Stem Cells: The Game Changers of Human Cardiac Disease Modelling and Regenerative Medicine
Abstract
:1. Introduction
2. Cardiac Disease Modeling
3. Cardiac Cell Therapy: Variety of Stem Cell Types Investigated
4. Cardiac Adult Cells and Progenitors
5. Pluripotent Stem Cells
6. Direct Reprogramming of Somatic Cells into Functional Cardiomyocytes
7. From 2D to 3D
8. Limitations of iPSCs Technology
9. Genome-Editing Technologies
10. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Piek, A.; de Boer, R.A.; Silljé, H.H.W. The fibrosis-cell death axis in heart failure. Heart Fail. Rev. 2016, 21, 199–211. [Google Scholar] [CrossRef] [PubMed]
- Stewart, S.; MacIntyre, K.; Hole, D.J.; Capewell, S.; McMurray, J.J.V. More “malignant” than cancer? Five-year survival following a first admission for heart failure. Eur. J. Heart Fail. 2001, 3, 315–322. [Google Scholar] [CrossRef]
- Romito, A.; Cobellis, G. Pluripotent stem cells: Current understanding and future directions. Stem Cells Int. 2016. [Google Scholar] [CrossRef] [PubMed]
- Hayashi, M.; Kawaguchi, T.; Durcova-Hills, G.; Imai, H. Generation of germ cells from pluripotent stem cells in mammals. Reprod. Med. Biol. 2018, 17, 107–114. [Google Scholar] [CrossRef]
- Zhu, Z.; Huangfu, D. Human pluripotent stem cells: An emerging model in developmental biology. Development 2013, 140, 705–717. [Google Scholar] [CrossRef]
- Tanaka, A.; Yuasa, S.; Node, K.; Fukuda, K. Cardiovascular disease modeling using patient-specific induced pluripotent stem cells. Int. J. Mol. Sci. 2015, 16, 18894–18922. [Google Scholar] [CrossRef]
- De Angelis, M.T.; Santamaria, G.; Parrotta, E.I.; Scalise, S.; Lo Conte, M.; Gasparini, S.; Ferlazzo, E.; Aguglia, U.; Ciampi, C.; Sgura, A.; et al. Establishment and characterization of induced pluripotent stem cells (iPSCs) from central nervous system lupus erythematosus. J. Cell. Mol. Med. 2019, 23, 7382–7394. [Google Scholar] [CrossRef]
- Singh, V.K.; Kalsan, M.; Kumar, N.; Saini, A.; Chandra, R. Induced pluripotent stem cells: Applications in regenerative medicine, disease modeling, and drug discovery. Front. Cell Dev. Biol. 2015, 3, 1–18. [Google Scholar] [CrossRef]
- Wiegand, C.; Banerjee, I. Recent advances in the applications of iPSC technology. Curr. Opin. Biotechnol. 2019, 60, 250–258. [Google Scholar] [CrossRef]
- Thomson, J.A. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282, 1145–1147. [Google Scholar] [CrossRef]
- Ghosh, D.; Mehta, N.; Patil, A.; Sengupta, J. Ethical issues in biomedical use of human embryonic stem cells (hESCs). J. Reprod. Heal. Med. 2016, 2, S37–S47. [Google Scholar] [CrossRef]
- Halevy, T.; Urbach, A. comparing ESC and iPSC—based models for human genetic disorders. J. Clin. Med. 2014, 3, 1146–1162. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef] [PubMed]
- Yu, J.; Vodyanik, M.; Smuga-Otto, K.; Antosiewicz-Bourget, J.; Frane, J.; Tian, S.; Nie, J.; Jonsdottir, G.; Ruotti, V.; Stewart, R.; et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318, 1917–1920. [Google Scholar] [CrossRef] [PubMed]
- Patel, P.; Mital, S. Stem cells in pediatric cardiology. Eur. J. Pediatr. 2013, 172, 1287–1292. [Google Scholar] [CrossRef]
- Park, S.-J.; Zhang, D.; Qi, Y.; Li, Y.; Lee, K.Y.; Bezzerides, V.J.; Yang, P.; Xia, S.; Kim, S.L.; Liu, X.; et al. Insights into the pathogenesis of catecholaminergic polymorphic ventricular tachycardia from engineered human heart tissue. Circulation 2019, 140, 390–404. [Google Scholar] [CrossRef]
- Kim, C.; Wong, J.; Wen, J.; Wang, S.; Wang, C.; Spiering, S.; Kan, N.G.; Forcales, S.; Puri, P.L.; Leone, T.C.; et al. Studying arrhythmogenic right ventricular dysplasia with patient-specific iPSCs. Nature 2013, 494, 105–110. [Google Scholar] [CrossRef]
- Dorn, T.; Kornherr, J.; Parrotta, E.I.; Zawada, D.; Ayetey, H.; Santamaria, G.; Iop, L.; Mastantuono, E.; Sinnecker, D.; Goedel, A.; et al. Interplay of cell-cell contacts and RhoA/MRTF-A signaling regulates cardiomyocyte identity. EMBO J. 2018. [Google Scholar] [CrossRef]
- Moretti, A.; Bellin, M.; Welling, A.; Jung, C.B.; Lam, J.T.; Bott-Flügel, L.; Dorn, T.; Goedel, A.; Höhnke, C.; Hofmann, F.; et al. Patient-Specific Induced Pluripotent Stem-Cell Models for Long-QT Syndrome. N. Engl. J. Med. 2010, 363, 1397–1409. [Google Scholar] [CrossRef]
- Terrenoire, C.; Wang, K.; Tung, K.W.C.; Chung, W.K.; Pass, R.H.; Lu, J.T.; Jean, J.; Omari, A.; Sampson, K.J.; Kotton, D.N.; et al. Induced pluripotent stem cells used to reveal drug actions in a long QT syndrome family with complex genetics. J. Gen. Physiol. 2013, 141, 61–72. [Google Scholar] [CrossRef]
- Kinnaer, C.; Chang, W.Y.; Khattak, S.; Hinek, A.; Thompson, T.; de Carvalho Rodrigues, D.; Kennedy, K.; Mahmut, N.; Pasceri, P.; Stanford, W.L.; et al. Modeling and rescue of the vascular phenotype of Williams-Beuren syndrome in patient induced pluripotent stem cells Syndrome in Patient Induced Pluripotent Stem Cells. Stem Cells Transl. Med. 2013, 2, 2–15. [Google Scholar] [CrossRef] [PubMed]
- Carvajal-Vergara, X.; Sevilla, A.; Dsouza, S.L.; Ang, Y.S.; Schaniel, C.; Lee, D.F.; Yang, L.; Kaplan, A.D.; Adler, E.D.; Rozov, R.; et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010, 465, 808–812. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Su, X.; Ashraf, M.; Kim, I.; Weintraub, N.L.; Jiang, M.; Tang, Y. Regenerative Therapy for Cardiomyopathies. J. Cardiovasc. Transl. Res. 2018, 2, 357–365. [Google Scholar] [CrossRef] [PubMed]
- Sanganalmath, S.K.; Bolli, R. Cell therapy for heart failure: A comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 2013, 113, 810–834. [Google Scholar] [CrossRef]
- Stamm, C.; Westphal, B.; Kleine, H.D.; Petzsch, M.; Kittner, C.; Klinge, H.; Schümichen, C.; Nienaber, C.A.; Freund, M.; Steinhoff, G. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 2003, 361, 45–46. [Google Scholar] [CrossRef]
- Zannad, F.; Agrinier, N.; Alla, F. Heart failure burden and therapy. Europace 2009, 11, v1–v9. [Google Scholar] [CrossRef]
- Yin, H.; Price, F.; Rudnicki, M.A. Satellite cells and the muscle stem cell niche. Physiol. Rev. 2013, 93, 23–67. [Google Scholar] [CrossRef]
- Durrani, S.; Konoplyannikov, M.; Ashraf, M.; Husnain, K. Skeletal myoblasts for cardiac repair. Regen. Med. 2010, 5, 919–932. [Google Scholar] [CrossRef]
- Hata, H.; Matsumiya, G.; Miyagawa, S.; Kondoh, H.; Kawaguchi, N.; Matsuura, N.; Shimizu, T.; Okano, T.; Matsuda, H.; Sawa, Y. Grafted skeletal myoblast sheets attenuate myocardial remodeling in pacing-induced canine heart failure model. J. Thorac. Cardiovasc. Surg. 2006, 132, 918–924. [Google Scholar] [CrossRef]
- Gavira, J.J.; Nasarre, E.; Abizanda, G.; Pérez-Ilzarbe, M.; De Martino-Rodriguez, A.; García De Jalón, J.A.; Mazo, M.; MacIas, A.; García-Bolao, I.; Pelacho, B.; et al. Repeated implantation of skeletal myoblast in a swine model of chronic myocardial infarction. Eur. Heart J. 2010, 31, 1013–1021. [Google Scholar] [CrossRef]
- Chachques, J.C.; Duarte, F.; Cattadori, B.; Shafy, A.; Lila, N.; Chatellier, G.; Fabiani, J.N.; Carpentier, A.F. Angiogenic growth factors and/or cellular therapy for myocardial regeneration: A comparative study. J. Thorac. Cardiovasc. Surg. 2004, 128, 245–253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Menasché, P.; Hagège, A.A.; Scorsin, M.; Pouzet, B.; Desnos, M.; Duboc, D.; Schwartz, K.; Vilquin, J.-T.; Marolleau, J.-P. Myoblast transplantation for heart failure. Lancet 2001, 357, 279–280. [Google Scholar] [CrossRef]
- Brickwedel, J.; Gulbins, H.; Reichenspurner, H. Long-term follow-up after autologous skeletal myoblast transplantation in ischaemic heart disease. Interact. Cardiovasc. Thorac. Surg. 2014, 18, 61–66. [Google Scholar] [CrossRef] [PubMed]
- Menasché, P.; Alfieri, O.; Janssens, S.; McKenna, W.; Reichenspurner, H.; Trinquart, L.; Vilquin, J.T.; Marolleau, J.P.; Seymour, B.; Larghero, J.; et al. The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: First randomized placebo-controlled study of myoblast transplantation. Circulation 2008, 117, 1189–1200. [Google Scholar] [CrossRef] [Green Version]
- Yoon, Y.S.; Wecker, A.; Heyd, L.; Park, J.S.; Tkebuchava, T.; Kusano, K.; Hanley, A.; Scadova, H.; Qin, G.; Cha, D.H.; et al. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J. Clin. Invest. 2005, 115, 326–338. [Google Scholar] [CrossRef]
- Lunde, K.; Solheim, S.; Aakhus, S.; Arnesen, H.; Abdelnoor, M.; Egeland, T.; Endresen, K.; Ilebekk, A.; Mangschau, A.; Fjeld, J.G.; et al. Intracoronary Injection of Mononuclear Bone Marrow Cells in Acute Myocardial Infarction. N. Engl. J. Med. 2006, 355, 1199–1209. [Google Scholar] [CrossRef]
- Orlic, D.; Kajstura, J.; Chimenti, S.; Jakoniuk, I.; Anderson, S.M.; Li, B.; Pickel, J.; Mckay, R.; Nadal-ginard, B.; Bodine, D.M.; et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001, 410, 701–705. [Google Scholar] [CrossRef]
- Murry, C.E.; Soonpaa, M.H.; Reinecke, H.; Nakajima, H.; Nakajima, H.O.; Rubart, M.; Pasumarthi, K.B.S.; Virag, J.I.; Bartelmez, S.H.; Poppa, V.; et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 2004, 428, 664–668. [Google Scholar] [CrossRef]
- Nygren, J.M.; Jovinge, S.; Breitbach, M.; Säwén, P.; Röll, W.; Hescheler, J.; Taneera, J.; Fleischmann, B.K.; Jacobsen, S.E.W. Bone marrow–derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat. Med. 2004, 10, 494–501. [Google Scholar] [CrossRef] [Green Version]
- Nasseri, B.A.; Ebell, W.; Dandel, M.; Kukucka, M.; Gebker, R.; Doltra, A.; Knosalla, C.; Choi, Y.H.; Hetzer, R.; Stamm, C. Autologous CD133+ bone marrow cells and bypass grafting for regeneration of ischaemic myocardium: The Cardio133 trial. Eur. Heart J. 2014, 35, 1263–1274. [Google Scholar] [CrossRef] [Green Version]
- Karantalis, V.; Schulman, I.H.; Balkan, W.; Hare, J.M. Allogeneic cell therapy: A new paradigm in therapeutics. Circ. Res. 2015, 116, 12–15. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.L.; Fang, W.W.; Ye, F.; Liu, Y.H.; Qian, J.; Shan, S.J.; Zhang, J.J.; Chunhua, R.Z.; Liao, L.M.; Lin, S.; et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am. J. Cardiol. 2004, 94, 92–95. [Google Scholar] [CrossRef] [PubMed]
- Toma, C.; Pittenger, M.F.; Cahill, K.S.; Byrne, B.J.; Kessler, P.D. Human Mesenchymal Stem Cells Differentiate to a Cardiomyocyte Phenotype in the Adult Murine Heart. Circulation 2002, 105, 93–98. [Google Scholar] [CrossRef] [PubMed]
- Wojakowski, W.; Tendera, M.; Michałowska, A.; Majka, M.; Kucia, M.; Maślankiewicz, K.; Wyderka, R.; Ochała, A.; Ratajczak, M.Z. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met + stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 2004, 110, 3213–3220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, P.; Wang, L.; Li, Q.; Xu, J.; Xu, J.; Xiong, Y.; Chen, G.; Qian, H. Combinatorial treatment of acute myocardial infarction using stem cells and their derived exosomes resulted in improved heart performance. Stem Cell Res. Ther. 2019, 10, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Houtgraaf, J.H.; Den Dekker, W.K.; Van Dalen, B.M.; Springeling, T.; De Jong, R.; Van Geuns, R.J.; Geleijnse, M.L.; Zijlsta, F.; Serruys, P.W.; Duckers, H.J. First experience in humans using adipose tissue–derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. JAC 2012, 59, 539–540. [Google Scholar] [CrossRef] [Green Version]
- Henry, T.D.; Pepine, C.J.; Lambert, C.R.; Traverse, J.H.; Schatz, R.; Costa, M.; Povsic, T.J.; Anderson, R.D.; Willerson, J.T.; Kesten, S.; et al. The Athena trials: Autologous adipose-derived regenerative cells for refractory chronic myocardial ischemia with left ventricular dysfunction. Catheter. Cardiovasc. Interv. 2017, 89, 169–177. [Google Scholar] [CrossRef]
- Bergmann, O.; Bhardwaj, R.D.; Bernard, S.; Zdunek, S.; Barnabé-Heider, F.; Walsh, S.; Zupicich, J.; Alkass, K.; Buchholz, B.A.; Druid, H.; et al. Evidence for Cardiomyocyte Renewal in Humans. Science 2009, 324, 98–102. [Google Scholar] [CrossRef] [Green Version]
- Smith, R.R.; Barile, L.; Cho, H.C.; Leppo, M.K.; Hare, J.M.; Messina, E.; Giacomello, A.; Abraham, M.R.; Marbán, E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115, 896–908. [Google Scholar] [CrossRef] [Green Version]
- Matsuura, K.; Nagai, T.; Nishigaki, N.; Oyama, T.; Nishi, J.; Wada, H.; Sano, M.; Toko, H.; Akazawa, H.; Sato, T.; et al. Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J. Biol. Chem. 2004, 279, 11384–11391. [Google Scholar] [CrossRef] [Green Version]
- Laugwitz, K.; Moretti, A.; Lam, J.; Gruber, P.; Chen, Y.; Woodard, S.; Lin, L.-Z.; Cai, C.-L.; Lu, M.M.; Reth, M.; et al. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 443, 647–653. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tallini, Y.N.; Su, K.; Craven, M.; Spealman, A.; Breitbach, M.; Smith, J.; Fisher, P.J.; Steffey, M.; Hesse, M.; Doran, R.M.; et al. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc. Natl. Acad. Sci. USA 2009, 106, 1808–1813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Meier, E.M.; Tian, S.; Lei, I.; Liu, L.; Xian, S.; Lam, M.T.; Wang, Z. Transplantation of Isl1 + cardiac progenitor cells in small intestinal submucosa improves infarcted heart function. Stem Cell Res. Ther. 2017, 8, 230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnston, P.V.; Sasano, T.; Mills, K.; Evers, R.; Lee, S.; Smith, R.R.; Lardo, A.C.; Lai, S.; Steenbergen, C.; Gerstenblith, G.; et al. Engraftment, differentiation, and functional benefits of autologous cardiosphere-derived cells in porcine. Circulation 2009, 120, 1075–1083. [Google Scholar] [CrossRef] [Green Version]
- Wang, S.; Chen, W.; Ma, L.; Zou, M.; Dong, W.; Yang, H.; Sun, L.; Chen, X.; Duan, J.; Yang, W.D.Á.H.; et al. Infant cardiosphere-derived cells exhibit non-durable heart protection in dilated cardiomyopathy rats. Cytotechnology 2019. [Google Scholar] [CrossRef]
- Oh, H.; Bradfute, S.B.; Gallardo, T.D.; Nakamura, T.; Gaussin, V.; Mishina, Y.; Pocius, J.; Michael, L.H.; Behringer, R.R.; Garry, D.J.; et al. Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 2003, 100, 12313–12318. [Google Scholar] [CrossRef] [Green Version]
- Gnecchi, M.; Zhang, Z.; Ni, A.; Dzau, V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 2008, 103, 1204–1219. [Google Scholar] [CrossRef]
- Mirotsou, M.; Jayawardena, T.M.; Schmeckpeper, J.; Gnecchi, M.; Dzau, V.J. Paracrine mechanisms of stem cell reparative and regenerative actions in the heart. J. Mol. Cell. Cardiol. 2011, 50, 280–289. [Google Scholar] [CrossRef] [Green Version]
- Madonna, R.; Van Laake, L.W.; Davidson, S.M.; Engel, F.B.; Hausenloy, D.J.; Lecour, S.; Leor, J.; Perrino, C.; Schulz, R.; Ytrehus, K.; et al. Position Paper of the European Society of Cardiology Working Group Cellular Biology of the Heart: Cell-based therapies for myocardial repair and regeneration in ischemic heart disease and heart failure. Eur. Heart J. 2016, 37, 1789–1798. [Google Scholar] [CrossRef]
- Behfar, A.; Zingman, L.V.; Hodgson, D.M.; Rauzier, J.; Kane, G.C.; Terzic, A.; Pucéat, M. Stem cell differentiation requires a paracrine pathway in the heart. FASEB J. 2002, 16, 1558–1566. [Google Scholar] [CrossRef] [Green Version]
- Caspi, O.; Huber, I.; Kehat, I.; Habib, M.; Arbel, G.; Gepstein, A.; Yankelson, L.; Aronson, D.; Beyar, R.; Gepstein, L. Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J. Am. Coll. Cardiol. 2007, 50, 1884–1893. [Google Scholar] [CrossRef] [PubMed]
- Chong, J.J.H.; Yang, X.; Don, C.W.; Minami, E.; Liu, Y.W.; Weyers, J.J.; Mahoney, W.M.; Van Biber, B.; Cook, S.M.; Palpant, N.J.; et al. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510, 273–277. [Google Scholar] [CrossRef] [PubMed]
- Zhu, K.; Wu, Q.; Ni, C.; Zhang, P.; Zhong, Z.; Wu, Y.; Wang, Y.; Xu, Y.; Kong, M.; Cheng, H.; et al. Lack of remuscularization following transplantation of human embryonic stem cell-derived cardiovascular progenitor cells in infarcted nonhuman primates. Circ. Res. 2018, 122, 958–969. [Google Scholar] [CrossRef] [PubMed]
- Menasché, P.; Vanneaux, V.; Fabreguettes, J.R.; Bel, A.; Tosca, L.; Garcia, S.; Bellamy, V.; Farouz, Y.; Pouly, J.; Damour, O.; et al. Towards a clinical use of human embryonic stem cell-derived cardiac progenitors: A translational experience. Eur. Heart J. 2015, 36, 743–750. [Google Scholar] [CrossRef] [PubMed]
- Robertson, J.A. Human embryonic stem cell research: Ethical and legal issues. Nat. Rev. Genet. 2001, 2, 74–78. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, Y.; Yamanaka, S. Induced pluripotent stem cells 10 years later: For cardiac applications. Circ. Res. 2017, 120, 1958–1968. [Google Scholar] [CrossRef] [PubMed]
- Matsa, E.; Burridge, P.W.; Wu, J.C. Human stem cells for modeling heart disease and for drug discovery. Sci. Transl. Med. 2014, 6, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Matsa, E.; Denning, C. In vitro uses of human pluripotent stem cell-derived cardiomyocytes. J. Cardiovasc. Transl. Res. 2012, 5, 581–592. [Google Scholar] [CrossRef]
- Shiba, Y.; Gomibuchi, T.; Seto, T.; Wada, Y.; Ichimura, H.; Tanaka, Y.; Ogasawara, T.; Okada, K.; Shiba, N.; Sakamoto, K.; et al. Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature 2016, 538, 388–391. [Google Scholar] [CrossRef]
- Qian, L.; Huang, Y.; Spencer, C.I.; Foley, A.; Vedantham, V.; Liu, L.; Conway, S.J.; Fu, J.D.; Srivastava, D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485, 593–598. [Google Scholar] [CrossRef]
- Dattola, E.; Parrotta, I.; Scalise, S.; Perozziello, G.; Limongi, T.; Candeloro, P.; Coluccio, L.; Maletta, C.; Bruno, L.; De Angelis, T.; et al. Development of 3D PVA scaffolds for cardiac tissue engineering and cell screening applications. RSC Adv. 2019, 9, 4246–4257. [Google Scholar] [CrossRef] [Green Version]
- Weinberger, F.; Breckwoldt, K.; Pecha, S.; Kelly, A.; Geertz, B.; Starbatty, J.; Yorgan, T.; Cheng, K.; Lessmann, K.; Stolen, T.; et al. Cardiac repair in guinea pigs with human engineered heart tissue from induced pluripotent stem cells. Sci. Transl. Med. 2016, 148, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Gao, L.; Gregorich, Z.R.; Zhu, W.; Mattapally, S.; Oduk, Y.; Lou, X.; Kannappan, R.; Borovjagin, A.V.; Walcott, G.P.; Pollard, A.E.; et al. Large cardiac muscle patches engineered from human induced-pluripotent stem cell-derived cardiac cells improve recovery from myocardial infarction in swine. Circulation 2018, 137, 1712–1730. [Google Scholar] [CrossRef] [PubMed]
- Parrotta, E.; De Angelis, M.T.; Scalise, S.; Candeloro, P.; Santamaria, G.; Paonessa, M.; Coluccio, M.L.; Perozziello, G.; De Vitis, S.; Sgura, A.; et al. Two sides of the same coin? Unraveling subtle differences between human embryonic and induced pluripotent stem cells by Raman spectroscopy. Stem Cell Res. Ther. 2017, 8, 271. [Google Scholar] [CrossRef] [Green Version]
- Orban, M.; Goedel, A.; Haas, J.; Sandrock-Lang, K.; Gartner, F.; Jung, C.B.; Zieger, B.; Parrotta, E.; Kurnik, K.; Sinnecker, D.; et al. Functional comparison of induced pluripotent stem cell- and blood-derived GPIIbIIIa deficient platelets. PLoS ONE 2015, 10, e0115978. [Google Scholar] [CrossRef] [Green Version]
- Parrotta, E.I.; Scalise, S.; Taverna, D.; De Angelis, M.T.; Sarro, G.; Gaspari, M.; Santamaria, G.; Cuda, G. Comprehensive proteogenomic analysis of human embryonic and induced pluripotent stem cells. J. Cell. Mol. Med. 2019, 23, 5440–5453. [Google Scholar] [CrossRef] [Green Version]
- De Angelis, M.T.; Parrotta, E.I.; Santamaria, G.; Cuda, G. Short-term retinoic acid treatment sustains pluripotency and suppresses differentiation of human induced pluripotent stem cells. Cell Death Dis. 2018, 9, 6. [Google Scholar] [CrossRef]
- Mauritz, C.; Martens, A.; Rojas, S.V.; Schnick, T.; Rathert, C.; Schecker, N.; Menke, S.; Glage, S.; Zweigerdt, R.; Haverich, A.; et al. Induced pluripotent stem cell (iPSC)-derived Flk-1 progenitor cells engraft, differentiate, and improve heart function in a mouse model of acute myocardial infarction. Eur. Heart J. 2011, 32, 2634–2641. [Google Scholar] [CrossRef] [Green Version]
- Kawamura, M.; Miyagawa, S.; Miki, K.; Saito, A.; Fukushima, S.; Higuchi, T.; Kawamura, T.; Kuratani, T.; Daimon, T.; Shimizu, T.; et al. Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model. Circulation 2012, 126, 29–37. [Google Scholar] [CrossRef] [Green Version]
- Lee, A.S.; Tang, C.; Rao, M.S.; Weissman, I.L.; Wu, J.C. Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat. Med. 2013, 19, 998–1004. [Google Scholar] [CrossRef] [Green Version]
- Tapia, N.; Schöler, H.R. Molecular obstacles to clinical translation of iPSCs. Cell Stem Cell 2016, 19, 298–309. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoshihara, M.; Hayashizaki, Y.; Murakawa, Y. Genomic instability of iPSCs: Challenges towards their clinical applications. Stem Cell Rev. Rep. 2017, 13, 7–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karakikes, I.; Ameen, M.; Termglinchan, V.; Wu, J.C. Human induced pluripotent stem cell–derived cardiomyocytes insights into molecular, cellular, and functional phenotypes. Circ. Res. 2015, 117, 80–88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masoudpour, H.; Laflamme, M.A. Cardiac repair with pluripotent stem cell–derived cardiomyocytes: Proof of concept but new challenges. J. Thorac. Cardiovasc. Surg. 2017, 154, 945–948. [Google Scholar] [CrossRef] [PubMed]
- Machiraju, P.; Greenway, S.C. Current methods for the maturation of induced pluripotent stem cell derived cardiomyocytes. World J. Stem Cells 2019, 11, 33–43. [Google Scholar] [CrossRef]
- Wu, S.M.; Hochedlinger, K. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat. Publ. Gr. 2011, 13, 497–505. [Google Scholar]
- Hartman, M.E.; Dai, D.; La, M.A. Human pluripotent stem cells: Prospects and challenges as a source of cardiomyocytes for in vitro modeling and cell-based cardiac repair. Adv. Drug Deliv. Rev. 2016, 96, 3–17. [Google Scholar] [CrossRef] [Green Version]
- Kong, C.; Akar, F.G.; Li, R.A. Translational potential of human embryonic and induced pluripotent stem cells for myocardial repair: Insights from experimental models. Thromb. Haemost. 2010, 104, 30–38. [Google Scholar] [CrossRef] [Green Version]
- Kehat, I.; Kenyagin-Karsenti, D.; Snir, M.; Segev, H.; Amit, M.; Gepstein, A.; Livne, E.; Binah, O.; Itskovitz-Eldor, J.; Gepstein, L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 2001, 108, 407–414. [Google Scholar] [CrossRef]
- Kattman, S.J.; Witty, A.D.; Gagliardi, M.; Dubois, N.C.; Niapour, M.; Hotta, A.; Ellis, J.; Keller, G. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell. 2011, 8, 228–240. [Google Scholar] [CrossRef] [Green Version]
- Yang, L.; Soonpaa, M.H.; Adler, E.D.; Roepke, T.K.; Kattman, S.J.; Kennedy, M.; Henckaerts, E.; Bonham, K.; Abbott, G.W.; Linden, R.M.; et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453, 524–528. [Google Scholar] [CrossRef] [PubMed]
- Willems, E.; Spiering, S.; Davidovics, H.; Lanier, M.; Xia, Z.; Dawson, M.; Cashman, J.; Mercola, M. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res. 2011, 109, 360–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elliott, D.A.; Braam, S.R.; Koutsis, K.; Ng, E.S.; Jenny, R.; Lagerqvist, E.L.; Biben, C.; Hatzistavrou, T.; Hirst, C.E.; Yu, Q.C.; et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat. Methods 2011, 8, 1037–1040. [Google Scholar] [CrossRef] [PubMed]
- Burridge, P.W.; Anderson, D.; Priddle, H.; Barbadillo Muñoz, M.D.; Chamberlain, S.; Allegrucci, C.; Young, L.E.; Denning, C. Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells 2007, 25, 929–938. [Google Scholar] [CrossRef] [PubMed]
- Burridge, P.W.; Thompson, S.; Millrod, M.A.; Weinberg, S.; Yuan, X.; Peters, A.; Mahairaki, V.; Koliatsos, V.E.; Tung, L.; Zambidis, E.T. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS ONE 2011, 6, e18293. [Google Scholar] [CrossRef] [PubMed]
- Hudson, J.; Titmarsh, D.; Hidalgo, A.; Wolvetang, E.; Cooper-White, J. Primitive cardiac cells from human embryonic stem cells. Stem Cells Dev. 2012, 21, 1513–1523. [Google Scholar] [CrossRef] [PubMed]
- Uosaki, H.; Fukushima, H.; Takeuchi, A.; Matsuoka, S.; Nakatsuji, N.; Yamanaka, S.; Yamashita, J.K. Efficient and scalable purification of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS ONE 2011, 6, e23657. [Google Scholar] [CrossRef]
- Laflamme, M.A.; Chen, K.Y.; Naumova, A.V.; Muskheli, V.; Fugate, J.A.; Dupras, S.K.; Reinecke, H.; Xu, C.; Hassanipour, M.; Police, S.; et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 2007, 25, 1015–1024. [Google Scholar] [CrossRef]
- Zhang, Q.; Jiang, J.; Han, P.; Yuan, Q.; Zhang, J.; Zhang, X.; Xu, Y.; Cao, H.; Meng, Q.; Chen, L.; et al. Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res. 2011, 21, 579–587. [Google Scholar] [CrossRef] [Green Version]
- Palpant, N.J.; Pabon, L.; Friedman, C.E.; Roberts, M.; Hadland, B.; Zaunbrecher, R.J.; Bernstein, I.; Zheng, Y.; Murry, C. Generating high-purity cardiac and endothelial derivatives from patterned mesoderm using human pluripotent stem cells. Nat. Protoc. 2017, 12, 5–31. [Google Scholar] [CrossRef] [Green Version]
- Passier, R.; Oostwaard, D.W.; Snapper, J.; Kloots, J.; Hassink, R.J.; Kuijk, E.; Roelen, B.; de la Riviere, A.B.; Mummery, C. Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 2005, 23, 772–780. [Google Scholar] [CrossRef] [PubMed]
- Graichen, R.; Xu, X.; Braam, S.R.; Balakrishnan, T.; Norfiza, S.; Sieh, S.; Soo, S.Y.; Tham, S.C.; Mummery, C.; Colman, A.; et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 2008, 76, 357–370. [Google Scholar] [CrossRef] [PubMed]
- Freund, C.; Davis, R.P.; Gkatzis, K.; Ward-van Oostwaard, D.; Mummery, C.L. The first reported generation of human induced pluripotent stem cells (iPS cells) and iPS cell-derived cardiomyocytes in the Netherlands. Neth. Heart J. 2010, 18, 51–54. [Google Scholar] [PubMed]
- Paige, S.L.; Plonowska, K.; Xu, A.; Wu, S.M. Molecular regulation of cardiomyocyte differentiation. Circ. Res. 2015, 116, 341–353. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.H.; Protze, S.I.; Laksman, Z.; Backx, P.H.; Keller, G.M. Human pluripotent stem cell-derived atrial and ventricular cardiomyocytes develop from distinct mesoderm populations. Cell Stem Cell 2017, 21, 179–194. [Google Scholar] [CrossRef]
- Cai, W.; Zhang, J.; De Lange, W.J.; Gregorich, Z.R.; Karp, H.; Emily, T.; Mitchell, S.D.; Tucholski, T.; Lin, Z.; Biermann, M.; et al. An unbiased proteomics method to assess the maturation of human pluripotent stem cell-derived cardiomyocytes. Circ. Res. 2019, 125, 936–953. [Google Scholar] [CrossRef]
- Collin, J.; Lako, M. Concise Review: Putting a Finger on Stem Cell Biology: Zinc Finger Nuclease-Driven Targeted Genetic Editing in Human Pluripotent Stem Cells. Stem Cells 2011, 29, 1021–1033. [Google Scholar] [CrossRef]
- Seeger, T.; Porteus, M.; Wu, J.C. Genome editing in cardiovascular biology. Circ. Res. 2017, 120, 778–780. [Google Scholar] [CrossRef] [Green Version]
- Riele, A.S.J.M.; Agullo-pascual, E.; James, C.A.; Leo-macias, A.; Cerrone, M.; Zhang, M.; Lin, X.; Lin, B.; Rothenberg, E.; Sobreira, N.L.; et al. Multilevel analyses of SCN5A mutations in arrhythmogenic right ventricular dysplasia/ cardiomyopathy suggest non-canonical mechanisms for disease pathogenesis. Cardiovasc. Res. 2017, 113, 102–111. [Google Scholar] [CrossRef]
Method | Molecules for mesoderm and cardiac specification | Ref. |
---|---|---|
⮚ FGF2, FGF2, BMP4, VEGFA, Dorsomorphin, SB431542, DKK1 | Kehat et al. 2001 [89] | |
⮚ BMP4, Activin A, bFGF, VEGF, DKK1 | Kattman et al. 2011 [90] | |
⮚ FGF2, FGF2, BMP4, IWR1, Triiodothyronine | Yang et al. 2008 [91] | |
Willems et al. 2011 [92] | ||
⮚ Activin A, bFGF, BMP4, SCF, VEGF, LI-BEL | Elliott et al. 2011 [93] | |
⮚ BMP4, Activin A, bFGF, VEGF, DKK1 | Burridge et al. 2007 [94] | |
⮚ FGF2, FGF2, BMP4, IWR1, Triiodothyronine | Burridge et al. 2011 [95] | |
⮚ Activin A, BMP4, IWR1 or IWR4 | Hudson et al. 2011 [96] | |
⮚ Activin A, BMP4, FGF2, VEGFA, DKK1 | Uosaki et al. 2011 [97] | |
⮚ Activin A, BMP4 | Laflamme et al., 2007 [98] | |
⮚ Activin A, BMP4, FGF2, RAi, Noggin, DKK1 | Zhang et al. 2011 [99] | |
⮚ CHIR99021, Activin A, BMP4, XAV-939 | Palpant et al. 2016 [100] | |
⮚ Insulin depletion, PGI2, p38 MAPK inhibition | Passier et al. 2005 [101] | |
Graichen et al. 2008 [102] | ||
Freund et al. 2010 [103] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Parrotta, E.I.; Scalise, S.; Scaramuzzino, L.; Cuda, G. Stem Cells: The Game Changers of Human Cardiac Disease Modelling and Regenerative Medicine. Int. J. Mol. Sci. 2019, 20, 5760. https://doi.org/10.3390/ijms20225760
Parrotta EI, Scalise S, Scaramuzzino L, Cuda G. Stem Cells: The Game Changers of Human Cardiac Disease Modelling and Regenerative Medicine. International Journal of Molecular Sciences. 2019; 20(22):5760. https://doi.org/10.3390/ijms20225760
Chicago/Turabian StyleParrotta, Elvira Immacolata, Stefania Scalise, Luana Scaramuzzino, and Giovanni Cuda. 2019. "Stem Cells: The Game Changers of Human Cardiac Disease Modelling and Regenerative Medicine" International Journal of Molecular Sciences 20, no. 22: 5760. https://doi.org/10.3390/ijms20225760