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

Tommaso Torcellan; Christin Friedrich; Rémi Doucet-Ladevèze; Thomas Ossner; Virgínia Visaconill Solé; Sofie Riedmann; Milas Ugur; Fabian Imdahl; Stephan P Rosshart; Sebastian J Arnold; Mercedes Gomez de Agüero; Nicola Gagliani; Richard A Flavell; Simone Backes; Wolfgang Kastenmüller; Georg Gasteiger

doi:10.1016/j.immuni.2023.11.018

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

Standard

Circulating NK cells establish tissue residency upon acute infection of skin and mediate accelerated effector responses to secondary infection. / Torcellan, Tommaso; Friedrich, Christin; Doucet-Ladevèze, Rémi; Ossner, Thomas; Solé, Virgínia Visaconill; Riedmann, Sofie; Ugur, Milas; Imdahl, Fabian; Rosshart, Stephan P; Arnold, Sebastian J; Gomez de Agüero, Mercedes; Gagliani, Nicola; Flavell, Richard A; Backes, Simone; Kastenmüller, Wolfgang; Gasteiger, Georg.

In: IMMUNITY, Vol. 57, No. 1, 09.01.2024, p. 124-140.e7.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Torcellan, T, Friedrich, C, Doucet-Ladevèze, R, Ossner, T, Solé, VV, Riedmann, S, Ugur, M, Imdahl, F, Rosshart, SP, Arnold, SJ, Gomez de Agüero, M, Gagliani, N, Flavell, RA, Backes, S, Kastenmüller, W & Gasteiger, G 2024, 'Circulating NK cells establish tissue residency upon acute infection of skin and mediate accelerated effector responses to secondary infection', IMMUNITY, vol. 57, no. 1, pp. 124-140.e7. https://doi.org/10.1016/j.immuni.2023.11.018

APA

Torcellan, T., Friedrich, C., Doucet-Ladevèze, R., Ossner, T., Solé, V. V., Riedmann, S., Ugur, M., Imdahl, F., Rosshart, S. P., Arnold, S. J., Gomez de Agüero, M., Gagliani, N., Flavell, R. A., Backes, S., Kastenmüller, W., & Gasteiger, G. (2024). Circulating NK cells establish tissue residency upon acute infection of skin and mediate accelerated effector responses to secondary infection. IMMUNITY, 57(1), 124-140.e7. https://doi.org/10.1016/j.immuni.2023.11.018

Vancouver

Torcellan T, Friedrich C, Doucet-Ladevèze R, Ossner T, Solé VV, Riedmann S et al. Circulating NK cells establish tissue residency upon acute infection of skin and mediate accelerated effector responses to secondary infection. IMMUNITY. 2024 Jan 9;57(1):124-140.e7. https://doi.org/10.1016/j.immuni.2023.11.018

Bibtex

@article{556588dde7cd4e2d9b271d7631ac9ed6,

title = "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, and these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigate whether circulating conventional NK (cNK) cells can develop into long-lived tissue-resident NK (trNK) 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 trNK cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK cells arose from interferon (IFN)-γ-producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK cell 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 tissue residency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny.",

keywords = "Humans, Coinfection, Killer Cells, Natural/metabolism, Cell Differentiation",

author = "Tommaso Torcellan and Christin Friedrich and R{\'e}mi Doucet-Ladev{\`e}ze and Thomas Ossner and Sol{\'e}, {Virg{\'i}nia Visaconill} and Sofie Riedmann and Milas Ugur and Fabian Imdahl and Rosshart, {Stephan P} and Arnold, {Sebastian J} and {Gomez de Ag{\"u}ero}, Mercedes and Nicola Gagliani and Flavell, {Richard A} and Simone Backes and Wolfgang Kastenm{\"u}ller and Georg Gasteiger",

year = "2024",

month = jan,

day = "9",

doi = "10.1016/j.immuni.2023.11.018",

language = "English",

volume = "57",

pages = "124--140.e7",

journal = "IMMUNITY",

issn = "1074-7613",

publisher = "Cell Press",

number = "1",

}

RIS

TY - JOUR

T1 - Circulating NK cells establish tissue residency upon acute infection of skin and mediate accelerated effector responses to secondary infection

AU - Torcellan, Tommaso

AU - Friedrich, Christin

AU - Doucet-Ladevèze, Rémi

AU - Ossner, Thomas

AU - Solé, Virgínia Visaconill

AU - Riedmann, Sofie

AU - Ugur, Milas

AU - Imdahl, Fabian

AU - Rosshart, Stephan P

AU - Arnold, Sebastian J

AU - Gomez de Agüero, Mercedes

AU - Gagliani, Nicola

AU - Flavell, Richard A

AU - Backes, Simone

AU - Kastenmüller, Wolfgang

AU - Gasteiger, Georg

PY - 2024/1/9

Y1 - 2024/1/9

N2 - Natural killer (NK) cells are present in the circulation and can also be found residing in tissues, and these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigate whether circulating conventional NK (cNK) cells can develop into long-lived tissue-resident NK (trNK) 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 trNK cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK cells arose from interferon (IFN)-γ-producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK cell 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 tissue residency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny.

AB - Natural killer (NK) cells are present in the circulation and can also be found residing in tissues, and these populations exhibit distinct developmental requirements and are thought to differ in terms of ontogeny. Here, we investigate whether circulating conventional NK (cNK) cells can develop into long-lived tissue-resident NK (trNK) 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 trNK cells that share transcriptional similarity with CD56brightTCF1hi NK cells in human tissues. Skin trNK cells arose from interferon (IFN)-γ-producing effector cells and required restricted expression of the transcriptional regulator Blimp1 to optimize Tcf1-dependent trNK cell 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 tissue residency that is distinct from Hobit-dependent developmental paths of NK cells and ILC1 seeding tissues during ontogeny.

KW - Humans

KW - Coinfection

KW - Killer Cells, Natural/metabolism

KW - Cell Differentiation

U2 - 10.1016/j.immuni.2023.11.018

DO - 10.1016/j.immuni.2023.11.018

M3 - SCORING: Journal article

C2 - 38157853

VL - 57

SP - 124-140.e7

JO - IMMUNITY

JF - IMMUNITY

SN - 1074-7613

IS - 1

ER -