Inflammasome-induced IL-1β secretion in microglia is characterized by delayed kinetics and is only partially dependent on inflammatory caspases

Journal of Neuroscience

Volumn 35, Issue 2, 2015, Pages 678-687

  Burm, Saskia M ^a   Zuiderwijk Sick, Ella A ^a   T Jong, Anke E J ^a   Van Der Putten, Céline ^a   Veth, Jennifer ^a   Kondova, Ivanela ^a   Bajramovic, Jeffrey J ^a  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

Author keywords

IL 1 ; Inflammasome; Inflammatory caspases; Macrophages; Microglia

Indexed keywords

ADAPTOR PROTEIN; CASPASE; CASPASE 3; CASPASE 4; CASPASE 5; CASPASE 7; CASPASE 8; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CRYOPYRIN; END BINDING PROTEIN 1; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; NEURONAL APTOSIS INHIBITORY PROTEIN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PEPTIDES AND PROTEINS; PROTEIN AIM2; PROTEIN ASC; PROTEIN CARDINAL; PROTEIN IPAF; PROTEIN KINASE R; PROTEIN NALP1; PROTEIN NALP14; PROTEIN NALP4; PROTEIN NOD4; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; UNINDEXED DRUG; CASPASE RECRUITMENT DOMAIN PROTEIN 15;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CYTOKINE RELEASE; DOWN REGULATION; FEMALE; GENE; INNATE IMMUNITY; MACROPHAGE; MALE; MICROGLIA; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA TRANSLOCATION GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; WESTERN BLOTTING; ANIMAL; CELL CULTURE; GENETICS; KINETICS; METABOLISM; REACTION TIME; SECRETION (PROCESS);

ANIMALS; CASPASES; CELLS, CULTURED; FEMALE; INFLAMMASOMES; INTERLEUKIN-1BETA; KINETICS; MACACA MULATTA; MACROPHAGES; MALE; MICROGLIA; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; REACTION TIME;

EID: 84920982518     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2510-14.2015     Document Type: Article

References (60)

1. Abulafia DP, de Rivero Vaccari JP, Lozano JD, Lotocki G, Keane RW, Dietrich WD (2009) Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J Cereb Blood Flow Metab 29:534-544. CrossRef Medline
2. Antonopoulos C, El Sanadi C, Kaiser WJ, Mocarski ES, Dubyak GR (2013) Proapoptotic chemotherapeutic drugs induce noncanonical processing and release of IL-1beta via caspase-8 in dendritic cells. J Immunol 191: 4789–4803. CrossRef Medline
3. Bajramovic JJ (2011) Regulation of innate immune responses in the central nervous system. CNS Neurol Disord Drug Targets 10:4–24. CrossRef Medline
4. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia- Quintanilla A, Cano J, Brundin P, Englund E, Venero JL, Joseph B (2011) Caspase signalling controls microglia activation and neurotoxicity. Nature 472:319-324. CrossRef Medline
5. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-_-dependent molecular and functional signature in microglia. Nat Neurosci 17:131–143. CrossRef Medline
6. Cassel SL, Janczy JR, Bing X, Wilson SP, Olivier AK, Otero JE, Iwakura Y, Shayakhmetov DM, Bassuk AG, Abu-Amer Y, Brogden KA, Burns TL, Sutterwala FS, Ferguson PJ (2014) Inflammasome-independent IL- 1beta mediates autoinflammatory disease in Pstpip2-deficient mice. Proc Natl Acad Sci U S A 111:1072–1077. CrossRef Medline
7. Chang J, Yang L, Kouadir M, Peng Y, Zhang S, Shi F, Zhou X, Yin X, Zhao D (2012) Antibody-mediated inhibition of integrin alpha5beta1 blocks neurotoxic prion peptide PrP106–126-induced activation of BV2 microglia. J Mol Neurosci 48:248-252. CrossRef Medline
8. Chiu IM, Morimoto ET, Goodarzi H, Liao JT, O’Keeffe S, Phatnani HP, Muratet M, Carroll MC, Levy S, Tavazoie S, Myers RM, Maniatis T (2013) A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. Cell Rep 4:385-401. CrossRef Medline
9. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, Ways JP, Gray JG (1994) NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J Immun 153:712–723. Medline
10. De Bosscher K, Vanden Berghe W, Haegeman G (2003) The interplay between the glucocorticoid receptor and nuclear factor-kappaB or activator protein-1: molecular mechanisms for gene repression. Endocr Rev 24: 488–522. CrossRef Medline
11. Edye ME, Lopez-Castejon G, Allan SM, Brough D (2013) Acidosis drives damage-associated molecular pattern (DAMP)-induced interleukin-1 secretion via a caspase-1-independent pathway. J Biol Chem 288:30485-30494. CrossRef Medline
12. Euser SM, Hofman A, Westendorp RG, Breteler MM (2009) Serum uric acid and cognitive function and dementia. Brain 132:377–382. CrossRef Medline
13. Furr SR, Chauhan VS, Sterka D Jr, Grdzelishvili V, Marriott I (2008) Characterization of retinoic acid-inducible gene-I expression in primary murine glia following exposure to vesicular stomatitis virus. J Neurovirol 14:503–513. CrossRef Medline
14. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841-845. CrossRef Medline
15. Greenhalgh AD, David S (2014) Differences in the phagocytic response of microglia and peripheral macrophages after spinal cord injury and its effects on cell death. J Neurosci 34:6316- 6322. CrossRef Medline
16. Gringhuis SI, Kaptein TM, Wevers BA, Theelen B, van der Vlist M, Boekhout T, Geijtenbeek TB (2012) Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1beta via a noncanonical caspase-8 inflammasome. Nat Immunol 13:246-254. CrossRef Medline
17. Hafner-Bratkovicˇ I, Bencˇina M, Fitzgerald KA, Golenbock D, Jerala R (2012) NLRP3 inflammasome activation in macrophage cell lines by prion protein fibrils as the source of IL-1beta and neuronal toxicity. Cell Mol Life Sci 69:4215-4228. CrossRef Medline
18. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT (2008) The NALP3 inflammasome is involved in the innate immune response to amyloidbeta. Nat Immunol 9:857-865. CrossRef Medline
19. Hanamsagar R, Torres V, Kielian T (2011) Inflammasome activation and IL-1beta/IL-18 processing are influenced by distinct pathways in microglia. J Neurochem 119:736-748. CrossRef Medline
20. Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, Gelpi E, Halle A, Korte M, Latz E, Golenbock DT (2013) NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature 493:674–678. CrossRef Medline
21. Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16:1896-1905. CrossRef Medline
22. Jamilloux Y, Pierini R, Querenet M, Juruj C, Fauchais AL, Jauberteau MO, Jarraud S, Lina G, Etienne J, Roy CR, Henry T, Davoust N, Ader F (2013) Inflammasome activation restricts Legionella pneumophila replication in primary microglial cells through flagellin detection. Glia 61:539-549. CrossRef Medline
23. Joosten LA, Netea MG, Fantuzzi G, Koenders MI, Helsen MM, Sparrer H, Pham CT, van der Meer JW, Dinarello CA, van den Berg WB (2009) Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum 60:3651–3662. CrossRef Medline
24. Karmakar M, Sun Y, Hise AG, Rietsch A, Pearlman E (2012) Cutting edge: IL-1beta processing during Pseudomonas aeruginosa infection is mediated by neutrophil serine proteases and is independent of NLRC4 and caspase-1. J Immunol 189:4231-4235. CrossRef Medline
25. Kaushik DK, Gupta M, Kumawat KL, Basu A (2012) NLRP3 inflammasome: key mediator of neuroinflammation in murine Japanese encephalitis. PloS One 7:e32270. CrossRef Medline
26. Khare S, Dorfleutner A, Bryan NB, Yun C, Radian AD, de Almeida L, Rojanasakul Y, Stehlik C (2012) An NLRP7-containing inflammasome mediates recognition of microbial lipopeptides in human macrophages. Immunity 36:464–476. CrossRef Medline
27. Latz E (2010) The inflammasomes: mechanisms of activation and function. Curr Opin Immunol 22:28-33. CrossRef Medline
28. Lee HM, Kang J, Lee SJ, Jo EK (2013) Microglial activation of the NLRP3 inflammasome by the priming signals derived from macrophages infected with mycobacteria. Glia 61:441-452. CrossRef Medline
29. Lee W, Mitchell P, Tjian R (1987) Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell 49:741–752. CrossRef Medline
30. Maetzler W, Stapf AK, Schulte C, Hauser AK, Lerche S, Wurster I, Schleicher E, Melms A, Berg D (2011) Serum and cerebrospinal fluid uric acid levels in lewy body disorders: associations with disease occurrence and amyloid-beta pathway. J Alzheimers Dis 27:119-126. CrossRef Medline
31. Martinon F, Tschopp J (2004) Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117:561-574. CrossRef Medline
32. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417-426. CrossRef Medline
33. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J (2006) Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440:237–241. CrossRef Medline
34. Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27:229-265. CrossRef Medline
35. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, Kepp O, Metivier D, Galluzzi L, Perfettini JL, Zitvogel L, Kroemer G (2014) Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 21:79-91. CrossRef Medline
36. McFarland NR, Burdett T, Desjardins CA, Frosch MP, Schwarzschild MA (2013) Postmortem brain levels of urate and precursors in Parkinson’s disease and related disorders. Neurodegener Dis 12:189–198. CrossRef Medline
37. Meissner F, Molawi K, Zychlinsky A (2010) Mutant superoxide dismutase 1-induced IL-1beta accelerates ALS pathogenesis. Proc Natl Acad Sci U S A 107:13046-13050. CrossRef Medline
38. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, van der Meer JH, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I, Funk CJ, Mason RJ, Kullberg BJ, Rubartelli A, van der Meer JW, Dinarello CA (2009) Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113:2324-2335. CrossRef Medline
39. Olson JK, Miller SD (2004) Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173: 3916–3924. CrossRef Medline
40. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. CrossRef Medline
41. Rabuffetti M, Sciorati C, Tarozzo G, Clementi E, Manfredi AA, Beltramo M (2000) Inhibition of caspase-1-like activity by Ac-Tyr-Val-Ala-Aspchloromethyl ketone induces long-lasting neuroprotection in cerebral ischemia through apoptosis reduction and decrease of proinflammatory cytokines. J Neurosci 20:4398–4404. Medline
42. Raivich G, Banati R (2004) Brain microglia and blood-derived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev 46:261–281. CrossRef Medline
43. Rock KL, Kono H (2008) The inflammatory response to cell death. Annu Rev Pathol 3:99-126. CrossRef Medline
44. Salminen A, Ojala J, Suuronen T, Kaarniranta K, Kauppinen A (2008) Amyloid-beta oligomers set fire to inflammasomes and induce Alzheimer’s pathology. J Cell Mol Med 12:2255–2262. CrossRef Medline
45. Schneider M, Zimmermann AG, Roberts RA, Zhang L, Swanson KV, Wen H, Davis BK, Allen IC, Holl EK, Ye Z, Rahman AH, Conti BJ, Eitas TK, Koller BH, Ting JP (2012) The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-kappaB. Nat Immunol 13:823–831. CrossRef Medline
46. Schonbeck U, Mach F, Libby P (1998) Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol 161:3340-3346. Medline
47. Shah VB, Huang Y, Keshwara R, Ozment-Skelton T, Williams DL, Keshvara L (2008) Beta-glucan activates microglia without inducing cytokine production in Dectin-1-dependent manner. J Immunol 180:2777–2785. CrossRef Medline
48. Shi F, Yang L, Kouadir M, Yang Y, Wang J, Zhou X, Yin X, Zhao D (2012) The NALP3 inflammasome is involved in neurotoxic prion peptide-induced microglial activation. J Neuroinflammation 9:73. CrossRef Medline
49. Shi F, Yang L, Kouadir M, Yang Y, Ding T, Wang J, Zhou X, Yin X, Zhao D (2013) Prion protein participates in the regulation of classical and alternative activation of BV2 microglia. J Neurochem 124:168–174. CrossRef Medline
50. Shi Y, Evans JE, Rock KL (2003) Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425:516-521. CrossRef Medline
51. Sollberger G, Strittmatter GE, Kistowska M, French LE, Beer HD (2012) Caspase-4 is required for activation of inflammasomes. J Immunol 188: 1992–2000. CrossRef Medline
52. Stehlik C (2009) Multiple interleukin-1beta-converting enzymes contribute to inflammatory arthritis. Arthritis Rheum 60:3524–3530. CrossRef Medline
53. Terada K, Yamada J, Hayashi Y, Wu Z, Uchiyama Y, Peters C, Nakanishi H (2010) Involvement of cathepsin B in the processing and secretion of interleukin-1beta in chromogranin A-stimulated microglia. Glia 58:114-124. CrossRef Medline
54. Ting JP, Duncan JA, Lei Y (2010) How the noninflammasome NLRs function in the innate immune system. Science 327:286–290. CrossRef Medline
55. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I, Ijzerman AP, Bajramovic JJ (2009) Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 182:7603–7612. CrossRef Medline
56. Walsh JG, Reinke SN, Mamik MK, McKenzie BA, Maingat F, Branton WG, Broadhurst DI, Power C (2014) Rapid inflammasome activation in microglia contributes to brain disease in HIV/AIDS. Retrovirology 11:35. CrossRef Medline
57. Wu Z, Sun L, Hashioka S, Yu S, Schwab C, Okada R, Hayashi Y, McGeer PL, Nakanishi H (2013) Differential pathways for interleukin-1beta production activated by chromogranin A and amyloid beta in microglia. Neurobiol Aging 34:2715–2725. CrossRef Medline
58. Xiao Y, Jin J, Chang M, Chang JH, Hu H, Zhou X, Brittain GC, Stansberg C, Torkildsen Ø, Wang X, Brink R, Cheng X, Sun SC (2013) Peli1 promotes microglia-mediated CNS inflammation by regulating Traf3 degradation. Nat Med 19:595-602. CrossRef Medline
59. Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469:221–225. CrossRef Medline
60. Zuiderwijk-Sick EA, van der Putten C, Bsibsi M, Deuzing IP, de Boer W, Persoon-Deen C, Kondova I, Boven LA, van Noort JM, ‘t Hart BA, Amor S, Bajramovic JJ (2007) Differentiation of primary adult microglia alters their response to TLR8-mediated activation but not their capacity as APC. Glia 55:1589-1600. CrossRef Medline