Decreased Expression of the DNA Mismatch Repair Gene Mlh1 under Hypoxic Stress in Mammalian Cells
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| Published in | Molecular and Cellular Biology Vol. 23; no. 9; pp. 3265 - 3273 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Microbiology
01.05.2003
Taylor & Francis |
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| Online Access | Get full text |
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| AbstractList | The hypoxic tumor microenvironment has been shown to contribute to genetic instability. As one possible mechanism for this effect, we report that expression of the DNA mismatch repair (MMR) gene Mlh1 is specifically reduced in mammalian cells under hypoxia, whereas expression of other MMR genes, including Msh2, Msh6, and Pms2, is not altered at the mRNA level. However, levels of the PMS2 protein are reduced, consistent with destabilization of PMS2 in the absence of its heterodimer partner, MLH1. The hypoxia-induced reduction in Mlh1 mRNA was prevented by the histone deacetylase inhibitor trichostatin A, suggesting that hypoxia causes decreased Mlh1 transcription via histone deacetylation. In addition, treatment of cells with the iron chelator desferrioxamine also reduced MLH1 and PMS2 levels, in keeping with low oxygen tension being the stress signal that provokes the altered MMR gene expression. Functional MMR deficiency under hypoxia was detected as induced instability of a (CA) sub(29) dinucleotide repeat and by increased mutagenesis in a chromosomal reporter gene. These results identify a potential new pathway of genetic instability in cancer: hypoxia-induced reduction in the expression of key MMR proteins. In addition, this stress-induced genetic instability may represent a conceptual parallel to the pathway of stationary-phase mutagenesis seen in bacteria. The hypoxic tumor microenvironment has been shown to contribute to genetic instability. As one possible mechanism for this effect, we report that expression of the DNA mismatch repair (MMR) gene Mlh1 is specifically reduced in mammalian cells under hypoxia, whereas expression of other MMR genes, including Msh2, Msh6, and Pms2, is not altered at the mRNA level. However, levels of the PMS2 protein are reduced, consistent with destabilization of PMS2 in the absence of its heterodimer partner, MLH1. The hypoxia-induced reduction in Mlh1 mRNA was prevented by the histone deacetylase inhibitor trichostatin A, suggesting that hypoxia causes decreased Mlh1 transcription via histone deacetylation. In addition, treatment of cells with the iron chelator desferrioxamine also reduced MLH1 and PMS2 levels, in keeping with low oxygen tension being the stress signal that provokes the altered MMR gene expression. Functional MMR deficiency under hypoxia was detected as induced instability of a (CA)(29) dinucleotide repeat and by increased mutagenesis in a chromosomal reporter gene. These results identify a potential new pathway of genetic instability in cancer: hypoxia-induced reduction in the expression of key MMR proteins. In addition, this stress-induced genetic instability may represent a conceptual parallel to the pathway of stationary-phase mutagenesis seen in bacteria. The hypoxic tumor microenvironment has been shown to contribute to genetic instability. As one possible mechanism for this effect, we report that expression of the DNA mismatch repair (MMR) gene Mlh1 is specifically reduced in mammalian cells under hypoxia, whereas expression of other MMR genes, including Msh2 , Msh6 , and Pms2 , is not altered at the mRNA level. However, levels of the PMS2 protein are reduced, consistent with destabilization of PMS2 in the absence of its heterodimer partner, MLH1. The hypoxia-induced reduction in Mlh1 mRNA was prevented by the histone deacetylase inhibitor trichostatin A, suggesting that hypoxia causes decreased Mlh1 transcription via histone deacetylation. In addition, treatment of cells with the iron chelator desferrioxamine also reduced MLH1 and PMS2 levels, in keeping with low oxygen tension being the stress signal that provokes the altered MMR gene expression. Functional MMR deficiency under hypoxia was detected as induced instability of a (CA) 29 dinucleotide repeat and by increased mutagenesis in a chromosomal reporter gene. These results identify a potential new pathway of genetic instability in cancer: hypoxia-induced reduction in the expression of key MMR proteins. In addition, this stress-induced genetic instability may represent a conceptual parallel to the pathway of stationary-phase mutagenesis seen in bacteria. The hypoxic tumor microenvironment has been shown to contribute to genetic instability. As one possible mechanism for this effect, we report that expression of the DNA mismatch repair (MMR) gene Mlh1 is specifically reduced in mammalian cells under hypoxia, whereas expression of other MMR genes, including Msh2, Msh6, and Pms2, is not altered at the mRNA level. However, levels of the PMS2 protein are reduced, consistent with destabilization of PMS2 in the absence of its heterodimer partner, MLH1. The hypoxia-induced reduction in Mlh1 mRNA was prevented by the histone deacetylase inhibitor trichostatin A, suggesting that hypoxia causes decreased Mlh1 transcription via histone deacetylation. In addition, treatment of cells with the iron chelator desferrioxamine also reduced MLH1 and PMS2 levels, in keeping with low oxygen tension being the stress signal that provokes the altered MMR gene expression. Functional MMR deficiency under hypoxia was detected as induced instability of a (CA) 29 dinucleotide repeat and by increased mutagenesis in a chromosomal reporter gene. These results identify a potential new pathway of genetic instability in cancer: hypoxia-induced reduction in the expression of key MMR proteins. In addition, this stress-induced genetic instability may represent a conceptual parallel to the pathway of stationary-phase mutagenesis seen in bacteria. Article Usage Stats Services MCB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue MCB About MCB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy MCB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0270-7306 Online ISSN: 1098-5549 Copyright © 2014 by the American Society for Microbiology. For an alternate route to MCB .asm.org, visit: MCB |
| Author | Denise Campisi Peter M. Glazer Frank Giordano Latha Narayanan Sara Rockwell Ranjit S. Bindra Jianling Yuan Ryan Jensen Randall S. Johnson Valia T. Mihaylova |
| AuthorAffiliation | Departments of Therapeutic Radiology, 1 Genetics, 2 Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520-8040, 3 Division of Biology, University of California, San Diego, La Jolla, California 92093 4 |
| AuthorAffiliation_xml | – name: Departments of Therapeutic Radiology, 1 Genetics, 2 Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 06520-8040, 3 Division of Biology, University of California, San Diego, La Jolla, California 92093 4 |
| Author_xml | – sequence: 1 givenname: Valia T. surname: Mihaylova fullname: Mihaylova, Valia T. organization: Genetics – sequence: 2 givenname: Ranjit S. surname: Bindra fullname: Bindra, Ranjit S. organization: Genetics – sequence: 3 givenname: Jianling surname: Yuan fullname: Yuan, Jianling organization: Departments of Therapeutic Radiology – sequence: 4 givenname: Denise surname: Campisi fullname: Campisi, Denise organization: Genetics – sequence: 5 givenname: Latha surname: Narayanan fullname: Narayanan, Latha organization: Genetics – sequence: 6 givenname: Ryan surname: Jensen fullname: Jensen, Ryan organization: Genetics – sequence: 7 givenname: Frank surname: Giordano fullname: Giordano, Frank organization: Internal Medicine, Yale University School of Medicine – sequence: 8 givenname: Randall S. surname: Johnson fullname: Johnson, Randall S. organization: Division of Biology, University of California, San Diego – sequence: 9 givenname: Sara surname: Rockwell fullname: Rockwell, Sara organization: Departments of Therapeutic Radiology – sequence: 10 givenname: Peter M. surname: Glazer fullname: Glazer, Peter M. email: peter.glazer@yale.edu organization: Genetics |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/12697826$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 Corresponding author. Mailing address: Department of Therapeutic Radiology, Yale University School of Medicine, P.O. Box 208040, New Haven, CT 06520-8040. Phone: (203) 737-2788. Fax: (203) 737-2630. E-mail: peter.glazer@yale.edu. |
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Mendeley... The hypoxic tumor microenvironment has been shown to contribute to genetic instability. As one possible mechanism for this effect, we report that expression of... |
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| SubjectTerms | Adaptor Proteins, Signal Transducing Adenosine Triphosphatases - genetics Adenosine Triphosphatases - metabolism Animals Base Pair Mismatch beta-Galactosidase - genetics Carrier Proteins Cell Hypoxia - genetics Cell Hypoxia - physiology Cells, Cultured Deferoxamine - pharmacology Dinucleotide Repeats DNA Dynamics and Chromosome Structure DNA Repair - genetics DNA Repair Enzymes DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Enzyme Inhibitors - pharmacology Fibroblasts - cytology Fibroblasts - metabolism Genes, Reporter HeLa Cells - cytology Humans Hydroxamic Acids - pharmacology Hypoxia-Inducible Factor 1, alpha Subunit Iron Chelating Agents - pharmacology Methylation Mice Mice, Transgenic Mismatch Repair Endonuclease PMS2 MutL Protein Homolog 1 MutS Homolog 2 Protein Neoplasm Proteins - genetics Neoplasm Proteins - metabolism Nuclear Proteins Proto-Oncogene Proteins - drug effects Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism RNA, Messenger - metabolism Transcription Factors - drug effects Transcription Factors - genetics |
| Title | Decreased Expression of the DNA Mismatch Repair Gene Mlh1 under Hypoxic Stress in Mammalian Cells |
| URI | http://mcb.asm.org/content/23/9/3265.abstract https://www.tandfonline.com/doi/abs/10.1128/MCB.23.9.3265-3273.2003 https://www.ncbi.nlm.nih.gov/pubmed/12697826 https://search.proquest.com/docview/18733952 https://pubmed.ncbi.nlm.nih.gov/PMC153206 |
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