Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3590-3599

  Wu, Jianbo ^a,b   Yan, Zhibo ^a,b   Schwartz, David E ^a   Yu, Jingui ^b   Malik, Asrar B ^a   Hu, Guochang ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPURINOL; CLODRONIC ACID; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EFFECT; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; VENTILATOR INDUCED LUNG INJURY;

ANIMALS; CARRIER PROTEINS; CASPASE 1; DISEASE MODELS, ANIMAL; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; PNEUMONIA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; URIC ACID; VENTILATOR-INDUCED LUNG INJURY;

EID: 84875464393     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200860     Document Type: Article

References (48)

1. Del Sorbo, L., and A. S. Slutsky. 2011. Acute respiratory distress syndrome and multiple organ failure. Curr. Opin. Crit. Care 17: 1-6.
2. Ganter, M. T., J. Roux, B. Miyazawa, M. Howard, J. A. Frank, G. Su, D. Sheppard, S. M. Violette, P. H. Weinreb, G. S. Horan, et al. 2008. Interleukin-1β causes acute lung injury via alphavbeta5 and alphavbeta6 integrin-dependent mechanisms. Circ. Res. 102: 804-812.
3. Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147.
4. Goodman, R. B., J. Pugin, J. S. Lee, and M. A. Matthay. 2003. Cytokinemediated inflammation in acute lung injury. Cytokine Growth Factor Rev. 14: 523-535.
5. Frank, J. A., J. F. Pittet, C. Wray, and M. A. Matthay. 2008. Protection from experimental ventilator-induced acute lung injury by IL-1 receptor blockade. Thorax 63: 147-153.
6. Conway Morris, A., K. Kefala, T. S. Wilkinson, O. L. Moncayo-Nieto, K. Dhaliwal, L. Farrell, T. S. Walsh, S. J. Mackenzie, D. G. Swann, P. J. Andrews, et al. 2010. Diagnostic importance of pulmonary interleukin-1β and interleukin-8 in ventilator-associated pneumonia. Thorax 65: 201-207.
7. Opitz, B., V. van Laak, J. Eitel, and N. Suttorp. 2010. Innate immune recognition in infectious and noninfectious diseases of the lung. Am. J. Respir. Crit. Care Med. 181: 1294-1309.
8. Dusinská, M., Z. Kovaciková, B. Vallová, and A. Collins. 1998. Responses of alveolar macrophages and epithelial type II cells to oxidative DNA damage caused by paraquat. Carcinogenesis 19: 809-812.
9. Holt, P. G., D. H. Strickland, M. E. Wikström, and F. L. Jahnsen. 2008. Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8: 142-152.
10. Eyal, F. G., C. R. Hamm, and J. C. Parker. 2007. Reduction in alveolar macrophages attenuates acute ventilator induced lung injury in rats. Intensive Care Med. 33: 1212-1218.
11. Frank, J. A., C. M. Wray, D. F. McAuley, R. Schwendener, and M. A. Matthay. 2006. Alveolar macrophages contribute to alveolar barrier dysfunction in ventilator-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 291: L1191-L1198.
12. Schroder, K., and J. Tschopp. 2010. The inflammasomes. Cell 140: 821-832.
13. van de Veerdonk, F. L., M. G. Netea, C. A. Dinarello, and L. A. Joosten. 2011. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol. 32: 110-116.
14. Chen, G. Y., and G. Nuñez. 2010. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10: 826-837.
15. Martinon, F., A. Mayor, and J. Tschopp. 2009. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27: 229-265.
16. Yu, H. B., and B. B. Finlay. 2008. The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 4: 198-208.
17. Lavnikova, N., S. Prokhorova, L. Helyar, and D. L. Laskin. 1993. Isolation and partial characterization of subpopulations of alveolar macrophages, granulocytes, and highly enriched interstitial macrophages from rat lung. Am. J. Respir. Cell Mol. Biol. 8: 384-392.
18. Martinon, F., V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
19. Wang, Y., R. D. Minshall, D. E. Schwartz, and G. Hu. 2011. Cyclic stretch induces alveolar epithelial barrier dysfunction via calpain-mediated degradation of p120-catenin. Am. J. Physiol. Lung Cell. Mol. Physiol. 301: L197-L206.
20. Tschumperlin, D. J., and S. S. Margulies. 1999. Alveolar epithelial surface areavolume relationship in isolated rat lungs. J. Appl. Physiol. 86: 2026-2033.
21. Wang, Y. L., A. B. Malik, Y. Sun, S. Hu, A. B. Reynolds, R. D. Minshall, and G. Hu. 2011. Innate immune function of the adherens junction protein p120-catenin in endothelial response to endotoxin. J. Immunol. 186: 3180-3187.
22. Dehne, N., U. Kerkweg, T. Otto, and J. Fandrey. 2007. The HIF-1 response to simulated ischemia in mouse skeletal muscle cells neither enhances glycolysis nor prevents myotube cell death. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R1693-R1701.
23. Zhou, R., A. S. Yazdi, P. Menu, and J. Tschopp. 2011. A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225.
24. Nakahira, K., J. A. Haspel, V. A. Rathinam, S. J. Lee, T. Dolinay, H. C. Lam, J. A. Englert, M. Rabinovitch, M. Cernadas, H. P. Kim, et al. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12: 222-230.
25. Hu, G., A. B. Malik, and R. D. Minshall. 2010. Toll-like receptor 4 mediates neutrophil sequestration and lung injury induced by endotoxin and hyperinflation. Crit. Care Med. 38: 194-201.
26. Liu, D., Z. Yan, R. D. Minshall, D. E. Schwartz, Y. Chen, and G. Hu. 2012. Activation of calpains mediates early lung neutrophilic inflammation in ventilator-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 302: L370-L379.
27. Provoost, S., T. Maes, N. S. Pauwels, T. Vanden Berghe, P. Vandenabeele, B. N. Lambrecht, G. F. Joos, and K. G. Tournoy. 2011. NLRP3/caspase-1- independent IL-1βeta production mediates diesel exhaust particle-induced pulmonary inflammation. J. Immunol. 187: 3331-3337.
28. Wen, H., D. Gris, Y. Lei, S. Jha, L. Zhang, M. T. Huang, W. J. Brickey, and J. P. Ting. 2011. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12: 408-415.
29. Carta, S., S. Tassi, I. Pettinati, L. Delfino, C. A. Dinarello, and A. Rubartelli. 2011. The rate of interleukin-1βeta secretion in different myeloid cells varies with the extent of redox response to Toll-like receptor triggering. J. Biol. Chem. 286: 27069-27080.
30. Rubartelli, A., F. Cozzolino, M. Talio, and R. Sitia. 1990. A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9: 1503-1510.
31. Le Feuvre, R. A., D. Brough, Y. K. Iwakura, K. Takeda, and N. J. Rothwell. 2002. Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J. Biol. Chem. 277: 3210-3218.
32. Hogquist, K. A., E. R. Unanue, and D. D. Chaplin. 1991. Release of IL-1 from mononuclear phagocytes. J. Immunol. 147: 2181-2186.
33. Dostert, C., V. Pétrilli, R. Van Bruggen, C. Steele, B. T. Mossman, and J. Tschopp. 2008. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320: 674-677.
34. Tsuchiya, K., H. Hara, I. Kawamura, T. Nomura, T. Yamamoto, S. Daim, S. R. Dewamitta, Y. Shen, R. Fang, and M. Mitsuyama. 2010. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. J. Immunol. 185: 1186-1195.
35. Dai, D. F., T. Chen, H. Szeto, M. Nieves-Cintrón, V. Kutyavin, L. F. Santana, and P. S. Rabinovitch. 2011. Mitochondrial targeted antioxidant Peptide ameliorates hypertensive cardiomyopathy. J. Am. Coll. Cardiol. 58: 73-82.
36. Li, N., K. Ragheb, G. Lawler, J. Sturgis, B. Rajwa, J. A. Melendez, and J. P. Robinson. 2003. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278: 8516-8525.
37. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425: 516-521.
38. Chen, C. J., H. Kono, D. Golenbock, G. Reed, S. Akira, and K. L. Rock. 2007. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 13: 851-856.
39. Kono, H., D. Karmarkar, Y. Iwakura, and K. L. Rock. 2010. Identification of the cellular sensor that stimulates the inflammatory response to sterile cell death. J. Immunol. 184: 4470-4478.
40. Kuipers, M. T., H. Aslami, J. R. Janczy, K. F. van der Sluijs, A. P. Vlaar, E. K. Wolthuis, G. Choi, J. J. Roelofs, R. A. Flavell, F. S. Sutterwala, et al. 2012. Ventilator-induced lung injury is mediated by the NLRP3 inflammasome. Anesthesiology 116: 1104-1115.
41. Dolinay, T., Y. S. Kim, J. Howrylak, G. M. Hunninghake, C. H. An, L. Fredenburgh, A. F. Massaro, A. Rogers, L. Gazourian, K. Nakahira, et al. 2012. Inflammasome-regulated cytokines are critical mediators of acute lung injury. Am. J. Respir. Crit. Care Med. 185: 1225-1234.
42. Cruz, C. M., A. Rinna, H. J. Forman, A. L. Ventura, P. M. Persechini, and D. M. Ojcius. 2007. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J. Biol. Chem. 282: 2871-2879.
43. Sorbara, M. T., and S. E. Girardin. 2011. Mitochondrial ROS fuel the inflammasome. Cell Res. 21: 558-560.
44. Kepp, O., L. Galluzzi, and G. Kroemer. 2011. Mitochondrial control of the NLRP3 inflammasome. Nat. Immunol. 12: 199-200.
45. Waters, C. M. 2004. Reactive oxygen species in mechanotransduction. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L484-L485.
46. Chapman, K. E., S. E. Sinclair, D. Zhuang, A. Hassid, L. P. Desai, and C. M. Waters. 2005. Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L834-L841.
47. Gasse, P., N. Riteau, S. Charron, S. Girre, L. Fick, V. Pétrilli, J. Tschopp, V. Lagente, V. F. Quesniaux, B. Ryffel, and I. Couillin. 2009. Uric acid is a danger signal activating NALP3 inflammasome in lung injury inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 179: 903-913.
48. Zaki, M. H., K. L. Boyd, P. Vogel, M. B. Kastan, M. Lamkanfi, and T. D. Kanneganti. 2010. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32: 379-391.