Radiation-related genomic profile of papillary thyroid carcinoma after the Chernobyl accident
The 1986 Chernobyl nuclear power plant accident increased papillary thyroid carcinoma (PTC) incidence in surrounding regions, particularly for radioactive iodine ( I)-exposed children. We analyzed genomic, transcriptomic, and epigenomic characteristics of 440 PTCs from Ukraine (from 359 individuals...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2021-05, Vol.372 (6543) |
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| creator | Morton, Lindsay M Karyadi, Danielle M Stewart, Chip Bogdanova, Tetiana I Dawson, Eric T Steinberg, Mia K Dai, Jieqiong Hartley, Stephen W Schonfeld, Sara J Sampson, Joshua N Maruvka, Yosef E Kapoor, Vidushi Ramsden, Dale A Carvajal-Garcia, Juan Perou, Charles M Parker, Joel S Krznaric, Marko Yeager, Meredith Boland, Joseph F Hutchinson, Amy Hicks, Belynda D Dagnall, Casey L Gastier-Foster, Julie M Bowen, Jay Lee, Olivia Machiela, Mitchell J Cahoon, Elizabeth K Brenner, Alina V Mabuchi, Kiyohiko Drozdovitch, Vladimir Masiuk, Sergii Chepurny, Mykola Zurnadzhy, Liudmyla Yu Hatch, Maureen Berrington de Gonzalez, Amy Thomas, Gerry A Tronko, Mykola D Getz, Gad Chanock, Stephen J |
| description | The 1986 Chernobyl nuclear power plant accident increased papillary thyroid carcinoma (PTC) incidence in surrounding regions, particularly for radioactive iodine (
I)-exposed children. We analyzed genomic, transcriptomic, and epigenomic characteristics of 440 PTCs from Ukraine (from 359 individuals with estimated childhood
I exposure and 81 unexposed children born after 1986). PTCs displayed radiation dose-dependent enrichment of fusion drivers, nearly all in the mitogen-activated protein kinase pathway, and increases in small deletions and simple/balanced structural variants that were clonal and bore hallmarks of nonhomologous end-joining repair. Radiation-related genomic alterations were more pronounced for individuals who were younger at exposure. Transcriptomic and epigenomic features were strongly associated with driver events but not radiation dose. Our results point to DNA double-strand breaks as early carcinogenic events that subsequently enable PTC growth after environmental radiation exposure. |
| doi_str_mv | 10.1126/science.abg2538 |
| format | Article |
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I)-exposed children. We analyzed genomic, transcriptomic, and epigenomic characteristics of 440 PTCs from Ukraine (from 359 individuals with estimated childhood
I exposure and 81 unexposed children born after 1986). PTCs displayed radiation dose-dependent enrichment of fusion drivers, nearly all in the mitogen-activated protein kinase pathway, and increases in small deletions and simple/balanced structural variants that were clonal and bore hallmarks of nonhomologous end-joining repair. Radiation-related genomic alterations were more pronounced for individuals who were younger at exposure. Transcriptomic and epigenomic features were strongly associated with driver events but not radiation dose. Our results point to DNA double-strand breaks as early carcinogenic events that subsequently enable PTC growth after environmental radiation exposure.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.abg2538</identifier><identifier>PMID: 33888599</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>Accidents ; Adolescent ; Adult ; Cancer ; Chernobyl Nuclear Accident ; Child ; Child, Preschool ; DNA Copy Number Variations ; DNA methylation ; Epigenome ; Female ; Gene Expression Profiling ; Genes, ras ; Genetic Variation ; Humans ; Infant ; Iodine Radioisotopes ; Kinases ; Loss of Heterozygosity ; Male ; Middle Aged ; Mutation ; Neoplasms, Radiation-Induced - genetics ; Nuclear accidents ; Nuclear accidents & safety ; Nuclear Energy ; Nuclear power plants ; Papillary thyroid cancer ; Proto-Oncogene Proteins B-raf - genetics ; Radiation ; Radiation Dosage ; Radioactive fallout ; RNA-Seq ; Thyroid ; Thyroid cancer ; Thyroid Cancer, Papillary - etiology ; Thyroid Cancer, Papillary - genetics ; Thyroid Gland - physiology ; Thyroid Gland - radiation effects ; Thyroid Neoplasms - etiology ; Thyroid Neoplasms - genetics ; Translocation, Genetic ; Ukraine ; Whole Genome Sequencing ; Young Adult</subject><ispartof>Science (American Association for the Advancement of Science), 2021-05, Vol.372 (6543)</ispartof><rights>Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.</rights><rights>Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c432t-8957d068e9255ec641173e592ec6d0f2151013bfbd3609ab24c2991dac6c03673</citedby><cites>FETCH-LOGICAL-c432t-8957d068e9255ec641173e592ec6d0f2151013bfbd3609ab24c2991dac6c03673</cites><orcidid>0000-0002-7952-379X ; 0000-0002-0936-0753 ; 0000-0003-4164-5625 ; 0000-0002-8028-0588 ; 0000-0001-5119-0236 ; 0000-0001-7334-4718 ; 0000-0001-5389-6267 ; 0000-0001-8014-4888 ; 0000-0002-2324-3393 ; 0000-0001-9827-2247 ; 0000-0002-4368-4647 ; 0000-0001-7141-8031 ; 0000-0001-5448-1653 ; 0000-0001-7257-3674 ; 0000-0001-6861-9043 ; 0000-0001-9767-2310 ; 0000-0003-3871-2225 ; 0000-0001-7642-5265 ; 0000-0002-8556-3907 ; 0000-0001-6776-1136 ; 0000-0001-6538-9705 ; 0000-0001-7421-0981 ; 0000-0001-6584-005X ; 0000-0002-5516-5799 ; 0000-0003-2245-9552 ; 0000-0003-2080-6901 ; 0000-0003-1575-4748 ; 0000-0002-7332-8387 ; 0000-0002-8867-8777 ; 0000-0002-4962-2711</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,2884,2885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33888599$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Morton, Lindsay M</creatorcontrib><creatorcontrib>Karyadi, Danielle M</creatorcontrib><creatorcontrib>Stewart, Chip</creatorcontrib><creatorcontrib>Bogdanova, Tetiana I</creatorcontrib><creatorcontrib>Dawson, Eric T</creatorcontrib><creatorcontrib>Steinberg, Mia K</creatorcontrib><creatorcontrib>Dai, Jieqiong</creatorcontrib><creatorcontrib>Hartley, Stephen W</creatorcontrib><creatorcontrib>Schonfeld, Sara J</creatorcontrib><creatorcontrib>Sampson, Joshua N</creatorcontrib><creatorcontrib>Maruvka, Yosef E</creatorcontrib><creatorcontrib>Kapoor, Vidushi</creatorcontrib><creatorcontrib>Ramsden, Dale A</creatorcontrib><creatorcontrib>Carvajal-Garcia, Juan</creatorcontrib><creatorcontrib>Perou, Charles M</creatorcontrib><creatorcontrib>Parker, Joel S</creatorcontrib><creatorcontrib>Krznaric, Marko</creatorcontrib><creatorcontrib>Yeager, Meredith</creatorcontrib><creatorcontrib>Boland, Joseph F</creatorcontrib><creatorcontrib>Hutchinson, Amy</creatorcontrib><creatorcontrib>Hicks, Belynda D</creatorcontrib><creatorcontrib>Dagnall, Casey L</creatorcontrib><creatorcontrib>Gastier-Foster, Julie M</creatorcontrib><creatorcontrib>Bowen, Jay</creatorcontrib><creatorcontrib>Lee, Olivia</creatorcontrib><creatorcontrib>Machiela, Mitchell J</creatorcontrib><creatorcontrib>Cahoon, Elizabeth K</creatorcontrib><creatorcontrib>Brenner, Alina V</creatorcontrib><creatorcontrib>Mabuchi, Kiyohiko</creatorcontrib><creatorcontrib>Drozdovitch, Vladimir</creatorcontrib><creatorcontrib>Masiuk, Sergii</creatorcontrib><creatorcontrib>Chepurny, Mykola</creatorcontrib><creatorcontrib>Zurnadzhy, Liudmyla Yu</creatorcontrib><creatorcontrib>Hatch, Maureen</creatorcontrib><creatorcontrib>Berrington de Gonzalez, Amy</creatorcontrib><creatorcontrib>Thomas, Gerry A</creatorcontrib><creatorcontrib>Tronko, Mykola D</creatorcontrib><creatorcontrib>Getz, Gad</creatorcontrib><creatorcontrib>Chanock, Stephen J</creatorcontrib><title>Radiation-related genomic profile of papillary thyroid carcinoma after the Chernobyl accident</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>The 1986 Chernobyl nuclear power plant accident increased papillary thyroid carcinoma (PTC) incidence in surrounding regions, particularly for radioactive iodine (
I)-exposed children. We analyzed genomic, transcriptomic, and epigenomic characteristics of 440 PTCs from Ukraine (from 359 individuals with estimated childhood
I exposure and 81 unexposed children born after 1986). PTCs displayed radiation dose-dependent enrichment of fusion drivers, nearly all in the mitogen-activated protein kinase pathway, and increases in small deletions and simple/balanced structural variants that were clonal and bore hallmarks of nonhomologous end-joining repair. Radiation-related genomic alterations were more pronounced for individuals who were younger at exposure. Transcriptomic and epigenomic features were strongly associated with driver events but not radiation dose. Our results point to DNA double-strand breaks as early carcinogenic events that subsequently enable PTC growth after environmental radiation exposure.</description><subject>Accidents</subject><subject>Adolescent</subject><subject>Adult</subject><subject>Cancer</subject><subject>Chernobyl Nuclear Accident</subject><subject>Child</subject><subject>Child, Preschool</subject><subject>DNA Copy Number Variations</subject><subject>DNA methylation</subject><subject>Epigenome</subject><subject>Female</subject><subject>Gene Expression Profiling</subject><subject>Genes, ras</subject><subject>Genetic Variation</subject><subject>Humans</subject><subject>Infant</subject><subject>Iodine Radioisotopes</subject><subject>Kinases</subject><subject>Loss of Heterozygosity</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Mutation</subject><subject>Neoplasms, Radiation-Induced - genetics</subject><subject>Nuclear accidents</subject><subject>Nuclear accidents & safety</subject><subject>Nuclear Energy</subject><subject>Nuclear power plants</subject><subject>Papillary thyroid cancer</subject><subject>Proto-Oncogene Proteins B-raf - genetics</subject><subject>Radiation</subject><subject>Radiation Dosage</subject><subject>Radioactive fallout</subject><subject>RNA-Seq</subject><subject>Thyroid</subject><subject>Thyroid cancer</subject><subject>Thyroid Cancer, Papillary - etiology</subject><subject>Thyroid Cancer, Papillary - genetics</subject><subject>Thyroid Gland - physiology</subject><subject>Thyroid Gland - radiation effects</subject><subject>Thyroid Neoplasms - etiology</subject><subject>Thyroid Neoplasms - genetics</subject><subject>Translocation, Genetic</subject><subject>Ukraine</subject><subject>Whole Genome Sequencing</subject><subject>Young 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genomic profile of papillary thyroid carcinoma after the Chernobyl accident</title><author>Morton, Lindsay M ; Karyadi, Danielle M ; Stewart, Chip ; Bogdanova, Tetiana I ; Dawson, Eric T ; Steinberg, Mia K ; Dai, Jieqiong ; Hartley, Stephen W ; Schonfeld, Sara J ; Sampson, Joshua N ; Maruvka, Yosef E ; Kapoor, Vidushi ; Ramsden, Dale A ; Carvajal-Garcia, Juan ; Perou, Charles M ; Parker, Joel S ; Krznaric, Marko ; Yeager, Meredith ; Boland, Joseph F ; Hutchinson, Amy ; Hicks, Belynda D ; Dagnall, Casey L ; Gastier-Foster, Julie M ; Bowen, Jay ; Lee, Olivia ; Machiela, Mitchell J ; Cahoon, Elizabeth K ; Brenner, Alina V ; Mabuchi, Kiyohiko ; Drozdovitch, Vladimir ; Masiuk, Sergii ; Chepurny, Mykola ; Zurnadzhy, Liudmyla Yu ; Hatch, Maureen ; Berrington de Gonzalez, Amy ; Thomas, Gerry A ; Tronko, Mykola D ; Getz, Gad ; Chanock, Stephen 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Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Morton, Lindsay M</au><au>Karyadi, Danielle M</au><au>Stewart, Chip</au><au>Bogdanova, Tetiana I</au><au>Dawson, Eric T</au><au>Steinberg, Mia K</au><au>Dai, Jieqiong</au><au>Hartley, Stephen W</au><au>Schonfeld, Sara J</au><au>Sampson, Joshua N</au><au>Maruvka, Yosef E</au><au>Kapoor, Vidushi</au><au>Ramsden, Dale A</au><au>Carvajal-Garcia, Juan</au><au>Perou, Charles M</au><au>Parker, Joel S</au><au>Krznaric, Marko</au><au>Yeager, Meredith</au><au>Boland, Joseph F</au><au>Hutchinson, Amy</au><au>Hicks, Belynda D</au><au>Dagnall, Casey L</au><au>Gastier-Foster, Julie M</au><au>Bowen, Jay</au><au>Lee, Olivia</au><au>Machiela, Mitchell J</au><au>Cahoon, Elizabeth K</au><au>Brenner, Alina V</au><au>Mabuchi, Kiyohiko</au><au>Drozdovitch, Vladimir</au><au>Masiuk, Sergii</au><au>Chepurny, Mykola</au><au>Zurnadzhy, Liudmyla Yu</au><au>Hatch, Maureen</au><au>Berrington de Gonzalez, Amy</au><au>Thomas, Gerry A</au><au>Tronko, Mykola D</au><au>Getz, Gad</au><au>Chanock, Stephen J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Radiation-related genomic profile of papillary thyroid carcinoma after the Chernobyl accident</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2021-05-14</date><risdate>2021</risdate><volume>372</volume><issue>6543</issue><issn>0036-8075</issn><eissn>1095-9203</eissn><abstract>The 1986 Chernobyl nuclear power plant accident increased papillary thyroid carcinoma (PTC) incidence in surrounding regions, particularly for radioactive iodine (
I)-exposed children. We analyzed genomic, transcriptomic, and epigenomic characteristics of 440 PTCs from Ukraine (from 359 individuals with estimated childhood
I exposure and 81 unexposed children born after 1986). PTCs displayed radiation dose-dependent enrichment of fusion drivers, nearly all in the mitogen-activated protein kinase pathway, and increases in small deletions and simple/balanced structural variants that were clonal and bore hallmarks of nonhomologous end-joining repair. Radiation-related genomic alterations were more pronounced for individuals who were younger at exposure. Transcriptomic and epigenomic features were strongly associated with driver events but not radiation dose. Our results point to DNA double-strand breaks as early carcinogenic events that subsequently enable PTC growth after environmental radiation exposure.</abstract><cop>United States</cop><pub>The American Association for the Advancement of Science</pub><pmid>33888599</pmid><doi>10.1126/science.abg2538</doi><orcidid>https://orcid.org/0000-0002-7952-379X</orcidid><orcidid>https://orcid.org/0000-0002-0936-0753</orcidid><orcidid>https://orcid.org/0000-0003-4164-5625</orcidid><orcidid>https://orcid.org/0000-0002-8028-0588</orcidid><orcidid>https://orcid.org/0000-0001-5119-0236</orcidid><orcidid>https://orcid.org/0000-0001-7334-4718</orcidid><orcidid>https://orcid.org/0000-0001-5389-6267</orcidid><orcidid>https://orcid.org/0000-0001-8014-4888</orcidid><orcidid>https://orcid.org/0000-0002-2324-3393</orcidid><orcidid>https://orcid.org/0000-0001-9827-2247</orcidid><orcidid>https://orcid.org/0000-0002-4368-4647</orcidid><orcidid>https://orcid.org/0000-0001-7141-8031</orcidid><orcidid>https://orcid.org/0000-0001-5448-1653</orcidid><orcidid>https://orcid.org/0000-0001-7257-3674</orcidid><orcidid>https://orcid.org/0000-0001-6861-9043</orcidid><orcidid>https://orcid.org/0000-0001-9767-2310</orcidid><orcidid>https://orcid.org/0000-0003-3871-2225</orcidid><orcidid>https://orcid.org/0000-0001-7642-5265</orcidid><orcidid>https://orcid.org/0000-0002-8556-3907</orcidid><orcidid>https://orcid.org/0000-0001-6776-1136</orcidid><orcidid>https://orcid.org/0000-0001-6538-9705</orcidid><orcidid>https://orcid.org/0000-0001-7421-0981</orcidid><orcidid>https://orcid.org/0000-0001-6584-005X</orcidid><orcidid>https://orcid.org/0000-0002-5516-5799</orcidid><orcidid>https://orcid.org/0000-0003-2245-9552</orcidid><orcidid>https://orcid.org/0000-0003-2080-6901</orcidid><orcidid>https://orcid.org/0000-0003-1575-4748</orcidid><orcidid>https://orcid.org/0000-0002-7332-8387</orcidid><orcidid>https://orcid.org/0000-0002-8867-8777</orcidid><orcidid>https://orcid.org/0000-0002-4962-2711</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0036-8075 |
| ispartof | Science (American Association for the Advancement of Science), 2021-05, Vol.372 (6543) |
| issn | 0036-8075 1095-9203 |
| language | eng |
| recordid | cdi_proquest_journals_2516991768 |
| source | MEDLINE; American Association for the Advancement of Science |
| subjects | Accidents Adolescent Adult Cancer Chernobyl Nuclear Accident Child Child, Preschool DNA Copy Number Variations DNA methylation Epigenome Female Gene Expression Profiling Genes, ras Genetic Variation Humans Infant Iodine Radioisotopes Kinases Loss of Heterozygosity Male Middle Aged Mutation Neoplasms, Radiation-Induced - genetics Nuclear accidents Nuclear accidents & safety Nuclear Energy Nuclear power plants Papillary thyroid cancer Proto-Oncogene Proteins B-raf - genetics Radiation Radiation Dosage Radioactive fallout RNA-Seq Thyroid Thyroid cancer Thyroid Cancer, Papillary - etiology Thyroid Cancer, Papillary - genetics Thyroid Gland - physiology Thyroid Gland - radiation effects Thyroid Neoplasms - etiology Thyroid Neoplasms - genetics Translocation, Genetic Ukraine Whole Genome Sequencing Young Adult |
| title | Radiation-related genomic profile of papillary thyroid carcinoma after the Chernobyl accident |
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