Inflammation-induced cell proliferation potentiates DNA damage-induced mutations in vivo

Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo. Of particular interest is inflammation, a known cancer risk facto...

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Published in:	PLoS genetics Vol. 11; no. 2; p. e1004901
Main Authors:	Kiraly, Orsolya, Gong, Guanyu, Olipitz, Werner, Muthupalani, Sureshkumar, Engelward, Bevin P
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 01-02-2015 Public Library of Science (PLoS)
Subjects:	Animals Cancer therapies Cell division Cell growth Cell proliferation Cell Proliferation - genetics Deoxyribonucleic acid Disease DNA DNA damage DNA Damage - genetics DNA Repair - genetics Drug resistance Environmental health Flow cytometry Gene mutation Genetic aspects Health sciences Histones - genetics Homologous Recombination Humans Identification and classification Inflammation Inflammation - complications Inflammation - genetics Inflammation - pathology Mice Mutation Neoplasms - etiology Neoplasms - genetics Neoplasms - pathology Pancreas - pathology Pancreatic cancer Physiology Risk Factors Rodents Studies Tissue engineering
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Abstract	Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo. Of particular interest is inflammation, a known cancer risk factor relevant to chronic inflammatory diseases and pathogen-induced inflammation. Here, we used the fluorescent yellow direct repeat (FYDR) mice that harbor a reporter to detect misalignments during homologous recombination (HR), an important class of mutations. FYDR mice were exposed to cerulein, a potent inducer of pancreatic inflammation. We show that inflammation induces DSBs (γH2AX foci) and that several days later there is an increase in cell proliferation. While isolated bouts of inflammation did not induce HR, overlap between inflammation-induced DNA damage and inflammation-induced cell proliferation induced HR significantly. To study exogenously-induced DNA damage, animals were exposed to methylnitrosourea, a model alkylating agent that creates DNA lesions relevant to both environmental exposures and cancer chemotherapy. We found that exposure to alkylation damage induces HR, and importantly, that inflammation-induced cell proliferation and alkylation induce HR in a synergistic fashion. Taken together, these results show that, during an acute bout of inflammation, there is a kinetic barrier separating DNA damage from cell proliferation that protects against mutations, and that inflammation-induced cell proliferation greatly potentiates exposure-induced mutations. These studies demonstrate a fundamental mechanism by which inflammation can act synergistically with DNA damage to induce mutations that drive cancer and cancer recurrence.
AbstractList	Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo. Of particular interest is inflammation, a known cancer risk factor relevant to chronic inflammatory diseases and pathogen-induced inflammation. Here, we used the fluorescent yellow direct repeat (FYDR) mice that harbor a reporter to detect misalignments during homologous recombination (HR), an important class of mutations. FYDR mice were exposed to cerulein, a potent inducer of pancreatic inflammation. We show that inflammation induces DSBs (γH2AX foci) and that several days later there is an increase in cell proliferation. While isolated bouts of inflammation did not induce HR, overlap between inflammation-induced DNA damage and inflammation-induced cell proliferation induced HR significantly. To study exogenously-induced DNA damage, animals were exposed to methylnitrosourea, a model alkylating agent that creates DNA lesions relevant to both environmental exposures and cancer chemotherapy. We found that exposure to alkylation damage induces HR, and importantly, that inflammation-induced cell proliferation and alkylation induce HR in a synergistic fashion. Taken together, these results show that, during an acute bout of inflammation, there is a kinetic barrier separating DNA damage from cell proliferation that protects against mutations, and that inflammation-induced cell proliferation greatly potentiates exposure-induced mutations. These studies demonstrate a fundamental mechanism by which inflammation can act synergistically with DNA damage to induce mutations that drive cancer and cancer recurrence. Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo . Of particular interest is inflammation, a known cancer risk factor relevant to chronic inflammatory diseases and pathogen-induced inflammation. Here, we used the fluorescent yellow direct repeat (FYDR) mice that harbor a reporter to detect misalignments during homologous recombination (HR), an important class of mutations. FYDR mice were exposed to cerulein, a potent inducer of pancreatic inflammation. We show that inflammation induces DSBs (γH2AX foci) and that several days later there is an increase in cell proliferation. While isolated bouts of inflammation did not induce HR, overlap between inflammation-induced DNA damage and inflammation-induced cell proliferation induced HR significantly. To study exogenously-induced DNA damage, animals were exposed to methylnitrosourea, a model alkylating agent that creates DNA lesions relevant to both environmental exposures and cancer chemotherapy. We found that exposure to alkylation damage induces HR, and importantly, that inflammation-induced cell proliferation and alkylation induce HR in a synergistic fashion. Taken together, these results show that, during an acute bout of inflammation, there is a kinetic barrier separating DNA damage from cell proliferation that protects against mutations, and that inflammation-induced cell proliferation greatly potentiates exposure-induced mutations. These studies demonstrate a fundamental mechanism by which inflammation can act synergistically with DNA damage to induce mutations that drive cancer and cancer recurrence. People with chronic inflammatory conditions have a markedly increased risk for cancer. In addition, many cancers have an inflammatory microenvironment that promotes tumor growth. Here, we show that inflammatory infiltration synergizes with tissue regeneration to induce DNA sequence rearrangements in vivo . Chronically inflamed issues that are continuously regenerating are thus at an increased risk for mutagenesis and malignant transformation. Further, rapidly dividing tumor cells in an inflammatory microenvironment can also acquire mutations, which have been shown to contribute to drug resistance and disease recurrence. Finally, inflammation-induced tissue regeneration sensitizes tissues to DNA damaging environmental exposures and chemotherapeutics. The work described here thus increases our understanding of how inflammation leads to genetic changes that drive cancer formation and recurrence. Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo. Of particular interest is inflammation, a known cancer risk factor relevant to chronic inflammatory diseases and pathogen-induced inflammation. Here, we used the fluorescent yellow direct repeat (FYDR) mice that harbor a reporter to detect misalignments during homologous recombination (HR), an important class of mutations. FYDR mice were exposed to cerulein, a potent inducer of pancreatic inflammation. We show that inflammation induces DSBs ([gamma]H2AX foci) and that several days later there is an increase in cell proliferation. While isolated bouts of inflammation did not induce HR, overlap between inflammation-induced DNA damage and inflammation-induced cell proliferation induced HR significantly. To study exogenously-induced DNA damage, animals were exposed to methylnitrosourea, a model alkylating agent that creates DNA lesions relevant to both environmental exposures and cancer chemotherapy. We found that exposure to alkylation damage induces HR, and importantly, that inflammation-induced cell proliferation and alkylation induce HR in a synergistic fashion. Taken together, these results show that, during an acute bout of inflammation, there is a kinetic barrier separating DNA damage from cell proliferation that protects against mutations, and that inflammation-induced cell proliferation greatly potentiates exposure-induced mutations. These studies demonstrate a fundamental mechanism by which inflammation can act synergistically with DNA damage to induce mutations that drive cancer and cancer recurrence. Mutations are a critical driver of cancer initiation. While extensive studies have focused on exposure-induced mutations, few studies have explored the importance of tissue physiology as a modulator of mutation susceptibility in vivo. Of particular interest is inflammation, a known cancer risk factor relevant to chronic inflammatory diseases and pathogen-induced inflammation. Here, we used the fluorescent yellow direct repeat (FYDR) mice that harbor a reporter to detect misalignments during homologous recombination (HR), an important class of mutations. FYDR mice were exposed to cerulein, a potent inducer of pancreatic inflammation. We show that inflammation induces DSBs (γH2AX foci) and that several days later there is an increase in cell proliferation. While isolated bouts of inflammation did not induce HR, overlap between inflammation-induced DNA damage and inflammation-induced cell proliferation induced HR significantly. To study exogenously-induced DNA damage, animals were exposed to methylnitrosourea, a model alkylating agent that creates DNA lesions relevant to both environmental exposures and cancer chemotherapy. We found that exposure to alkylation damage induces HR, and importantly, that inflammation-induced cell proliferation and alkylation induce HR in a synergistic fashion. Taken together, these results show that, during an acute bout of inflammation, there is a kinetic barrier separating DNA damage from cell proliferation that protects against mutations, and that inflammation-induced cell proliferation greatly potentiates exposure-induced mutations. These studies demonstrate a fundamental mechanism by which inflammation can act synergistically with DNA damage to induce mutations that drive cancer and cancer recurrence.
Audience	Academic
Author	Muthupalani, Sureshkumar Gong, Guanyu Olipitz, Werner Engelward, Bevin P Kiraly, Orsolya
AuthorAffiliation	1 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America 2 Singapore–MIT Alliance for Research and Technology, Singapore University of Washington, UNITED STATES 3 Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
AuthorAffiliation_xml	– name: 1 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: 2 Singapore–MIT Alliance for Research and Technology, Singapore – name: 3 Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – name: University of Washington, UNITED STATES
Author_xml	– sequence: 1 givenname: Orsolya surname: Kiraly fullname: Kiraly, Orsolya organization: Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America; Singapore-MIT Alliance for Research and Technology, Singapore – sequence: 2 givenname: Guanyu surname: Gong fullname: Gong, Guanyu organization: Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – sequence: 3 givenname: Werner surname: Olipitz fullname: Olipitz, Werner organization: Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – sequence: 4 givenname: Sureshkumar surname: Muthupalani fullname: Muthupalani, Sureshkumar organization: Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America – sequence: 5 givenname: Bevin P surname: Engelward fullname: Engelward, Bevin P organization: Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America; Singapore-MIT Alliance for Research and Technology, Singapore
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25647331$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	COPYRIGHT 2015 Public Library of Science 2015 Kiraly et al 2015 Kiraly et al 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 11(2): e1004901. doi:10.1371/journal.pgen.1004901
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: OK BPE. Performed the experiments: OK GG WO. Analyzed the data: OK WO SM BPE. Wrote the paper: OK BPE. The authors have declared that no competing interests exist.
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PublicationDecade	2010
PublicationPlace	United States
PublicationPlace_xml	– name: United States – name: San Francisco, CA USA
PublicationTitle	PLoS genetics
PublicationTitleAlternate	PLoS Genet
PublicationYear	2015
Publisher	Public Library of Science Public Library of Science (PLoS)
Publisher_xml	– name: Public Library of Science – name: Public Library of Science (PLoS)
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SubjectTerms	Animals Cancer therapies Cell division Cell growth Cell proliferation Cell Proliferation - genetics Deoxyribonucleic acid Disease DNA DNA damage DNA Damage - genetics DNA Repair - genetics Drug resistance Environmental health Flow cytometry Gene mutation Genetic aspects Health sciences Histones - genetics Homologous Recombination Humans Identification and classification Inflammation Inflammation - complications Inflammation - genetics Inflammation - pathology Mice Mutation Neoplasms - etiology Neoplasms - genetics Neoplasms - pathology Pancreas - pathology Pancreatic cancer Physiology Risk Factors Rodents Studies Tissue engineering
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Title	Inflammation-induced cell proliferation potentiates DNA damage-induced mutations in vivo
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