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Precision Medicine and Imaging

Autoantibody Landscape in Patients with Advanced Prostate Cancer

William S. Chen, Winston A. Haynes, Rebecca Waitz, Kathy Kamath, Agustin Vega-Crespo, Raunak Shrestha, Minlu Zhang, Adam Foye, Ignacio Baselga Carretero, Ivan Perez Garcilazo, Meng Zhang, Shuang G. Zhao, Martin Sjöström, David A. Quigley, Jonathan Chou, Tomasz M. Beer, Matthew Rettig, Martin Gleave, Christopher P. Evans, Primo Lara, Kim N. Chi, Robert E. Reiter, Joshi J. Alumkal, Alan Ashworth, Rahul Aggarwal, Eric J. Small, Patrick S. Daugherty, Antoni Ribas, David Y. Oh, John C. Shon and Felix Y. Feng
William S. Chen
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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Winston A. Haynes
3Serimmune, Inc. Santa Barbara, California.
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Rebecca Waitz
3Serimmune, Inc. Santa Barbara, California.
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Kathy Kamath
3Serimmune, Inc. Santa Barbara, California.
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  • ORCID record for Kathy Kamath
Agustin Vega-Crespo
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
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Raunak Shrestha
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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  • ORCID record for Raunak Shrestha
Minlu Zhang
3Serimmune, Inc. Santa Barbara, California.
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Adam Foye
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
5Department of Medicine, University of California San Francisco, San Francisco, California.
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Ignacio Baselga Carretero
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
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  • ORCID record for Ignacio Baselga Carretero
Ivan Perez Garcilazo
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
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Meng Zhang
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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Shuang G. Zhao
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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Martin Sjöström
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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  • ORCID record for Martin Sjöström
David A. Quigley
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
12Department of Urology, University of California San Francisco, San Francisco, California.
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Jonathan Chou
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
5Department of Medicine, University of California San Francisco, San Francisco, California.
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Tomasz M. Beer
6Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon.
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Matthew Rettig
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
7VA Greater Los Angeles Healthcare System, Los Angeles, California.
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Martin Gleave
8University of British Columbia, Vancouver, British Columbia, Canada.
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Christopher P. Evans
9University of California Davis, Davis, California.
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Primo Lara
9University of California Davis, Davis, California.
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Kim N. Chi
8University of British Columbia, Vancouver, British Columbia, Canada.
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Robert E. Reiter
10Department of Urology, University of California Los Angeles, Los Angeles, California.
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Joshi J. Alumkal
6Knight Cancer Institute, Oregon Health & Science University, Portland, Oregon.
11Department of Hematology and Oncology, University of Michigan, Ann Arbor, Michigan.
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Alan Ashworth
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
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Rahul Aggarwal
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
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Eric J. Small
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
5Department of Medicine, University of California San Francisco, San Francisco, California.
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Patrick S. Daugherty
3Serimmune, Inc. Santa Barbara, California.
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Antoni Ribas
4Division of Hematology and Oncology, University of California Los Angeles, Los Angeles, California.
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David Y. Oh
5Department of Medicine, University of California San Francisco, San Francisco, California.
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John C. Shon
3Serimmune, Inc. Santa Barbara, California.
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Felix Y. Feng
1Department of Radiation Oncology, University of California San Francisco, San Francisco, California.
2Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, California.
12Department of Urology, University of California San Francisco, San Francisco, California.
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  • For correspondence: Felix.Feng@ucsf.edu
DOI: 10.1158/1078-0432.CCR-20-1966 Published December 2020
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Abstract

Purpose: Autoantibody responses in cancer are of great interest, as they may be concordant with T-cell responses to cancer antigens or predictive of response to cancer immunotherapies. Thus, we sought to characterize the antibody landscape of metastatic castration-resistant prostate cancer (mCRPC).

Experimental Design: Serum antibody epitope repertoire analysis (SERA) was performed on patient serum to identify tumor-specific neoepitopes. Somatic mutation–specific neoepitopes were investigated by associating serum epitope enrichment scores with whole-genome sequencing results from paired solid tumor metastasis biopsies and germline blood samples. A protein-based immunome-wide association study (PIWAS) was performed to identify significantly enriched epitopes, and candidate serum antibodies enriched in select patients were validated by ELISA profiling. A distinct cohort of patients with melanoma was evaluated to validate the top cancer-specific epitopes.

Results: SERA was performed on 1,229 serum samples obtained from 72 men with mCRPC and 1,157 healthy control patients. Twenty-nine of 6,636 somatic mutations (0.44%) were associated with an antibody response specific to the mutated peptide. PIWAS analyses identified motifs in 11 proteins, including NY-ESO-1 and HERVK-113, as immunogenic in mCRPC, and ELISA confirmed serum antibody enrichment in candidate patients. Confirmatory PIWAS, Identifying Motifs Using Next-generation sequencing Experiments (IMUNE), and ELISA analyses performed on serum samples from 106 patients with melanoma similarly revealed enriched cancer-specific antibody responses to NY-ESO-1.

Conclusions: We present the first large-scale profiling of autoantibodies in advanced prostate cancer, utilizing a new antibody profiling approach to reveal novel cancer-specific antigens and epitopes. Our study recovers antigens of known importance and identifies novel tumor-specific epitopes of translational interest.

Footnotes

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

  • Clin Cancer Res 2020;26:6204–14

  • Received May 20, 2020.
  • Revision received August 3, 2020.
  • Accepted September 16, 2020.
  • Published first September 23, 2020.
  • ©2020 American Association for Cancer Research.
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Clinical Cancer Research: 26 (23)
December 2020
Volume 26, Issue 23
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Autoantibody Landscape in Patients with Advanced Prostate Cancer
William S. Chen, Winston A. Haynes, Rebecca Waitz, Kathy Kamath, Agustin Vega-Crespo, Raunak Shrestha, Minlu Zhang, Adam Foye, Ignacio Baselga Carretero, Ivan Perez Garcilazo, Meng Zhang, Shuang G. Zhao, Martin Sjöström, David A. Quigley, Jonathan Chou, Tomasz M. Beer, Matthew Rettig, Martin Gleave, Christopher P. Evans, Primo Lara, Kim N. Chi, Robert E. Reiter, Joshi J. Alumkal, Alan Ashworth, Rahul Aggarwal, Eric J. Small, Patrick S. Daugherty, Antoni Ribas, David Y. Oh, John C. Shon and Felix Y. Feng
Clin Cancer Res December 1 2020 (26) (23) 6204-6214; DOI: 10.1158/1078-0432.CCR-20-1966

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Autoantibody Landscape in Patients with Advanced Prostate Cancer
William S. Chen, Winston A. Haynes, Rebecca Waitz, Kathy Kamath, Agustin Vega-Crespo, Raunak Shrestha, Minlu Zhang, Adam Foye, Ignacio Baselga Carretero, Ivan Perez Garcilazo, Meng Zhang, Shuang G. Zhao, Martin Sjöström, David A. Quigley, Jonathan Chou, Tomasz M. Beer, Matthew Rettig, Martin Gleave, Christopher P. Evans, Primo Lara, Kim N. Chi, Robert E. Reiter, Joshi J. Alumkal, Alan Ashworth, Rahul Aggarwal, Eric J. Small, Patrick S. Daugherty, Antoni Ribas, David Y. Oh, John C. Shon and Felix Y. Feng
Clin Cancer Res December 1 2020 (26) (23) 6204-6214; DOI: 10.1158/1078-0432.CCR-20-1966
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