Nanotubular crosstalk with distressed cardiomyocytes stimulates the paracrine repair function of mesenchymal stem cells

Stem Cells

Volumn 32, Issue 1, 2014, Pages 216-230

  Figeac, Florence ^a,d   Lesault, Pierre François ^a,b,d   Le Coz, Olivier ^a,d   Damy, Thibaud ^a,b,d   Souktani, Richard ^a,d   Trebeau, Celine ^a,d   Schmitt, Alain ^c,e,f   Ribot, Jonathan ^a,d   Mounier, Remi ^c   Guguin, Aurélie ^a,d   Manier, Celine ^a,b,d   Surenaud, Mathieu ^a,b,d   Hittinger, Luc ^a,d   Dubois Rande, Jean Luc ^a,b,d   Rodriguez, Anne Marie ^a,d  

^a INSERM U955   (France)

^b HENRI MONDOR HOSPITAL   (France)

^c INSTITUT COCHIN   (France)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cell therapy; Mesenchymal stem cells; Myocardial infarction; Stem paracrine function; Tunneling nanotubes

Indexed keywords

LATRUNCULIN A; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; NANOTUBE; NOCODAZOLE; STROMAL CELL DERIVED FACTOR 1ALPHA; STROMELYSIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL COMMUNICATION; CELL DENSITY; CELL MIGRATION; CELL REGENERATION; CELL THERAPY; CHEMOTAXIS; COCULTURE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; GAP JUNCTION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

CELL THERAPY; MESENCHYMAL STEM CELLS; MYOCARDIAL INFARCTION; STEM PARACRINE FUNCTION; TUNNELING NANOTUBES;

ANIMALS; CELL COMPARTMENTATION; COCULTURE TECHNIQUES; HUMANS; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NANOTUBES; PARACRINE COMMUNICATION;

EID: 84889098431     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1560     Document Type: Article

References (58)

1. Shake JG, Gruber PJ, Baumgartner WA et al. Mesenchymal stem cell implantation in a swine myocardial infarct model: Engraftment and functional effects. Ann Thorac Surg 2002;73:1919-1925, discussion 1926.
2. Zeng L, Hu Q, Wang X et al. Bioenergetic and functional consequences of bone marrow-derived multipotent progenitor cell transplantation in hearts with postinfarction left ventricular remodeling. Circulation 2007; 115:1866-1875.
3. Zimmet JM, Hare JM. Emerging role for bone marrow derived mesenchymal stem cells in myocardial regenerative therapy. Basic Res Cardiol 2005;100:471-481.
4. Gnecchi M, He H, Liang OD et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 2005;11:367-368.
5. Huang M, Nguyen P, Jia F et al. Double knockdown of prolyl hydroxylase and factorinhibiting hypoxia-inducible factor with nonviral minicircle gene therapy enhances stem cell mobilization and angiogenesis after myocardial infarction. Circulation 2011;124:S46-S54.
6. Uemura R, Xu M, Ahmad N et al. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 2006;98:1414-1421.
7. Vrijsen KR, Chamuleau SA, Noort WA et al. Stem cell therapy for end-stage heart failure: Indispensable role for the cell? Curr Opin Organ Transplant 2009;14:560-565.
8. Ranganath SH, Levy O, Inamdar MS et al. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012;10:244-258.
9. Hosoda T, Zheng H, Cabral-da-Silva M et al. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation 2011;123:1287-1296.
10. Hristov M, Erl W, Linder S et al. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004;104:2761-2766.
11. Li F, Huang Q, Chen J et al. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci Signal 2010;3:ra13.
12. Wang Y, Cui J, Sun X et al. Tunnelingnanotube development in astrocytes depends on p53 activation. Cell Death Differ 2011;18: 732-742.
13. Yasuda K, Khandare A, Burianovskyy L et al. Tunneling nanotubes mediate rescue of prematurely senescent endothelial cells by endothelial progenitors: Exchange of lysosomal pool. Aging (Albany, Ny) 2011;3:597-608.
14. Acquistapace A, Bru T, Lesault PF et al. Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitorlike state through partial cell fusion and mitochondria transfer. Stem Cells 2011;29: 812-824.
15. Koyanagi M, Brandes RP, Haendeler J et al. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: A novel mechanism for cell fate changes? Circ Res 2005;96:1039-1041.
16. Plotnikov EY, Khryapenkova TG, Vasileva AK et al. Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture. J Cell Mol Med 2008;12:1622-1631.
17. Webster KA. Mitochondrial membrane permeabilization and cell death during myocardial infarction: Roles of calcium and reactive oxygen species. Future Cardiol 2012;8: 863-884.
18. Kung G, Konstantinidis K, Kitsis RN. Programmed necrosis, not apoptosis, in the heart. Circ Res 2011;108:1017-1036.
19. Rodriguez AM, Pisani D, Dechesne CA et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 2005;201: 1397-1405.
20. Okabe M, Ikawa M, Kominami K et al. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-319.
21. Mitra R, Morad M. A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol 1985;249:H1056-1060.
22. Burger D, Lei M, Geoghegan-Morphet N et al. Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res 2006;72:51-59.
23. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
24. Scorsin M, Hagege A, Vilquin JT et al. Comparison of the effects of fetal cardiomyocyte and skeletal myoblast transplantation on postinfarction left ventricular function. J Thorac Cardiovasc Surg 2000;119:1169-1175.
25. Vandervelde S, van Luyn MJ, Tio RA et al. Signaling factors in stem cell-mediated repair of infarcted myocardium. J Mol Cell Cardiol 2005;39:363-376.
26. Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res 2011;109:923-940.
27. Wollert KC, Drexler H. Cell therapy for the treatment of coronary heart disease: A critical appraisal. Nat Rev Cardiol 2010;7: 204-215.
28. Sambrano GR, Fraser I, Han H et al. Navigating the signalling network in mouse cardiac myocytes. Nature 2002;420:712-714.
29. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084.
30. Liu CH, Hwang SM. Cytokine interactions in mesenchymal stem cells from cord blood. Cytokine 2005;32:270-279.
31. Sadat S, Gehmert S, Song YH et al. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun 2007;363:674-679.
32. Kocher AA, Schuster MD, Bonaros N et al. Myocardial homing and neovascularization by human bone marrow angioblasts is regulated by IL-8/Gro CXC chemokines. J Mol Cell Cardiol 2006;40:455-464.
33. Kinnaird T, Stabile E, Burnett MS et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004;94:678-685.
34. Niu J, Kolattukudy PE. Role of MCP-1 in cardiovascular disease: Molecular mechanisms and clinical implications. Clin Sci (Lond) 2009;117:95-109.
35. Kelly D, Khan S, Cockerill G et al. Circulating stromelysin-1 (MMP-3): A novel predictor of LV dysfunction, remodelling and allcause mortality after acute myocardial infarction. Eur J Heart Failure 2008;10:133-139.
36. Cselenyak A, Pankotai E, Horvath EM et al. Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biol 2010;11:29.
37. Yoon J, Shim WJ, Ro YM et al. Transdifferentiation of mesenchymal stem cells into cardiomyocytes by direct cell-to-cell contact with neonatal cardiomyocyte but not adult cardiomyocytes. Ann Hematol 2005;84:715-721.
38. Rose RA, Jiang H, Wang X et al. Bone marrow-derived mesenchymal stromal cells express cardiac-specific markers, retain the stromal phenotype, and do not become functional cardiomyocytes in vitro. Stem Cells 2008;26:2884-2892.
39. Nishiyama N, Miyoshi S, Hida N et al. The significant cardiomyogenic potential of human umbilical cord blood-derived mesenchymal stem cells in vitro. Stem Cells 2007; 25:2017-2024.
40. Gallo MP, Ramella R, Alloatti G et al. Limited plasticity of mesenchymal stem cells cocultured with adult cardiomyocytes. J Cell Biochem 2007;100:86-99.
41. He K, Shi X, Zhang X et al. Long-distance intercellular connectivity between cardiomyocytes and cardiofibroblasts mediated by membrane nanotubes. Cardiovasc Res 2011; 92:39-47.
42. Lai RC, Arslan F, Tan SS et al. Derivation and characterization of human fetal MSCs: An alternative cell source for large-scale production of cardioprotective microparticles. J Mol Cell Cardiol 2010;48:1215-1224.
43. Burghoff S, Ding Z, Godecke S et al. Horizontal gene transfer from human endothelial cells to rat cardiomyocytes after intracoronary transplantation. Cardiovasc Res 2008;77: 534-543.
44. Camussi G, Deregibus MC, Bruno S et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78:838-848.
45. Tomita S, Mickle DA, Weisel RD et al. Improved heart function with myogenesis and angiogenesis after autologous porcine bone marrow stromal cell transplantation. J Thorac Cardiovasc Surg 2002;123:1132-1140.
46. Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701-705.
47. Tatsumi K, Otani H, Sato D et al. Granulocyte-colony stimulating factor increases donor mesenchymal stem cells in bone marrow and their mobilization into peripheral circulation but does not repair dystrophic heart after bone marrow transplantation. Circ J 2008;72:1351-1358.
48. Schuleri KH, Feigenbaum GS, Centola M et al. Autologous mesenchymal stem cells produce reverse remodelling in chronic ischaemic cardiomyopathy. Eur Heart J 2009; 30:2722-2732.
49. Grinnemo KH, Mansson-Broberg A, Leblanc K et al. Human mesenchymal stem cells do not differentiate into cardiomyocytes in a cardiac ischemic xenomodel. Ann Med 2006;38:144-153.
50. Flynn A, Chen X, O'Connell E et al. A comparison of the efficacy of transplantation of bone marrow-derived mesenchymal stem cells and unrestricted somatic stem cells on outcome after acute myocardial infarction. Stem Cell Res Ther 2012;3:36.
51. Dayan V, Yannarelli G, Filomeno P et al. Human mesenchymal stromal cells improve scar thickness without enhancing cardiac function in a chronic ischaemic heart failure model. Interact Cardiovasc Thorac Surg 2012; 14:516-520.
52. Bartunek J, Croissant JD, Wijns W et al. Pretreatment of adult bone marrow mesenchymal stem cells with cardiomyogenic growth factors and repair of the chronically infarcted myocardium. Am J Physiol Heart Circ Physiol 2007;292:H1095-H1104.
53. Gaebel R, Furlani D, Sorg H et al. Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. Plos One 2011;6: e15652.
54. Toma C, Pittenger MF, Cahill KS et al. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002;105:93-98.
55. Shinmura D, Togashi I, Miyoshi S et al. Pretreatment of human mesenchymal stem cells with pioglitazone improved efficiency of cardiomyogenic transdifferentiation and cardiac function. Stem Cells 2012;29:357-366.
56. Otto Beitnes J, Oie E, Shahdadfar A et al. Intramyocardial injections of human mesenchymal stem cells following acute myocardial infarction modulate scar formation and improve left ventricular function. Cell Transplant 2012;21:1697-1709.
57. Kim SW, Lee DW, Yu LH et al. Mesenchymal stem cells overexpressing GCP-2 improve heart function through enhanced angiogenic properties in a myocardial infarction model. Cardiovasc Res 2012;95:495-506.
58. Grinnemo KH, Mansson A, Dellgren G et al. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J Thorac Cardiovasc Surg 2004;127:1293-1300.