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Article ; Online: NK cell education: Physiological and pathological influences.

Rascle, Philippe / Woolley, Griffin / Jost, Stephanie / Manickam, Cordelia / Reeves, R Keith

2023 Volume 14, Page(s) 1087155

Abstract: Natural killer (NK) cells represent a critical defense against viral infections and cancers. NK cells require integration of activating and inhibitory NK cell receptors to detect target cells and the balance of these NK cell inputs defines the global NK ... ...

Abstract	Natural killer (NK) cells represent a critical defense against viral infections and cancers. NK cells require integration of activating and inhibitory NK cell receptors to detect target cells and the balance of these NK cell inputs defines the global NK cell response. The sensitivity of the response is largely defined by interactions between self-major histocompatibility complex class I (MHC-I) molecules and specific inhibitory NK cell receptors, so-called NK cell education. Thus, NK cell education is a crucial process to generate tuned effector NK cell responses in different diseases. In this review, we discuss the relationship between NK cell education and physiologic factors (type of self-MHC-I, self-MHC-I allelic variants, variant of the self-MHC-I-binding peptides, cytokine effects and inhibitory KIR expression) underlying NK cell education profiles (effector function or metabolism). Additionally, we describe the broad-spectrum of effector educated NK cell functions on different pathologies (such as HIV-1, CMV and tumors, among others).
MeSH term(s)	Receptors, KIR/metabolism ; Killer Cells, Natural ; Receptors, Natural Killer Cell/metabolism ; Histocompatibility Antigens Class I/metabolism
Chemical Substances	Receptors, KIR ; Receptors, Natural Killer Cell ; Histocompatibility Antigens Class I
Language	English
Publishing date	2023-01-20
Publishing country	Switzerland
Document type	Journal Article ; Review ; 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.2023.1087155
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Article ; Online: FcαRI (CD89) is upregulated on subsets of mucosal and circulating NK cells and regulates IgA-class specific signaling and functions.

Kroll, Kyle W / Hueber, Brady / Balachandran, Harikrishnan / Afifi, Ameera / Manickam, Cordelia / Nettere, Danielle / Pollara, Justin / Hudson, Andrew / Woolley, Griffin / Ndhlovu, Lishomwa C / Reeves, R Keith

Mucosal immunology

2024

Abstract: Immunoglobulin A (IgA) is the predominant mucosal antibody class with both anti- and pro-inflammatory ... ...

Abstract	Immunoglobulin A (IgA) is the predominant mucosal antibody class with both anti- and pro-inflammatory roles
Language	English
Publishing date	2024-04-25
Publishing country	United States
Document type	Journal Article
ZDB-ID	2411370-0
ISSN	1935-3456 ; 1933-0219
ISSN (online)	1935-3456
ISSN	1933-0219
DOI	10.1016/j.mucimm.2024.04.003
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Article ; Online: Natural killer like B cells are a distinct but infrequent innate immune cell subset modulated by SIV infection of rhesus macaques.

Manickam, Cordelia / Upadhyay, Amit A / Woolley, Griffin / Kroll, Kyle W / Terry, Karen / Broedlow, Courtney A / Klatt, Nichole R / Bosinger, Steven E / Reeves, R Keith

PLoS pathogens

2024 Volume 20, Issue 5, Page(s) e1012223

Abstract: Natural killer-like B (NKB) cells are unique innate immune cells expressing both natural killer (NK) and B cell receptors. As first responders to infection, they secrete IL-18 to induce a critical cascade of innate and adaptive immune cell infiltration ... ...

Abstract	Natural killer-like B (NKB) cells are unique innate immune cells expressing both natural killer (NK) and B cell receptors. As first responders to infection, they secrete IL-18 to induce a critical cascade of innate and adaptive immune cell infiltration and activation. However, limited research exists on the role of NKB cells in homeostasis and infection, largely due to incomplete and erroneous evaluations. To fill this knowledge gap, we investigated the expression of signaling and trafficking proteins, and the in situ localization and transcriptome of naïve NKB cells comparied to conventionally-defined NK and B cells, as well as modulations of these cells in SIV infection. Intracellular signaling proteins and trafficking markers were expressed differentially on naïve NKB cells, with high expression of CD62L and Syk, and low expression of CD69, α4β7, FcRg, Zap70, and CD3z, findings which were more similar to B cells than NK cells. CD20+NKG2a/c+ NKB cells were identified in spleen, mesenteric lymph nodes (MLN), colon, jejunum, and liver of naïve rhesus macaques (RM) via tissue imaging, with NKB cell counts concentrated in spleen and MLN. For the first time, single cell RNA sequencing (scRNAseq), including BCR sequencing, of sorted NKB cells confirmed that NKB cells are unique. Transcriptomic analysis of naïve splenic NKB cells by scRNAseq showed that NKB cells undergo somatic hypermutation and express Ig receptors, similar to B cells. While only 15% of sorted NKB cells showed transcript expression of both KLRC1 (NKG2A) and MS4A1 (CD20) genes, only 5% of cells expressed KLRC1, MS4A1, and IgH/IgL transcripts. We observed expanded NKB frequencies in RM gut and buccal mucosa as early as 14 and 35 days post-SIV infection, respectively. Further, mucosal and peripheral NKB cells were associated with colorectal cytokine mileu and oral microbiome changes, respectively. Our studies indicate that NKB cells gated on CD3-CD14-CD20+NKG2A/C+ cells were inclusive of transcriptomically conventional B and NK cells in addition to true NKB cells, confounding accurate phenotyping and frequency recordings that could only be resolved using genomic techniques. Although NKB cells were clearly elevated during SIV infection and associated with inflammatory changes during infection, further interrogation is necessary to acurately identify the true phenotype and significance of NKB cells in infection and inflammation.
Language	English
Publishing date	2024-05-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1012223
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Article ; Online: The Climate Change Burden on Immune Health: Are Persons Living With HIV More at Risk?

Woolley, Griffin / Kroll, Kyle / Hoffman, Kate / Ward, Ashley / Corneli, Amy / Mudrak, Sarah V / Qureshi, M Umar / Okeke, Nwora Lance / Chan, Cliburn / Jones, Akhenaton-Andrew D / Tomaras, Georgia D / Reeves, R Keith

AIDS research and human retroviruses

2024

Abstract: ... ...

Abstract	<no abstract>.
Language	English
Publishing date	2024-05-16
Publishing country	United States
Document type	Journal Article
ZDB-ID	639130-8
ISSN	1931-8405 ; 0889-2229
ISSN (online)	1931-8405
ISSN	0889-2229
DOI	10.1089/AID.2024.0050
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Article ; Online: Intersectional climate justice, health equity, and HIV.

Wilson, Sarah M / Woolley, Griffin / Hawn, Chris / Hoffman, Kate / Jones, Akhenaton-Andrew D / Chan, Cliburn / Mudrak, Sarah V / Qureshi, M Umar / Ward, Ashley / Knippler, Elizabeth T / Okeke, N Lance / Corneli, Amy / Tomaras, Georgia D / Reeves, R Keith

The lancet. HIV

2024 Volume 11, Issue 5, Page(s) e280–e281

MeSH term(s)	Humans ; HIV Infections/epidemiology ; HIV Infections/prevention & control ; Health Equity ; Social Justice ; Global Health
Language	English
Publishing date	2024-04-03
Publishing country	Netherlands
Document type	Journal Article
ISSN	2352-3018
ISSN (online)	2352-3018
DOI	10.1016/S2352-3018(24)00062-6
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Article: Multiplex analysis of cytokines and chemokines in persons aging with or without HIV.

Kroll, Kyle W / Woolley, Griffin / Terry, Karen / Premeaux, Thomas A / Shikuma, Cecilia M / Corley, Michael J / Bowler, Scott / Ndhlovu, Lishomwa C / Reeves, R Keith

bioRxiv : the preprint server for biology

2023

Abstract: People with HIV (PWH) on combined antiretroviral therapy (cART) are living longer lives due to modern cART advances and increased routine medical care. The full landscape of aging with HIV is unclear; given that HIV emerged relatively recently in human ... ...

Abstract	People with HIV (PWH) on combined antiretroviral therapy (cART) are living longer lives due to modern cART advances and increased routine medical care. The full landscape of aging with HIV is unclear; given that HIV emerged relatively recently in human history and initially had a high mortality rate, there has not been a substantially aged population to evaluate. In the present study, we set out to perform high throughput plasma analyte profiling by multiplex analysis, focusing on various T helper (Th)-related cytokines, chemokines, and pro- and anti-inflammatory cytokines. The primary goals being to provide reference ranges of these analytes for aging PWH cohorts, as well as testing the utility of high throughput multiplex plasma assays. The cohort used in this study was comprised of age-matched healthy donors (aged 32.6-73.5), PWH on cART (aged 26.7-60.2), and viremic PWH (aged 27.5-59.4). The patients in each group were then stratified across the age span to examine age-related impacts of these plasma biomarkers. Our results largely indicate feasibility of plasma analyte monitoring by multiplex and demonstrate a high degree of person-to-person variability regardless of age and HIV status. Nonetheless, we find multiple associations with age, duration of known infection, and viral load, all of which appear to be driven by either prolonged HIV disease progression or long-term use of cART.
Language	English
Publishing date	2023-02-02
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.30.526135
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Article ; Online: Multiplex interrogation of the NK cell signalome reveals global downregulation of CD16 signaling during lentivirus infection through an IL-18/ADAM17-dependent mechanism.

Sugawara, Sho / Hueber, Brady / Woolley, Griffin / Terry, Karen / Kroll, Kyle / Manickam, Cordelia / Ram, Daniel R / Ndhlovu, Lishomwa C / Goepfert, Paul / Jost, Stephanie / Reeves, R Keith

PLoS pathogens

2023 Volume 19, Issue 9, Page(s) e1011629

Abstract: Despite their importance, natural killer (NK) cell responses are frequently dysfunctional during human immunodeficiency virus-1 (HIV-1) and simian immunodeficiency virus (SIV) infections, even irrespective of antiretroviral therapies, with poorly ... ...

Abstract	Despite their importance, natural killer (NK) cell responses are frequently dysfunctional during human immunodeficiency virus-1 (HIV-1) and simian immunodeficiency virus (SIV) infections, even irrespective of antiretroviral therapies, with poorly understood underlying mechanisms. NK cell surface receptor modulation in lentivirus infection has been extensively studied, but a deeper interrogation of complex cell signaling is mostly absent, largely due to the absence of any comprehensive NK cell signaling assay. To fill this knowledge gap, we developed a novel multiplex signaling analysis to broadly assess NK cell signaling. Using this assay, we elucidated that NK cells exhibit global signaling reduction from CD16 both in people living with HIV-1 (PLWH) and SIV-infected rhesus macaques. Intriguingly, antiretroviral treatment did not fully restore diminished CD16 signaling in NK cells from PLWH. As a putative mechanism, we demonstrated that NK cells increased surface ADAM17 expression via elevated plasma IL-18 levels during HIV-1 infection, which in turn reduced surface CD16 downregulation. We also illustrated that CD16 expression and signaling can be restored by ADAM17 perturbation. In summary, our multiplex NK cell signaling analysis delineated unique NK cell signaling perturbations specific to lentiviral infections, resulting in their dysfunction. Our analysis also provides mechanisms that will inform the restoration of dysregulated NK cell functions, offering potential insights for the development of new NK cell-based immunotherapeutics for HIV-1 disease.
MeSH term(s)	Animals ; Humans ; Down-Regulation ; Interleukin-18 ; Macaca mulatta ; Lentivirus Infections ; Killer Cells, Natural ; Signal Transduction ; HIV-1 ; ADAM17 Protein
Chemical Substances	Interleukin-18 ; ADAM17 protein, human (EC 3.4.24.86) ; ADAM17 Protein (EC 3.4.24.86)
Language	English
Publishing date	2023-09-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1011629
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Article ; Online: Multiplex Analysis of Cytokines and Chemokines in Persons Aging With or Without HIV.

Kroll, Kyle W / Woolley, Griffin / Terry, Karen / Premeaux, Thomas A / Shikuma, Cecilia M / Corley, Michael J / Bowler, Scott / Ndhlovu, Lishomwa C / Reeves, R Keith

AIDS research and human retroviruses

2023 Volume 39, Issue 7, Page(s) 367–380

Abstract: People with HIV (PWH) on combination antiretroviral therapy (cART) are living longer lives due to modern cART advances and increased routine medical care. The full landscape of aging with HIV is unclear; given that HIV emerged relatively recently in ... ...

Abstract	People with HIV (PWH) on combination antiretroviral therapy (cART) are living longer lives due to modern cART advances and increased routine medical care. The full landscape of aging with HIV is unclear; given that HIV emerged relatively recently in human history and initially had a high mortality rate, there has not been a substantially aged population to evaluate. In this study, we set out to perform high-throughput plasma analyte profiling by multiplex analysis, focusing on various T helper (Th)-related cytokines, chemokines, and proinflammatory and anti-inflammatory cytokines. The primary goals being to provide reference ranges of these analytes for aging PWH cohorts, as well as testing the utility of high-throughput multiplex plasma assays. The cohort used in this study comprised age-matched healthy donors (32.6-73.5 years of age), PWH on cART (26.7-60.2 years of age), and viremic PWH (27.5-59.4 years of age). The patients in each group were then stratified across the age span to examine age-related impacts of these plasma biomarkers. Our results largely indicate feasibility of plasma analyte monitoring by multiplex and demonstrate a high degree of person-to-person variability regardless of age and HIV status. Nonetheless, we find multiple associations with age, duration of known infection, and viral load, all of which appear to be driven by either prolonged HIV disease progression or long-term use of cART.
MeSH term(s)	Humans ; Aged ; Adult ; Middle Aged ; Cytokines ; HIV Infections/complications ; Chemokines ; Aging ; Biomarkers
Chemical Substances	Cytokines ; Chemokines ; Biomarkers
Language	English
Publishing date	2023-06-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	639130-8
ISSN	1931-8405 ; 0889-2229
ISSN (online)	1931-8405
ISSN	0889-2229
DOI	10.1089/AID.2022.0183
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Article ; Online: Natural Killer Cells Regulate Acute SIV Replication, Dissemination, and Inflammation, but Do Not Impact Independent Transmission Events.

Woolley, Griffin / Mosher, Matthew / Kroll, Kyle / Jones, Rhianna / Hueber, Brady / Sugawara, Sho / Manickam, Cordelia / Terry, Karen / Varner, Valerie / Lifton, Michelle / Ram, Daniel / Fennessey, Christine M / Keele, Brandon F / Reeves, R Keith

Journal of virology

2022 Volume 97, Issue 1, Page(s) e0151922

Abstract: Natural killer (NK) cells are potent effector cells of the innate immune system possessing both cytotoxic and immunoregulatory capabilities, which contribute to their crucial role in controlling human immunodeficiency virus (HIV) and simian ... ...

Abstract	Natural killer (NK) cells are potent effector cells of the innate immune system possessing both cytotoxic and immunoregulatory capabilities, which contribute to their crucial role in controlling human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV) infections. However, despite significant evidence for NK cell modulation of HIV disease, their specific contribution to transmission and control of acute infection remains less clear. To elucidate the contribution of NK cells during acute SIV infection, we performed an acute necropsy study, where rhesus macaques (RM) were subjected to preinfection depletion of systemic NK cells using established methods of IL-15 neutralization, followed by subsequent challenge with barcoded SIVmac239X. Our study showed that depletion was highly effective, resulting in near total ablation of all NK cell subsets in blood, liver, oral, and rectal mucosae, and lymph nodes (LN) that persisted through the duration of the study. Meanwhile, frequencies and phenotypes of T cells remained virtually unchanged, indicating that our method of NK cell depletion had minimal off-target effects. Importantly, NK cell-depleted RM demonstrated an early and sustained 1 to 2 log increase in viremia over controls, but sequence analysis suggested no difference in the number of independent transmission events. Acute bulk, central memory (CM), and CCR5
MeSH term(s)	Animals ; Humans ; CD4-Positive T-Lymphocytes ; CD8-Positive T-Lymphocytes ; HIV Infections ; Killer Cells, Natural/virology ; Macaca mulatta ; Simian Acquired Immunodeficiency Syndrome/immunology ; Simian Acquired Immunodeficiency Syndrome/transmission ; Simian Immunodeficiency Virus ; Viral Load ; Viremia ; Virus Replication
Language	English
Publishing date	2022-12-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.01519-22
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Zs.A 609: Show issues

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Article ; Online: Mucosal-homing natural killer cells are associated with aging in persons living with HIV.

Kroll, Kyle W / Shah, Spandan V / Lucar, Olivier A / Premeaux, Thomas A / Shikuma, Cecilia M / Corley, Michael J / Mosher, Matthew / Woolley, Griffin / Bowler, Scott / Ndhlovu, Lishomwa C / Reeves, R Keith

Cell reports. Medicine

2022 Volume 3, Issue 10, Page(s) 100773

Abstract: Natural killer (NK) cells are critical modulators of HIV transmission and disease. Recent evidence suggests a loss of NK cell cytotoxicity during aging, yet analysis of NK cell biology and aging in people with HIV (PWH) is lacking. Herein, we perform ... ...

Abstract	Natural killer (NK) cells are critical modulators of HIV transmission and disease. Recent evidence suggests a loss of NK cell cytotoxicity during aging, yet analysis of NK cell biology and aging in people with HIV (PWH) is lacking. Herein, we perform comprehensive analyses of people aging with and without HIV to determine age-related NK phenotypic changes. Utilizing high-dimensional flow cytometry, we analyze 30 immune-related proteins on peripheral NK cells from healthy donors, PWH with viral suppression, and viremic PWH. NK cell phenotypes are dynamic across aging but change significantly in HIV and on antiretroviral drug therapy (ART). NK cells in healthy aging show increasing ⍺4β7 and decreasing CCR7 expression and a reverse phenomenon in PWH. These HIV-associated trafficking patterns could be due to NK cell recruitment to HIV reservoir formation in lymphoid tissue or failed mucosal signaling in the HIV-infected gut but appear to be tight delineators of age-related NK cell changes.
MeSH term(s)	Humans ; HIV-1 ; Receptors, CCR7/metabolism ; Killer Cells, Natural/metabolism ; Anti-Retroviral Agents/metabolism ; HIV Infections/drug therapy
Chemical Substances	Receptors, CCR7 ; Anti-Retroviral Agents
Language	English
Publishing date	2022-10-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2666-3791
ISSN (online)	2666-3791
DOI	10.1016/j.xcrm.2022.100773
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