The differentiation state of the Schwann cell progenitor drives phenotypic variation between two contagious cancers
Contagious cancers are a rare pathogenic phenomenon in which cancer cells gain the ability to spread between genetically distinct hosts. Nine examples have been identified across marine bivalves, dogs and Tasmanian devils, but the Tasmanian devil is the only mammalian species known to have given ris...
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description | Contagious cancers are a rare pathogenic phenomenon in which cancer cells gain the ability to spread between genetically distinct hosts. Nine examples have been identified across marine bivalves, dogs and Tasmanian devils, but the Tasmanian devil is the only mammalian species known to have given rise to two distinct lineages of contagious cancer, termed Devil Facial Tumour 1 (DFT1) and 2 (DFT2). Remarkably, DFT1 and DFT2 arose independently from the same cell type, a Schwann cell, and while their ultra-structural features are highly similar they exhibit variation in their mutational signatures and infection dynamics. As such, DFT1 and DFT2 provide a unique framework for investigating how a common progenitor cell can give rise to distinct contagious cancers. Using a proteomics approach, we show that DFT1 and DFT2 are derived from Schwann cells in different differentiation states, with DFT2 carrying a molecular signature of a less well differentiated Schwann cell. Under inflammatory signals DFT1 and DFT2 have different gene expression profiles, most notably involving Schwann cell markers of differentiation, reflecting the influence of their distinct origins. Further, DFT2 cells express immune cell markers typically expressed during nerve repair, consistent with an ability to manipulate their extracellular environment, facilitating the cell's ability to transmit between individuals. The emergence of two contagious cancers in the Tasmanian devil suggests that the inherent plasticity of Schwann cells confers a vulnerability to the formation of contagious cancers. |
doi_str_mv | 10.1371/journal.ppat.1010033 |
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Nine examples have been identified across marine bivalves, dogs and Tasmanian devils, but the Tasmanian devil is the only mammalian species known to have given rise to two distinct lineages of contagious cancer, termed Devil Facial Tumour 1 (DFT1) and 2 (DFT2). Remarkably, DFT1 and DFT2 arose independently from the same cell type, a Schwann cell, and while their ultra-structural features are highly similar they exhibit variation in their mutational signatures and infection dynamics. As such, DFT1 and DFT2 provide a unique framework for investigating how a common progenitor cell can give rise to distinct contagious cancers. Using a proteomics approach, we show that DFT1 and DFT2 are derived from Schwann cells in different differentiation states, with DFT2 carrying a molecular signature of a less well differentiated Schwann cell. Under inflammatory signals DFT1 and DFT2 have different gene expression profiles, most notably involving Schwann cell markers of differentiation, reflecting the influence of their distinct origins. Further, DFT2 cells express immune cell markers typically expressed during nerve repair, consistent with an ability to manipulate their extracellular environment, facilitating the cell's ability to transmit between individuals. The emergence of two contagious cancers in the Tasmanian devil suggests that the inherent plasticity of Schwann cells confers a vulnerability to the formation of contagious cancers.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1010033</identifier><identifier>PMID: 34780568</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animal Diseases - genetics ; Animal Diseases - metabolism ; Animal Diseases - pathology ; Animals ; Biological Variation, Population ; Biology and Life Sciences ; Biomarkers ; Breast cancer ; Cancer ; Cancer cells ; Cell Differentiation ; Cells (biology) ; Communicable Diseases - genetics ; Communicable Diseases - metabolism ; Communicable Diseases - pathology ; Differentiation ; Drug resistance ; Facial Neoplasms - classification ; Facial Neoplasms - veterinary ; Fibroblasts ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Neoplastic ; Genetic aspects ; Genotype & phenotype ; Growth ; Growth factors ; Immune system ; Inflammation ; Marsupialia ; Medicine and Health Sciences ; Metastasis ; Mollusks ; Nervous system ; Phenotypic variations ; Progenitor cells ; Protein expression ; Proteins ; Proteome - analysis ; Proteome - metabolism ; Proteomics ; Schwann cells ; Schwann Cells - metabolism ; Schwann Cells - pathology ; Shellfish ; Stem cells ; Transcriptome ; Tumors</subject><ispartof>PLoS pathogens, 2021-11, Vol.17 (11), p.e1010033-e1010033</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Owen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Owen et al 2021 Owen et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c661t-c5d4290bd98a9ea2e2d5e3ebfd05aa933604ad70495c689615ea1198e9c82bfb3</citedby><cites>FETCH-LOGICAL-c661t-c5d4290bd98a9ea2e2d5e3ebfd05aa933604ad70495c689615ea1198e9c82bfb3</cites><orcidid>0000-0002-2787-1282 ; 0000-0003-0023-8679 ; 0000-0002-2995-2959 ; 0000-0003-0532-8331 ; 0000-0002-8882-1502 ; 0000-0001-6441-2213 ; 0000-0003-2906-4385</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/PMC8629380/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8629380/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34780568$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Malik, Harmit S.</contributor><creatorcontrib>Owen, Rachel S</creatorcontrib><creatorcontrib>Ramarathinam, Sri H</creatorcontrib><creatorcontrib>Bailey, Alistair</creatorcontrib><creatorcontrib>Gastaldello, Annalisa</creatorcontrib><creatorcontrib>Hussey, Kathryn</creatorcontrib><creatorcontrib>Skipp, Paul J</creatorcontrib><creatorcontrib>Purcell, Anthony W</creatorcontrib><creatorcontrib>Siddle, Hannah V</creatorcontrib><title>The differentiation state of the Schwann cell progenitor drives phenotypic variation between two contagious cancers</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Contagious cancers are a rare pathogenic phenomenon in which cancer cells gain the ability to spread between genetically distinct hosts. 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Under inflammatory signals DFT1 and DFT2 have different gene expression profiles, most notably involving Schwann cell markers of differentiation, reflecting the influence of their distinct origins. Further, DFT2 cells express immune cell markers typically expressed during nerve repair, consistent with an ability to manipulate their extracellular environment, facilitating the cell's ability to transmit between individuals. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Owen, Rachel S</au><au>Ramarathinam, Sri H</au><au>Bailey, Alistair</au><au>Gastaldello, Annalisa</au><au>Hussey, Kathryn</au><au>Skipp, Paul J</au><au>Purcell, Anthony W</au><au>Siddle, Hannah V</au><au>Malik, Harmit S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The differentiation state of the Schwann cell progenitor drives phenotypic variation between two contagious cancers</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>17</volume><issue>11</issue><spage>e1010033</spage><epage>e1010033</epage><pages>e1010033-e1010033</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Contagious cancers are a rare pathogenic phenomenon in which cancer cells gain the ability to spread between genetically distinct hosts. Nine examples have been identified across marine bivalves, dogs and Tasmanian devils, but the Tasmanian devil is the only mammalian species known to have given rise to two distinct lineages of contagious cancer, termed Devil Facial Tumour 1 (DFT1) and 2 (DFT2). Remarkably, DFT1 and DFT2 arose independently from the same cell type, a Schwann cell, and while their ultra-structural features are highly similar they exhibit variation in their mutational signatures and infection dynamics. As such, DFT1 and DFT2 provide a unique framework for investigating how a common progenitor cell can give rise to distinct contagious cancers. Using a proteomics approach, we show that DFT1 and DFT2 are derived from Schwann cells in different differentiation states, with DFT2 carrying a molecular signature of a less well differentiated Schwann cell. Under inflammatory signals DFT1 and DFT2 have different gene expression profiles, most notably involving Schwann cell markers of differentiation, reflecting the influence of their distinct origins. Further, DFT2 cells express immune cell markers typically expressed during nerve repair, consistent with an ability to manipulate their extracellular environment, facilitating the cell's ability to transmit between individuals. The emergence of two contagious cancers in the Tasmanian devil suggests that the inherent plasticity of Schwann cells confers a vulnerability to the formation of contagious cancers.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34780568</pmid><doi>10.1371/journal.ppat.1010033</doi><orcidid>https://orcid.org/0000-0002-2787-1282</orcidid><orcidid>https://orcid.org/0000-0003-0023-8679</orcidid><orcidid>https://orcid.org/0000-0002-2995-2959</orcidid><orcidid>https://orcid.org/0000-0003-0532-8331</orcidid><orcidid>https://orcid.org/0000-0002-8882-1502</orcidid><orcidid>https://orcid.org/0000-0001-6441-2213</orcidid><orcidid>https://orcid.org/0000-0003-2906-4385</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animal Diseases - genetics Animal Diseases - metabolism Animal Diseases - pathology Animals Biological Variation, Population Biology and Life Sciences Biomarkers Breast cancer Cancer Cancer cells Cell Differentiation Cells (biology) Communicable Diseases - genetics Communicable Diseases - metabolism Communicable Diseases - pathology Differentiation Drug resistance Facial Neoplasms - classification Facial Neoplasms - veterinary Fibroblasts Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genetic aspects Genotype & phenotype Growth Growth factors Immune system Inflammation Marsupialia Medicine and Health Sciences Metastasis Mollusks Nervous system Phenotypic variations Progenitor cells Protein expression Proteins Proteome - analysis Proteome - metabolism Proteomics Schwann cells Schwann Cells - metabolism Schwann Cells - pathology Shellfish Stem cells Transcriptome Tumors |
title | The differentiation state of the Schwann cell progenitor drives phenotypic variation between two contagious cancers |
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