Breast and pancreatic cancer interrupt IRF8-dependent dendritic cell development to overcome immune surveillance

Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulat...

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Published inNature communications Vol. 9; no. 1; pp. 1250 - 19
Main Authors Meyer, Melissa A., Baer, John M., Knolhoff, Brett L., Nywening, Timothy M., Panni, Roheena Z., Su, Xinming, Weilbaecher, Katherine N., Hawkins, William G., Ma, Cynthia, Fields, Ryan C., Linehan, David C., Challen, Grant A., Faccio, Roberta, Aft, Rebecca L., DeNardo, David G.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 28.03.2018
Nature Publishing Group
Nature Portfolio
Subjects
13/1
13/105
13/106
13/109
13/21
13/31
13/51
14/63
38
38/61
45/88
631/250
631/250/232/2059
631/67/580
64/60
Animals
Antigens, CD - metabolism
Antigens, Surface - metabolism
Antineoplastic Agents - pharmacology
Bone marrow
Bone Marrow Cells - metabolism
Breast cancer
Breast Neoplasms - immunology
Breast Neoplasms - metabolism
CD103 antigen
CD8 antigen
CD8-Positive T-Lymphocytes - metabolism
Cell Differentiation
Cytokines - metabolism
Dendritic cells
Dendritic Cells - immunology
Dendritic Cells - metabolism
Disease Models, Animal
Female
Humanities and Social Sciences
Humans
Immunity
Immunologic Surveillance
Immunosuppression
Immunosurveillance
Immunotherapy
Integrin alpha Chains - metabolism
Interferon
Interferon regulatory factor
Interferon Regulatory Factors - metabolism
Leukocytes (granulocytic)
Lymphocytes T
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
multidisciplinary
Myeloid cells
Myelopoiesis
Oligonucleotide Array Sequence Analysis
Osteoprogenitor cells
Pancreatic cancer
Pancreatic Neoplasms - immunology
Pancreatic Neoplasms - metabolism
Rodents
Science
Science (multidisciplinary)
Stem Cells - metabolism
Surveillance
T cell receptors
T-Lymphocytes - immunology
Tumors
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Abstract Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulated that myelopoiesis might impact cDC development. The cDC subset, cDC1, which includes human CD141 + DCs and mouse CD103 + DCs, supports anti-tumor immunity by stimulating CD8 + T-cell responses. Here, to understand how cDC1 development changes during tumor progression, we investigated cDC bone marrow progenitors. We found localized breast and pancreatic cancers induce systemic decreases in cDC1s and their progenitors. Mechanistically, tumor-produced granulocyte-stimulating factor downregulates interferon regulatory factor-8 in cDC progenitors, and thus results in reduced cDC1 development. Tumor-induced reductions in cDC1 development impair anti-tumor CD8 + T-cell responses and correlate with poor patient outcomes. These data suggest immune surveillance can be impaired by tumor-induced alterations in cDC development. Tumors escape the immune system through many mechanisms. Here the authors show that certain tumors inhibit anti-tumor immunity by stopping the production of conventional dendritic cells (cDCs) in the bone marrow, therefore depleting the pool of cDCs available to present antigen to CD8 + T cells.
AbstractList Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulated that myelopoiesis might impact cDC development. The cDC subset, cDC1, which includes human CD141+ DCs and mouse CD103+ DCs, supports anti-tumor immunity by stimulating CD8+ T-cell responses. Here, to understand how cDC1 development changes during tumor progression, we investigated cDC bone marrow progenitors. We found localized breast and pancreatic cancers induce systemic decreases in cDC1s and their progenitors. Mechanistically, tumor-produced granulocyte-stimulating factor downregulates interferon regulatory factor-8 in cDC progenitors, and thus results in reduced cDC1 development. Tumor-induced reductions in cDC1 development impair anti-tumor CD8+ T-cell responses and correlate with poor patient outcomes. These data suggest immune surveillance can be impaired by tumor-induced alterations in cDC development.
Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulated that myelopoiesis might impact cDC development. The cDC subset, cDC1, which includes human CD141 + DCs and mouse CD103 + DCs, supports anti-tumor immunity by stimulating CD8 + T-cell responses. Here, to understand how cDC1 development changes during tumor progression, we investigated cDC bone marrow progenitors. We found localized breast and pancreatic cancers induce systemic decreases in cDC1s and their progenitors. Mechanistically, tumor-produced granulocyte-stimulating factor downregulates interferon regulatory factor-8 in cDC progenitors, and thus results in reduced cDC1 development. Tumor-induced reductions in cDC1 development impair anti-tumor CD8 + T-cell responses and correlate with poor patient outcomes. These data suggest immune surveillance can be impaired by tumor-induced alterations in cDC development. Tumors escape the immune system through many mechanisms. Here the authors show that certain tumors inhibit anti-tumor immunity by stopping the production of conventional dendritic cells (cDCs) in the bone marrow, therefore depleting the pool of cDCs available to present antigen to CD8 + T cells.
Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulated that myelopoiesis might impact cDC development. The cDC subset, cDC1, which includes human CD141 DCs and mouse CD103 DCs, supports anti-tumor immunity by stimulating CD8 T-cell responses. Here, to understand how cDC1 development changes during tumor progression, we investigated cDC bone marrow progenitors. We found localized breast and pancreatic cancers induce systemic decreases in cDC1s and their progenitors. Mechanistically, tumor-produced granulocyte-stimulating factor downregulates interferon regulatory factor-8 in cDC progenitors, and thus results in reduced cDC1 development. Tumor-induced reductions in cDC1 development impair anti-tumor CD8 T-cell responses and correlate with poor patient outcomes. These data suggest immune surveillance can be impaired by tumor-induced alterations in cDC development.
Tumors escape the immune system through many mechanisms. Here the authors show that certain tumors inhibit anti-tumor immunity by stopping the production of conventional dendritic cells (cDCs) in the bone marrow, therefore depleting the pool of cDCs available to present antigen to CD8+ T cells.
Abstract Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid cells can impair tumor immunity. As myeloid cells and conventional dendritic cells (cDCs) are derived from the same progenitors, we postulated that myelopoiesis might impact cDC development. The cDC subset, cDC1, which includes human CD141 + DCs and mouse CD103 + DCs, supports anti-tumor immunity by stimulating CD8 + T-cell responses. Here, to understand how cDC1 development changes during tumor progression, we investigated cDC bone marrow progenitors. We found localized breast and pancreatic cancers induce systemic decreases in cDC1s and their progenitors. Mechanistically, tumor-produced granulocyte-stimulating factor downregulates interferon regulatory factor-8 in cDC progenitors, and thus results in reduced cDC1 development. Tumor-induced reductions in cDC1 development impair anti-tumor CD8 + T-cell responses and correlate with poor patient outcomes. These data suggest immune surveillance can be impaired by tumor-induced alterations in cDC development.
ArticleNumber 1250
Author Panni, Roheena Z.
Baer, John M.
Knolhoff, Brett L.
Nywening, Timothy M.
Linehan, David C.
Aft, Rebecca L.
Weilbaecher, Katherine N.
Su, Xinming
DeNardo, David G.
Fields, Ryan C.
Meyer, Melissa A.
Challen, Grant A.
Faccio, Roberta
Ma, Cynthia
Hawkins, William G.
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  organization: Department of Medicine, Washington University School of Medicine
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  surname: Nywening
  fullname: Nywening, Timothy M.
  organization: Department of Surgery, Washington University School of Medicine
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  givenname: Xinming
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  organization: Department of Medicine, Washington University School of Medicine
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  surname: Ma
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  organization: Department of Medicine, Washington University School of Medicine, Siteman Cancer Center, Washington University School of Medicine
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  surname: Fields
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  organization: Department of Surgery, Washington University School of Medicine, Siteman Cancer Center, Washington University School of Medicine
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  givenname: Rebecca L.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29593283$$D View this record in MEDLINE/PubMed
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SSID ssj0000391844
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Snippet Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of immunosuppressive myeloid...
Abstract Tumors employ multiple mechanisms to evade immune surveillance. One mechanism is tumor-induced myelopoiesis, whereby the expansion of...
Tumors escape the immune system through many mechanisms. Here the authors show that certain tumors inhibit anti-tumor immunity by stopping the production of...
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Animals
Antigens, CD - metabolism
Antigens, Surface - metabolism
Antineoplastic Agents - pharmacology
Bone marrow
Bone Marrow Cells - metabolism
Breast cancer
Breast Neoplasms - immunology
Breast Neoplasms - metabolism
CD103 antigen
CD8 antigen
CD8-Positive T-Lymphocytes - metabolism
Cell Differentiation
Cytokines - metabolism
Dendritic cells
Dendritic Cells - immunology
Dendritic Cells - metabolism
Disease Models, Animal
Female
Humanities and Social Sciences
Humans
Immunity
Immunologic Surveillance
Immunosuppression
Immunosurveillance
Immunotherapy
Integrin alpha Chains - metabolism
Interferon
Interferon regulatory factor
Interferon Regulatory Factors - metabolism
Leukocytes (granulocytic)
Lymphocytes T
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
multidisciplinary
Myeloid cells
Myelopoiesis
Oligonucleotide Array Sequence Analysis
Osteoprogenitor cells
Pancreatic cancer
Pancreatic Neoplasms - immunology
Pancreatic Neoplasms - metabolism
Rodents
Science
Science (multidisciplinary)
Stem Cells - metabolism
Surveillance
T cell receptors
T-Lymphocytes - immunology
Tumors
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Title Breast and pancreatic cancer interrupt IRF8-dependent dendritic cell development to overcome immune surveillance
URI https://link.springer.com/article/10.1038/s41467-018-03600-6
https://www.ncbi.nlm.nih.gov/pubmed/29593283
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https://search.proquest.com/docview/2019812056
https://pubmed.ncbi.nlm.nih.gov/PMC5871846
https://doaj.org/article/8ebabe15d49943d1834201842048ea26
Volume 9
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