Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis
Staphylococcus aureus can survive within phagocytes. Indeed, we confirm in this study that approximately 10% of population persists in macrophages during S. aureus infection, while the rest are eliminated due to bacteriolysis, which is of particular interest to us. Herein, we observe that the bacter...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | Virulence |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/21505594.2022.2127209 |
| _version_ | 1811258677438447616 |
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| author | Shiyuan Feng Yongjun Yang Zhenzhen Liu Wei Chen Chongtao Du Guiqiu Hu Shuixing Yu Peixuan Song Jinfeng Miao |
| author_facet | Shiyuan Feng Yongjun Yang Zhenzhen Liu Wei Chen Chongtao Du Guiqiu Hu Shuixing Yu Peixuan Song Jinfeng Miao |
| author_sort | Shiyuan Feng |
| collection | DOAJ |
| description | Staphylococcus aureus can survive within phagocytes. Indeed, we confirm in this study that approximately 10% of population persists in macrophages during S. aureus infection, while the rest are eliminated due to bacteriolysis, which is of particular interest to us. Herein, we observe that the bacteriolysis is an early event accompanied by macrophage death during S. aureus infection. Furthermore, the cell death is significantly accelerated following increased intracellular bacteriolysis, indicating that intracellular bacteriolysis induces cell death. Subsequently, we establish that the cell death is not apoptosis or pyroptosis, but AIM2-mediated necroptosis, accompanied by AIM2 inflammasome activation. This finding challenges the classical model that the cell death that accompanies inflammasome activation is always pyroptosis. In addition, we observe that the apoptosis-associated genes are highly inhibited during S. aureus infection. Finally, we establish in vivo that increased bacteriolysis significantly enhances S. aureus pathogenicity by promoting its dissemination to kidney and leading to an inflammatory cytokine storm in AIM2-mediated manner. Collectively, our data demonstrate that bacteriolysis is detrimental when triggered in excess and its side effect is mediated by AIM2. Meanwhile, we propose a potential immune manipulation strategy by which S. aureus sacrifices the minority to trigger a limited necroptosis, thereby releasing signals from dead cells to inhibit apoptosis and other anti-inflammatory cascades of live cells, eventually surviving within host cells and establishing infection. |
| first_indexed | 2024-04-12T18:18:14Z |
| format | Article |
| id | doaj.art-c8359c36eda84b15a68724e880bbc8c6 |
| institution | Directory Open Access Journal |
| issn | 2150-5594 2150-5608 |
| language | English |
| last_indexed | 2024-04-12T18:18:14Z |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Virulence |
| spelling | doaj.art-c8359c36eda84b15a68724e880bbc8c62022-12-22T03:21:32ZengTaylor & Francis GroupVirulence2150-55942150-56082022-12-011311684169610.1080/21505594.2022.2127209Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosisShiyuan Feng0Yongjun Yang1Zhenzhen Liu2Wei Chen3Chongtao Du4Guiqiu Hu5Shuixing Yu6Peixuan Song7Jinfeng Miao8Ministry of Education Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaKey Laboratory of Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun, ChinaMinistry of Education Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaStaphylococcus aureus can survive within phagocytes. Indeed, we confirm in this study that approximately 10% of population persists in macrophages during S. aureus infection, while the rest are eliminated due to bacteriolysis, which is of particular interest to us. Herein, we observe that the bacteriolysis is an early event accompanied by macrophage death during S. aureus infection. Furthermore, the cell death is significantly accelerated following increased intracellular bacteriolysis, indicating that intracellular bacteriolysis induces cell death. Subsequently, we establish that the cell death is not apoptosis or pyroptosis, but AIM2-mediated necroptosis, accompanied by AIM2 inflammasome activation. This finding challenges the classical model that the cell death that accompanies inflammasome activation is always pyroptosis. In addition, we observe that the apoptosis-associated genes are highly inhibited during S. aureus infection. Finally, we establish in vivo that increased bacteriolysis significantly enhances S. aureus pathogenicity by promoting its dissemination to kidney and leading to an inflammatory cytokine storm in AIM2-mediated manner. Collectively, our data demonstrate that bacteriolysis is detrimental when triggered in excess and its side effect is mediated by AIM2. Meanwhile, we propose a potential immune manipulation strategy by which S. aureus sacrifices the minority to trigger a limited necroptosis, thereby releasing signals from dead cells to inhibit apoptosis and other anti-inflammatory cascades of live cells, eventually surviving within host cells and establishing infection.https://www.tandfonline.com/doi/10.1080/21505594.2022.2127209BacteriolysisAIM2inflammasomenecroptosisstaphylococcus aureuspathogenicity |
| spellingShingle | Shiyuan Feng Yongjun Yang Zhenzhen Liu Wei Chen Chongtao Du Guiqiu Hu Shuixing Yu Peixuan Song Jinfeng Miao Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis Virulence Bacteriolysis AIM2 inflammasome necroptosis staphylococcus aureus pathogenicity |
| title | Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis |
| title_full | Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis |
| title_fullStr | Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis |
| title_full_unstemmed | Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis |
| title_short | Intracellular bacteriolysis contributes to pathogenicity of Staphylococcus aureus by exacerbating AIM2-mediated inflammation and necroptosis |
| title_sort | intracellular bacteriolysis contributes to pathogenicity of staphylococcus aureus by exacerbating aim2 mediated inflammation and necroptosis |
| topic | Bacteriolysis AIM2 inflammasome necroptosis staphylococcus aureus pathogenicity |
| url | https://www.tandfonline.com/doi/10.1080/21505594.2022.2127209 |
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