Mitochondrial damage contributes to pseudomonas aeruginosa activation of the inflammasome and is downregulated by autophagy

Autophagy

Volumn 11, Issue 1, 2015, Pages 166-182

  Jabir, Majid Sakhi ^a,b   Hopkins, Lee ^c   Ritchie, Neil D ^a   Ullah, Ihsan ^a   Bayes, Hannah K ^a   Li, Dong ^a   Tourlomousis, Panagiotis ^c   Lupton, Alison ^d   Puleston, Daniel ^e   Simon, Anna Katharina ^e   Bryant, Clare ^c   Evans, Thomas J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF TECHNOLOGY   (Iraq)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d WESTERN INFIRMARY   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA detection; Infection; Mitophagy; NLR proteins; Secretion system; Type iii

Indexed keywords

3 METHYLADENINE; INFLAMMASOME; LACTATE DEHYDROGENASE; MICROTUBULE ASSOCIATED PROTEIN 1; MITOCHONDRIAL DNA; NLRC4 INFLAMMASOME; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; AIM2 PROTEIN, MOUSE; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; DNA BINDING PROTEIN; IPAF PROTEIN, MOUSE; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BONE MARROW CELL; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN DNA INTERACTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; FEMALE; HEK293 CELL LINE; METABOLISM; MICROBIOLOGY; MITOPHAGY; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BONE MARROW CELLS; CALCIUM-BINDING PROTEINS; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; DOWN-REGULATION; FEMALE; HEK293 CELLS; HUMANS; INFLAMMASOMES; MACROPHAGES; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REACTIVE OXYGEN SPECIES;

EID: 84923325462     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/15548627.2014.981915     Document Type: Article

References (39)

1. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol 2012; 13:325-32; PMID:22430785; http:// dx.doi.org/10.1038/ni.2231
2. Smith DE. The biological paths of IL-1 family members IL18 and IL-33. J Leukoc Biol 2011; 89:383-92; PMID:20952658; http://dx.doi.org/10.1189/jlb. 0810470
3. Franchi L, Stoolman J, Kanneganti TD, Verma A, Ramphal R, Nunez G. Critical role for Ipaf in Pseudomonas aeruginosa-induced CASP1 activation. Eur J Immunol 2007; 37:3030-9; PMID:17935074; http:// dx.doi.org/10.1002/eji.200737532
4. Miao EA, Ernst RK, Dors M, Mao DP, Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc Natl Acad Sci U S A 2008; 105:2562-7; PMID:18256184; http://dx.doi.org/10.1073/pnas. 0712183105
5. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 2010; 107:3076-80; PMID:20133635; http://dx.doi. org/10.1073/pnas.0913087107
6. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, Xu H, Liu L, Shao F. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 2011; 477:596-600; PMID:21918512; http://dx.doi. org/10.1038/nature10510
7. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, Dunipace EA, Henry T, Sun YH, Cado D, Dietrich WF, et al. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 2008; 9:1171-8; PMID:18724372; http://dx.doi.org/ 10.1038/ni.1646
8. Yang J, Zhao Y, Shi J, Shao F. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci U S A 2013; 110:14408-13; PMID:23940371
9. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. The inflammasome: a CASP1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 2009; 10:241-7; PMID:19221555; http://dx.doi.org/10.1038/ni.1703
10. Munoz-Planillo R, Kuffa P, Martinez-Colon G, Smith BL, Rajendiran TM, Nunez G. K(C) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity 2013; 38:1142-53; PMID:23809161; http://dx.doi. org/10.1016/j.immuni.2013.05.016
11. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012; 36:401-14; PMID:22342844; http:// dx.doi.org/10.1016/j.immuni.2012.01.009
12. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-30; PMID:21151103; http://dx.doi.org/10.1038/ni.1980
13. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang B-G, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456:264-8; PMID:18849965; http://dx. doi.org/10.1038/nature07383
14. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, Waggoner L, Vanaja SK, Monks BG, Ganesan S, Latz E, et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 2010; 11:395-402; PMID:20351692; http://dx.doi.org/10.1038/ni.1864
15. Subramanian N, Natarajan K, Clatworthy MR, Wang Z, Germain RN. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 2013; 153:348-61; PMID:23582325; http://dx.doi.org/10.1016/j.cell.2013.02.054
16. Higa N, Toma C, Koizumi Y, Nakasone N, Nohara T, Masumoto J, Kodama T, Iida T, Suzuki T, et al. Vibrio parahaemolyticus effector proteins suppress inflammasome activation by interfering with host autophagy signaling. PLoS Pathog 2013; 9:e1003142; PMID:23357873; http://dx.doi.org/10.1371/journal. ppat.1003142
17. Jabir MS, Ritchie ND, Li D, Bayes HK, Tourlomousis P, Puleston D, Lupton A, Hopkins L, Simon AK, Bryant C, et al. Caspase-1 Cleavage of the TLR Adaptor TRIF Inhibits Autophagy and beta-Interferon Production during Pseudomonas aeruginosa Infection. Cell Host Microbe 2014; 15:214-27; PMID:24528867; http://dx.doi.org/10.1016/j.chom.2014.01.010
18. Sutterwala FS, Mijares LA, Li L, Ogura Y, Kazmierczak BI, Flavell RA. Immune recognition of Pseudomonas aeruginosa mediated by the IPAFNLRC4 inflammasome. J Exp Med 2007; 204:3235-45; PMID: 18070936; http:// dx.doi.org/10.1084/jem.20071239
19. Arlehamn CS, Evans TJ. Pseudomonas aeruginosa pilin activates the inflammasome. Cell Microbiol 2011; 13:388-401; PMID: 20955240; http://dx.doi.org/ 10.1111/j.1462-5822.2010.01541.x
20. Yuan K, Huang C, Fox J, Laturnus D, Carlson E, Zhang B, Yin Q, Gao H, Wu M. Autophagy plays an essential role in the clearance of Pseudomonas aeruginosa by alveolar macrophages. J Cell Sci 2012; 125:507-15; PMID:22302984; http://dx.doi.org/ 10.1242/jcs.094573
21. Mortensen M, Ferguson DJ, Edelmann M, Kessler B, Morten KJ, Komatsu M, Simon AK. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci U S A 2010; 107:832-7; PMID:20080761; http://dx. doi.org/10.1073/pnas.0913170107
22. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
23. Stromhaug PE, Klionsky DJ. Approaching the molecular mechanism of autophagy. Traffic 2001; 2:524-31; PMID:11489210; http://dx.doi.org/10.1034/j.1600-0854.2001.20802.x
24. Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim Biophys Acta 2013; 1833:205-12; PMID:22406072; http://dx. doi.org/10.1016/j.bbamcr.2012.02.012
25. Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci 2012; 125:795-9; PMID: 22448035; http://dx.doi.org/10.1242/jcs.093849
26. Smith RA, Hartley RC, Murphy MP. Mitochondriatargeted small molecule therapeutics and probes. Antioxid Redox Signal 2011; 15:3021-38; PMID: 21395490; http://dx.doi.org/10.1089/ars.2011.3969
27. Kofoed EM, Vance RE. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011; 477:592-5; PMID: 21874021; http://dx.doi.org/10.1038/nature10394
28. Hashiguchi K, Zhang-Akiyama QM. Establishment of human cell lines lacking mitochondrial DNA. Methods Mol Biol 2009; 554:383-91; PMID:19513686; http:// dx.doi.org/10.1007/978-1-59745-521-3-23
29. Maki H, Sekiguchi M. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 1992; 355:273-5; PMID:1309939; http://dx.doi.org/10.1038/355273a0
30. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Vervatn A, Bjørkøy G, Johansen T. p62SQSTM1 binds directly to Atg8LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-45; PMID: 17580304; http://dx.doi.org/10.1074/jbc.M702824200
31. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. Cytoplasmic flagellin activates CASP1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 2006; 7:569-75; PMID: 16648853; http://dx.doi.org/10.1038/ni1344
32. Billen LP, Shamas-Din A, Andrews DW. Bid: a Bax-like BH3 protein. Oncogene 2008; 27 Suppl 1:S93-104; http://dx.doi.org/10.1038/onc.2009.47
33. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002; 10:417-26; PMID:12191486; http://dx.doi.org/ 10.1016/S1097-2765(02)00599-3
34. Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, Cresswell P, MacMicking JD. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 2012; 336:481-5; PMID: 22461501; http://dx.doi.org/10.1126/science.1217141
35. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, Leong JM, Fitzgerald KA. TRIF licenses CASP11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012; 150:606-19; PMID:22819539; http://dx.doi.org/ 10.1016/j.cell.2012.07.007
36. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S,Dong J,Newton K,Qu Y, Liu J, Heldens S, et al. Non-canonical inflammasome activation targetsCASP11. Nature 2011; 479:117-21; PMID: 22002608; http://dx. doi.org/10.1038/nature10558
37. Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, Stranks AJ, Glanville J, Knight S, Jacobsen SE, et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med 2011; 208:455-67; PMID: 21339326; http://dx.doi.org/10.1084/jem.20101145
38. Celada A, Gray PW, Rinderknecht E, Schreiber RD. Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J Exp Med 1984; 160:55-74; PMID:6330272; http://dx.doi.org/ 10.1084/jem.160.1.55
39. Eng KE, Panas MD, Karlsson Hedestam GB,McInerney GM. A novel quantitative flow cytometry-based assay for autophagy. Autophagy 2010; 6:634-41; PMID: 20458170; http://dx.doi.org/10.4161/auto.6.5.12112