CIS is a potent checkpoint in NK cell–mediated tumor immunity
IL-15-driven NK cells mediate anti-tumor immunity, but how IL-15 is negatively regulated remains unclear. Huntington and colleagues find that CIS, a member of the suppressor of cytokine signaling family, suppresses the response to IL-15 and, as a result, CIS-deficient mice are more resistant to canc...
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| Published in | Nature immunology Vol. 17; no. 7; pp. 816 - 824 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.07.2016
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | IL-15-driven NK cells mediate anti-tumor immunity, but how IL-15 is negatively regulated remains unclear. Huntington and colleagues find that CIS, a member of the suppressor of cytokine signaling family, suppresses the response to IL-15 and, as a result, CIS-deficient mice are more resistant to cancer metastasis.
The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by
Cish
) as a critical negative regulator of IL-15 signaling in NK cells.
Cish
was rapidly induced in response to IL-15, and deletion of
Cish
rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-γ production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which
Cish
was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation.
Cish
−/−
mice were resistant to melanoma, prostate and breast cancer metastasis
in vivo
, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell–mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. |
|---|---|
| AbstractList | The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-γ production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly,CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. [Cish.sup.-/-] mice were resistant to melanoma, prostate and breast cancer metastasis in vivo, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell-mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN- gamma production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. Cish super(-/-) mice were resistant to melanoma, prostate and breast cancer metastasis in vivo, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell-mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-γ production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. Cish(-/-) mice were resistant to melanoma, prostate and breast cancer metastasis in vivo, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell-mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-[gamma] production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. Cish[sup.-/-] mice were resistant to melanoma, prostate and breast cancer metastasis in vivo, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell-mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. IL-15-driven NK cells mediate anti-tumor immunity, but how IL-15 is negatively regulated remains unclear. Huntington and colleagues find that CIS, a member of the suppressor of cytokine signaling family, suppresses the response to IL-15 and, as a result, CIS-deficient mice are more resistant to cancer metastasis.The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-γ production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. Cish−/− mice were resistant to melanoma, prostate and breast cancer metastasis in vivo, and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell–mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. IL-15-driven NK cells mediate anti-tumor immunity, but how IL-15 is negatively regulated remains unclear. Huntington and colleagues find that CIS, a member of the suppressor of cytokine signaling family, suppresses the response to IL-15 and, as a result, CIS-deficient mice are more resistant to cancer metastasis. The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from cytokines such as IL-15. We identified cytokine-inducible SH2-containing protein (CIS, encoded by Cish ) as a critical negative regulator of IL-15 signaling in NK cells. Cish was rapidly induced in response to IL-15, and deletion of Cish rendered NK cells hypersensitive to IL-15, as evidenced by enhanced proliferation, survival, IFN-γ production and cytotoxicity toward tumors. This was associated with increased JAK-STAT signaling in NK cells in which Cish was deleted. Correspondingly, CIS interacted with the tyrosine kinase JAK1, inhibiting its enzymatic activity and targeting JAK for proteasomal degradation. Cish −/− mice were resistant to melanoma, prostate and breast cancer metastasis in vivo , and this was intrinsic to NK cell activity. Our data uncover a potent intracellular checkpoint in NK cell–mediated tumor immunity and suggest possibilities for new cancer immunotherapies directed at blocking CIS function. |
| Audience | Academic |
| Author | Shi, Wei Carotta, Sebastian Teh, Charis Rautela, Jai Smyth, Mark J Kolesnik, Tatiana B Sanvitale, Caroline E Babon, Jeffery J Putz, Eva M Belz, Gabrielle T Delconte, Rebecca B Ushiki, Takashi Degli-Esposti, Mariapia A Sharp, Phillip P Webb, Andrew I Infusini, Giuseppe Linossi, Edmond M Stannard, Kimberley Firth, Matt Nicholson, Sandra E Seillet, Cyril Huntington, Nicholas D Hutchinson, Dana S Alexander, Warren S Dagley, Laura F Zhang, Jian-Guo Gray, Daniel H D Burns, Christopher J Andoniou, Christopher E Li, Shawn S Bullock, Alex N Liau, Nicholas P D |
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Eva M orcidid: 0000-0002-9990-4477 surname: Putz fullname: Putz, Eva M organization: Immunology in Cancer and Infection Laboratory QIMR Berghofer Medical Research Institute – sequence: 7 givenname: Kimberley surname: Stannard fullname: Stannard, Kimberley organization: Immunology in Cancer and Infection Laboratory QIMR Berghofer Medical Research Institute – sequence: 8 givenname: Jian-Guo surname: Zhang fullname: Zhang, Jian-Guo organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 9 givenname: Charis surname: Teh fullname: Teh, Charis organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 10 givenname: Matt surname: Firth fullname: Firth, Matt organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 11 givenname: Takashi surname: Ushiki fullname: Ushiki, Takashi organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 12 givenname: Christopher E surname: Andoniou fullname: Andoniou, Christopher E organization: Immunology and Virology Program, Centre for Ophthalmology and Visual Science, The University of Western Australia and Centre for Experimental Immunology, Lions Eye Institute – sequence: 13 givenname: Mariapia A surname: Degli-Esposti fullname: Degli-Esposti, Mariapia A organization: Immunology and Virology Program, Centre for Ophthalmology and Visual Science, The University of Western Australia and Centre for Experimental Immunology, Lions Eye Institute – sequence: 14 givenname: Phillip P surname: Sharp fullname: Sharp, Phillip P organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 15 givenname: Caroline E surname: Sanvitale fullname: Sanvitale, Caroline E organization: Structural Genomics Consortium (SGC), University of Oxford – sequence: 16 givenname: Giuseppe surname: Infusini fullname: Infusini, Giuseppe organization: The Walter and Eliza Hall Institute of Medical Research – sequence: 17 givenname: Nicholas P D surname: Liau fullname: Liau, Nicholas P D organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 18 givenname: Edmond M surname: Linossi fullname: Linossi, Edmond M organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 19 givenname: Christopher J surname: Burns fullname: Burns, Christopher J organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 20 givenname: Sebastian surname: Carotta fullname: Carotta, Sebastian organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 21 givenname: Daniel H D surname: Gray fullname: Gray, Daniel H D organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 22 givenname: Cyril surname: Seillet fullname: Seillet, Cyril organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 23 givenname: Dana S surname: Hutchinson fullname: Hutchinson, Dana S organization: Monash Institute of Pharmaceutical Sciences, Monash University – sequence: 24 givenname: Gabrielle T surname: Belz fullname: Belz, Gabrielle T organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 25 givenname: Andrew I surname: Webb fullname: Webb, Andrew I organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 26 givenname: Warren S surname: Alexander fullname: Alexander, Warren S organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 27 givenname: Shawn S surname: Li fullname: Li, Shawn S organization: Department of Biochemistry and the Siebens-Drake Medical Research Institute, Schulich School of Medicine and Dentistry, University of Western Ontario – sequence: 28 givenname: Alex N orcidid: 0000-0001-6757-0436 surname: Bullock fullname: Bullock, Alex N organization: Structural Genomics Consortium (SGC), University of Oxford – sequence: 29 givenname: Jeffery J orcidid: 0000-0002-5408-6239 surname: Babon fullname: Babon, Jeffery J organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 30 givenname: Mark J surname: Smyth fullname: Smyth, Mark J organization: Immunology in Cancer and Infection Laboratory QIMR Berghofer Medical Research Institute, School of Medicine, University of Queensland – sequence: 31 givenname: Sandra E surname: Nicholson fullname: Nicholson, Sandra E email: snicholson@wehi.edu.au organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 32 givenname: Nicholas D orcidid: 0000-0002-5267-7211 surname: Huntington fullname: Huntington, Nicholas D email: huntington@wehi.edu.au organization: The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27213690$$D View this record in MEDLINE/PubMed |
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| Snippet | IL-15-driven NK cells mediate anti-tumor immunity, but how IL-15 is negatively regulated remains unclear. Huntington and colleagues find that CIS, a member of... The detection of aberrant cells by natural killer (NK) cells is controlled by the integration of signals from activating and inhibitory ligands and from... |
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| Title | CIS is a potent checkpoint in NK cell–mediated tumor immunity |
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