Cathepsin B contributes to autophagy-related 7 (Atg7)-induced nod-like receptor 3 (NLRP3)-dependent proinflammatory response and aggravates lipotoxicity in rat insulinoma cell line

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30094-30104

  Li, Shali ^a   Du, Leilei ^a   Zhang, Lu ^a   Hu, Yue ^a   Xia, Wenchun ^a   Wu, Jia ^a   Zhu, Jing ^a   Chen, Lingling ^a   Zhu, Fengqi ^a   Li, Chunxian ^a   Yang, Sijun ^a  

^a NANJING NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; CATHEPSIN B; INFLAMMASOME; INSULINOMA CELLS; NOD-LIKE RECEPTORS; PRO-INFLAMMATORY CYTOKINES; PROINFLAMMATORY RESPONSE; RELEASE MECHANISM;

BIOCHEMISTRY; BIOLOGY;

CELL CULTURE;

AUTOPHAGY PROTEIN 7; CATHEPSIN B; CELL PROTEIN; CRYOPYRIN; FATTY ACID; GLUCOSE; INFLAMMASOME; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; INFLAMMATION; INSULIN RELEASE; INSULINOMA CELL LINE; LIPOTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; RNA INTERFERENCE; TUMOR CELL LINE;

AUTOPHAGY; CYTOKINE; GLUCOSE METABOLISM; INFLAMMATION; INSULIN RESISTANCE; PANCREATIC ISLETS;

ANIMALS; CATHEPSIN B; CELL LINE, TUMOR; CYTOKINES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; INFLAMMASOMES; INFLAMMATION; INSULINOMA; NEOPLASM PROTEINS; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84886919052     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.494286     Document Type: Article

References (40)

1. Shao, S., Liu, Z., Yang, Y., Zhang, M., and Yu, X. (2010) SREBP-1c, Pdx-1, and GLP-1R involved in palmitate-EPA regulated glucose-stimulated insulin secretion in INS-1 cells. J. Cell. Biochem. 111, 634-642
2. Gregor, M. F., and Hotamisligil, G. S. (2011) Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29, 415-445
3. Donath, M. Y., and Shoelson, S. E. (2011) Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 11, 98-107
4. Festa, A., D'Agostino, R., Jr., Tracy, R. P., and Haffner, S. M. (2002) Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 51, 1131-1137
5. Osborn, O., Brownell, S. E., Sanchez-Alavez, M., Salomon, D., Gram, H., and Bartfai, T. (2008) Treatment with an Interleukin 1 antibody improves glycemic control in diet-induced obesity. Cytokine 44, 141-148
6. Larsen, C. M., Faulenbach, M., Vaag, A., Ehses, J. A., Donath, M. Y., and Mandrup-Poulsen, T. (2009) Sustained effects of interleukin-1 receptor antagonist treatment in type 2 diabetes. Diabetes Care 32, 1663-1668
7. Komatsu, M. (2012) Liver autophagy: physiology and pathology. J. Biochem. 152, 5-15
8. Dupont, N., Jiang, S., Pilli, M., Ornatowski, W., Bhattacharya, D., and Deretic, V. (2011) Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J. 30, 4701-4711
9. Ebato, C., Uchida, T., Arakawa, M., Komatsu, M., Ueno, T., Komiya, K., Azuma, K., Hirose, T., Tanaka, K., Kominami, E., Kawamori, R., Fujitani, Y., and Watada, H. (2008) Autophagy is important in islet homeostasis and compensatory increase of β cell mass in response to high-fat diet. Cell Metab. 8, 325-332
10. Lai, E., Bikopoulos, G., Wheeler, M. B., Rozakis-Adcock, M., and Volchuk, A. (2008) Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic β-cells. Am. J. Physiol. Endocrinol. Metab. 294, E540-E550
11. Liang, H., Zhong, Y., Zhou, S., and Li, Q. Q. (2011) Palmitic acid-induced apoptosis in pancreatic β-cells is increased by liver X receptor agonist and attenuated by eicosapentaenoate. In Vivo 25, 711-718
12. Saitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B. G., Satoh, T., Omori, H., Noda, T., Yamamoto, N., Komatsu, M., Tanaka, K., Kawai, T., Tsujimura, T., Takeuchi, O., Yoshimori, T., and Akira, S. (2008) Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature 456, 264-268
13. Meng, Q., and Cai, D. (2011) Defective hypothalamic autophagy directs the central pathogenesis of obesity via the IkB kinase β (IKKβ)/NF-kB pathway. J. Biol. Chem. 286, 32324-32332
14. Nakahira, K., Haspel, J. A., Rathinam, V. A., Lee, S. J., Dolinay, T., Lam, H. C., Englert, J. A., Rabinovitch, M., Cernadas, M., Kim, H. P., Fitzgerald, K. A., Ryter, S. W., and Choi, A. M. (2011) Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12, 222-230
15. Levine, B., and Yuan, J. (2005) Autophagy in cell death: an innocent convict? J. Clin. Investig. 115, 2679-2688
16. Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., and Levine, B. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939
17. Wang, X., Blagden, C., Fan, J., Nowak, S. J., Taniuchi, I., Littman, D. R., and Burden, S. J. (2005) Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev. 19, 1715-1722
18. Matsui, Y., Takagi, H., Qu, X., Abdellatif, M., Sakoda, H., Asano, T., Levine, B., and Sadoshima, J. (2007) Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 100, 914-922
19. Martino, L., Masini, M., Novelli, M., Beffy, P., Bugliani, M., Marselli, L., Masiello, P., Marchetti, P., and De Tata, V. (2012) Palmitate activates autophagy in INS-1E β-cells and in isolated rat and human pancreatic islets. PLoS One 7, e36188
20. Cao, L. Z., Tang, D. Q., Horb, M. E., Li, S. W., and Yang, L. J. (2004) High glucose is necessary for complete maturation of Pdx1-VP16-expressing hepatic cells into functional insulin-producing cells. Diabetes 53, 3168-3178
21. Choi, S. E., Lee, S. M., Lee, Y. J., Li, L. J., Lee, S. J., Lee, J. H., Kim, Y., Jun, H. S., Lee, K. W., and Kang, Y. (2009) Protective role of autophagy in palmitate-induced INS-1 β-cell death. Endocrinology 150, 126-134
22. Tan, S. H., Shui, G., Zhou, J., Li, J. J., Bay, B. H., Wenk, M. R., and Shen, H. M. (2012) Induction of autophagy by palmitic acid via protein kinase C-mediated signaling pathway independent of mTOR (mammalian target of rapamycin). J. Biol. Chem. 287, 14364-14376
23. Shimabukuro, M., Zhou, Y. T., Levi, M., and Unger, R. H. (1998) Fatty acid-induced β cell apoptosis: a link between obesity and diabetes. Proc. Natl. Acad. Sci. U.S.A. 95, 2498-2502
24. Karaskov, E., Scott, C., Zhang, L., Teodoro, T., Ravazzola, M., and Volchuk, A. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic β-cell apoptosis. Endocrinology 147, 3398-3407
25. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
26. Khan, M. J., Rizwan Alam, M., Waldeck-Weiermair, M., Karsten, F., Groschner, L., Riederer, M., Hallstrom, S., Rockenfeller, P., Konya, V., Heinemann, A., Madeo, F., Graier, W. F., and Malli, R. (2012) Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells. J. Biol. Chem. 287, 21110-21120
27. Masters, S. L., Dunne, A., Subramanian, S. L., Hull, R. L., Tannahill, G. M., Sharp, F. A., Becker, C., Franchi, L., Yoshihara, E., Chen, Z., Mullooly, N., Mielke, L. A., Harris, J., Coll, R. C., Mills, K. H., Mok, K. H., Newsholme, P., Nunez, G., Yodoi, J., Kahn, S. E., Lavelle, E. C., and O'Neill, L. A. (2010) Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat. Immunol. 11, 897-904
28. Song, M. K., Roufogalis, B. D., and Huang, T. H. (2012) Reversal of the caspase-dependent apoptotic cytotoxicity pathway by taurine from Lycium barbarum (goji berry) in human retinal pigment epithelial cells: potential benefit in diabetic retinopathy. Evid. Based Complement. Alternat. Med. 2012, 323784
29. Martino, L., Masini, M., Novelli, M., Beffy, P., Bugliani, M., Marselli, L., Masiello, P., Marchetti, P., and De Tata, V. (2012) Palmitate activates autophagy in INS-1E -cells and in isolated rat and human pancreatic islets. PLoS One 7, e36188
30. Lightfoot, Y. L., Chen, J., and Mathews, C. E. (2011) Role of the mitochondria in immune-mediated apoptotic death of the human pancreatic β cell line βLox5. PLoS One 6, e20617
31. Caglič, D., Globisch, A., Kindermann, M., Lim, N. H., Jeske, V., Juretschke, H. P., Bartnik, E., Weithmann, K. U., Nagase, H., Turk, B., and Wendt, K. U. (2011) Functional in vivo imaging of cysteine cathepsin activity in murine model of inflammation. Bioorg. Med. Chem. 19, 1055-1061
32. Sun, L., Wu, Z., Hayashi, Y., Peters, C., Tsuda, M., Inoue, K., and Nakanishi, H. (2012) Microglial cathepsin B contributes to the initiation of peripheral inflammation-induced chronic pain. J. Neurosci. 32, 11330-11342
33. Zhou, R., Yazdi, A. S., Menu, P., and Tschopp, J. (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225
34. Deretic, V. (2009) Multiple regulatory and effector roles of autophagy in immunity. Curr. Opin. Immunol. 21, 53-62
35. Rajamaki, K., Lappalainen, J., Oorni, K., Valimaki, E., Matikainen, S., Kovanen, P. T., and Eklund, K. K. (2010) Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One 5, e11765
36. Bauernfeind, F. G., Horvath, G., Stutz, A., Alnemri, E. S., MacDonald, K., Speert, D., Fernandes-Alnemri, T., Wu, J., Monks, B. G., Fitzgerald, K. A., Hornung, V., and Latz, E. (2009) Cutting edge: NF-B activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183, 787-791
37. Wen, H., Gris, D., Lei, Y., Jha, S., Zhang, L., Huang, M. T., Brickey, W. J., and Ting, J. P. (2011) Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12, 408-415
38. Niemi, K., Teirila, L., Lappalainen, J., Rajamaki, K., Baumann, M. H., Oorni, K., Wolff, H., Kovanen, P. T., Matikainen, S., and Eklund, K. K. (2011) Serum amyloid A activates the NLRP3 inflammasome via P2X7 receptor and a cathepsin B-sensitive pathway. J. Immunol. 186, 6119-6128
39. Orlichenko, L., Stolz, D. B., Noel, P., Behari, J., Liu, S., and Singh, V. P. (2012) ADP-ribosylation factor 1 protein regulates trypsinogen activation via organellar trafficking of procathepsin B protein and autophagic maturation in acute pancreatitis. J. Biol. Chem. 287, 24284-24293
40. Kolattukudy, P. E., and Niu, J. (2012) Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/ CCR2 pathway. Circ. Res. 110, 174-189