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Circulating NK cells establish tissue-residency upon acute infection of skin and mediate accelerated effector responses to secondary infection

ABSTRACT: Natural killer (NK) cells are present in the circulation and can also be found residing in tissues; these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigated whether circulating conventional NK (cNK) cells can develop into long-lived, tissue-resident cells following acute infections. We found that viral and bacterial infections of the skin triggered the recruitment of cNK cells and their differentiation into Tcf1hiCD69hi tissue-resident (trNK) cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK arose from IFN--producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK formation. Upon secondary infection, trNK cells rapidly gained effector function and mediated an accelerated NK cell response. Thus, cNK cells redistribute and permanently position at sites of previous infection via a mechanism promoting tissueresidency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny.

ORGANISM(S): Mus musculus

PROVIDER: GSE242313 | GEO | 2023/12/28

REPOSITORIES: GEO

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Circulating NK cells establish tissue-residency upon acute infection of skin and mediate accelerated effector responses to secondary infection

Project description:Natural killer (NK) cells are present in the circulation and can also be found residing in tissues; these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigated whether circulating conventional NK (cNK) cells can develop into long-lived, tissue-resident cells following acute infections. We found that viral and bacterial infections of the skin triggered the recruitment of cNK cells and their differentiation into Tcf1hiCD69hi tissue-resident (trNK) cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK arose from IFN-g-producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK formation. Upon secondary infection, trNK cells rapidly gained effector function and mediated an accelerated NK cell response. Thus, cNK cells redistribute and permanently position at sites of previous infection via a mechanism promoting tissueresidency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny

2023-12-28 | GSE226756 | GEO

Circulating NK cells establish tissue-residency upon acute infection of skin and mediate accelerated effector responses to secondary infection

Project description:Natural killer (NK) cells are present in the circulation and can also be found residing in tissues; these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigated whether circulating conventional NK (cNK) cells can develop into long-lived, tissue-resident cells following acute infections. We found that viral and bacterial infections of the skin triggered the recruitment of cNK cells and their differentiation into Tcf1hiCD69hi tissue-resident (trNK) cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK arose from IFN--producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK formation. Upon secondary infection, trNK cells rapidly gained effector function and mediated an accelerated NK cell response. Thus, cNK cells redistribute and permanently position at sites of previous infection via a mechanism promoting tissueresidency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny.

2023-12-28 | GSE227801 | GEO

Tissue-Resident Natural Killer (NK) Cells Are Cell Lineages Distinct From Thymic and Conventional Splenic NK Cells (part 1)

Project description:Natural killer (NK) cells belong to the innate immune system where they can control virus infections and developing tumors by cytotoxicity and production of inflammatory cytokines. Most studies of mouse NK cells, however, have focused on conventional NK (cNK) cells found in the spleen. Recently, we described two populations of NK cells within the liver, tissue-resident NK (trNK) cells and those resembling splenic cNK cells. However, the lineage relationship of trNK to cNK cells was unclear because trNK cells display a phenotype associated with immature, developing cNK cells. Moreover, liver trNK cells could be related to thymic NK cells or alternatively, a lineage distinct from both cNK and thymic NK cells. Herein we used detailed transcriptomic, flow cytometric, and functional analysis of mice deficient in several transcription factors to determine that liver trNK cells form a distinct lineage from cNK and thymic NK cells, especially because they do not require NFIL3 (E4BP4), the previously described NK cellspecification factor. Analysis of other tissues indicate the presence of trNK cells in skin and uterus with different transcription factor requirements. Thus, there are at least four distinct lineages of NK cells: cNK, thymic, liver (and skin) trNK, and uterine trNK cells. Liver NK 1.1+CD49+, liver NK 1.1+CD49-, spleen NK 1.1+ CD49- populations of NK cells were sorted with FACS pooling cells from individual mice to end up with ~100k cells for each samples. mRNA was derived from lysates using Invitrogen oligo-dT beads

2014-04-26 | E-GEOD-52043 | biostudies-arrayexpress

Tissue-Resident Natural Killer (NK) Cells Are Cell Lineages Distinct From Thymic and Conventional Splenic NK Cells (part 2)

Project description:Natural killer (NK) cells belong to the innate immune system where they can control virus infections and developing tumors by cytotoxicity and production of inflammatory cytokines. Most studies of mouse NK cells, however, have focused on conventional NK (cNK) cells found in the spleen. Recently, we described two populations of NK cells within the liver, tissue-resident NK (trNK) cells and those resembling splenic cNK cells. However, the lineage relationship of trNK to cNK cells was unclear because trNK cells display a phenotype associated with immature, developing cNK cells. Moreover, liver trNK cells could be related to thymic NK cells or alternatively, a lineage distinct from both cNK and thymic NK cells. Herein we used detailed transcriptomic, flow cytometric, and functional analysis of mice deficient in several transcription factors to determine that liver trNK cells form a distinct lineage from cNK and thymic NK cells, especially because they do not require NFIL3 (E4BP4), the previously described NK cellspecification factor. Analysis of other tissues indicate the presence of trNK cells in skin and uterus with different transcription factor requirements. Thus, there are at least four distinct lineages of NK cells: cNK, thymic, liver (and skin) trNK, and uterine trNK cells. Liver DX5-CD49+, liver DX5+CD49-, spleen DX5+ CD49- populations of NK cells were sorted with FACS pooling cells from individual mice to end up with ~100k cells for each samples. mRNA was derived from lysates using Invitrogen oligo-dT beads

2014-04-26 | E-GEOD-52045 | biostudies-arrayexpress

Tissue-Resident Natural Killer (NK) Cells Are Cell Lineages Distinct From Thymic and Conventional Splenic NK Cells (part 2)

2014-04-26 | GSE52045 | GEO

Tissue-Resident Natural Killer (NK) Cells Are Cell Lineages Distinct From Thymic and Conventional Splenic NK Cells (part 1)

2014-04-26 | GSE52043 | GEO

Activation of tissue-resident NK and conventional NK are fundamentally different as indicated by their particular genesets

Project description:Residential natural killer cells in peripheral tissues (trNK) act as pioneering responders during infectious challenges, and thus have attracted increasing attention recently. However, their discrimination with conventional NK (cNK) cells is still problematical, limiting the further knowledge of this particular NK subgroup. Here, through an integrative transcriptome comparison of the two NK subgroups from different tissues, two genesets are defined to efficiently distinguish them. From these genesets, we have also discovered a fundamental difference of the two NK subgroups in activation. Transcriptomic profiling of trNK and cNK activated in vivo after MCMV infection and in vitro by PMA/ionomycin stimulation further confirms this difference, and reveals a particular role of chromatin landscape in regulating the trNK activation. Additionally, trNK and cNK respectively highly express IL-21R and IL-18R, indicating that their activation is differentially regulated by cytokine milieu. Indeed, IL-21 is particular critical in accessorily promoting trNK activation, while IL-18 mainly facilitates cNK activation. Further, IL-21 is found to direct transcriptome changes in activated trNK using a bunch of bifunctional transcription factors. Together, our study sheds light on the bona fide difference between trNK and cNK, which will enrich our understanding of their distinct functionalities during immune responses.

2023-01-30 | GSE223677 | GEO

Hobit and Blimp1 instruct a universal transcriptional program of tissue-residency in lymphocytes

Project description:Tissue-resident memory T cells (Trm) are non-circulating memory T cells that localize to portals of pathogen entry such as the skin, gut and lung where they provide efficient early protection against reinfection. Trm are characterized by a molecular profile that actively prevents egress from peripheral sites including the constitutive expression of the lectin CD69 and down-regulation of the chemokine receptor (CCR)7 and sphingosine-1-phosphate receptor 1 (S1PR1). This program is partially mediated by down-regulation of the transcription factor KLF2; however, to date no transcriptional regulator specific to Trm has been identified. Here we show that the Blimp1 related transcription factor Hobit is specifically upregulated in Trm and together with Blimp1, mediates the development and maintenance of Trm in various tissues including skin, gut, liver and kidney. Importantly, we found that the Hobit/Blimp1 transcriptional module is also required for other tissue-resident lymphocytes including Natural Killer T (NKT) cells and liver tissue-resident NK cells (trNK). We show that these populations share a universal transcriptional program with Trm instructed by Hobit and Blimp1 that includes the repression of CCR7, S1PR1 and KLF2 thereby enforcing tissue retention. Our results identify Hobit and Blimp1 as major common regulators that drive the differentiation of distinct populations of tissue-resident lymphocytes.

2016-04-25 | GSE70813 | GEO

RNA sequencing of NK cells in human lung

Project description:Human lung tissue-resident NK cells (trNK cells) are likely to play important roles in viral infections, inflammation and cancer. However, knowledge about lung trNK cells is lacking but is fundamental for exploiting these cells in therapeutic approaches. Here we analysed the transcriptome of CD69+CD49a+CD103+CD16-CD56bright, CD69+CD49a+CD103-CD16-CD56bright, CD69+CD49a-CD103-CD16-CD56bright, CD69-CD49a-CD103-CD16-CD56bright, and CD56dimCD16+NKG2A+CD57- NK cells isolated from human lung.

| EGAS00001003544 | EGA

Transcriptional Reference Map of Human Natural Killler Cells

Project description:The functional diversity of NK cell repertoires stems from differentiation, homeostatic receptor-ligand interactions, and adaptive-like responses to viral infections. Here we performed single-cell RNA sequencing of both bulk NK and sorted NK subsets to establish a transcriptional reference map of human natural killer cells based on single-cell RNA sequencing profiles from 72,129 cells obtained from bulk (12 donors) and sorted phenotypically-defined NK cell subsets (2 donors) and tissue-resident NK cells (TrNK, 136 donors). Our own data is included here.

2023-10-27 | GSE245690 | GEO

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