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Cancer Immunology Research
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Inflammation-Induced Abnormal Expression of Self-molecules on Epithelial Cells: Targets for Tumor Immunoprevention

Camille Jacqueline, Amanda Lee, Nolan Frey, Jonathan S. Minden and Olivera J. Finn
Camille Jacqueline
1Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.
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Amanda Lee
2Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania.
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  • ORCID record for Amanda Lee
Nolan Frey
2Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania.
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Jonathan S. Minden
2Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania.
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Olivera J. Finn
1Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.
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  • For correspondence: ojfinn@pitt.edu
DOI: 10.1158/2326-6066.CIR-19-0870 Published August 2020
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Abstract

Tumor-associated antigens (TAA) are self-molecules abnormally expressed on tumor cells, which elicit humoral and cellular immunity and are targets of immunosurveillance. Immunity to TAAs is found in some healthy individuals with no history of cancer and correlates positively with a history of acute inflammatory and infectious events and cancer risk reduction. This suggests a potential role in cancer immunosurveillance for the immune memory elicited against disease-associated antigens (DAA) expressed on infected and inflamed tissues that are later recognized on tumors as TAAs. To understand probable sources for DAA generation, we investigated in vitro the role of inflammation that accompanies both infection and carcinogenesis. After exposure of normal primary breast epithelial cells to proinflammatory cytokines IL1β, IL6, and TNFα, or macrophages producing these cytokines, we saw transient overexpression of well-known TAAs, carcinoembryonic antigen and Her-2/neu, and overexpression and hypoglycosylation of MUC1. We documented inflammation-induced changes in the global cellular proteome by 2D difference gel electrophoresis combined with mass spectrometry and identified seven new DAAs. Through gene profiling, we showed that the cytokine treatment activated NF-κB and transcription of the identified DAAs. We tested three in vitro–identified DAAs, Serpin B1, S100A9, and SOD2, and found them overexpressed in premalignant and malignant breast tissues as well as in inflammatory conditions of the colon, stomach, and liver. This new category of TAAs, which are also DAAs, represent a potentially large number of predictable, shared, immunogenic, and safe antigens to use in preventative cancer vaccines and as targets for cancer therapies.

Footnotes

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

  • Cancer Immunol Res 2020;8:1027–38

  • Received November 4, 2019.
  • Revision received March 11, 2020.
  • Accepted May 22, 2020.
  • Published first May 28, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Immunology Research: 8 (8)
August 2020
Volume 8, Issue 8
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Inflammation-Induced Abnormal Expression of Self-molecules on Epithelial Cells: Targets for Tumor Immunoprevention
Camille Jacqueline, Amanda Lee, Nolan Frey, Jonathan S. Minden and Olivera J. Finn
Cancer Immunol Res August 1 2020 (8) (8) 1027-1038; DOI: 10.1158/2326-6066.CIR-19-0870

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Inflammation-Induced Abnormal Expression of Self-molecules on Epithelial Cells: Targets for Tumor Immunoprevention
Camille Jacqueline, Amanda Lee, Nolan Frey, Jonathan S. Minden and Olivera J. Finn
Cancer Immunol Res August 1 2020 (8) (8) 1027-1038; DOI: 10.1158/2326-6066.CIR-19-0870
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