NLRP3 inflammasome mediates albumin-induced renal tubular injury through impaired mitochondrial function

Journal of Biological Chemistry

Volumn 289, Issue 36, 2014, Pages 25101-25111

  Zhuang, Yibo ^a   Ding, Guixia ^a   Zhao, Min ^a   Bai, Mi ^a   Yang, Lingyun ^a   Ni, Jiajia ^a   Wang, Rong ^a   Jia, Zhanjun ^a   Huang, Songming ^a   Zhang, Aihua ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; MANGANESE;

CELL APOPTOSIS; CHRONIC KIDNEY DISEASE; EPITHELIAL CELLS; GENETIC DISRUPTION; MITOCHONDRIAL FUNCTION; PHENOTYPIC CHANGES; POTENTIAL TARGETS; SIGNALING PATHWAYS;

MITOCHONDRIA;

ALBUMIN; CRYOPYRIN; CYCLOSPORIN A; INTERLEUKIN 1BETA CONVERTING ENZYME; PORPHYRIN DERIVATIVE; TETRAKIS (4 BENZOIC ACID) PORPHYRIN; UNCLASSIFIED DRUG; BOVINE SERUM ALBUMIN; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; CYCLOSPORIN; IMMUNOSUPPRESSIVE AGENT; INFLAMMASOME; MANGANESE(III)-TETRAKIS(4-BENZOIC ACID)PORPHYRIN; METALLOPORPHYRIN;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; GENE DISRUPTION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY TUBULE CELL; KIDNEY TUBULE DAMAGE; MALE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN FUNCTION; PROTEINURIA; SIGNAL TRANSDUCTION; UPREGULATION; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; GENETICS; KIDNEY; KIDNEY PROXIMAL TUBULE; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; RNA INTERFERENCE; TOXICITY; WESTERN BLOTTING;

ADOLESCENT; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 1; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; CYCLOSPORINE; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMASOMES; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; METALLOPORPHYRINS; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; PROTEINURIA; RNA INTERFERENCE; SERUM ALBUMIN, BOVINE;

EID: 84906965435     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578260     Document Type: Article

References (39)

1. Burton, C., and Harris, K. P. (1996) The role of proteinuria in the progression of chronic renal failure. Am. J. Kidney Dis. 27, 765-775
2. Eddy, A. A. (2004) Proteinuria and interstitial injury. Nephrol. Dial Transplant. 19, 277-281
3. Zoja, C., Morigi, M., and Remuzzi, G. (2003) Proteinuria and phenotypic change of proximal tubular cells. J. Am. Soc. Nephrol. 14, S36-S41
4. Li, X., Pabla, N., Wei, Q., Dong, G., Messing, R. O., Wang, C. Y., and Dong, Z. (2010) PKC-δ promotes renal tubular cell apoptosis associated with proteinuria. J. Am. Soc. Nephrol. 21, 1115-1124
5. Niaudet, P., and Rötig, A. (1996) Renal involvement in mitochondrial cytopathies. Pediatr. Nephrol. 10, 368-373
6. Izzedine, H., Launay-Vacher, V., and Deray, G. (2005) Antiviral drug-induced nephrotoxicity. Am. J. Kidney Dis. 45, 804-817
7. Shanley, P. F., Rosen, M. D., Brezis, M., Silva, P., Epstein, F. H., and Rosen, S. (1986) Topography of focal proximal tubular necrosis after ischemia with reflow in the rat kidney. Am. J. Pathol. 122, 462-468
8. Kepp, O., Galluzzi, L., and Kroemer, G. (2011) Mitochondrial control of the NLRP3 inflammasome. Nat. Immunol. 12, 199-200
9. Erkan, E., Devarajan, P., and Schwartz, G. J. (2007) Mitochondria are the major targets in albumin-induced apoptosis in proximal tubule cells. J. Am. Soc. Nephrol. 18, 1199-1208
10. Tschopp, J., and Schroder, K. (2010) NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10, 210-215
11. Martinon, F., Burns, K., and Tschopp, J. (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-β. Mol. Cell 10, 417-426
12. Vilaysane, A., Chun, J., Seamone, M. E., Wang, W., Chin, R., Hirota, S., Li, Y., Clark, S. A., Tschopp, J., Trpkov, K., Hemmelgarn, B. R., Beck, P. L., and Muruve, D. A. (2010) The NLRP3 inflammasome promotes renal inflammation and contributes to CKD. J. Am. Soc. Nephrol. 21, 1732-1744
13. Bakker, P. J., Butter, L. M., Kors, L., Teske, G. J., Aten, J., Sutterwala, F. S., Florquin, S., and Leemans, J. C. (2014) Nlrp3 is a key modulator of diet-induced nephropathy and renal cholesterol accumulation. Kidney Int. 85, 1112-1122
14. Zhao, J., Wang, H., Dai, C., Zhang, H., Huang, Y., Wang, S., Gaskin, F., Yang, N., and Fu, S. M. (2013) P2X7 blockade attenuates murine lupus nephritis by inhibiting activation of the NLRP3/ASC/caspase 1 pathway. Arthritis Rheum. 65, 3176-3185
15. Green, D. R., Galluzzi, L., and Kroemer, G. (2011) Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333, 1109-1112
16. Dashdorj, A., Jyothi, K. R., Lim, S., Jo, A., Nguyen, M. N., Ha, J., Yoon, K. S., Kim, H. J., Park, J. H., Murphy, M. P., and Kim, S. S. (2013) Mitochondria-targeted antioxidant MitoQ ameliorates experimental mouse colitis by suppressing NLRP3 inflammasome-mediated inflammatory cytokines. BMC Med. 11, 178
17. Eddy, A. A., Kim, H., López-Guisa, J., Oda, T., and Soloway, P. D. (2000) Interstitial fibrosis in mice with overload proteinuria: deficiency of TIMP-1 is not protective. Kidney Int. 58, 618-628
18. Thomas, M. E., Harris, K. P., Walls, J., Furness, P. N., and Brunskill, N. J. (2002) Fatty acids exacerbate tubulointerstitial injury in protein-overload proteinuria. Am. J. Physiol. Renal Physiol. 283, F640-F647
19. Huang, S., Zhang, A., Ding, G., and Chen, R. (2009) Aldosterone-induced mesangial cell proliferation is mediated by EGF receptor transactivation. Am. J. Physiol. Renal Physiol. 296, F1323-F1333
20. Acton, B. M., Jurisicova, A., Jurisica, I., and Casper, R. F. (2004) Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol. Hum. Reprod. 10, 23-32
21. Wen, H., Ting, J. P., and O'Neill, L. A. (2012) A role for the NLRP3 inflammasome in metabolic diseases: did Warburg miss inflammation? Nat. Immunol. 13, 352-357
22. Strowig, T., Henao-Mejia, J., Elinav, E., and Flavell, R. (2012) Inflammasomes in health and disease. Nature 481, 278-286
23. Lichtnekert, J., Kulkarni, O. P., Mulay, S. R., Rupanagudi, K. V., Ryu, M., Allam, R., Vielhauer, V., Muruve, D., Lindenmeyer, M. T., Cohen, C. D., and Anders, H. J. (2011) Anti-GBM glomerulonephritis involves IL-1 but is independent of NLRP3/ASC inflammasome-mediated activation of caspase-1. PLoS One 6, e26778
24. Fang, L., Xie, D., Wu, X., Cao, H., Su, W., and Yang, J. (2013) Involvement of endoplasmic reticulum stress in albuminuria induced inflammasome activation in renal proximal tubular cells. PLoS One 8, e72344
25. Oosting, M., Buffen, K., Malireddi, S. R., Sturm, P., Verschueren, I., Koenders, M. I., van de Veerdonk, F. L., van der Meer, J. W., Netea, M. G., Kanneganti, T. D., and Joosten, L. A. (2012) Murine Borrelia arthritis is highly dependent on ASC and caspase-1, but independent of NLRP3. Arthritis Res. Ther. 14, R247
26. Cassel, S. L., Janczy, J. R., Bing, X., Wilson, S. P., Olivier, A. K., Otero, J. E., Iwakura, Y., Shayakhmetov, D. M., Bassuk, A. G., Abu-Amer, Y., Brogden, K. A., Burns, T. L., Sutterwala, F. S., and Ferguson, P. J. (2014) Inflammasome-independent IL-1β mediates autoinflammatory disease in Pstpip2-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 111, 1072-1077
27. Kim, H. J., Lee, D. W., Ravichandran, K.,OKeys, D., Akcay, A., Nguyen, Q., He, Z., Jani, A., Ljubanovic, D., and Edelstein, C. L. (2013) NLRP3 inflammasome knockout mice are protected against ischemic but not cisplatin-induced acute kidney injury. J. Pharmacol. Exp. Ther. 346, 465-472
28. Shigeoka, A. A., Mueller, J. L., Kambo, A., Mathison, J. C., King, A. J., Hall, W. F., Correia Jda, S., Ulevitch, R. J., Hoffman, H. M., and McKay, D. B. (2010) An inflammasome-independent role for epithelial-expressed Nlrp3 in renal ischemia-reperfusion injury. J. Immunol. 185, 6277-6285
29. Wang, C., Pan, Y., Zhang, Q. Y., Wang, F. M., and Kong, L. D. (2012) Quercetin and allopurinol ameliorate kidney injury in STZ-treated rats with regulation of renal NLRP3 inflammasome activation and lipid accumulation. PLoS One 7, e38285
30. Chen, K., Zhang, J., Zhang, W., Yang, J., Li, K., and He, Y. (2013) ATP-P2X4 signaling mediates NLRP3 inflammasome activation: a novel pathway of diabetic nephropathy. Int. J. Biochem. Cell Biol. 45, 932-943
31. Cassel, S. L., Joly, S., and Sutterwala, F. S. (2009) The NLRP3 inflammasome: a sensor of immune danger signals. Semin. Immunol. 21, 194-198
32. Kim, J. J., and Jo, E. K. (2013) NLRP3 inflammasome and host protection against bacterial infection. J. Korean Med. Sci. 28, 1415-1423
33. Pétrilli, V., Papin, S., Dostert, C., Mayor, A., Martinon, F., and Tschopp, J. (2007) Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14, 1583-1589
34. Marina-García, N., Franchi, L., Kim, Y. G., Miller, D., McDonald, C., Boons, G. J., and Núñez, G. (2008) Pannexin-1-mediated intracellular delivery of muramyl dipeptide induces caspase-1 activation via cryopyrin/NLRP3 independently of Nod2. J. Immunol. 180, 4050-4057
35. Zhou, R., Tardivel, A., Thorens, B., Choi, I., and Tschopp, J. (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136-140
36. Zhou, R., Yazdi, A. S., Menu, P., and Tschopp, J. (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225
37. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H., Rock, K. L., Fitzgerald, K. A., and Latz, E. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856
38. Dostert, C., Guarda, G., Romero, J. F., Menu, P., Gross, O., Tardivel, A., Suva, M. L., Stehle, J. C., Kopf, M., Stamenkovic, I., Corradin, G., and Tschopp, J. (2009) Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS One 4, e6510
39. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., and Golenbock, D. T. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 9, 857-865