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Tumor and Stem Cell Biology

ATDC/TRIM29 Drives Invasive Bladder Cancer Formation through miRNA-Mediated and Epigenetic Mechanisms

Phillip L. Palmbos, Lidong Wang, Huibin Yang, Yin Wang, Jacob Leflein, McKenzie L. Ahmet, John E. Wilkinson, Chandan Kumar-Sinha, Gina M. Ney, Scott A. Tomlins, Stephanie Daignault, Lakshmi. P. Kunju, Xue-Ru Wu, Yair Lotan, Monica Liebert, Mats E. Ljungman and Diane M. Simeone
Phillip L. Palmbos
Department of Internal Medicine, University of Michigan Medical Center, Ann Arbor, Michigan.Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.
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Lidong Wang
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.
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Huibin Yang
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.
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Yin Wang
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.
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Jacob Leflein
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.
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McKenzie L. Ahmet
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.
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John E. Wilkinson
Department of Pathology, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Laboratory Animal Medicine, University of Michigan Medical Center, Ann Arbor, Michigan.
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Chandan Kumar-Sinha
Department of Pathology, University of Michigan Medical Center, Ann Arbor, Michigan.
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Gina M. Ney
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Pediatrics, University of Michigan Medical Center, Ann Arbor, Michigan.
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Scott A. Tomlins
Department of Pathology, University of Michigan Medical Center, Ann Arbor, Michigan.
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Stephanie Daignault
Department of Biostatistics, University of Michigan Medical Center, Ann Arbor, Michigan.
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Lakshmi. P. Kunju
Department of Pathology, University of Michigan Medical Center, Ann Arbor, Michigan.
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Xue-Ru Wu
Departments of Urology and Pathology and Veterans Affairs Medical Center in Manhattan, New York University School of Medicine, New York, New York.
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Yair Lotan
Department of Urology, University of Texas Southwestern Medical Center, Dallas, Texas.
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Monica Liebert
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Urology, University of Michigan Medical Center, Ann Arbor, Michigan.
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Mats E. Ljungman
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Radiation Oncology, University of Michigan Medical Center, Ann Arbor, Michigan.
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Diane M. Simeone
Translational Oncology Program, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan.Department of Molecular and Integrative Physiology, University of Michigan Medical Center, Ann Arbor, Michigan.
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  • For correspondence: simeone@med.umich.edu
DOI: 10.1158/0008-5472.CAN-15-0603
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Abstract

Bladder cancer is a common and deadly malignancy but its treatment has advanced little due to poor understanding of the factors and pathways that promote disease. ATDC/TRIM29 is a highly expressed gene in several lethal tumor types, including bladder tumors, but its role as a pathogenic driver has not been established. Here we show that overexpression of ATDC in vivo is sufficient to drive both noninvasive and invasive bladder carcinoma development in transgenic mice. ATDC-driven bladder tumors were indistinguishable from human bladder cancers, which displayed similar gene expression signatures. Clinically, ATDC was highly expressed in bladder tumors in a manner associated with invasive growth behaviors. Mechanistically, ATDC exerted its oncogenic effects by suppressing miR-29 and subsequent upregulation of DNMT3A, leading to DNA methylation and silencing of the tumor suppressor PTEN. Taken together, our findings established a role for ATDC as a robust pathogenic driver of bladder cancer development, identified downstream effector pathways, and implicated ATDC as a candidate biomarker and therapeutic target. Cancer Res; 75(23); 1–12. ©2015 AACR.

Footnotes

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

  • Received March 3, 2015.
  • Revision received August 4, 2015.
  • Accepted September 3, 2015.
  • ©2015 American Association for Cancer Research.
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Published OnlineFirst November 18, 2015
doi: 10.1158/0008-5472.CAN-15-0603

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ATDC/TRIM29 Drives Invasive Bladder Cancer Formation through miRNA-Mediated and Epigenetic Mechanisms
Phillip L. Palmbos, Lidong Wang, Huibin Yang, Yin Wang, Jacob Leflein, McKenzie L. Ahmet, John E. Wilkinson, Chandan Kumar-Sinha, Gina M. Ney, Scott A. Tomlins, Stephanie Daignault, Lakshmi. P. Kunju, Xue-Ru Wu, Yair Lotan, Monica Liebert, Mats E. Ljungman and Diane M. Simeone
Cancer Res November 18 2015 DOI: 10.1158/0008-5472.CAN-15-0603

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ATDC/TRIM29 Drives Invasive Bladder Cancer Formation through miRNA-Mediated and Epigenetic Mechanisms
Phillip L. Palmbos, Lidong Wang, Huibin Yang, Yin Wang, Jacob Leflein, McKenzie L. Ahmet, John E. Wilkinson, Chandan Kumar-Sinha, Gina M. Ney, Scott A. Tomlins, Stephanie Daignault, Lakshmi. P. Kunju, Xue-Ru Wu, Yair Lotan, Monica Liebert, Mats E. Ljungman and Diane M. Simeone
Cancer Res November 18 2015 DOI: 10.1158/0008-5472.CAN-15-0603
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