Perturbation of ubiquitin homeostasis promotes macrophage oxidative defenses

被引:19
作者
Charbonneau, Marie-Eve [1 ]
Passalacqua, Karla D. [1 ]
Hagen, Susan E. [2 ]
Showalter, Hollis D. [2 ]
Wobus, Christiane E. [1 ]
O'Riordan, Mary X. D. [1 ]
机构
[1] Univ Michigan, Sch Med, Dept Microbiol & Immunol, Ann Arbor, MI 48109 USA
[2] Univ Michigan, Coll Pharm, Dept Med Chem, Ann Arbor, MI 48109 USA
关键词
DEUBIQUITINATING ENZYME; PROTEIN HOMEOSTASIS; EMERGING FUNCTIONS; MECHANISMS; PROTEASOME; DEGRADATION; INHIBITION; DISEASE; ROLES; HOST;
D O I
10.1038/s41598-019-46526-9
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The innate immune system senses microbial ligands through pattern recognition and triggers downstream signaling cascades to promote inflammation and immune defense mechanisms. Emerging evidence suggests that cells also recognize alterations in host processes induced by infection as triggers. Protein ubiquitination and deubiquitination are post-translational modification processes essential for signaling and maintenance of cellular homeostasis, and infections can cause global alterations in the host ubiquitin proteome. Here we used a chemical biology approach to perturb the cellular ubiquitin proteome as a simplified model to study the impact of ubiquitin homeostasis alteration on macrophage function. Perturbation of ubiquitin homeostasis led to a rapid and transient burst of reactive oxygen species (ROS) that promoted macrophage inflammatory and anti-infective capacity. Moreover, we found that ROS production was dependent on the NOX2 phagocyte NADPH oxidase. Global alteration of the ubiquitin proteome also enhanced proinflammatory cytokine production in mice stimulated with a sub-lethal dose of LPS. Collectively, our findings suggest that major changes in the host ubiquitin landscape may be a potent signal to rapidly deploy innate immune defenses.
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页数:14
相关论文
共 65 条
[1]   Bacterial E3 ligase effectors exploit host ubiquitin systems [J].
Ashida, Hiroshi ;
Sasakawa, Chihiro .
CURRENT OPINION IN MICROBIOLOGY, 2017, 35 :16-22
[2]   Discovery of 7-Methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1H-indol-5-yl)-7H-pyrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a Potent and Selective First-in-Class Inhibitor of Protein Kinase R (PKR)-like Endoplasmic Reticulum Kinase (PERK) [J].
Axten, Jeffrey M. ;
Medina, Jesus R. ;
Feng, Yanhong ;
Shu, Arthur ;
Romeril, Stuart P. ;
Grant, Seth W. ;
Li, William Hoi Hong ;
Heerding, Dirk A. ;
Minthorn, Elisabeth ;
Mencken, Thomas ;
Atkins, Charity ;
Liu, Qi ;
Rabindran, Sridhar ;
Kumar, Rakesh ;
Hong, Xuan ;
Goetz, Aaron ;
Stanley, Thomas ;
Taylor, J. David ;
Sigethy, Scott D. ;
Tomberlin, Ginger H. ;
Hassell, Annie M. ;
Kahler, Kirsten M. ;
Shewchuk, Lisa M. ;
Gampe, Robert T. .
JOURNAL OF MEDICINAL CHEMISTRY, 2012, 55 (16) :7193-7207
[3]   POSTTRANSLATIONAL MODIFICATION AS A CRITICAL DETERMINANT OF CYTOPLASMIC INNATE IMMUNE RECOGNITION [J].
Baker, Paul J. ;
De Nardo, Dominic ;
Moghaddas, Fiona ;
Le Son Tran ;
Bachem, Annabell ;
Tan Nguyen ;
Hayman, Thomas ;
Tye, Hazel ;
Vince, James E. ;
Bedoui, Sammy ;
Ferrero, Richard L. ;
Masters, Seth L. .
PHYSIOLOGICAL REVIEWS, 2017, 97 (03) :1165-1209
[4]   Adapting proteostasis for disease intervention [J].
Balch, William E. ;
Morimoto, Richard I. ;
Dillin, Andrew ;
Kelly, Jeffery W. .
SCIENCE, 2008, 319 (5865) :916-919
[5]   Ubiquitin-Specific Protease 25 Functions in Endoplasmic Reticulum-Associated Degradation [J].
Blount, Jessica R. ;
Burr, Aaron A. ;
Denuc, Amanda ;
Marfany, Gemma ;
Todi, Sokol V. .
PLOS ONE, 2012, 7 (05)
[6]  
Bodnar Nicholas, 2017, F1000Res, V6, P1318, DOI 10.12688/f1000research.11683.1
[7]   Nox family NADPH oxidases: Molecular mechanisms of activation [J].
Brandes, Ralf P. ;
Weissmann, Norbert ;
Schroeder, Katrin .
FREE RADICAL BIOLOGY AND MEDICINE, 2014, 76 :208-226
[8]   IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA [J].
Calfon, M ;
Zeng, HQ ;
Urano, F ;
Till, JH ;
Hubbard, SR ;
Harding, HP ;
Clark, SG ;
Ron, D .
NATURE, 2002, 415 (6867) :92-96
[9]   Small Molecule Deubiquitinase Inhibitors Promote Macrophage Anti-Infective Capacity [J].
Charbonneau, Marie-Eve ;
Gonzalez-Hernandez, Marta J. ;
Showalter, Hollis D. ;
Donato, Nicholas J. ;
Wobus, Christiane E. ;
O'Riordan, Mary X. D. .
PLOS ONE, 2014, 9 (08)
[10]   TRIM14 Inhibits cGAS Degradation Mediated by Selective Autophagy Receptor p62 to Promote Innate Immune Responses [J].
Chen, Meixin ;
Meng, Qingcai ;
Qin, Yunfei ;
Liang, Puping ;
Tan, Peng ;
He, Lian ;
Zhou, Yubin ;
Chen, Yongjun ;
Huang, Junjiu ;
Wang, Rong-Fu ;
Cui, Jun .
MOLECULAR CELL, 2016, 64 (01) :105-119