Large cardiac muscle patches engineered from human induced-pluripotent stem cell-derived cardiac cells improve recovery from myocardial infarction in swine

Circulation

Volumn 137, Issue 16, 2018, Pages 1712-1730

  Gao, Ling ^a   Gregorich, Zachery R ^b   Zhu, Wuqiang ^a   Mattapally, Saidulu ^a   Oduk, Yasin ^a   Lou, Xi ^a   Kannappan, Ramaswamy ^a   Borovjagin, Anton V ^a   Walcott, Gregory P ^a   Pollard, Andrew E ^a   Fast, Vladimir G ^a   Hu, Xinyang ^c   Lloyd, Steven G ^a   Ge, Ying ^b   Zhang, Jianyi ^a  

^a and Radiation Oncology   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Animal; Heart; Models; Myocardial infarction; Pluripotent stem cells; Tissue engineering

Indexed keywords

ALPHA ACTININ; ANGIOPOIETIN 1; ANGIOTENSIN II; CALPONIN; CONNEXIN 43; ERYTHROPOIETIN; FIBRIN; LACTATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SCATTER FACTOR; THROMBIN; TRANSCRIPTION FACTOR SOX2; TRANSGELIN; TROPONIN; TROPONIN I; VASCULAR ENDOTHELIAL CADHERIN; VON WILLEBRAND FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIAC MUSCLE CELL; CARDIAC MUSCLE PATCH; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; ELECTROCARDIOGRAM; ELECTROPHYSIOLOGICAL PROCEDURES; ELECTROSTIMULATION; ENDOTHELIUM CELL; EXOSOME; FEMALE; GENE EXPRESSION; HEART CELL CULTURE; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; HEMODYNAMICS; HUMAN; HUMAN CELL; HYPERPOLARIZATION; INDUCED PLURIPOTENT STEM CELL; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPEN FIBRIN PATCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; TISSUE CHARACTERIZATION; TISSUE ENGINEERING; TRANSMISSION ELECTRON MICROSCOPY; WALL STRESS; WESTERN BLOTTING; Y CHROMOSOME; ANIMAL; CARDIAC MUSCLE; CELL CULTURE; CONVALESCENCE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PIG; PROCEDURES; REGENERATION; SMOOTH MUSCLE CELL; STEM CELL TRANSPLANTATION; TIME FACTOR; TISSUE SCAFFOLD; TRANSPLANTATION; XENOGRAFT;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; MYOCYTES, SMOOTH MUSCLE; RECOVERY OF FUNCTION; REGENERATION; STEM CELL TRANSPLANTATION; SUS SCROFA; TIME FACTORS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSPLANTATION, HETEROLOGOUS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 85045404237     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.117.030785     Document Type: Article

References (39)

1. Sayed N, Liu C, Wu JC. Translation of human-induced pluripotent stem cells: from clinical trial in a dish to precision medicine. J Am Coll Cardiol. 2016;67:2161-2176. doi: 10.1016/j.jacc.2016.01.083.
2. Shiba Y, Gomibuchi T, Seto T, Wada Y, Ichimura H, Tanaka Y, Ogasawara T, Okada K, Shiba N, Sakamoto K, Ido D, Shiina T, Ohkura M, Nakai J, Uno N, Kazuki Y, Oshimura M, Minami I, Ikeda U. Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature. 2016;538:388-391. doi: 10.1038/nature19815.
3. Ye L, Chang YH, Xiong Q, Zhang P, Zhang L, Somasundaram P, Lepley M, Swingen C, Su L, Wendel JS, Guo J, Jang A, Rosenbush D, Greder L, Dutton JR, Zhang J, Kamp TJ, Kaufman DS, Ge Y, Zhang J. Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells. Cell Stem Cell. 2014;15:750-761. doi: 10.1016/j.stem.2014.11.009.
4. Riegler J, Tiburcy M, Ebert A, Tzatzalos E, Raaz U, Abilez OJ, Shen Q, Kooreman NG, Neofytou E, Chen VC, Wang M, Meyer T, Tsao PS, Connolly AJ, Couture LA, Gold JD, Zimmermann WH, Wu JC. Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ Res. 2015;117:720-730. doi: 10.1161/CIRCRESAHA.115.306985.
5. Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ, Mahoney WM, Van Biber B, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem HP, Laflamme MA, Murry CE. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature. 2014;510:273-277. doi: 10.1038/nature13233.
6. Sun X, Nunes SS. Bioengineering approaches to mature human pluripotent stem cell-derived cardiomyocytes. Front Cell Dev Biol. 2017;5:19. doi: 10.3389/fcell.2017.00019.
7. Robertson C, Tran DD, George SC. Concise review: maturation phases of human pluripotent stem cell-derived cardiomyocytes. Stem Cells. 2013;31:829-837. doi: 10.1002/stem.1331.
8. Tiburcy M, Hudson JE, Balfanz P, Schlick S, Meyer T, Chang Liao ML, Levent E, Raad F, Zeidler S, Wingender E, Riegler J, Wang M, Gold JD, Kehat I, Wettwer E, Ravens U, Dierickx P, van Laake LW, Goumans MJ, Khadjeh S, Toischer K, Hasenfuss G, Couture LA, Unger A, Linke WA, Araki T, Neel B, Keller G, Gepstein L, Wu JC, Zimmermann WH. Defined engineered human myocardium with advanced maturation for applications in heart failure modeling and repair. Circulation. 2017;135:1832-1847. doi: 10.1161/CIRCULATIONAHA.116.024145.
9. Jackman CP, Carlson AL, Bursac N. Dynamic culture yields engineered myocardium with near-adult functional output. Biomaterials. 2016;111:66-79. doi: 10.1016/j.biomaterials.2016.09.024.
10. Ruan JL, Tulloch NL, Razumova MV, Saiget M, Muskheli V, Pabon L, Reinecke H, Regnier M, Murry CE. Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation. 2016;134:1557-1567. doi: 10.1161/CIRCULATIONAHA.114.014998.
11. Gao L, Kupfer ME, Jung JP, Yang L, Zhang P, Da Sie Y, Tran Q, Ajeti V, Freeman BT, Fast VG, Campagnola PJ, Ogle BM, Zhang J. Myocardial tissue engineering with cells derived from human-induced pluripotent stem cells and a native-like, high-resolution, 3-dimensionally printed scaffold. Circ Res. 2017;120:1318-1325. doi: 10.1161/CIRCRESAHA. 116.310277.
12. Ogle BM, Bursac N, Domian I, Huang NF, Menasche P, Murry CE, Pruitt B, Radisic M, Wu JC, Wu SM, Zhang J, Zimmermann WH, Vunjak-Novakovic G. Distilling complexity to advance cardiac tissue engineering. Sci Transl Med. 2016;8:342ps13. doi: 10.1126/scitranslmed.aad2304.
13. Nguyen PK, Neofytou E, Rhee JW, Wu JC. Potential strategies to address the major clinical barriers facing stem cell regenerative therapy for cardiovascular disease: a review. JAMA Cardiol. 2016;1:953-962. doi: 10.1001/ jamacardio.2016.2750.
14. Tzatzalos E, Abilez OJ, Shukla P, Wu JC. Engineered heart tissues and induced pluripotent stem cells: macro- and microstructures for disease modeling, drug screening, and translational studies. Adv Drug Deliv Rev. 2016;96:234-244. doi: 10.1016/j.addr.2015.09.010.
15. Weinberger F, Breckwoldt K, Pecha S, Kelly A, Geertz B, Starbatty J, Yorgan T, Cheng KH, Lessmann K, Stolen T, Scherrer-Crosbie M, Smith G, Reichenspurner H, Hansen A, Eschenhagen T. Cardiac repair in guinea pigs with human engineered heart tissue from induced pluripotent stem cells. Sci Transl Med. 2016;8:363ra148. doi: 10.1126/scitranslmed.aaf8781.
16. Zhang D, Shadrin IY, Lam J, Xian HQ, Snodgrass HR, Bursac N. Tissue-engineered cardiac patch for advanced functional maturation of human ESCderived cardiomyocytes. Biomaterials. 2013;34:5813-20. doi: 10.1016/j. biomaterials.2013.04.026.
17. Zhang L, Guo J, Zhang P, Xiong Q, Wu SC, Xia L, Roy SS, Tolar J, O'Connell TD, Kyba M, Liao K, Zhang J. Derivation and high engraftment of patientspecific cardiomyocyte sheet using induced pluripotent stem cells generated from adult cardiac fibroblast. Circ Heart Fail. 2015;8:156-66. doi: 10.1161/CIRCHEARTFAILURE.114.001317.
18. Lux M, Andree B, Horvath T, Nosko A, Manikowski D, Hilfiker-Kleiner D, Haverich A, Hilfiker A. In vitro maturation of large-scale cardiac patches based on a perfusable starter matrix by cyclic mechanical stimulation. Acta Biomater. 2016;30:177-187. doi: 10.1016/j.actbio.2015.11.006.
19. Ye L, Zimmermann WH, Garry DJ, Zhang J. Patching the heart: cardiac repair from within and outside. Circ Res. 2013;113:922-932. doi: 10.1161/ CIRCRESAHA.113.300216.
20. Xiong Q, Ye L, Zhang P, Lepley M, Swingen C, Zhang L, Kaufman DS, Zhang J. Bioenergetic and functional consequences of cellular therapy: activation of endogenous cardiovascular progenitor cells. Circ Res. 2012;111:455-468. doi: 10.1161/CIRCRESAHA.112.269894.
21. Burridge PW, Matsa E, Shukla P, Lin ZC, Churko JM, Ebert AD, Lan F, Diecke S, Huber B, Mordwinkin NM, Plews JR, Abilez OJ, Cui B, Gold JD, Wu JC. Chemically defined generation of human cardiomyocytes. Nat Methods. 2014;11:855-860. doi: 10.1038/nmeth.2999.
22. Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, Hsiao C, Kamp TJ, Palecek SP. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc. 2013;8:162-175. doi: 10.1038/ nprot.2012.150.
23. Zhang S, Dutton JR, Su L, Zhang J, Ye L. The influence of a spatiotemporal 3D environment on endothelial cell differentiation of human induced pluripotent stem cells. Biomaterials. 2014;35:3786-3793. doi: 10.1016/j. biomaterials.2014.01.037.
24. Sequeira V, van der Velden J. Historical perspective on heart function: the Frank-Starling Law. Biophys Rev. 2015;7:421-447. doi: 10.1007/s12551-015-0184-4.
25. Wendel JS, Ye L, Tao R, Zhang J, Zhang J, Kamp TJ, Tranquillo RT. Functional effects of a tissue-engineered cardiac patch from human induced pluripotent stem cell-derived cardiomyocytes in a rat infarct model. Stem Cells Transl Med. 2015;4:1324-1332. doi: 10.5966/sctm.2015-0044.
26. Wang X, Huang W, Liu G, Cai W, Millard RW, Wang Y, Chang J, Peng T, Fan GC. Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol. 2014;74:139-150. doi: 10.1016/j.yjmcc.2014.05.001.
27. Anderson ME, Goldhaber J, Houser SR, Puceat M, Sussman MA. Embryonic stem cell-derived cardiac myocytes are not ready for human trials. Circ Res. 2014;115:335-338. doi: 10.1161/CIRCRESAHA.114.304616.
28. Jung JH, Fu X, Yang PC. Exosomes generated from iPSC-derivatives: new direction for stem cell therapy in human heart diseases. Circ Res. 2017;120:407-417. doi: 10.1161/CIRCRESAHA.116.309307.
29. Waldenstrom A, Ronquist G. Role of exosomes in myocardial remodeling. Circ Res. 2014;114:315-324. doi: 10.1161/CIRCRESAHA.114.300584.
30. Li J, Liu K, Liu Y, Xu Y, Zhang F, Yang H, Liu J, Pan T, Chen J, Wu M, Zhou X, Yuan Z. Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity. Nat Immunol. 2013;14:793-803. doi: 10.1038/ni.2647.
31. Peng Y, Gregorich ZR, Valeja SG, Zhang H, Cai W, Chen YC, Guner H, Chen AJ, Schwahn DJ, Hacker TA, Liu X, Ge Y. Top-down proteomics reveals concerted reductions in myofilament and Z-disc protein phosphorylation after acute myocardial infarction. Mol Cell Proteomics. 2014;13:2752-2764. doi: 10.1074/mcp.M114.040675.
32. van der Velden J, Merkus D, Klarenbeek BR, James AT, Boontje NM, Dekkers DH, Stienen GJ, Lamers JM, Duncker DJ. Alterations in myofilament function contribute to left ventricular dysfunction in pigs early after myocardial infarction. Circ Res. 2004;95:e85-e95. doi: 10.1161/01. RES.0000149531.02904.09.
33. Cai W, Tucholski TM, Gregorich ZR, Ge Y. Top-down proteomics: technology advancements and applications to heart diseases. Expert Rev Proteomics. 2016;13:717-730. doi: 10.1080/14789450.2016.1209414.
34. Yang X, Pabon L, Murry CE. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res. 2014;114:511-523. doi: 10.1161/CIRCRESAHA.114.300558.
35. Jackman CP, Shadrin IY, Carlson AL, Bursac N. Human cardiac tissue engineering: from pluripotent stem cells to heart repair. Curr Opin Chem Eng. 2015;7:57-64. doi: 10.1016/j.coche.2014.11.004.
36. Herron TJ, Lee P, Jalife J. Optical imaging of voltage and calcium in cardiac cells & tissues. Circ Res. 2012;110:609-623. doi: 10.1161/CIRCRESAHA. 111.247494.
37. Kong W, Fakhari N, Sharifov OF, Ideker RE, Smith WM, Fast VG. Optical measurements of intramural action potentials in isolated porcine hearts using optrodes. Heart Rhythm. 2007;4:1430-1436. doi: 10.1016/j. hrthm.2007.07.002.
38. Waits CM, Barr RC, Pollard AE. Sensor spacing affects the tissue impedance spectra of rabbit ventricular epicardium. Am J Physiol Heart Circ Physiol. 2014;306:H1660-H1668. doi: 10.1152/ajpheart.00661.2013.
39. Messer AE, Jacques AM, Marston SB. Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J Mol Cell Cardiol. 2007;42:247-259. doi: 10.1016/j.yjmcc.2006.08.017.