Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages

BackgroundPorphyromonas gingivalis (P. gingivalis), a major pathogen of periodontitis, can evade host immune defenses. Previously, we found that P. gingivalis W83 sialidase gene mutant strain (ΔPG0352) was more easily cleared by macrophages. The aims of this study were to investigate the effects of...

Full description

Bibliographic Details
Main Authors: Xiaomiao Fan, Shaowen Zheng, Chen Chen, Li Lin, Hongyan Wang, Yuqin Shen, Yaping Pan, Chen Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1173899/full
_version_ 1797815106923397120
author Xiaomiao Fan
Xiaomiao Fan
Shaowen Zheng
Chen Chen
Li Lin
Hongyan Wang
Yuqin Shen
Yaping Pan
Chen Li
author_facet Xiaomiao Fan
Xiaomiao Fan
Shaowen Zheng
Chen Chen
Li Lin
Hongyan Wang
Yuqin Shen
Yaping Pan
Chen Li
author_sort Xiaomiao Fan
collection DOAJ
description BackgroundPorphyromonas gingivalis (P. gingivalis), a major pathogen of periodontitis, can evade host immune defenses. Previously, we found that P. gingivalis W83 sialidase gene mutant strain (ΔPG0352) was more easily cleared by macrophages. The aims of this study were to investigate the effects of sialidase in P. gingivalis on the polarization, antigen presentation, and phagocytosis of infected macrophages and to clarify the mechanism of P. gingivalis immune evasion.MethodsHuman monocytes U937 were differentiated to macrophages and infected with P. gingivalis W83, ΔPG0352, comΔPG0352, and Escherichia coli (E. coli). The phagocytosis of macrophages was observed by transmission electron microscopy and flow cytometry. ELISA or Griess reaction were used to examine the levels of interleukin-12 (IL-12), inducible nitric oxide synthase (iNOS) and interleukin-10 (IL-10), and the expressions of CD68, CD80 and CD206 were determined by flow cytometry. The expression of major histocompatibility complex-II (MHC-II) was detected by immunofluorescence. A rat periodontitis model was established to determine the M1 and M2 polarization of macrophages.ResultsCompare with P. gingivalis W83, ΔPG0352 increased the levels of IL-12, iNOS, CD80, and MHC-II and inhibited the levels of IL-10 and CD206. Macrophages phagocytosed 75.4% of ΔPG0352 and 59.5% of P. gingivalis W83. In the rat periodontitis model, the levels of M1 and M2 macrophages in P. gingivalis W83 group were both higher than those in ΔPG0352 group, while the ratio of M1/M2 was higher in the ΔPG0352 group. Alveolar bone absorption was lower in ΔPG0352 group.ConclusionSialidase facilitates P. gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages.
first_indexed 2024-03-13T08:17:47Z
format Article
id doaj.art-7ab16e617a92410081775b6f568e135e
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-03-13T08:17:47Z
publishDate 2023-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-7ab16e617a92410081775b6f568e135e2023-05-31T13:59:00ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-05-011310.3389/fcimb.2023.11738991173899Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophagesXiaomiao Fan0Xiaomiao Fan1Shaowen Zheng2Chen Chen3Li Lin4Hongyan Wang5Yuqin Shen6Yaping Pan7Chen Li8Department of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontics, Affiliated Stomatology Hospital of Guangzhou Medical University, Guangdong Engineering Research Center of Oral Restoration and Reconstruction, Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine, Guangzhou, Guangdong, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontics, Affiliated Stomatology Hospital of Guangzhou Medical University, Guangdong Engineering Research Center of Oral Restoration and Reconstruction, Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine, Guangzhou, Guangdong, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaDepartment of Periodontology, School and Hospital of Stomatology, China Medical University, Liaoning Provincial Key Laboratory of Oral Disease, Shenyang, Liaoning, ChinaBackgroundPorphyromonas gingivalis (P. gingivalis), a major pathogen of periodontitis, can evade host immune defenses. Previously, we found that P. gingivalis W83 sialidase gene mutant strain (ΔPG0352) was more easily cleared by macrophages. The aims of this study were to investigate the effects of sialidase in P. gingivalis on the polarization, antigen presentation, and phagocytosis of infected macrophages and to clarify the mechanism of P. gingivalis immune evasion.MethodsHuman monocytes U937 were differentiated to macrophages and infected with P. gingivalis W83, ΔPG0352, comΔPG0352, and Escherichia coli (E. coli). The phagocytosis of macrophages was observed by transmission electron microscopy and flow cytometry. ELISA or Griess reaction were used to examine the levels of interleukin-12 (IL-12), inducible nitric oxide synthase (iNOS) and interleukin-10 (IL-10), and the expressions of CD68, CD80 and CD206 were determined by flow cytometry. The expression of major histocompatibility complex-II (MHC-II) was detected by immunofluorescence. A rat periodontitis model was established to determine the M1 and M2 polarization of macrophages.ResultsCompare with P. gingivalis W83, ΔPG0352 increased the levels of IL-12, iNOS, CD80, and MHC-II and inhibited the levels of IL-10 and CD206. Macrophages phagocytosed 75.4% of ΔPG0352 and 59.5% of P. gingivalis W83. In the rat periodontitis model, the levels of M1 and M2 macrophages in P. gingivalis W83 group were both higher than those in ΔPG0352 group, while the ratio of M1/M2 was higher in the ΔPG0352 group. Alveolar bone absorption was lower in ΔPG0352 group.ConclusionSialidase facilitates P. gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1173899/fullperiodontitisPorphyromonas gingivalissialidasemacrophagepolarization
spellingShingle Xiaomiao Fan
Xiaomiao Fan
Shaowen Zheng
Chen Chen
Li Lin
Hongyan Wang
Yuqin Shen
Yaping Pan
Chen Li
Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
Frontiers in Cellular and Infection Microbiology
periodontitis
Porphyromonas gingivalis
sialidase
macrophage
polarization
title Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
title_full Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
title_fullStr Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
title_full_unstemmed Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
title_short Sialidase facilitates Porphyromonas gingivalis immune evasion by reducing M1 polarization, antigen presentation, and phagocytosis of infected macrophages
title_sort sialidase facilitates porphyromonas gingivalis immune evasion by reducing m1 polarization antigen presentation and phagocytosis of infected macrophages
topic periodontitis
Porphyromonas gingivalis
sialidase
macrophage
polarization
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1173899/full
work_keys_str_mv AT xiaomiaofan sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT xiaomiaofan sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT shaowenzheng sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT chenchen sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT lilin sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT hongyanwang sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT yuqinshen sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT yapingpan sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages
AT chenli sialidasefacilitatesporphyromonasgingivalisimmuneevasionbyreducingm1polarizationantigenpresentationandphagocytosisofinfectedmacrophages