Deletion of the innate immune NLRP3 receptor abolishes cardiac ischemic preconditioning and is associated with decreased IL-6/STAT3 signaling

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Zuurbier, Coert J ^a   Jong, Willeke M C ^a   Eerbeek, Otto ^b   Koeman, Anneke ^a   Pulskens, Wilco P ^b   Butter, Loes M ^b   Leemans, Jaklien C ^b   Hollmann, Markus W ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTER APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN CONTAINING A C TERMINAL CARD; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; MULTIPROTEIN COMPLEX; NEUTRALIZING ANTIBODY; PHOSPHOTRANSFERASE; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DOWN REGULATION; ENZYME ANALYSIS; HEART INFARCTION PREVENTION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PERFORMANCE; HEART PERFUSION; HEART PROTECTION; INNATE IMMUNITY; ISOLATED HEART; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; CARRIER PROTEINS; GENE DELETION; IMMUNITY, INNATE; INFLAMMASOMES; INTERLEUKIN-1BETA; INTERLEUKIN-6; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MICE; MICE, KNOCKOUT; MYOCARDIUM; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

MUS;

EID: 84864403686     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040643     Document Type: Article

References (41)

1. Kono H, Rock KL, (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8: 279-289.
2. Mariathasan S, (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
3. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J, (2006) Gout-associated uric acid crystals activate the NLRP3 inflammasome. Nature 440: 237-241.
4. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, et al. (2007) Activation of the NLRP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Diff 14: 1583-1589.
5. Zhou R, Yazdi AS, Menu P, Tschopp J, (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225.
6. Murphy E, Steenbergen C, (2008) Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88: 581-609.
7. Eltzschig HK, Carmeliet P, (2011) Hypoxia and inflammation. New Engl J Med 364: 656-665.
8. Eckle T, Kohler D, Lehmann R, El Kasmi KC, Eltzschig HK, (2008) Hypoxia-inducible factor-1 is central to cardioprotection: A new paradigm for ischemic preconditioning. Circulation 118: 166-175.
9. Franchi L, Warner N, Viani K, Nunez G, (2009) Function of Nod-like receptors in microbial recognition and host defense. Immunolog Rev 227: 106-128.
10. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, et al. (2004) NLRP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20: 319-325.
11. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, et al. (2009) Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 15: 1170-1178.
12. Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, et al. (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 106: 20388-20393.
13. Yellon DM, Hausenloy DJ, (2007) Myocardial reperfusion injury. N Engl J Med 357: 1121-1135.
14. Pomerantz BJ, reznikov LL, Harken AH, Dinarello CA, (2001) Inhibition of caspase 1 reduces human myocardial ischemic dysfunction via inhibition of IL-18 and IL-1beta. Proc Natl Acad Sci 98: 2871-2876.
15. Dawn B, Xuan YT, Guo Y, Rezazadeh A, Stein AB, et al. (2004) IL-6 plays an obligatory role in late preconditioning via JAK-STAT signaling and upregulation of iNOS and COX-2. Cardiovasc Res 64: 61-71.
16. Smith RM, Suleman N, McCarthy J, Sack MN, (2002) Classic ischemic but not pharmacologic preconditioning is abrogated following genetic ablation of the TNFalpha gene. Cardiovasc Res 55: 553-560.
17. Weber A, Wasiliew P, Kracht M, (2010) Interleukin-1 (IL-1) pathway. Sci Signal 105: cm1.
18. Shigeoka AA, Mueller JL, Kambo A, Mathison JC, King AJ, et al. (2010) An inflammasome-independent role for epithelial-expressed Nlrp3 in renal ischemia-reperfusion injury. J Immunol 185: 6277-6285.
19. Ellebedy AH, Lupfer C, Ghoneim HE, Debeauchap J, Kannegantie TD, et al. (2011) Inflammasome-independent role of the apoptosis-associated speck-like protein containing CARD (ASC) in the adjuvant effect of MF59. Proc Natl Acad Sci USA 108: 2927-2972.
20. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, et al. (2006) Critical role for NLRP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
21. Gürel E, Smeele KM, Eerbeek O, Koeman A, Demirci C, et al. (2009) Ischemic preconditioning affects hexokinase activity and HKII in different subcellular compartments throughout cardiac ischemia-reperfusion. J Appl Physiol 106: 1909-1916.
22. Smeele KM, Southworth R, Wu R, Xie R, Nederlof R, et al. (2011) Disruption of mitochondrial hexokinase II- mitochondrial binding blocks ischemic preconditioning and causes rapid cardiac necrosis. Circ Res 108: 1165-1169.
23. Bergmeyer HU, (1970) Methoden der Enzymatischen analyse. Weinheim:Verlag Chemie.
24. Peart J, Headrick JP, (2003) Adenosine-mediated early preconditioning in mouse: protective signaling and concentration dependent effects. Cardiovasc Res 58: 589-601.
25. Kanno S, Lee PC, Zhang Y, Ho C, Griffith BP, et al. (2000) Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation 101: 2742-2748.
26. Izuishi K, Tsung A, Jeyabalan G, Critchlow ND, Li J, et al. (2006) Cutting edge: high-mobility group box 1 preconditioning protects against liver ischemia-reperfusion injury. J Immunol 176: 7154-7158.
27. Chao W, (2009) Toll-like receptor signaling: a critical modulator of cell survival and ischemic injury in the heart. Am J Physiol Heart Circ Physiol 296: H1-H12.
28. Dong JW, Vallejo JG, Tzeng HP, Thomas JA, Mann DL, (2010) Innate immunity mediates myocardial preconditioning through Toll-like receptor 2 and TIRAP-dependent signaling pathways. Am J Physiol Heart Circ Physiol 298: H1079-H1087.
29. Netea MG, Kullberg BJ, Verschueren I, Van der Meer JWM, (2000) Interleukin-18 induces production of proinflammatory cytokines in mice: no intermediate role for the cytokines of the tumor necrosis factor family and interleukin-1β. Eur J Immunol 30: 3057-3060.
30. Teoh N, Field J, Farrell G, (2006) Interleukin-6 is a key mediator of the hepatoprotective and pro-proliferative effects of ischaemic preconditioning in mice. J Hepatol 45: 20-27.
31. Belosjorow S, Schulz R, Dörge H, Ulrich Schade F, Heusch G, (1999) Endotoxin and ischemic preconditioning: TNF-α concentration and myocardial infarct development in rabbits. Am J Physiol Heart Circ Physiol 277: H2470-H2475.
32. Oba T, Yasukawa H, Futamata N, Mawatari K, Nagata T, et al. (2010) Activation of protective signaling pathways in heart by skeletal muscle-derived cytokines during remote ischemic preconditioning. Circulation 122: A13918.
33. Wenwu Z, Debing Z, Renwei C, Jian L, Guangxian Y, et al. (2010) Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants. Pediatr Cardiol 31: 22-29.
34. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, et al. (2007) Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370: 575-579.
35. Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, et al. (2010) Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Bas Res Cardiol 105: 657-664.
36. Hirano T, (2010) Interleukin-6 in autoimmune and inflammatory diseases: a personal memoir. Proc Jpn Acad Ser B 86: 717-730.
37. Xuan YT, Guo Y, Han H, Zhu Y, Bolli R, (2001) An essential role of the JAK-STAT pathway in ischemic preconditioning. Proc Natl Acad Sci USA 98: 9050-9055.
38. Hattori R, Maulik N, Otani H, Zhu L, Cordis G, et al. (2001) Role of STAT3 in ischemic preconditioning. J Mol Cell Cardiol 33: 1929-1936.
39. Aggarwal BB, Vijayalekshmi RV, Sung B, (2009) Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res 15: 425-430.
40. Yu H, Pardoll D, Jove R, (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9: 798-809.
41. Kawaguchi M, Masafumi T, Hata T, Kashima Y, Usui F, et al. (2011) Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation 123: 594-604.