TXNIP mediates NLRP3 inflammasome activation in cardiac microvascular endothelial cells as a novel mechanism in myocardial ischemia/reperfusion injury

Arslan F, Smeets MB, O’Neill LA, Keogh B, McGuirk P, Timmers L, Tersteeg C, Hoefer IE, Doevendans PA, Pasterkamp G, de Kleijn DP (2010) Myocardial ischemia/reperfusion injury is mediated by leukocytic toll-like receptor-2 and reduced by systemic administration of a novel anti-toll-like receptor-2 antibody. Circulation 121:80–90. doi: 10.1161/CIRCULATIONAHA.109.880187

Baars T, Konorza T, Kahlert P, Mohlenkamp S, Erbel R, Heusch G, Kleinbongard P (2013) Coronary aspirate TNF alpha reflects saphenous vein bypass graft restenosis risk in diabetic patients. Cardiovasc Diabetol 12:12. doi: 10.1186/1475-2840-12-12

Calvert JW, Gundewar S, Jha S, Greer JJ, Bestermann WH, Tian R, Lefer DJ (2008) Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 57:696–705

Cook-Mills JM, Deem TL (2005) Active participation of endothelial cells in inflammation. J Leukoc Biol 77:487–495

Danese S, Dejana E, Fiocchi C (2007) Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 178:6017–6022

Danese S, Dejana E, Fiocchi C (2007) Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 178:6017–6022

Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320:674–677. doi: 10.1126/science.1156995

Gao E, Lei YH, Shang X, Huang ZM, Zuo L, Boucher M, Fan Q, Chuprun JK, Ma XL, Koch WJ (2010) A novel and efficient model of coronary artery ligation and myocardial infarction in the mouse. Circ Res 107:1445–1453. doi: 10.1161/CIRCRESAHA.110.223925

Heidemann J, Domschke W, Kucharzik T, Maaser C (2006) Intestinal microvascular endothelium and innate immunity in inflammatory bowel disease: a second line of defense? Infect Immun 74:5425–5432

Heusch G, Kleinbongard P, Skyschally A (2013) Myocardial infarction and coronary microvascular obstruction: an intimate, but complicated relationship. Basic Res Cardiol 108:380. doi: 10.1007/s00395-013-0380-y

Hoetzenecker K, Assinger A, Lichtenauer M, Mildner M, Schweiger T, Starlinger P, Jakab A, Berenyi E, Pavo N, Zimmermann M, Gabriel C, Plass C, Gyongyosi M, Volf I, Ankersmit HJ (2012) Secretome of apoptotic peripheral blood cells (APOSEC) attenuates microvascular obstruction in a porcine closed chest reperfused acute myocardial infarction model: role of platelet aggregation and vasodilation. Basic Res Cardiol 107:292. doi: 10.1007/s00395-012-0292-2

Inohara N, Nunez G (2003) NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 3:371–382

Iyer SS, Pulskens WP, Sadler JJ, Butter LM, Teske GJ, Ulland TK, Eisenbarth SC, Florquin S, Flavell RA, Leemans JC, Sutterwala FS (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 106:20388–20393. doi: 10.1073/pnas.0908698106

Jin C, Flavell RA (2010) Molecular mechanism of NLRP3 inflammasome activation. J Clin Immunol 30:628–631. doi: 10.1007/s10875-010-9440-3

Jordan JE, Zhao ZQ, Vinten-Johansen J (1999) The role of neutrophils in myocardial ischemia-reperfusion injury. Cardiovasc Res 43:860–878

Kawaguchi M, Takahashi M, Hata T, Kashima Y, Usui F, Morimoto H, Izawa A, Takahashi Y, Masumoto J, Koyama J, Hongo M, Noda T, Nakayama J, Sagara J, Taniguchi S, Ikeda U (2011) Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation 123:594–604. doi: 10.1161/CIRCULATIONAHA.110.982777

Kleinbongard P, Bose D, Baars T, Mohlenkamp S, Konorza T, Schoner S, Elter-Schulz M, Eggebrecht H, Degen H, Haude M, Levkau B, Schulz R, Erbel R, Heusch G (2011) Vasoconstrictor potential of coronary aspirate from patients undergoing stenting of saphenous vein aortocoronary bypass grafts and its pharmacological attenuation. Circ Res 108:344–352. doi: 10.1161/CIRCRESAHA.110.235713

Liu Y, Ma Y, Wang R, Xia C, Zhang R, Lian K, Luan R, Sun L, Yang L, Lau WB, Wang H, Tao L (2011) Advanced glycation end products accelerate ischemia/reperfusion injury through receptor of advanced end product/nitrative thioredoxin inactivation in cardiac microvascular endothelial cells. Antioxid Redox Signal 15:1769–1778. doi: 10.1089/ars.2010.3764

Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417–426

Menu P, Vince JE (2011) The NLRP3 inflammasome in health and disease: the good, the bad and the ugly. Clin Exp Immunol 166:1–15. doi: 10.1111/j.1365-2249.2011.04440.x

Mezzaroma E, Toldo S, Farkas D, Seropian IM, Van Tassell BW, Salloum FN, Kannan HR, Menna AC, Voelkel NF, Abbate A (2011) The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc Natl Acad Sci USA 108:19725–19730. doi: 10.1073/pnas.1108586108

Nishida M, Carley WW, Gerritsen ME, Ellingsen O, Kelly RA, Smith TW (1993) Isolation and characterization of human and rat cardiac microvascular endothelial cells. Am J Physiol 264:H639–H652

Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, Takagi Y, Sono H, Gon Y, Yodoi J (1999) Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem 274:21645–21650

Pober JS, Sessa WC (2007) Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7:803–815

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 USA 98:2871–2876

Sandanger O, Ranheim T, Vinge LE, Bliksoen M, Alfsnes K, Finsen AV, Dahl CP, Askevold ET, Florholmen G, Christensen G, Fitzgerald KA, Lien E, Valen G, Espevik T, Aukrust P, Yndestad A (2013) The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischaemia-reperfusion injury. Cardiovasc Res 99:164–174. doi: 10.1093/cvr/cvt091

Scarabelli T, Stephanou A, Rayment N, Pasini E, Comini L, Curello S, Ferrari R, Knight R, Latchman D (2001) Apoptosis of endothelial cells precedes myocyte cell apoptosis in ischemia/reperfusion injury. Circulation 104:253–256

Schroder K, Tschopp J (2010) The inflammasomes. Cell 140:821–832. doi: 10.1016/j.cell.2010.01.040

Steffens S, Montecucco F, Mach F (2009) The inflammatory response as a target to reduce myocardial ischaemia and reperfusion injury. Thromb Haemost 102:240–247. doi: 10.1160/TH08-12-0837

Stutz A, Golenbock DT, Latz E (2009) Inflammasomes: too big to miss. J Clin Invest 119:3502–3511. doi: 10.1172/JCI40599

Tao L, Gao E, Bryan NS, Qu Y, Liu HR, Hu A, Christopher TA, Lopez BL, Yodoi J, Koch WJ, Feelisch M, Ma XL (2004) Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: role of S-nitrosation [corrected]. Proc Natl Acad Sci USA 101:11471–11476

Tschopp J, Martinon F, Burns K (2003) NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 4:95–104

Wanderer AA (2008) Ischemic-reperfusion syndromes: biochemical and immunologic rationale for IL-1 targeted therapy. Clin Immunol 128:127–132. doi: 10.1016/j.clim.2008.03.514

Wen H, Ting JP, O’Neill LA (2012) A role for the NLRP3 inflammasome in metabolic diseases–did warburg miss inflammation? Nat Immunol 13:352–357. doi: 10.1038/ni.2228

Yang D, Guo S, Zhang T, Li H (2009) Hypothermia attenuates ischemia/reperfusion-induced endothelial cell apoptosis via alterations in apoptotic pathways and JNK signaling. FEBS Lett 583:2500–2506. doi: 10.1016/j.febslet.2009.07.006

Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357:1121–1135

Yin Y, Yan Y, Jiang X, Mai J, Chen NC, Wang H, Yang XF (2009) Inflammasomes are differentially expressed in cardiovascular and other tissues. Int J Immunopathol Pharmacol 22:311–322

Yoshioka J, Chutkow WA, Lee S, Kim JB, Yan J, Tian R, Lindsey ML, Feener EP, Seidman CE, Seidman JG, Lee RT (2012) Deletion of thioredoxin-interacting protein in mice impairs mitochondrial function but protects the myocardium from ischemia-reperfusion injury. J Clin Invest 122:267–279. doi: 10.1172/JCI44927

Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11:136–140. doi: 10.1038/ni.1831