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Article ; Online: Editorial: Adaptive immunity to respiratory pathogens.

Iwanaga, Naoki / Devarajan, Priyadharshini / Shenoy, Anukul T

2023 Volume 14, Page(s) 1174178

MeSH term(s)	Humans ; Adaptive Immunity ; COVID-19
Language	English
Publishing date	2023-03-06
Publishing country	Switzerland
Document type	Editorial ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2023.1174178
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Article: Understanding the Heterogeneous Population of Age-Associated B Cells and Their Contributions to Autoimmunity and Immune Response to Pathogens.

Kugler-Umana, Olivia / Devarajan, Priyadharshini / Swain, Susan L

Critical reviews in immunology

2021 Volume 40, Issue 4, Page(s) 297–309

Abstract: In humans and mice, susceptibility to infections and autoimmunity increases with age due to age-associated changes in innate and adaptive immune responses. Aged innate cells are also less active, leading to decreased naive T- and B-cell responses. Aging ... ...

Abstract	In humans and mice, susceptibility to infections and autoimmunity increases with age due to age-associated changes in innate and adaptive immune responses. Aged innate cells are also less active, leading to decreased naive T- and B-cell responses. Aging innate cells contribute to an overall heightened inflammatory environment. Naive T and B cells undergo cell-intrinsic age-related changes that result in reduced effector and memory responses. However, previously established B- and T-cell memory responses persist with age. One dramatic change is the appearance of a newly recognized population of age-associated B cells (ABCs) that has a unique cluster of differentiation (CD)21-CD23- phenotype. Here, we discuss the discovery and origins of the naive phenotype immunoglobulin (Ig)D+ versus activated CD11c+T-bet+ ABCs, with a focus on protective and pathogenic properties. In humans and mice, antigen-experienced CD11c+T-bet+ ABCs increase with autoimmunity and appear in response to bacterial and viral infections. However, our analyses indicate that CD21-CD23- ABCs include a resting, naive, progenitor ABC population that expresses IgD. Similar to generation of CD11c+T-bet+ ABCs, naive ABC response to pathogens depends on toll-like receptor stimulation, making this a key feature of ABC activation. Here, we put forward a potential developmental map of distinct subsets from putative naive ABCs. We suggest that defining signals that can harness the naive ABC response may contribute to protection against pathogens in the elderly. CD11c+T-bet+ ABCs may be useful targets for therapeutic strategies to counter autoimmunity.
MeSH term(s)	Aged ; Aging ; Animals ; Autoimmunity ; B-Lymphocyte Subsets ; B-Lymphocytes ; CD11c Antigen ; Humans ; Mice
Chemical Substances	CD11c Antigen
Language	English
Publishing date	2021-01-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1353116-5
ISSN	1040-8401
ISSN	1040-8401
DOI	10.1615/CritRevImmunol.2020034934
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Article ; Online: Original Antigenic Sin: Friend or Foe in Developing a Broadly Cross-Reactive Vaccine to Influenza?

Devarajan, Priyadharshini / Swain, Susan L

Cell host & microbe

2019 Volume 25, Issue 3, Page(s) 354–355

Abstract: In this issue of Cell Host & Microbe, two articles (Lee et al., 2019; Henry et al., 2019) find the influenza-specific antibody repertoire in humans becomes static over time and with age, despite repeated exposures. Identified persistent dominant clones ... ...

Abstract	In this issue of Cell Host & Microbe, two articles (Lee et al., 2019; Henry et al., 2019) find the influenza-specific antibody repertoire in humans becomes static over time and with age, despite repeated exposures. Identified persistent dominant clones target conserved viral epitopes, supporting the feasibility of a universal influenza vaccine.
MeSH term(s)	Antibodies, Viral/immunology ; Cross Reactions ; Humans ; Influenza Vaccines/immunology ; Influenza, Human/immunology ; Vaccination
Chemical Substances	Antibodies, Viral ; Influenza Vaccines
Language	English
Publishing date	2019-03-06
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	2278004-X
ISSN	1934-6069 ; 1931-3128
ISSN (online)	1934-6069
ISSN	1931-3128
DOI	10.1016/j.chom.2019.02.009
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Article ; Online: Cytotoxic CD4 development requires CD4 effectors to concurrently recognize local antigen and encounter type I IFN-induced IL-15.

Devarajan, Priyadharshini / Vong, Allen M / Castonguay, Catherine H / Silverstein, Noah J / Kugler-Umana, Olivia / Bautista, Bianca L / Kelly, Karen A / Luban, Jeremy / Swain, Susan L

Cell reports

2023 Volume 42, Issue 10, Page(s) 113182

Abstract: Cytotoxic CD4 T cell effectors (ThCTLs) kill virus-infected major histocompatibility complex (MHC) class ... ...

Abstract	Cytotoxic CD4 T cell effectors (ThCTLs) kill virus-infected major histocompatibility complex (MHC) class II
MeSH term(s)	Interleukin-15 ; CD4-Positive T-Lymphocytes ; Histocompatibility Antigens Class II/metabolism ; T-Lymphocytes, Cytotoxic ; Antigens ; Antineoplastic Agents ; Interferon Type I
Chemical Substances	Interleukin-15 ; Histocompatibility Antigens Class II ; Antigens ; Antineoplastic Agents ; Interferon Type I
Language	English
Publishing date	2023-09-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.113182
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Article ; Online: Cytotoxic CD4 development requires CD4 effectors to concurrently recognize local antigen and encounter type I IFN-induced IL-15.

Devarajan, Priyadharshini / Vong, Allen M / Castonguay, Catherine H / Silverstein, Noah J / Kugler-Umana, Olivia / Bautista, Bianca L / Kelly, Karen A / Luban, Jeremy / Swain, Susan L

Cell reports

2023 Volume 42, Issue 11, Page(s) 113429

Language	English
Publishing date	2023-11-06
Publishing country	United States
Document type	Published Erratum
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.113429
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Article ; Online: CD4 Effector TCR Avidity for Peptide on APC Determines the Level of Memory Generated.

Jones, Michael C / Castonguay, Catherine / Nanaware, Padma P / Weaver, Grant C / Stadinski, Brian / Kugler-Umana, Olivia A / Huseby, Eric S / Stern, Lawrence J / McKinstry, Karl Kai / Strutt, Tara M / Devarajan, Priyadharshini / Swain, Susan L

Journal of immunology (Baltimore, Md. : 1950)

2023 Volume 210, Issue 12, Page(s) 1950–1961

Abstract: Initial TCR affinity for peptide Ag is known to impact the generation of memory; however, its contributions later, when effectors must again recognize Ag at 5-8 d postinfection to become memory, is unclear. We examined whether the effector TCR affinity ... ...

Abstract	Initial TCR affinity for peptide Ag is known to impact the generation of memory; however, its contributions later, when effectors must again recognize Ag at 5-8 d postinfection to become memory, is unclear. We examined whether the effector TCR affinity for peptide at this "effector checkpoint" dictates the extent of memory and degree of protection against rechallenge. We made an influenza A virus nucleoprotein (NP)-specific TCR transgenic mouse strain, FluNP, and generated NP-peptide variants that are presented by MHC class II to bind to the FluNP TCR over a broad range of avidity. To evaluate the impact of avidity in vivo, we primed naive donor FluNP in influenza A virus-infected host mice, purified donor effectors at the checkpoint, and cotransferred them with the range of peptides pulsed on activated APCs into second uninfected hosts. Higher-avidity peptides yielded higher numbers of FluNP memory cells in spleen and most dramatically in lung and draining lymph nodes and induced better protection against lethal influenza infection. Avidity determined memory cell number, not cytokine profile, and already impacted donor cell number within several days of transfer. We previously found that autocrine IL-2 production at the checkpoint prevents default effector apoptosis and supports memory formation. Here, we find that peptide avidity determines the level of IL-2 produced by these effectors and that IL-2Rα expression by the APCs enhances memory formation, suggesting that transpresentation of IL-2 by APCs further amplifies IL-2 availability. Secondary memory generation was also avidity dependent. We propose that this regulatory pathway selects CD4 effectors of highest affinity to progress to memory.
MeSH term(s)	Mice ; Animals ; CD4-Positive T-Lymphocytes/metabolism ; Interleukin-2/metabolism ; Peptides/metabolism ; Mice, Transgenic ; Receptors, Antigen, T-Cell/metabolism ; Immunologic Memory ; Mice, Inbred C57BL
Chemical Substances	Interleukin-2 ; Peptides ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2023-10-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2200337
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Article ; Online: Durable CD4 T-Cell Memory Generation Depends on Persistence of High Levels of Infection at an Effector Checkpoint that Determines Multiple Fates.

Swain, Susan L / Jones, Michael C / Devarajan, Priyadharshini / Xia, Jingya / Dutton, Richard W / Strutt, Tara M / McKinstry, K Kai

Cold Spring Harbor perspectives in biology

2021 Volume 13, Issue 11

Abstract: We have discovered that the determination of CD4 effector and memory fates after infection is regulated not only by initial signals from antigen and pathogen recognition, but also by a second round of such signals at a checkpoint during the effector ... ...

Abstract	We have discovered that the determination of CD4 effector and memory fates after infection is regulated not only by initial signals from antigen and pathogen recognition, but also by a second round of such signals at a checkpoint during the effector response. Signals to effectors determine their subsequent fate, inducing further progression to tissue-restricted follicular helpers, cytotoxic CD4 effectors, and long-lived memory cells. The follicular helpers help the germinal center B-cell responses that give rise to high-affinity long-lived antibody responses and memory B cells that synergize with T-cell memory to provide robust long-lived protection. We postulate that inactivated vaccines do not provide extended signals from antigen and pathogen beyond a few days, and thus elicit ineffective CD4 T- and B-cell effector responses and memory. Defining the mechanisms that underlie effective responses should provide insights necessary to develop vaccine strategies that induce more effective and durable immunity.
MeSH term(s)	Animals ; Antigen Presentation ; CD4-Positive T-Lymphocytes/physiology ; Humans ; Immunologic Memory ; Infections/immunology ; Influenza Vaccines/immunology ; Pathogen-Associated Molecular Pattern Molecules
Chemical Substances	Influenza Vaccines ; Pathogen-Associated Molecular Pattern Molecules
Language	English
Publishing date	2021-11-01
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1943-0264
ISSN (online)	1943-0264
DOI	10.1101/cshperspect.a038182
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Article ; Online: Autoimmune effector memory T cells: the bad and the good.

Devarajan, Priyadharshini / Chen, Zhibin

Immunologic research

2013 Volume 57, Issue 1-3, Page(s) 12–22

Abstract: Immunological memory is a hallmark of adaptive immunity, a defense mechanism endowed to vertebrates during evolution. However, an autoimmune pathogenic role of memory lymphocytes is also emerging with accumulating evidence, despite reasonable skepticism ... ...

Abstract	Immunological memory is a hallmark of adaptive immunity, a defense mechanism endowed to vertebrates during evolution. However, an autoimmune pathogenic role of memory lymphocytes is also emerging with accumulating evidence, despite reasonable skepticism on their existence in a chronic setting of autoimmune damage. It is conceivable that autoimmune memory would be particularly harmful since memory cells would constantly "remember" and attack the body's healthy tissues. It is even more detrimental given the resistance of memory T cells to immunomodulatory therapies. In this review, we focus on self-antigen-reactive CD(+) effector memory T (TEM) cells, surveying the evidence for the role of the T(EM) compartment in autoimmune pathogenesis. We will also discuss the role of T(EM) cells in chronic and acute infectious disease settings and how they compare to their counterparts in autoimmune diseases. With their long-lasting potency, the autoimmune T(EM) cells could also play a critical role in anti-tumor immunity, which may be largely based on their reactivity to self-antigens. Therefore, although autoimmune T(EM) cells are "bad" due to their role in relentless perpetration of tissue damage in autoimmune disease settings, they are unlikely a by-product of industrial development along the modern surge of autoimmune disease prevalence. Rather, they may be a product of evolution for their "good" in clearing damaged host cells in chronic infections and malignant cells in cancer settings.
MeSH term(s)	Animals ; Autoimmune Diseases/genetics ; Autoimmune Diseases/immunology ; Autoimmune Diseases/metabolism ; Autoimmunity ; CTLA-4 Antigen/genetics ; CTLA-4 Antigen/immunology ; Humans ; Immunologic Memory/physiology ; Neoplasms/genetics ; Neoplasms/immunology ; Neoplasms/therapy ; T-Lymphocyte Subsets/immunology ; T-Lymphocyte Subsets/metabolism
Chemical Substances	CTLA-4 Antigen
Language	English
Publishing date	2013-11-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	632857-x
ISSN	1559-0755 ; 0257-277X
ISSN (online)	1559-0755
ISSN	0257-277X
DOI	10.1007/s12026-013-8448-1
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Article ; Online: Strong influenza-induced T

Devarajan, Priyadharshini / Vong, Allen M / Castonguay, Catherine H / Kugler-Umana, Olivia / Bautista, Bianca L / Jones, Michael C / Kelly, Karen A / Xia, Jingya / Swain, Susan L

Proceedings of the National Academy of Sciences of the United States of America

2022 Volume 119, Issue 8

Abstract: While influenza infection induces robust, long-lasting, antibody responses and protection, including the T follicular helper cells ( ... ...

Abstract	While influenza infection induces robust, long-lasting, antibody responses and protection, including the T follicular helper cells (T
MeSH term(s)	Animals ; Antibodies, Viral/immunology ; Antibody Formation/immunology ; Antigens ; B-Lymphocytes/immunology ; CD4-Positive T-Lymphocytes/immunology ; CD4-Positive T-Lymphocytes/metabolism ; Female ; Germinal Center/immunology ; Humans ; Influenza Vaccines/immunology ; Influenza, Human/immunology ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; T Follicular Helper Cells/immunology ; T Follicular Helper Cells/metabolism ; T-Lymphocytes, Helper-Inducer/immunology ; Vaccines, Attenuated/immunology
Chemical Substances	Antibodies, Viral ; Antigens ; Influenza Vaccines ; Vaccines, Attenuated
Language	English
Publishing date	2022-02-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2111064119
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Article ; Online: IgD

Kugler-Umana, Olivia / Zhang, Wenliang / Kuang, Yi / Liang, Jialing / Castonguay, Catherine H / Tonkonogy, Susan L / Marshak-Rothstein, Ann / Devarajan, Priyadharshini / Swain, Susan L

Aging cell

2022 Volume 21, Issue 10, Page(s) e13705

Abstract: Age-associated B cells (ABC) accumulate with age and are associated with autoimmunity and chronic infection. However, their contributions to acute infection in the aged and their developmental pathways are unclear. We find that the response against ... ...

Abstract	Age-associated B cells (ABC) accumulate with age and are associated with autoimmunity and chronic infection. However, their contributions to acute infection in the aged and their developmental pathways are unclear. We find that the response against influenza A virus infection in aged mice is dominated by a Fas
MeSH term(s)	Animals ; Humans ; Mice ; Antibodies, Viral ; Immunoglobulin D ; Immunoglobulin G ; Immunoglobulin M ; Influenza Vaccines ; Influenza, Human ; Toll-Like Receptor 7 ; Toll-Like Receptor 9 ; Vaccines, Inactivated ; B-Lymphocytes ; T-Lymphocytes
Chemical Substances	Antibodies, Viral ; Immunoglobulin D ; Immunoglobulin G ; Immunoglobulin M ; Influenza Vaccines ; Toll-Like Receptor 7 ; Toll-Like Receptor 9 ; Vaccines, Inactivated
Language	English
Publishing date	2022-09-02
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2113083-8
ISSN	1474-9726 ; 1474-9718
ISSN (online)	1474-9726
ISSN	1474-9718
DOI	10.1111/acel.13705
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