Mutational signatures associated with tobacco smoking in human cancer

Alexandrov, L. B.; Ju, Y. S.; Haase, K.; Van Loo, P.; Martincorena, I.; Nik-Zainal, S.; Totoki, Y.; Fujimoto, A.; Nakagawa, H.; Shibata, T.; Campbell, P. J.; Vineis, P.; Phillips, D. H.; Stratton, M. R.

doi:10.1126/science.aag0299

Title: Mutational signatures associated with tobacco smoking in human cancer

Journal Article · Thu Nov 03 00:00:00 EDT 2016 · Science

DOI:https://doi.org/10.1126/science.aag0299· OSTI ID:1347826

Alexandrov, L. B.; Ju, Y. S.; Haase, K.; Van Loo, P.; Martincorena, I.; Nik-Zainal, S.; Totoki, Y.; Fujimoto, A.; Nakagawa, H.; Shibata, T.; Campbell, P. J.; Vineis, P.; Phillips, D. H.; Stratton, M. R.

Tobacco smoking increases the risk of at least 17 classes of cancer. Here, we analyzed somatic mutations and DNA methylation in 5,243 cancers of types for which tobacco smoking confers an elevated risk. Smoking is associated with increased mutation burdens of multiple distinct mutational signatures, which contribute to different extents in different cancers. One of these signatures, mainly found in cancers derived from tissues directly exposed to tobacco smoke, is attributable to misreplication of DNA damage caused by tobacco carcinogens. Others likely reflect indirect activation of DNA edi ting by APOBEC cytidine deaminases and of an endogenous clock-like mutational process. Smoking is associated with limited differences in methylation. The results are consistent with the proposition that smoking increases cancer risk by increasing the somatic mutation load, although direct evidence for this mechanism is lacking in some smoking-related cancer types.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA); Wellcome Trust; European Commission (EC)

Grant/Contract Number:: AC52-06NA25396; 098051; WT100183MA; 15ck0106094h0002; 308610-FP7; 101126/Z/13/Z; 101126/B/13/Z; WT088340MA; FC001202; C313/A14329; 02

OSTI ID:: 1347826

Alternate ID(s):: OSTI ID: 1340930

Report Number(s):: LA-UR-16-23165; 354/6312/618

Journal Information:: Science, Journal Name: Science Vol. 354 Journal Issue: 6312; ISSN 0036-8075

Publisher:: American Association for the Advancement of Science (AAAS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 614 works

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Cigarette smoking and lung cancer-relative risk estimates for the major histological types from a pooled analysis of case-control studies Pesch, Beate; Kendzia, Benjamin; Gustavsson, Per International Journal of Cancer, Vol. 131, Issue 5 https://doi.org/10.1002/ijc.27339	journal	December 2011
DNA and protein adducts in human tissues resulting from exposure to tobacco smoke Phillips, David H.; Venitt, Stan International Journal of Cancer, Vol. 131, Issue 12 https://doi.org/10.1002/ijc.27827	journal	October 2012
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Mutational signatures: the patterns of somatic mutations hidden in cancer genomes Alexandrov, Ludmil B.; Stratton, Michael R. Current Opinion in Genetics & Development, Vol. 24 https://doi.org/10.1016/j.gde.2013.11.014	journal	February 2014
Clustered Mutations in Yeast and in Human Cancers Can Arise from Damaged Long Single-Strand DNA Regions Roberts, Steven A.; Sterling, Joan; Thompson, Cole Molecular Cell, Vol. 46, Issue 4 https://doi.org/10.1016/j.molcel.2012.03.030	journal	May 2012
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Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants Fu, Wenqing; O’Connor, Timothy D.; Jun, Goo Nature, Vol. 493, Issue 7431 https://doi.org/10.1038/nature11690	journal	November 2012
Signatures of mutational processes in human cancer Alexandrov, Ludmil B.; Nik-Zainal, Serena; Wedge, David C. Nature, Vol. 500, Issue 7463 https://doi.org/10.1038/nature12477	journal	August 2013
Genome sequencing of normal cells reveals developmental lineages and mutational processes Behjati, Sam; Huch, Meritxell; van Boxtel, Ruben Nature, Vol. 513, Issue 7518 https://doi.org/10.1038/nature13448	journal	June 2014
Heterogeneity of genomic evolution and mutational profiles in multiple myeloma Bolli, Niccolo; Avet-Loiseau, Hervé; Wedge, David C. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms3997	journal	January 2014
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Clock-like mutational processes in human somatic cells Alexandrov, Ludmil B.; Jones, Philip H.; Wedge, David C. Nature Genetics, Vol. 47, Issue 12 https://doi.org/10.1038/ng.3441	journal	November 2015
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The genome as a record of environmental exposure Nik-Zainal, Serena; Kucab, Jill E.; Morganella, Sandro Mutagenesis https://doi.org/10.1093/mutage/gev073	journal	October 2015
dbSNP: the NCBI database of genetic variation Sherry, S. T. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.308	journal	January 2001
Transmissible Dog Cancer Genome Reveals the Origin and History of an Ancient Cell Lineage Murchison, E. P.; Wedge, D. C.; Alexandrov, L. B. Science, Vol. 343, Issue 6169 https://doi.org/10.1126/science.1247167	journal	January 2014
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