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Glycolipidomics of Liver Flukes and Host Tissues during Fascioliasis: Insights from Mass Spectrometry Imaging
Fascioliasis, a zoonotic disease caused by liver flukes of the genus Fasciola, poses significant health threats to both humans and livestock. While some infections remain asymptomatic, others can lead to fatal outcomes, particularly during the acute phase characterized by the migration of immature p...
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Published in: | ACS infectious diseases 2024-12, Vol.10 (12), p.4233-4245 |
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description | Fascioliasis, a zoonotic disease caused by liver flukes of the genus Fasciola, poses significant health threats to both humans and livestock. While some infections remain asymptomatic, others can lead to fatal outcomes, particularly during the acute phase characterized by the migration of immature parasites causing severe liver damage. Through the combination of data acquired via high-spatial-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI) and nanohydrophilic interaction chromatography tandem mass spectrometry, we investigated glycosphingolipids (GSLs) in both adult and immature parasite stages as well as the host liver and bile duct to unravel the intricacies of the host–pathogen interplay and associated pathology. Several GSLs showed characteristic distribution patterns within the parasite depending on the fatty acid composition of their ceramides, notably including GSLs carrying very long-chain fatty acids. Additionally, GSL compositions within the tegument of immature versus adult parasites varied, suggestive of tissue remodeling upon maturation. AP-SMALDI MSI further enabled the identification of GSLs potentially involved in in vivo interactions between the host and immature parasites. Moreover, our experiments unveiled alterations in other lipid classes during Fasciola infection, providing a broader understanding of lipidomic changes associated with the disease. Collectively, our findings contribute to a deeper comprehension of the molecular intricacies underlying fascioliasis, with a specific focus on GSLs. |
doi_str_mv | 10.1021/acsinfecdis.4c00551 |
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While some infections remain asymptomatic, others can lead to fatal outcomes, particularly during the acute phase characterized by the migration of immature parasites causing severe liver damage. Through the combination of data acquired via high-spatial-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI) and nanohydrophilic interaction chromatography tandem mass spectrometry, we investigated glycosphingolipids (GSLs) in both adult and immature parasite stages as well as the host liver and bile duct to unravel the intricacies of the host–pathogen interplay and associated pathology. Several GSLs showed characteristic distribution patterns within the parasite depending on the fatty acid composition of their ceramides, notably including GSLs carrying very long-chain fatty acids. Additionally, GSL compositions within the tegument of immature versus adult parasites varied, suggestive of tissue remodeling upon maturation. AP-SMALDI MSI further enabled the identification of GSLs potentially involved in in vivo interactions between the host and immature parasites. Moreover, our experiments unveiled alterations in other lipid classes during Fasciola infection, providing a broader understanding of lipidomic changes associated with the disease. Collectively, our findings contribute to a deeper comprehension of the molecular intricacies underlying fascioliasis, with a specific focus on GSLs.</description><identifier>ISSN: 2373-8227</identifier><identifier>EISSN: 2373-8227</identifier><identifier>DOI: 10.1021/acsinfecdis.4c00551</identifier><identifier>PMID: 39510517</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Animals ; Bile Ducts - parasitology ; Fasciola hepatica - chemistry ; Fascioliasis - parasitology ; Glycosphingolipids - analysis ; Glycosphingolipids - chemistry ; Host-Parasite Interactions ; Liver - parasitology ; Mice ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods ; Tandem Mass Spectrometry</subject><ispartof>ACS infectious diseases, 2024-12, Vol.10 (12), p.4233-4245</ispartof><rights>2024 The Authors. Published by American Chemical Society</rights><rights>2024 The Authors. 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Dis</addtitle><description>Fascioliasis, a zoonotic disease caused by liver flukes of the genus Fasciola, poses significant health threats to both humans and livestock. While some infections remain asymptomatic, others can lead to fatal outcomes, particularly during the acute phase characterized by the migration of immature parasites causing severe liver damage. Through the combination of data acquired via high-spatial-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI) and nanohydrophilic interaction chromatography tandem mass spectrometry, we investigated glycosphingolipids (GSLs) in both adult and immature parasite stages as well as the host liver and bile duct to unravel the intricacies of the host–pathogen interplay and associated pathology. Several GSLs showed characteristic distribution patterns within the parasite depending on the fatty acid composition of their ceramides, notably including GSLs carrying very long-chain fatty acids. Additionally, GSL compositions within the tegument of immature versus adult parasites varied, suggestive of tissue remodeling upon maturation. AP-SMALDI MSI further enabled the identification of GSLs potentially involved in in vivo interactions between the host and immature parasites. Moreover, our experiments unveiled alterations in other lipid classes during Fasciola infection, providing a broader understanding of lipidomic changes associated with the disease. Collectively, our findings contribute to a deeper comprehension of the molecular intricacies underlying fascioliasis, with a specific focus on GSLs.</description><subject>Animals</subject><subject>Bile Ducts - parasitology</subject><subject>Fasciola hepatica - chemistry</subject><subject>Fascioliasis - parasitology</subject><subject>Glycosphingolipids - analysis</subject><subject>Glycosphingolipids - chemistry</subject><subject>Host-Parasite Interactions</subject><subject>Liver - parasitology</subject><subject>Mice</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods</subject><subject>Tandem Mass Spectrometry</subject><issn>2373-8227</issn><issn>2373-8227</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9UUtLAzEQDqLYUv0FguTopZr3rl5EitVCxYN6DjGb1NTdTc3sCv33RlqlXjwlmfkeM_kQOqHknBJGL4yF0HpnqwDnwhIiJd1DQ8YLPi4ZK_Z37gN0DLAkhFBeSiHkIRrwS0mJpMUQNXf12sY6rEIVm2ABR4_n4dMlPK37dwfYtBW-j9Dh5wDQ50LVp9Au8NSADZloIMAVnrUQFm8dYJ9igx8MAH5aOdvll-vSGs8as8isI3TgTQ3ueHuO0Mv09nlyP54_3s0mN_Ox4Ux1Y8WkF1SVhJHSWSlM5ZSQVDCqpPKWK1-xQnFqy1z01FhLWSm5eZXGclEwPkLXG91V_9q4yrq2S6bWqxQak9Y6mqD_dtrwphfxU9PsQApVZoWzrUKKH3ntTjcBrKtr07rYg-bZkTMi8hgjxDdQmyJAcv7XhxL9HZbeCUtvw8qs090Rfzk_0WTAxQaQ2XoZ-9TmH_tX8gsGAKTO</recordid><startdate>20241213</startdate><enddate>20241213</enddate><creator>Luh, David</creator><creator>Ghezellou, Parviz</creator><creator>Heiles, Sven</creator><creator>Gramberg, Svenja</creator><creator>Haeberlein, Simone</creator><creator>Spengler, Bernhard</creator><general>American Chemical Society</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>5PM</scope><orcidid>https://orcid.org/0000-0003-3779-8071</orcidid><orcidid>https://orcid.org/0000-0003-0179-5653</orcidid></search><sort><creationdate>20241213</creationdate><title>Glycolipidomics of Liver Flukes and Host Tissues during Fascioliasis: Insights from Mass Spectrometry Imaging</title><author>Luh, David ; Ghezellou, Parviz ; Heiles, Sven ; Gramberg, Svenja ; Haeberlein, Simone ; Spengler, Bernhard</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a326t-625f41680208ec54ade6451421656fc36fd27631c8514f1acc12853ab5ac34723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Bile Ducts - parasitology</topic><topic>Fasciola hepatica - chemistry</topic><topic>Fascioliasis - parasitology</topic><topic>Glycosphingolipids - analysis</topic><topic>Glycosphingolipids - chemistry</topic><topic>Host-Parasite Interactions</topic><topic>Liver - parasitology</topic><topic>Mice</topic><topic>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods</topic><topic>Tandem Mass Spectrometry</topic><toplevel>online_resources</toplevel><creatorcontrib>Luh, David</creatorcontrib><creatorcontrib>Ghezellou, Parviz</creatorcontrib><creatorcontrib>Heiles, Sven</creatorcontrib><creatorcontrib>Gramberg, Svenja</creatorcontrib><creatorcontrib>Haeberlein, Simone</creatorcontrib><creatorcontrib>Spengler, Bernhard</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>PubMed Central (Full Participant titles)</collection><jtitle>ACS infectious diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Luh, David</au><au>Ghezellou, Parviz</au><au>Heiles, Sven</au><au>Gramberg, Svenja</au><au>Haeberlein, Simone</au><au>Spengler, Bernhard</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glycolipidomics of Liver Flukes and Host Tissues during Fascioliasis: Insights from Mass Spectrometry Imaging</atitle><jtitle>ACS infectious diseases</jtitle><addtitle>ACS Infect. 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subjects | Animals Bile Ducts - parasitology Fasciola hepatica - chemistry Fascioliasis - parasitology Glycosphingolipids - analysis Glycosphingolipids - chemistry Host-Parasite Interactions Liver - parasitology Mice Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods Tandem Mass Spectrometry |
title | Glycolipidomics of Liver Flukes and Host Tissues during Fascioliasis: Insights from Mass Spectrometry Imaging |
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