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Cancer Epidemiology, Biomarkers & Prevention
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CEBP Focus

The Key Characteristics of Carcinogens: Relationship to the Hallmarks of Cancer, Relevant Biomarkers, and Assays to Measure Them

Martyn T. Smith, Kathryn Z. Guyton, Nicole Kleinstreuer, Alexandre Borrel, Andres Cardenas, Weihsueh A. Chiu, Dean W. Felsher, Catherine F. Gibbons, William H. Goodson III, Keith A. Houck, Agnes B. Kane, Michele A. La Merrill, Herve Lebrec, Leroy Lowe, Cliona M. McHale, Sheroy Minocherhomji, Linda Rieswijk, Martha S. Sandy, Hideko Sone, Amy Wang, Luoping Zhang, Lauren Zeise and Mark Fielden
Martyn T. Smith
1Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California.
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  • For correspondence: martynts@berkeley.edu
Kathryn Z. Guyton
2Monographs Programme, International Agency for Research on Cancer, Lyon, France.
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Nicole Kleinstreuer
3Division of Intramural Research, Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences (NIEHS), Research Triangle Park, North Carolina.
4National Toxicology Program Interagency Center for the Evaluation of Alternative Toxicological Methods, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina.
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Alexandre Borrel
3Division of Intramural Research, Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences (NIEHS), Research Triangle Park, North Carolina.
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Andres Cardenas
1Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California.
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Weihsueh A. Chiu
5Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas.
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Dean W. Felsher
6Division of Oncology, Departments of Medicine and Pathology, Stanford University School of Medicine, Stanford, California.
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Catherine F. Gibbons
7Office of Research and Development, US Environmental Protection Agency, Washington, D.C.
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William H. Goodson III
8California Pacific Medical Center Research Institute, San Francisco, California.
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Keith A. Houck
9Office of Research and Development, US Environmental Protection Agency, Research Triangle Park, North Carolina.
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Agnes B. Kane
10Department of Pathology and Laboratory Medicine, Alpert Medical School, Brown University, Providence, Rhode Island.
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Michele A. La Merrill
11Department of Environmental Toxicology, University of California, Davis, California.
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Herve Lebrec
12Comparative Biology & Safety Sciences, Amgen Research, Amgen Inc., Thousand Oaks, California.
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Leroy Lowe
13Getting to Know Cancer, Truro, Nova Scotia, Canada.
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Cliona M. McHale
1Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California.
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Sheroy Minocherhomji
12Comparative Biology & Safety Sciences, Amgen Research, Amgen Inc., Thousand Oaks, California.
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Linda Rieswijk
1Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California.
14Institute of Data Science, Maastricht University, Maastricht, the Netherlands.
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Martha S. Sandy
15Office of Environmental Health Hazard Assessment, California Environmental Protection Agency, Oakland, California.
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Hideko Sone
16Yokohama University of Pharmacy and National Institute for Environmental Studies, Tsukuba Ibaraki, Japan.
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Amy Wang
17Office of the Report on Carcinogens, Division of National Toxicology Program, The National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina.
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Luoping Zhang
1Division of Environmental Health Sciences, School of Public Health, University of California Berkeley, Berkeley, California.
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Lauren Zeise
15Office of Environmental Health Hazard Assessment, California Environmental Protection Agency, Oakland, California.
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Mark Fielden
18Expansion Therapeutics Inc, San Diego, California.
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DOI: 10.1158/1055-9965.EPI-19-1346 Published October 2020
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Abstract

The key characteristics (KC) of human carcinogens provide a uniform approach to evaluating mechanistic evidence in cancer hazard identification. Refinements to the approach were requested by organizations and individuals applying the KCs. We assembled an expert committee with knowledge of carcinogenesis and experience in applying the KCs in cancer hazard identification. We leveraged this expertise and examined the literature to more clearly describe each KC, identify current and emerging assays and in vivo biomarkers that can be used to measure them, and make recommendations for future assay development. We found that the KCs are clearly distinct from the Hallmarks of Cancer, that interrelationships among the KCs can be leveraged to strengthen the KC approach (and an understanding of environmental carcinogenesis), and that the KC approach is applicable to the systematic evaluation of a broad range of potential cancer hazards in vivo and in vitro. We identified gaps in coverage of the KCs by current assays. Future efforts should expand the breadth, specificity, and sensitivity of validated assays and biomarkers that can measure the 10 KCs. Refinement of the KC approach will enhance and accelerate carcinogen identification, a first step in cancer prevention.

See all articles in this CEBP Focus section, “Environmental Carcinogenesis: Pathways to Prevention.”

Footnotes

  • Cancer Epidemiol Biomarkers Prev 2020;29:1887–903

  • Received November 1, 2019.
  • Revision received January 15, 2020.
  • Accepted March 4, 2020.
  • Published first March 9, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Epidemiology Biomarkers & Prevention: 29 (10)
October 2020
Volume 29, Issue 10
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The Key Characteristics of Carcinogens: Relationship to the Hallmarks of Cancer, Relevant Biomarkers, and Assays to Measure Them
Martyn T. Smith, Kathryn Z. Guyton, Nicole Kleinstreuer, Alexandre Borrel, Andres Cardenas, Weihsueh A. Chiu, Dean W. Felsher, Catherine F. Gibbons, William H. Goodson III, Keith A. Houck, Agnes B. Kane, Michele A. La Merrill, Herve Lebrec, Leroy Lowe, Cliona M. McHale, Sheroy Minocherhomji, Linda Rieswijk, Martha S. Sandy, Hideko Sone, Amy Wang, Luoping Zhang, Lauren Zeise and Mark Fielden
Cancer Epidemiol Biomarkers Prev October 1 2020 (29) (10) 1887-1903; DOI: 10.1158/1055-9965.EPI-19-1346

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The Key Characteristics of Carcinogens: Relationship to the Hallmarks of Cancer, Relevant Biomarkers, and Assays to Measure Them
Martyn T. Smith, Kathryn Z. Guyton, Nicole Kleinstreuer, Alexandre Borrel, Andres Cardenas, Weihsueh A. Chiu, Dean W. Felsher, Catherine F. Gibbons, William H. Goodson III, Keith A. Houck, Agnes B. Kane, Michele A. La Merrill, Herve Lebrec, Leroy Lowe, Cliona M. McHale, Sheroy Minocherhomji, Linda Rieswijk, Martha S. Sandy, Hideko Sone, Amy Wang, Luoping Zhang, Lauren Zeise and Mark Fielden
Cancer Epidemiol Biomarkers Prev October 1 2020 (29) (10) 1887-1903; DOI: 10.1158/1055-9965.EPI-19-1346
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