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Cancer Immunology Research
Cancer Immunology Research

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Research Articles

Computational Immune Monitoring Reveals Abnormal Double-Negative T Cells Present across Human Tumor Types

Allison R. Greenplate, Daniel D. McClanahan, Brian K. Oberholtzer, Deon B. Doxie, Caroline E. Roe, Kirsten E. Diggins, Nalin Leelatian, Megan L. Rasmussen, Mark C. Kelley, Vivian Gama, Peter J. Siska, Jeffrey C. Rathmell, P. Brent Ferrell, Douglas B. Johnson and Jonathan M. Irish
Allison R. Greenplate
Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee.Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.
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Daniel D. McClanahan
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Brian K. Oberholtzer
Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Deon B. Doxie
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Caroline E. Roe
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Kirsten E. Diggins
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Nalin Leelatian
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Megan L. Rasmussen
Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Mark C. Kelley
Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee.
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Vivian Gama
Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.Vanderbilt Center for Stem Cell Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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Peter J. Siska
Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Internal Medicine III, University Hospital Regensburg, Regensburg, Germany.
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  • ORCID record for Peter J. Siska
Jeffrey C. Rathmell
Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee.Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Vanderbilt Center for Immunobiology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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P. Brent Ferrell
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee.
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Douglas B. Johnson
Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee.
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Jonathan M. Irish
Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, Tennessee.Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee.Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee.Vanderbilt Center for Immunobiology, Vanderbilt University School of Medicine, Nashville, Tennessee.
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  • For correspondence: jonathan.irish@vanderbilt.edu
DOI: 10.1158/2326-6066.CIR-17-0692 Published January 2019
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Abstract

Advances in single-cell biology have enabled measurements of >40 protein features on millions of immune cells within clinical samples. However, the data analysis steps following cell population identification are susceptible to bias, time-consuming, and challenging to compare across studies. Here, an ensemble of unsupervised tools was developed to evaluate four essential types of immune cell information, incorporate changes over time, and address diverse immune monitoring challenges. The four complementary properties characterized were (i) systemic plasticity, (ii) change in population abundance, (iii) change in signature population features, and (iv) novelty of cellular phenotype. Three systems immune monitoring studies were selected to challenge this ensemble approach. In serial biopsies of melanoma tumors undergoing targeted therapy, the ensemble approach revealed enrichment of double-negative (DN) T cells. Melanoma tumor-resident DN T cells were abnormal and phenotypically distinct from those found in nonmalignant lymphoid tissues, but similar to those found in glioblastoma and renal cell carcinoma. Overall, ensemble systems immune monitoring provided a robust, quantitative view of changes in both the system and cell subsets, allowed for transparent review by human experts, and revealed abnormal immune cells present across multiple human tumor types.

Footnotes

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

  • Received December 1, 2017.
  • Revision received July 17, 2018.
  • Accepted November 5, 2018.
  • Published first November 9, 2018.
  • ©2018 American Association for Cancer Research.
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Cancer Immunology Research: 7 (1)
January 2019
Volume 7, Issue 1
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Computational Immune Monitoring Reveals Abnormal Double-Negative T Cells Present across Human Tumor Types
Allison R. Greenplate, Daniel D. McClanahan, Brian K. Oberholtzer, Deon B. Doxie, Caroline E. Roe, Kirsten E. Diggins, Nalin Leelatian, Megan L. Rasmussen, Mark C. Kelley, Vivian Gama, Peter J. Siska, Jeffrey C. Rathmell, P. Brent Ferrell, Douglas B. Johnson and Jonathan M. Irish
Cancer Immunol Res January 1 2019 (7) (1) 86-99; DOI: 10.1158/2326-6066.CIR-17-0692

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Computational Immune Monitoring Reveals Abnormal Double-Negative T Cells Present across Human Tumor Types
Allison R. Greenplate, Daniel D. McClanahan, Brian K. Oberholtzer, Deon B. Doxie, Caroline E. Roe, Kirsten E. Diggins, Nalin Leelatian, Megan L. Rasmussen, Mark C. Kelley, Vivian Gama, Peter J. Siska, Jeffrey C. Rathmell, P. Brent Ferrell, Douglas B. Johnson and Jonathan M. Irish
Cancer Immunol Res January 1 2019 (7) (1) 86-99; DOI: 10.1158/2326-6066.CIR-17-0692
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