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Molecular Cancer Therapeutics
Molecular Cancer Therapeutics
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Small Molecule Therapeutics

Repurposing the FDA-Approved Antiviral Drug Ribavirin as Targeted Therapy for Nasopharyngeal Carcinoma

Sakibul Huq, Joshua Casaos, Riccardo Serra, Michael Peters, Yuanxuan Xia, Andy S. Ding, Jeff Ehresman, Jayanidhi N. Kedda, Manuel Morales, Noah L. Gorelick, Tianna Zhao, Wataru Ishida, Alexander Perdomo-Pantoja, Arba Cecia, Chenchen Ji, Ian Suk, David Sidransky, Mariana Brait, Henry Brem, Nicolas Skuli and Betty Tyler
Sakibul Huq
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Joshua Casaos
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Riccardo Serra
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Michael Peters
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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  • ORCID record for Michael Peters
Yuanxuan Xia
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Andy S. Ding
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Jeff Ehresman
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Jayanidhi N. Kedda
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Manuel Morales
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Noah L. Gorelick
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Tianna Zhao
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Wataru Ishida
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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  • ORCID record for Wataru Ishida
Alexander Perdomo-Pantoja
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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  • ORCID record for Alexander Perdomo-Pantoja
Arba Cecia
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Chenchen Ji
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Ian Suk
2Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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David Sidransky
3Head and Neck Cancer Research Laboratory, Department of Otolaryngology and Head & Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Mariana Brait
3Head and Neck Cancer Research Laboratory, Department of Otolaryngology and Head & Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Henry Brem
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
4Departments of Biomedical Engineering, Oncology, and Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Nicolas Skuli
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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Betty Tyler
1Hunterian Neurosurgical Research Laboratory, Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland.
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  • For correspondence: btyler@jhmi.edu
DOI: 10.1158/1535-7163.MCT-19-0572 Published September 2020
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Abstract

Nasopharyngeal carcinoma (NPC) is a squamous cell carcinoma with a proclivity for systemic dissemination, leading many patients to present with advanced stage disease and fail available treatments. There is a notable lack of targeted therapies for NPC, despite working knowledge of multiple proteins with integral roles in NPC cancer biology. These proteins include EZH2, Snail, eIF4E, and IMPDH, which are all overexpressed in NPC and correlated with poor prognosis. These proteins are known to be modulated by ribavirin, an FDA-approved hepatitis C antiviral that has recently been repurposed as a promising therapeutic in several solid and hematologic malignancies. Here, we investigated the potential of ribavirin as a targeted anticancer agent in five human NPC cell lines. Using cellular growth assays, flow cytometry, BrdU cell proliferation assays, scratch wound assays, and invasion assays, we show in vitro that ribavirin decreases NPC cellular proliferation, migration, and invasion and promotes cell-cycle arrest and cell death. Modulation of EZH2, Snail, eIF4E, IMPDH, mTOR, and cyclin D1 were observed in Western blots and enzymatic activity assays in response to ribavirin treatment. As monotherapy, ribavirin reduced flank tumor growth in multiple NPC xenograft models in vivo. Most importantly, we demonstrate that ribavirin enhanced the effects of radiotherapy, a central component of NPC treatment, both in vitro and in vivo. Our work suggests that NPC responds to ribavirin-mediated EZH2, Snail, eIF4E, IMPDH, and mTOR changes and positions ribavirin for clinical evaluation as a potential addition to our NPC treatment armamentarium.

Footnotes

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

  • Mol Cancer Ther 2020;19:1797–808

  • Received June 5, 2019.
  • Revision received December 9, 2019.
  • Accepted June 9, 2020.
  • Published first June 30, 2020.
  • ©2020 American Association for Cancer Research.
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Molecular Cancer Therapeutics: 19 (9)
September 2020
Volume 19, Issue 9
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Repurposing the FDA-Approved Antiviral Drug Ribavirin as Targeted Therapy for Nasopharyngeal Carcinoma
Sakibul Huq, Joshua Casaos, Riccardo Serra, Michael Peters, Yuanxuan Xia, Andy S. Ding, Jeff Ehresman, Jayanidhi N. Kedda, Manuel Morales, Noah L. Gorelick, Tianna Zhao, Wataru Ishida, Alexander Perdomo-Pantoja, Arba Cecia, Chenchen Ji, Ian Suk, David Sidransky, Mariana Brait, Henry Brem, Nicolas Skuli and Betty Tyler
Mol Cancer Ther September 1 2020 (19) (9) 1797-1808; DOI: 10.1158/1535-7163.MCT-19-0572

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Repurposing the FDA-Approved Antiviral Drug Ribavirin as Targeted Therapy for Nasopharyngeal Carcinoma
Sakibul Huq, Joshua Casaos, Riccardo Serra, Michael Peters, Yuanxuan Xia, Andy S. Ding, Jeff Ehresman, Jayanidhi N. Kedda, Manuel Morales, Noah L. Gorelick, Tianna Zhao, Wataru Ishida, Alexander Perdomo-Pantoja, Arba Cecia, Chenchen Ji, Ian Suk, David Sidransky, Mariana Brait, Henry Brem, Nicolas Skuli and Betty Tyler
Mol Cancer Ther September 1 2020 (19) (9) 1797-1808; DOI: 10.1158/1535-7163.MCT-19-0572
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Molecular Cancer Therapeutics
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