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Research Articles

RBMS1 Suppresses Colon Cancer Metastasis through Targeted Stabilization of Its mRNA Regulon

Johnny Yu, Albertas Navickas, Hosseinali Asgharian, Bruce Culbertson, Lisa Fish, Kristle Garcia, John Paolo Olegario, Maria Dermit, Martin Dodel, Benjamin Hänisch, Yikai Luo, Ethan M. Weinberg, Rodrigo Dienstmann, Robert S. Warren, Faraz K. Mardakheh and Hani Goodarzi
Johnny Yu
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Albertas Navickas
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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  • ORCID record for Albertas Navickas
Hosseinali Asgharian
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Bruce Culbertson
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Lisa Fish
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Kristle Garcia
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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John Paolo Olegario
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Maria Dermit
4Centre for Cancer Cell & Molecular Biology, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom.
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Martin Dodel
4Centre for Cancer Cell & Molecular Biology, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom.
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Benjamin Hänisch
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Yikai Luo
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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Ethan M. Weinberg
5Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
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Rodrigo Dienstmann
6Medical Oncology Department, Vall d'Hebron University Hospital, Barcelona, Spain.
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Robert S. Warren
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
7Department of Surgery, University of California, San Francisco, San Francisco, California.
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Faraz K. Mardakheh
4Centre for Cancer Cell & Molecular Biology, Barts Cancer Institute, Queen Mary University of London, London, United Kingdom.
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Hani Goodarzi
1Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, California.
2Department of Urology, University of California, San Francisco, San Francisco, California.
3Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, California.
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  • For correspondence: hani.goodarzi@ucsf.edu
DOI: 10.1158/2159-8290.CD-19-1375 Published September 2020
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Abstract

Identifying master regulators that drive pathologic gene expression is a key challenge in precision oncology. Here, we have developed an analytic framework, named PRADA, that identifies oncogenic RNA-binding proteins through the systematic detection of coordinated changes in their target regulons. Application of this approach to data collected from clinical samples, patient-derived xenografts, and cell line models of colon cancer metastasis revealed the RNA-binding protein RBMS1 as a suppressor of colon cancer progression. We observed that silencing RBMS1 results in increased metastatic capacity in xenograft mouse models, and that restoring its expression blunts metastatic liver colonization. We have found that RBMS1 functions as a posttranscriptional regulator of RNA stability by directly binding its target mRNAs. Together, our findings establish a role for RBMS1 as a previously unknown regulator of RNA stability and as a suppressor of colon cancer metastasis with clinical utility for risk stratification of patients.

Significance: By applying a new analytic approach to transcriptomic data from clinical samples and models of colon cancer progression, we have identified RBMS1 as a suppressor of metastasis and as a post-transcriptional regulator of RNA stability. Notably, RBMS1 silencing and downregulation of its targets are negatively associated with patient survival.

See related commentary by Carter, p. 1261.

This article is highlighted in the In This Issue feature, p. 1241

Footnotes

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

  • Cancer Discov 2020;10:1410–23

  • Received November 24, 2019.
  • Revision received April 27, 2020.
  • Accepted June 2, 2020.
  • Published first June 8, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Discovery: 10 (9)
September 2020
Volume 10, Issue 9
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RBMS1 Suppresses Colon Cancer Metastasis through Targeted Stabilization of Its mRNA Regulon
Johnny Yu, Albertas Navickas, Hosseinali Asgharian, Bruce Culbertson, Lisa Fish, Kristle Garcia, John Paolo Olegario, Maria Dermit, Martin Dodel, Benjamin Hänisch, Yikai Luo, Ethan M. Weinberg, Rodrigo Dienstmann, Robert S. Warren, Faraz K. Mardakheh and Hani Goodarzi
Cancer Discov September 1 2020 (10) (9) 1410-1423; DOI: 10.1158/2159-8290.CD-19-1375

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RBMS1 Suppresses Colon Cancer Metastasis through Targeted Stabilization of Its mRNA Regulon
Johnny Yu, Albertas Navickas, Hosseinali Asgharian, Bruce Culbertson, Lisa Fish, Kristle Garcia, John Paolo Olegario, Maria Dermit, Martin Dodel, Benjamin Hänisch, Yikai Luo, Ethan M. Weinberg, Rodrigo Dienstmann, Robert S. Warren, Faraz K. Mardakheh and Hani Goodarzi
Cancer Discov September 1 2020 (10) (9) 1410-1423; DOI: 10.1158/2159-8290.CD-19-1375
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