The Cancer Microbiome: Distinguishing Direct and Indirect Effects Requires a Systemic View

Joao B Xavier; Vincent B Young; Joseph Skufca; Fiona Ginty; Traci Testerman; Alexander T Pearson; Paul Macklin; Amir Mitchell; Ilya Shmulevich; Lei Xie; J Gregory Caporaso; Keith A Crandall; Nicole L Simone; Filipa Godoy-Vitorino; Timothy J Griffin; Katrine L Whiteson; Heather H Gustafson; Daniel J Slade; Thomas M Schmidt; Marina R S Walther-Antonio; Tal Korem; Bobbie-Jo M Webb-Robertson; Mark P Styczynski; W Evan Johnson; Christian Jobin; Jason M Ridlon; Andrew Y Koh; Michael Yu; Libusha Kelly; Jennifer A Wargo

doi:10.1016/j.trecan.2020.01.004

The Cancer Microbiome: Distinguishing Direct and Indirect Effects Requires a Systemic View

Trends Cancer. 2020 Mar;6(3):192-204. doi: 10.1016/j.trecan.2020.01.004. Epub 2020 Feb 7.

Authors

Joao B Xavier¹, Vincent B Young², Joseph Skufca³, Fiona Ginty⁴, Traci Testerman⁵, Alexander T Pearson⁶, Paul Macklin⁷, Amir Mitchell⁸, Ilya Shmulevich⁹, Lei Xie¹⁰, J Gregory Caporaso¹¹, Keith A Crandall¹², Nicole L Simone¹³, Filipa Godoy-Vitorino¹⁴, Timothy J Griffin¹⁵, Katrine L Whiteson¹⁶, Heather H Gustafson¹⁷, Daniel J Slade¹⁸, Thomas M Schmidt¹⁹, Marina R S Walther-Antonio²⁰, Tal Korem²¹, Bobbie-Jo M Webb-Robertson²², Mark P Styczynski²³, W Evan Johnson²⁴, Christian Jobin²⁵, Jason M Ridlon²⁶, Andrew Y Koh²⁷, Michael Yu²⁸, Libusha Kelly²⁹, Jennifer A Wargo³⁰

Affiliations

¹ Program for Computational and Systems Biology, Memorial Sloan-Kettering Cancer Center, New York, NY, USA. Electronic address: xavierj@mskcc.org.
² Department of Internal Medicine, Division of Infectious Diseases, The University of Michigan Medical School, Ann Arbor, MI, USA.
³ Department of Mathematics, Clarkson University, Potsdam, NY, USA.
⁴ GE Research, Niskayuna, NY, USA.
⁵ Department of Pathology, Microbiology, and Immunology, University of South Carolina School of Medicine, Columbia, SC, USA.
⁶ Section of Hematology/Oncology, Department of Medicine, Comprehensive Cancer Center, University of Chicago, Chicago, Illinois, IL, USA.
⁷ Intelligent Systems Engineering, Indiana University, Bloomington, IN, USA.
⁸ Program in Systems Biology, University of Massachusetts Medical School, Worcester, MA, USA.
⁹ Institute for Systems Biology, Seattle, WA, USA.
¹⁰ Hunter College, Department of Computer Science, New York, NY, USA.
¹¹ Center for Applied Microbiome Science, Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, USA.
¹² Computational Biology Institute, Milken Institute School of Public Health, George Washington University, Washington, DC, USA.
¹³ Sidney Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, PA, USA.
¹⁴ Department of Microbiology and Medical Zoology, School of Medicine, University of Puerto Rico, San Juan, Puerto Rico.
¹⁵ Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN, USA.
¹⁶ Department of Molecular Biology and Biochemistry, University of California Irvine, Irvine, CA, USA.
¹⁷ Seattle Children's Research Institute, Ben Towne Center for Childhood Cancer Research, Seattle, WA, USA.
¹⁸ Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
¹⁹ University of Michigan, Ann Arbor, MI, USA.
²⁰ Department of Surgery, Department of Obstetrics and Gynecology, and Microbiome Program, Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.
²¹ Department of Systems Biology, Columbia University, New York, NY, USA.
²² Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA.
²³ School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA, USA.
²⁴ Division of Computational Biomedicine, Boston University School of Medicine, Boston, MA, USA.
²⁵ Departments of Medicine, Anatomy, and Cell Biology, and of Infectious Diseases and Immunology, University of Florida, Gainesville, FL, USA.
²⁶ Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
²⁷ University of Texas Southwestern Medical Center, Dallas, TX, USA.
²⁸ Toyota Technological Institute at Chicago, Chicago, IL, USA.
²⁹ Albert Einstein College of Medicine, Bronx, NY, USA.
³⁰ The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Abstract

The collection of microbes that live in and on the human body - the human microbiome - can impact on cancer initiation, progression, and response to therapy, including cancer immunotherapy. The mechanisms by which microbiomes impact on cancers can yield new diagnostics and treatments, but much remains unknown. The interactions between microbes, diet, host factors, drugs, and cell-cell interactions within the cancer itself likely involve intricate feedbacks, and no single component can explain all the behavior of the system. Understanding the role of host-associated microbial communities in cancer systems will require a multidisciplinary approach combining microbial ecology, immunology, cancer cell biology, and computational biology - a systems biology approach.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review

MeSH terms

Analgesics, Opioid / therapeutic use
Animals
Bacteria / metabolism
Central Nervous System / physiology
Drug Synergism
Environmental Microbiology
Gastritis / microbiology
Gastrointestinal Microbiome
Helicobacter Infections / complications
Host-Pathogen Interactions
Humans
Immunotherapy
Mice
Microbiota* / drug effects
Microbiota* / radiation effects
Neoplasms / etiology
Neoplasms / microbiology*
Neoplasms / therapy
Neoplasms / virology
Oncogenic Viruses / pathogenicity
Probiotics
Stomach Neoplasms / etiology
Stomach Neoplasms / microbiology
Symbiosis
Tumor Virus Infections

Substances

Analgesics, Opioid

Abstract

Publication types

MeSH terms

Substances

Grants and funding