The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation
Summary: Sensing stressful conditions and adjusting the cellular metabolism to adapt to the environment are essential activities for bacteria to survive in variable situations. Here, we describe a stress-related protein, YdiU, and characterize YdiU as an enzyme that catalyzes the covalent attachment...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2020-09-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124720311505 |
| _version_ | 1828750569131474944 |
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| author | Yinlong Yang Yingying Yue Nannan Song Cuiling Li Zenglin Yuan Yan Wang Yue Ma Hui Li Fengyu Zhang Weiwei Wang Haihong Jia Peng Li Xiaobing Li Qi Wang Zhe Ding Hongjie Dong Lichuan Gu Bingqing Li |
| author_facet | Yinlong Yang Yingying Yue Nannan Song Cuiling Li Zenglin Yuan Yan Wang Yue Ma Hui Li Fengyu Zhang Weiwei Wang Haihong Jia Peng Li Xiaobing Li Qi Wang Zhe Ding Hongjie Dong Lichuan Gu Bingqing Li |
| author_sort | Yinlong Yang |
| collection | DOAJ |
| description | Summary: Sensing stressful conditions and adjusting the cellular metabolism to adapt to the environment are essential activities for bacteria to survive in variable situations. Here, we describe a stress-related protein, YdiU, and characterize YdiU as an enzyme that catalyzes the covalent attachment of uridine-5′-monophosphate to a protein tyrosine/histidine residue, an unusual modification defined as UMPylation. Mn2+ serves as an essential co-factor for YdiU-mediated UMPylation. UTP and Mn2+ binding converts YdiU to an aggregate-prone state facilitating the recruitment of chaperones. The UMPylation of chaperones prevents them from binding co-factors or clients, thereby impairing their function. Consistent with the recent finding that YdiU acts as an AMPylator, we further demonstrate that the self-AMPylation of YdiU padlocks its chaperone-UMPylation activity. A detailed mechanism is proposed based on the crystal structures of Apo-YdiU and YdiU-AMPNPP-Mn2+ and on molecular dynamics simulation models of YdiU-UTP-Mn2+ and YdiU-UTP-peptide. In vivo data demonstrate that YdiU effectively protects Salmonella from stress-induced ATP depletion through UMPylation. |
| first_indexed | 2024-12-10T20:40:08Z |
| format | Article |
| id | doaj.art-8a319b3db9c04ee38abd5981f0db421e |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-10T20:40:08Z |
| publishDate | 2020-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-8a319b3db9c04ee38abd5981f0db421e2022-12-22T01:34:24ZengElsevierCell Reports2211-12472020-09-013212108161The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylationYinlong Yang0Yingying Yue1Nannan Song2Cuiling Li3Zenglin Yuan4Yan Wang5Yue Ma6Hui Li7Fengyu Zhang8Weiwei Wang9Haihong Jia10Peng Li11Xiaobing Li12Qi Wang13Zhe Ding14Hongjie Dong15Lichuan Gu16Bingqing Li17Key Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China; School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaState Key Laboratory of Microbial Technology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, Shandong 266003, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China; School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China; School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaState Key Laboratory of Microbial Technology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China; School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Sciences, Jinan, Shandong 250062, ChinaAdvanced Medical Research Institute, Translational Medicine Core Facility, Shandong University, Jinan, Shandong 250012, ChinaState Key Laboratory of Microbial Technology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaState Key Laboratory of Microbial Technology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaKey Laboratory of Rare and Uncommon Diseases, Department of Microbiology, Institute of Basic Medicine, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China; Corresponding authorSummary: Sensing stressful conditions and adjusting the cellular metabolism to adapt to the environment are essential activities for bacteria to survive in variable situations. Here, we describe a stress-related protein, YdiU, and characterize YdiU as an enzyme that catalyzes the covalent attachment of uridine-5′-monophosphate to a protein tyrosine/histidine residue, an unusual modification defined as UMPylation. Mn2+ serves as an essential co-factor for YdiU-mediated UMPylation. UTP and Mn2+ binding converts YdiU to an aggregate-prone state facilitating the recruitment of chaperones. The UMPylation of chaperones prevents them from binding co-factors or clients, thereby impairing their function. Consistent with the recent finding that YdiU acts as an AMPylator, we further demonstrate that the self-AMPylation of YdiU padlocks its chaperone-UMPylation activity. A detailed mechanism is proposed based on the crystal structures of Apo-YdiU and YdiU-AMPNPP-Mn2+ and on molecular dynamics simulation models of YdiU-UTP-Mn2+ and YdiU-UTP-peptide. In vivo data demonstrate that YdiU effectively protects Salmonella from stress-induced ATP depletion through UMPylation.http://www.sciencedirect.com/science/article/pii/S2211124720311505post-translational modificationUMPylationAMPylationthe YdiU domainchaperonesbacterial stress resistence |
| spellingShingle | Yinlong Yang Yingying Yue Nannan Song Cuiling Li Zenglin Yuan Yan Wang Yue Ma Hui Li Fengyu Zhang Weiwei Wang Haihong Jia Peng Li Xiaobing Li Qi Wang Zhe Ding Hongjie Dong Lichuan Gu Bingqing Li The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation Cell Reports post-translational modification UMPylation AMPylation the YdiU domain chaperones bacterial stress resistence |
| title | The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation |
| title_full | The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation |
| title_fullStr | The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation |
| title_full_unstemmed | The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation |
| title_short | The YdiU Domain Modulates Bacterial Stress Signaling through Mn2+-Dependent UMPylation |
| title_sort | ydiu domain modulates bacterial stress signaling through mn2 dependent umpylation |
| topic | post-translational modification UMPylation AMPylation the YdiU domain chaperones bacterial stress resistence |
| url | http://www.sciencedirect.com/science/article/pii/S2211124720311505 |
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