early clinical outcomes in patients with haematological malignancies in Lithuania: a national prospective cohort study. Lancet Haematol. 2021;8:e583–92.
pubmed: 34224668 pmcid: 8253543 doi: 10.1016/S2352-3026(21)00169-1
Le Bourgeois A, Coste-Burel M, Guillaume T, Peterlin P, Garnier A, Béné MC, et al. Safety and antibody response after 1 and 2 doses of BNT162b2 mRNA vaccine in recipients of allogeneic hematopoietic stem cell transplant. JAMA Netw Open. 2021;4: e2126344.
pubmed: 34519770 pmcid: 8441592 doi: 10.1001/jamanetworkopen.2021.26344
Dhakal B, Abedin S, Fenske T, Chhabra S, Ledeboer N, Hari P, et al. Response to SARS-CoV-2 vaccination in patients after hematopoietic cell transplantation and CAR T-cell therapy. Blood. 2021;138:1278–81.
pubmed: 34339501 pmcid: 8332674 doi: 10.1182/blood.2021012769
Canti L, Humblet-Baron S, Desombere I, Neumann J, Pannus P, Heyndrickx L, et al. Predictors of neutralizing antibody response to BNT162b2 vaccination in allogeneic hematopoietic stem cell transplant recipients. J Hematol Oncol. 2021;14:174.
pubmed: 34689821 pmcid: 8542409 doi: 10.1186/s13045-021-01190-3
Tamari R, Politikos I, Knorr DA, Vardhana SA, Young JC, Marcello LT, et al. Predictors of humoral response to SARS-CoV-2 vaccination after hematopoietic cell transplantation and CAR T-cell therapy. Blood Cancer Discov. 2021;2:577–85.
pubmed: 34778798 pmcid: 8580614 doi: 10.1158/2643-3230.BCD-21-0142
Bergman P, Blennow O, Hansson L, Mielke S, Nowak P, Chen P, et al. Safety and efficacy of the mRNA BNT162b2 vaccine against SARS-CoV-2 in five groups of immunocompromised patients and healthy controls in a prospective open-label clinical trial. EBioMedicine. 2021;74: 103705.
pubmed: 34861491 pmcid: 8629680 doi: 10.1016/j.ebiom.2021.103705
Mamez AC, Pradier A, Giannotti F, Petitpas A, Urdiola MF, Vu DL, et al. Antibody responses to SARS-CoV2 vaccination in allogeneic hematopoietic stem cell transplant recipients. Bone Marrow Transplant. 2021;56:3094–6.
pubmed: 34584239 pmcid: 8477622 doi: 10.1038/s41409-021-01466-9
Piñana JL, López-Corral L, Martino R, Montoro J, Vazquez L, Pérez A, et al. SARS-CoV-2-reactive antibody detection after SARS-CoV-2 vaccination in hematopoietic stem cell transplant recipients: prospective survey from the Spanish Hematopoietic Stem Cell Transplantation and Cell Therapy Group. Am J Hematol. 2022;97:30–42.
pubmed: 34695229 doi: 10.1002/ajh.26385
Maillard A, Redjoul R, Klemencie M, Labussière Wallet H, Le Bourgeois A, D’Aveni M, et al. Antibody response after 2 and 3 doses of SARS-CoV-2 mRNA vaccine in allogeneic hematopoietic cell transplant recipients. Blood. 2022;139:134–7.
pubmed: 34818411 doi: 10.1182/blood.2021014232
Morsink LM, van Doesum J, Choi G, Hazenberg CLE, Biswana A, Meppelink F, et al. Robust COVID-19 vaccination response after allogeneic stem cell transplantation using post transplantation cyclophosphamide conditioning. Blood Cancer J. 2022;12:6.
pubmed: 35022420 pmcid: 8754065 doi: 10.1038/s41408-021-00605-1
Shem-Tov N, Yerushalmi R, Danylesko I, Litachevsky V, Levy I, Olmer L, et al. Immunogenicity and safety of the BNT162b2 mRNA COVID-19 vaccine in haematopoietic stem cell transplantation recipients. Br J Haematol. 2022;196:884–91.
pubmed: 34713441 doi: 10.1111/bjh.17918
Attolico I, Tarantini F, Carluccio P, Schifone CP, Delia M, Gagliardi VP, et al. Serological response following BNT162b2 anti-SARS-CoV-2 mRNA vaccination in haematopoietic stem cell transplantation patients. Br J Haematol. 2022;196:928–31.
pubmed: 34664267 doi: 10.1111/bjh.17873
Yeshurun M, Pasvolsky O, Shargian L, Yahav D, Ben-Zvi H, Rubinstein M, et al. Humoral serological response to the BNT162b2 vaccine after allogeneic haematopoietic cell transplantation. Clin Microbiol Infect. 2022;28:303.e1-303.e4.
pubmed: 34715348 doi: 10.1016/j.cmi.2021.10.007
Tsushima T, Terao T, Narita K, Fukumoto A, Ikeda D, Kamura Y, et al. Antibody response to COVID-19 vaccine in 130 recipients of hematopoietic stem cell transplantation. Int J Hematol. 2022;115:611–5.
pubmed: 35426579 pmcid: 9011370 doi: 10.1007/s12185-022-03325-9
Huang A, Cicin-Sain C, Pasin C, Epp S, Audigé A, Müller NJ, et al. Antibody response to SARS-CoV-2 vaccination in patients following allogeneic hematopoietic cell transplantation. Transplant Cell Ther. 2022;28:214.e1-214.e11.
pubmed: 35092892 doi: 10.1016/j.jtct.2022.01.019
Mori Y, Uchida N, Harada T, Katayama Y, Wake A, Iwasaki H, et al. Predictors of impaired antibody response after SARS-CoV-2 mRNA vaccination in hematopoietic cell transplant recipients: a Japanese multicenter observational study. Am J Hematol. 2023;98:102–11.
pubmed: 36260658 doi: 10.1002/ajh.26769
Toya T, Atsuta Y, Sanada T, Honda T, Sadato D, Sekiya N, et al. Attenuated humoral response against SARS-CoV-2 mRNA vaccination in allogeneic stem cell transplantation recipients. Cancer Sci. 2023;114:586–95.
pubmed: 36161681 doi: 10.1111/cas.15603
Lindemann M, Klisanin V, Thümmler L, Fisenkci N, Tsachakis-Mück N, Ditschkowski M, et al. Humoral and cellular vaccination responses against SARS-CoV-2 in hematopoietic stem cell transplant recipients. Vaccines (Basel). 2021;9:1075.
pubmed: 34696183 doi: 10.3390/vaccines9101075
Ram R, Hagin D, Kikozashvilli N, Freund T, Amit O, Bar-On Y, et al. Safety and immunogenicity of the BNT162b2 mRNA COVID-19 vaccine in patients after allogeneic HCT or CD19-based CART therapy-a single-center prospective cohort study. Transplant Cell Ther. 2021;27:788–94.
pubmed: 34214738 pmcid: 8242200 doi: 10.1016/j.jtct.2021.06.024
Jiménez M, Roldán E, Fernández-Naval C, Villacampa G, Martinez-Gallo M, Medina-Gil D, et al. Cellular and humoral immunogenicity of the mRNA-1273 SARS-CoV-2 vaccine in patients with hematologic malignancies. Blood Adv. 2022;6:774–84.
pubmed: 34844263 pmcid: 8632354 doi: 10.1182/bloodadvances.2021006101
Clémenceau B, Guillaume T, Coste-Burel M, Peterlin P, Garnier A, Le Bourgeois A, et al. SARS-CoV-2 T-cell responses in allogeneic hematopoietic stem cell recipients following two doses of BNT162b2 mRNA vaccine. Vaccines (Basel). 2022;10:448.
pubmed: 35335079 doi: 10.3390/vaccines10030448
Thümmler L, Koldehoff M, Fisenkci N, Brochhagen L, Horn PA, Krawczyk A, et al. Cellular and humoral immunity after the third vaccination against SARS-CoV-2 in hematopoietic stem-cell transplant recipients. Vaccines (Basel). 2022;10:972.
pubmed: 35746580 doi: 10.3390/vaccines10060972
Gavriilaki E, Papadopoulou A, Touloumenidou T, Stavridou F, Koravou EE, Giannaki M, et al. Neutralizing antibody and T cell responses to SARS-CoV-2 vaccination in hematopoietic cell transplant recipients. Bone Marrow Transplant. 2022;57:1183–6.
pubmed: 35449455 pmcid: 9022618 doi: 10.1038/s41409-022-01675-w
Cuffel A, Maylin S, Le Buanec H, Delaugerre C, Minier M, Bergerat D, et al. Humoral and cellular responses to SARS-CoV-2 BNT162b2 vaccination in allogeneic hematopoietic stem cell transplantation recipients. Vaccine. 2022;40:4682–5.
pubmed: 35840470 pmcid: 9271460 doi: 10.1016/j.vaccine.2022.07.006
Malard F, Gaugler B, Gozlan J, Bouquet L, Fofana D, Siblany L, et al. Weak immunogenicity of SARS-CoV-2 vaccine in patients with hematologic malignancies. Blood Cancer J. 2021;11:142.
pubmed: 34376633 pmcid: 8353615 doi: 10.1038/s41408-021-00534-z
Murray SM, Barbanti M, Campbell C, Brown A, Chen L, Dhanapal J, et al. Impaired humoral and cellular response to primary COVID-19 vaccination in patients less than 2 years after allogeneic bone marrow transplant. Br J Haematol. 2022;198:668–79.
pubmed: 35655410 doi: 10.1111/bjh.18312
Clémenceau B, Le Bourgeois A, Guillaume T, Coste-Burel M, Peterlin P, Garnier A, et al. Strong SARS-CoV-2 T-cell responses after one or two COVID-19 vaccine boosters in allogeneic hematopoietic stem cell recipients. Cells. 2022;11:3010.
pubmed: 36230971 pmcid: 9563037 doi: 10.3390/cells11193010
Meyer T, Ihorst G, Bartsch I, Zeiser R, Wäsch R, Bertz H, et al. Cellular and humoral SARS-CoV-2 vaccination responses in 192 adult recipients of allogeneic hematopoietic cell transplantation. Vaccines (Basel). 2022;10:1782.
pubmed: 36366291 doi: 10.3390/vaccines10111782
Zuo J, Dowell AC, Pearce H, Verma K, Long HM, Begum J, et al. Robust SARS-CoV-2-specific T cell immunity is maintained at 6 months following primary infection. Nat Immunol. 2021;22:620–6.
pubmed: 33674800 pmcid: 7610739 doi: 10.1038/s41590-021-00902-8
Almendro-Vázquez P, Laguna-Goya R, Ruiz-Ruigomez M, Utrero-Rico A, Lalueza A, Maestro de la Calle G, et al. Longitudinal dynamics of SARS-CoV-2-specific cellular and humoral immunity after natural infection or BNT162b2 vaccination. PLoS Pathog. 2021;17: e1010211.
pubmed: 34962970 pmcid: 8757952 doi: 10.1371/journal.ppat.1010211
Adachi E, Nagai E, Saito M, Isobe M, Konuma T, Koga M, et al. Anti-spike protein antibody titer at the time of breakthrough infection of SARS-CoV-2 omicron. J Infect Chemother. 2022;28:1015–7.
pubmed: 35397976 pmcid: 8971116 doi: 10.1016/j.jiac.2022.03.021
Cook LB, O’Dell G, Vourvou E, Palanicawandar R, Marks S, Milojkovic D, et al. Third primary SARS-CoV-2 mRNA vaccines enhance antibody responses in most patients with haematological malignancies. Nat Commun. 2022;13:6922.
pubmed: 36376307 pmcid: 9662771 doi: 10.1038/s41467-022-34657-z
Gilbert PB, Montefiori DC, McDermott AB, Fong Y, Benkeser D, Deng W, et al. Immune correlates analysis of the mRNA-1273 COVID-19 vaccine efficacy clinical trial. Science. 2022;375:43–50.
pubmed: 34812653 doi: 10.1126/science.abm3425
Schwarzkopf S, Krawczyk A, Knop D, Klump H, Heinold A, Heinemann FM, et al. Cellular immunity in COVID-19 convalescents with PCR-confirmed infection but with undetectable SARS-CoV-2-specific IgG. Emerg Infect Dis. 2021;27:122–9.
pmcid: 7774536 doi: 10.3201/eid2701.203772
Yi JS, Rosa-Bray M, Staats J, Zakroysky P, Chan C, Russo MA, et al. Establishment of normative ranges of the healthy human immune system with comprehensive polychromatic flow cytometry profiling. PLoS ONE. 2019;14: e0225512.
pubmed: 31825961 pmcid: 6905525 doi: 10.1371/journal.pone.0225512
Widge AT, Rouphael NG, Jackson LA, Anderson EJ, Roberts PC, Makhene M, et al. Durability of responses after SARS-CoV-2 mRNA-1273 vaccination. N Engl J Med. 2021;384:80–2.
pubmed: 33270381 doi: 10.1056/NEJMc2032195
Shrotri M, Navaratnam AMD, Nguyen V, Byrne T, Geismar C, Fragaszy E, et al. Spike-antibody waning after second dose of BNT162b2 or ChAdOx1. Lancet. 2021;398:385–7.
pubmed: 34274038 pmcid: 8285117 doi: 10.1016/S0140-6736(21)01642-1
Levin EG, Lustig Y, Cohen C, Fluss R, Indenbaum V, Amit S, et al. Waning immune humoral response to BNT162b2 Covid-19 vaccine over 6 months. N Engl J Med. 2021;385: e84.
pubmed: 34614326 doi: 10.1056/NEJMoa2114583
Ibarrondo FJ, Fulcher JA, Goodman-Meza D, Elliott J, Hofmann C, Hausner MA, et al. Rapid decay of anti-SARS-CoV-2 antibodies in persons with mild Covid-19. N Engl J Med. 2020;383:1085–7.
pubmed: 32706954 doi: 10.1056/NEJMc2025179
Long QX, Tang XJ, Shi QL, Li Q, Deng HJ, Yuan J, et al. Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections. Nat Med. 2020;26:1200–4.
pubmed: 32555424 doi: 10.1038/s41591-020-0965-6
Leclerc M, Redjoul R, Le Bouter A, Beckerich F, Robin C, Parinet V, et al. Determinants of SARS-CoV-2 waning immunity in allogeneic hematopoietic stem cell transplant recipients. J Hematol Oncol. 2022;15:27.
pubmed: 35303906 pmcid: 8931584 doi: 10.1186/s13045-022-01250-2
Piñana JL, Martino R, Vazquez L, López-Corral L, Pérez A, Chorão P, et al. SARS-CoV-2-reactive antibody waning, booster effect and breakthrough SARS-CoV-2 infection in hematopoietic stem cell transplant and cell therapy recipients at one year after vaccination. Bone Marrow Transplant. 2023;58:567–80.
pubmed: 36854892 pmcid: 9974060 doi: 10.1038/s41409-023-01946-0
Laurén I, Havervall S, Ng H, Lord M, Pettke A, Greilert-Norin N, et al. Long-term SARS-CoV-2-specific and cross-reactive cellular immune responses correlate with humoral responses, disease severity, and symptomatology. Immun Inflamm Dis. 2022;10: e595.
pubmed: 35349756 pmcid: 8962644 doi: 10.1002/iid3.595
Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell. 2020;183:996–1012.
pubmed: 33010815 pmcid: 7494270 doi: 10.1016/j.cell.2020.09.038
Mathew D, Giles JR, Baxter AE, Oldridge DA, Greenplate AR, Wu JE, et al. Deep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implications. Science. 2020;369: eabc8511.
pubmed: 32669297 pmcid: 7402624 doi: 10.1126/science.abc8511
Turner JS, Kim W, Kalaidina E, Goss CW, Rauseo AM, Schmitz AJ, et al. SARS-CoV-2 infection induces long-lived bone marrow plasma cells in humans. Nature. 2021;595:421–5.
pubmed: 34030176 doi: 10.1038/s41586-021-03647-4
Millington KA, Innes JA, Hackforth S, Hinks TS, Deeks JJ, Dosanjh DP, et al. Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J Immunol. 2007;178:5217–26.
pubmed: 17404305 doi: 10.4049/jimmunol.178.8.5217
Kundu R, Narean JS, Wang L, Fenn J, Pillay T, Fernandez ND, et al. Cross-reactive memory T cells associate with protection against SARS-CoV-2 infection in COVID-19 contacts. Nat Commun. 2022;13:80.
pubmed: 35013199 pmcid: 8748880 doi: 10.1038/s41467-021-27674-x
Poon MML, Rybkina K, Kato Y, Kubota M, Matsumoto R, Bloom NI, et al. SARS-CoV-2 infection generates tissue-localized immunological memory in humans. Sci Immunol. 2021;6: eabl9105.
pubmed: 34618554 pmcid: 8626868 doi: 10.1126/sciimmunol.abl9105
Roukens AHE, Pothast CR, König M, Huisman W, Dalebout T, Tak T, et al. Prolonged activation of nasal immune cell populations and development of tissue-resident SARS-CoV-2-specific CD8+ T cell responses following COVID-19. Nat Immunol. 2022;23:23–32.
pubmed: 34937933 doi: 10.1038/s41590-021-01095-w
Isho B, Abe KT, Zuo M, Jamal AJ, Rathod B, Wang JH, et al. Persistence of serum and saliva antibody responses to SARS-CoV-2 spike antigens in COVID-19 patients. Sci Immunol. 2020;5: eabe5511.
pubmed: 33033173 pmcid: 8050884 doi: 10.1126/sciimmunol.abe5511
Wang Z, Lorenzi JCC, Muecksch F, Finkin S, Viant C, Gaebler C, et al. Enhanced SARS-CoV-2 neutralization by dimeric IgA. Sci Transl Med. 2021;13: eabf1555.
pubmed: 33288661 doi: 10.1126/scitranslmed.abf1555
Molodtsov IA, Kegeles E, Mitin AN, Mityaeva O, Musatova OE, Panova AE, et al. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)-specific T cells and antibodies in coronavirus disease 2019 (COVID-19) protection: a prospective study. Clin Infect Dis. 2022;75:e1–9.
pubmed: 35435222 pmcid: 9047235 doi: 10.1093/cid/ciac278
Goel RR, Painter MM, Apostolidis SA, Mathew D, Meng W, Rosenfeld AM, et al. mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern. Science. 2021;374: abm0829.
pubmed: 34648302 pmcid: 9284784 doi: 10.1126/science.abm0829
Tarke A, Coelho CH, Zhang Z, Dan JM, Yu ED, Methot N, et al. SARS-CoV-2 vaccination induces immunological T cell memory able to cross-recognize variants from Alpha to Omicron. Cell. 2022;185:847–59.
pubmed: 35139340 pmcid: 8784649 doi: 10.1016/j.cell.2022.01.015

Auteurs

Takaaki Konuma (T)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan. tkonuma@ims.u-tokyo.ac.jp.

Megumi Hamatani-Asakura (M)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan.

Etsuko Nagai (E)

Department of Laboratory Medicine, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Eisuke Adachi (E)

Department of Infectious Diseases and Applied Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Seiko Kato (S)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan.

Masamichi Isobe (M)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan.

Maki Monna-Oiwa (M)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan.

Satoshi Takahashi (S)

Division of Clinical Precision Research Platform, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Hiroshi Yotsuyanagi (H)

Department of Infectious Diseases and Applied Immunology, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Yasuhito Nannya (Y)

Department of Hematology/Oncology, The Institute of Medical Science, The University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo, Japan.

Classifications MeSH