Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis

Abstract Periodontal pathogen Porphyromonas gingivalis (P. gingivalis) is believed to possess immune evasion capabilities, but it remains unclear whether this immune evasion is related to host gene alternative splicing (AS). In this study, RNA-sequencing revealed significant changes in both AS lands...

Full description

Saved in:
Bibliographic Details
Main Authors: Yilin Zheng, Ziyi Wang, Yao Weng, Heriati Sitosari, Yuhan He, Xiu Zhang, Noriko Shiotsu, Yoko Fukuhara, Mika Ikegame, Hirohiko Okamura
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-94954-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849392251011072000
author Yilin Zheng
Ziyi Wang
Yao Weng
Heriati Sitosari
Yuhan He
Xiu Zhang
Noriko Shiotsu
Yoko Fukuhara
Mika Ikegame
Hirohiko Okamura
author_facet Yilin Zheng
Ziyi Wang
Yao Weng
Heriati Sitosari
Yuhan He
Xiu Zhang
Noriko Shiotsu
Yoko Fukuhara
Mika Ikegame
Hirohiko Okamura
author_sort Yilin Zheng
collection DOAJ
description Abstract Periodontal pathogen Porphyromonas gingivalis (P. gingivalis) is believed to possess immune evasion capabilities, but it remains unclear whether this immune evasion is related to host gene alternative splicing (AS). In this study, RNA-sequencing revealed significant changes in both AS landscape and transcriptomic profile of macrophages following P. gingivalis infection with/without knockout of gingipain (a unique toxic protease of P. gingivalis). P. gingivalis infection increased the PD-L1 transcripts expression and selectively upregulated a specific coding isoform that more effectively binds to PD-1 on T cells, thereby inhibiting immune function. Biological experiments also detected AS switch of PD-L1 in P. gingivalis-infected or gingipain-treated macrophages. AlphaFold 3 predictions indicated that the protein docking compatibility between PD-1 and P. gingivalis-upregulated PD-L1 isoform was over 80% higher than another coding isoform. These findings suggest that P. gingivalis employs gingipain to modulate the AS of PD-L1, facilitating immune evasion.
format Article
id doaj-art-8b4eec7b51da4c06a6e79788505166bd
institution Kabale University
issn 2045-2322
language English
publishDate 2025-03-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-8b4eec7b51da4c06a6e79788505166bd2025-08-20T03:40:48ZengNature PortfolioScientific Reports2045-23222025-03-0115111510.1038/s41598-025-94954-7Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalisYilin Zheng0Ziyi Wang1Yao Weng2Heriati Sitosari3Yuhan He4Xiu Zhang5Noriko Shiotsu6Yoko Fukuhara7Mika Ikegame8Hirohiko Okamura9Department of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Molecular Biology and Biochemistry, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityComprehensive Dental Clinic, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityDepartment of Oral Morphology, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University Hospital, Okayama UniversityAbstract Periodontal pathogen Porphyromonas gingivalis (P. gingivalis) is believed to possess immune evasion capabilities, but it remains unclear whether this immune evasion is related to host gene alternative splicing (AS). In this study, RNA-sequencing revealed significant changes in both AS landscape and transcriptomic profile of macrophages following P. gingivalis infection with/without knockout of gingipain (a unique toxic protease of P. gingivalis). P. gingivalis infection increased the PD-L1 transcripts expression and selectively upregulated a specific coding isoform that more effectively binds to PD-1 on T cells, thereby inhibiting immune function. Biological experiments also detected AS switch of PD-L1 in P. gingivalis-infected or gingipain-treated macrophages. AlphaFold 3 predictions indicated that the protein docking compatibility between PD-1 and P. gingivalis-upregulated PD-L1 isoform was over 80% higher than another coding isoform. These findings suggest that P. gingivalis employs gingipain to modulate the AS of PD-L1, facilitating immune evasion.https://doi.org/10.1038/s41598-025-94954-7Porphyromonas gingivalisGingipainMacrophageAlternative splicingPD-L1Immune evasion
spellingShingle Yilin Zheng
Ziyi Wang
Yao Weng
Heriati Sitosari
Yuhan He
Xiu Zhang
Noriko Shiotsu
Yoko Fukuhara
Mika Ikegame
Hirohiko Okamura
Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
Scientific Reports
Porphyromonas gingivalis
Gingipain
Macrophage
Alternative splicing
PD-L1
Immune evasion
title Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
title_full Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
title_fullStr Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
title_full_unstemmed Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
title_short Gingipain regulates isoform switches of PD-L1 in macrophages infected with Porphyromonas gingivalis
title_sort gingipain regulates isoform switches of pd l1 in macrophages infected with porphyromonas gingivalis
topic Porphyromonas gingivalis
Gingipain
Macrophage
Alternative splicing
PD-L1
Immune evasion
url https://doi.org/10.1038/s41598-025-94954-7
work_keys_str_mv AT yilinzheng gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT ziyiwang gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT yaoweng gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT heriatisitosari gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT yuhanhe gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT xiuzhang gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT norikoshiotsu gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT yokofukuhara gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT mikaikegame gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis
AT hirohikookamura gingipainregulatesisoformswitchesofpdl1inmacrophagesinfectedwithporphyromonasgingivalis