Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection
Jennifer M Dan, Jose Mateus, Yu Kato, Kathryn M Hastie, Esther Dawen Yu, Caterina E Faliti, Alba Grifoni, Sydney I Ramirez, Sonya Haupt, April Frazier, Catherine Nakao, Vamseedhar Rayaprolu, Stephen A Rawlings, Bjoern Peters, Florian Krammer, Viviana Simon, Erica Ollmann Saphire, Davey M Smith, Daniela Weiskopf, Alessandro Sette, Shane Crotty, Jennifer M Dan, Jose Mateus, Yu Kato, Kathryn M Hastie, Esther Dawen Yu, Caterina E Faliti, Alba Grifoni, Sydney I Ramirez, Sonya Haupt, April Frazier, Catherine Nakao, Vamseedhar Rayaprolu, Stephen A Rawlings, Bjoern Peters, Florian Krammer, Viviana Simon, Erica Ollmann Saphire, Davey M Smith, Daniela Weiskopf, Alessandro Sette, Shane Crotty
Abstract
Understanding immune memory to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is critical for improving diagnostics and vaccines and for assessing the likely future course of the COVID-19 pandemic. We analyzed multiple compartments of circulating immune memory to SARS-CoV-2 in 254 samples from 188 COVID-19 cases, including 43 samples at ≥6 months after infection. Immunoglobulin G (IgG) to the spike protein was relatively stable over 6+ months. Spike-specific memory B cells were more abundant at 6 months than at 1 month after symptom onset. SARS-CoV-2-specific CD4+ T cells and CD8+ T cells declined with a half-life of 3 to 5 months. By studying antibody, memory B cell, CD4+ T cell, and CD8+ T cell memory to SARS-CoV-2 in an integrated manner, we observed that each component of SARS-CoV-2 immune memory exhibited distinct kinetics.
Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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References
- Stephens D. S., McElrath M. J., COVID-19 and the Path to Immunity. JAMA 324, 1279–1281 (2020). 10.1001/jama.2020.16656
- Grifoni A., Weiskopf D., Ramirez S. I., Mateus J., Dan J. M., Moderbacher C. R., Rawlings S. A., Sutherland A., Premkumar L., Jadi R. S., Marrama D., de Silva A. M., Frazier A., Carlin A. F., Greenbaum J. A., Peters B., Krammer F., Smith D. M., Crotty S., Sette A., Targets of T Cell Responses to SARS-CoV-2 Coronavirus in Humans with COVID-19 Disease and Unexposed Individuals. Cell 181, 1489–1501.e15 (2020). 10.1016/j.cell.2020.05.015
- Krammer F., SARS-CoV-2 vaccines in development. Nature 586, 516–527 (2020). 10.1038/s41586-020-2798-3
- Suthar M. S., Zimmerman M. G., Kauffman R. C., Mantus G., Linderman S. L., Hudson W. H., Vanderheiden A., Nyhoff L., Davis C. W., Adekunle O., Affer M., Sherman M., Reynolds S., Verkerke H. P., Alter D. N., Guarner J., Bryksin J., Horwath M. C., Arthur C. M., Saakadze N., Smith G. H., Edupuganti S., Scherer E. M., Hellmeister K., Cheng A., Morales J. A., Neish A. S., Stowell S. R., Frank F., Ortlund E., Anderson E. J., Menachery V. D., Rouphael N., Mehta A. K., Stephens D. S., Ahmed R., Roback J. D., Wrammert J., Rapid generation of neutralizing antibody responses in COVID-19 patients. Cell Rep. Med. 1, 100040 (2020). 10.1016/j.xcrm.2020.100040
- Rydyznski Moderbacher C., Ramirez S. I., Dan J. M., Grifoni A., Hastie K. M., Weiskopf D., Belanger S., Abbott R. K., Kim C., Choi J., Kato Y., Crotty E. G., Kim C., Rawlings S. A., Mateus J., Tse L. P. V., Frazier A., Baric R., Peters B., Greenbaum J., Ollmann Saphire E., Smith D. M., Sette A., Crotty S., Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 183, 996–1012.e19 (2020). 10.1016/j.cell.2020.09.038
- Zhou R., To K. K.-W., Wong Y.-C., Liu L., Zhou B., Li X., Huang H., Mo Y., Luk T.-Y., Lau T. T.-K., Yeung P., Chan W.-M., Wu A. K.-L., Lung K.-C., Tsang O. T.-Y., Leung W.-S., Hung I. F.-N., Yuen K.-Y., Chen Z., Acute SARS-CoV-2 infection impairs dendritic cell and T cell responses. Immunity 53, 864–877.e5 (2020). 10.1016/j.immuni.2020.07.026
- Liao M., Liu Y., Yuan J., Wen Y., Xu G., Zhao J., Cheng L., Li J., Wang X., Wang F., Liu L., Amit I., Zhang S., Zhang Z., Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med. 26, 842–844 (2020). 10.1038/s41591-020-0901-9
- Laing A. G., Lorenc A., Del Molino Del Barrio I., Das A., Fish M., Monin L., Muñoz-Ruiz M., McKenzie D. R., Hayday T. S., Francos-Quijorna I., Kamdar S., Joseph M., Davies D., Davis R., Jennings A., Zlatareva I., Vantourout P., Wu Y., Sofra V., Cano F., Greco M., Theodoridis E., Freedman J. D., Gee S., Chan J. N. E., Ryan S., Bugallo-Blanco E., Peterson P., Kisand K., Haljasmägi L., Chadli L., Moingeon P., Martinez L., Merrick B., Bisnauthsing K., Brooks K., Ibrahim M. A. A., Mason J., Lopez Gomez F., Babalola K., Abdul-Jawad S., Cason J., Mant C., Seow J., Graham C., Doores K. J., Di Rosa F., Edgeworth J., Shankar-Hari M., Hayday A. C., A dynamic COVID-19 immune signature includes associations with poor prognosis. Nat. Med. 26, 1623–1635 (2020). 10.1038/s41591-020-1038-6
- Blanco-Melo D., Nilsson-Payant B. E., Liu W.-C., Uhl S., Hoagland D., Møller R., Jordan T. X., Oishi K., Panis M., Sachs D., Wang T. T., Schwartz R. E., Lim J. K., Albrecht R. A., tenOever B. R., Imbalanced Host Response to SARS-CoV-2 Drives Development of COVID-19. Cell 181, 1036–1045.e9 (2020). 10.1016/j.cell.2020.04.026
- Arunachalam P. S., Wimmers F., Mok C. K. P., Perera R. A. P. M., Scott M., Hagan T., Sigal N., Feng Y., Bristow L., Tak-Yin Tsang O., Wagh D., Coller J., Pellegrini K. L., Kazmin D., Alaaeddine G., Leung W. S., Chan J. M. C., Chik T. S. H., Choi C. Y. C., Huerta C., Paine McCullough M., Lv H., Anderson E., Edupuganti S., Upadhyay A. A., Bosinger S. E., Maecker H. T., Khatri P., Rouphael N., Peiris M., Pulendran B., Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans. Science 369, 1210–1220 (2020). 10.1126/science.abc6261
- Bastard P., Rosen L. B., Zhang Q., Michailidis E., Hoffmann H.-H., Zhang Y., Dorgham K., Philippot Q., Rosain J., Béziat V., Manry J., Shaw E., Haljasmägi L., Peterson P., Lorenzo L., Bizien L., Trouillet-Assant S., Dobbs K., de Jesus A. A., Belot A., Kallaste A., Catherinot E., Tandjaoui-Lambiotte Y., Le Pen J., Kerner G., Bigio B., Seeleuthner Y., Yang R., Bolze A., Spaan A. N., Delmonte O. M., Abers M. S., Aiuti A., Casari G., Lampasona V., Piemonti L., Ciceri F., Bilguvar K., Lifton R. P., Vasse M., Smadja D. M., Migaud M., Hadjadj J., Terrier B., Duffy D., Quintana-Murci L., van de Beek D., Roussel L., Vinh D. C., Tangye S. G., Haerynck F., Dalmau D., Martinez-Picado J., Brodin P., Nussenzweig M. C., Boisson-Dupuis S., Rodríguez-Gallego C., Vogt G., Mogensen T. H., Oler A. J., Gu J., Burbelo P. D., Cohen J. I., Biondi A., Bettini L. R., D’Angio M., Bonfanti P., Rossignol P., Mayaux J., Rieux-Laucat F., Husebye E. S., Fusco F., Ursini M. V., Imberti L., Sottini A., Paghera S., Quiros-Roldan E., Rossi C., Castagnoli R., Montagna D., Licari A., Marseglia G. L., Duval X., Ghosn J., Tsang J. S., Goldbach-Mansky R., Kisand K., Lionakis M. S., Puel A., Zhang S. Y., Holland S. M., Gorochov G., Jouanguy E., Rice C. M., Cobat A., Notarangelo L. D., Abel L., Su H. C., Casanova J. L.; HGID Lab; NIAID-USUHS Immune Response to COVID Group; COVID Clinicians; COVID-STORM Clinicians; Imagine COVID Group; French COVID Cohort Study Group; Milieu Intérieur Consortium; CoV-Contact Cohort; Amsterdam UMC Covid-19 Biobank; COVID Human Genetic Effort , Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science 370, eabd4585 (2020). 10.1126/science.abd4585
- Zhang Q., Bastard P., Liu Z., Le Pen J., Moncada-Velez M., Chen J., Ogishi M., Sabli I. K. D., Hodeib S., Korol C., Rosain J., Bilguvar K., Ye J., Bolze A., Bigio B., Yang R., Arias A. A., Zhou Q., Zhang Y., Onodi F., Korniotis S., Karpf L., Philippot Q., Chbihi M., Bonnet-Madin L., Dorgham K., Smith N., Schneider W. M., Razooky B. S., Hoffmann H.-H., Michailidis E., Moens L., Han J. E., Lorenzo L., Bizien L., Meade P., Neehus A.-L., Ugurbil A. C., Corneau A., Kerner G., Zhang P., Rapaport F., Seeleuthner Y., Manry J., Masson C., Schmitt Y., Schlüter A., Le Voyer T., Khan T., Li J., Fellay J., Roussel L., Shahrooei M., Alosaimi M. F., Mansouri D., Al-Saud H., Al-Mulla F., Almourfi F., Al-Muhsen S. Z., Alsohime F., Al Turki S., Hasanato R., van de Beek D., Biondi A., Bettini L. R., D’Angio’ M., Bonfanti P., Imberti L., Sottini A., Paghera S., Quiros-Roldan E., Rossi C., Oler A. J., Tompkins M. F., Alba C., Vandernoot I., Goffard J.-C., Smits G., Migeotte I., Haerynck F., Soler-Palacin P., Martin-Nalda A., Colobran R., Morange P.-E., Keles S., Çölkesen F., Ozcelik T., Yasar K. K., Senoglu S., Karabela Ş. N., Rodríguez-Gallego C., Novelli G., Hraiech S., Tandjaoui-Lambiotte Y., Duval X., Laouénan C., Snow A. L., Dalgard C. L., Milner J. D., Vinh D. C., Mogensen T. H., Marr N., Spaan A. N., Boisson B., Boisson-Dupuis S., Bustamante J., Puel A., Ciancanelli M. J., Meyts I., Maniatis T., Soumelis V., Amara A., Nussenzweig M., García-Sastre A., Krammer F., Pujol A., Duffy D., Lifton R. P., Zhang S. Y., Gorochov G., Béziat V., Jouanguy E., Sancho-Shimizu V., Rice C. M., Abel L., Notarangelo L. D., Cobat A., Su H. C., Casanova J. L.; COVID-STORM Clinicians; COVID Clinicians; Imagine COVID Group; French COVID Cohort Study Group; CoV-Contact Cohort; Amsterdam UMC Covid-19 Biobank; COVID Human Genetic Effort; NIAID-USUHS/TAGC COVID Immunity Group , Inborn errors of type I IFN immunity in patients with life-threatening COVID-19. Science 370, eabd4570 (2020). 10.1126/science.abd4570
- Del Valle D. M., Kim-Schulze S., Huang H.-H., Beckmann N. D., Nirenberg S., Wang B., Lavin Y., Swartz T. H., Madduri D., Stock A., Marron T. U., Xie H., Patel M., Tuballes K., Van Oekelen O., Rahman A., Kovatch P., Aberg J. A., Schadt E., Jagannath S., Mazumdar M., Charney A. W., Firpo-Betancourt A., Mendu D. R., Jhang J., Reich D., Sigel K., Cordon-Cardo C., Feldmann M., Parekh S., Merad M., Gnjatic S., An inflammatory cytokine signature predicts COVID-19 severity and survival. Nat. Med. 26, 1636–1643 (2020). 10.1038/s41591-020-1051-9
- Kuri-Cervantes L., Pampena M. B., Meng W., Rosenfeld A. M., Ittner C. A. G., Weisman A. R., Agyekum R. S., Mathew D., Baxter A. E., Vella L. A., Kuthuru O., Apostolidis S. A., Bershaw L., Dougherty J., Greenplate A. R., Pattekar A., Kim J., Han N., Gouma S., Weirick M. E., Arevalo C. P., Bolton M. J., Goodwin E. C., Anderson E. M., Hensley S. E., Jones T. K., Mangalmurti N. S., Luning Prak E. T., Wherry E. J., Meyer N. J., Betts M. R., Comprehensive mapping of immune perturbations associated with severe COVID-19. Sci. Immunol. 5, eabd7114 (2020). 10.1126/sciimmunol.abd7114
- Li S., Jiang L., Li X., Lin F., Wang Y., Li B., Jiang T., An W., Liu S., Liu H., Xu P., Zhao L., Zhang L., Mu J., Wang H., Kang J., Li Y., Huang L., Zhu C., Zhao S., Lu J., Ji J., Zhao J., Clinical and pathological investigation of patients with severe COVID-19. JCI Insight 5, (2020). 10.1172/jci.insight.138070
- Radermecker C., Detrembleur N., Guiot J., Cavalier E., Henket M., d’Emal C., Vanwinge C., Cataldo D., Oury C., Delvenne P., Marichal T., Neutrophil extracellular traps infiltrate the lung airway, interstitial, and vascular compartments in severe COVID-19. J. Exp. Med. 217, e20201012 (2020). 10.1084/jem.20201012
- Schurink B., Roos E., Radonic T., Barbe E., Bouman C. S. C., de Boer H. H., de Bree G. J., Bulle E. B., Aronica E. M., Florquin S., Fronczek J., Heunks L. M. A., de Jong M. D., Guo L., du Long R., Lutter R., Molenaar P. C. G., Neefjes-Borst E. A., Niessen H. W. M., van Noesel C. J. M., Roelofs J. J. T. H., Snijder E. J., Soer E. C., Verheij J., Vlaar A. P. J., Vos W., van der Wel N. N., van der Wal A. C., van der Valk P., Bugiani M., Viral presence and immunopathology in patients with lethal COVID-19: A prospective autopsy cohort study. Lancet Microbe 1, e290–e299 (2020). 10.1016/S2666-5247(20)30144-0
- Aid M., Busman-Sahay K., Vidal S. J., Maliga Z., Bondoc S., Starke C., Terry M., Jacobson C. A., Wrijil L., Ducat S., Brook O. R., Miller A. D., Porto M., Pellegrini K. L., Pino M., Hoang T. N., Chandrashekar A., Patel S., Stephenson K., Bosinger S. E., Andersen H., Lewis M. G., Hecht J. L., Sorger P. K., Martinot A. J., Estes J. D., Barouch D. H., Vascular Disease and Thrombosis in SARS-CoV-2-Infected Rhesus Macaques. Cell 183, 1354–1366.e13 (2020). 10.1016/j.cell.2020.10.005
- Baumgarth N., Nikolich-Žugich J., Lee F. E.-H., Bhattacharya D., Antibody Responses to SARS-CoV-2: Let’s Stick to Known Knowns. J. Immunol. 205, 2342–2350 (2020). 10.4049/jimmunol.2000839
- Wajnberg A., Amanat F., Firpo A., Altman D. R., Bailey M. J., Mansour M., McMahon M., Meade P., Mendu D. R., Muellers K., Stadlbauer D., Stone K., Strohmeier S., Simon V., Aberg J., Reich D. L., Krammer F., Cordon-Cardo C., Robust neutralizing antibodies to SARS-CoV-2 infection persist for months. Science 370, 1227–1230 (2020). 10.1126/science.abd7728
- Sariol A., Perlman S., Lessons for COVID-19 immunity from other coronavirus infections. Immunity 53, 248–263 (2020). 10.1016/j.immuni.2020.07.005
- Subbarao K., SARS-CoV-2: A New Song Recalls an Old Melody. Cell Host Microbe 27, 692–694 (2020). 10.1016/j.chom.2020.04.019
- Deng W., Bao L., Liu J., Xiao C., Liu J., Xue J., Lv Q., Qi F., Gao H., Yu P., Xu Y., Qu Y., Li F., Xiang Z., Yu H., Gong S., Liu M., Wang G., Wang S., Song Z., Liu Y., Zhao W., Han Y., Zhao L., Liu X., Wei Q., Qin C., Primary exposure to SARS-CoV-2 protects against reinfection in rhesus macaques. Science 369, 818–823 (2020). 10.1126/science.abc5343
- Gao Q., Bao L., Mao H., Wang L., Xu K., Yang M., Li Y., Zhu L., Wang N., Lv Z., Gao H., Ge X., Kan B., Hu Y., Liu J., Cai F., Jiang D., Yin Y., Qin C., Li J., Gong X., Lou X., Shi W., Wu D., Zhang H., Zhu L., Deng W., Li Y., Lu J., Li C., Wang X., Yin W., Zhang Y., Qin C., Development of an inactivated vaccine candidate for SARS-CoV-2. Science 369, 77–81 (2020). 10.1126/science.abc1932
- Chandrashekar A., Liu J., Martinot A. J., McMahan K., Mercado N. B., Peter L., Tostanoski L. H., Yu J., Maliga Z., Nekorchuk M., Busman-Sahay K., Terry M., Wrijil L. M., Ducat S., Martinez D. R., Atyeo C., Fischinger S., Burke J. S., Slein M. D., Pessaint L., Van Ry A., Greenhouse J., Taylor T., Blade K., Cook A., Finneyfrock B., Brown R., Teow E., Velasco J., Zahn R., Wegmann F., Abbink P., Bondzie E. A., Dagotto G., Gebre M. S., He X., Jacob-Dolan C., Kordana N., Li Z., Lifton M. A., Mahrokhian S. H., Maxfield L. F., Nityanandam R., Nkolola J. P., Schmidt A. G., Miller A. D., Baric R. S., Alter G., Sorger P. K., Estes J. D., Andersen H., Lewis M. G., Barouch D. H., SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science 369, 812–817 (2020). 10.1126/science.abc4776
- Zost S. J., Gilchuk P., Case J. B., Binshtein E., Chen R. E., Nkolola J. P., Schäfer A., Reidy J. X., Trivette A., Nargi R. S., Sutton R. E., Suryadevara N., Martinez D. R., Williamson L. E., Chen E. C., Jones T., Day S., Myers L., Hassan A. O., Kafai N. M., Winkler E. S., Fox J. M., Shrihari S., Mueller B. K., Meiler J., Chandrashekar A., Mercado N. B., Steinhardt J. J., Ren K., Loo Y.-M., Kallewaard N. L., McCune B. T., Keeler S. P., Holtzman M. J., Barouch D. H., Gralinski L. E., Baric R. S., Thackray L. B., Diamond M. S., Carnahan R. H., Crowe J. E. Jr., Potently neutralizing and protective human antibodies against SARS-CoV-2. Nature 584, 443–449 (2020). 10.1038/s41586-020-2548-6
- Rogers T. F., Zhao F., Huang D., Beutler N., Burns A., He W. T., Limbo O., Smith C., Song G., Woehl J., Yang L., Abbott R. K., Callaghan S., Garcia E., Hurtado J., Parren M., Peng L., Ramirez S., Ricketts J., Ricciardi M. J., Rawlings S. A., Wu N. C., Yuan M., Smith D. M., Nemazee D., Teijaro J. R., Voss J. E., Wilson I. A., Andrabi R., Briney B., Landais E., Sok D., Jardine J. G., Burton D. R., Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model. Science 369, 956–963 (2020). 10.1126/science.abc7520
- Baum A., Ajithdoss D., Copin R., Zhou A., Lanza K., Negron N., Ni M., Wei Y., Mohammadi K., Musser B., Atwal G. S., Oyejide A., Goez-Gazi Y., Dutton J., Clemmons E., Staples H. M., Bartley C., Klaffke B., Alfson K., Gazi M., Gonzalez O., Dick E. Jr., Carrion R. Jr., Pessaint L., Porto M., Cook A., Brown R., Ali V., Greenhouse J., Taylor T., Andersen H., Lewis M. G., Stahl N., Murphy A. J., Yancopoulos G. D., Kyratsous C. A., REGN-COV2 antibodies prevent and treat SARS-CoV-2 infection in rhesus macaques and hamsters. Science 370, 1110–1115 (2020). 10.1126/science.abe2402
- Weinreich D. M., Sivapalasingam S., Norton T., Ali S., Gao H., Bhore R., Musser B. J., Soo Y., Rofail D., Im J., Perry C., Pan C., Hosain R., Mahmood A., Davis J. D., Turner K. C., Hooper A. T., Hamilton J. D., Baum A., Kyratsous C. A., Kim Y., Cook A., Kampman W., Kohli A., Sachdeva Y., Graber X., Kowal B., DiCioccio T., Stahl N., Lipsich L., Braunstein N., Herman G., Yancopoulos G. D.; Trial Investigators , REGN-COV2, a Neutralizing Antibody Cocktail, in Outpatients with Covid-19. N. Engl. J. Med. NEJMoa2035002 (2020). 10.1056/NEJMoa2035002
- Lilly announces proof of concept data for neutralizing antibody LY-CoV555 in the COVID-19 outpatient setting | Eli Lilly and Company; .
- Altmann D. M., Boyton R. J., SARS-CoV-2 T cell immunity: Specificity, function, durability, and role in protection. Sci. Immunol. 5, eabd6160 (2020). 10.1126/sciimmunol.abd6160
- Van Damme P., Van Herck K., A review of the long-term protection after hepatitis A and B vaccination. Travel Med. Infect. Dis. 5, 79–84 (2007). 10.1016/j.tmaid.2006.04.004
- Rosado M. M., Scarsella M., Pandolfi E., Cascioli S., Giorda E., Chionne P., Madonne E., Gesualdo F., Romano M., Ausiello C. M., Rapicetta M., Zanetti A. R., Tozzi A., Carsetti R., Switched memory B cells maintain specific memory independently of serum antibodies: The hepatitis B example. Eur. J. Immunol. 41, 1800–1808 (2011). 10.1002/eji.201041187
- Zhou F., Yu T., Du R., Fan G., Liu Y., Liu Z., Xiang J., Wang Y., Song B., Gu X., Guan L., Wei Y., Li H., Wu X., Xu J., Tu S., Zhang Y., Chen H., Cao B., Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 395, 1054–1062 (2020). 10.1016/S0140-6736(20)30566-3
- Orenstein W. A., Ahmed R., Simply put: Vaccination saves lives. Proc. Natl. Acad. Sci. U.S.A. 114, 4031–4033 (2017). 10.1073/pnas.1704507114
- Piot P., Larson H. J., O’Brien K. L., N’kengasong J., Ng E., Sow S., Kampmann B., Immunization: Vital progress, unfinished agenda. Nature 575, 119–129 (2019). 10.1038/s41586-019-1656-7
- S. Plotkin, W. Orenstein, P. Offit, Plotkin’s Vaccines (Elsevier, ed. 7, 2018).
- Sallusto F., Lanzavecchia A., Araki K., Ahmed R., From vaccines to memory and back. Immunity 33, 451–463 (2010). 10.1016/j.immuni.2010.10.008
- Crotty S., Ahmed R., Immunological memory in humans. Semin. Immunol. 16, 197–203 (2004). 10.1016/j.smim.2004.02.008
- Weisel F., Shlomchik M., Memory B Cells of Mice and Humans. Annu. Rev. Immunol. 35, 255–284 (2017). 10.1146/annurev-immunol-041015-055531
- Kissler S. M., Tedijanto C., Goldstein E., Grad Y. H., Lipsitch M., Projecting the transmission dynamics of SARS-CoV-2 through the postpandemic period. Science 368, 860–868 (2020). 10.1126/science.abb5793
- Saad-Roy C. M., Wagner C. E., Baker R. E., Morris S. E., Farrar J., Graham A. L., Levin S. A., Mina M. J., Metcalf C. J. E., Grenfell B. T., Immune life history, vaccination, and the dynamics of SARS-CoV-2 over the next 5 years. Science 370, 811–818 (2020). 10.1126/science.abd7343
- Long Q.-X., Tang X.-J., Shi Q.-L., Li Q., Deng H.-J., Yuan J., Hu J.-L., Xu W., Zhang Y., Lv F.-J., Su K., Zhang F., Gong J., Wu B., Liu X.-M., Li J.-J., Qiu J.-F., Chen J., Huang A.-L., Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections. Nat. Med. 26, 1200–1204 (2020). 10.1038/s41591-020-0965-6
- Gudbjartsson D. F., Norddahl G. L., Melsted P., Gunnarsdottir K., Holm H., Eythorsson E., Arnthorsson A. O., Helgason D., Bjarnadottir K., Ingvarsson R. F., Thorsteinsdottir B., Kristjansdottir S., Birgisdottir K., Kristinsdottir A. M., Sigurdsson M. I., Arnadottir G. A., Ivarsdottir E. V., Andresdottir M., Jonsson F., Agustsdottir A. B., Berglund J., Eiriksdottir B., Fridriksdottir R., Gardarsdottir E. E., Gottfredsson M., Gretarsdottir O. S., Gudmundsdottir S., Gudmundsson K. R., Gunnarsdottir T. R., Gylfason A., Helgason A., Jensson B. O., Jonasdottir A., Jonsson H., Kristjansson T., Kristinsson K. G., Magnusdottir D. N., Magnusson O. T., Olafsdottir L. B., Rognvaldsson S., le Roux L., Sigmundsdottir G., Sigurdsson A., Sveinbjornsson G., Sveinsdottir K. E., Sveinsdottir M., Thorarensen E. A., Thorbjornsson B., Thordardottir M., Saemundsdottir J., Kristjansson S. H., Josefsdottir K. S., Masson G., Georgsson G., Kristjansson M., Moller A., Palsson R., Gudnason T., Thorsteinsdottir U., Jonsdottir I., Sulem P., Stefansson K., Humoral Immune Response to SARS-CoV-2 in Iceland. N. Engl. J. Med. 383, 1724–1734 (2020). 10.1056/NEJMoa2026116
- Wajnberg A., Amanat F., Firpo A., Altman D. R., Bailey M. J., Mansour M., McMahon M., Meade P., Mendu D. R., Muellers K., Stadlbauer D., Stone K., Strohmeier S., Simon V., Aberg J., Reich D. L., Krammer F., Cordon-Cardo C., Robust neutralizing antibodies to SARS-CoV-2 infection persist for months. Science 370, 1227–1230 (2020). 10.1126/science.abd7728
- Piccoli L., Park Y.-J., Tortorici M. A., Czudnochowski N., Walls A. C., Beltramello M., Silacci-Fregni C., Pinto D., Rosen L. E., Bowen J. E., Acton O. J., Jaconi S., Guarino B., Minola A., Zatta F., Sprugasci N., Bassi J., Peter A., De Marco A., Nix J. C., Mele F., Jovic S., Rodriguez B. F., Gupta S. V., Jin F., Piumatti G., Lo Presti G., Pellanda A. F., Biggiogero M., Tarkowski M., Pizzuto M. S., Cameroni E., Havenar-Daughton C., Smithey M., Hong D., Lepori V., Albanese E., Ceschi A., Bernasconi E., Elzi L., Ferrari P., Garzoni C., Riva A., Snell G., Sallusto F., Fink K., Virgin H. W., Lanzavecchia A., Corti D., Veesler D., Mapping neutralizing and immunodominant sites on the SARS-CoV-2 spike receptor-binding domain by structure-guided high-resolution serology. Cell 183, 1024–1042.e21 (2020). 10.1016/j.cell.2020.09.037
- Robbiani D. F., Gaebler C., Muecksch F., Lorenzi J. C. C., Wang Z., Cho A., Agudelo M., Barnes C. O., Gazumyan A., Finkin S., Hägglöf T., Oliveira T. Y., Viant C., Hurley A., Hoffmann H.-H., Millard K. G., Kost R. G., Cipolla M., Gordon K., Bianchini F., Chen S. T., Ramos V., Patel R., Dizon J., Shimeliovich I., Mendoza P., Hartweger H., Nogueira L., Pack M., Horowitz J., Schmidt F., Weisblum Y., Michailidis E., Ashbrook A. W., Waltari E., Pak J. E., Huey-Tubman K. E., Koranda N., Hoffman P. R., West A. P. Jr., Rice C. M., Hatziioannou T., Bjorkman P. J., Bieniasz P. D., Caskey M., Nussenzweig M. C., Convergent antibody responses to SARS-CoV-2 in convalescent individuals. Nature 584, 437–442 (2020). 10.1038/s41586-020-2456-9
- Yu J., Tostanoski L. H., Peter L., Mercado N. B., McMahan K., Mahrokhian S. H., Nkolola J. P., Liu J., Li Z., Chandrashekar A., Martinez D. R., Loos C., Atyeo C., Fischinger S., Burke J. S., Slein M. D., Chen Y., Zuiani A., Lelis F. J. N., Travers M., Habibi S., Pessaint L., Van Ry A., Blade K., Brown R., Cook A., Finneyfrock B., Dodson A., Teow E., Velasco J., Zahn R., Wegmann F., Bondzie E. A., Dagotto G., Gebre M. S., He X., Jacob-Dolan C., Kirilova M., Kordana N., Lin Z., Maxfield L. F., Nampanya F., Nityanandam R., Ventura J. D., Wan H., Cai Y., Chen B., Schmidt A. G., Wesemann D. R., Baric R. S., Alter G., Andersen H., Lewis M. G., Barouch D. H., DNA vaccine protection against SARS-CoV-2 in rhesus macaques. Science 369, 806–811 (2020). 10.1126/science.abc6284
- Isho B., Abe K. T., Zuo M., Jamal A. J., Rathod B., Wang J. H., Li Z., Chao G., Rojas O. L., Bang Y. M., Pu A., Christie-Holmes N., Gervais C., Ceccarelli D., Samavarchi-Tehrani P., Guvenc F., Budylowski P., Li A., Paterson A., Yue F. Y., Marin L. M., Caldwell L., Wrana J. L., Colwill K., Sicheri F., Mubareka S., Gray-Owen S. D., Drews S. J., Siqueira W. L., Barrios-Rodiles M., Ostrowski M., Rini J. M., Durocher Y., McGeer A. J., Gommerman J. L., Gingras A.-C., Persistence of serum and saliva antibody responses to SARS-CoV-2 spike antigens in COVID-19 patients. Sci. Immunol. 5, eabe5511 (2020). 10.1126/sciimmunol.abe5511
- Rodda L. B., Netland J., Shehata L., Pruner K. B., Morawski P. A., Thouvenel C. D., Takehara K. K., Eggenberger J., Hemann E. A., Waterman H. R., Fahning M. L., Chen Y., Hale M., Rathe J., Stokes C., Wrenn S., Fiala B., Carter L., Hamerman J. A., King N. P., Gale M. Jr., Campbell D. J., Rawlings D. J., Pepper M., Functional SARS-CoV-2-specific immune memory persists after mild COVID-19. Cell S0092-8674(20)31565-8 (2020). 10.1016/j.cell.2020.11.029
- Davis C. W., Jackson K. J. L., McElroy A. K., Halfmann P., Huang J., Chennareddy C., Piper A. E., Leung Y., Albariño C. G., Crozier I., Ellebedy A. H., Sidney J., Sette A., Yu T., Nielsen S. C. A., Goff A. J., Spiropoulou C. F., Saphire E. O., Cavet G., Kawaoka Y., Mehta A. K., Glass P. J., Boyd S. D., Ahmed R., Longitudinal Analysis of the Human B Cell Response to Ebola Virus Infection. Cell 177, 1566–1582.e17 (2019). 10.1016/j.cell.2019.04.036
- Wec A. Z., Haslwanter D., Abdiche Y. N., Shehata L., Pedreño-Lopez N., Moyer C. L., Bornholdt Z. A., Lilov A., Nett J. H., Jangra R. K., Brown M., Watkins D. I., Ahlm C., Forsell M. N., Rey F. A., Barba-Spaeth G., Chandran K., Walker L. M., Longitudinal dynamics of the human B cell response to the yellow fever 17D vaccine. Proc. Natl. Acad. Sci. U.S.A. 117, 6675–6685 (2020). 10.1073/pnas.1921388117
- Kotturi M. F., Peters B., Buendia-Laysa F. Jr., Sidney J., Oseroff C., Botten J., Grey H., Buchmeier M. J., Sette A., The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: Uncovering new tricks for an old virus. J. Virol. 81, 4928–4940 (2007). 10.1128/JVI.02632-06
- Neidleman J., Luo X., Frouard J., Xie G., Gill G., Stein E. S., McGregor M., Ma T., George A. F., Kosters A., Greene W. C., Vasquez J., Ghosn E., Lee S., Roan N. R., SARS-CoV-2-specific T cells exhibit phenotypic features of helper function, lack of terminal differentiation, and high proliferation potential. Cell Rep. Med. 1, 100081 (2020). 10.1016/j.xcrm.2020.100081
- Sridhar S., Begom S., Bermingham A., Hoschler K., Adamson W., Carman W., Bean T., Barclay W., Deeks J. J., Lalvani A., Cellular immune correlates of protection against symptomatic pandemic influenza. Nat. Med. 19, 1305–1312 (2013). 10.1038/nm.3350
- Akondy R. S., Fitch M., Edupuganti S., Yang S., Kissick H. T., Li K. W., Youngblood B. A., Abdelsamed H. A., McGuire D. J., Cohen K. W., Alexe G., Nagar S., McCausland M. M., Gupta S., Tata P., Haining W. N., McElrath M. J., Zhang D., Hu B., Greenleaf W. J., Goronzy J. J., Mulligan M. J., Hellerstein M., Ahmed R., Origin and differentiation of human memory CD8 T cells after vaccination. Nature 552, 362–367 (2017). 10.1038/nature24633
- Crotty S., T Follicular Helper Cell Biology: A Decade of Discovery and Diseases. Immunity 50, 1132–1148 (2019). 10.1016/j.immuni.2019.04.011
- Juno J. A., Tan H.-X., Lee W. S., Reynaldi A., Kelly H. G., Wragg K., Esterbauer R., Kent H. E., Batten C. J., Mordant F. L., Gherardin N. A., Pymm P., Dietrich M. H., Scott N. E., Tham W.-H., Godfrey D. I., Subbarao K., Davenport M. P., Kent S. J., Wheatley A. K., Humoral and circulating follicular helper T cell responses in recovered patients with COVID-19. Nat. Med. 26, 1428–1434 (2020). 10.1038/s41591-020-0995-0
- A. T. Tan, M. Linster, C. W. Tan, N. L. Bert, W. N. Chia, K. Kunasegaran, Y. Zhuang, C. Y. L. Tham, A. Chia, G. J. Smith, B. Young, S. Kalimuddin, J. G. H. Low, D. Lye, L.-F. Wang, A. Bertoletti, Early induction of SARS-CoV-2 specific T cells associates with rapid viral clearance and mild disease in COVID-19 patients. bioRxiv 2020.10.15.341958 [Preprint]. 16 October 2020. .10.1101/2020.10.15.341958
- Gaebler C., Wang Z., Lorenzi J. C. C., Muecksch F., Finkin S., Tokuyama M., Ladinsky M., Cho A., Jankovic M., Schaefer-Babajew D., Oliveira T. Y., Cipolla M., Viant C., Barnes C. O., Hurley A., Turroja M., Gordon K., Millard K. G., Ramos V., Schmidt F., Weisblum Y., Jha D., Tankelevich M., Yee J., Shimeliovich I., Robbiani D. F., Zhao Z., Gazumyan A., Hatziioannou T., Bjorkman P. J., Mehandru S., Bieniasz P. D., Caskey M., Nussenzweig M. C., Evolution of Antibody Immunity to SARS-CoV-2. bioRxiv 2020.11.03.367391 (2020). 10.1101/2020.11.03.367391
- Crotty S., Felgner P., Davies H., Glidewell J., Villarreal L., Ahmed R., Cutting edge: Long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171, 4969–4973 (2003). 10.4049/jimmunol.171.10.4969
- Yu X., Tsibane T., McGraw P. A., House F. S., Keefer C. J., Hicar M. D., Tumpey T. M., Pappas C., Perrone L. A., Martinez O., Stevens J., Wilson I. A., Aguilar P. V., Altschuler E. L., Basler C. F., Crowe J. E. Jr., Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455, 532–536 (2008). 10.1038/nature07231
- J. Zuo, A. Dowell, H. Pearce, K. Verma, H. Long, J. Begum, F. Aiano, Z. Amin-Chowdhury, B. Hallis, L. Stapley, R. Borrow, E. Linley, S. Ahmad, B. Parker, A. Horsley, G. Amirthalingam, K. Brown, M. Ramsay, S. Ladhani, P. Moss, Robust SARS-CoV-2-specific T-cell immunity is maintained at 6 months following primary infection. bioRxiv 2020.11.01.362319 [Preprint]. .10.1101/2020.11.01.362319
- Hammarlund E., Lewis M. W., Hansen S. G., Strelow L. I., Nelson J. A., Sexton G. J., Hanifin J. M., Slifka M. K., Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9, 1131–1137 (2003). 10.1038/nm917
- Le Bert N., Tan A. T., Kunasegaran K., Tham C. Y. L., Hafezi M., Chia A., Chng M. H. Y., Lin M., Tan N., Linster M., Chia W. N., Chen M. I.-C., Wang L.-F., Ooi E. E., Kalimuddin S., Tambyah P. A., Low J. G.-H., Tan Y.-J., Bertoletti A., SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature 584, 457–462 (2020). 10.1038/s41586-020-2550-z
- Mercado N. B., Zahn R., Wegmann F., Loos C., Chandrashekar A., Yu J., Liu J., Peter L., McMahan K., Tostanoski L. H., He X., Martinez D. R., Rutten L., Bos R., van Manen D., Vellinga J., Custers J., Langedijk J. P., Kwaks T., Bakkers M. J. G., Zuijdgeest D., Rosendahl Huber S. K., Atyeo C., Fischinger S., Burke J. S., Feldman J., Hauser B. M., Caradonna T. M., Bondzie E. A., Dagotto G., Gebre M. S., Hoffman E., Jacob-Dolan C., Kirilova M., Li Z., Lin Z., Mahrokhian S. H., Maxfield L. F., Nampanya F., Nityanandam R., Nkolola J. P., Patel S., Ventura J. D., Verrington K., Wan H., Pessaint L., Van Ry A., Blade K., Strasbaugh A., Cabus M., Brown R., Cook A., Zouantchangadou S., Teow E., Andersen H., Lewis M. G., Cai Y., Chen B., Schmidt A. G., Reeves R. K., Baric R. S., Lauffenburger D. A., Alter G., Stoffels P., Mammen M., Van Hoof J., Schuitemaker H., Barouch D. H., Single-shot Ad26 vaccine protects against SARS-CoV-2 in rhesus macaques. Nature 586, 583–588 (2020). 10.1038/s41586-020-2607-z
- Corbett K. S., Flynn B., Foulds K. E., Francica J. R., Boyoglu-Barnum S., Werner A. P., Flach B., O’Connell S., Bock K. W., Minai M., Nagata B. M., Andersen H., Martinez D. R., Noe A. T., Douek N., Donaldson M. M., Nji N. N., Alvarado G. S., Edwards D. K., Flebbe D. R., Lamb E., Doria-Rose N. A., Lin B. C., Louder M. K., O’Dell S., Schmidt S. D., Phung E., Chang L. A., Yap C., Todd J. M., Pessaint L., Van Ry A., Browne S., Greenhouse J., Putman-Taylor T., Strasbaugh A., Campbell T.-A., Cook A., Dodson A., Steingrebe K., Shi W., Zhang Y., Abiona O. M., Wang L., Pegu A., Yang E. S., Leung K., Zhou T., Teng I.-T., Widge A., Gordon I., Novik L., Gillespie R. A., Loomis R. J., Moliva J. I., Stewart-Jones G., Himansu S., Kong W.-P., Nason M. C., Morabito K. M., Ruckwardt T. J., Ledgerwood J. E., Gaudinski M. R., Kwong P. D., Mascola J. R., Carfi A., Lewis M. G., Baric R. S., McDermott A., Moore I. N., Sullivan N. J., Roederer M., Seder R. A., Graham B. S., Evaluation of the mRNA-1273 Vaccine against SARS-CoV-2 in Nonhuman Primates. N. Engl. J. Med. 383, 1544–1555 (2020). 10.1056/NEJMoa2024671
- Corey L., Mascola J. R., Fauci A. S., Collins F. S., A strategic approach to COVID-19 vaccine R&D. Science 368, 948–950 (2020). 10.1126/science.abc5312
- Zhao J., Zhao J., Mangalam A. K., Channappanavar R., Fett C., Meyerholz D. K., Agnihothram S., Baric R. S., David C. S., Perlman S., Airway Memory CD4+ T Cells Mediate Protective Immunity against Emerging Respiratory Coronaviruses. Immunity 44, 1379–1391 (2016). 10.1016/j.immuni.2016.05.006
- Purtha W. E., Tedder T. F., Johnson S., Bhattacharya D., Diamond M. S., Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J. Exp. Med. 208, 2599–2606 (2011). 10.1084/jem.20110740
- Masopust D., Soerens A. G., Tissue-Resident T Cells and Other Resident Leukocytes. Annu. Rev. Immunol. 37, 521–546 (2019). 10.1146/annurev-immunol-042617-053214
- Whittle H. C., Aaby P., Samb B., Jensen H., Bennett J., Simondon F., Effect of subclinical infection on maintaining immunity against measles in vaccinated children in West Africa. Lancet 353, 98–102 (1999). 10.1016/S0140-6736(98)02364-2
- Plotkin S. A., Vaccines: Correlates of vaccine-induced immunity. Clin. Infect. Dis. 47, 401–409 (2008). 10.1086/589862
- Burdin N., Handy L. K., Plotkin S. A., What Is Wrong with Pertussis Vaccine Immunity? The Problem of Waning Effectiveness of Pertussis Vaccines. Cold Spring Harb. Perspect. Biol. 9, a029454 (2017). 10.1101/cshperspect.a029454
- van Doremalen N., Lambe T., Spencer A., Belij-Rammerstorfer S., Purushotham J. N., Port J. R., Avanzato V. A., Bushmaker T., Flaxman A., Ulaszewska M., Feldmann F., Allen E. R., Sharpe H., Schulz J., Holbrook M., Okumura A., Meade-White K., Pérez-Pérez L., Edwards N. J., Wright D., Bissett C., Gilbride C., Williamson B. N., Rosenke R., Long D., Ishwarbhai A., Kailath R., Rose L., Morris S., Powers C., Lovaglio J., Hanley P. W., Scott D., Saturday G., de Wit E., Gilbert S. C., Munster V. J., ChAdOx1 nCoV-19 vaccine prevents SARS-CoV-2 pneumonia in rhesus macaques. Nature 586, 578–582 (2020). 10.1038/s41586-020-2608-y
- Tillett R. L., Sevinsky J. R., Hartley P. D., Kerwin H., Crawford N., Gorzalski A., Laverdure C., Verma S. C., Rossetto C. C., Jackson D., Farrell M. J., Van Hooser S., Pandori M., Genomic evidence for reinfection with SARS-CoV-2: A case study. Lancet Infect. Dis. 21, 52–58 (2021). 10.1016/S1473-3099(20)30764-7
- To K. K.-W., Hung I. F.-N., Ip J. D., Chu A. W.-H., Chan W.-M., Tam A. R., Fong C. H.-Y., Yuan S., Tsoi H.-W., Ng A. C.-K., Lee L. L.-Y., Wan P., Tso E., To W.-K., Tsang D., Chan K.-H., Huang J.-D., Kok K.-H., Cheng V. C.-C., Yuen K.-Y., COVID-19 re-infection by a phylogenetically distinct SARS-coronavirus-2 strain confirmed by whole genome sequencing. Clin. Infect. Dis. ciaa1275 (2020). 10.1093/cid/ciaa1275
- D. Wyllie, R. Mulchandani, H. E. Jones, S. Taylor-Phillips, T. Brooks, A. Charlett, A. E. Ades, EDSAB-Home Investigators, A. Makin, I. Oliver, P. Moore, J. Boyes, A. Hormis, N. Todd, I. Reckless, SARS-CoV-2 responsive T cell numbers are associated with protection from COVID-19: A prospective cohort study in keyworkers. medRxiv 2020.11.02.20222778 [Preprint]. 4 November 2020. .10.1101/2020.11.02.20222778
- S. F. Lumley, D. O’Donnell, N. E. Stoesser, P. C. Matthews, A. Howarth, S. B. Hatch, B. D. Marsden, S. Cox, T. James, F. Warren, L. J. Peck, T. G. Ritter, Z. de Toledo, L. Warren, D. Axten, R. J. Cornall, E. Y. Jones, D. I. Stuart, G. Screaton, D. Ebner, S. Hoosdally, M. Chand, O. U. H. S. T. Group, D. W. Crook, A.-M. O’Donnell, C. P. Conlon, K. B. Pouwels, A. S. Walker, T. E. Peto, S. Hopkins, T. M. Walker, K. Jeffery, D. W. Eyre, Antibodies to SARS-CoV-2 are associated with protection against reinfection. medRxiv 2020.11.18.20234369 [Preprint]. 19 November 2020. .10.1101/2020.11.18.20234369
- Beigel J. H., Tomashek K. M., Dodd L. E., Mehta A. K., Zingman B. S., Kalil A. C., Hohmann E., Chu H. Y., Luetkemeyer A., Kline S., Lopez de Castilla D., Finberg R. W., Dierberg K., Tapson V., Hsieh L., Patterson T. F., Paredes R., Sweeney D. A., Short W. R., Touloumi G., Lye D. C., Ohmagari N., Oh M.-D., Ruiz-Palacios G. M., Benfield T., Fätkenheuer G., Kortepeter M. G., Atmar R. L., Creech C. B., Lundgren J., Babiker A. G., Pett S., Neaton J. D., Burgess T. H., Bonnett T., Green M., Makowski M., Osinusi A., Nayak S., Lane H. C.; ACTT-1 Study Group Members , Remdesivir for the Treatment of Covid-19 - Final Report. N. Engl. J. Med. 383, 1813–1826 (2020). 10.1056/NEJMoa2007764
- Wrapp D., Wang N., Corbett K. S., Goldsmith J. A., Hsieh C.-L., Abiona O., Graham B. S., McLellan J. S., Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 367, 1260–1263 (2020). 10.1126/science.abb2507
- Amanat F., Stadlbauer D., Strohmeier S., Nguyen T. H. O., Chromikova V., McMahon M., Jiang K., Arunkumar G. A., Jurczyszak D., Polanco J., Bermudez-Gonzalez M., Kleiner G., Aydillo T., Miorin L., Fierer D. S., Lugo L. A., Kojic E. M., Stoever J., Liu S. T. H., Cunningham-Rundles C., Felgner P. L., Moran T., García-Sastre A., Caplivski D., Cheng A. C., Kedzierska K., Vapalahti O., Hepojoki J. M., Simon V., Krammer F., A serological assay to detect SARS-CoV-2 seroconversion in humans. Nat. Med. 26, 1033–1036 (2020). 10.1038/s41591-020-0913-5
- Mestecky J., Hamilton R. G., Magnusson C. G. M., Jefferis R., Vaerman J. P., Goodall M., de Lange G. G., Moro I., Aucouturier P., Radl J., Cambiaso C., Silvain C., Preud’homme J. L., Kusama K., Carlone G. M., Biewenga J., Kobayashi K., Skvaril F., Reimer C. B., Evaluation of monoclonal antibodies with specificity for human IgA, IgA subclasses and allotypes and secretory component. Results of an IUIS/WHO collaborative study. J. Immunol. Methods 193, 103–148 (1996). 10.1016/0022-1759(95)00289-8
- GraphPad, GraphPad Prism 8 Curve Fitting Guide (2020); .
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