Distilling complexity to advance cardiac tissue engineering

Science Translational Medicine

Volumn 8, Issue 342, 2016, Pages

  Ogle, Brenda M ^a   Bursac, Nenad ^b   Domian, Ibrahim ^c   Huang, Ngan F ^d,e   Menasché, Philippe ^f   Murry, Charles E ^g   Pruitt, Beth ^h   Radisic, Milica ⁱ   Wu, Joseph C ^j   Wu, Sean M ^j   Zhang, Jianyi ^k   Zimmermann, Wolfram Hubertus ^l   Vunjak Novakovic, Gordana ^m  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Duke University   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d STANFORD UNIVERSITY   (United States)

^e VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^f PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^g UNIVERSITY OF WASHINGTON   (United States)

^h Stanford University   (United States)

ⁱ UNIVERSITY OF TORONTO   (Canada)

^j STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k and Radiation Oncology   (United States)

^l UNIVERSITY OF GÖTTINGEN   (Germany)

^m NONE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED CADIAC TISSUE ENGINEERING; CARDIAC MUSCLE CELL; CARDIAC REGENERATION; CARDIOVASCULAR THERAPEUTIC DEVICE; CELL MATURATION; CELL PROLIFERATION; CELL VIABILITY; CLINICAL PRACTICE; DEVICE SAFETY; DISEASE MODEL; EQUIPMENT DESIGN; GENE EDITING; HUMAN; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; MOLECULAR GENETICS; MUTATIONAL ANALYSIS; ORGANS ON A CHIP; PHENOTYPE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; REVIEW; TISSUE ENGINEERING; TISSUE GRAFT; TISSUE REGENERATION; TISSUE SCAFFOLD; ANIMAL; CARDIAC MUSCLE; CYTOLOGY; HEART DISEASE; METABOLISM; PROCEDURES;

ANIMALS; HEART DISEASES; HUMANS; MYOCARDIUM; MYOCYTES, CARDIAC; TISSUE ENGINEERING;

EID: 84973882625     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aad2304     Document Type: Review

References (33)

1. K. L. K. Coulombe, V. K. Bajpai, S. T. Andreadis, C. E. Murry, Heart regeneration with engineered myocardial tissue. Annu. Rev. Biomed. Eng. 16, 1-28 (2014).
2. P. Menasché, V. Vanneaux, A. Hagège, A. Bel, B. Cholley, I. Cacciapuoti, A. Parouchev, N. Benhamouda, G. Tachdjian, L. Tosca, J.-H. Trouvin, J.-R. Fabreguettes, V. Bellamy, R. Guillemain, C. Suberbielle Boissel, E. Tartour, M. Desnos, J. Larghero, Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: First clinical case report. Eur. Heart J. 36, 2011-2017 (2015).
3. S. N. Bhatia, D. E. Ingber, Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760-772 (2014).
4. E. Cimetta, A. Godier-Furnémont, G. Vunjak-Novakovic, Bioengineering heart tissue for in vitro testing. Curr. Opin. Biotechnol. 24, 926-932 (2013).
5. A.Mathur, P. Loskill, K. Shao, N. Huebsch, S. Hong, S. G. Marcus, N. Marks, M. Mandegar, B. R. Conklin, L. P. Lee, K. E. Healy, Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep. 5, 8883 (2015).
6. A. J. S. Ribeiro, Y.-S. Ang, J.-D. Fu, R. N. Rivas, T. M. A. Mohamed, G. C. Higgs, D. Srivastava, B. L. Pruitt, Contractility of single cardiomyocytes differentiated from pluripotent stem cells depends on physiological shape and substrate stiffness. Proc. Natl. Acad. Sci. U.S.A. 112, 12705-12710 (2015).
7. N. Sun, M. Yazawa, J. Liu, L. Han, V. Sanchez-Freire, O. J. Abilez, E. G. Navarrete, S. Hu, L. Wang, A. Lee, A. Pavlovic, S. Lin, R. Chen, R. J. Hajjar, M. P. Snyder, R. E. Dolmetsch, M. J. Butte, E. A. Ashley, M. T. Longaker, R. C. Robbins, J. C. Wu, Patientspecific induced pluripotent stem cells as amodel for familial dilated cardiomyopathy. Sci. Transl. Med. 4, 130ra47 (2012).
8. G. Wang, M. L. McCain, L. Yang, A. He, F. S. Pasqualini, A. Agarwal, H. Yuan, D. Jiang, D. Zhang, L. Zangi, J. Geva, A. E. Roberts, Q. Ma, J. Ding, J. Chen, D.-Z. Wang, K. Li, J. Wang, R. J. A. Wanders, W. Kulik, F. M. Vaz, M. A. Laflamme, C. E. Murry, K. R. Chien, R. I. Kelley, G. M. Church, K. K. Parker, W. T. Pu, Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat. Med. 20, 616-623 (2014).
9. J. T. Hinson, A. Chopra, N. Nafissi, W. J. Polacheck, C. C. Benson, S. Swist, J. Gorham, L. Yang, S. Schafer, C. C. Sheng, A. Haghighi, J. Homsy, N. Hubner, G. Church, S. A. Cook, W. A. Linke, C. S. Chen, J. G. Seidman, C. E. Seidman, Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science 349, 982-986 (2015).
10. S. S. Nunes, J.W. Miklas, J. Liu, R. Aschar-Sobbi, Y. Xiao, B. Zhang, J. Jiang, S. Massé, M. Gagliardi, A. Hsieh, N. Thavandiran, M. A. Laflamme, K. Nanthakumar, G. J. Gross, P. H. Backx, G. Keller, M. Radisic, Biowire: A platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat. Methods 10, 781-787 (2013).
11. G. Eng, B. W. Lee, L. Protas, M. Gagliardi, K. Brown, R. S. Kass, G. Keller, R. B. Robinson, G. Vunjak-Novakovic, Autonomous beating rate adaptation in human stem cell-derived cardiomyocytes. Nat. Commun. 7, 10312 (2016).
12. D. Zhang, I. Y. Shadrin, J. Lam, H.-Q. Xian, H. R. Snodgrass, N. Bursac, Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34, 5813-5820 (2013).
13. J. P. Jung, D. Hu, I. J. Domian, B. M. Ogle, An integrated statisticalmodel for enhanced murine cardiomyocyte differentiation via optimized engagement of 3D extracellular matrices. Sci. Rep. 5, 18705 (2015).
14. K. R. Stevens, K. L. Kreutziger, S. K. Dupras, F. S. Korte, M. Regnier, V.Muskheli, M. B. Nourse, K. Bendixen, H. Reinecke, C. E. Murry, Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. U.S.A. 106, 16568-16573 (2009).
15. M. R. Rosen, R. B. Robinson, P. R. Brink, I. S. Cohen, The road to biological pacing. Nat. Rev. Cardiol. 8, 656-666 (2011).
16. N. Smart, C. A. Risebro, A. A. D. Melville, K. Moses, R. J. Schwartz, K. R. Chien, P. R. Riley, Thymosin b4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445, 177-182 (2007).
17. A. D. Witty, A. Mihic, R. Y. Tam, S. A. Fisher, A. Mikryukov, M. S. Shoichet, R.-K. Li, S. J. Kattman, G. Keller, Generation of the epicardial lineage from human pluripotent stem cells. Nat. Biotechnol. 32, 1026-1035 (2014).
18. R. D. Kirkton, N. Bursac, Engineering biosynthetic excitable tissues from unexcitable cells for electrophysiological and cell therapy studies. Nat. Commun. 2, 300 (2011).
19. K. A. Gerbin, X. Yang, C. E. Murry, K. L. K. Coulombe, Enhanced electrical integration of engineered human myocardium via intramyocardial versus epicardial delivery in infarcted rat hearts. PLOS One 10, e0131446 (2015).
20. N. J. Palpant, L. Pabon, M. Roberts, B. Hadland, D. Jones, C. Jones, R. T. Moon, W. L. Ruzzo, I. Bernstein, Y. Zheng, C. E. Murry, Inhibition of b-catenin signaling respecifies anterior-like endothelium into beating human cardiomyocytes. Development 142, 3198-3209 (2015).
21. N. L. Tulloch, V. Muskheli, M. V. Razumova, F. S. Korte, M. Regnier, K. D. Hauch, L. Pabon, H. Reinecke, C. E. Murry, Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 109, 47-59 (2011).
22. N. Hedhli, Q. Huang, A. Kalinowski, M. Palmeri, X. Hu, R. R. Russell, K. S. Russell, Endothelium-derived neuregulin protects the heart against ischemic injury. Circulation 123, 2254-2262 (2011).
23. D. Huh, Y.-s. Torisawa, G. A. Hamilton, H. J. Kim, D. E. Ingber, Microengineered physiological biomimicry: Organson-chips. Lab Chip 12, 2156-2164 (2012).
24. Y. Shiba, S. Fernandes, W.-Z. Zhu, D. Filice, V. Muskheli, J. Kim, N. J. Palpant, J. Gantz, K. W. Moyes, H. Reinecke, B. Van Biber, T. Dardas, J. L. Mignone, A. Izawa, R. Hanna, M. Viswanathan, J. D. Gold, M. I. Kotlikoff, N. Sarvazyan, M. W. Kay, C. E. Murry, M. A. Laflamme, Human ES-cellderived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 489, 322-325 (2012).
25. M. Kawamura, S. Miyagawa, K. Miki, A. Saito, S. Fukushima, T. Higuchi, T. Kawamura, T. Kuratani, T. Daimon, T. Shimizu, T. Okano, Y. Sawa, Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 126 (suppl. 1), S29-S37 (2012).
26. Q. Xiong, L. Ye, P. Zhang, M. Lepley, C. Swingen, L. Zhang, D. S. Kaufman, J. Zhang, Bioenergetic and functional consequences of cellular therapy: Activation of endogenous cardiovascular progenitor cells. Circ. Res. 111, 455-468 (2012).
27. H. Masumoto, T. Matsuo, K. Yamamizu, H. Uosaki, G. Narazaki, S. Katayama, A. Marui, T. Shimizu, T. Ikeda, T. Okano, R. Sakata, J. K. Yamashita, Pluripotent stem cell-engineered cell sheets reassembled with defined cardiovascular populations ameliorate reduction in infarct heart function through cardiomyocyte-mediated neovascularization. Stem Cells 30, 1196-1205 (2012).
28. J. J. H. Chong, X. Yang, C. W. Don, E. Minami, Y.-W. Liu, J. J. Weyers, W. M. Mahoney, B. Van Biber, S. M. Cook, N. J. Palpant, J. A. Gantz, J. A. Fugate, V. Muskheli, G. M. Gough, K.W. Vogel, C. A. Astley, C. E. Hotchkiss, A. Baldessari, L. Pabon, H. Reinecke, E. A. Gill, V. Nelson, H.-P. Kiem, M. A. Laflamme, C. E. Murry, Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510, 273-277 (2014).
29. L. Ye, Y.-H. Chang, Q. Xiong, P. Zhang, L. Zhang, P. Somasundaram, M. Lepley, C. Swingen, L. Su, J. S. Wendel, J. Guo, A. Jang, D. Rosenbush, L. Greder, J. R. Dutton, J. Zhang, T. J. Kamp, D. S. Kaufman, Y. Ge, J. Zhang, Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell 15, 750-761 (2014).
30. S. D. Anker, A. J. S. Coats, G. Cristian, D. Dragomir, E. Pusineri, M. Piredda, L. Bettari, R. Dowling, M. Volterrani, B.-A. Kirwan, G. Filippatos, J.-L. Mas, N. Danchin, S. D. Solomon, R. J. Lee, F. Ahmann, A. Hinson, H. N. Sabbah, D. L. Mann, A prospective comparison of alginate-hydrogel with standard medical therapy to determine impact on functional capacity and clinical outcomes in patients with advanced heart failure (AUGMENT-HF trial). Eur. Heart J. 36, 2297-2309 (2015).
31. T. Pilgrim, D. Heg, M. Roffi, D. Tüller, O. Muller, A. Vuilliomenet, S. Cook, D. Weilenmann, C. Kaiser, P. Jamshidi, T. Fahrni, A. Moschovitis, S. Noble, F. R. Eberli, P. Wenaweser, P. Jüni, S. Windecker, Ultrathin strut biodegradable polymer sirolimuseluting stent versus durable polymer everolimus-eluting stent for percutaneous coronary revascularisation (BIOSCIENCE): A randomised, single-blind, non-inferiority trial. Lancet 384, 2111-2122 (2014).
32. E. Neofytou, C. G. O'Brien, L. A. Couture, J. C. Wu, Hurdles to clinical translation of human induced pluripotent stem cells. J. Clin. Invest. 125, 2551-2557 (2015).
33. V. Serpooshan, S. M. Wu, Patching up broken hearts: Cardiac cell therapy gets a bioengineered boost. Cell Stem Cell 15, 671-673 (2014).