Creating the bioartificial myocardium for cardiac repair: Challenges and clinical targets

Expert Review of Cardiovascular Therapy

Volumn 11, Issue 12, 2013, Pages 1701-1711

  Chachques, Juan C ^a   Pradas, Manuel Monleon ^b   Bayes Genis, Antoni ^c   Semino, Carlos ^d  

^a HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^b UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^c HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^d UNIVERSITAT RAMON LLULL   (Spain)

Author keywords

Bioartificial myocardium; Biohybrid scaffolds; Bionanomaterials; Cardiac bioregeneration; Cardiomyoplasty; Cell transplantation; Heart failure; Myocardial infarction; Myocardial regeneration; Tissue engineering

Indexed keywords

AZACITIDINE; CAPROLACTONE METHACRYLOXYL ETHYL ESTER; COLLAGEN TYPE 1; HYALURONIC ACID; NANOFIBER; NANOMATERIAL; POLY(ETHYL ACRYLATE); POLYMER; TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

ARTIFICIAL HEART; BIOARTIFICIAL MYOCARDIUM; BIOPROSTHESIS; CARDIOMYOPLASTY; ELECTRODE; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; ENGRAFTMENT; EXTRACELLULAR MATRIX; HEART DILATATION; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART REPAIR; HEART VENTRICLE REMODELING; HUMAN; IMPEDANCE; ISCHEMIC HEART DISEASE; MESENCHYMAL STEM CELL; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE REPAIR;

ANIMALS; BIOPROSTHESIS; DISEASE PROGRESSION; HEART FAILURE; HEART VENTRICLES; HUMANS; MYOCARDIUM; REGENERATION; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84888046327     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1586/14779072.2013.854165     Document Type: Review

References (64)

1. Chachques JC. Cellular cardiac regenerative therapy in which patients? Expert Rev. Cardiovasc. Ther. 7, 911-919 (2009).
2. Rajnoch C, Chachques JC, Berrebi A, Bruneval P, Benoit MO, Carpentier A. Cellular therapy reverses myocardial dysfunction. J. Thorac. Cardiovasc. Surg. 121, 871-878 (2001).
3. Schussler O, Chachques JC, Mesana TG, Suuronen EJ, Lecarpentier Y, Ruel M. 3-dimensional structures to enhance cell therapy and engineer contractile tissue. Asian Cardiovasc. Thorac. Ann. 18, 188-198 (2010).
4. Spadaccio C, Rainer A, Chachques JC, Covino E, Herreros J, Genovese JA. Stem cells cardiac differentiation in 3D systems. Front. Biosci. (Schol. Ed.) 3901-3918 (2011).
5. Chachques JC. Development of bioartificial myocardium using stem cells and nanobiotechnology templates. Cardiol. Res. Pract. 2011,806795 (2010).
6. Zhang Y, Liang X, Lian Q, Tse HF. Perspective and challenges of mesenchymal stem cells for cardiovascular regeneration. Expert Rev. Cardiovasc. Ther. 11, 505-517 (2013).
7. Christalla P, Hudson JE, Zimmermann WH. The cardiogenic niche as a fundamental building block of engineered myocardium. Cells Tissues Organs. 195, 82-93 (2012).
8. Kensah G, Roa Lara A, Dahlmann J et al. Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. Eur. Heart J. 34, 1134-1346 (2013).
9. Tulloch NL, Muskheli V, Murry CE et al. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 109, 47-59 (2011).
10. Dahlmann J, Krause A, Möller L et al. Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering. Biomaterials 34, 940-951 (2013).
11. Cortes-Morichetti M, Frati G, Schussler O, Van Huyen JP, Carpentier A, Chachques JC. Association between a cell-seeded collagen matrix and cellular cardiomyoplasty for myocardial support and regeneration. Tissue Eng. 13, 2681-2687 (2007).
12. Lilyanna S, Martinez EC, Kofidis T et al. Cord lining-mesenchymal stem cells graft supplemented with an omental flap induces myocardial revascularization and ameliorates cardiac dysfunction in a rat model of chronic ischemic heart failure. Tissue Eng. Part A (Epub ahead of print) (2013).
13. Turner WS, Wang X, Johnson S et al. Cardiac tissue development for delivery of embryonic stem cell-derived endothelial and cardiac cells in natural matrices. J. Biomed. Mater. Res. B Appl. Biomater. 100, 2060-2072 (2012).
14. Habib M, Shapira-Schweitzer K, Gepstein L et al. A combined cell therapy and in-situ tissue-engineering approach for myocardial repair. Biomaterials 32, 7514-7523 (2011).
15. Chachques JC, Trainini JC, Lago N, Cortes-Morichetti M, Schussler O, Carpentier A. Myocardial assistance by grafting a new bioartificial upgraded myocardium (MAGNUM trial): clinical feasibility study. Ann. Thorac. Surg. 85, 901-908 (2008).
16. Shafy A, Fink T, Zachar V, Lila N, Carpentier A, Chachques JC. Development of cardiac support bioprostheses for ventricular restoration and myocardial regeneration. Eur. J. Cardiothorac. Surg. 43, 1211-1219 (2013).
17. Castells-Sala C, Semino CE. Biomaterials for stem cell culture and seeding for the generation and delivery of cardiac myocytes. Curr. Opin. Organ. Transplant. 17, 681-687 (2012).
18. Arnal-Pastor M, Vallés-Lluch A, Keicher M, Pradas MM. Coating typologies and constrained swelling of hyaluronic acid gels within scaffold pores. J. Colloid Interface Sci. 361, 361-369 (2011).
19. Sicari BM, Johnson SA, Badylak S et al. The effect of source animal age upon the in vivo remodeling characteristics of an extracellular matrix scaffold. Biomaterials 33, 5524-5533 (2012).
20. Ott HC, Matthiesen TS, Goh SK et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14, 213-221 (2008).
21. Taylor DA. From stem cells and cadaveric matrix to engineered organs. Curr. Opin. Biotechnol. 20, 598-605 (2009).
22. Song JJ, Ott HC. Organ engineering based on decellularized matrix scaffolds. Trends Mol. Med. 17, 424-432 (2011).
23. Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials 32, 3233-3243 (2011).
24. Mari-Buye N, Semino CE. Differentiation of mouse embryonic stem cells in self-assembling peptide scaffolds. Methods Mol. Biol. 690, 217-237 (2011).
25. Izal I, Aranda P, Sanz-Ramos P et al. Culture of human bone marrow-derived mesenchymal stem cells on of poly(L: -lactic acid) scaffolds: potential application for the tissue engineering of cartilage. Knee Surg. Sports Traumatol. Arthrosc. 21, 1737-1750 (2013).
26. Soler-Botija C, Bagó JR, Bayes-Genis A. A bird's-eye view of cell therapy and tissue engineering for cardiac regeneration. Ann. N. Y. Acad. Sci. 1254, 57-65 (2012).
27. Yan J, Dong L, Zhang B, Qi N. Effects of extremely low-frequency magnetic field on growth and differentiation of human mesenchymal stem cells. Electromagn. Biol. Med. 29, 165-176 (2010).
28. Flaibani M, Boldrin L, Cimetta E, Piccoli M, De Coppi P, Elvassore N. Muscle differentiation and myotubes alignment is influenced by micropatterned surfaces and exogenous electrical stimulation. Tissue Eng. Part A 15, 2447-257 (2009).
29. Michalopoulos E, Knight RL, Korossis S, Kearney JN, Fisher J, Ingham E. Development of methods for studying the differentiation of human mesenchymal stem cells under cyclic compressive strain. Tissue Eng. Part C Methods 18, 252-262 (2012).
30. Schraufstatter IU, Discipio RG, Khaldoyanidi S. Mesenchymal stem cells and their microenvironment. Front. Biosci. 17, 2271-2288 (2011).
31. Ling SK, Wang R, Dai ZQ et al. Pretreatment of rat bone marrow mesenchymal stem cells with a combination of hypergravity and 5-azacytidine enhances therapeutic efficacy for myocardial infarction. Biotechnol. Prog. 27, 473-482 (2011).
32. Haneef K, Lila N, Benadda S, Legrand F, Carpentier A, Chachques JC. Development of bioartificial myocardium by electrostimulation of 3D collagen scaffolds seeded with stem cells. Heart Int. 7, e14 (2012).
33. Shafy A, Lavergne T, Latrémouille C, Cortes-Morichetti M, Carpentier A, Chachques JC. Association of electrostimulation with cell transplantation in ischemic heart disease. J. Thorac. Cardiovasc. Surg. 138, 994-1001 (2009).
34. Genovese JA, Spadaccio C, Chachques E, Schussler O, Carpentier A, Chachques JC. Cardiac pre-differentiation of human mesenchymal stem cells by electrostimulation. Front. Biosci. 14, 2996-3002 (2009).
35. Llucià-Valldeperas A, Sanchez B, Soler-Botija C, Gálvez-Montón C, Prat-Vidal C, Bayes-Genis A. Electrical stimulation of cardiac adipose tissue-derived progenitor cells modulates cell phenotype and genetic machinery. J. Tissue Eng. Regen. Med. (Epub ahead of print) (2013) (doi: 10.1002/term.1710).
36. Schussler O, Coirault C, Louis-Tisserand M et al. Use of Arginine-Glycine-Aspartic acid adhesion peptides coupled with a new collagen scaffold to engineer a myocardium-like tissue graft. Nat. Clin. Pract. Cardiovasc. Med. 6, 240-249 (2009).
37. Chachques JC, Jegaden O, Mesana T, Glock Y, Grandjean PA, Carpentier AF; French Cardiomyoplasty Investigators. Cardiac bioassist: results of the French multicenter cardiomyoplasty study. Asian Cardiovasc. Thorac. Ann. 17, 573-580 (2009).
38. Chachques JC. Cardiomyoplasty: is it still a viable option in patients with end-stage heart failure? Eur. J. Cardiothorac. Surg. 35, 201-203 (2009).
39. Wenk JF, Ge L, Zhang Z, Mojsejenko D, Guccione JM, Ratcliffe MB. Biventricular finite element modeling of the Acorn CorCap Cardiac Support Device on a failing heart. Ann. Thorac. Surg. 95, 2022-2027 (2013).
40. Klodell CT Jr, Aranda JM Jr, McGiffin DC et al. Worldwide surgical experience with the Paracor HeartNet cardiac restraint device. J. Thorac. Cardiovasc. Surg. 135, 188-195 (2008).
41. Torrent-Guasp F, Kocica MJ, Corno AF, Komeda M, Cosin-Aguillar J, Wen H. Towards new understanding of the heart structure and function. Eur. J. Cardiothorac. Surg. 27,191-201 (2005).
42. Buckberg G, Hoffman JI, Nanda NC, Coghlan C, Saleh S, Athanasuleas C. Ventricular torsion and untwisting: further insights into mechanics and timing interdependence: a viewpoint. Echocardiography 28, 782-804 (2011).
43. Houtgraaf JH, den Dekker WK, Fernandez-Aviles F, Zijlsta F, Serruys PW, Duckers HJ. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J. Am. Coll. Cardiol. 59, 539-540 (2012).
44. Díez Villanueva P, Sanz-Ruiz R, Núñez García A, Fernández Santos ME, Sánchez PL, Fernández-Avilés F. Functional multipotency of stem cells: what do we need from them in the heart? Stem Cells Int. 2012,817364 (2012).
45. Zhang D, Shadrin IY, Lam J, Xian HQ, Snodgrass HR, Bursac N. Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34, 5813-5820 (2013).
46. Didié M, Christalla P, Zimmermann WH et al. Parthenogenetic stem cells for tissue-engineered heart repair. J. Clin. Invest. 123, 1285-1298 (2013).
47. Smith RR, Marbán E, Marbán L. Enhancing retention and efficacy of cardiosphere-derived cells administered after myocardial infarction using a hyaluronan-gelatin hydrogel. Biomatter (Epub ahead of print) (2013) (doi: pii: e24490).
48. Chimenti I, Gaetani R, Barile L, Frati G, Messina E, Giacomello A. Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol. Biol. 879, 327-338 (2012).
49. Chugh AR, Beache GM, Loughran JH, Mewton N, Anversa P, Bolli R. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 126 (11 Suppl. 1), S54-S64 (2012).
50. Makkar RR, Smith RR, Marbán E et al. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379, 895-904 (2012).
51. Bath C, Yang S, Muttuvelu D, Fink T, Emmersen J, Vorum H, Hjortdal J, Zachar V. Hypoxia is a key regulator of limbal epithelial stem cell growth and differentiation. Stem Cell Res. 10, 349-360 (2013).
52. Hu X, Yu SP, Fraser JL et al. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J. Thorac. Cardiovasc. Surg. 135, 799-808 (2008).
53. Ferreira RJ, Irioda AC, Cunha RC, Guarita-Souza LC, Chachques JC, de Carvalho KA. Controversies about the chromosomal stability of cultivated mesenchymal stem cells: their clinical use is it safe? Curr. Stem Cell Res. Ther. 7, 356-363 (2012).
54. Chachques JC, Herreros J, Trainini J, Juffe A, Prosper F, Genovese J. Autologous human serum for cell culture avoids the implantation of cardioverter-defibrillators in cellular cardiomyoplasty. Int. J. Cardiol. 95 (Suppl. 1), S29-S33 (2004).
55. Tekkatte C, Gunasingh GP, Cherian KM, Sankaranarayanan K. "Humanized" stem cell culture techniques: the animal serum controversy. Stem Cells Int. 2011, 504723 (2011).
56. Pennisi CP, Zachar V, Fink T, Gurevich L, Fojan P. Patterned polymeric surfaces to study the influence of nanotopography on the growth and differentiation of mesenchymal stem cells. Methods Mol. Biol. 1058, 77-88 (2013).
57. Sawada T, Mihara H, Serizawa T. Peptides as new smart bionanomaterials: molecular-recognition and self-assembly capabilities. Chem. Rec. 13, 172-186 (2013).
58. Laaksonen P, Szilvay GR, Linder MB. Genetic engineering in biomimetic composites. Trends Biotechnol. 30, 191-197 (2012).
59. An J, Chua CK, Yu T, Li H, Tan LP. Advanced nanobiomaterial strategies for the development of organized tissue engineering constructs. Nanomedicine (Lond.) 8, 591-602 (2013).
60. Chachques JC. Bio-hybrid tissue engineering for cellular cardiomyoplasty: future directions. Methods Mol. Biol. 1036, 151-62 (2013).
61. Chachques JC, Bayes-Genis A, Monleon Pradas M, Semino CE, Zur Nieden N, Jenny PH. Bioactive implants for myocardial regeneration and ventricular chamber restoration. WO134957 (2011); EP-2422823-A1; US20130116789.
62. Chachques JC, Leonhardt H: Method of providing a dynamic cellular cardiac support. US7341062 (2008).
63. Chachques JC, Grandjean PA, Smits K. Cardiomyoplasty: method and apparatus including a sliding insulation lead for cardiac assistance. US4735205 (1988).
64. RECATABI PROJECT (Regeneration of Cardiac Tissue Assisted by Bioactive Implants), financially supported by the 7th Framework Programme (FP7) of the European Commission. www.recatabi.com/