Natural killer (NK)–dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4<sup>+</sup>T cells

Nakayama, Masafumi; Takeda, Kazuyoshi; Kawano, Mitsuko; Takai, Toshiyuki; Ishii, Naoto; Ogasawara, Kunio

doi:10.1073/pnas.1110584108

Cited by 102 publications

(103 citation statements)

References 34 publications

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“…For one, mNK cells exhibit low levels of CD11c, 15 whereas the expression of B220 and MHC II can be up-regulated on mNK cells, at least on in vitro activation. 9,12 Secondly, several groups could not replicate the finding that IKDCs produced IFN␣, [16][17][18][19] suggesting that the IKDC preparation in the original studies 13 may have been contaminated with pDCs. Finally, 3 independent groups found that cells exhibiting the IKDC phenotype were part of the NK lineage and challenged the idea that these cells also exhibit DC properties.…”

Section: Introductionmentioning

confidence: 56%

“…[5][6][7] Finally, on activation, mNK cells gain the expression of additional activation markers, namely CD69, CD44, FasL, CD86, and MHC II. [8][9][10][11][12] In addition, activated mNK cells increase in size and show heightened functional properties such as an enhanced cytolytic potential and increased ability to produce cytokines. 2 Notably, activated mNK cells show a striking phenotypic resemblance to the IFN-producing killer dendritic cells (IKDCs), which were initially described as a hybrid cell type exhibiting properties of both mNK cells and plasmacytoid DCs (pDCs).…”

Section: Introductionmentioning

confidence: 99%

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Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Guimont-Desrochers

Boucher

Dong

et al. 2012

Blood

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The cell lineage origin of IFN-producing killer dendritic cells (IKDCs), which exhibit prominent antitumoral activity, has been subject to debate. Although IKDCs were first described as a cell type exhibiting both plasmacytoid DC and natural killer (NK) cell properties, the current view reflects that IKDCs merely represent activated NK cells expressing B220, which were thus renamed B220 ؉ NK cells. Herein, we further investigate the lineage relation of B220 ؉ NK cells with regard to other NK-cell subsets. We surprisingly find that, after adoptive transfer, B220 ؊ NK cells did not acquire B220 expression, even in the presence of potent activating stimuli. These findings strongly argue against the concept that B220 IntroductionNatural killer (NK) cells are large granular lymphocytes that were first described for their capacity to spontaneously eliminate tumor cells and virus-infected cells without prior sensitization. 1 These functions are mediated by an array of Ig-like and C-type lectin receptors that deliver both activating and inhibitory signals. 1 In addition to their cytotoxic activity, NK cells rapidly produce vast amounts of cytokines, such as IFN-␥, as well as other cellular mediators, including chemokines. NK cells thus act as an important first line of defense in the early control of virus infection, in tumor immunosurveillance, and in immunoregulation.The differentiation of NK cells from hematopoietic stem cells in the BM is incompletely understood, but it is thought to occur in a sequential manner that involves multiple stages of development that is based on phenotype, function, and turnover. 2 The first committed NK-cell precursor (NKP) is characterized by CD122 ϩ expression in the absence of the expression of other lineage markers, 3 although a pre-NKP cell lacking CD122 expression has recently been characterized as a NK cell-committed progenitor preceding NKP in the differentiation stages. 4 NKPs subsequently give rise to immature NK (iNK) cells that express CD122 along with NK1.1 and CD94/NKG2. As iNK cells differentiate further, they undergo education to achieve their full functional competence, and they acquire CD49b expression to finally become mature NK (mNK) cells. 2 These CD49b ϩ mNK cells still compose a heterogeneous cell population that may be segregated according to their phenotype, function, and tissue distribution. Indeed, functional maturation of CD49b ϩ mNK cells proceeds along 4 stages from the CD11b Ϫ CD27 Ϫ to the CD11b Ϫ CD27 ϩ then to the CD11b ϩ CD27 ϩ and finally to the CD11b ϩ CD27 Ϫ subset. 5 Several other markers are acquired along this differentiation process, including CD43, CD94-NKG2, and Ly49 receptors. [5][6][7] Finally, on activation, mNK cells gain the expression of additional activation markers, namely CD69, CD44, FasL, CD86, and MHC II. [8][9][10][11][12] In addition, activated mNK cells increase in size and show heightened functional properties such as an enhanced cytolytic potential and increased ability to produce cytokines. 2 Notably, activated mNK cells show ...

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Section: Introductionmentioning

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Guimont-Desrochers

Boucher

Dong

et al. 2012

Blood

View full text Add to dashboard Cite

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“…3D) lead us to address the possibility that NK cells acquire Rae-1 from target cells, rather than through de novo synthesis. We and others have recently reported that NK cells have the ability to acquire cell surface proteins from target cells in a cell-cell contact-dependent manner, referred to as trogocytosis (21,28,29). Likewise, acquisition of Rae-1 expression occurred only with direct cell-cell contact and did not occur on NK cells cultured with RMA/Rae-1δ in Transwell plates (Fig.…”

Section: Nk Cell Deathmentioning

confidence: 98%

“…NK cells were prepared from mouse splenocytes as described previously (28). In brief, splenocytes were incubated with anti-CD4 mAb (clone GK1.5) and anti-CD8 mAb (clone 53-6.7), followed by magnetic beads coated with goat anti-mouse Ig and goat anti-rat Ig Abs (Qiagen).…”

Section: Methodsmentioning

confidence: 99%

Fratricide of natural killer cells dressed with tumor-derived NKG2D ligand

Nakamura

Nakayama

Kawano

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The natural killer group 2 membrane D (NKG2D) activating receptor plays crucial roles not only in host defense against tumors and viral infections, but also in autoimmune diseases. After NKG2D-mediated activation, Natural killer (NK) cells must be regulated to avoid potentially harmful reactivity. However, the negative regulation of these activated NK cells is poorly understood. Here, we reveal that the engagement of NKG2D by its ligand elicits not only target cell lysis, but also NK cell fratricide. Conventional mouse NK cells underwent cell death when cocultured with RMA cells expressing the NKG2D ligand retinoic acid early-inducible protein 1 (Rae-1), but not with RMA cells lacking MHC class I. NK cells from mice deficient for DAP10 and DAP12 or perforin did not undergo death, highlighting the importance of the NKG2D pathway for NK cell death. However, NKG2D does not transmit direct death signals in NK cells. Rather, the interaction between NKG2D and Rae-1 allowed NK cells to acquire tumor-derived Rae-1 by a membrane transfer process known as "trogocytosis," which was associated with clathrin-dependent NKG2D endocytosis. NK cells dressed with Rae-1 were lysed by neighboring NK cells through the NKG2D-induced perforin pathway in vitro and in vivo. These results provide the unique NKG2D function in negative regulation of activated NK cells.

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“…Acquisition of MHC-I by NK cells from tumor cells leads to a reduced NK cytotoxic function (41). Acquisition of MHC-II from DCs via trogocytosis has been shown in CD4 T cells, NK cells, DCs, macrophages, and lymph node stromal cells (28,(42)(43)(44)(45). MHC-II-dressed recipient cells either stimulate or suppress T cells, perhaps depending on the expression and acquisition of costimulatory molecules (28).…”

Section: Cd11cmentioning

confidence: 99%

Trogocytosis of peptide–MHC class II complexes from dendritic cells confers antigen-presenting ability on basophils

Miyake

Shiozawa

Nagao

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

108

101

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Th2 immunity plays important roles in both protective and allergic responses. Nevertheless, the nature of antigen-presenting cells responsible for Th2 cell differentiation remains ill-defined compared with the nature of the cells responsible for Th1 and Th17 cell differentiation. Basophils have attracted attention as a producer of Th2-inducing cytokine IL-4, whereas their MHC class II (MHC-II) expression and function as antigen-presenting cells are matters of considerable controversy. Here we revisited the MHC-II expression on basophils and explored its functional relevance in Th2 cell differentiation. Basophils generated in vitro from bone marrow cells in culture with IL-3 plus GM-CSF displayed MHC-II on the cell surface, whereas those generated in culture with IL-3 alone did not. Of note, these MHC-II–expressing basophils showed little or no transcription of the corresponding MHC-II gene. The GM-CSF addition to culture expanded dendritic cells (DCs) other than basophils. Coculture of basophils and DCs revealed that basophils acquired peptide–MHC-II complexes from DCs via cell contact-dependent trogocytosis. The acquired complexes, together with CD86, enabled basophils to stimulate peptide-specific T cells, leading to their proliferation and IL-4 production, indicating that basophils can function as antigen-presenting cells for Th2 cell differentiation. Transfer of MHC-II from DCs to basophils was also detected in draining lymph nodes of mice with atopic dermatitis-like skin inflammation. Thus, the present study defined the mechanism by which basophils display MHC-II on the cell surface and appears to reconcile some discrepancies observed in previous studies.

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Natural killer (NK)–dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4⁺T cells

Cited by 102 publications

References 34 publications

Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Fratricide of natural killer cells dressed with tumor-derived NKG2D ligand

Trogocytosis of peptide–MHC class II complexes from dendritic cells confers antigen-presenting ability on basophils

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Natural killer (NK)–dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4+T cells

Cited by 102 publications

References 34 publications

Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Redefining interferon-producing killer dendritic cells as a novel intermediate in NK-cell differentiation

Fratricide of natural killer cells dressed with tumor-derived NKG2D ligand

Trogocytosis of peptide–MHC class II complexes from dendritic cells confers antigen-presenting ability on basophils

Contact Info

Product

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Natural killer (NK)–dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4⁺T cells