Rapid functional impairment of natural killer cells following tumor entry limits anti-tumor immunity

Isaac Dean(University of Birmingham), Colin Y.C. Lee(MRC Laboratory of Molecular Biology), Zewen Kelvin Tuong(MRC Laboratory of Molecular Biology), Zhi Li(University of Birmingham), Christopher A. Tibbitt(Karolinska Institutet), Claire Willis(University of Birmingham), Fabrina Gaspal(University of Birmingham), Bethany C. Kennedy(University of Birmingham), Veronika Matei‐Rascu(University of Birmingham), Rémi Fiancette(University of Birmingham), Caroline Nordenvall(Karolinska University Hospital), Ulrik Lindforss(Karolinska University Hospital), Syed Murtuza Baker(Manchester Academic Health Science Centre), Christian Stockmann, Veronika Sexl(University of Veterinary Medicine Vienna), Scott A. Hammond(AstraZeneca (United States)), Simon J. Dovedi(AstraZeneca (United Kingdom)), Jenny Mjösberg(Karolinska University Hospital), Matthew R. Hepworth(Manchester Academic Health Science Centre), Gianluca Carlesso(AstraZeneca (United States)), Menna R. Clatworthy(MRC Laboratory of Molecular Biology), David R. Withers(University of Birmingham)
Nature Communications
January 24, 2024
Cited by 158Open Access
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Abstract

Immune cell dysfunction within the tumor microenvironment (TME) undermines the control of cancer progression. Established tumors contain phenotypically distinct, tumor-specific natural killer (NK) cells; however, the temporal dynamics, mechanistic underpinning and functional significance of the NK cell compartment remains incompletely understood. Here, we use photo-labeling, combined with longitudinal transcriptomic and cellular analyses, to interrogate the fate of intratumoral NK cells. We reveal that NK cells rapidly lose effector functions and adopt a distinct phenotypic state with features associated with tissue residency. NK cell depletion from established tumors did not alter tumor growth, indicating that intratumoral NK cells cease to actively contribute to anti-tumor responses. IL-15 administration prevented loss of function and improved tumor control, generating intratumoral NK cells with both tissue-residency characteristics and enhanced effector function. Collectively, our data reveals the fate of NK cells after recruitment into tumors and provides insight into how their function may be revived.


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