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Programmed cell death-1 receptor mediated regulation of Tbet+ NK1.1- innate lymphoid cells within the tumor microenvironment

Programmed cell death-1 receptor mediated regulation of Tbet+ NK1.1- innate lymphoid cells within the tumor microenvironment
Programmed cell death-1 receptor mediated regulation of Tbet+ NK1.1- innate lymphoid cells within the tumor microenvironment
Innate Lymphoid Cells (ILCs) play a key role in tissue mediated immunity and can be controlled by co-receptor signaling. Here we define a subset of ILCs that are Tbet+NK1.1- and are present within the tumor microenvironment (TME). We show programmed death-1 receptor (PD-1) expression on ILCs within TME is found in Tbet+NK1.1-ILCs. PD-1 significantly controlled the proliferation and function of Tbet+NK1.1-ILCs in multiple murine and human tumors. We found tumor derived lactate enhanced PD-1 expression on Tbet+NK1.1-ILCs within the TME, which resulted in dampened mTOR signaling along with increased fatty acid uptake. In line with these metabolic changes, PD-1 deficient Tbet+NK1.1-ILCs expressed significantly increased IFN, granzyme B and K. Furthermore, PD-1 deficient Tbet+NK1.1- ILCs contributed towards diminished tumor growth in an experimental murine model of melanoma. These data demonstrate that PD-1 can regulate anti-tumor responses of Tbet+NK1.1-ILCs within the tumor microenvironment.
0027-8424
Lim, Jing Xuan
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Lai, Chester
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Mallett, Grace
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McDonald, David
cd408480-9dbb-4727-ae54-e52dae16d770
Hulme, Gillian
48e509ca-e104-4e18-a9cd-c0fc9f90828d
Laba, Stephanie
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Shapanis, Andrew
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Payne, Megan
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Patterson, Warren
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Alexander, Michael
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Coxhead, Jonathan
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Filby, Andrew
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Plummer, Ruth
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Lovat, Penny E.
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Sciume, Guiseppe
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Healy, Eugene
400fc04d-f81a-474a-ae25-7ff894be0ebd
Amarnath, Shoba
073e9bac-df55-4de7-bd62-2b6e1681222f
Lim, Jing Xuan
e173e9d7-3516-4ae7-a012-325d919b34ed
Lai, Chester
31e6848a-758b-45ba-8478-caa0acaa0398
Mallett, Grace
442724b1-958b-43fe-8033-3d4f05afc8f2
McDonald, David
cd408480-9dbb-4727-ae54-e52dae16d770
Hulme, Gillian
48e509ca-e104-4e18-a9cd-c0fc9f90828d
Laba, Stephanie
f74c5c6d-4ff4-4dc7-871a-7942db25d53c
Shapanis, Andrew
98b07884-92a9-4c00-afad-12194e339cbc
Payne, Megan
a2606e5b-2911-4b1d-9135-58b5b110a1aa
Patterson, Warren
c4accbff-83aa-4e57-baa0-fb68d840fe71
Alexander, Michael
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Coxhead, Jonathan
6776f622-7866-4670-a52a-8f30183a1633
Filby, Andrew
28aaba57-a559-4917-bda8-340ece5da4b5
Plummer, Ruth
03c83cc8-27d5-4b07-8058-fe391e873905
Lovat, Penny E.
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Sciume, Guiseppe
5482c9ba-1ac3-41be-aeee-28e6dc169b64
Healy, Eugene
400fc04d-f81a-474a-ae25-7ff894be0ebd
Amarnath, Shoba
073e9bac-df55-4de7-bd62-2b6e1681222f

Lim, Jing Xuan, Lai, Chester, Mallett, Grace, McDonald, David, Hulme, Gillian, Laba, Stephanie, Shapanis, Andrew, Payne, Megan, Patterson, Warren, Alexander, Michael, Coxhead, Jonathan, Filby, Andrew, Plummer, Ruth, Lovat, Penny E., Sciume, Guiseppe, Healy, Eugene and Amarnath, Shoba (2023) Programmed cell death-1 receptor mediated regulation of Tbet+ NK1.1- innate lymphoid cells within the tumor microenvironment. Proceedings of the National Academy of Sciences of the United States of America, 120 (18), [e2216587120]. (doi:10.1073/pnas.221658712).

Record type: Article

Abstract

Innate Lymphoid Cells (ILCs) play a key role in tissue mediated immunity and can be controlled by co-receptor signaling. Here we define a subset of ILCs that are Tbet+NK1.1- and are present within the tumor microenvironment (TME). We show programmed death-1 receptor (PD-1) expression on ILCs within TME is found in Tbet+NK1.1-ILCs. PD-1 significantly controlled the proliferation and function of Tbet+NK1.1-ILCs in multiple murine and human tumors. We found tumor derived lactate enhanced PD-1 expression on Tbet+NK1.1-ILCs within the TME, which resulted in dampened mTOR signaling along with increased fatty acid uptake. In line with these metabolic changes, PD-1 deficient Tbet+NK1.1-ILCs expressed significantly increased IFN, granzyme B and K. Furthermore, PD-1 deficient Tbet+NK1.1- ILCs contributed towards diminished tumor growth in an experimental murine model of melanoma. These data demonstrate that PD-1 can regulate anti-tumor responses of Tbet+NK1.1-ILCs within the tumor microenvironment.

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Accepted/In Press date: 7 March 2023
e-pub ahead of print date: 25 April 2023
Published date: 2 May 2023
Additional Information: Chester Lai is joint 1st author on this manuscript

Identifiers

Local EPrints ID: 483818
URI: http://eprints.soton.ac.uk/id/eprint/483818
ISSN: 0027-8424
PURE UUID: c7e387f9-3ad4-43c2-9b55-aafde9da5930
ORCID for Andrew Shapanis: ORCID iD orcid.org/0000-0003-4147-6956

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Date deposited: 06 Nov 2023 18:15
Last modified: 17 Mar 2024 03:58

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Contributors

Author: Jing Xuan Lim
Author: Chester Lai
Author: Grace Mallett
Author: David McDonald
Author: Gillian Hulme
Author: Stephanie Laba
Author: Andrew Shapanis ORCID iD
Author: Megan Payne
Author: Warren Patterson
Author: Michael Alexander
Author: Jonathan Coxhead
Author: Andrew Filby
Author: Ruth Plummer
Author: Penny E. Lovat
Author: Guiseppe Sciume
Author: Eugene Healy
Author: Shoba Amarnath

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