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Tumor Biology and Immunology

IL1 Receptor Antagonist Controls Transcriptional Signature of Inflammation in Patients with Metastatic Breast Cancer

Te-Chia Wu, Kangling Xu, Jan Martinek, Robyn R. Young, Romain Banchereau, Joshy George, Jacob Turner, Kyung In Kim, Sandra Zurawski, Xuan Wang, Derek Blankenship, Hannah M. Brookes, Florentina Marches, Gerlinde Obermoser, Elizabeth Lavecchio, Maren K. Levin, Sookyoung Bae, Cheng-Han Chung, Jennifer L. Smith, Alma-Martina Cepika, Kyp L. Oxley, George J. Snipes, Jacques Banchereau, Virginia Pascual, Joyce O'Shaughnessy and A. Karolina Palucka
Te-Chia Wu
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Kangling Xu
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Jan Martinek
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
3Department of Biomedical Studies, Baylor University, Waco, Texas.
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Robyn R. Young
4The Center for Cancer and Blood Disorders, Fort Worth, Texas.
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Romain Banchereau
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Joshy George
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Jacob Turner
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Kyung In Kim
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Sandra Zurawski
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Xuan Wang
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Derek Blankenship
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Hannah M. Brookes
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Florentina Marches
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Gerlinde Obermoser
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Elizabeth Lavecchio
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Maren K. Levin
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Sookyoung Bae
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Cheng-Han Chung
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
3Department of Biomedical Studies, Baylor University, Waco, Texas.
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Jennifer L. Smith
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Alma-Martina Cepika
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Kyp L. Oxley
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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George J. Snipes
5Baylor University Medical Center, Sammons Cancer Center, Dallas, Texas.
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Jacques Banchereau
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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Virginia Pascual
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
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Joyce O'Shaughnessy
6Baylor University Medical Center, Charles A. Sammons Cancer Center, Texas Oncology, Dallas, Texas.
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A. Karolina Palucka
1Baylor Institute for Immunology Research, Baylor Research Institute, Dallas, Texas.
2The Jackson Laboratory for Genomic Medicine, Farmington, Connecticut.
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  • For correspondence: karolina.palucka@jax.org
DOI: 10.1158/0008-5472.CAN-18-0413 Published September 2018
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Abstract

Inflammation affects tumor immune surveillance and resistance to therapy. Here, we show that production of IL1β in primary breast cancer tumors is linked with advanced disease and originates from tumor-infiltrating CD11c+ myeloid cells. IL1β production is triggered by cancer cell membrane–derived TGFβ. Neutralizing TGFβ or IL1 receptor prevents breast cancer progression in humanized mouse model. Patients with metastatic HER2− breast cancer display a transcriptional signature of inflammation in the blood leukocytes, which is attenuated after IL1 blockade. When present in primary breast cancer tumors, this signature discriminates patients with poor clinical outcomes in two independent public datasets (TCGA and METABRIC).

Significance: IL1β orchestrates tumor-promoting inflammation in breast cancer and can be targeted in patients using an IL1 receptor antagonist. Cancer Res; 78(18); 5243–58. ©2018 AACR.

See related commentary by Dinarello, p. 5200

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • J. O'Shaughnessy and A.K. Palucka are co-senior authors of this article.

  • Received February 7, 2018.
  • Revision received April 4, 2018.
  • Accepted May 11, 2018.
  • Published first July 16, 2018.
  • ©2018 American Association for Cancer Research.
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Cancer Research: 78 (18)
September 2018
Volume 78, Issue 18
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IL1 Receptor Antagonist Controls Transcriptional Signature of Inflammation in Patients with Metastatic Breast Cancer
Te-Chia Wu, Kangling Xu, Jan Martinek, Robyn R. Young, Romain Banchereau, Joshy George, Jacob Turner, Kyung In Kim, Sandra Zurawski, Xuan Wang, Derek Blankenship, Hannah M. Brookes, Florentina Marches, Gerlinde Obermoser, Elizabeth Lavecchio, Maren K. Levin, Sookyoung Bae, Cheng-Han Chung, Jennifer L. Smith, Alma-Martina Cepika, Kyp L. Oxley, George J. Snipes, Jacques Banchereau, Virginia Pascual, Joyce O'Shaughnessy and A. Karolina Palucka
Cancer Res September 15 2018 (78) (18) 5243-5258; DOI: 10.1158/0008-5472.CAN-18-0413

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IL1 Receptor Antagonist Controls Transcriptional Signature of Inflammation in Patients with Metastatic Breast Cancer
Te-Chia Wu, Kangling Xu, Jan Martinek, Robyn R. Young, Romain Banchereau, Joshy George, Jacob Turner, Kyung In Kim, Sandra Zurawski, Xuan Wang, Derek Blankenship, Hannah M. Brookes, Florentina Marches, Gerlinde Obermoser, Elizabeth Lavecchio, Maren K. Levin, Sookyoung Bae, Cheng-Han Chung, Jennifer L. Smith, Alma-Martina Cepika, Kyp L. Oxley, George J. Snipes, Jacques Banchereau, Virginia Pascual, Joyce O'Shaughnessy and A. Karolina Palucka
Cancer Res September 15 2018 (78) (18) 5243-5258; DOI: 10.1158/0008-5472.CAN-18-0413
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