A preliminary approach to the repair of myocardial infarction using adipose tissue-derived stem cells encapsulated in magnetic resonance-labelled alginate microspheres in a porcine model

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 84, Issue 1, 2013, Pages 29-39

  Gomez Mauricio, Remedios Guadalupe ^a   Acarregui, Argia ^b,c   Sánchez Margallo, Francisco Miguel ^a   Crisóstomo, Verónica ^a   Gallo, Ignacio ^d   Hernández, Rosa María ^b,c   Pedraz, José Luis ^b,c   Orive, Gorka ^b,c   Martín Cancho, María Fernanda ^a  

^a JESÚS USÓN MINIMALLY INVASIVE SURGERY CENTRE   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^d Policlínica Gipuzkoa ^*  (Spain)

Author keywords

Adipose stem cells; Alginate; Cell encapsulation; Magnetic Resonance Imaging; Magnetocapsules; Myocardial infarction

Indexed keywords

ALGINIC ACID; IRON OXIDE; MICROSPHERE; NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE;

ADIPOSE TISSUE; ADIPOSE TISSUE DERIVED STEM CELL; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ENCAPSULATION; CELL MIGRATION; CELL SURVIVAL; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART OUTPUT; HEART RATE; IN VITRO STUDY; IN VIVO STUDY; MICROCAPSULE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; STEM CELL;

ADIPOSE TISSUE; ALGINATES; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GLUCURONIC ACID; HEXURONIC ACIDS; MAGNETIC RESONANCE IMAGING; MICROSPHERES; MYOCARDIAL INFARCTION; RANDOM ALLOCATION; STEM CELL TRANSPLANTATION; SWINE;

EID: 84876900241     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2012.11.028     Document Type: Article

References (52)

1. Ministerio de Sanidad Y Política Social, Estrategia en Cardiopatía Isquémica del Sistema Nacional de Salud (Actualización aprobada por el Consejo Interterritorial del Sistema Nacional de Salud el 22 de octubre de 2009.) (22 de octubre de 2009).
2. M. Mazo, J.J. Gavira, B. Pelacho, and F. Prosper Adipose-derived stem cells for myocardial infarction J. Cardiovasc. Transl. Res. 4 2011 145 153
3. F. Wang, and J. Guan Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy Adv. Drug Deliv. Rev. 62 2010 784 797
4. J. Lee, and A. Asakura Jianyi Zhang, Experimental cell transplantation for myocardial repair P.A. Iazzo, Handbook of Cardiac Anatomy, Physiology and Devices 2005 Humana Press Inc. Totowa, NJ 427 438
5. S.L. Beeres, D.E. Atsma, J. van Ramshorst, M.J. Schalij, and J.J. Bax Cell therapy for ischaemic heart disease Heart 94 2008 1214 1226
6. D. Choi, K.C. Hwang, K.Y. Lee, and Y.H. Kim Ischemic heart diseases: current treatments and future J. Control. Release 140 2009 194 202
7. R. Sanz-Ruiz, E. Fernandez-Santos, M. Dominguez-Munoa, R. Parma, A. Villa, L. Fernandez, P.L. Sanchez, and F. Fernandez-Aviles Early translation of adipose-derived cell therapy for cardiovascular disease Cell Transplant. 18 2009 245 254
8. C. Valina, K. Pinkernell, Y.H. Song, X. Bai, S. Sadat, R.J. Campeau, T.H. Le Jemtel, and E. Alt Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction Eur. Heart J. 28 2007 2667 2677
9. L. Cai, B.H. Johnstone, T.G. Cook, J. Tan, M.C. Fishbein, P.S. Chen, and K.L. March IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function Stem cells 27 2009 230 237
10. M. Mazo, V. Planat-Benard, G. Abizanda, B. Pelacho, B. Leobon, J.J. Gavira, I. Penuelas, A. Cemborain, L. Penicaud, P. Laharrague, C. Joffre, M. Boisson, M. Ecay, M. Collantes, J. Barba, L. Casteilla, and F. Prosper Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction Eur. J. Heart Fail. 10 2008 454 462
11. Y. Miyahara, N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, H. Hao, K. Ishino, H. Ishida, T. Shimizu, K. Kangawa, S. Sano, T. Okano, S. Kitamura, and H. Mori Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat. Med. 12 2006 459 465
12. M. Rigol, N. Solanes, J. Farre, S. Roura, M. Roque, A. Berruezo, N. Bellera, L. Novensa, D. Tamborero, C. Prat-Vidal, M.A. Huzman, M. Batlle, M. Hoefsloot, M. Sitges, J. Ramirez, A.P. Dantas, A. Merino, G. Sanz, J. Brugada, A. Bayes-Genis, and M. Heras Effects of adipose tissue-derived stem cell therapy after myocardial infarction: impact of the route of administration J. Card. Fail. 16 2010 357 366
13. K. Suzuki, B. Murtuza, J.R. Beauchamp, N.J. Brand, P.J. Barton, A. Varela-Carver, S. Fukushima, S.R. Coppen, T.A. Partridge, and M.H. Yacoub Role of interleukin-1beta in acute inflammation and graft death after cell transplantation to the heart Circulation 110 2004 II219 II224
14. J. Muller-Ehmsen, P. Whittaker, R.A. Kloner, J.S. Dow, T. Sakoda, T.I. Long, P.W. Laird, and L. Kedes Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium J. Mol. Cell. Cardiol. 34 2002 107 116
15. T. Yasuda, R.D. Weisel, C. Kiani, D.A. Mickle, M. Maganti, and R.K. Li Quantitative analysis of survival of transplanted smooth muscle cells with real-time polymerase chain reaction J. Thorac. Cardiovasc. Surg. 129 2005 904 911
16. C.J. Teng, J. Luo, R.C. Chiu, and D. Shum-Tim Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty J. Thorac. Cardiovasc. Surg. 132 2006 628 632
17. A. Paul, Y. Ge, S. Prakash, and D. Shum-Tim Microencapsulated stem cells for tissue repairing: implications in cell-based myocardial therapy Regen. Med. 4 2009 733 745
18. A. Murua, E. Herran, G. Orive, M. Igartua, F.J. Blanco, J.L. Pedraz, and R.M. Hernandez Design of a composite drug delivery system to prolong functionality of cell-based scaffolds Int. J. Pharm. 407 2011 142 150
19. E. Santos, G. Orive, A. Calvo, R. Catena, P. Fernandez-Robredo, A.G. Layana, R.M. Hernandez, and J.L. Pedraz Optimization of 100 μm alginate-poly-L-lysine-alginate capsules for intravitreous administration J. Control. Release 158 2012 450
20. J. Dubrot, A. Portero, G. Orive, R.M. Hernandez, A. Palazon, A. Rouzaut, J.L. Perez-Gracia, S. Hervas-Stubbs, J.L. Pedraz, and I. Melero Delivery of immunostimulatory monoclonal antibodies by encapsulated hybridoma cells Cancer Immunol. Immunother. 59 2010 1621 1631
21. R.M. Hernandez, G. Orive, A. Murua, and J.L. Pedraz Microcapsules and microcarriers for in situ cell delivery Adv. Drug Deliv. Rev. 62 2010 711 730
22. H. Uludag, P. De Vos, and P.A. Tresco Technology of mammalian cell encapsulation Adv. Drug Deliv. Rev. 42 2000 29 64
23. A.H. Al Kindi, J.F. Asenjo, Y. Ge, G.Y. Chen, J. Bhathena, R.C. Chiu, S. Prakash, and D. Shum-Tim Microencapsulation to reduce mechanical loss of microspheres: implications in myocardial cell therapy Eur. J. Cardiothorac. Surg. 39 2010 241 247
24. D.L. Kraitchman, W.D. Gilson, and C.H. Lorenz Stem cell therapy: MRI guidance and monitoring J. Magn. Reson. Imag. 27 2008 299 310
25. Y. Ye, and J. Bogaert Cell therapy in myocardial infarction: emphasis on the role of MRI Eur. Radiol. 18 2008 548 569
26. L.C. Amado, A.P. Saliaris, K.H. Schuleri, M. St John, J.S. Xie, S. Cattaneo, D.J. Durand, T. Fitton, J.Q. Kuang, G. Stewart, S. Lehrke, W.W. Baumgartner, B.J. Martin, A.W. Heldman, and J.M. Hare Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction Proc. Natl. Acad. Sci. USA 102 2005 11474 11479
27. R.W. Grauss, J. van Tuyn, P. Steendijk, E.M. Winter, D.A. Pijnappels, B. Hogers, A.C. Gittenberger-De Groot, R. van der Geest, A. van der Laarse, A.A. de Vries, M.J. Schalij, and D.E. Atsma Forced myocardin expression enhances the therapeutic effect of human mesenchymal stem cells after transplantation in ischemic mouse hearts Stem Cells 26 2008 1083 1093
28. S.M. Hashemi, S. Ghods, F.D. Kolodgie, K. Parcham-Azad, M. Keane, D. Hamamdzic, R. Young, M.K. Rippy, R. Virmani, H. Litt, and R.L. Wilensky A placebo controlled, dose-ranging, safety study of allogenic mesenchymal stem cells injected by endomyocardial delivery after an acute myocardial infarction Eur. Heart J. 29 2008 251 259
29. F. Cao, S. Lin, X. Xie, P. Ray, M. Patel, X. Zhang, M. Drukker, S.J. Dylla, A.J. Connolly, X. Chen, I.L. Weissman, S.S. Gambhir, and J.C. Wu In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery Circulation 113 2006 1005 1014
30. A.V. Naumova, H. Reinecke, V. Yarnykh, J. Deem, C. Yuan, and C.E. Murry Ferritin overexpression for noninvasive magnetic resonance imaging-based tracking of stem cells transplanted into the heart Mol. Imag. 9 2010 201 210
31. Y.J. Kim, Y.M. Huh, K.O. Choe, B.W. Choi, E.J. Choi, Y. Jang, J.M. Lee, and J.S. Suh In vivo magnetic resonance imaging of injected mesenchymal stem cells in rat myocardial infarction; simultaneous cell tracking and left ventricular function measurement Int. J. Cardiovasc. Imag. 25 Suppl. 1 2009 99 109
32. J.B. Mitchell, K. McIntosh, S. Zvonic, S. Garrett, Z.E. Floyd, A. Kloster, Y. Di Halvorsen, R.W. Storms, B. Goh, G. Kilroy, X. Wu, and J.M. Gimble Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers Stem Cells 24 2006 376 385
33. C.Q. Qu, G.H. Zhang, L.J. Zhang, and G.S. Yang Osteogenic and adipogenic potential of porcine adipose mesenchymal stem cells In Vitro Cell. Dev. Biol. Anim. 43 2007 95 100
34. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, D. Prockop, and E. Horwitz Minimal criteria for defining multipotent mesenchymal stromal cells The International Society for Cellular Therapy Position Statement, Cytotherapy 8 2006 315 317
35. F. Lim, and A.M. Sun Microencapsulated islets as bioartificial endocrine pancreas Science 210 1980 908 910
36. S.D. Collins, R. Baffour, and R. Waksman Cell therapy in myocardial infarction Cardiovasc. Revasc Med. 8 2007 43 51
37. P.J. Psaltis, A.C. Zannettino, S.G. Worthley, and S. Gronthos Concise review: mesenchymal stromal cells: potential for cardiovascular repair Stem Cells 26 2008 2201 2210
38. T. Kinnaird, E. Stabile, M.S. Burnett, C.W. Lee, S. Barr, S. Fuchs, and S.E. Epstein 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. 94 2004 678 685
39. M. Xu, R. Uemura, Y. Dai, Y. Wang, Z. Pasha, and M. Ashraf In vitro and in vivo effects of bone marrow stem cells on cardiac structure and function J. Mol. Cell. Cardiol. 42 2007 441 448
40. M. Mirotsou, T.M. Jayawardena, J. Schmeckpeper, M. Gnecchi, and V.J. Dzau Paracrine mechanisms of stem cell reparative and regenerative actions in the heart J. Mol. Cell. Cardiol. 50 2011 280 289
41. M. Gnecchi, Z. Zhang, A. Ni, and V.J. Dzau Paracrine mechanisms in adult stem cell signaling and therapy Circ. Res. 103 2008 1204 1219
42. A. Paul, A. Cantor, D. Shum-Tim, and S. Prakash Superior cell delivery features of genipin crosslinked polymeric microcapsules: preparation, in vitro characterization and pro-angiogenic applications using human adipose stem cells Mol. Biotechnol. 48 2011 116 127
43. H. Zhang, S.J. Zhu, W. Wang, Y.J. Wei, and S.S. Hu Transplantation of microencapsulated genetically modified xenogeneic cells augments angiogenesis and improves heart function Gene Ther. 15 2008 40 48
44. J. Yu, K.T. Du, Q. Fang, Y. Gu, S.S. Mihardja, R.E. Sievers, J.C. Wu, and R.J. Lee The use of human mesenchymal stem cells encapsulated in RGD modified alginate microspheres in the repair of myocardial infarction in the rat Biomaterials 31 2010 7012 7020
45. X.P. Bai, H.X. Zheng, R. Fang, T.R. Wang, X.L. Hou, Y. Li, X.B. Chen, and W.M. Tian Fabrication of engineered heart tissue grafts from alginate/collagen barium composite microbeads Biomed. Mater. 6 2011 045002
46. X. Bai, and E. Alt Myocardial regeneration potential of adipose tissue-derived stem cells Biochem. Biophys. Res. Commun. 401 2010 321 326
47. J. Yang, H. Zhang, L. Zhao, Y. Chen, H. Liu, and T. Zhang Human adipose tissue-derived stem cells protect impaired cardiomyocytes from hypoxia/reoxygenation injury through hypoxia-induced paracrine mechanism Cell Biochem. Funct. 30 2012 505 514
48. R. Madonna, Y.J. Geng, and R. De Caterina Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair Arterioscler. Thromb. Vasc. Biol. 29 2009 1723 1729
49. A.J. Salgado, R.L. Reis, N.J. Sousa, and J.M. Gimble Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine Curr. Stem Cell. Res. Ther. 5 2010 103 110
50. G. Orive, R.M. Hernandez, A.R. Gascon, R. Calafiore, T.M. Chang, P. De Vos, G. Hortelano, D. Hunkeler, I. Lacik, A.M. Shapiro, and J.L. Pedraz Cell encapsulation: promise and progress Nat. Med. 9 2003 104 107
51. G. Orive, A.R. Gascon, R.M. Hernandez, A. Dominguez-Gil, and J.L. Pedraz Techniques: new approaches to the delivery of biopharmaceuticals Trends Pharmacol. Sci. 25 2004 382 387
52. G. Orive, S.K. Tam, J.L. Pedraz, and J.P. Halle Biocompatibility of alginate-poly-L-lysine microcapsules for cell therapy Biomaterials 27 2006 3691 3700