A multistep procedure to prepare pre-vascularized cardiac tissue constructs using adult stem sells, dynamic cell cultures, and porous scaffolds

Frontiers in Physiology

Volumn 5 JUN, Issue , 2014, Pages

  Pagliari, Stefania ^a,b   Tirella, Annalisa ^c,d   Ahluwalia, Arti ^c,d   Duim, Sjoerd ^e   Goumans, Marie Josè ^e   Aoyagi, Takao ^a   Forte, Giancarlo ^a,b  

^a NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^b ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^c UNIVERSITY OF PISA   (Italy)

^d INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Adult stem cells; Cardiac tissue engineering; Dynamic culture; Patient derived stem cells; Vascularized three dimensional (3D) scaffolds

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2;

ACE2 GENE; ARTICLE; BLOOD PRESSURE REGULATION; DISEASE MODEL; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME POLYMORPHISM; GENE DELETION; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HYPERTENSION; NONHUMAN; PATHOGENESIS; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; TREATMENT RESPONSE;

EID: 84904427920     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00210     Document Type: Article

References (73)

1. Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophoton. Int. 11, 36-42.
2. Akhyari, P., Fedak, P. W., Weisel, R. D., Lee, T. Y., Verma, S., Mickle, D. A., et al. (2002). Mechanical stretch regimen enhances the formation of bioengineered autologous cardiac muscle grafts. Circulation 106, I137-I142. doi: 10.1161/01.cir.0000032893.55215.fc
3. Bai, K., Huang, Y., Jia, X., Fan, Y., and Wang, W. (2010). Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. J. Biomech. 43, 1176-1181. doi: 10.1016/j.jbiomech.2009.11.030
4. Beltrami, A. P., Barlucchi, L., Torella, D., Baker, M., Limana, F., Chimenti, S., et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776. doi: 10.1016/S0092-8674(03)00687-1
5. Bolli, R., Chugh, A. R., D'Amario, D., Loughran, J. H., Stoddard, M. F., Ikram, S., et al. (2011). Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378, 1847-1857. doi: 10.1016/S0140-6736(11)61590-0
6. Boschetti, F., Raimondi, M. T., Migliavacca, F., and Dubini, G. (2006). Prediction of the micro-fluid dynamic environment imposed to three-dimensional engineered cell systems in bioreactors. J. Biomech. 39, 418-425. doi: 10.1016/j.jbiomech.2004.12.022
7. Brannon-Peppas, L., and Peppas, N. A. (1990). Dynamic and equilibrium swelling behaviour of pH-sensitive hydrogels containing 2-hydroxyethyl methacrylate. Biomaterials 11, 635-644.
8. Bround, M. J., Asghari, P., Wambolt, R. B., Bohunek, L., Smits, C., Philit, M., et al. (2012). Cardiac ryanodine receptors control heart rate and rhythmicity in adult mice. Cardiovasc. Res. 96, 372-380. doi: 10.1093/cvr/cvs260
9. Burdick, J. A., and Vunjak-Novakovic, G. (2009). Engineered microenvironments for controlled stem cell differentiation. Tissue Eng. Part A 15, 205-219. doi: 10.1089/ten.tea.2008.0131
10. Caspi, O., Lesman, A., Basevitch, Y., Gepstein, A., Arbel, G., Habib, I. H., et al. (2007). Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ. Res. 100, 263-272. doi: 10.1161/01.RES.0000257776.05673.ff
11. Chiu, L. L., and Radisic, M. (2010). Scaffolds with covalently immobilized VEGF and angiopoietin-1 for vascularization of engineered tissues. Biomaterials 31, 226-241. doi: 10.1016/j.biomaterials.2009.09.039
12. Cimetta, E., Flaibani, M., Mella, M., Serena, E., Boldrin, L., De Coppi, P., et al. (2007). Enhancement of viability of muscle precursor cells on 3D scaffold in a perfusion bioreactor. Int. J. Artif. Organs 30, 415-428.
13. Cipolleschi, M. G., Dello Sbarba, P., and Olivotto, M. (1993). The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 82, 2031-2037.
14. Dreesmann, L., Ahlers, M., and Schlosshauera, B. (2007). The pro-angiogenic characteristics of a cross-linked gelatin matrix. Biomaterials 28, 5536-5543. doi: 10.1016/j.biomaterials.2007.08.040
15. Dubois, C., Liu, X., Claus, P., Marsboom, G., Pokreisz, P., Vandenwijngaert, S., et al. (2010). Differential effects of progenitor cell populations on left ventricular remodeling and myocardial neovascularization after myocardial infarction. J. Am. Coll. Cardiol. 55, 2232-2243. doi: 10.1016/j.jacc.2009.10.081
16. Dvir, T., Kedem, A., Ruvinov, E., Levy, O., Freeman, I., Landa, N., et al. (2009). Prevascularization of cardiac patch on the omentum improves its therapeutic outcome. Proc. Natl. Acad. Sci. U.S.A. 106, 14990-14995. doi: 10.1073/pnas.0812242106
17. Engler, A. J., Rehfeldt, F., Sen, S., and Discher, D. E. (2007). Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation. Methods Cell Biol. 83, 521-545. doi: 10.1016/S0091-679X(07)83022-6
18. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. doi: 10.1016/j.cell.2006.06.044
19. Forte, G., Pagliari, S., Pagliari, F., Ebara, M., Di Nardo, P., and Aoyagi, T. (2013). Towards the generation of patient-specific patches for cardiac repair. Stem Cell Rev. 9, 313-325. doi: 10.1007/s12015-011-9325-8
20. Forte, G., Pietronave, S., Nardone, G., Zamperone, A., Magnani, E., Pagliari, S., et al. (2011). Human cardiac progenitor cell grafts as unrestricted source of super-numerary cardiac cells in healthy murine hearts. Stem Cells 29, 2051-2061. doi: 10.1002/stem.763
21. Gaetani, R., Doevendans, P. A., Metz, C. H., Alblas, J., Messina, E., Giacomello, A., et al. (2012). Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. Biomaterials 33, 1782-1790. doi: 10.1016/j.biomaterials.2011.11.003
22. Gnecchi, M., He, H., Liang, O. D., Melo, L. G., Morello, F., Mu, H., et al. (2005). Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11, 367-368. doi: 10.1038/nm0405-367
23. Gnecchi, M., Zhang, Z., Ni, A., and Dzau, V. J. (2008). Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 103, 1204-1219. doi: 10.1161/CIRCRESAHA.108.176826
24. Goumans, M. J., de Boer, T. P., Smits, A. M., van Laake, L. W., van Vliet, P., Metz, C. H., et al. (2007). TGF-beta1 induces efficient differentiation of human cardiomyocyte progenitor cells into functional cardiomyocytes in vitro. Stem Cell Res. 1, 138-149. doi: 10.1016/j.scr.2008.02.003
25. Haraguchi, Y., Shimizu, T., Yamato, M., Kikuchi, A., and Okano, T. (2006). Electrical coupling of cardiomyocyte sheets occurs rapidly via functional gap junction formation. Biomaterials 27, 4765-4774. doi: 10.1016/j.biomaterials.2006.04.034
26. Heng, B. C., Haider, H. Kh., Sim, E. K., Cao, T., and Ng, S. C. (2004). Strategies for directing the differentiation of stem cells into the cardiomyogenic lineage in vitro. Cardiovasc. Res. 62, 34-42. doi: 10.1016/j.cardiores.2003.12.022
27. Jazayeri, M., Allameh, A., Soleimani, M., Jazayeri, S. H., Piryaei, A., and Kazemnejad, S. (2008). Molecular and ultrastructural characterization of endothelial cells differentiated from human bone marrow mesenchymal stem cells. Cell Biol. Int. 32, 1183-1192. doi: 10.1016/j.cellbi.2008.07.020
28. Kang, K. T., Coggins, M., Xiao, C., Rosenzweig, A., and Bischoff, J. (2013). Human vasculogenic cells form functional blood vessels and mitigate adverse remodeling after ischemia reperfusion injury in rats. Angiogenesis 16, 773-784. doi: 10.1007/s10456-013-9354-9
29. Lalu, M. M., McIntyre, L., Pugliese, C., Fergusson, D., Winston, B. W., Marshall, J. C., et al. (2012). Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS ONE 7:e47559. doi: 10.1371/journal.pone.0047559
30. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E. S., Kohane, D. S., Darland, D. C., et al. (2005). Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23, 879-884. doi: 10.1038/nbt1109
31. Lian, F., Xue, S., Gu, P., and Zhu, H. S. (2008). The long-term effect of autologous endothelial progenitor cells from peripheral blood implantation on infarcted myocardial contractile force. J. Int. Med. Res. 36, 40-46. doi: 10.1177/147323000803600106
32. Lien, S. M., Ko, L. Y., and Huang, T. J. (2009). Effect of pore size and ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering. Acta Biomater. 5, 670-679. doi: 10.1016/j.actbio.2008.09.020
33. Loffredo, F. S., Steinhauser, M. L., Gannon, J., and Lee, R. T. (2011). Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 8, 389-398. doi: 10.1016/j.stem.2011.02.002
34. Lovett, M., Lee, K., Edwards, A., and Kaplan, D. L. (2009). Vascularization strategies for tissue engineering. Tissue Eng. Part B Rev. 15, 353-370. doi: 10.1089/ten.TEB.2009.0085
35. Lozito, T. P., Kuo, C. K., Taboas, J. M., and Tuan, R. S. (2009). Human mesenchymal stem cells express vascular cell phenotypes upon interaction with endothelial cell matrix. J. Cell. Biochem. 107, 714-722. doi: 10.1002/jcb.22167
36. Maidhof, R., Tandon, N., Lee, E. J., Luo, J., Duan, Y., Yeager, K., et al. (2012). Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue. J. Tissue Eng. Regen. Med. 6, e12-e23. doi: 10.1002/term.525
37. Makkar, R. R., Smith, R. R., Cheng, K., Malliaras, K., Thomson, L. E., Berman, D., et al. (2012). Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet 379, 895-904. doi: 10.1016/S0140-6736(12)60195-0
38. Martucci, J. F., Ruseckaite, R. A., and Vàzquez, A. (2006). Creep of glutaraldehyde-crosslinked gelatin films. Mater. Sci. Eng. A 435-436, 681-686. doi: 10.1016/j.msea.2006.07.097CrossRef Full Text
39. Matsuura, K., Wada, M., Konishi, K., Sato, M., Iwamoto, U., Sato, Y., et al. (2012). Fabrication of mouse embryonic stem cell-derived layered cardiac cell sheets using a bioreactor culture system. PLoS ONE 7:e52176. doi: 10.1371/journal.pone.0052176
40. Mazzei, D., Guzzardi, M. A., Giusti, S., and Ahluwalia, A. (2010). A low shear stress modular bioreactor for connected cell culture under high flow rates. Biotechnol. Bioeng. 106, 127-137. doi: 10.1002/bit.22671
41. Mehta, A., and Shim, W. (2013). Cardiac stem cell therapy: stemness or commitment? Cell Transplant. 22, 1-14. doi: 10.3727/096368912X653282
42. Menasche, P. (2011). Cardiac cell therapy: lessons from clinical trials. J. Mol. Cell. Cardiol. 50, 258-265. doi: 10.1016/j.yjmcc.2010.06.010
43. Meyer, G. P., Wollert, K. C., Lotz, J., Pirr, J., Rager, U., Lippolt, P., et al. (2009). Intracoronary bone marrow cell transfer after myocardial infarction: 5-year follow-up from the randomized-controlled BOOST trial. Eur. Heart J. 30, 2978-2984. doi: 10.1093/eurheartj/ehp374
44. Mosqueira, D., Pagliari, S., Uto, K., Ebara, M., Romanazzo, S., Escobedo-Lucea, C., et al. (2014). Hippo pathway effectors control cardiac progenitor cell fate by acting as dynamic sensors of substrate mechanics and nanostructure. ACS Nano 8, 2033-2047. doi: 10.1021/nn4058984
45. Muraglia, A., Cancedda, R., and Quarto, R. (2000). Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J. Cell Sci. 113, 1161-1166.
46. Mwangi, J. W., and Ofner, C. M. 3rd (2004). Crosslinked gelatin matrices: release of a random coil macromolecular solute. Int. J. Pharm. 278, 319-327. doi: 10.1016/j.ijpharm.2004.03.024
47. Oswald, J., Boxberger, S., Jorgensen, B., Feldmann, S., Ehninger, G., Bornhauser, M., et al. (2004). Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22, 377-384. doi: 10.1634/stemcells.22-3-377
48. Pagliari, S., Romanazzo, S., Mosqueira, D., Pinto-do-ó, P., Aoyagi, T., and Forte, G. (2013). Adult stem cells and biocompatible scaffolds as powerful drug delivery tools for cardiac repair. Curr. Med. Chem. 20, 3429-3447. doi: 10.2174/09298673113209990032
49. Pagliari, S., Vilela-Silva, A. C., Forte, G., Pagliari, F., Mandoli, C., Vozzi, G., et al. (2011). Cooperation of biological and mechanical signals in cardiac progenitor cell differentiation. Adv. Mater. 23, 514-518. doi: 10.1002/adma.201003479
50. Pampaloni, F., Reynaud, E. G., and, Stelzer, E. H. (2007). The third dimension bridges between cell culture and live tissue. Nat. Rev. Mol. Cell Biol. 8, 839-845. doi: 10.1038/nrm2236
51. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., et al. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284,143-147. doi: 10.1126/science.284.5411.143
52. Portalska, K. J., Leferink, A., Groen, N., Fernandes, H., Moroni, L., van Blitterswijk, C., et al. (2012). Endothelial differentiation of mesenchymal stromal cells. PLoS ONE 7:e46842. doi: 10.1371/journal.pone.0046842
53. Sakaguchi, K., Shimizu, T., Haraguchi, S., Sekine, H., Yamato, M., Umezu, M., et al. (2013). In vitro engineering of vascularized tissue surrogates. Sci. Rep. 3:1316. doi: 10.1038/srep01316
54. Sakai, T., Li, R. K., Weisel, R. D., Mickle, D. A., Kim, E. T., Jia, Z. Q., et al. (2001). The fate of a tissue-engineered cardiac graft in the right ventricular outflow tract of the rat. J. Thorac. Cardiovasc. Surg. 121, 932-942. doi: 10.1067/mtc.2001.113600
55. Sato, K., Wu, T., Laham, R. J., Johnson, R. B., Douglas, P., Li, J., et al. (2001). Efficacy of intracoronary or intravenous VEGF165 in a pig model of chronic myocardial ischemia. J. Am. Coll. Cardiol. 37, 616-623. doi: 10.1016/S0735-1097(00)01144-X
56. Segers, V. F. M., and Lee, R. T. (2011). Biomaterials to enhance stem cell function in the heart. Circ. Res. 109, 910-922. doi: 10.1161/CIRCRESAHA.111.249052
57. Sekine, H., Shimizu, T., Sakaguchi, K., Dobashi, I., Wada, M., Yamato, M., et al. (2013). In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels. Nat. Commun. 4:1399. doi: 10.1038/ncomms2406
58. Simons, M., and Ware, J. A. (2003). Therapeutic angiogenesis in cardiovascular disease. Nat. Rev. Drug Discov. 2, 863-871. doi: 10.1038/nrd1226
59. Simón-Yarza, T., Formiga, F. R., Tamayo, E., Pelacho, B., Prosper, F., and Blanco-Prieto, M. J. (2012). Vascular endothelial growth factor-delivery systems for cardiac repair: an overview. Theranostics 2, 541-552. doi: 10.7150/thno.3682
60. Singh, S., Wu, B. M., and Dunn, J. C. (2012). Delivery of VEGF using collagen-coated polycaprolactone scaffolds stimulates angiogenesis. J. Biomed. Mater. Res. 100, 720-727. doi: 10.1002/jbm.a.34010
61. Smits, A. M., van Laake, L. W., den Ouden, K., Schreurs, C., Szuhai, K., van Echteld, C. J., et al. (2009a). Human cardiomyocyte progenitor cell transplantation preserves long-term function of the infarcted mouse myocardium. Cardiovasc. Res. 83, 527-535. doi: 10.1093/cvr/cvp146
62. Smits, A. M., van Vliet, P., Metz, C. H., Korfage, T., Sluijter, J. P., Doevendans, P. A., et al. (2009b). Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat. Protoc. 4, 232-243. doi: 10.1038/nprot.2008.229
63. Spinelli, A., Vinci, B., Tirella, A., Matteucci, M., Gargani, L., Ahluwalia, A., et al. (2012). Realization of a poro-elastic ultrasound replica of pulmonary tissue. Biomatter 2, 37-42. doi: 10.4161/biom.19835
64. Terrovitis, J. V., Smith, R. R., and Marbán, E. (2010). Assessment and optimization of cell engraftment after transplantation into the heart Circ. Res. 106, 479-494. doi: 10.1161/CIRCRESAHA.109.208991
65. Thomas, M., and Augustin, H. G. (2009). The role of the Angiopoietins in vascular morphogenesis. Angiogenesis 12, 125-137. doi: 10.1007/s10456-009-9147-3
66. Urbich, C., Heeschen, C., Aicher, A., Sasaki, K., Bruhl, T., Farhadi, M. R., et al. (2005). Cathepsin L is required for endothelial progenitor cell-induced neovascularization. Nat. Med. 11, 206-213. doi: 10.1038/nm1182
67. Varum, S., Rodrigues, A. S., Moura, M. B., Momcilovic, O., Easley, C. A. 4th, Ramalho-Santos, J., et al. (2011). Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS ONE 6:e20914. doi: 10.1371/journal.pone.0020914
68. Vozzi, F., Mazzei, D., Vinci, B., Vozzi, G., Sbrana, T., Ricotti, L., et al. (2011). A flexible bioreactor system for constructing in vitro tissue and organ models. Biotechnol. Bioeng. 108, 2129-2140. doi: 10.1002/bit.23164
69. Wang, D. M., and Tarbell, J. M. (1995). Modeling interstitial flow in an artery wall allows estimation of wall shear stress on smooth muscle cells. J. Biomech. Eng. 117, 358-366.
70. Wöhrle, J., Merkle, N., Mailänder, V., Nusser, T., Schauwecker, P., von Scheidt, F., et al. (2010). Results of intracoronary stem cell therapy after acute myocardial infarction. Am. J. Cardiol. 105, 804-812. doi: 10.1016/j.amjcard.2009.10.060
71. Wu, S. C., Chang, W. H., Dong, C. G., Chen, K. Y., Chen, Y. S., and Yao, C. H. (2011). Cell adhesion and proliferation enhancement by gelatin nanofiber scaffolds. J. Bioact. Compat. Polym. 26, 565-577. doi: 10.1177/0883911511423563
72. Xing, Q., Yates, K., Vogt, C., Qian, Z., Frost, M. C., and Zhao, F. (2014). Increasing mechanical strength of gelatin hydrogels by divalent metal ion removal. Sci. Rep. 4:4706. doi: 10.1038/srep04706
73. Zimmermann, W. H., Melnychenko, I., Wasmeier, G., Didié, M., Naito, H., Nixdorff, U., et al. (2006). Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat. Med. 12, 452-458. doi: 10.1038/nm1394