Mesenchymal stromal cells inhibit NLRP3 inflammasome activation in a model of Coxsackievirus B3-induced inflammatory cardiomyopathy

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Miteva, Kapka ^a,b   Pappritz, Kathleen ^a,b   Sosnowski, Marzena ^a   El Shafeey, Muhammad ^a,c   Müller, Irene ^a,b   Dong, Fengquan ^a   Savvatis, Konstantinos ^a   Ringe, Jochen ^a   Tschöpe, Carsten ^a,b   Van Linthout, Sophie ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c Universities and Research centers District   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRP3 PROTEIN, MOUSE;

ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CARDIOMYOPATHY; COXSACKIE VIRUS INFECTION; HEART; HUMAN; INFLAMMATION; MACROPHAGE; MALE; MESENCHYMAL STEM CELL; METABOLISM; MOUSE; MYOCARDITIS; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; CARDIOMYOPATHIES; CASPASE 1; COXSACKIEVIRUS INFECTIONS; HEART; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MYOCARDITIS; MYOCARDIUM; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN;

EID: 85041963346     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-20686-6     Document Type: Article

References (48)

1. Caforio, A. L. et al. Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J. 34(2636-2648), 2648a-2648d (2013).
2. Janeway, C. A. Jr. & Medzhitov, R. Innate immune recognition. Annu Rev Immunol. 20, 197-216 (2002).
3. Müller, I. et al. Pathogenic role of the damage-associated molecular patterns S100A8 and S100A9 in Coxsackievirus B3-induced myocarditis. Circ Heart Fail.; In Press (2017).
4. Sutterwala, F. S., Haasken, S. & Cassel, S. L. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci. 1319, 82-95 (2014).
5. Sabbah, A. et al. Activation of innate immune antiviral responses by Nod2. Nat Immunol. 10, 1073-1080 (2009).
6. Li, X. et al. NOD2 deficiency protects against cardiac remodeling after myocardial infarction in mice. Cell Physiol Biochem. 32, 1857-1866 (2013).
7. Van Tassell, B. W., Toldo, S., Mezzaroma, E. & Abbate, A. Targeting interleukin-1 in heart disease. Circulation. 128, 1910-1923 (2013).
8. McTiernan, C. F. et al. Interleukin-1 beta inhibits phospholamban gene expression in cultured cardiomyocytes. Circ Res. 81, 493-503 (1997).
9. Pomerantz, B. J., Reznikov, L. L., Harken, A. H. & Dinarello, C. A. 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 (2001).
10. Abbate, A. et al. Anakinra, a recombinant human interleukin-1 receptor antagonist, inhibits apoptosis in experimental acute myocardial infarction. Circulation. 117, 2670-2683 (2008).
11. Kawaguchi, M. et al. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation. 123, 594-604 (2011).
12. Wang, Y., Gao, B. & Xiong, S. Involvement of NLRP3 inflammasome in CVB3-induced viral myocarditis. Am J Physiol Heart Circ Physiol. 307, H1438-1447 (2014).
13. Tschope, C. et al. NOD2 (Nucleotide-Binding Oligomerization Domain 2) Is a Major Pathogenic Mediator of Coxsackievirus B3-Induced Myocarditis. Circ Heart Fail. 10 (2017).
14. Ridker, P. M. et al. Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease. N Engl J Med. 377, 1119-1131 (2017).
15. Miteva, K., Van Linthout, S., Volk, H. D. & Tschope, C. Immunomodulatory effects of mesenchymal stromal cells revisited in the context of inflammatory cardiomyopathy. Stem Cells Int. 2013, 353097 (2013).
16. Tschope, C., Miteva, K., Schultheiss, H. P. & Linthout, S. V. Mesenchymal stromal cells: a promising cell source for the treatment of inflammatory cardiomyopathy. Curr Pharm Des. 17, 3295-3307 (2011).
17. Van Linthout, S. et al. Placenta-Derived Adherent Stromal Cells Improve Diabetes Mellitus-Associated Left Ventricular Diastolic Performance. Stem Cells Transl Med (2017).
18. Van Linthout, S. et al. Mesenchymal stem cells improve murine acute coxsackievirus B3-induced myocarditis. Eur Heart J. 32, 2168-2178 (2011).
19. Savvatis, K. et al. Mesenchymal stromal cells but not cardiac fibroblasts exert beneficial systemic immunomodulatory effects in experimental myocarditis. PLOS One. 7, e41047 (2012).
20. Oh, J. Y. et al. Mesenchymal stem/stromal cells inhibit the NLRP3 inflammasome by decreasing mitochondrial reactive oxygen species. Stem Cells. 32, 1553-1563 (2014).
21. Martinon, F. Signaling by ROS drives inflammasome activation. Eur J Immunol. 40, 616-619 (2010).
22. Hofnagel, O. et al. Proinflammatory cytokines regulate LOX-1 expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 24, 1789-1795 (2004).
23. Toldo, S. et al. Formation of the inflammasome in acute myocarditis. Int J Cardiol. 171, e119-121 (2014).
24. Kuhl, U. et al. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation. 111, 887-893 (2005).
25. Kuhl, U. et al. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation. 112, 1965-1970 (2005).
26. Andreoletti, L. et al. Viral causes of human myocarditis. Arch Cardiovasc Dis. 102, 559-568 (2009).
27. Mezzaroma, E. et al. The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc Natl Acad Sci USA 108, 19725-19730 (2011).
28. Lech, M. et al. Quantitative expression of RIG-like helicase, NOD-like receptor and inflammasome-related mRNAs in humans and mice. Int Immunol. 22, 717-728 (2010).
29. Si, X. et al. Pyrrolidine dithiocarbamate reduces coxsackievirus B3 replication through inhibition of the ubiquitin-proteasome pathway. J Virol. 79, 8014-8023 (2005).
30. Badorff, C. et al. Nitric oxide inhibits dystrophin proteolysis by coxsackieviral protease 2A through S-nitrosylation: A protective mechanism against enteroviral cardiomyopathy. Circulation. 102, 2276-2281 (2000).
31. Fritz, J. H. et al. Synergistic stimulation of human monocytes and dendritic cells by Toll-like receptor 4 and NOD1-and NOD2-activating agonists. Eur J Immunol. 35, 2459-2470 (2005).
32. Coulombe, F. et al. Muramyl dipeptide induces NOD2-dependent Ly6C(high) monocyte recruitment to the lungs and protects against influenza virus infection. PLoS One. 7, e36734 (2012).
33. Miteva, K. et al. Mesenchymal Stromal Cells Modulate Monocytes Trafficking in Coxsackievirus B3-Induced Myocarditis. Stem Cells Transl Med (2017).
34. Davis, K. M., Nakamura, S. & Weiser, J. N. Nod2 sensing of lysozyme-digested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J Clin Invest. 121, 3666-3676 (2011).
35. Liu, L., Yue, Y. & Xiong, S. NK-derived IFN-gamma/IL-4 triggers the sexually disparate polarization of macrophages in CVB3-induced myocarditis. J Mol Cell Cardiol. 76, 15-25 (2014).
36. Li, K. et al. Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res. 105, 353-364 (2009).
37. Eriksson, U. et al. Dendritic cell-induced autoimmune heart failure requires cooperation between adaptive and innate immunity. Nat Med. 9, 1484-1490 (2003).
38. Neu, N. et al. Autoantibodies specific for the cardiac myosin isoform are found in mice susceptible to Coxsackievirus B3-induced myocarditis. J Immunol. 138, 2488-2492 (1987).
39. Neu, N. et al. Coxsackievirus induced myocarditis in mice: cardiac myosin autoantibodies do not cross-react with the virus. Clin Exp Immunol. 69, 566-574 (1987).
40. Neumann, D. A. et al. Circulating heart-reactive antibodies in patients with myocarditis or cardiomyopathy. J Am Coll Cardiol. 16, 839-846 (1990).
41. Shaw, P. J., McDermott, M. F. & Kanneganti, T. D. Inflammasomes and autoimmunity. Trends Mol Med. 17, 57-64 (2011).
42. Ong, S. et al. Natural killer cells limit cardiac inflammation and fibrosis by halting eosinophil infiltration. Am J Pathol. 185, 847-861 (2015).
43. Escher, F. et al. Presence of perforin in endomyocardial biopsies of patients with inflammatory cardiomyopathy predicts poor outcome. Eur J Heart Fail. 16, 1066-1072 (2014).
44. Abbate, A. 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. 105, 1371-1377 e1371 (2010).
45. Kiss, E., Jakab, G., Kranias, E. G. & Edes, I. Thyroid hormone-induced alterations in phospholamban protein expression. Regulatory effects on sarcoplasmic reticulum Ca2+ transport and myocardial relaxation. Circ Res. 75, 245-251 (1994).
46. Kasner, M. et al. Diastolic tissue Doppler indexes correlate with the degree of collagen expression and cross-linking in heart failure and normal ejection fraction. J Am Coll Cardiol. 57, 977-985 (2011).
47. Yang, J. et al. Targeting LOXL2 for cardiac interstitial fibrosis and heart failure treatment. Nat Commun. 7, 13710 (2016).
48. Binger, T. et al. Migration potential and gene expression profile of human mesenchymal stem cells induced by CCL25. Exp Cell Res. 315, 1468-1479 (2009).