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Translational Cancer Mechanisms and Therapy

Comparative Genomics Reveals Distinct Immune-oncologic Pathways in African American Men with Prostate Cancer

Shivanshu Awasthi, Anders Berglund, Julieta Abraham-Miranda, Robert J. Rounbehler, Kevin Kensler, Amparo Serna, Adriana Vidal, Sungyong You, Michael R. Freeman, Elai Davicioni, Yang Liu, R. Jeffrey Karnes, Eric A. Klein, Robert B. Den, Bruce J. Trock, Joshua D. Campbell, David J. Einstein, Raavi Gupta, Steven Balk, Priti Lal, Jong Y. Park, John L. Cleveland, Timothy R. Rebbeck, Stephen J. Freedland and Kosj Yamoah
Shivanshu Awasthi
1Department of Cancer Epidemiology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Anders Berglund
2Department of Biostatistics and Bioinformatics, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Julieta Abraham-Miranda
1Department of Cancer Epidemiology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Robert J. Rounbehler
3Department of Tumor Biology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Kevin Kensler
4Dana-Farber Cancer Institute and Harvard TH Chan School of Public Health, Boston, Massachusetts.
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Amparo Serna
1Department of Cancer Epidemiology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Adriana Vidal
5Cedar-Sinai Medical Center, Los Angeles, California.
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Sungyong You
5Cedar-Sinai Medical Center, Los Angeles, California.
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Michael R. Freeman
5Cedar-Sinai Medical Center, Los Angeles, California.
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Elai Davicioni
6Decipher Bioscience, Inc, Vancouver, British Columbia, Canada.
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Yang Liu
6Decipher Bioscience, Inc, Vancouver, British Columbia, Canada.
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R. Jeffrey Karnes
7Department of Urology, Mayo Clinic, Rochester, Minnesota.
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Eric A. Klein
8Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio.
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Robert B. Den
9Thomas Jefferson University, Philadelphia, Pennsylvania.
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Bruce J. Trock
10Department of Epidemiology, Johns Hopkins School of Medicine, Baltimore, Maryland.
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Joshua D. Campbell
11Department of Computational Biomedicine, Boston University, Boston, Massachusetts.
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David J. Einstein
12Beth Israel Deaconess Medical Center, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Raavi Gupta
13Department of Pathology, SUNY Downstate Health Sciences University, Brooklyn, New York.
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Steven Balk
12Beth Israel Deaconess Medical Center, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Priti Lal
14Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
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Jong Y. Park
1Department of Cancer Epidemiology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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John L. Cleveland
3Department of Tumor Biology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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Timothy R. Rebbeck
4Dana-Farber Cancer Institute and Harvard TH Chan School of Public Health, Boston, Massachusetts.
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Stephen J. Freedland
5Cedar-Sinai Medical Center, Los Angeles, California.
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Kosj Yamoah
1Department of Cancer Epidemiology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
15Department of Radiation Oncology, H Lee Moffitt Cancer Center & Research Institutes, Tampa, Florida.
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  • For correspondence: kosj.yamoah@moffitt.org
DOI: 10.1158/1078-0432.CCR-20-2925 Published January 2021
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Abstract

Purpose: The role of immune-oncologic mechanisms of racial disparities in prostate cancer remains understudied. Limited research exists to evaluate the molecular underpinnings of immune differences in African American men (AAM) and European American men (EAM) prostate tumor microenvironment (TME).

Experimental Design: A total of 1,173 radiation-naïve radical prostatectomy samples with whole transcriptome data from the Decipher GRID registry were used. Transcriptomic expressions of 1,260 immune-specific genes were selected to assess immune-oncologic differences between AAM and EAM prostate tumors. Race-specific differential expression of genes was assessed using a rank test, and intergene correlational matrix and gene set enrichment was used for pathway analysis.

Results: AAM prostate tumors have significant enrichment of major immune-oncologic pathways, including proinflammatory cytokines, IFNα, IFNγ, TNFα signaling, ILs, and epithelial–mesenchymal transition. AAM TME has higher total immune content score (ICSHIGH) compared with 0 (37.8% vs. 21.9%, P = 0.003). AAM tumors also have lower DNA damage repair and are genomically radiosensitive as compared with EAM. IFITM3 (IFN-inducible transmembrane protein 3) was one of the major proinflammatory genes overexpressed in AAM that predicted increased risk of biochemical recurrence selectively for AAM in both discovery [HRAAM = 2.30; 95% confidence interval (CI), 1.21–4.34; P = 0.01] and validation (HRAAM = 2.42; 95% CI, 1.52–3.86; P = 0.0001) but not in EAM.

Conclusions: Prostate tumors of AAM manifest a unique immune repertoire and have significant enrichment of proinflammatory immune pathways that are associated with poorer outcomes. Observed immune-oncologic differences can aid in a genomically adaptive approach to treating prostate cancer in AAM.

Footnotes

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

  • Clin Cancer Res 2021;27:320–9

  • Received July 26, 2020.
  • Revision received September 2, 2020.
  • Accepted October 6, 2020.
  • Published first October 9, 2020.
  • ©2020 American Association for Cancer Research.
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Clinical Cancer Research: 27 (1)
January 2021
Volume 27, Issue 1
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Comparative Genomics Reveals Distinct Immune-oncologic Pathways in African American Men with Prostate Cancer
Shivanshu Awasthi, Anders Berglund, Julieta Abraham-Miranda, Robert J. Rounbehler, Kevin Kensler, Amparo Serna, Adriana Vidal, Sungyong You, Michael R. Freeman, Elai Davicioni, Yang Liu, R. Jeffrey Karnes, Eric A. Klein, Robert B. Den, Bruce J. Trock, Joshua D. Campbell, David J. Einstein, Raavi Gupta, Steven Balk, Priti Lal, Jong Y. Park, John L. Cleveland, Timothy R. Rebbeck, Stephen J. Freedland and Kosj Yamoah
Clin Cancer Res January 1 2021 (27) (1) 320-329; DOI: 10.1158/1078-0432.CCR-20-2925

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Comparative Genomics Reveals Distinct Immune-oncologic Pathways in African American Men with Prostate Cancer
Shivanshu Awasthi, Anders Berglund, Julieta Abraham-Miranda, Robert J. Rounbehler, Kevin Kensler, Amparo Serna, Adriana Vidal, Sungyong You, Michael R. Freeman, Elai Davicioni, Yang Liu, R. Jeffrey Karnes, Eric A. Klein, Robert B. Den, Bruce J. Trock, Joshua D. Campbell, David J. Einstein, Raavi Gupta, Steven Balk, Priti Lal, Jong Y. Park, John L. Cleveland, Timothy R. Rebbeck, Stephen J. Freedland and Kosj Yamoah
Clin Cancer Res January 1 2021 (27) (1) 320-329; DOI: 10.1158/1078-0432.CCR-20-2925
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Clinical Cancer Research
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