Case Western Reserve University
United States
Biomarkers for Reducing Mortality of Cancers of the Colon and Esophagus
The goal of this EDRN renewal proposal is the discovery and validation of biomarkers for reducing mortality from gastrointestinal cancers. We particularly target cancers of the colon (CRC), the second leading cause of U.S. cancer deaths, and adenocarcinomas of the esophagus (EAC), the fastest increasing cause of U.S. cancer deaths. In our first funding period, our group prominently advanced early detection of colon cancers through detection of aberrantly methylated tumor DNA in stools. Our work testing methylated VIM (M-VIM) DNA in stools led to an EDRN prospective validation study (GLNE-10), a commercial colon cancer test (ColoSure, from Exact Sciences & LabCorp), and to proof of principal for the Exact Cologuard test of methylated stool DNA that is now FDA approved. Our work studying the 15-PGDH tumor suppressor gene identified the first biomarker for personalized chemoprevention, showing NSAIDs lower colon cancer risk only in individuals with high, but not low, colon 15-PGDH expression. And our further studies of M-VIM showed this biomarker to also be highly sensitive and specific for detecting Barrett's esophagus (BE) and EAC, specifically in tests using esophageal brushings. In this renewal application, for colon cancer we propose EDRN phase 2 validation studies testing biomarkers that identify individuals at high risk of developing colon cancer by testing normal colon mucosa for RNA and DNA markers of elevated cancer risk that are: a) low levels of 15-PGDH transcript expression, and/or b) high levels of DNA methylation at specific colon cancer risk loci. For EAC, we first propose an EDRN phase 2 validation study testing sensitivity and specificity of a panel of candidate DNA methylation biomarkers for identifying BE, the currently best recognized marker of EAC susceptibility, in assays of samples collected from esophageal brushings. We follow these BE assays by then proposing an EDRN phase 2 study of a set of markers that detect EAC, and its precursor lesion HGD, while not detecting BE, thus providing surveillance markers for catching early BE progression, again by testing samples from esophageal brushings. Our candidate progression marker panel includes DNA loci we find aberrantly methylated in HGD and EAC (but not BE); novel non-coding lincRNAs we find highly expressed in EAC (but not in BE); and mutations in TP53. We also further test the ability of this panel to discriminate low grade BE dysplasias (LGD) that are or are not associated with progression to HGD and EAC. Last, we propose new biomarker discovery to identify methylated DNA and/or RNA biomarkers that, in esophageal brushings, will detect the minority subset of EAC or HGD that are negative for our current EAC/HGD marker panel. Our goals are to: 1) develop effective risk stratification assays to optimize primary prevention of CRC; and 2) replace the current ineffective paradigm for preventing EAC deaths by developing inexpensive biomarker based tests of non-endoscopic esophagus brushings, thus: enabling cost-effective population screening to detect BE, enabling cost effective surveillance to catch early progression of BE to HGD and EAC, reducing EAC deaths, and reducing over-treatment of LGD.
Publications
- Cooper GS, Markowitz SD, Chen Z, Tuck M, Willis JE, Berger BM, Brenner DE, Li L. Evaluation of Patients with an Apparent False Positive Stool DNA Test: The Role of Repeat Stool DNA Testing. Digestive diseases and sciences. 2018 Jun;63(6):1449-1453. Epub 2018 Mar 7. PMID: 29516325
- Yu M, Carter KT, Baker KK, Redman MW, Wang T, Vickers K, Li CI, Cohen SA, Krane M, Ose J, Gigic B, Figueiredo JC, Toriola AT, Siegel EM, Shibata D, Schneider M, Ulrich CM, Dzubinski LA, Schoen RE, Grady WM. Elevated EVL Methylation Level in the Normal Colon Mucosa Is a Potential Risk Biomarker for Developing Recurrent Adenomas. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2023 Sep 1;32(9):1146-1152. PMID: 37294695
- Bresalier RS, Grady WM, Markowitz SD, Nielsen HJ, Batra SK, Lampe PD. Biomarkers for Early Detection of Colorectal Cancer: The Early Detection Research Network, a Framework for Clinical Translation. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2020 Dec;29(12):2431-2440. Epub 2020 Apr 16. PMID: 32299850
- Hattangady NG, Carter K, Maroni-Rana B, Wang T, Ayers JL, Yu M, Grady WM. Mapping the core senescence phenotype of primary human colon fibroblasts. Aging. 2024 Feb 21;16(4):3068-3087. Epub 2024 Feb 21. PMID: 38385965
- Moinova HR, Verma S, Dumot J, Faulx A, Iyer PG, Canto MI, Wang JS, Shaheen NJ, Thota PN, Aklog L, Willis JE, Markowitz SD, Chak A. Multicenter, Prospective Trial of Nonendoscopic Biomarker-Driven Detection of Barrett's Esophagus and Esophageal Adenocarcinoma. The American journal of gastroenterology. 2024 Nov 1;119(11):2206-2214. Epub 2024 Apr 30. PMID: 38686933
- Cooper GS, Markowitz SD, Chen Z, Tuck M, Willis JE, Berger BM, Brenner DE, Li L. Performance of multitarget stool DNA testing in African American patients. Cancer. 2018 Oct 1;124(19):3876-3880. Epub 2018 Sep 7. PMID: 30193399
- Garman KS, Purkayastha BPD, Hogue JA, Fecteau R, BETRNet CONSORTIUM, Guda K, Chak A, Falk GW, Becker TC, von Furstenberg R, Dawson D, Willis JE, McCall SJ, Blum AE, Kresak AM, Gupta R, Brock W. Genetic Defect in Submucosal Gland-Associated Caveolin-3: A New Paradigm in Esophageal Adenocarcinoma Risk. Gastroenterology. 2023 Dec;165(6):1561-1564.e3. Epub 2023 Sep 1. PMID: 37659676
- Douville C, Moinova HR, Thota PN, Shaheen NJ, Iyer PG, Canto MI, Wang JS, Dumot JA, Faulx A, Kinzler KW, Papadopoulos N, Vogelstein B, Markowitz SD, Bettegowda C, Willis JE, Chak A. Massively Parallel Sequencing of Esophageal Brushings Enables an Aneuploidy-Based Classification of Patients With Barrett's Esophagus. Gastroenterology. 2021 May;160(6):2043-2054.e2. Epub 2021 Jan 22. PMID: 33493502
- Yu M, O'Leary RM, Kaz AM, Morris SM, Carter KT, Chak A, Chandar A, Willis JE, Moinova HR, Markowitz SD, Brenner DE, Anandabapasathy S, Westerhoff M, Wong CJ, Shaheen NJ, Chen Y, Barnholtz-Sloan JS, Grady WM. Methylated B3GAT2 and ZNF793 Are Potential Detection Biomarkers for Barrett's Esophagus. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2015 Dec;24(12):1890-7. Epub 2015 Nov 6. PMID: 26545406