Bone Marrow-Derived Mesenchymal Stem Cells Have Innate Procoagulant Activity and Cause Microvascular Obstruction Following Intracoronary Delivery: Amelioration by Antithrombin Therapy

Stem Cells

Volumn 33, Issue 9, 2015, Pages 2726-2737

  Gleeson, Birgitta M ^a   Martin, Kenneth ^a   Ali, Mohammed T ^a   Kumar, Arun H S ^a   Pillai, M Gopala Krishnan ^a   Kumar, Sujith P G ^a   O'Sullivan, John F ^a   Whelan, Derek ^a   Stocca, Alessia ^a   Khider, Wisam ^a   Barry, Frank P ^b   O'Brien, Timothy ^b   Caplice, Noel M ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Coronary flow reserve; Heparin; Mesenchymal stem cells; Myocardial infarction; Tissue factor

Indexed keywords

COLLAGEN; HEPARIN; PROCOAGULANT; THROMBIN; THROMBOPLASTIN; FIBRINOLYTIC AGENT;

ACUTE HEART INFARCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD CLOTTING; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CONTROLLED STUDY; CORONARY FLOW RESERVE; FEMALE; FIBROBLAST; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE VOLUME; HEART LEFT VENTRICLE WALL MOTION; HEART MUSCLE PERFUSION; HISTOLOGY; IN VITRO STUDY; INNATE IMMUNITY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SCAR FORMATION; THROMBOCYTE; THROMBUS; TISSUE ENGINEERING; ADVERSE EFFECTS; ANIMAL; BONE MARROW; CELL CULTURE; CORONARY BLOOD VESSEL; DRUG EFFECTS; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; MICROVASCULATURE; MYOCARDIAL INFARCTION; PATHOLOGY; PHYSIOLOGY; PIG; PROCEDURES;

SUS;

ANIMALS; BLOOD COAGULATION; BONE MARROW; CELLS, CULTURED; CORONARY VESSELS; FEMALE; FIBRINOLYTIC AGENTS; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICROVESSELS; MYOCARDIAL INFARCTION; SWINE; THROMBOPLASTIN;

EID: 84939788568     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2050     Document Type: Article

References (43)

1. Amado LC, Saliaris AP, Schuleri KH, et al., Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci USA 2005; 102: 11474-11479.
2. Quevedo HC, Hatzistergos KE, Oskouei BN, et al., Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009; 106: 14022-14027.
3. Poncelet AJ, Hiel AL, Vercruysse J, et al., Intracardiac allogeneic mesenchymal stem cell transplantation elicits neo-angiogenesis in a fully immunocompetent ischaemic swine model. Eur J Cardiothorac Surg 2010; 38: 781-787.
4. He AN, Jiang Y, Gui C, et al., The antiapoptotic effect of mesenchymal stem cell transplantation on ischemic myocardium is enhanced by anoxic preconditioning. Can J Cardiol 2009; 25: 353-358.
5. Hatzistergos KE, Quevedo H, Oskouei BN, et al., Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res 2010; 107: 913-922.
6. 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.
7. Dayan V, Yannarelli G, Billia F, et al., Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction. Basic Res Cardiol 2011; 106: 1299-1310.
8. Aggarwal S, Pittenger MF,. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105: 1815-1822.
9. Wigren M, Bjorkbacka H, Andersson L, et al., Low levels of circulating CD4+FoxP3+ T cells are associated with an increased risk for development of myocardial infarction but not for stroke. Arterioscler Thromb Vasc Biol 2012; 32: 2000-2004.
10. Hare JM, Fishman JE, Gerstenblith G, et al., Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: The POSEIDON randomized trial. JAMA 2012; 308: 2369-2379.
11. 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 (PROMETHEUS) Trial. Circ Res 2014; 114: 1302-1310.
12. Furlani D, Ugurlucan M, Ong L, et al., Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc Res 2009; 77: 370-376.
13. Vulliet PR, Greeley M, Halloran SM, et al., Intra-coronary arterial injection of mesenchymal stromal cells and microinfarction in dogs. Lancet 2004; 363: 783-784.
14. Tatsumi K, Ohashi K, Matsubara Y, et al., Tissue factor triggers procoagulation in transplanted mesenchymal stem cells leading to thromboembolism. Biochem Biophys Res Commun 2013; 431: 203-209.
15. Mylotte LA, Duffy AM, Murphy M, et al., Metabolic flexibility permits mesenchymal stem cell survival in an ischemic environment. Stem Cells 2008; 26: 1325-1336.
16. Weir C, Morel-Kopp M-C, Gill A, et al., Mesenchymal stem cells: Isolation, characterisation and in vivo fluorescent dye tracking. Heart Lung Circ 2008; 17: 395-403.
17. Metharom P, Martin K, Kumar A, et al., Pleiotropic role for monocyte C-fms protein in response to vascular injury: Potential therapeutic target. Atherosclerosis 2011; 216: 74-82.
18. Doyle B, Sorajja P, Hynes B, et al., Progenitor cell therapy in a porcine acute myocardial infarction model induces cardiac hypertrophy, mediated by paracrine secretion of cardiotrophic factors including TGFbeta1. Stem Cells Dev 2008; 17: 941-951.
19. Klein HH, Schubothe M, Nebendahl K, et al., Temporal and spatial development of infarcts in porcine hearts. Basic Res Cardiol 1984; 79: 440-447.
20. Kondo K, Shibata R, Unno K, et al., Impact of a single intracoronary administration of adiponectin on myocardial ischemia/reperfusion injury in a pig model. Circ Cardiovasc Interv 2010; 3: 166-173.
21. O'Sullivan JF, Leblond AL, Kelly G, et al., Potent long-term cardioprotective effects of single low-dose insulin-like growth factor-1 treatment postmyocardial infarction. Circ Cardiovasc Interv 2011; 4: 327-335.
22. Whittaker P, Kloner RA, Boughner DR, et al., Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light. Basic Res Cardiol 1994; 89: 397-410.
23. Savage B, Almus-Jacobs F, Ruggeri ZM,. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 1998; 94: 657-666.
24. Lim SY, Kim YS, Ahn Y, et al., The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model. Cardiovasc Res 2006; 70: 530-542.
25. Stephenne X, Nicastro E, Eeckhoudt S, et al., Bivalirudin in combination with heparin to control mesenchymal cell procoagulant activity. PLoS One 2012; 7: e42819.
26. Rao LV, Rapaport SI,. Activation of factor VII bound to tissue factor: A key early step in the tissue factor pathway of blood coagulation. Proc Natl Acad Sci USA 1988; 85: 6687-6691.
27. Andrade-Gordon P, Derian CK, Maryanoff BE, et al., Administration of a potent antagonist of protease-activated receptor-1 (PAR-1) attenuates vascular restenosis following balloon angioplasty in rats. J Pharmacol Exp Ther 2001; 298: 34-42.
28. Freyman T, Polin G, Osman H, et al., A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J 2006; 27: 1114-1122.
29. Orn S, Manhenke C, Greve OJ, et al., Microvascular obstruction is a major determinant of infarct healing and subsequent left ventricular remodelling following primary percutaneous coronary intervention. Eur Heart J 2009; 30: 1978-1985.
30. Murthy VL, Naya M, Foster CR, et al., Association between coronary vascular dysfunction and cardiac mortality in patients with and without diabetes mellitus. Circulation 2012; 126: 1858-1868.
31. Bonderman D, Teml A, Jakowitsch J, et al., Coronary no-reflow is caused by shedding of active tissue factor from dissected atherosclerotic plaque. Blood 2002; 99: 2794-2800.
32. Rao SV, Ohman EM,. Anticoagulant therapy for percutaneous coronary intervention. Circ Cardiovasc Interven 2010; 3: 80-88.
33. Houtgraaf JH, de Jong R, Kazemi K, et al., Intracoronary infusion of allogeneic mesenchymal precursor cells directly following experimental acute myocardial infarction reduces infarct size, abrogates adverse remodeling and improves cardiac function. Circ Res 2013; 113: 153-166.
34. Seeger FH, Rasper T, Fischer A, et al., Heparin disrupts the CXCR4/SDF-1 axis and impairs the functional capacity of bone marrow-derived mononuclear cells used for cardiovascular repair. Circ Res 2012; 111: 854-862.
35. Uygun BE, Stojsih SE, Matthew HW,. Effects of immobilized glycosaminoglycans on the proliferation and differentiation of mesenchymal stem cells. Tissue Eng Part A. 2009; 15: 3499-3512.
36. Wehner R, Taubert C, Mende T, et al., Engineered extracellular matrix components do not alter the immunomodulatory properties of mesenchymal stromal cells in vitro. J Tissue Eng Regen Med 2012.
37. Petitou M, Casu B, Lindahl U,. 1976-1983, a critical period in the history of heparin: The discovery of the antithrombin binding site. Biochimie 2003; 85: 83-89.
38. Maraveyas A, Ettelaie C, Echrish H, et al., Weight-adjusted dalteparin for prevention of vascular thromboembolism in advanced pancreatic cancer patients decreases serum tissue factor and serum-mediated induction of cancer cell invasion. Blood Coagul Fibrinolysis 2010; 21: 452-458.
39. Ettelaie C, Fountain D, Collier MEW, et al., Low molecular weight heparin downregulates tissue factor expression and activity by modulating growth factor receptor-mediated induction of nuclear factor-kappa B. Biochim Biophys Acta 2011; 1812: 1591-1600.
40. Bartosh TJ, Ylostalo JH,. Preparation of anti-inflammatory mesenchymal stem/precursor cells (MSCs) through sphere formation using hanging-drop culture technique. Curr Protoc Stem Cell Biol 2014; 28:Unit 2B.6.
41. Karantalis V, Balkan W, Schulman IH, et al., Cell-based therapy for prevention and reversal of myocardial remodeling. Am J Physiol Heart Circ Physiol 2012; 303: H256-H270.
42. Trachtenberg B, Velazquez DL, Williams AR, et al., Rationale and design of the transendocardial injection of autologous human cells (bone marrow or mesenchymal) in chronic ischemic left ventricular dysfunction and heart failure secondary to myocardial infarction (TAC-HFT) trial: A randomized, double-blind, placebo-controlled study of safety and efficacy. Am Heart J 2011; 161: 487-493.
43. Heldman AW, Difede DL, Fishman JE, et al., Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: The TAC-HFT randomized trial. JAMA 2014; 311: 62-73.