Autophagy deficiency in macrophages enhances NLRP3 inflammasome activity and chronic lung disease following silica exposure

Toxicology and Applied Pharmacology

Volumn 309, Issue , 2016, Pages 101-110

  Jessop, Forrest ^a   Hamilton, Raymond F ^a   Rhoderick, Joseph F ^a   Shaw, Pamela K ^a   Holian, Andrij ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Atg5; Autophagy; HMGB1; IL 18; NLRP3 Inflammasome; Silicosis

Indexed keywords

AUTOPHAGY PROTEIN 5; CATHEPSIN B; CATHEPSIN L; CATHEPSIN V; CRYOPYRIN; CXCL1 CHEMOKINE; HIGH MOBILITY GROUP B1 PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; SILICON DIOXIDE; HMGB1 PROTEIN, MOUSE; NLRP3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BONE MARROW CELL; BONE MARROW DERIVED MACROPHAGE; BRONCHOALVEOLAR LAVAGE FLUID; CHRONIC LUNG DISEASE; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DISEASE COURSE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LUNG ALVEOLUS MACROPHAGE; LUNG FIBROSIS; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; SILICOSIS; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; LUNG; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; AUTOPHAGY; FEMALE; HMGB1 PROTEIN; LUNG; MACROPHAGES, ALVEOLAR; MALE; MICE; MICE, TRANSGENIC; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; SILICON DIOXIDE;

EID: 84986556228     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2016.08.029     Document Type: Article

References (44)

1. Abdel Fattah, E., Bhattacharya, A., Herron, A., Safdar, Z., Eissa, N.T., Critical role for IL-18 in spontaneous lung inflammation caused by autophagy deficiency. J. Immunol. 194 (2015), 5407–5416.
2. Beamer, C.A., Migliaccio, C.T., Jessop, F., Trapkus, M., Yuan, D., Holian, A., Innate immune processes are sufficient for driving silicosis in mice. J. Leukoc. Biol. 88 (2010), 547–557.
3. Biswas, R., Hamilton, R.F. Jr., Holian, A., Role of lysosomes in silica-induced inflammasome activation and inflammation in absence of MARCO. J Immunol Res, 2014, 2014, 304180.
4. Cassel, S.L., Eisenbarth, S.C., Iyer, S.S., Sadler, J.J., Colegio, O.R., Tephly, L.A., Carter, A.B., Rothman, P.B., Flavell, R.A., Sutterwala, F.S., The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 9035–9040.
5. Castillo, E.F., Dekonenko, A., Arko-Mensah, J., Mandell, M.A., Dupont, N., Jiang, S., Delgado-Vargas, M., Timmins, G.S., Bhattacharya, D., Yang, H., Hutt, J., Lyons, C.R., Dobos, K.M., Deretic, V., Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E3168–E3176.
6. Chen, Z.H., Kim, H.P., Sciurba, F.C., Lee, S.J., Feghali-Bostwick, C., Stolz, D.B., Dhir, R., Landreneau, R.J., Schuchert, M.J., Yousem, S.A., Nakahira, K., Pilewski, J.M., Lee, J.S., Zhang, Y., Ryter, S.W., Choi, A.M., Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS One, 3, 2008, e3316.
7. Chen, S., Yuan, J., Yao, S., Jin, Y., Chen, G., Tian, W., Xi, J., Xu, Z., Weng, D., Chen, J., Lipopolysaccharides may aggravate apoptosis through accumulation of autophagosomes in alveolar macrophages of human silicosis. Autophagy 11 (2015), 2346–2357.
8. Cohen, R.A., Petsonk, E.L., Rose, C., Young, B., Regier, M., Najmuddin, A., Abraham, J.L., Churg, A., Green, F.H., Lung pathology in U.S. coal workers with rapidly progressive pneumoconiosis implicates silica and silicates. Am. J. Respir. Crit. Care Med. 193 (2016), 673–680.
9. Dinarello, C.A., Interleukin-18 and the pathogenesis of inflammatory diseases. Semin. Nephrol. 27 (2007), 98–114.
10. Dinarello, C.A., Novick, D., Kim, S., Kaplanski, G., Interleukin-18 and IL-18 binding protein. Front. Immunol., 4, 2013, 289.
11. Dupont, N., Jiang, S., Pilli, M., Ornatowski, W., Bhattacharya, D., Deretic, V., Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1beta. EMBO J. 30 (2011), 4701–4711.
12. Girtsman, T.A., Beamer, C.A., Wu, N., Buford, M., Holian, A., IL-1R signalling is critical for regulation of multi-walled carbon nanotubes-induced acute lung inflammation in C57Bl/6 mice. Nanotoxicology 8 (2014), 17–27.
13. Hamilton, R.F., Wu, N., Xiang, C., Li, M., Yang, F., Wolfarth, M., Porter, D.W., Holian, A., Synthesis, characterization, and bioactivity of carboxylic acid-functionalized titanium dioxide nanobelts. Part Fibre Toxicol, 11, 2014, 43.
14. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., Mizushima, N., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889.
15. Harris, J., Hartman, M., Roche, C., Zeng, S.G., O'Shea, A., Sharp, F.A., Lambe, E.M., Creagh, E.M., Golenbock, D.T., Tschopp, J., Kornfeld, H., Fitzgerald, K.A., Lavelle, E.C., Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J. Biol. Chem. 286 (2011), 9587–9597.
16. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E.O., Kono, H., Rock, K.L., Fitzgerald, K.A., Latz, E., Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9 (2008), 847–856.
17. Jessop, F., Holian, A., Extracellular HMGB1 regulates multi-walled carbon nanotube-induced inflammation in vivo. Nanotoxicology 9 (2015), 365–372.
18. Klionsky, D.J., Elazar, Z., Seglen, P.O., Rubinsztein, D.C., Does bafilomycin A1 block the fusion of autophagosomes with lysosomes?. Autophagy 4 (2008), 849–850.
19. Lamkanfi, M., Sarkar, A., Vande Walle, L., Vitari, A.C., Amer, A.O., Wewers, M.D., Tracey, K.J., Kanneganti, T.D., Dixit, V.M., Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 185 (2010), 4385–4392.
20. Lee, J., Kim, H.R., Quinley, C., Kim, J., Gonzalez-Navajas, J., Xavier, R., Raz, E., Autophagy suppresses interleukin-1beta (IL-1beta) signaling by activation of p62 degradation via lysosomal and proteasomal pathways. J. Biol. Chem. 287 (2012), 4033–4040.
21. Li, R., Ji, Z., Qin, H., Kang, X., Sun, B., Wang, M., Chang, C.H., Wang, X., Zhang, H., Zou, H., Nel, A.E., Xia, T., Interference in autophagosome fusion by rare earth nanoparticles disrupts autophagic flux and regulation of an interleukin-1beta producing inflammasome. ACS Nano 8 (2014), 10280–10292.
22. Liu, Y., Levine, B., Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ. 22 (2015), 367–376.
23. Lu, M., Yu, S., Xu, W., Gao, B., Xiong, S., HMGB1 promotes systemic lupus erythematosus by enhancing macrophage inflammatory response. J Immunol Res, 2015, 2015, 946748.
24. Luciani, A., Villella, V.R., Esposito, S., Brunetti-Pierri, N., Medina, D., Settembre, C., Gavina, M., Pulze, L., Giardino, I., Pettoello-Mantovani, M., D'Apolito, M., Guido, S., Masliah, E., Spencer, B., Quaratino, S., Raia, V., Ballabio, A., Maiuri, L., Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat. Cell Biol. 12 (2010), 863–875.
25. Matsumoto, G., Wada, K., Okuno, M., Kurosawa, M., Nukina, N., Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol. Cell 44 (2011), 279–289.
26. Migliaccio, C.T., Hamilton, R.F. Jr., Holian, A., Increase in a distinct pulmonary macrophage subset possessing an antigen-presenting cell phenotype and in vitro APC activity following silica exposure. Toxicol. Appl. Pharmacol. 205 (2005), 168–176.
27. Migliaccio, C.T., Buford, M.C., Jessop, F., Holian, A., The IL-4Ralpha pathway in macrophages and its potential role in silica-induced pulmonary fibrosis. J. Leukoc. Biol. 83 (2008), 630–639.
28. Mizushima, N., Ohsumi, Y., Yoshimori, T., Autophagosome formation in mammalian cells. Cell Struct. Funct. 27 (2002), 421–429.
29. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., Ohsumi, Y., In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15 (2004), 1101–1111.
30. Monick, M.M., Powers, L.S., Walters, K., Lovan, N., Zhang, M., Gerke, A., Hansdottir, S., Hunninghake, G.W., Identification of an autophagy defect in smokers' alveolar macrophages. J. Immunol. 185 (2010), 5425–5435.
31. Nakahira, K., Choi, A.M., Autophagy: a potential therapeutic target in lung diseases. Am. J. Phys. Lung Cell. Mol. Phys. 305 (2013), L93–107.
32. Pankiv, S., Clausen, T.H., Lamark, T., Brech, A., Bruun, J.A., Outzen, H., Overvatn, A., Bjorkoy, G., Johansen, T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282 (2007), 24131–24145.
33. Patel, A.S., Lin, L., Geyer, A., Haspel, J.A., An, C.H., Cao, J., Rosas, I.O., Morse, D., Autophagy in idiopathic pulmonary fibrosis. PLoS One, 7, 2012, e41394.
34. Sager, T.M., Wolfarth, M.W., Andrew, M., Hubbs, A., Friend, S., Chen, T.H., Porter, D.W., Wu, N., Yang, F., Hamilton, R.F., Holian, A., Effect of multi-walled carbon nanotube surface modification on bioactivity in the C57BL/6 mouse model. Nanotoxicology 8 (2014), 317–327.
35. Scaffidi, P., Misteli, T., Bianchi, M.E., Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418 (2002), 191–195.
36. Shi, C.S., Shenderov, K., Huang, N.N., Kabat, J., Abu-Asab, M., Fitzgerald, K.A., Sher, A., Kehrl, J.H., Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13 (2012), 255–263.
37. Shimizu, Y., Dobashi, K., Nagase, H., Ohta, K., Sano, T., Matsuzaki, S., Ishii, Y., Satoh, T., Koka, M., Yokoyama, A., Ohkubo, T., Ishii, Y., Kamiya, T., Co-localization of iron binding on silica with p62/sequestosome1 (SQSTM1) in lung granulomas of mice with acute silicosis. J. Clin. Biochem. Nutr. 56 (2015), 74–83.
38. Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A.M., Czaja, M.J., Autophagy regulates lipid metabolism. Nature 458 (2009), 1131–1135.
39. Tang, D., Shi, Y., Kang, R., Li, T., Xiao, W., Wang, H., Xiao, X., Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J. Leukoc. Biol. 81 (2007), 741–747.
40. Venereau, E., Casalgrandi, M., Schiraldi, M., Antoine, D.J., Cattaneo, A., De Marchis, F., Liu, J., Antonelli, A., Preti, A., Raeli, L., Shams, S.S., Yang, H., Varani, L., Andersson, U., Tracey, K.J., Bachi, A., Uguccioni, M., Bianchi, M.E., Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 209 (2012), 1519–1528.
41. Willingham, S.B., Allen, I.C., Bergstralh, D.T., Brickey, W.J., Huang, M.T., Taxman, D.J., Duncan, J.A., Ting, J.P., NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and -independent pathways. J. Immunol. 183 (2009), 2008–2015.
42. Wirawan, E., Vanden Berghe, T., Lippens, S., Agostinis, P., Vandenabeele, P., Autophagy: for better or for worse. Cell Res. 22 (2012), 43–61.
43. Zhang, Z., Shen, H.M., Zhang, Q.F., Ong, C.N., Involvement of oxidative stress in crystalline silica-induced cytotoxicity and genotoxicity in rat alveolar macrophages. Environ. Res. 82 (2000), 245–252.
44. Zhao, Z., Thackray, L.B., Miller, B.C., Lynn, T.M., Becker, M.M., Ward, E., Mizushima, N.N., Denison, M.R., Virgin, H.W.t., Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3 (2007), 581–585.