Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189

Abstract Mycobacterium tuberculosis (Mtb) infection significantly alters host cellular signaling and protein functions, facilitating immune evasion and intracellular survival. However, the molecular mechanisms underlying these interactions remain incompletely characterized. Here, we employed a multi...

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Main Authors: Tianxian Liu, Jun‐Yu Xu, Lei Zhao, Yameng Fan, Shuyu Xie, Ke Ma, Ying Zhou, Minjia Tan, Bang‐Ce Ye
Format: Article
Language:English
Published: Wiley 2025-03-01
Series:iMetaOmics
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Online Access:https://doi.org/10.1002/imo2.53
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author Tianxian Liu
Jun‐Yu Xu
Lei Zhao
Yameng Fan
Shuyu Xie
Ke Ma
Ying Zhou
Minjia Tan
Bang‐Ce Ye
author_facet Tianxian Liu
Jun‐Yu Xu
Lei Zhao
Yameng Fan
Shuyu Xie
Ke Ma
Ying Zhou
Minjia Tan
Bang‐Ce Ye
author_sort Tianxian Liu
collection DOAJ
description Abstract Mycobacterium tuberculosis (Mtb) infection significantly alters host cellular signaling and protein functions, facilitating immune evasion and intracellular survival. However, the molecular mechanisms underlying these interactions remain incompletely characterized. Here, we employed a multi‐omics strategy, including proteomics, phosphoproteomics, transcriptomics and interactomics, to investigate the impact of Mtb infection on host cellular processes. Our study revealed that mycobacteria modulate RNA alternative splicing in host cells by reducing the phosphorylation levels within the spliceosome complex. We identified the serine/threonine protein phosphatase (PstP) as a key effector, dephosphorylating the spliceosome RNA‐binding motif protein (RBMX) at the serine 189 site (S189). This modification influences the alternative splicing of PLA2G7, which encodes platelet‐activating factor acetylhydrolase, resulting an increase in the mRNA levels of a transcript containing exon9 (PLA2G7‐exon9+). Importantly, PLA2G7 isoform encoded by PLA2G7‐exon9+, in contrast to the isoform lacking exon9, acquires the ability to potentiate inflammatory responses. Collectively, our findings not only provide a comprehensive view of Mtb‐induced host regulatory networks but also elucidate a role for PstP in controlling a critical mediator of alterative splicing during infection.
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spelling doaj-art-c71e20f1606043f2b56572f40efafddf2025-08-20T02:15:16ZengWileyiMetaOmics2996-95062996-95142025-03-0121n/an/a10.1002/imo2.53Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189Tianxian Liu0Jun‐Yu Xu1Lei Zhao2Yameng Fan3Shuyu Xie4Ke Ma5Ying Zhou6Minjia Tan7Bang‐Ce Ye8Laboratory of Biosystems and Microanalysis, State Key Laboratory of Bioreactor Engineering East China University of Science and Technology Shanghai ChinaState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica Chinese Academy of Sciences Shanghai ChinaLaboratory of Biosystems and Microanalysis, State Key Laboratory of Bioreactor Engineering East China University of Science and Technology Shanghai ChinaState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica Chinese Academy of Sciences Shanghai ChinaState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica Chinese Academy of Sciences Shanghai ChinaState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica Chinese Academy of Sciences Shanghai ChinaLaboratory of Biosystems and Microanalysis, State Key Laboratory of Bioreactor Engineering East China University of Science and Technology Shanghai ChinaState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica Chinese Academy of Sciences Shanghai ChinaLaboratory of Biosystems and Microanalysis, State Key Laboratory of Bioreactor Engineering East China University of Science and Technology Shanghai ChinaAbstract Mycobacterium tuberculosis (Mtb) infection significantly alters host cellular signaling and protein functions, facilitating immune evasion and intracellular survival. However, the molecular mechanisms underlying these interactions remain incompletely characterized. Here, we employed a multi‐omics strategy, including proteomics, phosphoproteomics, transcriptomics and interactomics, to investigate the impact of Mtb infection on host cellular processes. Our study revealed that mycobacteria modulate RNA alternative splicing in host cells by reducing the phosphorylation levels within the spliceosome complex. We identified the serine/threonine protein phosphatase (PstP) as a key effector, dephosphorylating the spliceosome RNA‐binding motif protein (RBMX) at the serine 189 site (S189). This modification influences the alternative splicing of PLA2G7, which encodes platelet‐activating factor acetylhydrolase, resulting an increase in the mRNA levels of a transcript containing exon9 (PLA2G7‐exon9+). Importantly, PLA2G7 isoform encoded by PLA2G7‐exon9+, in contrast to the isoform lacking exon9, acquires the ability to potentiate inflammatory responses. Collectively, our findings not only provide a comprehensive view of Mtb‐induced host regulatory networks but also elucidate a role for PstP in controlling a critical mediator of alterative splicing during infection.https://doi.org/10.1002/imo2.53inflammatory responseintegrative multi‐omic analysismycobacteriaPLA2G7RBMX S189RNA alternative splicing
spellingShingle Tianxian Liu
Jun‐Yu Xu
Lei Zhao
Yameng Fan
Shuyu Xie
Ke Ma
Ying Zhou
Minjia Tan
Bang‐Ce Ye
Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
iMetaOmics
inflammatory response
integrative multi‐omic analysis
mycobacteria
PLA2G7
RBMX S189
RNA alternative splicing
title Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
title_full Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
title_fullStr Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
title_full_unstemmed Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
title_short Mycobacterial PstP impairs host RNA alternative splicing by dephosphorylation of spliceosome RBMX at S189
title_sort mycobacterial pstp impairs host rna alternative splicing by dephosphorylation of spliceosome rbmx at s189
topic inflammatory response
integrative multi‐omic analysis
mycobacteria
PLA2G7
RBMX S189
RNA alternative splicing
url https://doi.org/10.1002/imo2.53
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