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Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22

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Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22. / Giannou, Anastasios D; Kempski, Jan; Shiri, Ahmad Mustafa; Lücke, Jöran; Zhang, Tao; Zhao, Lilan; Zazara, Dimitra E; Cortesi, Filippo; Riecken, Kristoffer; Amezcua Vesely, Maria Carolina; Low, Jun Siong; Xu, Hao; Kaffe, Eleanna; Garcia-Perez, Laura; Agalioti, Theodora; Yamada, Yoshito; Jungraithmayr, Wolfgang; Zigmond, Ehud; Karstens, Karl-Frederick; Steglich, Babett; Wagner, Jonas; Konczalla, Leonie; Carambia, Antonella; Schulze, Kornelius; von Felden, Johann; May, Peter; Briukhovetska, Daria; Bedke, Tanja; Brockmann, Leonie; Starzonek, Sarah; Lange, Tobias; Koch, Claudia; Riethdorf, Sabine; Pelczar, Penelope; Böttcher, Marius; Sabihi, Morsal; Huber, Francis J; Reeh, Matthias; Grass, Julia Kristin; Wahib, Ramez; Seese, Hannes; Stüben, Björn-Ole; Fard-Aghaie, Mohammad; Duprée, Anna; Scognamiglio, Pasquale; Plitzko, Gabriel; Meiners, Jan; Soukou, Shiwa; Wittek, Agnes; Manthey, Caroline; Maroulis, Ioannis C; Arck, Petra C; Perez, Daniel; Gao, Bin; Zarogiannis, Sotirios G; Strowig, Till; Pasqualini, Renata; Arap, Wadih; Gosálvez, Javier Suárez; Kobold, Sebastian; Prinz, Immo; Guse, Andreas H; Tachezy, Michael; Ghadban, Tarik; Heumann, Asmus; Li, Jun; Melling, Nathaniel; Mann, Oliver; Izbicki, Jakob R; Pantel, Klaus; Schumacher, Udo; Lohse, Ansgar W; Flavell, Richard A; Gagliani, Nicola; Huber, Samuel.

In: IMMUNITY, Vol. 56, No. 1, 10.01.2023, p. 125-142.e12.

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

Harvard

Giannou, AD, Kempski, J, Shiri, AM, Lücke, J, Zhang, T, Zhao, L, Zazara, DE, Cortesi, F, Riecken, K, Amezcua Vesely, MC, Low, JS, Xu, H, Kaffe, E, Garcia-Perez, L, Agalioti, T, Yamada, Y, Jungraithmayr, W, Zigmond, E, Karstens, K-F, Steglich, B, Wagner, J, Konczalla, L, Carambia, A, Schulze, K, von Felden, J, May, P, Briukhovetska, D, Bedke, T, Brockmann, L, Starzonek, S, Lange, T, Koch, C, Riethdorf, S, Pelczar, P, Böttcher, M, Sabihi, M, Huber, FJ, Reeh, M, Grass, JK, Wahib, R, Seese, H, Stüben, B-O, Fard-Aghaie, M, Duprée, A, Scognamiglio, P, Plitzko, G, Meiners, J, Soukou, S, Wittek, A, Manthey, C, Maroulis, IC, Arck, PC, Perez, D, Gao, B, Zarogiannis, SG, Strowig, T, Pasqualini, R, Arap, W, Gosálvez, JS, Kobold, S, Prinz, I, Guse, AH, Tachezy, M, Ghadban, T, Heumann, A, Li, J, Melling, N, Mann, O, Izbicki, JR, Pantel, K, Schumacher, U, Lohse, AW, Flavell, RA, Gagliani, N & Huber, S 2023, 'Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22', IMMUNITY, vol. 56, no. 1, pp. 125-142.e12. https://doi.org/10.1016/j.immuni.2022.12.014

APA

Giannou, A. D., Kempski, J., Shiri, A. M., Lücke, J., Zhang, T., Zhao, L., Zazara, D. E., Cortesi, F., Riecken, K., Amezcua Vesely, M. C., Low, J. S., Xu, H., Kaffe, E., Garcia-Perez, L., Agalioti, T., Yamada, Y., Jungraithmayr, W., Zigmond, E., Karstens, K-F., ... Huber, S. (2023). Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22. IMMUNITY, 56(1), 125-142.e12. https://doi.org/10.1016/j.immuni.2022.12.014

Vancouver

Giannou AD, Kempski J, Shiri AM, Lücke J, Zhang T, Zhao L et al. Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22. IMMUNITY. 2023 Jan 10;56(1):125-142.e12. https://doi.org/10.1016/j.immuni.2022.12.014

Bibtex

@article{bc3aad0f69044e888cd291cd5bdd20de,
title = "Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22",
abstract = "During metastasis, cancer cells invade, intravasate, enter the circulation, extravasate, and colonize target organs. Here, we examined the role of interleukin (IL)-22 in metastasis. Immune cell-derived IL-22 acts on epithelial tissues, promoting regeneration and healing upon tissue damage, but it is also associated with malignancy. Il22-deficient mice and mice treated with an IL-22 antibody were protected from colon-cancer-derived liver and lung metastasis formation, while overexpression of IL-22 promoted metastasis. Mechanistically, IL-22 acted on endothelial cells, promoting endothelial permeability and cancer cell transmigration via induction of endothelial aminopeptidase N. Multi-parameter flow cytometry and single-cell sequencing of immune cells isolated during cancer cell extravasation into the liver revealed iNKT17 cells as source of IL-22. iNKT-cell-deficient mice exhibited reduced metastases, which was reversed by injection of wild type, but not Il22-deficient, invariant natural killer T (iNKT) cells. IL-22-producing iNKT cells promoting metastasis were tissue resident, as demonstrated by parabiosis. Thus, IL-22 may present a therapeutic target for prevention of metastasis.",
keywords = "Animals, Mice, Endothelial Cells/metabolism, Interleukins/metabolism, Liver Neoplasms/pathology, Mice, Inbred C57BL, Natural Killer T-Cells/metabolism, Colorectal Neoplasms/metabolism",
author = "Giannou, {Anastasios D} and Jan Kempski and Shiri, {Ahmad Mustafa} and J{\"o}ran L{\"u}cke and Tao Zhang and Lilan Zhao and Zazara, {Dimitra E} and Filippo Cortesi and Kristoffer Riecken and {Amezcua Vesely}, {Maria Carolina} and Low, {Jun Siong} and Hao Xu and Eleanna Kaffe and Laura Garcia-Perez and Theodora Agalioti and Yoshito Yamada and Wolfgang Jungraithmayr and Ehud Zigmond and Karl-Frederick Karstens and Babett Steglich and Jonas Wagner and Leonie Konczalla and Antonella Carambia and Kornelius Schulze and {von Felden}, Johann and Peter May and Daria Briukhovetska and Tanja Bedke and Leonie Brockmann and Sarah Starzonek and Tobias Lange and Claudia Koch and Sabine Riethdorf and Penelope Pelczar and Marius B{\"o}ttcher and Morsal Sabihi and Huber, {Francis J} and Matthias Reeh and Grass, {Julia Kristin} and Ramez Wahib and Hannes Seese and Bj{\"o}rn-Ole St{\"u}ben and Mohammad Fard-Aghaie and Anna Dupr{\'e}e and Pasquale Scognamiglio and Gabriel Plitzko and Jan Meiners and Shiwa Soukou and Agnes Wittek and Caroline Manthey and Maroulis, {Ioannis C} and Arck, {Petra C} and Daniel Perez and Bin Gao and Zarogiannis, {Sotirios G} and Till Strowig and Renata Pasqualini and Wadih Arap and Gos{\'a}lvez, {Javier Su{\'a}rez} and Sebastian Kobold and Immo Prinz and Guse, {Andreas H} and Michael Tachezy and Tarik Ghadban and Asmus Heumann and Jun Li and Nathaniel Melling and Oliver Mann and Izbicki, {Jakob R} and Klaus Pantel and Udo Schumacher and Lohse, {Ansgar W} and Flavell, {Richard A} and Nicola Gagliani and Samuel Huber",
note = "Copyright {\textcopyright} 2022 The Authors. Published by Elsevier Inc. All rights reserved.",
year = "2023",
month = jan,
day = "10",
doi = "10.1016/j.immuni.2022.12.014",
language = "English",
volume = "56",
pages = "125--142.e12",
journal = "IMMUNITY",
issn = "1074-7613",
publisher = "Cell Press",
number = "1",

}

RIS

TY - JOUR

T1 - Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22

AU - Giannou, Anastasios D

AU - Kempski, Jan

AU - Shiri, Ahmad Mustafa

AU - Lücke, Jöran

AU - Zhang, Tao

AU - Zhao, Lilan

AU - Zazara, Dimitra E

AU - Cortesi, Filippo

AU - Riecken, Kristoffer

AU - Amezcua Vesely, Maria Carolina

AU - Low, Jun Siong

AU - Xu, Hao

AU - Kaffe, Eleanna

AU - Garcia-Perez, Laura

AU - Agalioti, Theodora

AU - Yamada, Yoshito

AU - Jungraithmayr, Wolfgang

AU - Zigmond, Ehud

AU - Karstens, Karl-Frederick

AU - Steglich, Babett

AU - Wagner, Jonas

AU - Konczalla, Leonie

AU - Carambia, Antonella

AU - Schulze, Kornelius

AU - von Felden, Johann

AU - May, Peter

AU - Briukhovetska, Daria

AU - Bedke, Tanja

AU - Brockmann, Leonie

AU - Starzonek, Sarah

AU - Lange, Tobias

AU - Koch, Claudia

AU - Riethdorf, Sabine

AU - Pelczar, Penelope

AU - Böttcher, Marius

AU - Sabihi, Morsal

AU - Huber, Francis J

AU - Reeh, Matthias

AU - Grass, Julia Kristin

AU - Wahib, Ramez

AU - Seese, Hannes

AU - Stüben, Björn-Ole

AU - Fard-Aghaie, Mohammad

AU - Duprée, Anna

AU - Scognamiglio, Pasquale

AU - Plitzko, Gabriel

AU - Meiners, Jan

AU - Soukou, Shiwa

AU - Wittek, Agnes

AU - Manthey, Caroline

AU - Maroulis, Ioannis C

AU - Arck, Petra C

AU - Perez, Daniel

AU - Gao, Bin

AU - Zarogiannis, Sotirios G

AU - Strowig, Till

AU - Pasqualini, Renata

AU - Arap, Wadih

AU - Gosálvez, Javier Suárez

AU - Kobold, Sebastian

AU - Prinz, Immo

AU - Guse, Andreas H

AU - Tachezy, Michael

AU - Ghadban, Tarik

AU - Heumann, Asmus

AU - Li, Jun

AU - Melling, Nathaniel

AU - Mann, Oliver

AU - Izbicki, Jakob R

AU - Pantel, Klaus

AU - Schumacher, Udo

AU - Lohse, Ansgar W

AU - Flavell, Richard A

AU - Gagliani, Nicola

AU - Huber, Samuel

N1 - Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2023/1/10

Y1 - 2023/1/10

N2 - During metastasis, cancer cells invade, intravasate, enter the circulation, extravasate, and colonize target organs. Here, we examined the role of interleukin (IL)-22 in metastasis. Immune cell-derived IL-22 acts on epithelial tissues, promoting regeneration and healing upon tissue damage, but it is also associated with malignancy. Il22-deficient mice and mice treated with an IL-22 antibody were protected from colon-cancer-derived liver and lung metastasis formation, while overexpression of IL-22 promoted metastasis. Mechanistically, IL-22 acted on endothelial cells, promoting endothelial permeability and cancer cell transmigration via induction of endothelial aminopeptidase N. Multi-parameter flow cytometry and single-cell sequencing of immune cells isolated during cancer cell extravasation into the liver revealed iNKT17 cells as source of IL-22. iNKT-cell-deficient mice exhibited reduced metastases, which was reversed by injection of wild type, but not Il22-deficient, invariant natural killer T (iNKT) cells. IL-22-producing iNKT cells promoting metastasis were tissue resident, as demonstrated by parabiosis. Thus, IL-22 may present a therapeutic target for prevention of metastasis.

AB - During metastasis, cancer cells invade, intravasate, enter the circulation, extravasate, and colonize target organs. Here, we examined the role of interleukin (IL)-22 in metastasis. Immune cell-derived IL-22 acts on epithelial tissues, promoting regeneration and healing upon tissue damage, but it is also associated with malignancy. Il22-deficient mice and mice treated with an IL-22 antibody were protected from colon-cancer-derived liver and lung metastasis formation, while overexpression of IL-22 promoted metastasis. Mechanistically, IL-22 acted on endothelial cells, promoting endothelial permeability and cancer cell transmigration via induction of endothelial aminopeptidase N. Multi-parameter flow cytometry and single-cell sequencing of immune cells isolated during cancer cell extravasation into the liver revealed iNKT17 cells as source of IL-22. iNKT-cell-deficient mice exhibited reduced metastases, which was reversed by injection of wild type, but not Il22-deficient, invariant natural killer T (iNKT) cells. IL-22-producing iNKT cells promoting metastasis were tissue resident, as demonstrated by parabiosis. Thus, IL-22 may present a therapeutic target for prevention of metastasis.

KW - Animals

KW - Mice

KW - Endothelial Cells/metabolism

KW - Interleukins/metabolism

KW - Liver Neoplasms/pathology

KW - Mice, Inbred C57BL

KW - Natural Killer T-Cells/metabolism

KW - Colorectal Neoplasms/metabolism

U2 - 10.1016/j.immuni.2022.12.014

DO - 10.1016/j.immuni.2022.12.014

M3 - SCORING: Journal article

C2 - 36630911

VL - 56

SP - 125-142.e12

JO - IMMUNITY

JF - IMMUNITY

SN - 1074-7613

IS - 1

ER -