Independent roles of the priming and the triggering of the NLRP3 inflammasome in the heart

Cardiovascular Research

Volumn 105, Issue 2, 2015, Pages 203-212

  Toldo, Stefano ^a   Mezzaroma, Eleonora ^a   McGeough, Matthew D ^b   Pena, Carla A ^b   Marchetti, Carlo ^a   Sonnino, Chiara ^a   Van Tassell, Benjamin W ^a   Salloum, Fadi N ^a   Voelkel, Norbert F ^a   Hoffman, Hal M ^b   Abbate, Antonio ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cardiomyopathy; Caspase 1; Cryopyrinopathy; Inflammasome; NLRP3; Priming

Indexed keywords

ALANINE; CRE RECOMBINASE; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; TAMOXIFEN; VALINE; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HEART; HEART FUNCTION; HEART LEFT VENTRICLE; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; LEFT VENTRICULAR SYSTOLIC DYSFUNCTION; LOW DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPLEEN; WESTERN BLOTTING; WILD TYPE; ANIMAL; CARDIOMYOPATHIES; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CARDIOMYOPATHIES; CARRIER PROTEINS; CASPASE 1; DISEASE MODELS, ANIMAL; INFLAMMASOMES; LIPOPOLYSACCHARIDES; MICE, TRANSGENIC;

EID: 84922461226     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu259     Document Type: Article

References (43)

1. Braunwald E. Heart failure. JACC Heart Fail 2013;1:1-20.
2. Mann DL. Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ Res 2002;91:988-998.
3. Satoh M, Minami Y, Takahashi Y, Nakamura M. Immune modulation: role of the inflammatory cytokine cascade in the failing human heart. Curr Heart Fail Rep 2008;5:69-74.
4. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011;117:3720-3732.
5. Van Tassell BW, Seropian IM, Toldo S, Mezzaroma E, Abbate A. Interleukin-1b induces a reversible cardiomyopathy in the mouse. Inflamm Res 2013;62:637-640.
6. Toldo S, Mezzaroma E, O'Brien L, Marchetti C, Seropian IM, Voelkel NF, Van Tassell BW, Dinarello CA, Abbate A. Interleukin-18 mediates interleukin-1-induced cardiac dysfunction. Am J Physiol Heart Circ Physiol 2014;306:H1025-H1031.
7. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 2013;13:397-411.
8. Mezzaroma E, Toldo S, Farkas D, Seropian IM, Van Tassell BW, Salloum FN, Kannan HR, Menna AC, Voelkel NF, Abbate A. The inflammasomepromotesadversecardiacremod-eling following acute myocardial infarctionin the mouse. Proc Natl Acad Sci USA 2011;108: 19725-19730.
9. 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.
10. Sandanger Ø, Ranheim T, Vinge LE, Bliksøen 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.
11. Merkle S, Frantz S, Schön MP, Bauersachs J, Buitrago M, Frost RJ, Schmitteckert EM, Lohse MJ, Engelhardt S. A role for caspase-1 in heart failure. Circ Res 2007;100:645-653.
12. Bracey NA, Beck PL, Muruve DA, Hirota SA, Guo J, Jabagi H, Wright JR Jr, Macdonald JA, Lees-Miller JP, Roach D, Semeniuk LM, Duff HJ. The Nlrp3 inflammasome promotes myocardial dysfunction in structural cardiomyopathy through interleukin-1b. Exp Physiol 2013;98:462-472.
13. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 2009;183: 787-791.
14. Hoffman HM, Brydges SD. Genetic and molecular basis of inflammasome-mediated disease. J Biol Chem 2011;286:10889-10896.
15. Dinarello CA, van der Meer JW. Treating inflammation by blocking interleukin-1 in humans. Semin Immunol 2013;25:469-484.
16. Brydges SD, Mueller JL, McGeough MD, Pena CA, Misaghi A, Gandhi C, Putnam CD, Boyle DL, Firestein GS, Horner AA, Soroosh P, Watford WT, O'Shea JJ, Kastner DL, Hoffman HM. Inflammasome-mediated disease animal models reveal roles for innate but not adaptive immunity. Immunity 2009;30:875-887.
17. Bonar SL, Brydges SD, Mueller JL, McGeough MD, Pena C, Chen D, Grimston SK, Hickman-Brecks CL, Ravindran S, McAlinden A, Novack DV, Kastner DL, Civitelli R, Hoffman HM, Mbalaviele G. Constitutively activated NLRP3 inflammasome causes inflammation and abnormal skeletal development in mice. PLoS ONE 2012;7:e35979.
18. McGeough MD, Pena CA, Mueller JL, Pociask DA, Broderick L, Hoffman HM, Brydges SD. Cutting edge: IL-6 is a marker of inflammation with no direct role in inflammasome-mediated mouse models. J Immunol 2012;189:2707-2711.
19. Seropian IM, Abbate A, Toldo S, Harrington J, Smithson L, Ockaili R, Mezzaroma E, Damilano F, Hirsch E, Van Tassell BW. Pharmacologic inhibition of phosphoinositide 3-kinase gamma (PI3Kg) promotes infarct resorption and prevents adverse cardiac remodeling after myocardial infarction in mice. J Cardiovasc Pharmacol 2010;56:651-658.
20. Lech M, Avila-Ferrufino A, Skuginna V, Susanti EH, Anders HJ. Quantitative expression of RIG-like helicase, NOD-like receptor and inflammasome-related mRNAsin humans and mice. Int Immunol 2010;22:717-728.
21. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, van der Meer JH, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I, Funk CJ, Mason RJ, Kullberg BJ, Rubartelli A, van der Meer JW, Dinarello CA. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macro-phages. Blood 2009;113:2324-2335.
22. Yin Y, Yan Y, Jiang X, Mai J, Chen NC, Wang H, Yang XF. Inflammasomes are differentially expressed in cardiovascular and other tissues. Int J Immunopathol Pharmacol 2009;22: 311-322.
23. Davis BK, Wen H, Ting JP. The inflammasome NLRs inimmunity, inflammation, and associated diseases. Annu Rev Immunol 2011;29:707-735.
24. Takahashi M. NLRP3 Inflammasome asaNovel Player inMyocardial Infarction. Int Heart J 2014;55:101-105.
25. Mitchell JA, Paul-Clark MJ, Clarke GW, McMaster SK, Cartwright N. Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J Endocrinol 2007;193:323-330.
26. Van Tassell BW, Seropian IM, Toldo S, Salloum FN, Smithson L, Varma A, Hoke NN, Gelwix C, Chau V, Abbate A. Pharmacologic inhibition of myeloid differentiation factor 88 (MyD88) prevents left ventricular dilation and hypertrophy after experimental acute myocardial infarction in the mouse. J Cardiovasc Pharmacol 2010;55:385-390.
27. Hoffman HM, Wanderer AA. Inflammasome and IL-1beta-mediated disorders. Curr Allergy Asthma Rep 2010;10:229-235.
28. Fallach R, Shainberg A, Avlas O, Fainblut M, Chepurko Y, Porat E, Hochhauser E. Cardi-omyocyte Toll-like receptor 4 is involved in heart dysfunction following septic shock or myocardial ischemia. J Mol Cell Cardiol 2010;48:1236-1244.
29. Toldo S, Mezzaroma E, Mauro AG, Salloum FN, Van Tassell BW, Abbate AS. The inflam-masome in myocardial injury and cardiac remodeling. Antioxid Redox Signal 2014. [Epub ahead of print].
30. ver Elst KM, Spapen HD, Nguyen DN, Garbar C, Huyghens LP, Gorus FK. Cardiac troponins I and T are biological markers of left ventricular dysfunction in septic shock. Clin Chem 2000; 46: 650-657.
31. 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 ische-mic preconditioning and is associated with decreased Il-6/STAT3 signaling. PLoS ONE 2012;7:e40643.
32. Brydges SD, Broderick L, McGeough MD, Pena CA, Mueller JL, Hoffman HM. Divergence of IL-1, IL-18, and cell death in NLRP3 inflammasomopathies. J Clin Invest 2013;123: 4695-4705.
33. Van Tassell BW, Arena RA, Toldo S, Mezzaroma E, Azam T, Seropian IM, Shah K, Canada J, Voelkel NF, Dinarello CA, Abbate A. Enhanced interleukin-1 activity contributes to exercise intolerance in patients with systolic heart failure. PLoS ONE 2012;7: e33438.
34. 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.
35. Shishido T, Nozaki N, Yamaguchi S, Shibata Y, Nitobe J, Miyamoto T, Takahashi H, Arimoto T, Maeda K, Yamakawa M, Takeuchi O, Akira S, Takeishi Y, Kubota I. Toll-like receptor-2 modulates ventricular remodeling after myocardial infarction. Circulation 2003;108:2905-2910.
36. Riad A, Jäger S, Sobirey M, Escher F, Yaulema-Riss A, Westermann D, Karatas A, Heimesaat MM, Bereswill S, Dragun D, Pauschinger M, Schultheiss HP, Tschöpe C. Toll-like receptor-4 modulates survival by induction of left ventricular remodeling after myocardial infarction in mice. J Immunol 2008;180:6954-6961.
37. Chong AJ, Shimamoto A, Hampton CR, Takayama H, Spring DJ, Rothnie CL, Yada M, Pohlman TH, Verrier ED. Toll-like receptor 4 mediates ischemia/reperfusion injury of the heart. J Thorac Cardiovasc Surg 2004;128:170-179.
38. Feng Y, Zou L, Si R, Nagasaka Y, Chao W. Bone marrow MyD88 signalingmodulates neu-trophil function and ischemic myocardial injury. Am J Physiol Cell Physiol 2010;299: C760-C769.
39. Sauter KA, Wood LJ, Wong J, Iordanov M, Magun BE. Doxorubicin and daunorubicin induce processing and releaseof interleukin-1b through activation of the NLRP3 inflam-masome. Cancer Biol Ther 2011;11:1008-1016.
40. Nozaki N, Shishido T, Takeishi Y, Kubota I. Modulation of doxorubicin-induced cardiac dysfunction in toll-like receptor-2-knockout mice. Circulation 2004;110:2869-2874.
41. Krysko DV, Kaczmarek A, Krysko O, Heyndrickx L, Woznicki J, Bogaert P, Cauwels A, Takahashi N, Magez S, Bachert C, Vandenabeele P. TLR-2 and TLR-9 are sensorsofapop-tosis in a mouse model of doxorubicin-induced acute inflammation. Cell Death Differ 2011;18:1316-1325.
42. 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 inflam-masome limits myocardial injury after ischemia-reperfusion in the mouse. J Cardiovasc Pharmacol 2014;63:316-322.
43. Van Tassell BW, Toldo S, Mezzaroma E, Abbate A. Targeting interleukin-1 in heart disease. Circulation 2013;128:1910-1923.