Interleukin-18 as a therapeutic target in acute myocardial infarction and heart failure

Molecular Medicine

Volumn 20, Issue 1, 2014, Pages 221-229

  O'Brien, Laura C ^a   Mezzaroma, Eleonora ^a   Van Tassell, Benjamin W ^a   Marchetti, Carlo ^a   Carbone, Salvatore ^a   Abbate, Antonio ^a   Toldo, Stefano ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ADRENERGIC RECEPTOR; INTERLEUKIN 18;

ACUTE HEART INFARCTION; APOPTOSIS; ARTICLE; DOWN REGULATION; EXTRACELLULAR MATRIX; HEART FAILURE; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; HUMAN; IN VIVO STUDY; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; HEART CONTRACTION; HEART DISEASE; METABOLISM;

ANIMALS; APOPTOSIS; HEART DISEASES; HUMANS; INTERLEUKIN-18; MYOCARDIAL CONTRACTION; RECEPTORS, ADRENERGIC, BETA;

EID: 84902280933     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2014.00034     Document Type: Article

References (102)

1. Van Tassell BW, et al. (2012) Enhanced interleukin-1 activity contributes to exercise intolerance in patients with systolic heart failure. PloS One. 7:e33438.
2. Go AS, et al. (2013) Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation. 127:e6-e245.
3. Seropian IM, Toldo S, Van Tassell BW, Abbate A. (2014) Anti-inflammatory strategies for ventricular remodeling following ST-segment elevation acute myocardial infarction. J. Amer. Coll. Cardiol. 63:1593-603.
4. Gullestad L, et al. (2012) Inflammatory cytokines in heart failure: mediators and markers. Cardiology. 122:23-35.
5. Kalogeropoulos AP, Georgiopoulou VV, Butler J. (2012) From risk factors to structural heart disease: the role of inflammation. Heart Fail. Clin. 8:113-23.
6. Dinarello CA, Pomerantz BJ. (2001) Proinflammatory cytokines in heart disease. Blood Purif. 19:314-21.
7. Mann DL. (2002) Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ. Res. 91:988-98.
8. Prabhu SD. (2004) Cytokine-induced modulation of cardiac function. Circ. Res. 95:1140-53.
9. Nakamura K, Okamura H, Wada M, Nagata K, Tamura T. (1989) Endotoxin-induced serum factor that stimulates gamma interferon production. Infec. Immun. 57:590-5.
10. Munder M, Mallo M, Eichmann K, Modolell M. (1998) Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J. Exp. Med. 187:2103-8.
11. Okamura H, et al. (1995) Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature. 378:88-91.
12. Ahn HJ, et al. (1997) A mechanism underlying synergy between IL-12 and IFN-gamma-inducing factor in enhanced production of IFN-gamma. J. Immunol. 159:2125-2131.
13. Bazan JF, Timans JC, Kastelein RA. (1996) A newly defined interleukin-1? Nature. 379:591.
14. Artlett CM. (2012) The role of the NLRP3 inflammasome in fibrosis. Open Rheumatol. J. 6:80-6.
15. Mezzaroma E, et al. (2011) The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc. Nat. Acad. Sci. U. S. A. 108:19725-30.
16. Gu Y. (1997) Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science. 275:206-9.
17. Ghayur T, et al. (1997) Caspase-1 processes IFNgamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature. 386:619-23.
18. Puren AJ, Fantuzzi G, Dinarello CA. (1999) Gene expression, synthesis, and secretion of interleukin 18 and interleukin 1beta are differentially regulated in human blood mononuclear cells and mouse spleen cells. Proc. Nat. Acad. Sci. U. S. A. 96:2256-61.
19. Lamkanfi M, Dixit VM. (2012) Inflammasomes and their roles in health and disease. Annu. Rev. Cell. Dev. Biol. 28:137-61.
20. Toldo S, et al. (2013) Interleukin-1beta immunoneutralization improves cardiac remodeling after myocardial infarction without interrupting the inflammasome in the mouse. Exp. Physiol. 98:734-45.
21. Kawaguchi M, et al. (2011) Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation. 123:594-604.
22. Takahashi M. (2014) NLRP3 Inflammasome as a novel player in myocardial infarction. Int. Heart J. 55:101-5.
23. Saxena A, et al. (2013) IL-1 induces proinflammatory leukocyte infiltration and regulates fibroblast phenotype in the infarcted myocardium. J. Immunol. 191:4838-48.
24. Sugawara S, et al. (2001) Neutrophil proteinase 3-mediated induction of bioactive IL-18 secretion by human oral epithelial cells. J. Immunol. 167:6568-75.
25. Joosten LA, et al. (2009) Inflammatory arthritis in caspase 1 gene-deficient mice: contribution of proteinase 3 to caspase 1-independent production of bioactive interleukin-1beta. Arthritis Rheum. 60:3651-62.
26. Omoto Y, et al. (2006) Human mast cell chymase cleaves pro-IL-18 and generates a novel and biologically active IL-18 fragment. J. Immunol. 177:8315-9.
27. Omoto Y, et al. (2010) Granzyme B is a novel in-terleukin-18 converting enzyme. J. Dermatol. Sci. 59:129-35.
28. Dinarello CA. (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 117:3720-32.
29. Robertson SE, et al. (2006) Expression and alternative processing of IL-18 in human neutrophils. Eur. J. Immunol. 36:722-31.
30. Bellora F, et al. (2012) M-CSF induces the expression of a membrane-bound form of IL-18 in a subset of human monocytes differentiating in vitro toward macrophages. Eur. J. Immunol. 42:1618-26.
31. Dinarello CA. (2012) Membrane interleukin-18 revisits membrane IL-1alpha in T-helper type 1 responses. Eur. J. Immunol. 42:1385-7.
32. Akita K, et al. (1997) Involvement of caspase-1 and caspase-3 in the production and processing of mature human interleukin 18 in monocytic THP.1 cells. J. Biol. Chem. 272:26595-603.
33. Torigoe K, et al. (1997) Purification and characterization of the human interleukin-18 receptor. J. Biol. Chem. 272:25737-42.
34. Born TL, Thomassen E, Bird TA, Sims JE. (1998) Cloning of a novel receptor subunit, AcPL, required for interleukin-18 signaling. J. Biol. Chem. 273:29445-50.
35. Parnet P, Garka KE, Bonnert TP, Dower SK, Sims JE. (1996) IL-1Rrp is a novel receptor-like molecule similar to the type I interleukin-1 receptor and its homologues T1/ST2 and IL-1R AcP. J. Biol. Chem. 271:3967-70.
36. Boraschi D, et al. (2011) IL-37: a new antiinflammatory cytokine of the IL-1 family. Eur. Cytokine Net. 22:127-47.
37. Nold MF, et al. (2010) IL-37 is a fundamental inhibitor of innate immunity. Nat. Immunol. 11:1014-22.
38. Riva F, et al. (2012) TIR8/SIGIRR is an interleukin-1 receptor/toll like receptor family member with regulatory functions in inflammation and immunity. Front Immunol. 3:322.
39. Lee JK, et al. (2004) Differences in signaling pathways by IL-1beta and IL-18. Proc. Natl. Acad. Sci. U. S. A. 101:8815-20.
40. Adachi O, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity. 9:143-50.
41. Kanakaraj P, et al. (1999) Defective interleukin (IL)-18-mediated natural killer and T helper cell type 1 responses in IL-1 receptor-associated kinase (IRAK)-deficient mice. J. Exp. Med. 189:1129-38.
42. Kojima H, et al. (1998) Interleukin-18 activates the IRAK-TRAF6 pathway in mouse EL-4 cells. Biochem. Biophys. Res. Comm. 244:183-6.
43. Wyman TH, et al. (2002) Physiological levels of interleukin-18 stimulate multiple neutrophil functions through p38 MAP kinase activation. J. Leukoc. Biol. 72:401-9.
44. Novick D, et al. (1999) Interleukin-18 binding protein: a novel modulator of the Th1 cytokine response. Immunity. 10:127-36.
45. Kim SH, et al. (2000) Structural requirements of six naturally occurring isoforms of the IL-18 binding protein to inhibit IL-18. Proc. Nat. Acad. Sci. U. S. A. 97:1190-5.
46. Mallat Z, et al. (2001) Expression of interleukin-18 in human atherosclerotic plaques and relation to plaque instability. Circulation. 104:1598-603.
47. Hong SN, et al. (2013) Atherosclerotic biomarkers and aortic atherosclerosis by cardiovascular magnetic resonance imaging in the Framingham Heart Study. J. Am. Heart Assoc. 2:e000307.
48. Blankenberg S. (2002) Interleukin-18 is a strong predictor of cardiovascular death in stable and unstable angina. Circulation. 106:24-30.
49. Jefferis BJ, et al. (2011) Interleukin 18 and coronary heart disease: prospective study and systematic review. Atherosclerosis. 217:227-33.
50. Hartford M, et al. (2010) Interleukin-18 as a predictor of future events in patients with acute coronary syndromes. Arterioscler. Thromb. Vasc. Biol. 30:2039-46.
51. Blankenberg S, et al. (2003) Interleukin-18 and the risk of coronary heart disease in European men: the Prospective Epidemiological Study of Myocardial Infarction (PRIME). Circulation. 108:2453-9.
52. Kaptoge S, et al. (2013) Inflammatory cytokines and risk of coronary heart disease: new prospective study and updated meta-analysis. Europ. Heart J. 35:578-89.
53. Seta Y, et al. (2000) Interleukin 18 in acute myocardial infarction. Heart. 84:668.
54. Mallat Z, et al. (2004) Evidence for altered interleukin 18 (IL)-18 pathway in human heart failure. FASEB J. 18:1752-4.
55. Gangemi S, et al. (2003) Increased circulating Interleukin-18 levels in centenarians with no signs of vascular disease: another paradox of longevity? Exp. Gerontol. 38:669-72.
56. Chandrasekar B, Mummidi S, Claycomb WC, Mestril R, Nemer M. (2005) Interleukin-18 is a pro-hypertrophic cytokine that acts through a phosphatidylinositol 3-kinase-phosphoinositidedependent kinase-1-Akt-GATA4 signaling pathway in cardiomyocytes. J. Biol. Chem. 280:4553-67.
57. Gardner D. (2003) Natriuretic peptides: markers or modulators of cardiac hypertrophy? Trends Endocrinol. Metabol. 14:411-6.
58. Woldbaek PR, et al. (2005) Daily administration of interleukin-18 causes myocardial dysfunction in healthy mice. Am. J. Physiol. Heart Circ. Physiol. 289:H708-14.
59. Platis A, et al. (2008) The effect of daily administration of IL-18 on cardiac structure and function. Perfusion. 23:237-42.
60. Colston JT, et al. (2007) Interleukin-18 knockout mice display maladaptive cardiac hypertrophy in response to pressure overload. Biochem. Biophys. Res. Commun. 354:552-8.
61. Chang H, et al. (2013) Effect of hydrodynamicsbased delivery of IL-18BP fusion gene on rat experimental autoimmune myocarditis. Clin. Exp. Med. 2013 Oct 12. [Epub ahead of print].
62. Woldbaek PR, et al. (2003) Increased cardiac IL-18 mRNA, pro-IL-18 and plasma IL-18 after myocardial infarction in the mouse; a potential role in cardiac dysfunction. Cardiovasc. Res. 59:122-31.
63. Venkatachalam K, et al. (2009) Neutralization of interleukin-18 ameliorates ischemia/reperfusioninduced myocardial injury. J. Biol. Chem. 284:7853-65.
64. Wang M, et al. (2009) IL-18 binding protein-expressing mesenchymal stem cells improve myocardial protection after ischemia or infarction. Proc. Nat. Acad. Sci. U. S. A. 106:17499-504.
65. Toldo S, et al. (2014) Formation of the inflammasome in acute myocarditis. Int. J. Cardiol. 171:e119-21.
66. Hedayat M, Mahmoudi MJ, Rose NR, Rezaei N. (2010) Proinflammatory cytokines in heart failure: double-edged swords. Heart Fail. Rev. 15:543-62.
67. Puren AJ, Fantuzzi G, Gu Y, Su MS, Dinarello CA. (1998) Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-CD14+ human blood mononuclear cells. J. Clin. Invest. 101:711-21.
68. Morel JC, Park CC, Kumar P, Koch AE. (2001) Interleukin-18 induces rheumatoid arthritis synovial fibroblast CXC chemokine production through NFkappaB activation. Lab. Invest. 81:1371-83.
69. Netea MG, Kullberg BJ, Verschueren I, Van Der Meer JW. (2000) Interleukin-18 induces production of proinflammatory cytokines in mice: no intermediate role for the cytokines of the tumor necrosis factor family and interleukin-1beta. Eur. J. Immunol. 30:3057-60.
70. Dinarello CA. (1999) IL-18: A TH1-inducing, pro inflammatory cytokine and new member of the IL-1 family. J. Allergy Clin. Immunol. 103:11-24.
71. 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. 98:2871-6.
72. Raeburn CD, et al. (2002) Neutralization of IL-18 attenuates lipopolysaccharide-induced myocardial dysfunction. Am. J. Physiol. Heart Circ. Phys. 283: H650-7.
73. Leung BP, et al. (2001) A role for IL-18 in neutrophil activation. J. Immunol. 167:2879-86.
74. Toldo S, et al. (2014) Interleukin-18 mediates interleukin-1-induced cardiac dysfunction. Am. J. Physiol. Heart Circ. Physiol. 306:H1025-31.
75. Fowler MB, Laser JA, Hopkins GL, Minobe W, Bristow MR. (1986) Assessment of the beta-adrenergic receptor pathway in the intact failing human heart: progressive receptor down-regulation and subsensitivity to agonist response. Circulation. 74:1290-302.
76. Lefkowitz RJ, Rockman HA, Koch WJ. (2000) Catecholamines, cardiac beta-adrenergic receptors, and heart failure. Circulation. 101:1634-7.
77. Naga Prasad SV, Nienaber J, Rockman HA. (2001) Beta-adrenergic axis and heart disease. Trends Gen. 17:S44-49.
78. Murray DR, et al. (2012) Beta2 adrenergic activation induces the expression of IL-18 binding protein, a potent inhibitor of isoproterenol induced cardiomyocyte hypertrophy in vitro and myocardial hypertrophy in vivo. J. Mol. Cell. Cardiol. 52:206-18.
79. Chandrasekar B, et al. (2004) Beta-adrenergic stimulation induces interleukin-18 expression via beta2-AR, PI3K, Akt, IKK, and NF-kappaB. Biochem. Biophys. Res. Comm. 319:304-11.
80. Chandrasekar B, et al. (2004) Activation of intrinsic and extrinsic proapoptotic signaling pathways in interleukin-18-mediated human cardiac endothelial cell death. J. Biol. Chem. 279:20221-33.
81. Dao T, Ohashi K, Kayano T, Kurimoto M, Okamura H. (1996) Interferon-gamma-inducing factor, a novel cytokine, enhances Fas ligand-mediated cytotoxicity of murine T helper 1 cells. Cell. Immunol. 173:230-5.
82. Tsutsui H, et al. (1996) IFN-gamma-inducing factor up-regulates Fas ligand-mediated cytotoxic activity of murine natural killer cell clones. J. Immunol. 157:3967-73.
83. Chandrasekar B, Valente AJ, Freeman GL, Mahimainathan L, Mummidi S. (2006) Interleukin-18 induces human cardiac endothelial cell death via a novel signaling pathway involving NF-kappaBdependent PTEN activation. Biochem. Biophys. Res. Comm. 339:956-63.
84. Yu Q, et al. (2009) IL-18 induction of osteopontin mediates cardiac fibrosis and diastolic dysfunction in mice. Am. J. Physiol. Heart Circ. Physiol. 297:H76-85.
85. Stawowy P, et al. (2002) Increased myocardial expression of osteopontin in patients with advanced heart failure. Eur. J. Heart Fail. 4:139-46.
86. Reddy VS, et al. (2008) Interleukin-18 stimulates fibronectin expression in primary human cardiac fibroblasts via PI3K-Akt-dependent NF-kappaB activation. J. Cell. Physiol. 215:697-707.
87. Fix C, Bingham K, Carver W. (2011) Effects of interleukin-18 on cardiac fibroblast function and gene expression. Cytokine. 53:19-28.
88. First Time in Human Study of Intravenous Interleukin-18 Antibody (A18110040) [Internet]. [Bethesda (MD)]: U.S. National Institutes of Health, U.S. National Library of Medicine.; [updated 2012 Dec 19; cited 2014 May 2]. Available from: http:// clinicaltrials.gov/ct2/show/ NCT01035645. NLM identifier, NCT01035645.
89. Tak PP, Bacchi M, Bertolino M. (2006) Pharmacokinetics of IL-18 binding protein in healthy volunteers and subjects with rheumatoid arthritis or plaque psoriasis. Eur. J. Drug Metab. Pharmacokinet. 31:109-16.
90. Marchetti C, et al. (2013) A novel pharmacologic inhibitor of the NLRP3 inflammasome limits myocardial injury following ischemia-reperfusion in the mouse. J. Cardiovasc. Pharmacol. 63:316-22.
91. Investigate the Efficacy and Safety of GSK1070806 in Obese Subjects With T2DM [Internet]. [Bethesda (MD)]: U.S. National Institutes of Health, U.S. National Library of Medicine; [updated 2014 Apr 14; cited 2014 May 2]. Available from: http://www.clinicaltrials.gov/ct2/show/ NCT01648153?term=GSK1070806&rank=1. NLM identifier, NCT01648153.
92. Crossman DC, et al. (2008) Investigation of the effect of Interleukin-1 receptor antagonist (IL-1ra) on markers of inflammation in non-ST elevation acute coronary syndromes (The MRCILA-HEART Study). Trials. 9:8.
93. Abbate A, et al. (2010) Interleukin-1 blockade with anakinra to prevent adverse cardiac remodeling after acute myocardial infarction (Virginia Commonwealth University Anakinra Remodeling Trial [VCU-ART] Pilot study). Am. J. Cardiol. 105:1371-7, e1.
94. Abbate A, et al. (2013) Effects of interleukin-1 blockade with anakinra on adverse cardiac remodeling and heart failure after acute myocardial infarction [from the Virginia Commonwealth University-Anakinra Remodeling Trial (2) (VCU-ART2) pilot study]. Am. J. Cardiol. 111:1394-400.
95. IL-1 Blockade in Acute Myocardial Infarction (VCU-ART3) [Internet]. [Bethesda (MD)]: U.S. National Institutes of Health, U.S. National Library of Medicine; [updated 2013 Sep 20; cited 2014 May 2]. Available from: http://clinicaltrials. gov/ct2/show/NCT01950299?term=nct01950299 &rank=1. NLM identifier, NCT01950299.
96. Van Tassell BW, et al. (2014) Effects of interleukin-1 blockade with anakinra on aerobic exercise capacity in patients with heart failure and preserved ejection fraction (from the D-HART pilot study). Am. J. Cardiol. 113:321-7.
97. Van Tassell BW, Toldo S, Mezzaroma E, Abbate A. (2013) Targeting interleukin-1 in heart disease. Circulation. 128:1910-23.
98. Borlaug BA, Paulus WJ. (2011) Heart failure with preserved ejection fraction: pathophysiology, diagnosis, and treatment. Eur. Heart J. 32:670-9.
99. Westermann D, et al. (2011) Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction. Circ. Heart Fail. 4:44-52.
100. Stuyt RJ, et al. (2002) Role of interleukin-18 in host defense against disseminated Candida albicans infection. Infect. Immun. 70:3284-6.
101. Huang X, McClellan SA, Barrett RP, Hazlett LD. (2002) IL-18 contributes to host resistance against infection with Pseudomonas aeruginosa through induction of IFN-gamma production. J. Immunol. 168:5756-63.
102. Liu B, et al. (2004) Interleukin-18 improves the early defence system against influenza virus infection by augmenting natural killer cell-mediated cytotoxicity. J. Gen. Virol. 85:423-8.