Cancer-Specific Loss of p53 Leads to a Modulation of Myeloid and T Cell Responses
Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the...
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| Vydané v: | Cell reports (Cambridge) Ročník 30; číslo 2; s. 481 - 496.e6 |
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| Hlavní autori: | , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
Elsevier Inc
14.01.2020
Cell Press Elsevier |
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| ISSN: | 2211-1247, 2211-1247 |
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| Abstract | Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance.
[Display omitted]
•Tumor-specific loss of p53 delays tumor rejection in immune-competent hosts•p53 loss increases myeloid infiltration through enhanced cytokine secretion•The increase in Treg cells in response to loss of p53 is independent of Kras mutation•Kras mutations coordinate with p53 loss to regulate myeloid recruitment
TP53 is one of the most frequently mutated genes in cancer; however, its significance in controlling tumor-immune crosstalk is not fully understood. Blagih et al. highlight a key role for tumor-associated loss of p53, a common oncogenic event, in regulating myeloid and T cell responses. |
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| AbstractList | Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance.
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Tumor-specific loss of p53 delays tumor rejection in immune-competent hosts
•
p53 loss increases myeloid infiltration through enhanced cytokine secretion
•
The increase in Treg cells in response to loss of p53 is independent of Kras mutation
•
Kras mutations coordinate with p53 loss to regulate myeloid recruitment
TP53 is one of the most frequently mutated genes in cancer; however, its significance in controlling tumor-immune crosstalk is not fully understood. Blagih et al. highlight a key role for tumor-associated loss of p53, a common oncogenic event, in regulating myeloid and T cell responses. Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance.Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance. Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance. : TP53 is one of the most frequently mutated genes in cancer; however, its significance in controlling tumor-immune crosstalk is not fully understood. Blagih et al. highlight a key role for tumor-associated loss of p53, a common oncogenic event, in regulating myeloid and T cell responses. Keywords: p53, Kras, tumor, myeloid cells, T cell response Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4 T helper 1 (Th1) and CD8 T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance. Loss of p53 function contributes to the development of many cancers. While cell-autonomous consequences of p53 mutation have been studied extensively, the role of p53 in regulating the anti-tumor immune response is still poorly understood. Here, we show that loss of p53 in cancer cells modulates the tumor-immune landscape to circumvent immune destruction. Deletion of p53 promotes the recruitment and instruction of suppressive myeloid CD11b+ cells, in part through increased expression of CXCR3/CCR2-associated chemokines and macrophage colony-stimulating factor (M-CSF), and attenuates the CD4+ T helper 1 (Th1) and CD8+ T cell responses in vivo. p53-null tumors also show an accumulation of suppressive regulatory T (Treg) cells. Finally, we show that two key drivers of tumorigenesis, activation of KRAS and deletion of p53, cooperate to promote immune tolerance. [Display omitted] •Tumor-specific loss of p53 delays tumor rejection in immune-competent hosts•p53 loss increases myeloid infiltration through enhanced cytokine secretion•The increase in Treg cells in response to loss of p53 is independent of Kras mutation•Kras mutations coordinate with p53 loss to regulate myeloid recruitment TP53 is one of the most frequently mutated genes in cancer; however, its significance in controlling tumor-immune crosstalk is not fully understood. Blagih et al. highlight a key role for tumor-associated loss of p53, a common oncogenic event, in regulating myeloid and T cell responses. |
| Author | Gronroos, Eva Zani, Fabio Hobor, Sebastijan Vousden, Karen H. Pilley, Steven Morton, Jennifer P. Swanton, Charles Walton, Josephine B. Chakravarty, Probir Hock, Andreas K. Blyth, Karen Blagih, Julianna Mason, Susan Yang, Ming McNeish, Iain Hennequart, Marc |
| AuthorAffiliation | 4 Discovery Sciences, R&D BioPharmaceuticals, AstraZeneca, Cambridge CB4 0WG, UK 5 Ovarian Cancer Action Research Centre, Department of Surgery and Cancer, Imperial College London, London W12 0NN, UK 2 Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK 3 Institute of Cancer Sciences, University of Glasgow, Garscube Estate, Glasgow G61 1QH, UK 1 The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK |
| AuthorAffiliation_xml | – name: 1 The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – name: 5 Ovarian Cancer Action Research Centre, Department of Surgery and Cancer, Imperial College London, London W12 0NN, UK – name: 2 Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK – name: 4 Discovery Sciences, R&D BioPharmaceuticals, AstraZeneca, Cambridge CB4 0WG, UK – name: 3 Institute of Cancer Sciences, University of Glasgow, Garscube Estate, Glasgow G61 1QH, UK |
| Author_xml | – sequence: 1 givenname: Julianna surname: Blagih fullname: Blagih, Julianna organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 2 givenname: Fabio surname: Zani fullname: Zani, Fabio organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 3 givenname: Probir surname: Chakravarty fullname: Chakravarty, Probir organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 4 givenname: Marc surname: Hennequart fullname: Hennequart, Marc organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 5 givenname: Steven surname: Pilley fullname: Pilley, Steven organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 6 givenname: Sebastijan surname: Hobor fullname: Hobor, Sebastijan organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 7 givenname: Andreas K. surname: Hock fullname: Hock, Andreas K. organization: Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK – sequence: 8 givenname: Josephine B. surname: Walton fullname: Walton, Josephine B. organization: Institute of Cancer Sciences, University of Glasgow, Garscube Estate, Glasgow G61 1QH, UK – sequence: 9 givenname: Jennifer P. surname: Morton fullname: Morton, Jennifer P. organization: Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK – sequence: 10 givenname: Eva surname: Gronroos fullname: Gronroos, Eva organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 11 givenname: Susan surname: Mason fullname: Mason, Susan organization: Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK – sequence: 12 givenname: Ming surname: Yang fullname: Yang, Ming organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 13 givenname: Iain surname: McNeish fullname: McNeish, Iain organization: Institute of Cancer Sciences, University of Glasgow, Garscube Estate, Glasgow G61 1QH, UK – sequence: 14 givenname: Charles surname: Swanton fullname: Swanton, Charles organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK – sequence: 15 givenname: Karen surname: Blyth fullname: Blyth, Karen organization: Cancer Research UK Beatson Institute, Switchback Road, Glasgow G61 1BD, UK – sequence: 16 givenname: Karen H. surname: Vousden fullname: Vousden, Karen H. email: karen.vousden@crick.ac.uk organization: The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31940491$$D View this record in MEDLINE/PubMed |
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| Keywords | Kras myeloid cells tumor T cell response p53 |
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