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Schistosoma mansoni mucin gene (SmPoMuc) expression: epigenetic control to shape adaptation to a new host.

Perrin C, Lepesant JM, Roger E, Duval D, Fneich S, Thuillier V, Alliene JF, Mitta G, Grunau C, Cosseau C - PLoS Pathog. (2013)

Bottom Line: We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni strains that are either compatible (C) or incompatible (IC) with a reference snail host.In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains.Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded.

View Article: PubMed Central - PubMed

Affiliation: Université de Perpignan Via Domitia, Perpignan, France.

ABSTRACT
The digenetic trematode Schistosoma mansoni is a human parasite that uses the mollusc Biomphalaria glabrata as intermediate host. Specific S. mansoni strains can infect efficiently only certain B. glabrata strains (compatible strain) while others are incompatible. Strain-specific differences in transcription of a conserved family of polymorphic mucins (SmPoMucs) in S. mansoni are the principle determinants for this compatibility. In the present study, we investigated the bases of the control of SmPoMuc expression that evolved to evade B. glabrata diversified antigen recognition molecules. We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni strains that are either compatible (C) or incompatible (IC) with a reference snail host. We reveal that although sequence differences are observed between active promoter regions of SmPoMuc genes, the sequences of the promoters are not diverse and are conserved between IC and C strains, suggesting that genetics alone cannot explain the evolution of compatibility polymorphism. In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains. Moreover, we show that modifications of the structure of the chromatin of the parasite modify transcription of SmPoMuc in the IC strain compared to the C strain and correlate with the presence of additional combinations of SmPoMuc transcripts only observed in the IC phenotype. Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded. These strain-specific epigenetic marks are heritable, but can change while the underlying genetic information remains stable. This suggests that epigenetic changes may be important for the early steps in the adaptation of pathogens to new hosts, and might be an initial step in adaptive evolution in general.

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Related in: MedlinePlus

Expression of EGFP under control of the SmPoMuc group 3.1(r1–r2) promoter in HeLa cells.HeLa cells were transiently transfected with (A.) promoterless pEGFP1 vector backbone, (B.) pCMV-EGFP or (C) pSmPoMuc-EGFP. Cell nuclei were labelled with DAPI. Visualization of the fluorescence separately (right panel) or overlaid (left panel) is presented. Magnification is ×400.
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ppat-1003571-g002: Expression of EGFP under control of the SmPoMuc group 3.1(r1–r2) promoter in HeLa cells.HeLa cells were transiently transfected with (A.) promoterless pEGFP1 vector backbone, (B.) pCMV-EGFP or (C) pSmPoMuc-EGFP. Cell nuclei were labelled with DAPI. Visualization of the fluorescence separately (right panel) or overlaid (left panel) is presented. Magnification is ×400.

Mentions: To investigate the mechanisms underlying differences of transcription between SmPoMuc groups and subgroups, we characterized the minimal promoter region of the SmPoMuc genes. We sequenced a region spanning 1.04 to 2.00 kb upstream of the transcriptional start site (TSS) for 4 groups of SmPoMuc (Groups 1, 2, 3.1 and 3.1(r1–r2). We produced a PCR product of a 996 bp of the region of the promoter of the group 3.1(r1–r2) and a PCR product of 1002 bp of the group 3.1 just upstream of the transcriptional start site. Plasmids containing these sequences upstream of a reporter gene (EGFP) were transfected into HeLa cells and fluorescence was observed under a microscope (fig. 2). These experiments showed that these sequences are sufficient to drive the heterologous expression of the reporter gene and contain the minimal promoter sufficient for transcription.


Schistosoma mansoni mucin gene (SmPoMuc) expression: epigenetic control to shape adaptation to a new host.

Perrin C, Lepesant JM, Roger E, Duval D, Fneich S, Thuillier V, Alliene JF, Mitta G, Grunau C, Cosseau C - PLoS Pathog. (2013)

Expression of EGFP under control of the SmPoMuc group 3.1(r1–r2) promoter in HeLa cells.HeLa cells were transiently transfected with (A.) promoterless pEGFP1 vector backbone, (B.) pCMV-EGFP or (C) pSmPoMuc-EGFP. Cell nuclei were labelled with DAPI. Visualization of the fluorescence separately (right panel) or overlaid (left panel) is presented. Magnification is ×400.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3757033&req=5

ppat-1003571-g002: Expression of EGFP under control of the SmPoMuc group 3.1(r1–r2) promoter in HeLa cells.HeLa cells were transiently transfected with (A.) promoterless pEGFP1 vector backbone, (B.) pCMV-EGFP or (C) pSmPoMuc-EGFP. Cell nuclei were labelled with DAPI. Visualization of the fluorescence separately (right panel) or overlaid (left panel) is presented. Magnification is ×400.
Mentions: To investigate the mechanisms underlying differences of transcription between SmPoMuc groups and subgroups, we characterized the minimal promoter region of the SmPoMuc genes. We sequenced a region spanning 1.04 to 2.00 kb upstream of the transcriptional start site (TSS) for 4 groups of SmPoMuc (Groups 1, 2, 3.1 and 3.1(r1–r2). We produced a PCR product of a 996 bp of the region of the promoter of the group 3.1(r1–r2) and a PCR product of 1002 bp of the group 3.1 just upstream of the transcriptional start site. Plasmids containing these sequences upstream of a reporter gene (EGFP) were transfected into HeLa cells and fluorescence was observed under a microscope (fig. 2). These experiments showed that these sequences are sufficient to drive the heterologous expression of the reporter gene and contain the minimal promoter sufficient for transcription.

Bottom Line: We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni strains that are either compatible (C) or incompatible (IC) with a reference snail host.In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains.Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded.

View Article: PubMed Central - PubMed

Affiliation: Université de Perpignan Via Domitia, Perpignan, France.

ABSTRACT
The digenetic trematode Schistosoma mansoni is a human parasite that uses the mollusc Biomphalaria glabrata as intermediate host. Specific S. mansoni strains can infect efficiently only certain B. glabrata strains (compatible strain) while others are incompatible. Strain-specific differences in transcription of a conserved family of polymorphic mucins (SmPoMucs) in S. mansoni are the principle determinants for this compatibility. In the present study, we investigated the bases of the control of SmPoMuc expression that evolved to evade B. glabrata diversified antigen recognition molecules. We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni strains that are either compatible (C) or incompatible (IC) with a reference snail host. We reveal that although sequence differences are observed between active promoter regions of SmPoMuc genes, the sequences of the promoters are not diverse and are conserved between IC and C strains, suggesting that genetics alone cannot explain the evolution of compatibility polymorphism. In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains. Moreover, we show that modifications of the structure of the chromatin of the parasite modify transcription of SmPoMuc in the IC strain compared to the C strain and correlate with the presence of additional combinations of SmPoMuc transcripts only observed in the IC phenotype. Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded. These strain-specific epigenetic marks are heritable, but can change while the underlying genetic information remains stable. This suggests that epigenetic changes may be important for the early steps in the adaptation of pathogens to new hosts, and might be an initial step in adaptive evolution in general.

Show MeSH
Related in: MedlinePlus