Mass Spectrometry Imaging of Lipid and Metabolite Distributions in Cysts of Besnoitia besnoiti-Infected Bovine Skin

Katja R. Wiedemann; Stefanie Gerbig; Parviz Ghezellou; Alejandra Pilgram; Carlos Hermosilla; Anja Taubert; Liliana M.R. Silva; Bernhard Spengler

doi:10.1021/jasms.4c00466

Mass Spectrometry Imaging of Lipid and Metabolite Distributions in Cysts of Besnoitia besnoiti-Infected Bovine Skin

Katja R. Wiedemann, Stefanie Gerbig, Parviz Ghezellou, Alejandra Pilgram, Carlos Hermosilla, Anja Taubert, Liliana M.R. Silva, Bernhard Spengler

Research output: Contribution to journal › Article › peer-review

Abstract

Bovine besnoitiosis is a disease caused by the obligate intracellular parasite Besnoitia besnoiti. During its chronic stage, the parasite forms large, thick-walled cysts of up to 600 μm in diameter in the skin and other tissues. To assess an overview of parasite-induced metabolic changes during chronic infection, B. besnoiti-infected skin samples were analyzed by high-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI). Overall, infection-driven, significant changes of 467 lipids and metabolites were found in comparison to noninfected control samples. Most of them belong to the group of phosphatidic acids (PAs), phosphatidylserines (PSs), phosphatidylcholines (PCs)/phosphatidylethanolamines (PEs), triacylglycerides (TGs), phosphatidylinositols (PIs) and phosphatidylglycerols (PGs). When these quantitative data were combined with analyses on the lateral distribution of respective infection markers, MS images of significantly changed ion signals with specific lateral distributions were generated, matching with typical biological structures as observed in Hematoxylin and eosin (H&E)-stained tissue sections. Ultrahigh-resolution MALDI MSI with a pixel size of 2 μm and 3-dimensional reconstruction gave further insights into cyst construction.

Original language	English
Pages (from-to)	1017-1026
Number of pages	10
Journal	Journal of the American Society for Mass Spectrometry
Volume	36
Issue number	5
DOIs	https://doi.org/10.1021/jasms.4c00466
Publication status	Published - 7 May 2025

Keywords

AP-SMALDI
Apicomplexa
Besnoitia besnoiti
Besnoitiosis
Host−parasite interaction
Ultrahigh-resolution mass spectrometry imaging

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10.1021/jasms.4c00466

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title = "Mass Spectrometry Imaging of Lipid and Metabolite Distributions in Cysts of Besnoitia besnoiti-Infected Bovine Skin",

abstract = "Bovine besnoitiosis is a disease caused by the obligate intracellular parasite Besnoitia besnoiti. During its chronic stage, the parasite forms large, thick-walled cysts of up to 600 μm in diameter in the skin and other tissues. To assess an overview of parasite-induced metabolic changes during chronic infection, B. besnoiti-infected skin samples were analyzed by high-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI). Overall, infection-driven, significant changes of 467 lipids and metabolites were found in comparison to noninfected control samples. Most of them belong to the group of phosphatidic acids (PAs), phosphatidylserines (PSs), phosphatidylcholines (PCs)/phosphatidylethanolamines (PEs), triacylglycerides (TGs), phosphatidylinositols (PIs) and phosphatidylglycerols (PGs). When these quantitative data were combined with analyses on the lateral distribution of respective infection markers, MS images of significantly changed ion signals with specific lateral distributions were generated, matching with typical biological structures as observed in Hematoxylin and eosin (H\&E)-stained tissue sections. Ultrahigh-resolution MALDI MSI with a pixel size of 2 μm and 3-dimensional reconstruction gave further insights into cyst construction.",

keywords = "AP-SMALDI, Apicomplexa, Besnoitia besnoiti, Besnoitiosis, Host−parasite interaction, Ultrahigh-resolution mass spectrometry imaging",

author = "Wiedemann, \{Katja R.\} and Stefanie Gerbig and Parviz Ghezellou and Alejandra Pilgram and Carlos Hermosilla and Anja Taubert and Silva, \{Liliana M.R.\} and Bernhard Spengler",

note = "Publisher Copyright: {\textcopyright} 2025 The Authors. Published by American Chemical Society.",

year = "2025",

month = may,

day = "7",

doi = "10.1021/jasms.4c00466",

language = "English",

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T1 - Mass Spectrometry Imaging of Lipid and Metabolite Distributions in Cysts of Besnoitia besnoiti-Infected Bovine Skin

AU - Wiedemann, Katja R.

AU - Gerbig, Stefanie

AU - Ghezellou, Parviz

AU - Pilgram, Alejandra

AU - Hermosilla, Carlos

AU - Taubert, Anja

AU - Silva, Liliana M.R.

AU - Spengler, Bernhard

PY - 2025/5/7

Y1 - 2025/5/7

N2 - Bovine besnoitiosis is a disease caused by the obligate intracellular parasite Besnoitia besnoiti. During its chronic stage, the parasite forms large, thick-walled cysts of up to 600 μm in diameter in the skin and other tissues. To assess an overview of parasite-induced metabolic changes during chronic infection, B. besnoiti-infected skin samples were analyzed by high-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI). Overall, infection-driven, significant changes of 467 lipids and metabolites were found in comparison to noninfected control samples. Most of them belong to the group of phosphatidic acids (PAs), phosphatidylserines (PSs), phosphatidylcholines (PCs)/phosphatidylethanolamines (PEs), triacylglycerides (TGs), phosphatidylinositols (PIs) and phosphatidylglycerols (PGs). When these quantitative data were combined with analyses on the lateral distribution of respective infection markers, MS images of significantly changed ion signals with specific lateral distributions were generated, matching with typical biological structures as observed in Hematoxylin and eosin (H&E)-stained tissue sections. Ultrahigh-resolution MALDI MSI with a pixel size of 2 μm and 3-dimensional reconstruction gave further insights into cyst construction.

AB - Bovine besnoitiosis is a disease caused by the obligate intracellular parasite Besnoitia besnoiti. During its chronic stage, the parasite forms large, thick-walled cysts of up to 600 μm in diameter in the skin and other tissues. To assess an overview of parasite-induced metabolic changes during chronic infection, B. besnoiti-infected skin samples were analyzed by high-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI). Overall, infection-driven, significant changes of 467 lipids and metabolites were found in comparison to noninfected control samples. Most of them belong to the group of phosphatidic acids (PAs), phosphatidylserines (PSs), phosphatidylcholines (PCs)/phosphatidylethanolamines (PEs), triacylglycerides (TGs), phosphatidylinositols (PIs) and phosphatidylglycerols (PGs). When these quantitative data were combined with analyses on the lateral distribution of respective infection markers, MS images of significantly changed ion signals with specific lateral distributions were generated, matching with typical biological structures as observed in Hematoxylin and eosin (H&E)-stained tissue sections. Ultrahigh-resolution MALDI MSI with a pixel size of 2 μm and 3-dimensional reconstruction gave further insights into cyst construction.

KW - AP-SMALDI

KW - Apicomplexa

KW - Besnoitia besnoiti

KW - Besnoitiosis

KW - Host−parasite interaction

KW - Ultrahigh-resolution mass spectrometry imaging

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JO - Journal of the American Society for Mass Spectrometry

JF - Journal of the American Society for Mass Spectrometry

IS - 5

ER -

Mass Spectrometry Imaging of Lipid and Metabolite Distributions in Cysts of Besnoitia besnoiti-Infected Bovine Skin

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Keywords

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