Commensal bacteria-induced inflammasome activation in mouse and human macrophages is dependent on potassium efflux but does not require phagocytosis or bacterial viability

PLoS ONE

Volumn 11, Issue 8, 2016, Pages

  Chen, Kejie ^a,b   Shanmugam, Nanda Kumar N ^a   Pazos, Michael A ^a   Hurley, Bryan P ^a   Cherayil, Bobby J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; CYTOCHALASIN D; INFLAMMASOME; INTERLEUKIN 1BETA; POTASSIUM; RUTHENIUM RED; INTERLEUKIN 1BETA CONVERTING ENZYME;

ANIMAL CELL; ARTICLE; BACTERIAL VIABILITY; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM INFANTIS; BONE MARROW DERIVED MACROPHAGE; COMMENSAL; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; INTESTINE; MACROPHAGE; MONOCYTE; MONOCYTE DERIVED MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; POTASSIUM TRANSPORT; PROTEIN ACTIVATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MODIFICATION; ANIMAL; BIFIDOBACTERIUM LONGUM; BONE MARROW CELL; C57BL MOUSE; CELL LINE; CYTOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIFIDOBACTERIUM LONGUM; BIOLOGICAL TRANSPORT; BONE MARROW CELLS; CASPASE 1; CELL LINE; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROBIAL VIABILITY; PHAGOCYTOSIS; POTASSIUM;

EID: 84983756999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0160937     Document Type: Article

References (45)

1. Vanaja SK, Rathinam VAK, Fitzgerald KA. Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol. 2015; 25: 308-315. doi: 10.1016/j.tcb.2014.12.009 PMID: 25639489
2. Storek KM, Monak DM. Bacterial recognition pathways that lead to inflammasome activation. Immunol Rev. 2015; 265: 112-129. doi: 10.1111/imr.12289 PMID: 25879288
3. Garlanda C, Dinarello CA, Mantovani A. The interleukin-1 family: back to the future. Immunity. 2013; 39: 1003-1018. doi: 10.1016/j.immuni.2013.11.010 PMID: 24332029
4. Schett G, Dayer JM, Manger B. Interleukin-1 function and role in rheumatic disease. Nat Rev Rheumatol. 2016; 12: 14-24. doi: 10.1038/nrrheum.2016.166 PMID: 26656658
5. Haneklaus M, O'Neill LA, Coll RC. Modulatory mechanisms controlling the NLRP3 inflammasome in inflammation: recent developments. Curr Opin Immunol. 2013; 25: 40-45. doi: 10.1016/j.coi.2012.12.004 PMID: 23305783
6. Wlodarska M, Kostic AD, Xavier RJ. An integrative view of microbiome-host interactions in inflammatory bowel diseases. Cell Host Microbe. 2015; 17: 577-591. doi: 10.1016/j.chom.2015.04.008 PMID: 25974300
7. Mahida YR, Wu K, Jewell DP. Enhanced production of IL-1β by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease. Gut. 1989; 30: 835-838. PMID: 2787769
8. Opipari A, Franchi L. Role of inflammasomes in intestinal inflammation and Crohn's disease. Inflamm Bowel Dis. 2015; 21: 173-181. doi: 10.1097/MIB.0000000000000230 PMID: 25517598
9. Seo SU, Kamada N, Munoz-Planillo R, Kim YG, Kim D, Koizumi Y, et al. Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury. Immunity. 2015; 42: 744-755. doi: 10.1016/j.immuni.2015.03.004 PMID: 25862092
10. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489: 220-230. doi: 10.1038/nature11550 PMID: 22972295
11. Yang J, Zhao Y, Shao F. Non-canonical activation of inflammatory caspases by cytosolic LPS in innate immunity. Curr Opin Immunol. 2015; 32: 78-83. doi: 10.1016/j.coi.2015.01.007 PMID: 25621708
12. Wang L, Trebicka E, Fu Y, Waggoner L, Akira L, Fitzgerald KA, et al. Regulation of lipopolysaccharide-induced translation of tumor necrosis factor-alpha by the Toll-like receptor 4 adaptor protein TRAM. J Innate Immun. 2011; 3: 437-446. doi: 10.1159/000324833 PMID: 21494017
13. Su CW, Cao Y, Zhang M, Kaplan J, Su L, Fu Y, et al. Helminth infection impairs autophagy-mediated killing of bacterial enteropathogens by macrophages. J Immunol. 2012; 189: 1459-1466. doi: 10.4049/jimmunol.1200484 PMID: 22732589
14. Kalantari P, DeOliveira RB, Chan J, Corbett Y, Rathinam V, Stutz A, et al. Dual engagement of the NLRP3 and AIM2 inflammasomes by Plasmodium-derived hemazoin and DNA during malaria. Cell Rep. 2014; 6: 196-210. doi: 10.1016/j.celrep.2013.12.014 PMID: 24388751
15. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008; 9: 847-856. doi: 10.1038/ni.1631 PMID: 18604214
16. Bonham KS, Orzalli MH, Hayashi K, Wolf AI, Glanemann C, Weninger W, et al. A promiscuous lipid-binding protein diversifies the subcellular sites of Toll-like receptor signal transduction. Cell. 2014; 156: 705-716. doi: 10.1016/j.cell.2014.01.019 PMID: 24529375
17. Shanmugam NK, Chen K, Cherayil BJ. Commensal bacteria-induced interleukin-1β (IL-1β) secreted by macrophages up-regulates hepcidin expression in hepatocytes by activating the bone morphogenetic protein signaling pathway. J Biol Chem. 2015; 290: 30637-30647. doi: 10.1074/jbc.M115.689190 PMID: 26515063
18. Vijayan D. Isolation and differentiation of monocyte-macrophages from human blood. Methods Mol Biol. 2012; 844: 183-187. doi: 10.1007/978-1-61779-527-5-13 PMID: 22262443
19. Lahiri A, Abraham C. Activation of pattern recognition receptors up-regulates metallothioneins, thereby increasing intracellular accumulation of zinc, autophagy, and bacterial clearance by macrophages. Gastroenterology. 2014; 147: 835-846. doi: 10.1053/j.gastro.2014.06.024 PMID: 24960189
20. Rhee SJ, Walker WA, Cherayil BJ. Developmentally regulated intestinal expression of IFNγ and its target genes and the age-specific response to enteric Salmonella infection. J Immunol. 2005; 175: 1127-1136. PMID: 16002714
21. Wang L, Johnson EE, Shi HN, Walker WA, Wessling-Resnick M, Cherayil BJ. Attenuated inflammatory responses in hemochromatosis reveal a role for iron in the regulation of macrophage cytokine translation. J Immunol. 2008; 181: 2723-2731. PMID: 18684963
22. Wang L, Harrington L, Trebicka E, Shi HN, Kagan JC, Hong CC, et al. Selective modulation of TLR4-activated inflammatory responses by altered iron homeostasis in mice. J Clin Invest. 2009; 119: 3322-3328. doi: 10.1172/JCI39939 PMID: 19809161
23. Liu Z, Zaki MH, Vogel P, Gurung P, Finlay BB, Deng W, et al. Role of inflammasomes in host defense against Citrobacter rodentium infection. J Biol Chem. 2012; 287: 16955-16964. doi: 10.1074/jbc.M112.358705 PMID: 22461621
24. + for caspase-1 activation induced by intracellular and extracellular bacteria. J Biol Chem. 2007; 282: 18810-18818. PMID: 17491021
25. Miller CM, Boulter NR, Fuller SJ, Zakrzewski AM, Lees MP, Saunders BM, et al. The role of the P2X7 receptor in infectious diseases. PLoS Pathog. 2011; 7: e1002212. doi: 10.1371/journal.ppat.1002212 PMID: 22102807
26. Eldridge MJG, Shenoy AR. Antimicrobial inflammasomes: unified signaling against diverse bacterial pathogens. Curr Opin Microbiol. 2015; 23: 32-41. doi: 10.1016/j.mib.2014.10.008 PMID: 25461570
27. Kankkune P, Teirilia L, Rintahaka J, Alenius H, Wolff H, Matikainen S. (1,3)-β-glucans activate both dectin-1 and NLRP3 inflammasome in human macrophages. J. Immunol. 2010; 184: 6335-6342. doi: 10.4049/jimmunol.0903019 PMID: 20421639
28. Shenderov K, Barber DL, Mayer-Barber KD, Gurcha SS, Jankovic D, Feng CG, et al. Cord factor and peptidoglycan recapitulate the Th17-promoting adjuvant activity of mycobacteria through mincle/CARD9 sgnaling and the inflammasome. J. Immunol. 2013; 190: 5722-5730. doi: 10.4049/jimmunol.1203343 PMID: 23630357
29. Ganesan S, Rathinam VA, Bossaller L, Army K, Kaiser WJ, Mocarski ES, et al. Caspase-8 modulates dectin-1 and complement receptor 3-driven IL-1β production in response to β-glucans and the fungal pathogen, Candida albicans. J. Immunol. 2014; 193: 2519-2530. doi: 10.4049/jimmunol.1400276 PMID: 25063877
30. Gringhuis SI, Kaptein TM, Wevers BA, Theelen B, van der Vlist M, Boekhout T, et al. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a non-canonical caspase-8 inflammasome. Nat. Immunol. 2012; 13: 246-54. doi: 10.1038/ni.2222 PMID: 22267217
31. Jun HK, Lee SH, Lee HR, Choi BK. Integrin α5β1 activates the NLRP3 inflammasome by direct interaction with a bacterial surface protein. Immunity. 2012; 36: 755-768. doi: 10.1016/j.immuni.2012.05.002 PMID: 22608495
32. Mortimer L, Moreau F, Cormick S, Chadee K. The NLRP3 inflammasome is a pathogen sensor for invasive Entamoeba histolytica via activation of α5β1 integrin at the macrophage-amebae intercellular junction. PLoS Pathog. 2015; 11: e1004887. doi: 10.1371/journal.ppat.1004887 PMID: 25955828
33. Hari A, Zhang Y, Tu Z, Detample P, Stenner M, Ganguly A, et al. Activation of NLRP3 inflammasome by crystalline structures via cell surface contact. Sci Rep. 2014; 4: 7281. doi: 10.1038/srep07281 PMID: 25445147
34. Canton J, Neculai D, Grinstein S. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol. 2013; 13: 621-634. doi: 10.1038/nri3515 PMID: 23928573
35. Sheedy FJ, Grebe A, Rayner KJ, Kalantari P, Ramkhelawon B, Carpenter SB, et al. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol. 2013; 14: 812-820. doi: 10.1038/ni.2639 PMID: 23812099
36. Liu W, Yin Y, Zhou Z, He M, Dai Y. OxLDL-induced IL-1β secretion promoting foam cells formation was mainly via CD36-mediated ROS production leading to NLRP3 inflammasome activation. Inflamm Res. 2014; 63: 33-43. PMID: 24121974
37. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature. 2008; 456: 264-268. doi: 10.1038/nature07383 PMID: 18849965
38. Coccia M, Harrison OJ, Schiering C, Asquith MJ, Becher B, Powrie F, et al. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J Exp Med. 2012; 209: 1595-1609. doi: 10.1084/jem.20111453 PMID: 22891275
39. Bersudsky M, Luski L, Fishman D, White RM, Ziv-Sokolovskaya N, Dotan S, et al. Non-redundant properties of IL-1α and IL-1β during acute colon inflammation in mice. Gut. 2014; 63: 598-609. doi: 10.1136/gutjnl-2012-303329 PMID: 23793223
40. Allen IC, TeKippe EM, Woodford RM, Uronis JM, Holl EK, Rogers AB, et al. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J Exp Med. 2010; 207: 1045-1056. doi: 10.1084/jem.20100050 PMID: 20385749
41. Bauer C, Duewell P, Mayer C, Lehr HA, Fitzgerald KA, Dauer M, et al. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 2010; 59: 1192-1199. doi: 10.1136/gut.2009.197822 PMID: 20442201
42. Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity. 2010; 32:379-391. doi: 10.1016/j.immuni.2010.03.003 PMID: 20303296
43. Bauer C, Duewell P, Lehr HA, Endres S, Schnurr M. Protective and aggravating effects of NLRP3 inflammasome activation in IBD models: influence of genetic and environmental factors. Dig Dis. 2012; 30: 82-90. doi: 10.1159/000341681 PMID: 23075874
44. Plantinga TS, Crisan TO, Oosting M, van de Veerdonk FL, de Jong DJ, Philpott DJ, et al. Crohn's disease-associated ATG16L1 polymorphism modulates pro-inflammatory cytokine responses selectively upon activation of NOD2. Gut. 2011; 60: 1229-1235. doi: 10.1136/gut.2010.228908 PMID: 21406388
45. de Luca A, Smeekens SP, Casagrande A, Iannitti R, Conway KL, Gresnigt MS, et al. IL-1 receptor blockade restores autophagy and reduces inflammation in chronic granulomatous disease in mice and in humans. Proc Natl Acad Sci USA. 2014; 111: 3526-3531. doi: 10.1073/pnas.1322831111 PMID: 24550444