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Article ; Online: Local memory CD4 T cell niches in respiratory viral infection.

Pruner, Kurt B / Pepper, Marion

2021 Volume 218, Issue 8

Abstract: Respiratory viral infections present a major threat to global health and prosperity. Over the past century, several have developed into crippling pandemics, including the SARS-CoV-2 virus. Although the generation of neutralizing serum antibodies in ... ...

Abstract	Respiratory viral infections present a major threat to global health and prosperity. Over the past century, several have developed into crippling pandemics, including the SARS-CoV-2 virus. Although the generation of neutralizing serum antibodies in response to natural immunity and vaccination are considered to be hallmarks of viral immune protection, antibodies from long-lived plasma cells are subject to immune escape from heterologous clades of zoonotic, recombined, or mutated viruses. Local immunity in the lung can be generated through resident memory immune subsets that rapidly respond to secondary infection and protect from heterologous infection. Although many immune cells are required to achieve the phenomenon of resident memory, herein we highlight the pleiotropic functions of CD4 tissue resident memory T cells in the lung and discuss the implications of resident memory for vaccine design.
MeSH term(s)	Animals ; CD4-Positive T-Lymphocytes/immunology ; Humans ; Immunologic Memory ; Respiratory Tract Infections/immunology ; Respiratory Tract Infections/virology ; SARS-CoV-2/physiology ; Species Specificity ; Vaccination
Language	English
Publishing date	2021-06-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20201733
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Article ; Online: Allergen exposure functionally alters influenza-specific CD4+ Th1 memory cells in the lung.

Rüterbusch, Mikel J / Hondowicz, Brian D / Takehara, Kennidy K / Pruner, Kurt B / Griffith, Thomas S / Pepper, Marion

The Journal of experimental medicine

2023 Volume 220, Issue 11

Abstract: CD4+ lung-resident memory T cells (TRM) generated in response to influenza infection confer effective protection against subsequent viral exposures. Whether these cells can be altered by environmental antigens and cytokines released during heterologous, ... ...

Abstract	CD4+ lung-resident memory T cells (TRM) generated in response to influenza infection confer effective protection against subsequent viral exposures. Whether these cells can be altered by environmental antigens and cytokines released during heterologous, antigen-independent immune responses is currently unclear. We therefore investigated how influenza-specific CD4+ Th1 TRM in the lung are impacted by a subsequent Th2-inducing respiratory house dust mite (HDM) exposure. Although naïve influenza-specific CD4+ T cells in the lymph nodes do not respond to HDM, influenza-specific CD4+ TRM in the lungs do respond to a subsequent allergen exposure by decreasing expression of the transcription factor T-bet. This functional alteration is associated with decreased IFN-γ production upon restimulation and improved disease outcomes following heterosubtypic influenza challenge. Further investigation revealed that ST2 signaling in CD4+ T cells during allergic challenge is necessary to induce these changes in lung-resident influenza-specific CD4+ TRM. Thus, heterologous antigen exposure or ST2-signaling can drive persistent changes in CD4+ Th1 TRM populations and impact protection upon reinfection.
MeSH term(s)	Animals ; Humans ; Influenza, Human ; Interleukin-1 Receptor-Like 1 Protein ; CD4-Positive T-Lymphocytes ; Th1 Cells ; Pyroglyphidae ; Allergens
Chemical Substances	Interleukin-1 Receptor-Like 1 Protein ; Allergens
Language	English
Publishing date	2023-09-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20230112
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Article ; Online: In Vivo CD4

Ruterbusch, Mikel / Pruner, Kurt B / Shehata, Laila / Pepper, Marion

Annual review of immunology

2020 Volume 38, Page(s) 705–725

Abstract: The discovery of ... ...

Abstract	The discovery of CD4
MeSH term(s)	Animals ; B-Lymphocytes/immunology ; B-Lymphocytes/metabolism ; CD4-Positive T-Lymphocytes/cytology ; CD4-Positive T-Lymphocytes/immunology ; CD4-Positive T-Lymphocytes/metabolism ; Cell Differentiation/genetics ; Cell Differentiation/immunology ; Cytokines/metabolism ; Humans ; Lymphocyte Activation/immunology ; Receptors, Antigen, T-Cell/metabolism ; T-Lymphocyte Subsets/immunology ; T-Lymphocyte Subsets/metabolism ; Th1 Cells/immunology ; Th1 Cells/metabolism ; Th2 Cells/immunology ; Th2 Cells/metabolism
Chemical Substances	Cytokines ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2020-05-18
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	604953-9
ISSN	1545-3278 ; 0732-0582
ISSN (online)	1545-3278
ISSN	0732-0582
DOI	10.1146/annurev-immunol-103019-085803
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Article ; Online: Imprinted SARS-CoV-2-specific memory lymphocytes define hybrid immunity.

Rodda, Lauren B / Morawski, Peter A / Pruner, Kurt B / Fahning, Mitchell L / Howard, Christian A / Franko, Nicholas / Logue, Jennifer / Eggenberger, Julie / Stokes, Caleb / Golez, Inah / Hale, Malika / Gale, Michael / Chu, Helen Y / Campbell, Daniel J / Pepper, Marion

Cell

2022 Volume 185, Issue 9, Page(s) 1588–1601.e14

Abstract: ... previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant ...

Abstract	Immune memory is tailored by cues that lymphocytes perceive during priming. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic created a situation in which nascent memory could be tracked through additional antigen exposures. Both SARS-CoV-2 infection and vaccination induce multifaceted, functional immune memory, but together, they engender improved protection from disease, termed hybrid immunity. We therefore investigated how vaccine-induced memory is shaped by previous infection. We found that following vaccination, previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant-neutralizing antibodies and a distinct population of IFN-γ and IL-10-expressing memory SARS-CoV-2 spike-specific CD4
MeSH term(s)	Antibodies, Neutralizing ; Antibodies, Viral ; COVID-19/immunology ; COVID-19 Vaccines/immunology ; Humans ; Immunity, Humoral ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus ; T-Lymphocytes
Chemical Substances	Antibodies, Neutralizing ; Antibodies, Viral ; COVID-19 Vaccines ; Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2022-03-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2022.03.018
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Article: Imprinted SARS-CoV-2-specific memory lymphocytes define hybrid immunity

Rodda, Lauren B. / Morawski, Peter A. / Pruner, Kurt B. / Fahning, Mitchell L. / Howard, Christian A. / Franko, Nicholas / Logue, Jennifer / Eggenberger, Julie / Stokes, Caleb / Golez, Inah / Hale, Malika / Gale, Michael / Chu, Helen Y. / Campbell, Daniel J. / Pepper, Marion

Cell. 2022 Mar. 14,

2022

Abstract: ... previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant ...

Abstract	Immune memory is tailored by cues that lymphocytes perceive during priming. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic created a situation in which nascent memory could be tracked through additional antigen exposures. Both SARS-CoV-2 infection and vaccination induce multifaceted, functional immune memory, but together they engender improved protection from disease, termed hybrid immunity. We therefore investigated how vaccine-induced memory is shaped by previous infection. We found that following vaccination, previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant-neutralizing antibodies and a distinct population of IFN-γ and IL-10-expressing memory SARS-CoV-2 spike-specific CD4⁺ T cells than previously naive individuals. While additional vaccination could increase humoral memory in previously naive individuals, it did not recapitulate the distinct CD4⁺ T cell cytokine profile observed in previously infected subjects. Thus, imprinted features of SARS-CoV-2-specific memory lymphocytes define hybrid immunity.
Keywords	Severe acute respiratory syndrome coronavirus 2 ; antigens ; cytokines ; immunologic memory ; memory ; pandemic ; vaccination
Language	English
Dates of publication	2022-0314
Publishing place	Elsevier Inc.
Document type	Article
Note	Pre-press version
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2022.03.018
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Article: A Mixed-chimerism Protocol Utilizing Thymoglobulin and Belatacept Did Not Induce Lung Allograft Tolerance, Despite Previous Success in Renal Allotransplantation.

Sommer, Wiebke / O, Jane M / Pruner, Kurt B / Dehnadi, Abbas / Ha Huh, Kyu / Robinson, Kortney A / Hanekamp, Isabel / Rosales, Ivy / Bean, Alison S / Paster, Josh / Oura, Tetsu / Neal Smith, Rex / Colvin, Robert / Benichou, Gilles / Kawai, Tatsuo / Madsen, Joren C / Allan, James S

Transplantation direct

2021 Volume 7, Issue 6, Page(s) e705

Abstract: Background: In kidney transplantation, long-term allograft acceptance in cynomolgus macaques was achieved using a mixed-chimerism protocol based on the clinically available reagents, rabbit anti-thymocyte globulin (ATG), and belatacept. Here, we have ... ...

Abstract	Background: In kidney transplantation, long-term allograft acceptance in cynomolgus macaques was achieved using a mixed-chimerism protocol based on the clinically available reagents, rabbit anti-thymocyte globulin (ATG), and belatacept. Here, we have tested the same protocol in cynomolgus macaques transplanted with fully allogeneic lung grafts. Methods: Five cynomolgus macaques underwent left orthotopic lung transplantation. Initial immunosuppression included equine ATG and anti-IL6RmAb induction, followed by triple-drug immunosuppression for 4 mo. Post-transplant, a nonmyeloablative conditioning regimen was applied, including total body and thymic irradiation. Rabbit ATG, belatacept, anti-IL6RmAb, and donor bone marrow transplantation (DBMT) were given, in addition to a 28-d course of cyclosporine. All immunosuppressant drugs were stopped on day 29 after DBMT. Results: One monkey rejected its lung before DBMT due to AMR, after developing donor-specific antibodies. Two monkeys developed fatal post-transplant lymphoproliferative disorder, and both monkeys had signs of cellular rejection in their allografts upon autopsy. The remaining 2 monkeys showed severe cellular rejection on days 42 and 70 post-DBMT. Cytokine analysis suggested higher levels of pro-inflammatory markers in the lung transplant cohort, as compared to kidney recipients. Conclusion: Although the clinically applicable protocol showed success in kidney transplantation, the study did not show long-term survival in a lung transplant model, highlighting the organ-specific differences in tolerance induction.
Language	English
Publishing date	2021-05-25
Publishing country	United States
Document type	Journal Article
ISSN	2373-8731
ISSN	2373-8731
DOI	10.1097/TXD.0000000000001150
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Article ; Online: Imprinted SARS-CoV-2-specific memory lymphocytes define hybrid immunity

medRxiv

Abstract: ... previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant ...

Abstract	Immune memory is tailored by cues that lymphocytes perceive during priming. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic created a situation in which nascent memory could be tracked through additional antigen exposures. Both SARS-CoV-2 infection and vaccination induce multifaceted, functional immune memory, but together they engender improved protection from disease, termed hybrid immunity. We therefore investigated how vaccine-induced memory is shaped by previous infection. We found that following vaccination, previously infected individuals generated more SARS-CoV-2 RBD-specific memory B cells and variant-neutralizing antibodies and a distinct population of IFN- and IL-10-expressing memory SARS-CoV-2 spike-specific CD4+ T cells than previously naive individuals. While additional vaccination could increase humoral memory, it did not recapitulate the distinct CD4+ T cell cytokine profile in previously naive individuals. Thus, imprinted features of SARS-CoV-2-specific memory lymphocytes define hybrid immunity.
Keywords	covid19
Language	English
Publishing date	2022-01-13
Publisher	Cold Spring Harbor Laboratory Press
Document type	Article ; Online
DOI	10.1101/2022.01.12.22269192
Database	COVID19

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Article: Functional SARS-CoV-2-specific immune memory persists after mild COVID-19.

medRxiv : the preprint server for health sciences

2020

Abstract: ... specific memory B and T cells that not only persisted, but in some cases increased numerically over three ... re-encounter, while memory B cells expressed receptors capable of neutralizing virus when expressed ...

Abstract	The recently emerged SARS-CoV-2 virus is currently causing a global pandemic and cases continue to rise. The majority of infected individuals experience mildly symptomatic coronavirus disease 2019 (COVID-19), but it is unknown whether this can induce persistent immune memory that might contribute to herd immunity. Thus, we performed a longitudinal assessment of individuals recovered from mildly symptomatic COVID-19 to determine if they develop and sustain immunological memory against the virus. We found that recovered individuals developed SARS-CoV-2-specific IgG antibody and neutralizing plasma, as well as virus-specific memory B and T cells that not only persisted, but in some cases increased numerically over three months following symptom onset. Furthermore, the SARS-CoV-2-specific memory lymphocytes exhibited characteristics associated with potent antiviral immunity: memory T cells secreted IFN-γ and expanded upon antigen re-encounter, while memory B cells expressed receptors capable of neutralizing virus when expressed as antibodies. These findings demonstrate that mild COVID-19 elicits memory lymphocytes that persist and display functional hallmarks associated with antiviral protective immunity.
Keywords	covid19
Language	English
Publishing date	2020-08-15
Publishing country	United States
Document type	Preprint
DOI	10.1101/2020.08.11.20171843
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Article: Functional SARS-CoV-2-specific immune memory persists after mild COVID-19.

Research square

2020

Abstract	The recently emerged SARS-CoV-2 virus is currently causing a global pandemic and cases continue to rise. The majority of infected individuals experience mildly symptomatic coronavirus disease 2019 (COVID-19), but it is unknown whether this can induce persistent immune memory that might contribute to herd immunity. Thus, we performed a longitudinal assessment of individuals recovered from mildly symptomatic COVID-19 to determine if they develop and sustain immunological memory against the virus. We found that recovered individuals developed SARS-CoV-2-specific IgG antibody and neutralizing plasma, as well as virus-specific memory B and T cells that not only persisted, but in some cases increased numerically over three months following symptom onset. Furthermore, the SARS-CoV-2-specific memory lymphocytes exhibited characteristics associated with potent antiviral immunity: memory T cells secreted IFN-γ and expanded upon antigen re-encounter, while memory B cells expressed receptors capable of neutralizing virus when expressed as antibodies. These findings demonstrate that mild COVID-19 elicits memory lymphocytes that persist and display functional hallmarks associated with antiviral protective immunity.
Keywords	covid19
Language	English
Publishing date	2020-08-13
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-57112/v1
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Article ; Online: Functional SARS-CoV-2-Specific Immune Memory Persists after Mild COVID-19.

Rodda, Lauren B / Netland, Jason / Shehata, Laila / Pruner, Kurt B / Morawski, Peter A / Thouvenel, Christopher D / Takehara, Kennidy K / Eggenberger, Julie / Hemann, Emily A / Waterman, Hayley R / Fahning, Mitchell L / Chen, Yu / Hale, Malika / Rathe, Jennifer / Stokes, Caleb / Wrenn, Samuel / Fiala, Brooke / Carter, Lauren / Hamerman, Jessica A /

King, Neil P / Gale, Michael / Campbell, Daniel J / Rawlings, David J / Pepper, Marion

Cell

2020 Volume 184, Issue 1, Page(s) 169–183.e17

Abstract: ... individuals developed SARS-CoV-2-specific immunoglobulin (IgG) antibodies, neutralizing plasma, and memory B ... specific IgG memory B cells increased over time. Additionally, SARS-CoV-2-specific memory lymphocytes ... expanded upon antigen re-encounter, whereas memory B cells expressed receptors capable of neutralizing ...

Abstract	The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus is causing a global pandemic, and cases continue to rise. Most infected individuals experience mildly symptomatic coronavirus disease 2019 (COVID-19), but it is unknown whether this can induce persistent immune memory that could contribute to immunity. We performed a longitudinal assessment of individuals recovered from mild COVID-19 to determine whether they develop and sustain multifaceted SARS-CoV-2-specific immunological memory. Recovered individuals developed SARS-CoV-2-specific immunoglobulin (IgG) antibodies, neutralizing plasma, and memory B and memory T cells that persisted for at least 3 months. Our data further reveal that SARS-CoV-2-specific IgG memory B cells increased over time. Additionally, SARS-CoV-2-specific memory lymphocytes exhibited characteristics associated with potent antiviral function: memory T cells secreted cytokines and expanded upon antigen re-encounter, whereas memory B cells expressed receptors capable of neutralizing virus when expressed as monoclonal antibodies. Therefore, mild COVID-19 elicits memory lymphocytes that persist and display functional hallmarks of antiviral immunity.
MeSH term(s)	Adult ; Antibodies, Neutralizing/blood ; Antibodies, Neutralizing/immunology ; B-Lymphocytes/immunology ; COVID-19/blood ; COVID-19/immunology ; COVID-19/physiopathology ; Female ; Humans ; Immunoglobulin G/blood ; Immunoglobulin G/immunology ; Immunologic Memory ; Male ; Middle Aged ; SARS-CoV-2/chemistry ; SARS-CoV-2/physiology ; Severity of Illness Index ; Spike Glycoprotein, Coronavirus/metabolism ; T-Lymphocytes/immunology
Chemical Substances	Antibodies, Neutralizing ; Immunoglobulin G ; Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2020-11-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2020.11.029
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