Targeting Interleukin-1 in Heart Failure and Inflammatory Heart Disease

Current Heart Failure Reports

Volumn 12, Issue 1, 2015, Pages 33-41

  Van Tassell, Benjamin W ^a   Raleigh, Juan M Valle ^a   Abbate, Antonio ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Acute myocardial infarction; Anakinra; Heart failure; Inflammation; Interleukin 1

Indexed keywords

CANAKINUMAB; INTERLEUKIN 1; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; AUTACOID; CARDIOVASCULAR AGENT; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT;

CARDIAC PATIENT; CARDIOMYOPATHY; EXERCISE; HEART FAILURE; HEART FUNCTION; HEART VENTRICLE REMODELING; HUMAN; INCIDENCE; ISCHEMIC CARDIOMYOPATHY; MYOCARDITIS; NONHUMAN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; SYSTEMATIC REVIEW; UPREGULATION; ANTAGONISTS AND INHIBITORS; COMPLICATION; HEART INFARCTION; PHYSIOLOGY;

CARDIOVASCULAR AGENTS; HEART FAILURE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; MYOCARDIAL INFARCTION; MYOCARDITIS; VENTRICULAR REMODELING;

EID: 84920671060     PISSN: 15469530     EISSN: 15469549     Source Type: Journal    
DOI: 10.1007/s11897-014-0231-7     Document Type: Review

References (65)

1. Braunwald E. Heart failure. JACC Heart Fail. 2013;1(1):1–20. This is a review article on epidemiology, pathophysiology, and recent developments in the management of HF.
2. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, et al. Heart disease and stroke statistics-2013 update a report from the American Heart Association. Circulation. 2013;127:E6–245.
3. Borlaug BA. The pathophysiology of heart failure with preserved ejection fraction. Nat Rev Cardiol. 2014;11(9):507–15. This is a recent review article which focuses on the current understanding of the pathophysiological mechanisms on HFpEF.
4. Mann DL. Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ Res. 2002;91(11):988–98.
5. Frangogiannis NG. The inflammatory response in myocardial injury, repair, and remodelling. Nat Rev Cardiol. 2014;11(5):255–65. This review article emphasizes on inflammatory mechanism on myocardial infarction and possible therapeutic targets related.
6. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011;117:3720–32. This review article focuses on molecular mechanisms of IL-1 and on acute and chronic inflammatory diseases treated by reducing IL-1 activity.
7. Testa M, Yeh M, Lee P, Fanelli R, Loperfido F, Berman JW, et al. Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension. J Am Coll Cardiol. 1996;28:964–71.
8. Mann DL, Young JB. Basic mechanisms in congestive heart failure. Recognizing the role of proinflammatory cytokines. Chest. 1994;105(3):897–904.
9. Anker SD, von Haehling S. Inflammatory mediators in chronic heart failure: an overview. Heart. 2004;90(4):464–70.
10. Yndestad A, Damås JK, Oie E, Ueland T, Gullestad L, Aukrust P. Systemic inflammation in heart failure—the whys and wherefores. Heart Fail Rev. 2006;11(1):83–92.
11. Blake GJ, Ridker PM. C-reactive protein and other inflammatory risk markers in acute coronary syndromes. J Am Coll Cardiol. 2003;41(4 Suppl S):37S–42.
12. Sonnino C, Toldo S, Mezzaorma E, Abbate A. Inflammasome: a new villain in heart disease. Inflammasome. 2014;1:30–5.
13. Van Tassell BW, Toldo S, Mezzaroma E, Abbate A. Targeting interleukin-1 in heart disease. Circulation. 2013;128(17):1910–23.
14. Mezzaroma E, Toldo S, Farkas D, Seropian IM, Van Tassell BW, Salloum FN, et al. The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc Natl Acad Sci U S A. 2011;108(49):19725–30.
15. Abbate A, Salloum FN, Van Tassell BW, Vecile E, Toldo S, Seropian I, et al. Alterations in the interleukin-1/interleukin-1 receptor antagonist balance modulate cardiac remodeling following myocardial infarction in the mouse. PLoS One. 2011;6(11):e27923.
16. Abbate A, Van Tassell BW, Seropian IM, Toldo S, Robati R, Varma A, et al. Interleukin-1beta modulation using a genetically engineered antibody prevents adverse cardiac remodelling following acute myocardial infarction in the mouse. Eur J Heart Fail. 2010;12(4):319–22.
17. Van Tassell BW, Varma A, Salloum FN, Das A, Seropian IM, Toldo S, et al. Interleukin-1 trap attenuates cardiac remodeling after experimental acute myocardial infarction in mice. J Cardiovasc Pharmacol. 2010;55(2):117–22.
18. Abbate A, Salloum FN, Vecile E, Das A, Hoke NN, Straino S, et al. Anakinra, a recombinant human interleukin-1 receptor antagonist, inhibits apoptosis in experimental acute myocardial infarction. Circulation. 2008;117(20):2670–83.
19. Toldo S, Mezzaroma E, Van Tassell BW, Farkas D, Marchetti C, Voelkel NF, et al. Interleukin-1β blockade improves cardiac remodelling after myocardial infarction without interrupting the inflammasome in the mouse. Exp Physiol. 2013;98(3):734–45.
20. Toldo S, Mezzaroma E, Bressi E, Marchetti C, Carbone S, Sonnino C, et al. Interleukin-1β blockade improves left ventricular systolic/diastolic function and restores contractility reserve in severe ischemic cardiomyopathy in the mouse. J Cardiovasc Pharmacol. 2014;64(1):1–6.
21. Abbate A, Kontos MC, Grizzard JD, Biondi-Zoccai GG, Van Tassell BW, Robati R, et al. 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. 2010;105(10):1371–7. The first pilot clinical study on IL-1 blockade in STEMI population.
22. Abbate A, Van Tassell BW, Biondi-Zoccai G, Kontos MC, Grizzard JD, Spillman DW, et al. 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. 2013;111(10):1394–400. Similar to VCU-ART, this pilot study evaluated IL-1 blockade in STEMI population and recruited 30 more patients.
23. http://www.clinicaltrials.gov (NCT NCT01950299), Accessed 9 May 2014.
24. Morton AC, Rothman AM, Greenwood JP, Gunn J, Chase A, Clarke B, et al. The effect of interleukin-1 receptor antagonist therapy on markers of inflammation in non-ST elevation acute coronary syndromes: the MRC-ILA Heart Study. Eur Heart J. 2014;30:ehu272. The first clinical trial (phase II) on effects of IL-1 blockade with anakinra in NSTEMI patients.
25. Abbate A, Dinarello CA. Anti-inflammatory therapies in acute coronary syndromes: is IL-1 blockade a solution? Eur Heart J. 2014 – in press.
26. Bracey NA, Beck PL, Muruve DA, Hirota SA, Guo J, Jabagi H, et al. The Nlrp3 inflammasome promotes myocardial dysfunction in structural cardiomyopathy through interleukin-1β. Exp Physiol. 2013;98(2):462–72.
27. Toldo S, Kannan H, Bussani R, Anzini M, Sonnino C, Sinagra G, et al. Formation of the inflammasome in acute myocarditis. Int J Cardiol. 2014;171(3):e119–21.
28. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR. Role of IL-1 and tumor necrosis factor in coxsackie virus-induced autoimmune myocarditis. J Immunol. 1993;151(3):1682–90.
29. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR. Interleukin 1 or tumor necrosis factor can promote Coxsackie B3-induced myocarditis in resistant B10.A mice. J Exp Med. 1992;175(4):1123–9.
30. Lim BK, Choe SC, Shin JO, Ho SH, Kim JM, Yu SS, et al. Local expression of interleukin-1 receptor antagonist by plasmid DNA improves mortality and decreases myocardial inflammation in experimental coxsackieviral myocarditis. Circulation. 2002;105(11):1278–81.
31. Van Tassell BW, Seropian IM, Toldo S, Mezzaroma E, Abbate A. Interleukin-1β induces a reversible cardiomyopathy in the mouse. Inflamm Res. 2013;62(7):637–40.
32. Van Tassell BW, Arena RA, Toldo S, Mezzaroma E, Azam T, Seropian IM, et al. Enhanced interleukin-1 activity contributes to exercise intolerance in patients with systolic heart failure. PLoS One. 2012;7(3):e33438. The first pilot study that evaluated exercise capacity in patients with HFrEF and IL-1 blockade with anakinra.
33. Zhu J, Zhang J, Zhang L, Du R, Xiang D, Wu M, et al. Interleukin-1 signaling mediates acute doxorubicin-induced cardiotoxicity. Biomed Pharmacother. 2011;65(7):481–5.
34. Zhu J, Zhang J, Xiang D, Zhang Z, Zhang L, Wu M, et al. Recombinant human interleukin-1 receptor antagonist protects mice against acute doxorubicin-induced cardiotoxicity. Eur J Pharmacol. 2010;643(2–3):247–53.
35. Mezzaroma E, Toldo S, Cardnell RJ, Van Tassell BW, Mikkelsen RB, Gewirtz DA, et al. Role of interleukin-1 in acute radiation-induced cardiomyopathy. Circulation. 2012;126:A17799.
36. Mezzorma E, Toldo S, Van Tassell BW, Marchetti C, Mikkelsen RB, Gewirtz DA, et al. Preserved left ventricular contractile reserve after thoracic irradiation in the interleukin-1 receptor knock out mouse. Circulation. 2013;128:A14774.
37. Toldo S, Mezzaroma E, O’Brien L, Marchetti C, Seropian IM, Voelkel NF, et al. Interleukin-18 mediates interleukin-1-induced cardiac dysfunction. Am J Physiol Heart Circ Physiol. 2014;306(7):H1025–31.
38. Kumar A, Thota V, Dee L, Olson J, Uretz E, Parrillo JE. Tumor necrosis factor alpha and interleukin 1beta are responsible for in vitro myocardial cell depression induced by human septic shock serum. J Exp Med. 1996;183(3):949–58.
39. Chung MK, Gulick TS, Rotondo RE, Schreiner GF, Lange LG. Mechanism of cytokine inhibition of beta-adrenergic agonist stimulation of cyclic AMP in rat cardiac myocytes. Impairment of signal transduction. Circ Res. 1990;67:753–63.
40. Liu SJ, Zhou W, Kennedy RH. Suppression of beta-adrenergic responsiveness of L-type Ca2+ current by IL-1beta in rat ventricular myocytes. Am J Physiol. 1999;276:H141–8.
41. Schreur KD, Liu S. Involvement of ceramide in inhibitory effect of IL-1 beta on L-type Ca2+ current in adult rat ventricular myocytes. Am J Physiol. 1997;272:H2591–8.
42. Liu S, Schreur KD. G protein-mediated suppression of L-type Ca2+ current by interleukin-1 beta in cultured rat ventricular myocytes. Am J Physiol. 1995;268:C339–49.
43. Combes A, Frye CS, Lemster BH, Brooks SS, Watkins SC, Feldman AM, et al. Chronic exposure to interleukin 1beta induces a delayed and reversible alteration in excitation-contraction coupling of cultured cardiomyocytes. Pflugers Arch. 2002;445:246–56.
44. McTiernan CF, Lemster BH, Frye C, Brooks S, Combes A, Feldman AM. Interleukin-1 beta inhibits phospholamban gene expression in cultured cardiomyocytes. Circ Res. 1997;81:493–503.
45. Tatsumi T, Matoba S, Kawahara A, Keira N, Shiraishi J, Akashi K, et al. Cytokine-induced nitric oxide production inhibits mitochondrial energy production and impairs contractile function in rat cardiac myocytes. J Am Coll Cardiol. 2000;35:1338–46.
46. Schulz R, Panas DL, Catena R, Moncada S, Olley PM, Lopaschuk GD. The role of nitric oxide in cardiac depression induced by interleukin-1 beta and tumour necrosis factor-alpha. Br J Pharmacol. 1995;114:27–34.
47. Tsujino M, Hirata Y, Imai T, Kanno K, Eguchi S, Ito H, et al. Induction of nitric oxide synthase gene by interleukin-1 beta in cultured rat cardiocytes. Circulation. 1994;90:375–83.
48. Deswal A, Petersen NJ, Feldman AM, Young JB, White BG, Mann DL. Cytokines and cytokine receptors in advanced heart failure—an analysis of the cytokine database from the vesnarinone trial (VEST). Circulation. 2001;103:2055–9.
49. Ikonomidis I, Lekakis JP, Nikolaou M, Paraskevaidis I, Andreadou I, Kaplanoglou T, et al. Inhibition of interleukin-1 by anakinra improves vascular and left ventricular function in patients with rheumatoid arthritis. Circulation. 2008;117:2662–9.
50. Ikonomidis I, Tzortzis S, Lekakis J, Paraskevaidis I, Andreadou I, Nikolaou M, et al. Lowering interleukin-1 activity with anakinra improves myocardial deformation in rheumatoid arthritis. Heart. 2009;95(18):1502–7.
51. Ikonomidis I, Tzortzis S, Lekakis J, Paraskevaidis I, Dasou P, Parissis J, et al. Association of soluble apoptotic markers with impaired left ventricular deformation in patients with rheumatoid arthritis. Effects of inhibition of interleukin-1 activity by anakinra. Thromb Haemost. 2011;106(5):959–67.
52. Ikonomidis I, Tzortzis S, Andreadou I, Paraskevaidis I, Katseli C, Katsimbri P, et al. Increased benefit of interleukin-1 inhibition on vascular function, myocardial deformation, and twisting in patients with coronary artery disease and coexisting rheumatoid arthritis. Circ Cardiovasc Imaging. 2014;7(4):619–28.
53. Abbate A, Canada JM, Van Tassell BW, Wise CM, Dinarello CA. Interleukin-1 blockade in rheumatoid arthritis and heart failure: a missed opportunity? Int J Cardiol. 2014;171:E125–6. Case report in a patient with rheumatoid arthritis and heart failure in which improvement of cardiovascular health after treatment with anakinra was significant.
54. Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician’s Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122:191–225.
55. Dinarello CA, Ikejima T, Warner SJ, Orencole SF, Lonnemann G, Cannon JG, et al. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J Immunol. 1987;139(6):1902–10.
56. Shah SJ, Marcus GM, Gerber IL, McKeown BH, Vessey JC, Jordan MV, et al. High-sensitivity C-reactive protein and parameters of left ventricular dysfunction. J Card Fail. 2006;12:61–5.
57. Michowitz Y, Arbel Y, Wexler D, Sheps D, Rogowski O, Shapira I, et al. Predictive value of high sensitivity CRP in patients with diastolic heart failure. Int J Cardiol. 2008;125:347–51.
58. Van Tassell BW, Arena R, Biondi-Zoccai G, McNair Canada J, Oddi C, Abouzaki NA, Jahangiri A, Falcao RA, Kontos MC, Shah KB, Voelkel NF, Dinarello CA, Abbate A. 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. 2014;113(2):321–7. First clinical pilot study that evaluated exercise capacity in patients with HFpEF and increased IL-1 activity (measured by CRP levels) treated with anakinra.
59. Paulus WJ, Tschöpe C, Sanderson JE, Rusconi C, Flachskampf FA, Rademakers FE, et al. How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur Heart J. 2007;28(20):2539–50.
60. http://www.clinicaltrials.gov (NCT01936844), Accessed 9 May 2014.
61. http://www.clinicaltrials.gov (NCT01936909), Accessed 9 May 2014.
62. http://www.clinicaltrials.gov (NCT02173548), Accessed 9 May 2014.
63. Ridker PM, Thuren T, Zalewski A, Libby P. Interleukin-1β inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-inflammatory Thrombosis Outcomes Study (CANTOS). Am Heart J. 2011;162(4):597–605.
64. Howard C, Noe A, Skerjanec A, Holzhauer B, Wernsing M, Ligueros-Saylan M, et al. Safety and tolerability of canakinumab, an IL-1β inhibitor, in type 2 diabetes mellitus patients: a pooled analysis of three randomised double-blind studies. Cardiovasc Diabetol. 2014;13:94.
65. http://www.clinicaltrials.gov (NCT01900600), Accessed 9 May 2014.