|
|
|
|||||||
|
|||||||||
J. Biol. Chem., Vol. 282, Issue 26, 18810-18818, June 29, 2007
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Differential Requirement of P2X7 Receptor and Intracellular K+ for Caspase-1 Activation Induced by Intracellular and Extracellular Bacteria*
1
2
From the
Department of Pathology and Comprehensive Cancer Center, The University of Michigan Medical School, Ann Arbor, Michigan 48109 and the Department of Physiology and Biophysics, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106
Interleukin-1
(IL-1) is a pro-inflammatory cytokine that plays an important role in host defense and inflammatory diseases. The maturation and secretion of IL-1 are mediated by caspase-1, a protease that processes pro-IL-1 into biologically active IL-1. The activity of caspase-1 is controlled by the inflammasome, a multiprotein complex formed by NLR proteins and the adaptor ASC, that induces the activation of caspase-1. The current model proposes that changes in the intracellular concentration of K+ potentiate caspase-1 activation induced by the recognition of bacterial products. However, the roles of P2X7 receptor and intracellular K+ in IL-1 secretion induced by bacterial infection remain unknown. Here we show that, in response to Toll-like receptor agonists such as lipopolysaccharide or infection with extracellular bacteria Staphylococcus aureus and Escherichia coli, efficient caspase-1 activation is only triggered by addition of ATP, a signal that promotes caspase-1 activation through depletion of intracellular K+ caused by stimulation of the purinergic P2X7 receptor. In contrast, activation of caspase-1 that relies on cytosolic sensing of flagellin or intracellular bacteria did not require ATP stimulation or depletion of cytoplasmic K+. Consistently, caspase-1 activation induced by intracellular Salmonella or Listeria was unimpaired in macrophages deficient in P2X7 receptor. These results indicate that, unlike caspase-1 induced by Toll-like receptor agonists and ATP, activation of the inflammasome by intracellular bacteria and cytosolic flagellin proceeds normally in the absence of P2X7 receptor-mediated cytoplasmic K+ perturbations.
Received for publication, November 20, 2006 , and in revised form, April 5, 2007.
* This work was supported in part by National Institutes of Health Grants AI063331, AR051790, and AI064748 (to G. N.) and GM36387 (to G. R. D.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1 Recipient of a postdoctoral fellowship from the Arthritis Foundation.
2 To whom correspondence should be addressed: University of Michigan Medical School, 1500 E. Medical Center Dr., Ann Arbor, MI 48109. Tel.: 734-764-8514; Fax: 734-647-9654; E-mail: bclx{at}umich.ed.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati What's this?
This article has been cited by other articles:
|
|
 |
|
  L. Franchi, T. Eigenbrod, and G. Nunez Cutting Edge: TNF-{alpha} Mediates Sensitization to ATP and Silica via the NLRP3 Inflammasome in the Absence of Microbial Stimulation J. Immunol., July 15, 2009; 183(2): 792 - 796. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. R. Silverman, J. P. de Rivero Vaccari, S. Locovei, F. Qiu, S. K. Carlsson, E. Scemes, R. W. Keane, and G. Dahl The Pannexin 1 Channel Activates the Inflammasome in Neurons and Astrocytes J. Biol. Chem., July 3, 2009; 284(27): 18143 - 18151. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. E. Winter, P. Thiennimitr, S.-P. Nuccio, T. Haneda, M. G. Winter, R. P. Wilson, J. M. Russell, T. Henry, Q. T. Tran, S. D. Lawhon, et al. Contribution of Flagellin Pattern Recognition to Intestinal Inflammation during Salmonella enterica Serotype Typhimurium Infection Infect. Immun., May 1, 2009; 77(5): 1904 - 1916. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. L. Case, S. Shin, and C. R. Roy Asc and Ipaf Inflammasomes Direct Distinct Pathways for Caspase-1 Activation in Response to Legionella pneumophila Infect. Immun., May 1, 2009; 77(5): 1981 - 1991. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-H. Park, Y.-G. Kim, and G. Nunez RICK Promotes Inflammation and Lethality after Gram-Negative Bacterial Infection in Mice Stimulated with Lipopolysaccharide Infect. Immun., April 1, 2009; 77(4): 1569 - 1578. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Kawai and S. Akira The roles of TLRs, RLRs and NLRs in pathogen recognition Int. Immunol., April 1, 2009; 21(4): 317 - 337. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. A. Sharp, D. Ruane, B. Claass, E. Creagh, J. Harris, P. Malyala, M. Singh, D. T. O'Hagan, V. Petrilli, J. Tschopp, et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome PNAS, January 20, 2009; 106(3): 870 - 875. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Yilmaz The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay Microbiology, October 1, 2008; 154(10): 2897 - 2903. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kool, V. Petrilli, T. De Smedt, A. Rolaz, H. Hammad, M. van Nimwegen, I. M. Bergen, R. Castillo, B. N. Lambrecht, and J. Tschopp Cutting Edge: Alum Adjuvant Stimulates Inflammatory Dendritic Cells through Activation of the NALP3 Inflammasome J. Immunol., September 15, 2008; 181(6): 3755 - 3759. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Heiss, N. Janner, B. Mahnss, V. Schumacher, F. Koch-Nolte, F. Haag, and H.-W. Mittrucker High Sensitivity of Intestinal CD8+ T Cells to Nucleotides Indicates P2X7 as a Regulator for Intestinal T Cell Responses J. Immunol., September 15, 2008; 181(6): 3861 - 3869. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Hara, K. Tsuchiya, T. Nomura, I. Kawamura, S. Shoma, and M. Mitsuyama Dependency of Caspase-1 Activation Induced in Macrophages by Listeria monocytogenes on Cytolysin, Listeriolysin O, after Evasion from Phagosome into the Cytoplasm J. Immunol., June 15, 2008; 180(12): 7859 - 7868. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Piccini, S. Carta, S. Tassi, D. Lasiglie, G. Fossati, and A. Rubartelli ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1{beta} and IL-18 secretion in an autocrine way PNAS, June 10, 2008; 105(23): 8067 - 8072. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. E. Warren, D. P. Mao, A. E. Rodriguez, E. A. Miao, and A. Aderem Multiple Nod-Like Receptors Activate Caspase 1 during Listeria monocytogenes Infection J. Immunol., June 1, 2008; 180(11): 7558 - 7564. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Dostert, V. Petrilli, R. Van Bruggen, C. Steele, B. T. Mossman, and J. Tschopp Innate Immune Activation Through Nalp3 Inflammasome Sensing of Asbestos and Silica Science, May 2, 2008; 320(5876): 674 - 677. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Marina-Garcia, L. Franchi, Y.-G. Kim, D. Miller, C. McDonald, G.-J. Boons, and G. Nunez Pannexin-1-Mediated Intracellular Delivery of Muramyl Dipeptide Induces Caspase-1 Activation via Cryopyrin/NLRP3 Independently of Nod2 J. Immunol., March 15, 2008; 180(6): 4050 - 4057. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Cheng, P. Shivshankar, Z. Li, L. Chen, I-T. Yeh, and G. Zhong Caspase-1 Contributes to Chlamydia trachomatis-Induced Upper Urogenital Tract Inflammatory Pathologies without Affecting the Course of Infection Infect. Immun., February 1, 2008; 76(2): 515 - 522. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. M. Wilmanski, T. Petnicki-Ocwieja, and K. S. Kobayashi NLR proteins: integral members of innate immunity and mediators of inflammatory diseases J. Leukoc. Biol., January 1, 2008; 83(1): 13 - 30. [Abstract] [Full Text] [PDF]
|
|
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| All ASBMB Journals | Molecular and Cellular Proteomics |
| Journal of Lipid Research | ASBMB Today |