IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis
Tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. A novel cancer metastasis pathway That tumorigenesis can be closely linked to an inflammatory microenvironment has been well established. In a new study,...
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| Veröffentlicht in: | Nature (London) Jg. 522; H. 7556; S. 345 - 348 |
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| Hauptverfasser: | , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
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London
Nature Publishing Group UK
18.06.2015
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| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
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| Abstract | Tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis.
A novel cancer metastasis pathway
That tumorigenesis can be closely linked to an inflammatory microenvironment has been well established. In a new study, Karin de Visser and colleagues estimate the more systemic inflammatory effects observed in a mouse model of breast cancer. They find that interleukin (IL)-1β expression in tumours elicits IL-17 expression in γδ T cells at a local level, which through granulocyte colony-stimulating factor production promotes systemic accumulation of neutrophils in multiple organs. Interfering with this cascade of events, for example at the level of neutrophil activation, reduces lung and lymph node metastases in this breast cancer model. These findings illustrate the perhaps wider than anticipated systemic effects elicited by localized tumours, at the same time offering multiple points of potential therapeutic interference.
Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal interactions between cancer cells and their microenvironment. Within this local microenvironment and in distant organs, immune cells and their mediators are known to facilitate metastasis formation
1
,
2
. However, the precise contribution of tumour-induced systemic inflammation to metastasis and the mechanisms regulating systemic inflammation are poorly understood. Here we show that tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. We mechanistically demonstrate that interleukin (IL)-1β elicits IL-17 expression from gamma delta (γδ) T cells, resulting in systemic, granulocyte colony-stimulating factor (G-CSF)-dependent expansion and polarization of neutrophils in mice bearing mammary tumours. Tumour-induced neutrophils acquire the ability to suppress cytotoxic T lymphocytes carrying the CD8 antigen, which limit the establishment of metastases. Neutralization of IL-17 or G-CSF and absence of γδ T cells prevents neutrophil accumulation and downregulates the T-cell-suppressive phenotype of neutrophils. Moreover, the absence of γδ T cells or neutrophils profoundly reduces pulmonary and lymph node metastases without influencing primary tumour progression. Our data indicate that targeting this novel cancer-cell-initiated domino effect within the immune system—the γδ T cell/IL-17/neutrophil axis—represents a new strategy to inhibit metastatic disease. |
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| AbstractList | Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal interactions between cancer cells and their microenvironment. Within this local microenvironment and in distant organs, immune cells and their mediators are known to facilitate metastasis formation. However, the precise contribution of tumour-induced systemic inflammation to metastasis and the mechanisms regulating systemic inflammation are poorly understood. Here we show that tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. We mechanistically demonstrate that interleukin (IL)-1β elicits IL-17 expression from gamma delta (γδ) T cells, resulting in systemic, granulocyte colony-stimulating factor (G-CSF)-dependent expansion and polarization of neutrophils in mice bearing mammary tumours. Tumour-induced neutrophils acquire the ability to suppress cytotoxic T lymphocytes carrying the CD8 antigen, which limit the establishment of metastases. Neutralization of IL-17 or G-CSF and absence of γδ T cells prevents neutrophil accumulation and downregulates the T-cell-suppressive phenotype of neutrophils. Moreover, the absence of γδ T cells or neutrophils profoundly reduces pulmonary and lymph node metastases without influencing primary tumour progression. Our data indicate that targeting this novel cancer-cell-initiated domino effect within the immune system--the γδ T cell/IL-17/neutrophil axis--represents a new strategy to inhibit metastatic disease.Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal interactions between cancer cells and their microenvironment. Within this local microenvironment and in distant organs, immune cells and their mediators are known to facilitate metastasis formation. However, the precise contribution of tumour-induced systemic inflammation to metastasis and the mechanisms regulating systemic inflammation are poorly understood. Here we show that tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. We mechanistically demonstrate that interleukin (IL)-1β elicits IL-17 expression from gamma delta (γδ) T cells, resulting in systemic, granulocyte colony-stimulating factor (G-CSF)-dependent expansion and polarization of neutrophils in mice bearing mammary tumours. Tumour-induced neutrophils acquire the ability to suppress cytotoxic T lymphocytes carrying the CD8 antigen, which limit the establishment of metastases. Neutralization of IL-17 or G-CSF and absence of γδ T cells prevents neutrophil accumulation and downregulates the T-cell-suppressive phenotype of neutrophils. Moreover, the absence of γδ T cells or neutrophils profoundly reduces pulmonary and lymph node metastases without influencing primary tumour progression. Our data indicate that targeting this novel cancer-cell-initiated domino effect within the immune system--the γδ T cell/IL-17/neutrophil axis--represents a new strategy to inhibit metastatic disease. Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal interactions between cancer cells and their microenvironment. Within this local microenvironment and in distant organs, immune cells and their mediators are known to facilitate metastasis formation. However, the precise contribution of tumour-induced systemic inflammation to metastasis and the mechanisms regulating systemic inflammation are poorly understood. Here we show that tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. We mechanistically demonstrate that interleukin (IL)-1β elicits IL-17 expression from gamma delta (γδ) T cells, resulting in systemic, granulocyte colony-stimulating factor (G-CSF)-dependent expansion and polarization of neutrophils in mice bearing mammary tumours. Tumour-induced neutrophils acquire the ability to suppress cytotoxic T lymphocytes carrying the CD8 antigen, which limit the establishment of metastases. Neutralization of IL-17 or G-CSF and absence of γδ T cells prevents neutrophil accumulation and downregulates the T-cell-suppressive phenotype of neutrophils. Moreover, the absence of γδ T cells or neutrophils profoundly reduces pulmonary and lymph node metastases without influencing primary tumour progression. Our data indicate that targeting this novel cancer-cell-initiated domino effect within the immune system--the γδ T cell/IL-17/neutrophil axis--represents a new strategy to inhibit metastatic disease. Tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. A novel cancer metastasis pathway That tumorigenesis can be closely linked to an inflammatory microenvironment has been well established. In a new study, Karin de Visser and colleagues estimate the more systemic inflammatory effects observed in a mouse model of breast cancer. They find that interleukin (IL)-1β expression in tumours elicits IL-17 expression in γδ T cells at a local level, which through granulocyte colony-stimulating factor production promotes systemic accumulation of neutrophils in multiple organs. Interfering with this cascade of events, for example at the level of neutrophil activation, reduces lung and lymph node metastases in this breast cancer model. These findings illustrate the perhaps wider than anticipated systemic effects elicited by localized tumours, at the same time offering multiple points of potential therapeutic interference. Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal interactions between cancer cells and their microenvironment. Within this local microenvironment and in distant organs, immune cells and their mediators are known to facilitate metastasis formation 1 , 2 . However, the precise contribution of tumour-induced systemic inflammation to metastasis and the mechanisms regulating systemic inflammation are poorly understood. Here we show that tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis. We mechanistically demonstrate that interleukin (IL)-1β elicits IL-17 expression from gamma delta (γδ) T cells, resulting in systemic, granulocyte colony-stimulating factor (G-CSF)-dependent expansion and polarization of neutrophils in mice bearing mammary tumours. Tumour-induced neutrophils acquire the ability to suppress cytotoxic T lymphocytes carrying the CD8 antigen, which limit the establishment of metastases. Neutralization of IL-17 or G-CSF and absence of γδ T cells prevents neutrophil accumulation and downregulates the T-cell-suppressive phenotype of neutrophils. Moreover, the absence of γδ T cells or neutrophils profoundly reduces pulmonary and lymph node metastases without influencing primary tumour progression. Our data indicate that targeting this novel cancer-cell-initiated domino effect within the immune system—the γδ T cell/IL-17/neutrophil axis—represents a new strategy to inhibit metastatic disease. |
| Author | Kersten, Kelly Coffelt, Seth B. Ciampricotti, Metamia Jonkers, Jos Vrijland, Kim Hau, Cheei-Sing Weiden, Jorieke Hawinkels, Lukas J. A. C. de Visser, Karin E. Doornebal, Chris W. Verstegen, Niels J. M. |
| Author_xml | – sequence: 1 givenname: Seth B. surname: Coffelt fullname: Coffelt, Seth B. organization: Division of Immunology, Netherlands Cancer Institute – sequence: 2 givenname: Kelly surname: Kersten fullname: Kersten, Kelly organization: Division of Immunology, Netherlands Cancer Institute – sequence: 3 givenname: Chris W. surname: Doornebal fullname: Doornebal, Chris W. organization: Division of Immunology, Netherlands Cancer Institute – sequence: 4 givenname: Jorieke surname: Weiden fullname: Weiden, Jorieke organization: Division of Immunology, Netherlands Cancer Institute – sequence: 5 givenname: Kim surname: Vrijland fullname: Vrijland, Kim organization: Division of Immunology, Netherlands Cancer Institute – sequence: 6 givenname: Cheei-Sing surname: Hau fullname: Hau, Cheei-Sing organization: Division of Immunology, Netherlands Cancer Institute – sequence: 7 givenname: Niels J. M. surname: Verstegen fullname: Verstegen, Niels J. M. organization: Division of Immunology, Netherlands Cancer Institute – sequence: 8 givenname: Metamia surname: Ciampricotti fullname: Ciampricotti, Metamia organization: Division of Immunology, Netherlands Cancer Institute – sequence: 9 givenname: Lukas J. A. C. surname: Hawinkels fullname: Hawinkels, Lukas J. A. C. organization: Department of Molecular Cell Biology, Leiden University Medical Center, Centre for Biomedical Genetics, Leiden University Medical Center – sequence: 10 givenname: Jos surname: Jonkers fullname: Jonkers, Jos organization: Division of Molecular Pathology, Netherlands Cancer Institute – sequence: 11 givenname: Karin E. surname: de Visser fullname: de Visser, Karin E. email: k.d.visser@nki.nl organization: Division of Immunology, Netherlands Cancer Institute |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25822788$$D View this record in MEDLINE/PubMed |
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| Snippet | Tumours maximize their chance of metastasizing by evoking a systemic inflammatory cascade in mouse models of spontaneous breast cancer metastasis.
A novel... Metastatic disease remains the primary cause of death for patients with breast cancer. The different steps of the metastatic cascade rely on reciprocal... |
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| Title | IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis |
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