Innate immunity as a target for acute cardioprotection

Cardiovascular Research

Volumn 115, Issue 7, 2019, Pages 1131-1142

  Zuurbier, Coert J ^a   Abbate, Antonio ^b   Cabrera Fuentes, Hector A ^c,d,e,f,g   Cohen, Michael V ^h   Collino, Massimo ⁱ   De Kleijn, Dominique P V ^j,k   Downey, James M ^h   Pagliaro, Pasquale ^i,l   Preissner, Klaus T ^g   Takahashi, Masafumi ^m   Davidson, Sean M ⁿ  

^a AMSTERDAM UMC   (Netherlands)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d DEPARTMENT OF CARDIOLOGY   (Singapore)

^e SCHOOL OF ENGINEERING AND SCIENCES   (Mexico)

^f KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^g JUSTUS LIEBIG UNIVERSITY   (Germany)

^h UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

ⁱ UNIVERSITY OF TURIN   (Italy)

^j UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^k INTERUNIVERSITY CARDIOLOGY INSTITUTE OF THE NETHERLANDS   (Netherlands)

^l National Institute for Cardiovascular Research   (Italy)

^m JICHI MEDICAL UNIVERSITY   (Japan)

ⁿ UNIVERSITY COLLEGE LONDON   (United Kingdom)

more..

Author keywords

Cardioprotection; Inflammasome; Innate immunity; Ischaemia; Reperfusion

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; TOLL LIKE RECEPTOR; ANTIINFLAMMATORY AGENT; CARDIOVASCULAR AGENT; CASPASE INHIBITOR; CRYOPYRIN; IMMUNOGLOBULIN RECEPTOR; NLRP3 PROTEIN, HUMAN;

CARDIAC MUSCLE; CELL DEATH; COMORBIDITY; HEART INFARCTION; HEART MUSCLE INJURY; HEART PROTECTION; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NONHUMAN; PRIORITY JOURNAL; PYROPTOSIS; REVIEW; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; ANIMAL; DRUG EFFECT; HEART FAILURE; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CARDIOVASCULAR AGENTS; CASPASE 1; CASPASE INHIBITORS; HEART FAILURE; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; MOLECULAR TARGETED THERAPY; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; ST ELEVATION MYOCARDIAL INFARCTION;

EID: 85064070761     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvy304     Document Type: Review

References (134)

1. Hausenloy DJ, Botker HE, Engstrom T, Erlinge D, Heusch G, Ibanez B, Kloner RA, Ovize M, Yellon DM, Garcia-Dorado D. Targeting reperfusion injury in patients with ST-segment elevation myocardial infarction: Trials and tribulations. Eur Heart J 2017;38:935-941.
2. Stone GW, Selker HP, Thiele H, Patel MR, Udelson JE, Ohman EM, Maehara A, Eitel I, Granger CB, Jenkins PL, Nichols M, Ben-Yehuda O. Relationship between infarct size and outcomes following primary PCI: patient-level analysis from 10 randomized trials. J Am Coll Cardiol 2016;67:1674-1683.
3. Hausenloy DJ, Garcia-Dorado D, Botker HE, Davidson SM, Downey J, Engel FB, Jennings R, Lecour S, Leor J, Madonna R, Ovize M, Perrino C, Prunier F, Schulz R, Sluijter JPG, Van Laake LW, Vinten-Johansen J, Yellon DM, Ytrehus K, Heusch G, Ferdinandy P. Novel targets and future strategies for acute cardioprotection: position paper of the European Society of Cardiology Working Group on Cellular Biology of the Heart. Cardiovasc Res 2017;113:564-585.
4. Hausenloy DJ, Barrabes JA, Botker HE, Davidson SM, Di Lisa F, Downey J, Engstrom T, Ferdinandy P, Carbrera-Fuentes HA, Heusch G, Ibanez B, Iliodromitis EK, Inserte J, Jennings R, Kalia N, Kharbanda R, Lecour S, Marber M, Miura T, Ovize M, Perez-Pinzon MA, Piper HM, Przyklenk K, Schmidt MR, Redington A, Ruiz-Meana M, Vilahur G, Vinten-Johansen J, Yellon DM, Garcia-Dorado D. Ischaemic conditioning and targeting reperfusion injury: A 30 year voyage of discovery. Basic Res Cardiol 2016;111:70.
5. Bell RM, Botker HE, Carr RD, Davidson SM, Downey JM, Dutka DP, Heusch G, Ibanez B, Macallister R, Stoppe C, Ovize M, Redington A, Walker JM, Yellon DM. 9th Hatter Biannual Meeting: position document on ischaemia/reperfusion injury, conditioning and the ten commandments of cardioprotection. Basic Res Cardiol 2016;111:41.
6. Davidson SM, Arjun S, Basalay MV, Bell RM, Bromage DI, Botker HE, Carr RD, Cunningham J, Ghosh AK, Heusch G, Ibanez B, Kleinbongard P, Lecour S, Maddock H, Ovize M, Walker M, Wiart M, Yellon DM. The 10th Biennial Hatter Cardiovascular Institute workshop: cellular protection-evaluating new directions in the setting of myocardial infarction, ischaemic stroke, and cardio-oncology. Basic Res Cardiol 2018;113:43.
7. Andreadou I, Cabrera-Fuentes HA, Devaux Y, Frangogiannis NG, Frantz S, Guzik T, Liehn EA, Gomes CPC, Schulz R, Hausenloy DJ. Immune cells as targets for cardioprotection: new players and novel therapeutic opportunities. Cardiovasc Res 2019; 115:1117-1130.
8. Toldo S, Abbate A. The NLRP3 inflammasome in acute myocardial infarction. Nat Rev Cardiol 2018;15:203-214.
9. Arslan F, de Kleijn DP, Pasterkamp G. Innate immune signaling in cardiac ischemia. Nat Rev Cardiol 2011;8:292-300.
10. Vilahur G, Badimon L. Ischemia/reperfusion activates myocardial innate immune response: The key role of the toll-like receptor. Front Physiol 2014;5:496.
11. Deftereos S, Angelidis C, Bouras G, Raisakis K, Gerckens U, Cleman MW, Giannopoulos G. Innate immune inflammatory response in the acutely ischemic myocardium. Med Clin 2014;10:653-662.
12. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:191-195.
13. Schiopu A, Cotoi OS. S100A8 and S100A9: DAMPs at the crossroads between innate immunity, traditional risk factors, and cardiovascular disease. Mediators Inflamm 2013;2013:828354.
14. Preissner KT, Herwald H. Extracellular nucleic acids in immunity and cardiovascular responses: between alert and disease. Thromb Haemost 2017;117: 1272-1282.
15. Kaczorowski DJ, Scott MJ, Pibris JP, Afrazi A, Nakao A, Edmonds RD, Kim S, Kwak JH, Liu Y, Fan J, Billiar TR. Mammalian DNA is an endogenous danger signal that stimulates local synthesis and release of complement factor B. Mol Med 2012;18: 851-860.
16. Kurashima Y, Amiya T, Nochi T, Fujisawa K, Haraguchi T, Iba H, Tsutsui H, Sato S, Nakajima S, Iijima H, Kubo M, Kunisawa J, Kiyono H. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat Commun 2012;3:1034.
17. Timmers L, Pasterkamp G, de Hoog VC, Arslan F, Appelman Y, de Kleijn DP. The innate immune response in reperfused myocardium. Cardiovasc Res 2012;94:276-283.
18. Oozawa S, Mori S, Kanke T, Takahashi H, Liu K, Tomono Y, Asanuma M, Miyazaki I, Nishibori M, Sano S. Effects of HMGB1 on ischemia-reperfusion injury in the rat heart. Circ J 2008;72:1178-1184.
19. Yang H, Biermann MH, Brauner JM, Liu Y, Zhao Y, Herrmann M. New insights into neutrophil extracellular traps: mechanisms of formation and role in inflammation. Front Immunol 2016;7:302.
20. Mangold A, Alias S, Scherz T, Hofbauer T, Jakowitsch J, Panzenbock A, Simon D, Laimer D, Bangert C, Kammerlander A, Mascherbauer J, Winter MP, Distelmaier K, Adlbrecht C, Preissner KT, Lang IM. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ Res 2015;116:1182-1192.
21. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP, Lohmeyer J, Preissner KT. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: A predominant role of histones. PLoS One 2012;7:e32366.
22. Lee SM, Hutchinson M, Saint DA. The role of Toll-like receptor 4 (TLR4) in cardiac ischaemic-reperfusion injury, cardioprotection and preconditioning. Clin Exp Pharmacol Physiol 2016;43:864-871.
23. von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012;209:819-835.
24. Cabrera-Fuentes HA, Ruiz-Meana M, Simsekyilmaz S, Kostin S, Inserte J, Saffarzadeh M, Galuska SP, Vijayan V, Barba I, Barreto G, Fischer S, Lochnit G, Ilinskaya ON, Baumgart-Vogt E, Bö ning A, Lecour S, Hausenloy DJ, Liehn EA, Garcia-Dorado D, Schlüter K-D, Preissner KT. RNase1 prevents the damaging interplay between extracellular RNA and tumour necrosis factor-Alpha in cardiac ischaemia/reperfusion injury. Thromb Haemost 2014;112:1110-1119.
25. Yan X, Anzai A, Katsumata Y, Matsuhashi T, Ito K, Endo J, Yamamoto T, Takeshima A, Shinmura K, Shen W, Fukuda K, Sano M. Temporal dynamics of cardiac immune cell accumulation following acute myocardial infarction. J Mol Cell Cardiol 2013;62: 24-35.
26. Pinto AR, Paolicelli R, Salimova E, Gospocic J, Slonimsky E, Bilbao-Cortes D, Godwin JW, Rosenthal NA. An abundant tissue macrophage population in the adult murine heart with a distinct alternatively-Activated macrophage profile. PLoS One 2012;7:e36814.
27. Bajpai G, Schneider C, Wong N, Bredemeyer A, Hulsmans M, Nahrendorf M, Epelman S, Kreisel D, Liu Y, Itoh A, Shankar TS, Selzman CH, Drakos SG, Lavine KJ. The human heart contains distinct macrophage subsets with divergent origins and functions. Nat Med 2018;24:1234-1245.
28. Bonner F, Borg N, Burghoff S, Schrader J. Resident cardiac immune cells and expression of the ectonucleotidase enzymes CD39 and CD73 after ischemic injury. PLoS One 2012;7:e34730.
29. Yu YR, O?Koren EG, Hotten DF, Kan MJ, Kopin D, Nelson ER, Que L, Gunn MD. A protocol for the comprehensive flow cytometric analysis of immune cells in normal and inflamed murine non-lymphoid tissues. PLoS One 2016;11:e0150606.
30. Janicki JS, Brower GL, Levick SP. The emerging prominence of the cardiac mast cell as a potent mediator of adverse myocardial remodeling. Methods Mol Biol 2015; 1220:121-139.
31. Macri SC, Bailey CC, de Oca NM, Silva NA, Rosene DL, Mansfield KG, Miller AD. Immunophenotypic alterations in resident immune cells and myocardial fibrosis in the aging rhesus macaque (Macaca mulatta) heart. Toxicol Pathol 2012;40:637-646.
32. Frangogiannis NG, Lindsey ML, Michael LH, Youker KA, Bressler RB, Mendoza LH, Spengler RN, Smith CW, Entman ML. Resident cardiac mast cells degranulate and release preformed TNF-Alpha, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation 1998;98:699-710.
33. Bhattacharya K, Farwell K, Huang M, Kempuraj D, Donelan J, Papaliodis D, Vasiadi M, Theoharides TC. Mast cell deficient W/Wv mice have lower serum IL-6 and less cardiac tissue necrosis than their normal littermates following myocardial ischemiareperfusion. Int J Immunopathol Pharmacol 2007;20:69-74.
34. Yang MQ, Ma YY, Ding J, Li JY. The role of mast cells in ischemia and reperfusion injury. Inflamm Res 2014;63:899-905.
35. Hooshdaran B, Kolpakov MA, Guo X, Miller SA, Wang T, Tilley DG, Rafiq K, Sabri A. Dual inhibition of cathepsin G and chymase reduces myocyte death and improves cardiac remodeling after myocardial ischemia reperfusion injury. Basic Res Cardiol 2017;112:62.
36. Rork TH, Wallace KL, Kennedy DP, Marshall MA, Lankford AR, Linden J. Adenosine A2A receptor activation reduces infarct size in the isolated, perfused mouse heart by inhibiting resident cardiac mast cell degranulation. Am J Physiol Heart Circ Physiol 2008;295:H1825-H1833.
37. Levick SP, Melendez GC, Plante E, McLarty JL, Brower GL, Janicki JS. Cardiac mast cells: The centrepiece in adverse myocardial remodelling. Cardiovasc Res 2011;89: 12-19.
38. Reil JC, Gilles S, Zahler S, Brandl A, Drexler H, Hultner L, Matrisian LM, Welsch U, Becker BF. Insights from knock-out models concerning postischemic release of TNFalpha from isolated mouse hearts. J Mol Cell Cardiol 2007;42:133-141.
39. Wang P, Downey JM, Cohen MV. Mast cell degranulation does not contribute to ischemic preconditioning in isolated rabbit hearts. Basic Res Cardiol 1996;91: 458-467.
40. Parikh V, Singh M. Cardiac mast cell stabilization and cardioprotective effect of ischemic preconditioning in isolated rat heart. J Cardiovasc Pharmacol 1998;31: 779-785.
41. Navarro R, Compte M, Alvarez-Vallina L, Sanz L. Immune regulation by pericytes: modulating innate and adaptive immunity. Front Immunol 2016;7:480.
42. Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gartner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and ?instruct? them with pattern-recognition and motility programs. Nat Immunol 2013;14:41-51.
43. O?Farrell FM, Mastitskaya S, Hammond-Haley M, Freitas F, Wah WR, Attwell D. Capillary pericytes mediate coronary no-reflow after myocardial ischaemia. Elife 2017;6. pii: e29280.
44. Matzinger P. The danger model: A renewed sense of self. Science 2002;296:301-305.
45. Seong SY, Matzinger P. Hydrophobicity: An ancient damage-Associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004;4:469-478.
46. Schett G, Metzler B, Kleindienst R, Amberger A, Recheis H, Xu Q, Wick G. Myocardial injury leads to a release of heat shock protein (hsp) 60 and a suppression of the anti-hsp65 immune response. Cardiovasc Res 1999;42:685-695.
47. Kim SC, Stice JP, Chen L, Jung JS, Gupta S, Wang Y, Baumgarten G, Trial J, Knowlton AA. Extracellular heat shock protein 60, cardiac myocytes, and apoptosis. Circ Res 2009;105:1186-1195.
48. Xie L, Liu S, Cheng J, Wang L, Liu J, Gong J. Exogenous administration of mitochondrial DNA promotes ischemia reperfusion injury via TLR9-p38 MAPK pathway. Regul Toxicol Pharmacol 2017;89:148-154.
49. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012;485:251-255.
50. Goldstein RS, Gallowitsch-Puerta M, Yang L, Rosas-Ballina M, Huston JM, Czura CJ, Lee DC, Ward MF, Bruchfeld AN, Wang H, Lesser ML, Church AL, Litroff AH, Sama AE, Tracey KJ. Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock 2006;25:571-574.
51. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004;279:7370-7377.
52. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ. Tolllike receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007;8:487-496.
53. Andrassy M, Volz HC, Igwe JC, Funke B, Eichberger SN, Kaya Z, Buss S, Autschbach F, Pleger ST, Lukic IK, Bea F, Hardt SE, Humpert PM, Bianchi ME, Mairbaurl H, Nawroth PP, Remppis A, Katus HA, Bierhaus A. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 2008;117:3216-3226.
54. He SJ, Cheng J, Feng X, Yu Y, Tian L, Huang Q. The dual role and therapeutic potential of high-mobility group box 1 in cancer. Oncotarget 2017;8:64534-64550.
55. Dobaczewski M, Bujak M, Zymek P, Ren G, Entman ML, Frangogiannis NG. Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res 2006;324:475-488.
56. Gariboldi S, Palazzo M, Zanobbio L, Selleri S, Sommariva M, Sfondrini L, Cavicchini S, Balsari A, Rumio C. Low molecular weight hyaluronic acid increases the selfdefense of skin epithelium by induction of beta-defensin 2 via TLR2 and TLR4. J Immunol 2008;181:2103-2110.
57. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, Homer RJ, Goldstein DR, Bucala R, Lee PJ, Medzhitov R, Noble PW. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-1179.
58. Schoneveld AH, Hoefer I, Sluijter JP, Laman JD, de Kleijn DP, Pasterkamp G. Atherosclerotic lesion development and Toll like receptor 2 and 4 responsiveness. Atherosclerosis 2008;197:95-104.
59. Arslan F, Smeets MB, Riem Vis PW, Karper JC, Quax PH, Bongartz LG, Peters JH, Hoefer IE, Doevendans PA, Pasterkamp G, de Kleijn DP. Lack of fibronectin-EDA promotes survival and prevents adverse remodeling and heart function deterioration after myocardial infarction. Circ Res 2011;108:582-592.
60. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, Lee RT, Kelly RA. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest 1999;104:271-280.
61. Connolly DJ, O?Neill LA. New developments in Toll-like receptor targeted therapeutics. Curr Opin Pharmacol 2012;12:510-518.
62. Arslan F, Houtgraaf JH, Keogh B, Kazemi K, de Jong R, McCormack WJ, O?Neill LA, McGuirk P, Timmers L, Smeets MB, Akeroyd L, Reilly M, Pasterkamp G, de Kleijn DP. Treatment with OPN-305, a humanized anti-Toll-Like receptor-2 antibody, reduces myocardial ischemia/reperfusion injury in pigs. Circ Cardiovasc Interv 2012;5: 279-287.
63. Arslan F, Smeets MB, O?Neill LA, Keogh B, McGuirk P, Timmers L, Tersteeg C, Hoefer IE, Doevendans PA, Pasterkamp G, de Kleijn DP. 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 2010;121:80-90.
64. Dong JW, Vallejo JG, Tzeng HP, Thomas JA, Mann DL. Innate immunity mediates myocardial preconditioning through Toll-like receptor 2 and TIRAP-dependent signaling pathways. Am J Physiol Heart Circ Physiol 2010;298:H1079-H1087.
65. Lu C, Ren D, Wang X, Ha T, Liu L, Lee EJ, Hu J, Kalbfleisch J, Gao X, Kao R, Williams D, Li C. Toll-like receptor 3 plays a role in myocardial infarction and ischemia/reperfusion injury. Biochim Biophys Acta 2014;1842:22-31.
66. Ding HS, Yang J, Chen P, Yang J, Bo SQ, Ding JW, Yu QQ. The HMGB1-TLR4 axis contributes to myocardial ischemia/reperfusion injury via regulation of cardiomyocyte apoptosis. Gene 2013;527:389-393.
67. Oyama J, Blais C Jr, Liu X, Pu M, Kobzik L, Kelly RA, Bourcier T. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 2004;109:784-789.
68. Shimamoto A, Chong AJ, Yada M, Shomura S, Takayama H, Fleisig AJ, Agnew ML, Hampton CR, Rothnie CL, Spring DJ, Pohlman TH, Shimpo H, Verrier ED. Inhibition of Toll-like receptor 4 with eritoran attenuates myocardial ischemiareperfusion injury. Circulation 2006;114:I270-I274.
69. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP, Roose-Girma M, Erickson S, Dixit VM. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004;430:213-218.
70. Martinon F, Burns K, Tschopp J. The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002;10: 417-426.
71. Vande Walle L, Lamkanfi M. Pyroptosis. Curr Biol 2016;26:R568-R572.
72. Mezzaroma E, Toldo S, Farkas D, Seropian IM, Van Tassell BW, Salloum FN, Kannan HR, Menna AC, Voelkel NF, Abbate A. The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc Natl Acad Sci USA 2011;108:19725-19730.
73. Yang XM, Downey JM, Cohen MV, Housley NA, Alvarez DF, Audia JP. The highly selective caspase-1 inhibitor VX-765 provides additive protection against myocardial infarction in rat hearts when combined with a platelet inhibitor. J Cardiovasc Pharmacol Ther 2017;22:574-578.
74. Do Carmo H, Arjun S, Petrucci O, Yellon DM, Davidson SM. The caspase 1 inhibitor VX-765 protects the isolated rat heart via the RISK pathway. Cardiovasc Drugs Ther 2018;32:165-168.
75. 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. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation 2011;123:594-604.
76. Zuurbier CJ, Jong WM, Eerbeek O, Koeman A, Pulskens WP, Butter LM, Leemans JC, Hollmann MW. Deletion of the innate immune NLRP3 receptor abolishes cardiac ischemic preconditioning and is associated with decreased IL-6/STAT3 signaling. PLoS One 2012;7:e40643.
77. 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. The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischaemia-reperfusion injury. Cardiovasc Res 2013;99:164-174.
78. Liu Y, Lian K, Zhang L, Wang R, Yi F, Gao C, Xin C, Zhu D, Li Y, Yan W, Xiong L, Gao E, Wang H, Tao L. TXNIP mediates NLRP3 inflammasome activation in cardiac microvascular endothelial cells as a novel mechanism in myocardial ischemia/reperfusion injury. Basic Res Cardiol 2014;109:415.
79. Mastrocola R, Penna C, Tullio F, Femmino S, Nigro D, Chiazza F, Serpe L, Collotta D, Alloatti G, Cocco M, Bertinaria M, Pagliaro P, Aragno M, Collino M. Pharmacological inhibition of NLRP3 inflammasome attenuates myocardial ischemia/reperfusion injury by activation of RISK and mitochondrial pathways. Oxid Med Cell Longev 2016;2016:5271251.
80. Jong WM, Leemans JC, Weber NC, Juffermans NP, Schultz MJ, Hollmann MW, Zuurbier CJ. Nlrp3 plays no role in acute cardiac infarction due to low cardiac expression. Int J Cardiol 2014;177:41-43.
81. Marchetti C, Chojnacki J, Toldo S, Mezzaroma E, Tranchida N, Rose SW, Federici M, Van Tassell BW, Zhang S, Abbate A. A novel pharmacologic inhibitor of the NLRP3 inflammasome limits myocardial injury after ischemia-reperfusion in the mouse. J Cardiovasc Pharmacol 2014;63:316-322.
82. Toldo S, Marchetti C, Mauro AG, Chojnacki J, Mezzaroma E, Carbone S, Zhang S, Van Tassell B, Salloum FN, Abbate A. Inhibition of the NLRP3 inflammasome limits the inflammatory injury following myocardial ischemia-reperfusion in the mouse. Int J Cardiol 2016;209:215-220.
83. van Hout GP, Bosch L, Ellenbroek GH, de Haan JJ, van Solinge WW, Cooper MA, Arslan F, de Jager SC, Robertson AA, Pasterkamp G, Hoefer IE. The selective NLRP3-inflammasome inhibitor MCC950 reduces infarct size and preserves cardiac function in a pig model of myocardial infarction. Eur Heart J 2017;38: 828-836.
84. Sandanger O, Gao E, Ranheim T, Bliksoen M, Kaasboll OJ, Alfsnes K, Nymo SH, Rashidi A, Ohm IK, Attramadal H, Aukrust P, Vinge LE, Yndestad A. NLRP3 inflammasome activation during myocardial ischemia reperfusion is cardioprotective. Biochem Biophys Res Commun 2016;469:1012-1020.
85. Stokman G, Kors L, Bakker PJ, Rampanelli E, Claessen N, Teske GJD, Butter L, van Andel H, van den Bergh Weerman MA, Larsen PWB, Dessing MC, Zuurbier CJ, Girardin SE, Florquin S, Leemans JC. NLRX1 dampens oxidative stress and apoptosis in tissue injury via control of mitochondrial activity. J Exp Med 2017;214: 2405-2420.
86. Mangan MSJ, Olhava EJ, Roush WR, Seidel HM, Glick GD, Latz E. Targeting the NLRP3 inflammasome in inflammatory diseases. Nat Rev Drug Discov 2018;17: 588-606.
87. Zuurbier CJ, Demirci C, Koeman A, Vink H, Ince C. Short-Term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. J Appl Physiol (1985) 2005;99:1471-1476.
88. Makhdoumi P, Roohbakhsh A, Karimi G. MicroRNAs regulate mitochondrial apoptotic pathway in myocardial ischemia-reperfusion-injury. Biomed Pharmacother 2016;84:1635-1644.
89. Nederlof R, Eerbeek O, Hollmann MW, Southworth R, Zuurbier CJ. Targeting hexokinase II to mitochondria to modulate energy metabolism and reduce ischaemia-reperfusion injury in heart. Br J Pharmacol 2014;171:2067-2079.
90. Zhang Y, Rong H, Zhang FX, Wu K, Mu L, Meng J, Xiao B, Zamponi GW, Shi Y. A membrane potential-And calpain-dependent reversal of caspase-1 inhibition regulates canonical NLRP3 inflammasome. Cell Rep 2018;24:2356-2369.e2355.
91. Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J. Inflammasome-Activated gasdermin D causes pyroptosis by forming membrane pores. Nature 2016; 535:153-158.
92. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015;526:660-665.
93. Barry R, John SW, Liccardi G, Tenev T, Jaco I, Chen CH, Choi J, Kasperkiewicz P, Fernandes-Alnemri T, Alnemri E, Drag M, Chen Y, Meier P. SUMO-mediated regulation of NLRP3 modulates inflammasome activity. Nat Commun 2018;9:3001.
94. Juliana C, Fernandes-Alnemri T, Wu J, Datta P, Solorzano L, Yu JW, Meng R, Quong AA, Latz E, Scott CP, Alnemri ES. Anti-inflammatory compounds parthenolide and Bay 11-7082 are direct inhibitors of the inflammasome. J Biol Chem 2010;285: 9792-9802.
95. Kim YS, Kim JS, Kwon JS, Jeong MH, Cho JG, Park JC, Kang JC, Ahn Y. BAY 11-7082, a nuclear factor-jB inhibitor, reduces inflammation and apoptosis in a rat cardiac ischemia-reperfusion injury model. Int Heart J 2010;51:348-353.
96. Cocco M, Miglio G, Giorgis M, Garella D, Marini E, Costale A, Regazzoni L, Vistoli G, Orioli M, Massulaha-Ahmed R, Detraz-Durieux I, Groslambert M, Py BF, Bertinaria M. Design, synthesis, and evaluation of acrylamide derivatives as direct NLRP3 inflammasome inhibitors. ChemMedChem 2016;11:1790-1803.
97. Marchetti C, Swartzwelter B, Gamboni F, Neff CP, Richter K, Azam T, Carta S, Tengesdal I, Nemkov T, D?Alessandro A, Henry C, Jones GS, Goodrich SA, St. Laurent JP, Jones TM, Scribner CL, Barrow RB, Altman RD, Skouras DB, Gattorno M, Grau V, Janciauskiene S, Rubartelli A, Joosten LAB, Dinarello CA. OLT1177, a beta-sulfonyl nitrile compound, safe in humans, inhibits the NLRP3 inflammasome and reverses the metabolic cost of inflammation. Proc Natl Acad Sci USA 2018;115:E1530-E1539.
98. Toldo S, Mauro AG, Marchetti C, Mezzaroma E, van Tassell B, Skouras D, La Neve F, Dinarello C, Abbate A. Novel NLRP3 inflammasome inhibitor OLT1177 reduces infarct size in a mouse model of myocardial ischemia reperfusion injury. Circulation 2018;136: A18066.
99. Sheedy FJ, Grebe A, Rayner KJ, Kalantari P, Ramkhelawon B, Carpenter SB, Becker CE, Ediriweera HN, Mullick AE, Golenbock DT, Stuart LM, Latz E, Fitzgerald KA, Moore KJ. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol 2013;14:812-820.
100. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010;464:1357-1361.
101. Niemi K, Teirila L, Lappalainen J, Rajamaki K, Baumann MH, Oorni K, Wolff H, Kovanen PT, Matikainen S, Eklund KK. Serum amyloid A activates the NLRP3 inflammasome via P2X7 receptor and a cathepsin B-sensitive pathway. J Immunol 2011;186:6119-6128.
102. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. Fatty acidinduced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011;12:408-415.
103. Kang R, Chen R, Xie M, Cao L, Lotze MT, Tang D, Zeh HJ. The receptor for advanced glycation end products activates the AIM2 inflammasome in acute pancreatitis. J Immunol 2016;196:4331-4337.
104. Cannito S, Morello E, Bocca C, Foglia B, Benetti E, Novo E, Chiazza F, Rogazzo M, Fantozzi R, Povero D, Sutti S, Bugianesi E, Feldstein AE, Albano E, Collino M, Parola M. Microvesicles released from fat-laden cells promote activation of hepatocellular NLRP3 inflammasome: A pro-inflammatory link between lipotoxicity and nonalcoholic steatohepatitis. PLoS One 2017;12:e0172575.
105. Mastrocola R, Aragno M, Alloatti G, Collino M, Penna C, Pagliaro P. Metaflammation: Tissue-specific alterations of the NLRP3 inflammasome platform in metabolic syndrome. CMC 2018;25:1294-1310.
106. Benetti E, Chiazza F, Patel NS, Collino M. The NLRP3 inflammasome as a novel player of the intercellular crosstalk in metabolic disorders. Mediators Inflamm 2013; 2013:678627.
107. Bando S, Fukuda D, Soeki T, Nishimoto S, Uematsu E, Matsuura T, Ise T, Tobiume T, Yamaguchi K, Yagi S, Iwase T, Yamada H, Wakatsuki T, Shimabukuro M, Sata M. Expression of NLRP3 in subcutaneous adipose tissue is associated with coronary atherosclerosis. Atherosclerosis 2015;242:407-414.
108. Mastrocola R, Collino M, Penna C, Nigro D, Chiazza F, Fracasso V, Tullio F, Alloatti G, Pagliaro P, Aragno M. Maladaptive modulations of NLRP3 inflammasome and cardioprotective pathways are involved in diet-induced exacerbation of myocardial ischemia/reperfusion injury in mice. Oxid Med Cell Longev 2016;2016:3480637.
109. Hong P, Li FX, Gu RN, Fang YY, Lai LY, Wang YW, Tao T, Xu SY, You ZJ, Zhang HF. Inhibition of NLRP3 inflammasome ameliorates cerebral ischemia-reperfusion injury in diabetic mice. Neural Plast 2018;2018:1.
110. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, Rentsendorj A, Vargas M, Guerrero C, Wang Y, Fitzgerald KA, Underhill DM, Town T, Arditi M. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012;36:401-414.
111. Yang XM, Cui L, White J, Kuck J, Ruchko MV, Wilson GL, Alexeyev M, Gillespie MN, Downey JM, Cohen MV. Mitochondrially targeted Endonuclease III has a powerful anti-infarct effect in an in vivo rat model of myocardial ischemia/reperfusion. Basic Res Cardiol 2015;110:3.
112. Zhao Y, Shao F. The NAIP-NLRC4 inflammasome in innate immune detection of bacterial flagellin and type III secretion apparatus. Immunol Rev 2015;265:85-102.
113. Shao W, Yeretssian G, Doiron K, Hussain SN, Saleh M. The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J Biol Chem 2007;282:36321-36329.
114. Pomerantz BJ, Reznikov LL, Harken AH, Dinarello CA. Inhibition of caspase 1 reduces human myocardial ischemic dysfunction via inhibition of IL-18 and IL-1b. Proc Natl Acad Sci USA 2001;98:2871-2876.
115. Audia JP, Yang X-M, Crockett ES, Housley N, Ul Haq E, O?Donnell K, Cohen MV, Downey JM, Alvarez DF. Caspase-1 inhibition by VX-765 administered at reperfusion in P2Y12 receptor antagonist-Treated rats provides long-Term reduction in myocardial infarct size and preservation of ventricular function. Basic Res Cardiol 2018;113:32.
116. Vilahur G, Gutierrez M, Casani L, Varela L, Capdevila A, Pons-Llado G, Carreras F, Carlsson L, Hidalgo A, Badimon L. Protective effects of ticagrelor on myocardial injury after infarction. Circulation 2016;134:1708-1719.
117. Ye Y, Birnbaum GD, Perez-Polo JR, Nanhwan MK, Nylander S, Birnbaum Y. Ticagrelor protects the heart against reperfusion injury and improves remodeling after myocardial infarction. Arterioscler Thromb Vasc Biol 2015;35:1805-1814.
118. Yang XM, Cui L, Alhammouri A, Downey JM, Cohen MV. Triple therapy greatly increases myocardial salvage during ischemia/reperfusion in the in situ rat heart. Cardiovasc Drugs Ther 2013;27:403-412.
119. Davidson SM, Andreadou I, Barile L, Birnbaum Y, Cabrera-Fuentes HA, Cohen MV, Downey JM, Girao H, Pagliaro P, Penna C, Pernow J, Preissner KT, Ferdinandy P. Circulating blood cells and extracellular vesicles in acute cardioprotection. Cardiovasc Res 2019;115:1156-1166.
120. Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R. Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 2014;66:1142-1174.
121. Lecour S, Bøtker HE, Condorelli G, Davidson SM, Garcia-Dorado D, Engel FB, Ferdinandy P, Heusch G, Madonna R, Ovize M, Ruiz-Meana M, Schulz R, Sluijter JP, Van Laake LW, Yellon DM, Hausenloy DJ. ESC working group cellular biology of the heart: position paper: improving the preclinical assessment of novel cardioprotective therapies. Cardiovasc Res 2014;104:399-411.
122. Mishra PK, Ying W, Nandi SS, Bandyopadhyay GK, Patel KK, Mahata SK. Diabetic cardiomyopathy: An immunometabolic perspective. Front Endocrinol (Lausanne) 2017;8:72.
123. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O?Neill LA, Xavier RJ. Trained immunity: A program of innate immune memory in health and disease. Science 2016;352:aaf1098.
124. van der Meer JW, Joosten LA, Riksen N, Netea MG. Trained immunity: A smart way to enhance innate immune defence. Mol Immunol 2015;68:40-44.
125. Li C, Ha T, Kelley J, Gao X, Qiu Y, Kao RL, Browder W, Williams DL. Modulating Toll-like receptor mediated signaling by (1->3)-beta-D-glucan rapidly induces cardioprotection. Cardiovasc Res 2004;61:538-547.
126. Qian J, Liu AJ, Zhang W, Wen ZP, Lin LL, Wang JH, Su DF, Liu JG. Protective effects of betaglucin on myocardial tissue during myocardial infarction in rats and dogs. Acta Pharmacol Sin 2009;30:1092-1098.
127. Irwin MR, Cole SW. Reciprocal regulation of the neural and innate immune systems. Nat Rev Immunol 2011;11:625-632.
128. Garcia-Prieto J, Villena-Gutierrez R, Gomez M, Bernardo E, Pun-Garcia A, Garcia-Lunar I, Crainiciuc G, Fernandez-Jimenez R, Sreeramkumar V, Bourio-Martinez R, Garcia-Ruiz JM, Del Valle AS, Sanz-Rosa D, Pizarro G, Fernandez-Ortiz A, Hidalgo A, Fuster V, Ibanez B. Neutrophil stunning by metoprolol reduces infarct size. Nat Commun 2017;8:14780.
129. Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med 2013;368:1575-1584.
130. Jackel S, Kiouptsi K, Lillich M, Hendrikx T, Khandagale A, Kollar B, Hormann N, Reiss C, Subramaniam S, Wilms E, Ebner K, Bruhl MV, Rausch P, Baines JF, Haberichter S, Lammle B, Binder CJ, Jurk K, Ruggeri ZM, Massberg S, Walter U, Ruf W, Reinhardt C. Gut microbiota regulate hepatic von Willebrand factor synthesis and arterial thrombus formation via Toll-like receptor-2. Blood 2017;130:542-553.
131. Haghikia A, Li XS, Liman TG, Bledau N, Schmidt D, Zimmermann F, Krankel N, Widera C, Sonnenschein K, Haghikia A, Weissenborn K, Fraccarollo D, Heimesaat MM, Bauersachs J, Wang Z, Zhu W, Bavendiek U, Hazen SL, Endres M, Landmesser U. Gut microbiota-dependent trimethylamine n-oxide predicts risk of cardiovascular events in patients with stroke and is related to proinflammatory monocytes. Arterioscler Thromb Vasc Biol 2018;38:2225-2235.
132. Zhou X, Li J, Guo J, Geng B, Ji W, Zhao Q, Li J, Liu X, Liu J, Guo Z, Cai W, Ma Y, Ren D, Miao J, Chen S, Zhang Z, Chen J, Zhong J, Liu W, Zou M, Li Y, Cai J. Gut-dependent microbial translocation induces inflammation and cardiovascular events after ST-elevation myocardial infarction. Microbiome 2018;6:66.
133. Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C, Fonseca F, Nicolau J, Koenig W, Anker SD, Kastelein JJP, Cornel JH, Pais P, Pella D, Genest J, Cifkova R, Lorenzatti A, Forster T, Kobalava Z, Vida-Simiti L, Flather M, Shimokawa H, Ogawa H, Dellborg M, Rossi PRF, Troquay RPT, Libby P, Glynn RJ; CANTOS Trial Group. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med 2017;377:1119-1131.
134. Panahi M, Papanikolaou A, Torabi A, Zhang JG, Khan H, Vazir A, Hasham MG, Cleland JGF, Rosenthal NA, Harding SE, Sattler S. Immunomodulatory interventions in myocardial infarction and heart failure: A systematic review of clinical trials and meta-Analysis of IL-1 inhibition. Cardiovasc Res 2018;114:1445-1461.