Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain

Abstract We characterize the integrated response of a rat host to the liver fluke Fasciola hepatica using a combination of 1H nuclear magnetic resonance spectroscopic profiles (liver, kidney, intestine, brain, spleen, plasma, urine, feces) and multiplex cytokine markers of systemic inflammation. Mul...

Full description

Bibliographic Details
Main Authors: Jasmina Saric, Jia V Li, Jürg Utzinger, Yulan Wang, Jennifer Keiser, Stephan Dirnhofer, Olaf Beckonert, Mansour T A Sharabiani, Judith M Fonville, Jeremy K Nicholson, Elaine Holmes
Format: Article
Language:English
Published: Springer Nature 2010-07-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2010.49
_version_ 1826990468163960832
author Jasmina Saric
Jia V Li
Jürg Utzinger
Yulan Wang
Jennifer Keiser
Stephan Dirnhofer
Olaf Beckonert
Mansour T A Sharabiani
Judith M Fonville
Jeremy K Nicholson
Elaine Holmes
author_facet Jasmina Saric
Jia V Li
Jürg Utzinger
Yulan Wang
Jennifer Keiser
Stephan Dirnhofer
Olaf Beckonert
Mansour T A Sharabiani
Judith M Fonville
Jeremy K Nicholson
Elaine Holmes
author_sort Jasmina Saric
collection DOAJ
description Abstract We characterize the integrated response of a rat host to the liver fluke Fasciola hepatica using a combination of 1H nuclear magnetic resonance spectroscopic profiles (liver, kidney, intestine, brain, spleen, plasma, urine, feces) and multiplex cytokine markers of systemic inflammation. Multivariate mathematical models were built to describe the main features of the infection at the systems level. In addition to the expected modulation of hepatic choline and energy metabolism, we found significant perturbations of the nucleotide balance in the brain, together with increased plasma IL‐13, suggesting a shift toward modulation of immune reactions to minimize inflammatory damage, which may favor the co‐existence of the parasite in the host. Subsequent analysis of brain extracts from other trematode infection models (i.e. Schistosoma mansoni, and Echinostoma caproni) did not elicit a change in neural nucleotide levels, indicating that the neural effects of F. hepatica infection are specific. We propose that the topographically extended response to invasion of the host as characterized by the modulated global metabolic phenotype is stratified across several bio‐organizational levels and reflects the direct manipulation of host–nucleotide balance.
first_indexed 2024-03-07T16:38:44Z
format Article
id doaj.art-c5f2b867c9e94694b1d010bb41d92d71
institution Directory Open Access Journal
issn 1744-4292
language English
last_indexed 2025-02-18T08:21:03Z
publishDate 2010-07-01
publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj.art-c5f2b867c9e94694b1d010bb41d92d712024-11-03T12:53:46ZengSpringer NatureMolecular Systems Biology1744-42922010-07-016111010.1038/msb.2010.49Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brainJasmina Saric0Jia V Li1Jürg Utzinger2Yulan Wang3Jennifer Keiser4Stephan Dirnhofer5Olaf Beckonert6Mansour T A Sharabiani7Judith M Fonville8Jeremy K Nicholson9Elaine Holmes10Biomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonBiomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonDepartment of Epidemiology and Public Health, Swiss Tropical and Public Health InstituteState Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Center for Magnetic Resonance, Wuhan Institute of Physics and Mathematics, Chinese Academy of SciencesUniversity of BaselInstitute of Pathology, University Hospital BaselBiomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonDepartment of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College LondonBiomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonBiomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonBiomolecular Medicine, Department of Surgery and Cancer, Faculty of Medicine, Imperial College LondonAbstract We characterize the integrated response of a rat host to the liver fluke Fasciola hepatica using a combination of 1H nuclear magnetic resonance spectroscopic profiles (liver, kidney, intestine, brain, spleen, plasma, urine, feces) and multiplex cytokine markers of systemic inflammation. Multivariate mathematical models were built to describe the main features of the infection at the systems level. In addition to the expected modulation of hepatic choline and energy metabolism, we found significant perturbations of the nucleotide balance in the brain, together with increased plasma IL‐13, suggesting a shift toward modulation of immune reactions to minimize inflammatory damage, which may favor the co‐existence of the parasite in the host. Subsequent analysis of brain extracts from other trematode infection models (i.e. Schistosoma mansoni, and Echinostoma caproni) did not elicit a change in neural nucleotide levels, indicating that the neural effects of F. hepatica infection are specific. We propose that the topographically extended response to invasion of the host as characterized by the modulated global metabolic phenotype is stratified across several bio‐organizational levels and reflects the direct manipulation of host–nucleotide balance.https://doi.org/10.1038/msb.2010.49brainFasciola hepaticaimmunologymetabolic profilingnuclear magnetic resonance spectroscopy
spellingShingle Jasmina Saric
Jia V Li
Jürg Utzinger
Yulan Wang
Jennifer Keiser
Stephan Dirnhofer
Olaf Beckonert
Mansour T A Sharabiani
Judith M Fonville
Jeremy K Nicholson
Elaine Holmes
Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
Molecular Systems Biology
brain
Fasciola hepatica
immunology
metabolic profiling
nuclear magnetic resonance spectroscopy
title Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
title_full Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
title_fullStr Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
title_full_unstemmed Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
title_short Systems parasitology: effects of Fasciola hepatica on the neurochemical profile in the rat brain
title_sort systems parasitology effects of fasciola hepatica on the neurochemical profile in the rat brain
topic brain
Fasciola hepatica
immunology
metabolic profiling
nuclear magnetic resonance spectroscopy
url https://doi.org/10.1038/msb.2010.49
work_keys_str_mv AT jasminasaric systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT jiavli systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT jurgutzinger systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT yulanwang systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT jenniferkeiser systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT stephandirnhofer systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT olafbeckonert systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT mansourtasharabiani systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT judithmfonville systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT jeremyknicholson systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain
AT elaineholmes systemsparasitologyeffectsoffasciolahepaticaontheneurochemicalprofileintheratbrain