A2AR Adenosine Signaling Suppresses Natural Killer Cell Maturation in the Tumor Microenvironment
Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both g...
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| Published in | Cancer research (Chicago, Ill.) Vol. 78; no. 4; pp. 1003 - 1016 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Association for Cancer Research, Inc
15.02.2018
American Association for Cancer Research |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0008-5472 1538-7445 1538-7445 |
| DOI | 10.1158/0008-5472.CAN-17-2826 |
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| Abstract | Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell–specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell–based therapies may heighten therapeutic benefits by augmenting NK cell–mediated antitumor immunity.
Significance: Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. Cancer Res; 78(4); 1003–16. ©2017 AACR. |
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| AbstractList | Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell-specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell-based therapies may heighten therapeutic benefits by augmenting NK cell-mediated antitumor immunity.Significance: Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. Cancer Res; 78(4); 1003-16. ©2017 AACR.Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell-specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell-based therapies may heighten therapeutic benefits by augmenting NK cell-mediated antitumor immunity.Significance: Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. Cancer Res; 78(4); 1003-16. ©2017 AACR. Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth.Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell–specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell–based therapies may heighten therapeutic benefits by augmenting NK cell–mediated antitumor immunity.Significance: Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. Cancer Res; 78(4); 1003–16. ©2017 AACR. Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell-specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell-based therapies may heighten therapeutic benefits by augmenting NK cell-mediated antitumor immunity. Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. . Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here, we show that engagement of A2A adenosine receptor (A2AR) acts as a checkpoint that limits the maturation of natural killer (NK) cells. Both global and NK-cell–specific conditional deletion of A2AR enhanced proportions of terminally mature NK cells at homeostasis, following reconstitution, and in the tumor microenvironment. Notably, A2AR-deficient, terminally mature NK cells retained proliferative capacity and exhibited heightened reconstitution in competitive transfer assays. Moreover, targeting A2AR specifically on NK cells also improved tumor control and delayed tumor initiation. Taken together, our results establish A2AR-mediated adenosine signaling as an intrinsic negative regulator of NK-cell maturation and antitumor immune responses. On the basis of these findings, we propose that administering A2AR antagonists concurrently with NK cell–based therapies may heighten therapeutic benefits by augmenting NK cell–mediated antitumor immunity. Significance: Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth. Cancer Res; 78(4); 1003–16. ©2017 AACR. |
| Author | Barkauskas, Deborah S. Zitvogel, Laurence Waddell, Nicola Linden, Joel Souza-Fonseca-Guimaraes, Fernando Lin, Gene Gao, Yulong Degli-Esposti, Mariapia A. Young, Arabella Coudert, Jerome D. Vivier, Eric Ngiow, Shin Foong Huntington, Nicholas D. Smyth, Mark J. Messaoudene, Meriem Stannard, Kimberley A. Patch, Ann-Marie |
| Author_xml | – sequence: 1 givenname: Arabella surname: Young fullname: Young, Arabella – sequence: 2 givenname: Shin Foong surname: Ngiow fullname: Ngiow, Shin Foong – sequence: 3 givenname: Yulong surname: Gao fullname: Gao, Yulong – sequence: 4 givenname: Ann-Marie surname: Patch fullname: Patch, Ann-Marie – sequence: 5 givenname: Deborah S. surname: Barkauskas fullname: Barkauskas, Deborah S. – sequence: 6 givenname: Meriem surname: Messaoudene fullname: Messaoudene, Meriem – sequence: 7 givenname: Gene surname: Lin fullname: Lin, Gene – sequence: 8 givenname: Jerome D. surname: Coudert fullname: Coudert, Jerome D. – sequence: 9 givenname: Kimberley A. surname: Stannard fullname: Stannard, Kimberley A. – sequence: 10 givenname: Laurence surname: Zitvogel fullname: Zitvogel, Laurence – sequence: 11 givenname: Mariapia A. surname: Degli-Esposti fullname: Degli-Esposti, Mariapia A. – sequence: 12 givenname: Eric surname: Vivier fullname: Vivier, Eric – sequence: 13 givenname: Nicola surname: Waddell fullname: Waddell, Nicola – sequence: 14 givenname: Joel surname: Linden fullname: Linden, Joel – sequence: 15 givenname: Nicholas D. surname: Huntington fullname: Huntington, Nicholas D. – sequence: 16 givenname: Fernando surname: Souza-Fonseca-Guimaraes fullname: Souza-Fonseca-Guimaraes, Fernando – sequence: 17 givenname: Mark J. surname: Smyth fullname: Smyth, Mark J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29229601$$D View this record in MEDLINE/PubMed https://amu.hal.science/hal-02024322$$DView record in HAL |
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| Snippet | Extracellular adenosine is a key immunosuppressive metabolite that restricts activation of cytotoxic lymphocytes and impairs antitumor immune responses. Here,... Ablating adenosine signaling is found to promote natural killer cell maturation and antitumor immunity and reduce tumor growth.Extracellular adenosine is a key... |
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| SubjectTerms | Adenosine Antagonists Antitumor activity Cancer Cell activation Clonal deletion Cytotoxicity Homeostasis Immune response Immunosuppression Life Sciences Lymphocytes Maturation Natural killer cells T cell receptors |
| Title | A2AR Adenosine Signaling Suppresses Natural Killer Cell Maturation in the Tumor Microenvironment |
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