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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Veröffentlicht in:PLoS pathogens 2021-11, Vol.17 (11), p.e1010033-e1010033
Hauptverfasser: Owen, Rachel S, Ramarathinam, Sri H, Bailey, Alistair, Gastaldello, Annalisa, Hussey, Kathryn, Skipp, Paul J, Purcell, Anthony W, Siddle, Hannah V
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container_issue 11
container_start_page e1010033
container_title PLoS pathogens
container_volume 17
creator Owen, Rachel S
Ramarathinam, Sri H
Bailey, Alistair
Gastaldello, Annalisa
Hussey, Kathryn
Skipp, Paul J
Purcell, Anthony W
Siddle, Hannah V
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. 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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. 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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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