Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor
Canine transmissible venereal tumor (CTVT) is a parasitic cancer clone that has propagated for thousands of years via sexual transfer of malignant cells. Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell...
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| Veröffentlicht in: | Genome research 2015-11, Vol.25 (11), p.1646-1655 |
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| creator | Decker, Brennan Davis, Brian W Rimbault, Maud Long, Adrienne H Karlins, Eric Jagannathan, Vidhya Reiman, Rebecca Parker, Heidi G Drögemüller, Cord Corneveaux, Jason J Chapman, Erica S Trent, Jeffery M Leeb, Tosso Huentelman, Matthew J Wayne, Robert K Karyadi, Danielle M Ostrander, Elaine A |
| description | Canine transmissible venereal tumor (CTVT) is a parasitic cancer clone that has propagated for thousands of years via sexual transfer of malignant cells. Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell lineage. We created the largest existing catalog of canine genome-wide variation and compared it against two CTVT genome sequences, thereby separating alleles derived from the founder's genome from somatic mutations that must drive clonal transmissibility. We show that CTVT has undergone continuous adaptation to its transmissible allograft niche, with overlapping mutations at every step of immunosurveillance, particularly self-antigen presentation and apoptosis. We also identified chronologically early somatic mutations in oncogenesis- and immune-related genes that may represent key initiators of clonal transmissibility. Thus, we provide the first insights into the specific genomic aberrations that underlie CTVT's dogged perseverance in canids around the world. |
| doi_str_mv | 10.1101/gr.190314.115 |
| format | Article |
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Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell lineage. We created the largest existing catalog of canine genome-wide variation and compared it against two CTVT genome sequences, thereby separating alleles derived from the founder's genome from somatic mutations that must drive clonal transmissibility. We show that CTVT has undergone continuous adaptation to its transmissible allograft niche, with overlapping mutations at every step of immunosurveillance, particularly self-antigen presentation and apoptosis. We also identified chronologically early somatic mutations in oncogenesis- and immune-related genes that may represent key initiators of clonal transmissibility. Thus, we provide the first insights into the specific genomic aberrations that underlie CTVT's dogged perseverance in canids around the world.</description><identifier>ISSN: 1088-9051</identifier><identifier>EISSN: 1549-5469</identifier><identifier>DOI: 10.1101/gr.190314.115</identifier><identifier>PMID: 26232412</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; Apoptosis ; Autoantigens - genetics ; CARD Signaling Adaptor Proteins - genetics ; Cell Adhesion Molecules - genetics ; Cell Line, Tumor ; Cell Lineage - genetics ; Collagen Type XI - genetics ; DNA-Binding Proteins - genetics ; Dog Diseases - diagnosis ; Dog Diseases - genetics ; Dogs - genetics ; Genetic Association Studies ; Genetic Variation ; Genome ; Guanine Nucleotide Exchange Factors - genetics ; Heparan Sulfate Proteoglycans - genetics ; Microfilament Proteins - genetics ; Mutation ; Myotonin-Protein Kinase - genetics ; Phylogeny ; Principal Component Analysis ; Sequence Analysis, DNA ; Venereal Tumors, Veterinary - diagnosis ; Venereal Tumors, Veterinary - genetics</subject><ispartof>Genome research, 2015-11, Vol.25 (11), p.1646-1655</ispartof><rights>2015 Decker et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c420t-afee11766eac5de8a710e9afe1d11177ff353f5104b84bcde927ba5e1fe10e1b3</citedby><cites>FETCH-LOGICAL-c420t-afee11766eac5de8a710e9afe1d11177ff353f5104b84bcde927ba5e1fe10e1b3</cites><orcidid>0000-0002-6121-135X ; 0000-0003-4516-7421</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4617961/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4617961/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26232412$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Decker, Brennan</creatorcontrib><creatorcontrib>Davis, Brian W</creatorcontrib><creatorcontrib>Rimbault, Maud</creatorcontrib><creatorcontrib>Long, Adrienne H</creatorcontrib><creatorcontrib>Karlins, Eric</creatorcontrib><creatorcontrib>Jagannathan, Vidhya</creatorcontrib><creatorcontrib>Reiman, Rebecca</creatorcontrib><creatorcontrib>Parker, Heidi G</creatorcontrib><creatorcontrib>Drögemüller, Cord</creatorcontrib><creatorcontrib>Corneveaux, Jason J</creatorcontrib><creatorcontrib>Chapman, Erica S</creatorcontrib><creatorcontrib>Trent, Jeffery M</creatorcontrib><creatorcontrib>Leeb, Tosso</creatorcontrib><creatorcontrib>Huentelman, Matthew J</creatorcontrib><creatorcontrib>Wayne, Robert K</creatorcontrib><creatorcontrib>Karyadi, Danielle M</creatorcontrib><creatorcontrib>Ostrander, Elaine A</creatorcontrib><title>Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor</title><title>Genome research</title><addtitle>Genome Res</addtitle><description>Canine transmissible venereal tumor (CTVT) is a parasitic cancer clone that has propagated for thousands of years via sexual transfer of malignant cells. Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell lineage. We created the largest existing catalog of canine genome-wide variation and compared it against two CTVT genome sequences, thereby separating alleles derived from the founder's genome from somatic mutations that must drive clonal transmissibility. We show that CTVT has undergone continuous adaptation to its transmissible allograft niche, with overlapping mutations at every step of immunosurveillance, particularly self-antigen presentation and apoptosis. We also identified chronologically early somatic mutations in oncogenesis- and immune-related genes that may represent key initiators of clonal transmissibility. Thus, we provide the first insights into the specific genomic aberrations that underlie CTVT's dogged perseverance in canids around the world.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Autoantigens - genetics</subject><subject>CARD Signaling Adaptor Proteins - genetics</subject><subject>Cell Adhesion Molecules - genetics</subject><subject>Cell Line, Tumor</subject><subject>Cell Lineage - genetics</subject><subject>Collagen Type XI - genetics</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Dog Diseases - diagnosis</subject><subject>Dog Diseases - genetics</subject><subject>Dogs - genetics</subject><subject>Genetic Association Studies</subject><subject>Genetic Variation</subject><subject>Genome</subject><subject>Guanine Nucleotide Exchange Factors - genetics</subject><subject>Heparan Sulfate Proteoglycans - genetics</subject><subject>Microfilament Proteins - genetics</subject><subject>Mutation</subject><subject>Myotonin-Protein Kinase - genetics</subject><subject>Phylogeny</subject><subject>Principal Component Analysis</subject><subject>Sequence Analysis, DNA</subject><subject>Venereal Tumors, Veterinary - diagnosis</subject><subject>Venereal Tumors, Veterinary - genetics</subject><issn>1088-9051</issn><issn>1549-5469</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1TAQhS0EoqVlyRZ5ySbFEz_ibJDQFY9KldjQteU4k9TIsS92clGX_HPc3lLRHSt7Zj4dnZlDyBtgFwAM3s_5AnrGQdRSPiOnIEXfSKH65_XPtG56JuGEvCrlB2OMC61fkpNWtbwV0J6S37u07G32JUVqZ-tjWSloRZ2NfqS_blLAZsaYFqQFf24YHRaa8YA2FFq2fPAHG2hZs11x9nWWJmqrVHQe40pdSNGGcEsrEMviS_FDwHv1iHTdlpTPyYupiuHrh_eMXH_-9H33tbn69uVy9_GqcaJla2MnRIBOKbROjqhtBwz72oURar-bJi75JIGJQYvBjdi33WAlQiUYwsDPyIej7n4bFhxdtZdtMPvsF5tvTbLePJ1Ef2PmdDBCQdcrqALvHgRyqpcoq6n7OAzBRkxbMdUE16Lt9P-gnLFWdYpXtDmiLqdSMk6PjoCZu4TNnM0x4VrKyr_9d41H-m-k_A-gmKXI</recordid><startdate>201511</startdate><enddate>201511</enddate><creator>Decker, Brennan</creator><creator>Davis, Brian W</creator><creator>Rimbault, Maud</creator><creator>Long, Adrienne H</creator><creator>Karlins, Eric</creator><creator>Jagannathan, Vidhya</creator><creator>Reiman, Rebecca</creator><creator>Parker, Heidi G</creator><creator>Drögemüller, Cord</creator><creator>Corneveaux, Jason J</creator><creator>Chapman, Erica S</creator><creator>Trent, Jeffery M</creator><creator>Leeb, Tosso</creator><creator>Huentelman, Matthew J</creator><creator>Wayne, Robert K</creator><creator>Karyadi, Danielle M</creator><creator>Ostrander, Elaine A</creator><general>Cold Spring Harbor Laboratory Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6121-135X</orcidid><orcidid>https://orcid.org/0000-0003-4516-7421</orcidid></search><sort><creationdate>201511</creationdate><title>Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor</title><author>Decker, Brennan ; Davis, Brian W ; Rimbault, Maud ; Long, Adrienne H ; Karlins, Eric ; Jagannathan, Vidhya ; Reiman, Rebecca ; Parker, Heidi G ; Drögemüller, Cord ; Corneveaux, Jason J ; Chapman, Erica S ; Trent, Jeffery M ; Leeb, Tosso ; Huentelman, Matthew J ; Wayne, Robert K ; Karyadi, Danielle M ; Ostrander, Elaine A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c420t-afee11766eac5de8a710e9afe1d11177ff353f5104b84bcde927ba5e1fe10e1b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Autoantigens - genetics</topic><topic>CARD Signaling Adaptor Proteins - genetics</topic><topic>Cell Adhesion Molecules - genetics</topic><topic>Cell Line, Tumor</topic><topic>Cell Lineage - genetics</topic><topic>Collagen Type XI - genetics</topic><topic>DNA-Binding Proteins - genetics</topic><topic>Dog Diseases - diagnosis</topic><topic>Dog Diseases - genetics</topic><topic>Dogs - genetics</topic><topic>Genetic Association Studies</topic><topic>Genetic Variation</topic><topic>Genome</topic><topic>Guanine Nucleotide Exchange Factors - genetics</topic><topic>Heparan Sulfate Proteoglycans - genetics</topic><topic>Microfilament Proteins - genetics</topic><topic>Mutation</topic><topic>Myotonin-Protein Kinase - genetics</topic><topic>Phylogeny</topic><topic>Principal Component Analysis</topic><topic>Sequence Analysis, DNA</topic><topic>Venereal Tumors, Veterinary - diagnosis</topic><topic>Venereal Tumors, Veterinary - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Decker, Brennan</creatorcontrib><creatorcontrib>Davis, Brian W</creatorcontrib><creatorcontrib>Rimbault, Maud</creatorcontrib><creatorcontrib>Long, Adrienne H</creatorcontrib><creatorcontrib>Karlins, Eric</creatorcontrib><creatorcontrib>Jagannathan, Vidhya</creatorcontrib><creatorcontrib>Reiman, Rebecca</creatorcontrib><creatorcontrib>Parker, Heidi G</creatorcontrib><creatorcontrib>Drögemüller, Cord</creatorcontrib><creatorcontrib>Corneveaux, Jason J</creatorcontrib><creatorcontrib>Chapman, Erica S</creatorcontrib><creatorcontrib>Trent, Jeffery M</creatorcontrib><creatorcontrib>Leeb, Tosso</creatorcontrib><creatorcontrib>Huentelman, Matthew J</creatorcontrib><creatorcontrib>Wayne, Robert K</creatorcontrib><creatorcontrib>Karyadi, Danielle M</creatorcontrib><creatorcontrib>Ostrander, Elaine A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Decker, Brennan</au><au>Davis, Brian W</au><au>Rimbault, Maud</au><au>Long, Adrienne H</au><au>Karlins, Eric</au><au>Jagannathan, Vidhya</au><au>Reiman, Rebecca</au><au>Parker, Heidi G</au><au>Drögemüller, Cord</au><au>Corneveaux, Jason J</au><au>Chapman, Erica S</au><au>Trent, Jeffery M</au><au>Leeb, Tosso</au><au>Huentelman, Matthew J</au><au>Wayne, Robert K</au><au>Karyadi, Danielle M</au><au>Ostrander, Elaine A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor</atitle><jtitle>Genome research</jtitle><addtitle>Genome Res</addtitle><date>2015-11</date><risdate>2015</risdate><volume>25</volume><issue>11</issue><spage>1646</spage><epage>1655</epage><pages>1646-1655</pages><issn>1088-9051</issn><eissn>1549-5469</eissn><abstract>Canine transmissible venereal tumor (CTVT) is a parasitic cancer clone that has propagated for thousands of years via sexual transfer of malignant cells. Little is understood about the mechanisms that converted an ancient tumor into the world's oldest known continuously propagating somatic cell lineage. We created the largest existing catalog of canine genome-wide variation and compared it against two CTVT genome sequences, thereby separating alleles derived from the founder's genome from somatic mutations that must drive clonal transmissibility. We show that CTVT has undergone continuous adaptation to its transmissible allograft niche, with overlapping mutations at every step of immunosurveillance, particularly self-antigen presentation and apoptosis. We also identified chronologically early somatic mutations in oncogenesis- and immune-related genes that may represent key initiators of clonal transmissibility. Thus, we provide the first insights into the specific genomic aberrations that underlie CTVT's dogged perseverance in canids around the world.</abstract><cop>United States</cop><pub>Cold Spring Harbor Laboratory Press</pub><pmid>26232412</pmid><doi>10.1101/gr.190314.115</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-6121-135X</orcidid><orcidid>https://orcid.org/0000-0003-4516-7421</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Apoptosis Autoantigens - genetics CARD Signaling Adaptor Proteins - genetics Cell Adhesion Molecules - genetics Cell Line, Tumor Cell Lineage - genetics Collagen Type XI - genetics DNA-Binding Proteins - genetics Dog Diseases - diagnosis Dog Diseases - genetics Dogs - genetics Genetic Association Studies Genetic Variation Genome Guanine Nucleotide Exchange Factors - genetics Heparan Sulfate Proteoglycans - genetics Microfilament Proteins - genetics Mutation Myotonin-Protein Kinase - genetics Phylogeny Principal Component Analysis Sequence Analysis, DNA Venereal Tumors, Veterinary - diagnosis Venereal Tumors, Veterinary - genetics |
| title | Comparison against 186 canid whole-genome sequences reveals survival strategies of an ancient clonally transmissible canine tumor |
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