ArticleImmunity2023
Tissue resident iNKT17 cells facilitate cancer cell extravasation in liver metastasis via interleukin-22.
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Article in Immunity, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 45 papers.
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45citing papers in PubMed
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45 citing papers in PubMed, 57 citations in OpenAlex.
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Authors and funding
75 authors at 12 institutions in 6 countries.
Anastasios D GiannouSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany. Electronic address: a.giannou@uke.de.
Jan KempskiSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; The Calcium Signalling Group, Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Mildred Scheel Cancer Career Center HaTriCS4, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Ahmad Mustafa ShiriSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Jöran LückeSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Tao ZhangSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Lilan ZhaoDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Dimitra E ZazaraDivision for Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; University Children's Hospital, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Filippo CortesiDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Kristoffer RieckenResearch Department Cell and Gene Therapy, Department of Stem Cell Transplantation, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Maria Carolina Amezcua VeselyDepartment of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06520, USA.
Jun Siong LowDepartment of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06520, USA.
Hao XuDepartment of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06520, USA.
Eleanna KaffeDepartment of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06520, USA.
Laura Garcia-PerezSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Theodora AgaliotiDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Yoshito YamadaDepartment of Thoracic Surgery, Kyoto University Hospital, Kyoto, Japan; Department of Thoracic Surgery, University Hospital Zurich, Zurich, Switzerland.
Wolfgang JungraithmayrDepartment of Thoracic Surgery, University Hospital Zurich, Zurich, Switzerland; Department of Thoracic Surgery, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Ehud ZigmondThe Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel; The Research Center for Digestive Tract and Liver Diseases, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
Karl-Frederick KarstensDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Babett SteglichSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Jonas WagnerDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Leonie KonczallaDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Mildred Scheel Cancer Career Center HaTriCS4, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Antonella CarambiaI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg 20246, Germany.
Kornelius SchulzeI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg 20246, Germany.
Johann von FeldenI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg 20246, Germany.
Peter MayDivision of Clinical Pharmacology, Department of Medicine IV, Klinikum der Universität München, Munich, Germany.
Daria BriukhovetskaDivision of Clinical Pharmacology, Department of Medicine IV, Klinikum der Universität München, Munich, Germany.
Tanja BedkeSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Leonie BrockmannSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Sarah StarzonekInstitute of Anatomy and Experimental Morphology, University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Tobias LangeInstitute of Anatomy and Experimental Morphology, University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Institute of Anatomy I, University Hospital Jena, 07743 Jena, Germany.
Claudia KochDepartment of Tumor Biology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Sabine RiethdorfDepartment of Tumor Biology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Penelope PelczarSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Marius BöttcherSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Morsal SabihiSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Francis J HuberSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Matthias ReehDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Julia Kristin GrassDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Ramez WahibDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Hannes SeeseDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Björn-Ole StübenDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Mohammad Fard-AghaieDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Anna DupréeDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Pasquale ScognamiglioDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Gabriel PlitzkoDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Jan MeinersDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Shiwa SoukouSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Agnes WittekSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Caroline MantheyI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg 20246, Germany.
Ioannis C MaroulisDepartment of Surgery, University of Patras Medical School, Patras, Greece.
Petra C ArckDivision for Experimental Feto-Maternal Medicine, Department of Obstetrics and Fetal Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Daniel PerezDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Bin GaoLaboratory of Liver Diseases, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, MD, USA.
Sotirios G ZarogiannisDepartment of Physiology, Faculty of Medicine, University of Thessaly, BIOPOLIS, Larissa, Greece; Center for Pediatric and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany.
Till StrowigDepartment of Microbial Immune Regulation, Helmholtz Center for Infection Research, 38124 Braunschweig, Germany.
Renata PasqualiniRutgers Cancer Institute of New Jersey and Division of Cancer Biology, Department of Radiation Oncology, Rutgers New Jersey Medical School, Newark, NJ, USA.
Wadih ArapRutgers Cancer Institute of New Jersey and Division of Hematology/Oncology, Department of Medicine, Rutgers New Jersey Medical School, Newark, NJ, USA.
Javier Suárez GosálvezDivision of Clinical Pharmacology, Department of Medicine IV, Klinikum der Universität München, Munich, Germany.
Sebastian KoboldDivision of Clinical Pharmacology, Department of Medicine IV, Klinikum der Universität München, Munich, Germany; German Center for Translational Cancer Research (DKTK), Partner Site Munich, Munich, Germany; Einheit für Klinische Pharmakologie (EKLiP), Helmholtz Zentrum München, German Research Center for Environmental Health (HMGU), Neuherberg, Germany.
Immo PrinzInstitute of Immunology, Hannover Medical School, Hannover, Germany; Institute of Systems Immunology, Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Andreas H GuseThe Calcium Signalling Group, Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Michael TachezyDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Tarik GhadbanDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Asmus HeumannDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Jun LiDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Nathaniel MellingDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Oliver MannDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Jakob R IzbickiDepartment of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Klaus PantelDepartment of Tumor Biology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Udo SchumacherInstitute of Anatomy and Experimental Morphology, University Cancer Center Hamburg, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Medical School Berlin, 10117 Berlin, Germany.
Ansgar W LohseI. Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg 20246, Germany.
Richard A FlavellDepartment of Immunobiology, School of Medicine, Yale University, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06520, USA.
Nicola GaglianiSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Department of General, Visceral and Thoracic Surgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.
Samuel HuberSection of Molecular Immunology und Gastroenterology, I. Department of Medicine, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany; Hamburg Center for Translational Immunology (HCTI), University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany. Electronic address: shuber@uke.de.
Universität Hamburg · DEHoward Hughes Medical Institute · USLMU Klinikum · DERutgers, The State University of New Jersey · USHelmholtz Centre for Infection Research · DEHelmholtz Zentrum München · DENational Institutes of Health · USTel Aviv University · ILUniversity Hospital of Zurich · CHUniversity of Freiburg · DEUniversity of Patras · GRUniversity of Thessaly · GR
Funding
Howard Hughes Medical Institute
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.
Indexed as
InterleukinsLiver NeoplasmsNatural Killer T-CellsAnimalsColorectal NeoplasmsEndothelial CellsInterleukin-22MiceMice, Inbred C57BLInterleukin-22InterleukinsANPEPcancer cell extravasationendothelial cellsextravasationIL-22metastasismetastasis formationtissue resident cells
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