TRIF Licenses Caspase-11-Dependent NLRP3 Inflammasome Activation by Gram-Negative Bacteria

被引:584
作者
Rathinam, Vijay A. K. [1 ]
Vanaja, Sivapriya Kailasan [1 ,2 ]
Waggoner, Lisa [1 ]
Sokolovska, Anna [3 ]
Becker, Christine [3 ]
Stuart, Lynda M. [3 ]
Leong, John M. [2 ]
Fitzgerald, Katherine A. [1 ]
机构
[1] Univ Massachusetts, Sch Med, Dept Med, Div Infect Dis & Immunol, Worcester, MA 01605 USA
[2] Tufts Univ, Sch Med, Dept Mol Biol & Microbiol, Boston, MA 02111 USA
[3] Harvard Univ, Massachusetts Gen Hosp, Sch Med, Boston, MA 02114 USA
关键词
NF-KAPPA-B; CASPASE-1; ACTIVATION; GENE-EXPRESSION; CELL-DEATH; ASC; APOPTOSIS; RECEPTOR; TRAM; INTERLEUKIN-1-BETA; RECOGNITION;
D O I
10.1016/j.cell.2012.07.007
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Systemic infections with Gram-negative bacteria are characterized by high mortality rates due to the "sepsis syndrome," a widespread and uncontrolled inflammatory response. Though it is well recognized that the immune response during Gram-negative bacterial infection is initiated after the recognition of endotoxin by Toll-like receptor 4, the molecular mechanisms underlying the detrimental inflammatory response during Gram-negative bacteremia remain poorly defined. Here, we identify a TRIF pathway that licenses NLRP3 inflammasome activation by all Gram-negative bacteria. By engaging TRIF, Gram-negative bacteria activate caspase-11. TRIF activates caspase-11 via type I IFN signaling, an event that is both necessary and sufficient for caspase-11 induction and autoactivation. Caspase-11 subsequently synergizes with the assembled NLRP3 inflammasome to regulate caspase-1 activation and leads to caspase-1-independent cell death. These events occur specifically during infection with Gram-negative, but not Gram-positive, bacteria. The identification of TRIF as a regulator of caspase-11 underscores the importance of TLRs as master regulators of inflammasomes during Gram-negative bacterial infection.
引用
收藏
页码:606 / 619
页数:14
相关论文
共 46 条
[1]   Activation of the NLRP3 Inflammasome by Group B Streptococci [J].
Costa, Alessandro ;
Gupta, Rahul ;
Signorino, Giacomo ;
Malara, Antonio ;
Cardile, Francesco ;
Biondo, Carmelo ;
Midiri, Angelina ;
Galbo, Roberta ;
Trieu-Cuot, Patrick ;
Papasergi, Salvatore ;
Teti, Giuseppe ;
Henneke, Philipp ;
Mancuso, Giuseppe ;
Golenbock, Douglas T. ;
Beninati, Concetta .
JOURNAL OF IMMUNOLOGY, 2012, 188 (04) :1953-1960
[2]   Rip1 mediates the Trif-dependent Toll-like receptor 3- and 4-induced NF-κB activation but does not contribute to interferon regulatory factor 3 activation [J].
Cusson-Hermance, N ;
Khurana, S ;
Lee, TH ;
Fitzgerald, KA ;
Kelliher, MA .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2005, 280 (44) :36560-36566
[3]   Neisseria gonorrhoeae Activates the Proteinase Cathepsin B to Mediate the Signaling Activities of the NLRP3 and ASC-Containing Inflammasome [J].
Duncan, Joseph A. ;
Gao, Xi ;
Huang, Max Tze-Han ;
O'Connor, Brian P. ;
Thomas, Christopher E. ;
Willingham, Stephen B. ;
Bergstralh, Daniel T. ;
Jarvis, Gary A. ;
Sparling, P. Frederick ;
Ting, Jenny P. -Y. .
JOURNAL OF IMMUNOLOGY, 2009, 182 (10) :6460-6469
[4]   Critical Roles of ASC Inflammasomes in Caspase-1 Activation and Host Innate Resistance to Streptococcus pneumoniae Infection [J].
Fang, Rendong ;
Tsuchiya, Kohsuke ;
Kawamura, Ikuo ;
Shen, Yanna ;
Hara, Hideki ;
Sakai, Shunsuke ;
Yamamoto, Takeshi ;
Fernandes-Alnemri, Teresa ;
Yang, Ruili ;
Hernandez-Cuellar, Eduardo ;
Dewamitta, Sita R. ;
Xu, Yanting ;
Qu, Huixin ;
Alnemri, Emad S. ;
Mitsuyama, Masao .
JOURNAL OF IMMUNOLOGY, 2011, 187 (09) :4890-4899
[5]   The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation [J].
Fernandes-Alnemri, T. ;
Wu, J. ;
Yu, J-W ;
Datta, P. ;
Miller, B. ;
Jankowski, W. ;
Rosenberg, S. ;
Zhang, J. ;
Alnemri, E. S. .
CELL DEATH AND DIFFERENTIATION, 2007, 14 (09) :1590-1604
[6]   LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the toll adapters TRAM and TRIF [J].
Fitzgerald, KA ;
Rowe, DC ;
Barnes, BJ ;
Caffrey, DR ;
Visintin, A ;
Latz, E ;
Monks, B ;
Pitha, PM ;
Golenbock, DT .
JOURNAL OF EXPERIMENTAL MEDICINE, 2003, 198 (07) :1043-1055
[7]   Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria [J].
Franchi, Luigi ;
Kanneganti, Thirumala-Devi ;
Dubyak, George R. ;
Nunez, Gabriel .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (26) :18810-18818
[8]   Sensing and reacting to microbes through the inflammasomes [J].
Franchi, Luigi ;
Munoz-Planillo, Raul ;
Nunez, Gabriel .
NATURE IMMUNOLOGY, 2012, 13 (04) :325-332
[9]   Immunomodulatory functions of type I interferons [J].
Gonzalez-Navajas, Jose M. ;
Lee, Jongdae ;
David, Michael ;
Raz, Eyal .
NATURE REVIEWS IMMUNOLOGY, 2012, 12 (02) :125-135
[10]   Type I Interferon Inhibits Interleukin-1 Production and Inflammasome Activation [J].
Guarda, Greta ;
Braun, Marion ;
Staehli, Francesco ;
Tardivel, Aubry ;
Mattmann, Chantal ;
Foerster, Irmgard ;
Farlik, Matthias ;
Decker, Thomas ;
Du Pasquier, Renaud A. ;
Romero, Pedro ;
Tschopp, Juerg .
IMMUNITY, 2011, 34 (02) :213-223