Preconditioning of skeletal myoblast-based engineered tissue constructs enables functional coupling to myocardium in vivo

Journal of Thoracic and Cardiovascular Surgery

Volumn 149, Issue 1, 2015, Pages 348-356

  Treskes, Philipp ^a   Neef, Klaus ^a   Srinivasan, Sureshkumar Perumal ^a   Halbach, Marcel ^a   Stamm, Christof ^b   Cowan, Douglas ^c   Scherner, Maximilian ^a   Madershahian, Navid ^a   Wittwer, Thorsten ^a   Hescheler, Jürgen ^a   Wahlers, Thorsten ^a   Choi, Yeong Hoon ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Berlin Brandenburg Center for Regenerative Therapies   (Germany)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; HEPTANOL; BIOLOGICAL MARKER; GJA1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL COMMUNICATION; CELL TRANSPLANTATION; FLOW CYTOMETRY; HEART ELECTROPHYSIOLOGY; HEART MUSCLE; HISTOLOGY; IN VIVO STUDY; MOUSE; MYOBLAST; NERVE BLOCK; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKELETAL MYOBLAST TRANSPLANTATION; TISSUE ENGINEERING; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL SURVIVAL; CHROMOSOME; CULTURE TECHNIQUE; EXCITATION CONTRACTION COUPLING; FEMALE; HEART CONTRACTION; HEART MUSCLE CELL; MECHANICAL STRESS; METABOLISM; PROCEDURES; TIME; TRANSPLANTATION; Y CHROMOSOME;

ACTION POTENTIALS; ANIMALS; BIOMARKERS; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOMES, MAMMALIAN; CONNEXIN 43; EXCITATION CONTRACTION COUPLING; FEMALE; MICE, INBRED C57BL; MYOBLASTS, SKELETAL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; STRESS, MECHANICAL; TIME FACTORS; TISSUE ENGINEERING; Y CHROMOSOME;

EID: 84922287191     PISSN: 00225223     EISSN: 1097685X     Source Type: Journal    
DOI: 10.1016/j.jtcvs.2014.09.034     Document Type: Article

References (34)

1. Finegold JA, Asaria P, Francis DP. Mortality from ischaemic heart disease by country, region, and age: Statistics from World Health Organisation and United Nations. Int J Cardiol. 2013;168:934-45.
2. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, et al. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med. 2001;344:1750-7.
3. Dimmeler S, Leri A. Aging and disease as modifiers of efficacy of cell therapy. Circ Res. 2008;102:1319-30.
4. Menasche P, Hagege AA, Vilquin J-T, Desnos M, Abergel E, Pouzet B, et al. Autologous skeletal myoblast transplantation for severe postinfarction left ventricular dysfunction. J Am Coll Cardiol. 2003;41:1078-83.
5. Jennings RB, Reimer KA. Lethal myocardial ischemic injury. Am J Pathol. 1981; 102:241-55.
6. Scorsin M, Hagege A, Vilquin JT, Fiszman M, Marotte F, Samuel JL, et al. Comparison of the effects of fetal cardiomyocyte and skeletal myoblast transplantation on postinfarction left ventricular function. J Thorac Cardiovasc Surg. 2000;119:1169-75.
7. Menasche P, Hagege AA, Scorsin M, Pouzet B, Desnos M, Duboc D, et al. Myoblast transplantation for heart failure. Lancet. 2001;357:279-80.
8. Steendijk P, Smits PC, Valgimigli M, van der Giessen WJ, Onderwater EE, Serruys PW. Intramyocardial injection of skeletal myoblasts: long-term follow-up with pressure-volume loops. Nat Clin Pract Cardiovasc Med. 2006; 3(Suppl 1):S94-100.
9. Siminiak T, Kalawski R, Fiszer D, Jerzykowska O, Rzezniczak J, Rozwadowska N, et al. Autologous skeletal myoblast transplantation for the treatment of postinfarction myocardial injury: phase I clinical study with 12 months of follow-up. Am Heart J. 2004;148:531-7.
10. Hagege AA, Marolleau J-P, Vilquin J-T, Alheritiere A, Peyrard S, Duboc D, et al. Skeletal myoblast transplantation in ischemic heart failure: long-term follow-up of the first phase I cohort of patients. Circulation. 2006;114:108-13.
11. Roell W, Lewalter T, Sasse P, Tallini YN, Choi B-R, Breitbach M, et al. Engraftment of connexin 43-expressing cells prevents post-infarct arrhythmia. Nature. 2007;450:819-24.
12. Suzuki K, Brand NJ, Allen S, Khan MA, Farrell AO, Murtuza B, et al. Overexpression of connexin 43 in skeletal myoblasts: relevance to cell transplantation to the heart. J Thorac Cardiovasc Surg. 2001;122:759-66.
13. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B, et al. Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation. 2005;111:2198-202.
14. Muller-Ehmsen J, Krausgrill B, Burst V, Schenk K, Neisen UC, Fries JW, et al. Effective engraftment but poor mid-term persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. J Mol Cell Cardiol. 2006;41:876-84.
15. Hamdi H, Furuta A, Bellamy V, Bel A, Puymirat E, Peyrard S, et al. Cell delivery: intramyocardial injections or epicardial deposition? A head-to-head comparison. Ann Thorac Surg. 2009;87:1196-203.
16. Siepe M, Giraud MN, Pavlovic M, Receputo C, Beyersdorf F, Menasche P, et al. Myoblast-seeded biodegradable scaffolds to prevent post-myocardial infarction evolution toward heart failure. J Thorac Cardiovasc Surg. 2006;132: 124-31.
17. Christman KL, Lee RJ. Biomaterials for the treatment of myocardial infarction. J Am Coll Cardiol. 2006;48:907-13.
18. Perumal Srinivasan S, Neef K, Treskes P, Liakopoulos OJ, Stamm C, Cowan DB, et al. Enhanced gap junction expression in myoblast-containing engineered tissue. Biochem Biophys Res Commun. 2012;422:462-8.
19. Neef K, Choi YH, Perumal Srinivasan S, Treskes P, Cowan DB, Stamm C, et al. Mechanical preconditioning enables electrophysiologic coupling of skeletal myoblast cells to myocardium. J Thorac Cardiovasc Surg. 2012;144: 1176-84.e1.
20. Halbach M, Pillekamp F, Brockmeier K, Hescheler J, Muller-Ehmsen J, Reppel M. Ventricular slices of adult mouse hearts-a new multicellular in vitro model for electrophysiological studies. Cell Physiol Biochem. 2006;18:1-8.
21. Choi YH, Stamm C, Hammer PE, Kwaku KF, Marler JJ, Friehs I, et al. Cardiac conduction through engineered tissue. Am J Pathol. 2006;169:72-85.
22. Drey F, Choi YH, Neef K, Ewert B, Tenbrock A, Treskes P, et al. Noninvasive in vivo tracking of mesenchymal stem cells and evaluation of cell therapeutic effects in a murine model using a clinical 3.0 T MRI. Cell Transplant. 2013; 22:1971-80.
23. Lambert JF, Benoit BO, Colvin GA, Carlson J, Delville Y, Quesenberry PJ. Quick sex determination of mouse fetuses. J Neurosci Methods. 2000;95: 127-32.
24. Li H, Choudhary SK, Milner DJ, Munir MI, Kuisk IR, Capetanaki Y. Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators Myo D and myogenin. J Cell Biol. 1994;124:827-41.
25. Matsumura K, Tome FM, Collin H, Leturcq F, Jeanpierre M, Kaplan JC, et al. Expression of dystrophin-associated proteins in dystrophin-positive muscle fibers (revertants) in Duchenne muscular dystrophy. Neuromuscul Disord. 1994;4:115-20.
26. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, et al. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin 43. Circ Res. 2001;88:333-9.
27. Fromaget C, el Aoumari A, Gros D. Distribution pattern of connexin 43, a gap junctional protein, during the differentiation of mouse heart myocytes. Differentiation. 1992;51:9-20.
28. Davis LM, Saffitz JE, Beyer EC. Modulation of connexin 43 expression: effects on cellular coupling. J Cardiovasc Electrophysiol. 1995;6:103-14.
29. Gepstein L, Ding C, Rahmutula D, Wilson EE, Yankelson L, Caspi O, et al. In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells. 2010;28: 2151-61.
30. Chang MG, Tung L, Sekar RB, Chang CY, Cysyk J, Dong P, et al. Proarrhythmic potential of mesenchymal stem cell transplantation revealed in an in vitro coculture model. Circulation. 2006;113:1832-41.
31. Halbach M, Pfannkuche K, Pillekamp F, Ziomka A, Hannes T, Reppel M, et al. Electrophysiological maturation and integration of murine fetal cardiomyocytes after transplantation. Circ Res. 2007;101:484-92.
32. Kramer K, van Acker SA, Voss HP, Grimbergen JA, van der Vijgh WJ, Bast A. Use of telemetry to record electrocardiogram and heart rate in freely moving mice. J Pharmacol Toxicol Methods. 1993;30:209-15.
33. Takens-Kwak BR, Jongsma HJ, Rook MB, Van Ginneken AC. Mechanism of heptanol-induced uncoupling of cardiac gap junctions: a perforated patch-clamp study. Am J Physiol. 1992;262:C1531-8.
34. Fernandes S, van Rijen HV, Forest V, Evain S, Leblond AL, Merot J, et al. Cardiac cell therapy: overexpression of connexin 43 in skeletal myoblasts and prevention of ventricular arrhythmias. J Cell Mol Med. 2009;13:3703-12.