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

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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839362/
https://www.ncbi.nlm.nih.gov/pubmed/36630911
http://dx.doi.org/10.1016/j.immuni.2022.12.014
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author 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
author_facet 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
author_sort Giannou, Anastasios D.
collection PubMed
description 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.
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spelling pubmed-98393622023-01-18 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 Immunity Article 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. Cell Press 2023-01-10 /pmc/articles/PMC9839362/ /pubmed/36630911 http://dx.doi.org/10.1016/j.immuni.2022.12.014 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
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
Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title_full Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title_fullStr Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title_full_unstemmed Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title_short Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
title_sort tissue resident inkt17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9839362/
https://www.ncbi.nlm.nih.gov/pubmed/36630911
http://dx.doi.org/10.1016/j.immuni.2022.12.014
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