Mesenchymal stromal cells modulate monocytes trafficking in coxsackievirus B3-induced myocarditis

Stem Cells Translational Medicine

Volumn 6, Issue 4, 2017, Pages 1249-1261

  Miteva, Kapka ^a,b   Pappritz, Kathleen ^a,b   El Shafeey, Muhammad ^a   Dong, Fengquan ^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)

Author keywords

Mesenchymal stromal cells; Monocytes trafficking; Myocarditis

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; RANTES; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD ANALYSIS; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; COXSACKIEVIRUS B3; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; MALE; MESENCHYMAL STROMA CELL; MOLECULAR BIOLOGY; MONOCYTE; MOUSE; MYELOPOIESIS; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; VIRUS MYOCARDITIS; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CELL CULTURE; COMPLICATION; COXSACKIE VIRUS INFECTION; CYTOLOGY; MESENCHYMAL STEM CELL; METABOLISM; MYOCARDITIS; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; CHEMOKINE CCL2; CHEMOKINE CCL7; COXSACKIEVIRUS INFECTIONS; HUMANS; INTERLEUKIN-12; INTERLEUKIN-6; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MONOCYTES; MYOCARDITIS; MYOCARDIUM; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85017532632     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.1002/sctm.16-0353     Document Type: Article

References (52)

1. Kindermann I, Kindermann M, Kandolf R et al. Predictors of outcome in patients with suspected myocarditis. Circulation 2008;118: 639–648.
2. Ismahil MA, Hamid T, Bansal SS et al. Remodeling of the mononuclear phagocyte network underlies chronic inflammation and disease progression in heart failure: Critical importance of the cardiosplenic axis. Circ Res 2014;114:266–282.
3. Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circ Res 2013;112:1624–1633.
4. Nahrendorf M, Pittet MJ, Swirski FK. Monocytes: Protagonists of infarct inflammation and repair after myocardial infarction. Circulation 2010;121:2437–2445.
5. Apostolakis S, Lip GY, Shantsila E. Monocytes in heart failure: Relationship to a deteriorating immune overreaction or a desperate attempt for tissue repair? Cardiovasc Res 2010;85:649–660.
6. Yang J, Zhang L, Yu C et al. Monocyte and macrophage differentiation: Circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res 2014;2:1.
7. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 2006;354:610–621.
8. Swirski FK, Nahrendorf M, Etzrodt M et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009;325:612–616.
9. Leuschner F, Courties G, Dutta P et al. Silencing of CCR2 in myocarditis. Eur Heart J 2015;36:1478–1488.
10. Tsou CL, Peters W, Si Y et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007;117: 902–909.
11. Nahrendorf M, Swirski FK, Aikawa E et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007;204:3037–3047.
12. Karantalis V, Hare JM. Use of mesenchymal stem cells for therapy of cardiac disease. Circ Res 2015;116:1413–1430.
13. Karantalis V, DiFede DL, Gerstenblith G et al. Autologous mesenchymal stem cells produce concordant improvements in regional function, tissue perfusion, and fibrotic burden when administered to patients undergoing coronary artery bypass grafting: The Prospective Randomized Study of Mesenchymal Stem Cell Therapy in Patients Undergoing Cardiac Surgery (PROME-THEUS) trial. Circ Res 2014;114:1302–1310.
14. Mushtaq M, DiFede DL, Golpanian S et al. Rationale and design of the Percutaneous Stem Cell Injection Delivery Effects on Neomyogenesis in Dilated Cardiomyopathy (the POSEIDON-DCM study): A phase I/II, randomized pilot study of the comparative safety and efficacy of transendocardial injection of autologous mesenchymal stem cell vs. allogeneic mesenchymal stem cells in patients with non-ischemic dilated cardiomyopathy. J Cardiovasc Transl Res 2014;7:769–780.
15. Savvatis K, van Linthout S, Miteva K et al. Mesenchymal stromal cells but not cardiac fibroblasts exert beneficial systemic immunomodulatory effects in experimental myocarditis. PLoS One 2012;7:e41047.
16. Van Linthout S, Savvatis K, Miteva K et al. Mesenchymal stem cells improve murine acute coxsackievirus B3-induced myocarditis. Eur Heart J 2011;32:2168–2178.
17. Maekawa Y, Anzai T, Yoshikawa T et al. Prognostic significance of peripheral monocytosis after reperfused acute myocardial infarction: A possible role for left ventricular remodeling. J Am Coll Cardiol 2002;39:241–246.
18. Binger T, Stich S, Andreas K et al. Migration potential and gene expression profile of human mesenchymal stem cells induced by CCL25. Exp Cell Res 2009;315:1468–1479.
19. Dutta P, Hoyer FF, Grigoryeva LS et al. Macrophages retain hematopoietic stem cells in the spleen via VCAM-1. J Exp Med 2015; 212:497–512.
20. Lee JH, Wang C, Kim CH. FoxP31 regulatory T cells restrain splenic extramedullary myelopoiesis via suppression of hemopoietic cytokine-producing T cells. J Immunol 2009; 183:6377–6386.
21. Shen Y, Xu W, Chu YW et al. Coxsackievirus group B type 3 infection upregulates expression of monocyte chemoattractant protein 1 in cardiac myocytes, which leads to enhanced migration of mononuclear cells in viral myocarditis. J Virol 2004;78:12548–12556.
22. Ghigo A, Franco I, Morello F et al. Myo-cyte signalling in leucocyte recruitment to the heart. Cardiovasc Res 2014;102:270–280.
23. Mestas J, Ley K. Monocyte-endothelial cell interactions in the development of atherosclerosis. Trends Cardiovasc Med 2008;18: 228–232.
24. Serbina NV, Jia T, Hohl TM et al. Mono-cyte-mediated defense against microbial pathogens. Annu Rev Immunol 2008;26:421–452.
25. Barbalat R, Lau L, Locksley RM et al. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat Immunol 2009;10:1200–1207.
26. Grainger JR, Wohlfert EA, Fuss IJ, et al. Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med 2013;19:713–721.
27. Dunay IR, Damatta RA, Fux B et al. Gr1(1) inflammatory monocytes are required for mucosal resistance to the pathogen Toxo-plasma gondii. Immunity 2008;29:306–317.
28. Mason JW, O’Connell JB, Herskowitz A et al. A clinical trial of immunosuppressive therapy for myocarditis. The Myocarditis Treatment Trial Investigators. N Engl J Med 1995;333:269–275.
29. Hahn EA, Hartz VL, Moon TE et al. The Myocarditis Treatment Trial: Design, methods and patients enrollment. Eur Heart J 1995; 16(suppl O):162–167.
30. Parrillo JE, Cunnion RE, Epstein SE et al. A prospective, randomized, controlled trial of prednisone for dilated cardiomyopathy. N Engl J Med 1989;321:1061–1068.
31. Tschope C, Miteva K, Schultheiss HP et al. Mesenchymal stromal cells: A promising cell source for the treatment of inflammatory cardiomyopathy. Curr Pharm Des 2011;17: 3295–3307.
32. Zhao F, Zhang YF, Liu YG et al. Therapeutic effects of bone marrow-derived mesenchymal stem cells engraftment on bleomycin-induced lung injury in rats. Transplant Proc 2008;40:1700–1705.
33. von Bahr L, Batsis I, Moll G et al. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells 2012;30:1575–1578.
34. Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: Immune evasive, not immune privileged. Nat Biotechnol 2014;32:252–260.
35. Maumus M, Jorgensen C, Noel D. Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: Role of secretome and exosomes. Biochimie 2013;95: 2229–2234.
36. Ren G, Zhang G, Zhao X et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008;2:141–150.
37. Ma S, Xie N, Li W et al. Immunobiology of mesenchymal stem cells. Cell Death Differ 2014;21:216–225.
38. Benvenuto F, Voci V, Carminati E et al. Human mesenchymal stem cells target adhesion molecules and receptors involved in T cell extravasation. Stem Cell Res Ther 2015;6: 245.
39. Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: Biological aspects and clinical applications. J Immunol Res 2015;2015:394917.
40. Du Rocher B, Mencalha AL, Gomes BE et al. Mesenchymal stromal cells impair the differentiation of CD14(11) CD16(-) CD64(1) classical monocytes into CD14(11) CD16(1) CD64(11) activate monocytes. Cytotherapy 2012;14:12–25.
41. Chen PM, Liu KJ, Hsu PJ et al. Induction of immunomodulatory monocytes by human mesenchymal stem cell-derived hepatocyte growth factor through ERK1/2. J Leukoc Biol 2014;96:295–303.
42. Dutta P, Nahrendorf M. Regulation and consequences of monocytosis. Immunol Rev 2014;262:167–178.
43. Frantz S, Hofmann U, Fraccarollo D et al. Monocytes/macrophages prevent healing defects and left ventricular thrombus formation after myocardial infarction. FASEB J 2013;27:871–881.
44. Panizzi P, Swirski FK, Figueiredo JL et al. Impaired infarct healing in atherosclerotic mice with Ly-6C(hi) monocytosis. J Am Coll Cardiol 2010;55:1629–1638.
45. Swirski FK, Libby P, Aikawa E et al. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007;117:195–205.
46. Auffray C, Fogg D, Garfa M et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007;317:666–670.
47. Henke A, Spengler HP, Stelzner A et al. Lipopolysaccharide suppresses cytokine release from coxsackie virus-infected human monocytes. Res Immunol 1992;143:65–70.
48. Yu JZ, Wilson JE, Wood SM et al. Secondary heterotypic versus homotypic infection by Coxsackie B group viruses: Impact on early and late histopathological lesions and virus genome prominence. Cardiovasc Pathol 1999; 8:93–102.
49. Terry RL, Getts DR, Deffrasnes C et al. Inflammatory monocytes and the pathogenesis of viral encephalitis. J Neuroinflammation 2012;9:270.
50. Penn MS, Pastore J, Miller T et al. SDF-1 in myocardial repair. Gene Ther 2012;19:583–587.
51. Krieger JR, Ogle ME, McFaline-Figueroa J et al. Spatially localized recruitment of anti-inflammatory monocytes by SDF-1alpha-releasing hydrogels enhances microvascular network remodeling. Biomaterials 2016;77: 280–290.
52. Marchant DJ, Boyd JH, Lin DC et al. Inflammation in myocardial diseases. Circ Res 2012;110:126–144.