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Research Articles

Selective Estrogen Receptor Modulators and Pharmacogenomic Variation in ZNF423 Regulation of BRCA1 Expression: Individualized Breast Cancer Prevention

James N. Ingle, Mohan Liu, D. Lawrence Wickerham, Daniel J. Schaid, Liewei Wang, Taisei Mushiroda, Michiaki Kubo, Joseph P. Costantino, Victor G. Vogel, Soonmyung Paik, Matthew P. Goetz, Matthew M. Ames, Gregory D. Jenkins, Anthony Batzler, Erin E. Carlson, David A. Flockhart, Norman Wolmark, Yusuke Nakamura and Richard M. Weinshilboum
James N. Ingle
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Mohan Liu
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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D. Lawrence Wickerham
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Daniel J. Schaid
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Liewei Wang
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Taisei Mushiroda
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Michiaki Kubo
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Joseph P. Costantino
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Victor G. Vogel
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Soonmyung Paik
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Matthew P. Goetz
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Matthew M. Ames
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Gregory D. Jenkins
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Anthony Batzler
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Erin E. Carlson
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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David A. Flockhart
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Norman Wolmark
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Yusuke Nakamura
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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Richard M. Weinshilboum
1Division of Medical Oncology, 2Division of Clinical Pharmacology, Department of Molecular Pharmacology and Experimental Therapeutics, and 3Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota; 4Section of Cancer Genetics and Prevention and 5Department of Human Oncology, Allegheny General Hospital; 6National Surgical Adjuvant Breast and Bowel Project (NSABP), 7NSABP Biostatistical Center, 8Department of Biostatistics, Graduate School of Public Health, and 9Department of Medical Oncology, University of Pittsburgh, Pittsburgh, Pennsylvania; 10Indiana University, Indianapolis, Indiana; 11RIKEN Center for Genomic Medicine, Tokyo, Japan
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DOI: 10.1158/2159-8290.CD-13-0038 Published July 2013
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Abstract

The selective estrogen receptor modulators (SERM) tamoxifen and raloxifene can reduce the occurrence of breast cancer in high-risk women by 50%, but this U.S. Food and Drug Administration-approved prevention therapy is not often used. We attempted to identify genetic factors that contribute to variation in SERM breast cancer prevention, using DNA from the NSABP P-1 and P-2 breast cancer prevention trials. An initial discovery genome-wide association study identified common single-nucleotide polymorphisms (SNP) in or near the ZNF423 and CTSO genes that were associated with breast cancer risk during SERM therapy. We then showed that both ZNF423 and CTSO participated in the estrogen-dependent induction of BRCA1 expression, in both cases with SNP-dependent variation in induction. ZNF423 appeared to be an estrogen-inducible BRCA1 transcription factor. The OR for differences in breast cancer risk during SERM therapy for subjects homozygous for both protective or both risk alleles for ZNF423 and CTSO was 5.71.

Significance: This study identified novel, functionally polymorphic genes involved in the estrogen-dependent regulation of BRCA1 expression, as well as a novel mechanism for genetic variation in SERM therapeutic effect. These observations, and definition of their underlying mechanisms, represent steps toward pharmacogenomically individualized SERM breast cancer prevention. Cancer Discov; 3(7); 812–25. ©2013 AACR.

See related commentary by Machiela and Chanock, p. 728

This article is highlighted in the In This Issue feature, p. 705

Footnotes

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

  • Received January 30, 2013.
  • Revision received April 2, 2013.
  • Accepted April 10, 2013.
  • ©2013 American Association for Cancer Research.
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Cancer Discovery: 3 (7)
July 2013
Volume 3, Issue 7
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Selective Estrogen Receptor Modulators and Pharmacogenomic Variation in ZNF423 Regulation of BRCA1 Expression: Individualized Breast Cancer Prevention
James N. Ingle, Mohan Liu, D. Lawrence Wickerham, Daniel J. Schaid, Liewei Wang, Taisei Mushiroda, Michiaki Kubo, Joseph P. Costantino, Victor G. Vogel, Soonmyung Paik, Matthew P. Goetz, Matthew M. Ames, Gregory D. Jenkins, Anthony Batzler, Erin E. Carlson, David A. Flockhart, Norman Wolmark, Yusuke Nakamura and Richard M. Weinshilboum
Cancer Discov July 1 2013 (3) (7) 812-825; DOI: 10.1158/2159-8290.CD-13-0038

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Selective Estrogen Receptor Modulators and Pharmacogenomic Variation in ZNF423 Regulation of BRCA1 Expression: Individualized Breast Cancer Prevention
James N. Ingle, Mohan Liu, D. Lawrence Wickerham, Daniel J. Schaid, Liewei Wang, Taisei Mushiroda, Michiaki Kubo, Joseph P. Costantino, Victor G. Vogel, Soonmyung Paik, Matthew P. Goetz, Matthew M. Ames, Gregory D. Jenkins, Anthony Batzler, Erin E. Carlson, David A. Flockhart, Norman Wolmark, Yusuke Nakamura and Richard M. Weinshilboum
Cancer Discov July 1 2013 (3) (7) 812-825; DOI: 10.1158/2159-8290.CD-13-0038
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