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Cancer Prevention Research
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Research Article

HIST1H2BB and MAGI2 Methylation and Somatic Mutations as Precision Medicine Biomarkers for Diagnosis and Prognosis of High-grade Serous Ovarian Cancer

Blanca L. Valle, Sebastian Rodriguez-Torres, Elisabetta Kuhn, Teresa Díaz-Montes, Edgardo Parrilla-Castellar, Fahcina P. Lawson, Oluwasina Folawiyo, Carmen Ili-Gangas, Priscilla Brebi-Mieville, James R. Eshleman, James Herman, Ie-Ming Shih, David Sidransky and Rafael Guerrero-Preston
Blanca L. Valle
1Otolaryngology Department, Head and Neck Cancer Research Division, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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Sebastian Rodriguez-Torres
2Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
3Department of Medicine, University of Pittsburgh, School of Medicine, Pittsburgh, Pennsylvania.
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  • ORCID record for Sebastian Rodriguez-Torres
Elisabetta Kuhn
4Division of Pathology, Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico; Department of Biomedical, Surgical, and Dental Sciences, University of Milan, Italy.
5Departments of Pathology, Gynecology and Obstetrics, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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Teresa Díaz-Montes
6The Lya Segall Ovarian Cancer Institute, Mercy Medical Center, Baltimore, Maryland.
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Edgardo Parrilla-Castellar
7Department of Pathology, University of Washington, Seattle, Washington.
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Fahcina P. Lawson
1Otolaryngology Department, Head and Neck Cancer Research Division, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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Oluwasina Folawiyo
1Otolaryngology Department, Head and Neck Cancer Research Division, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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Carmen Ili-Gangas
8Laboratory Integrative Biology (LIBi), Center for Excellence in Translational Medicine-Scientific and Technological Bioresources Nucleus (CEMT-BIOREN), Universidad de La Frontera, Temuco, Chile.
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  • ORCID record for Carmen Ili-Gangas
Priscilla Brebi-Mieville
8Laboratory Integrative Biology (LIBi), Center for Excellence in Translational Medicine-Scientific and Technological Bioresources Nucleus (CEMT-BIOREN), Universidad de La Frontera, Temuco, Chile.
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James R. Eshleman
9Department of Pathology, Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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James Herman
3Department of Medicine, University of Pittsburgh, School of Medicine, Pittsburgh, Pennsylvania.
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Ie-Ming Shih
4Division of Pathology, Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico; Department of Biomedical, Surgical, and Dental Sciences, University of Milan, Italy.
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David Sidransky
1Otolaryngology Department, Head and Neck Cancer Research Division, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
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Rafael Guerrero-Preston
1Otolaryngology Department, Head and Neck Cancer Research Division, The Johns Hopkins University, School of Medicine, Baltimore, Maryland.
10University of Puerto Rico School of Medicine, Department of Obstetrics and Gynecology, San Juan, Puerto Rico.
11LifeGene Biomarks Inc., San Juan, Puerto Rico.
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  • For correspondence: rafael.guerrero@upr.edu
DOI: 10.1158/1940-6207.CAPR-19-0412 Published September 2020
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Abstract

Molecular alterations that contribute to long-term (LT) and short-term (ST) survival in ovarian high-grade serous carcinoma (HGSC) may be used as precision medicine biomarkers. DNA promoter methylation is an early event in tumorigenesis, which can be detected in blood and urine, making it a feasible companion biomarker to somatic mutations for early detection and targeted treatment workflows. We compared the methylation profile in 12 HGSC tissue samples to 30 fallopian tube epithelium samples, using the Infinium Human Methylation 450K Array. We also used 450K methylation arrays to compare methylation among HGSCs long-term survivors (more than 5 years) and short-term survivors (less than 3 years). We verified the array results using bisulfite sequencing and methylation-specific PCR (qMSP). in another cohort of HGSC patient samples (n = 35). Immunoblot and clonogenic assays after pharmacologic unmasking show that HIST1H2BB and MAGI2 promoter methylation downregulates mRNA expression levels in ovarian cancer cells. We then used qMSP in paired tissue, ascites, plasma/serum, vaginal swabs, and urine from a third cohort of patients with HGSC cancer (n = 85) to test the clinical potential of HIST1H2BB and MAGI2 in precision medicine workflows. We also performed next-generation exome sequencing of 50 frequently mutated in human cancer genes, using the Ion AmpliSeqCancer Hotspot Panel, to show that the somatic mutation profile found in tissue and plasma can be quantified in paired urine samples from patients with HGSC. Our results suggest that HIST1H2BB and MAGI2 have growth-suppressing roles and can be used as HGSC precision medicine biomarkers.

Footnotes

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

  • Cancer Prev Res 2020;13:783–94

  • Received August 29, 2019.
  • Revision received April 15, 2020.
  • Accepted June 11, 2020.
  • Published first June 24, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Prevention Research: 13 (9)
September 2020
Volume 13, Issue 9
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HIST1H2BB and MAGI2 Methylation and Somatic Mutations as Precision Medicine Biomarkers for Diagnosis and Prognosis of High-grade Serous Ovarian Cancer
Blanca L. Valle, Sebastian Rodriguez-Torres, Elisabetta Kuhn, Teresa Díaz-Montes, Edgardo Parrilla-Castellar, Fahcina P. Lawson, Oluwasina Folawiyo, Carmen Ili-Gangas, Priscilla Brebi-Mieville, James R. Eshleman, James Herman, Ie-Ming Shih, David Sidransky and Rafael Guerrero-Preston
Cancer Prev Res September 1 2020 (13) (9) 783-794; DOI: 10.1158/1940-6207.CAPR-19-0412

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HIST1H2BB and MAGI2 Methylation and Somatic Mutations as Precision Medicine Biomarkers for Diagnosis and Prognosis of High-grade Serous Ovarian Cancer
Blanca L. Valle, Sebastian Rodriguez-Torres, Elisabetta Kuhn, Teresa Díaz-Montes, Edgardo Parrilla-Castellar, Fahcina P. Lawson, Oluwasina Folawiyo, Carmen Ili-Gangas, Priscilla Brebi-Mieville, James R. Eshleman, James Herman, Ie-Ming Shih, David Sidransky and Rafael Guerrero-Preston
Cancer Prev Res September 1 2020 (13) (9) 783-794; DOI: 10.1158/1940-6207.CAPR-19-0412
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