Metagenomics and metaproteomics alterations are associated with kidney disease in opisthorchiasis hamsters fed a high-fat and high-fructose diet.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2024
Historique:
received: 02 10 2023
accepted: 24 03 2024
medline: 30 5 2024
pubmed: 30 5 2024
entrez: 30 5 2024
Statut: epublish

Résumé

Opisthorchis viverrini (O. viverrini, Ov) infection and consumption of high-fat and high-fructose (HFF) diet exacerbate liver and kidney disease. Here, we investigated the effects of a combination of O. viverrini infection and HFF diet on kidney pathology via changes in the gut microbiome and host proteome in hamsters. Twenty animals were divided into four groups; 1) fed a normal diet not infected with O. viverrini (normal group), 2) fed an HFF diet and not infected with O. viverrini (HFF), 3) fed a normal diet and infected with O. viverrini (Ov), and 4) fed an HFF diet and infected with O. viverrini (HFFOv). DNA was extracted from fecal samples and the V3-V4 region of the bacterial 16S rRNA gene sequenced on an Illumina MiSeq sequencing platform. In addition, LC/MS-MS analysis was done. Histopathological studies and biochemical assays were also conducted. The results indicated that the HFFOv group exhibited the most severe kidney injury, manifested as elevated KIM-1 expression and accumulation of fibrosis in kidney tissue. The microbiome of the HFFOv group was more diverse than in the HFF group: there were increased numbers of Ruminococcaceae, Lachnospiraceae, Desulfovibrionaceae and Akkermansiaceae, but fewer Eggerthellaceae. In total, 243 host proteins were identified across all groups. Analysis using STITCH predicted that host proteome changes may lead to leaking of the gut, allowing molecules such as soluble CD14 and p-cresol to pass through to promote kidney disease. In addition, differential expression of TGF-beta-activated kinase 1 and MAP3K7-binding protein 2 (Tab2, involving renal inflammation and injury) are predicted to be associated with kidney disease. The combination of HFF diet and O. viverrini infection may promote kidney injury through alterations in the gut microbiome and host proteome. This knowledge may suggest an effective strategy to prevent kidney disease beyond the early stages.

Sections du résumé

BACKGROUND BACKGROUND
Opisthorchis viverrini (O. viverrini, Ov) infection and consumption of high-fat and high-fructose (HFF) diet exacerbate liver and kidney disease. Here, we investigated the effects of a combination of O. viverrini infection and HFF diet on kidney pathology via changes in the gut microbiome and host proteome in hamsters.
METHODOLOGY/PRINCIPAL FINDINGS RESULTS
Twenty animals were divided into four groups; 1) fed a normal diet not infected with O. viverrini (normal group), 2) fed an HFF diet and not infected with O. viverrini (HFF), 3) fed a normal diet and infected with O. viverrini (Ov), and 4) fed an HFF diet and infected with O. viverrini (HFFOv). DNA was extracted from fecal samples and the V3-V4 region of the bacterial 16S rRNA gene sequenced on an Illumina MiSeq sequencing platform. In addition, LC/MS-MS analysis was done. Histopathological studies and biochemical assays were also conducted. The results indicated that the HFFOv group exhibited the most severe kidney injury, manifested as elevated KIM-1 expression and accumulation of fibrosis in kidney tissue. The microbiome of the HFFOv group was more diverse than in the HFF group: there were increased numbers of Ruminococcaceae, Lachnospiraceae, Desulfovibrionaceae and Akkermansiaceae, but fewer Eggerthellaceae. In total, 243 host proteins were identified across all groups. Analysis using STITCH predicted that host proteome changes may lead to leaking of the gut, allowing molecules such as soluble CD14 and p-cresol to pass through to promote kidney disease. In addition, differential expression of TGF-beta-activated kinase 1 and MAP3K7-binding protein 2 (Tab2, involving renal inflammation and injury) are predicted to be associated with kidney disease.
CONCLUSIONS/SIGNIFICANCE CONCLUSIONS
The combination of HFF diet and O. viverrini infection may promote kidney injury through alterations in the gut microbiome and host proteome. This knowledge may suggest an effective strategy to prevent kidney disease beyond the early stages.

Identifiants

pubmed: 38814931
doi: 10.1371/journal.pone.0301907
pii: PONE-D-23-32011
doi:

Substances chimiques

Fructose 30237-26-4
Proteome 0
RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0301907

Informations de copyright

Copyright: © 2024 Tunbenjasiri et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Keerapach Tunbenjasiri (K)

Biomedical Science Program, Graduate School, Khon Kaen University, Khon Kaen, Thailand.
Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.

Thatsanapong Pongking (T)

Biomedical Science Program, Graduate School, Khon Kaen University, Khon Kaen, Thailand.
Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.

Chutima Sitthirach (C)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Suppakrit Kongsintaweesuk (S)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand.

Sitiruk Roytrakul (S)

Functional Proteomics Technology Laboratory, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Pathum Thani, Thailand.

Sawanya Charoenlappanit (S)

Functional Proteomics Technology Laboratory, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Pathum Thani, Thailand.

Sirinapha Klungsaeng (S)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Sirirat Anutrakulchai (S)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Department of Medicine, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Chalongchai Chalermwat (C)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Department of Biochemistry, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Chawalit Pairojkul (C)

Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Somchai Pinlaor (S)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Porntip Pinlaor (P)

Chronic Kidney Disease Prevention in Northeastern Thailand, Khon Kaen University, Khon Kaen, Thailand.
Centre for Research and Development of Medical Diagnostic Laboratories, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand.
Department of Microbiology, Faculty of Associated Medical Sciences, Khon Kaen University, Khon Kaen, Thailand.

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Classifications MeSH