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Cancer Immunology Research
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Research Articles

Impact of TCR Diversity on the Development of Transplanted or Chemically Induced Tumors

Karin Schreiber, Theodore G. Karrison, Steven P. Wolf, Kazuma Kiyotani, Madeline Steiner, Eric R. Littmann, Eric G. Pamer, Thomas Kammertoens, Hans Schreiber and Matthias Leisegang
Karin Schreiber
1Department of Pathology, The University of Chicago, Chicago, Illinois.
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Theodore G. Karrison
2Department of Public Health Sciences, The University of Chicago, Chicago, Illinois.
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Steven P. Wolf
1Department of Pathology, The University of Chicago, Chicago, Illinois.
3Institute of Immunology, Charité - Universitätsmedizin Berlin, Campus Buch, Berlin, Germany.
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Kazuma Kiyotani
4Cancer Precision Medicine Center, Japanese Foundation for Cancer Research, Tokyo, Japan.
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Madeline Steiner
1Department of Pathology, The University of Chicago, Chicago, Illinois.
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Eric R. Littmann
5Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York.
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Eric G. Pamer
5Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York.
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Thomas Kammertoens
3Institute of Immunology, Charité - Universitätsmedizin Berlin, Campus Buch, Berlin, Germany.
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Hans Schreiber
1Department of Pathology, The University of Chicago, Chicago, Illinois.
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  • For correspondence: hszz@uchicago.edu
Matthias Leisegang
3Institute of Immunology, Charité - Universitätsmedizin Berlin, Campus Buch, Berlin, Germany.
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DOI: 10.1158/2326-6066.CIR-19-0567 Published February 2020
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Abstract

Burnet postulated that the diversity of T-cell receptors (TCR) allows T cells to protect against the development of cancers that display antigens with a similar, seemingly endless diversity. To test this hypothesis, we developed a strategy in which a single breeding pair of mice gives rise to four groups of sibling mice. Three of the four groups had a similar number of CD8+ T cells, but TCR diversity was either broad, significantly reduced, or absent when expressing only one type of TCR. The fourth group had no T cells. All mice shared the same housing, and, therefore, their microbial environment was similar. Only slight differences in the intestinal flora were observed under these conditions. An undisturbed broad TCR repertoire was required for the rejection of inoculated cancers displaying the natural antigenic heterogeneity of primary tumors, whereas even one type of TCR was sufficient to protect against artificial cancers stably expressing cognate antigens. The three groups of mice with limited or no TCR repertoire showed an increased risk of developing primary tumors after chemical induction. However, the risk of early death or morbidity in these cohorts of mice was significantly higher than in mice with a diverse TCR repertoire, and it remains unknown whether mice with reduced TCR diversity, who died early without cancer, would have developed tumors with higher, lower, or equal probability after induction. Together, TCR diversity seems crucial to overcome the natural genetic instability of cancers and their antigenic heterogeneity, which impacts the design of cellular therapies.

Footnotes

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

  • Cancer Immunol Res 2020;8:192–202

  • Received July 31, 2019.
  • Revision received September 24, 2019.
  • Accepted December 6, 2019.
  • Published first December 12, 2019.
  • ©2019 American Association for Cancer Research.
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Cancer Immunology Research: 8 (2)
February 2020
Volume 8, Issue 2
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Impact of TCR Diversity on the Development of Transplanted or Chemically Induced Tumors
Karin Schreiber, Theodore G. Karrison, Steven P. Wolf, Kazuma Kiyotani, Madeline Steiner, Eric R. Littmann, Eric G. Pamer, Thomas Kammertoens, Hans Schreiber and Matthias Leisegang
Cancer Immunol Res February 1 2020 (8) (2) 192-202; DOI: 10.1158/2326-6066.CIR-19-0567

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Impact of TCR Diversity on the Development of Transplanted or Chemically Induced Tumors
Karin Schreiber, Theodore G. Karrison, Steven P. Wolf, Kazuma Kiyotani, Madeline Steiner, Eric R. Littmann, Eric G. Pamer, Thomas Kammertoens, Hans Schreiber and Matthias Leisegang
Cancer Immunol Res February 1 2020 (8) (2) 192-202; DOI: 10.1158/2326-6066.CIR-19-0567
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