An intraepithelial ILC1-like natural killer cell subset produces IL-13

Natural killer (NK) cells are innate immune effectors with considerable heterogeneity and potent antitumor capabilities. Intraepithelial ILC1 (ieILC1)-like NK cells, a population of cytotoxic tissue-resident innate lymphoid cells, have recently been documented in the microenvironment of head and nec...

Full description

Saved in:
Bibliographic Details
Main Authors: Sainiteesh Maddineni, Krishna Sharma, Imran A. Mohammad, Alistaire D. Ruggiero-Sherman, Ivan Stepanek, June Ho Shin, Jennifer K. Bando, John B. Sunwoo
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1521086/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849773527731798016
author Sainiteesh Maddineni
Krishna Sharma
Imran A. Mohammad
Alistaire D. Ruggiero-Sherman
Ivan Stepanek
June Ho Shin
Jennifer K. Bando
John B. Sunwoo
author_facet Sainiteesh Maddineni
Krishna Sharma
Imran A. Mohammad
Alistaire D. Ruggiero-Sherman
Ivan Stepanek
June Ho Shin
Jennifer K. Bando
John B. Sunwoo
author_sort Sainiteesh Maddineni
collection DOAJ
description Natural killer (NK) cells are innate immune effectors with considerable heterogeneity and potent antitumor capabilities. Intraepithelial ILC1 (ieILC1)-like NK cells, a population of cytotoxic tissue-resident innate lymphoid cells, have recently been documented in the microenvironment of head and neck squamous cell carcinomas (HNSCC) and other solid tumors. These cells have antitumor cytolytic potential and are potent producers of type 1 cytokines, including IFNγ. Here, we identify a subpopulation of ex vivo differentiated ieILC1-like NK cells that produce IL-13 upon stimulation. Functional characterization revealed that these cells co-expressed IFNγ and IL-13 while maintaining an ILC1 transcriptional signature. IL-13 was induced either upon co-culture with tumor cell lines, or in response to TGF-β and IL-15. IL-13-expressing ieILC1-like NK cells were identified among tumor infiltrating lymphocytes expanded from patient HNSCC tumors, in support of their in vivoexistence in primary tumors. These data demonstrate additional heterogeneity within the ieILC1-like NK cell population than previously appreciated and highlight a unique form of ILC plasticity in which cells with clear ILC1 transcriptional profiles express a type 2 cytokine. With the known roles of IL-13 in cancer cell growth dynamics and immunoregulation, the identification of this subset within tumor microenvironments presents a potential target for therapeutic manipulation.
format Article
id doaj-art-cf71f148d17e498e8733ce181dbd5796
institution DOAJ
issn 1664-3224
language English
publishDate 2025-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-cf71f148d17e498e8733ce181dbd57962025-08-20T03:02:02ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-03-011610.3389/fimmu.2025.15210861521086An intraepithelial ILC1-like natural killer cell subset produces IL-13Sainiteesh Maddineni0Krishna Sharma1Imran A. Mohammad2Alistaire D. Ruggiero-Sherman3Ivan Stepanek4June Ho Shin5Jennifer K. Bando6John B. Sunwoo7Department of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Microbiology & Immunology, Stanford University School of Medicine, Palo Alto, CA, United StatesDepartment of Otolaryngology — Head & Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, United StatesNatural killer (NK) cells are innate immune effectors with considerable heterogeneity and potent antitumor capabilities. Intraepithelial ILC1 (ieILC1)-like NK cells, a population of cytotoxic tissue-resident innate lymphoid cells, have recently been documented in the microenvironment of head and neck squamous cell carcinomas (HNSCC) and other solid tumors. These cells have antitumor cytolytic potential and are potent producers of type 1 cytokines, including IFNγ. Here, we identify a subpopulation of ex vivo differentiated ieILC1-like NK cells that produce IL-13 upon stimulation. Functional characterization revealed that these cells co-expressed IFNγ and IL-13 while maintaining an ILC1 transcriptional signature. IL-13 was induced either upon co-culture with tumor cell lines, or in response to TGF-β and IL-15. IL-13-expressing ieILC1-like NK cells were identified among tumor infiltrating lymphocytes expanded from patient HNSCC tumors, in support of their in vivoexistence in primary tumors. These data demonstrate additional heterogeneity within the ieILC1-like NK cell population than previously appreciated and highlight a unique form of ILC plasticity in which cells with clear ILC1 transcriptional profiles express a type 2 cytokine. With the known roles of IL-13 in cancer cell growth dynamics and immunoregulation, the identification of this subset within tumor microenvironments presents a potential target for therapeutic manipulation.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1521086/fullNK cellstumor immunologyIL-13cytokinesILCallergy
spellingShingle Sainiteesh Maddineni
Krishna Sharma
Imran A. Mohammad
Alistaire D. Ruggiero-Sherman
Ivan Stepanek
June Ho Shin
Jennifer K. Bando
John B. Sunwoo
An intraepithelial ILC1-like natural killer cell subset produces IL-13
Frontiers in Immunology
NK cells
tumor immunology
IL-13
cytokines
ILC
allergy
title An intraepithelial ILC1-like natural killer cell subset produces IL-13
title_full An intraepithelial ILC1-like natural killer cell subset produces IL-13
title_fullStr An intraepithelial ILC1-like natural killer cell subset produces IL-13
title_full_unstemmed An intraepithelial ILC1-like natural killer cell subset produces IL-13
title_short An intraepithelial ILC1-like natural killer cell subset produces IL-13
title_sort intraepithelial ilc1 like natural killer cell subset produces il 13
topic NK cells
tumor immunology
IL-13
cytokines
ILC
allergy
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1521086/full
work_keys_str_mv AT sainiteeshmaddineni anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT krishnasharma anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT imranamohammad anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT alistairedruggierosherman anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT ivanstepanek anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT junehoshin anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT jenniferkbando anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT johnbsunwoo anintraepithelialilc1likenaturalkillercellsubsetproducesil13
AT sainiteeshmaddineni intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT krishnasharma intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT imranamohammad intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT alistairedruggierosherman intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT ivanstepanek intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT junehoshin intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT jenniferkbando intraepithelialilc1likenaturalkillercellsubsetproducesil13
AT johnbsunwoo intraepithelialilc1likenaturalkillercellsubsetproducesil13