Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Organoid Models of Heart Diseases: Find a New Channel in Improvements of Cardiac Regenerative Medicine

Author(s): Saade Abdalkareem Jasim, Dmitry Olegovich Bokov*, Wanich Suksatan, Fahad Alsaikhan, Mohammed Abed Jawad, Satish Kumar Sharma, Supat Chupradit and Lakshmi Thangavelu

Volume 30, Issue 33, 2023

Published on: 28 December, 2022

Page: [3726 - 3742] Pages: 17

DOI: 10.2174/0929867330666221021122603

Price: $65

conference banner
Abstract

We are experiencing a revolution in regenerative medicine. Recent developments in organoid technology have provided unique opportunities for studying human biology and diseases. Indeed, organoid models have revolutionized the in vitro culture tools for biomedical research by creating robust three-dimensional (3D) architecture to recapitulate the primary tissues' cellular heterogeneity, structure, and functions. Such organoid technology enables researchers to re-create human organs and diseases model in a culture dish. It thus holds excellent promises for many translational applications such as regenerative medicine, drug discovery, and precision medicine. This review summarizes the current knowledge on the progression and promotion of organoid models, particularly with the heart disease approach. We discuss the usefulness of clinical applications of cardiac organoids and ultimately highlight the currently advanced therapeutic strategies in vitro model of organoids aimed at personalizing heart disease treatment.

Keywords: Cardiac organoid, heart diseases, regenerative medicine, organoid technology, drug discovery, personalizing heart disease treatment.

[1]
Marks, P.; Gottlieb, S. Balancing safety and innovation for cell-based regenerative medicine. N. Engl. J. Med., 2018, 378(10), 954-959.
[http://dx.doi.org/10.1056/NEJMsr1715626] [PMID: 29514023]
[2]
Mills, R.J.; Parker, B.L.; Quaife-Ryan, G.A.; Voges, H.K.; Needham, E.J.; Bornot, A.; Ding, M.; Andersson, H.; Polla, M.; Elliott, D.A.; Drowley, L.; Clausen, M.; Plowright, A.T.; Barrett, I.P.; Wang, Q.D.; James, D.E.; Porrello, E.R.; Hudson, J.E. Drug screening in human PSC-cardiac organoids identifies pro-proliferative compounds acting via the mevalonate pathway. Cell Stem Cell, 2019, 24(6), 895-907.e6.
[http://dx.doi.org/10.1016/j.stem.2019.03.009] [PMID: 30930147]
[3]
Boström, P.; Frisén, J. New cells in old hearts. N. Engl. J. Med., 2013, 368(14), 1358-1360.
[http://dx.doi.org/10.1056/NEJMcibr1300157] [PMID: 23550676]
[4]
Parmacek, M.S.; Epstein, J.A. Cardiomyocyte renewal. N. Engl. J. Med., 2009, 361(1), 86-88.
[http://dx.doi.org/10.1056/NEJMcibr0903347] [PMID: 19571289]
[5]
Roth, G.A.; Mensah, G.A.; Johnson, C.O.; Addolorato, G.; Ammirati, E.; Baddour, L.M.; Barengo, N.C.; Beaton, A.Z.; Benjamin, E.J.; Benziger, C.P.; Bonny, A.; Brauer, M.; Brodmann, M.; Cahill, T.J.; Carapetis, J.; Catapano, A.L.; Chugh, S.S.; Cooper, L.T.; Coresh, J.; Criqui, M.; DeCleene, N.; Eagle, K.A.; Emmons-Bell, S.; Feigin, V.L.; Fernández-Solà, J.; Fowkes, G.; Gakidou, E.; Grundy, S.M.; He, F.J.; Howard, G.; Hu, F.; Inker, L.; Karthikeyan, G.; Kassebaum, N.; Koroshetz, W.; Lavie, C.; Lloyd-Jones, D.; Lu, H.S.; Mirijello, A.; Temesgen, A.M.; Mokdad, A.; Moran, A.E.; Muntner, P.; Narula, J.; Neal, B.; Ntsekhe, M.; Moraes de Oliveira, G.; Otto, C.; Owolabi, M.; Pratt, M.; Rajagopalan, S.; Reitsma, M.; Ribeiro, A.L.P.; Rigotti, N.; Rodgers, A.; Sable, C.; Shakil, S.; Sliwa-Hahnle, K.; Stark, B.; Sundström, J.; Timpel, P.; Tleyjeh, I.M.; Valgimigli, M.; Vos, T.; Whelton, P.K.; Yacoub, M.; Zuhlke, L.; Murray, C.; Fuster, V.; Roth, G.A.; Mensah, G.A.; Johnson, C.O.; Addolorato, G.; Ammirati, E.; Baddour, L.M.; Barengo, N.C.; Beaton, A.; Benjamin, E.J.; Benziger, C.P.; Bonny, A.; Brauer, M.; Brodmann, M.; Cahill, T.J.; Carapetis, J.R.; Catapano, A.L.; Chugh, S.; Cooper, L.T.; Coresh, J.; Criqui, M.H.; DeCleene, N.K.; Eagle, K.A.; Emmons-Bell, S.; Feigin, V.L.; Fernández-Sola, J.; Fowkes, F.G.R.; Gakidou, E.; Grundy, S.M.; He, F.J.; Howard, G.; Hu, F.; Inker, L.; Karthikeyan, G.; Kassebaum, N.J.; Koroshetz, W.J.; Lavie, C.; Lloyd-Jones, D.; Lu, H.S.; Mirijello, A.; Misganaw, A.T.; Mokdad, A.H.; Moran, A.E.; Muntner, P.; Narula, J.; Neal, B.; Ntsekhe, M.; Oliveira, G.M.M.; Otto, C.M.; Owolabi, M.O.; Pratt, M.; Rajagopalan, S.; Reitsma, M.B.; Ribeiro, A.L.P.; Rigotti, N.A.; Rodgers, A.; Sable, C.A.; Shakil, S.S.; Sliwa, K.; Stark, B.A.; Sundström, J.; Timpel, P.; Tleyjeh, I.I.; Valgimigli, M.; Vos, T.; Whelton, P.K.; Yacoub, M.; Zuhlke, L.J.; Abbasi-Kangevari, M.; Abdi, A.; Abedi, A.; Aboyans, V.; Abrha, W.A.; Abu-Gharbieh, E.; Abushouk, A.I.; Acharya, D.; Adair, T.; Adebayo, O.M.; Ademi, Z.; Advani, S.M.; Afshari, K.; Afshin, A.; Agarwal, G.; Agasthi, P.; Ahmad, S.; Ahmadi, S.; Ahmed, M.B.; Aji, B.; Akalu, Y.; Akande-Sholabi, W.; Aklilu, A.; Akunna, C.J.; Alahdab, F.; Al-Eyadhy, A.; Alhabib, K.F.; Alif, S.M.; Alipour, V.; Aljunid, S.M.; Alla, F.; Almasi-Hashiani, A.; Almustanyir, S.; Al-Raddadi, R.M.; Amegah, A.K.; Amini, S.; Aminorroaya, A.; Amu, H.; Amugsi, D.A.; Ancuceanu, R.; Anderlini, D.; Andrei, T.; Andrei, C.L.; Ansari-Moghaddam, A.; Anteneh, Z.A.; Antonazzo, I.C.; Antony, B.; Anwer, R.; Appiah, L.T.; Arabloo, J.; Ärnlöv, J.; Artanti, K.D.; Ataro, Z.; Ausloos, M.; Avila-Burgos, L.; Awan, A.T.; Awoke, M.A.; Ayele, H.T.; Ayza, M.A.; Azari, S.; B, D.B.; Baheiraei, N.; Baig, A.A.; Bakhtiari, A.; Banach, M.; Banik, P.C.; Baptista, E.A.; Barboza, M.A.; Barua, L.; Basu, S.; Bedi, N.; Béjot, Y.; Bennett, D.A.; Bensenor, I.M.; Berman, A.E.; Bezabih, Y.M.; Bhagavathula, A.S.; Bhaskar, S.; Bhattacharyya, K.; Bijani, A.; Bikbov, B.; Birhanu, M.M.; Boloor, A.; Brant, L.C.; Brenner, H.; Briko, N.I.; Butt, Z.A.; Caetano dos Santos, F.L.; Cahill, L.E.; Cahuana-Hurtado, L.; Cámera, L.A.; Campos-Nonato, I.R.; Cantu-Brito, C.; Car, J.; Carrero, J.J.; Carvalho, F.; Castañeda-Orjuela, C.A.; Catalá-López, F.; Cerin, E.; Charan, J.; Chattu, V.K.; Chen, S.; Chin, K.L.; Choi, J-Y.J.; Chu, D-T.; Chung, S-C.; Cirillo, M.; Coffey, S.; Conti, S.; Costa, V.M.; Cundiff, D.K.; Dadras, O.; Dagnew, B.; Dai, X.; Damasceno, A.A.M.; Dandona, L.; Dandona, R.; Davletov, K.; De la Cruz-Góngora, V.; De la Hoz, F.P.; De Neve, J-W.; Denova-Gutiérrez, E.; Derbew Molla, M.; Derseh, B.T.; Desai, R.; Deuschl, G.; Dharmaratne, S.D.; Dhimal, M.; Dhungana, R.R.; Dianatinasab, M.; Diaz, D.; Djalalinia, S.; Dokova, K.; Douiri, A.; Duncan, B.B.; Duraes, A.R.; Eagan, A.W.; Ebtehaj, S.; Eftekhari, A.; Eftekharzadeh, S.; Ekholuenetale, M.; El Nahas, N.; Elgendy, I.Y.; Elhadi, M.; El-Jaafary, S.I.; Esteghamati, S.; Etisso, A.E.; Eyawo, O.; Fadhil, I.; Faraon, E.J.A.; Faris, P.S.; Farwati, M.; Farzadfar, F.; Fernandes, E.; Fernandez Prendes, C.; Ferrara, P.; Filip, I.; Fischer, F.; Flood, D.; Fukumoto, T.; Gad, M.M.; Gaidhane, S.; Ganji, M.; Garg, J.; Gebre, A.K.; Gebregiorgis, B.G.; Gebregzabiher, K.Z.; Gebremeskel, G.G.; Getacher, L.; Obsa, A.G.; Ghajar, A.; Ghashghaee, A.; Ghith, N.; Giampaoli, S.; Gilani, S.A.; Gill, P.S.; Gillum, R.F.; Glushkova, E.V.; Gnedovskaya, E.V.; Golechha, M.; Gonfa, K.B.; Goudarzian, A.H.; Goulart, A.C.; Guadamuz, J.S.; Guha, A.; Guo, Y.; Gupta, R.; Hachinski, V.; Hafezi-Nejad, N.; Haile, T.G.; Hamadeh, R.R.; Hamidi, S.; Hankey, G.J.; Hargono, A.; Hartono, R.K.; Hashemian, M.; Hashi, A.; Hassan, S.; Hassen, H.Y.; Havmoeller, R.J.; Hay, S.I.; Hayat, K.; Heidari, G.; Herteliu, C.; Holla, R.; Hosseini, M.; Hosseinzadeh, M.; Hostiuc, M.; Hostiuc, S.; Househ, M.; Huang, J.; Humayun, A.; Iavicoli, I.; Ibeneme, C.U.; Ibitoye, S.E.; Ilesanmi, O.S.; Ilic, I.M.; Ilic, M.D.; Iqbal, U.; Irvani, S.S.N.; Islam, S.M.S.; Islam, R.M.; Iso, H.; Iwagami, M.; Jain, V.; Javaheri, T.; Jayapal, S.K.; Jayaram, S.; Jayawardena, R.; Jeemon, P.; Jha, R.P.; Jonas, J.B.; Jonnagaddala, J.; Joukar, F.; Jozwiak, J.J.; Jürisson, M.; Kabir, A.; Kahlon, T.; Kalani, R.; Kalhor, R.; Kamath, A.; Kamel, I.; Kandel, H.; Kandel, A.; Karch, A.; Kasa, A.S.; Katoto, P.D.M.C.; Kayode, G.A.; Khader, Y.S.; Khammarnia, M.; Khan, M.S.; Khan, M.N.; Khan, M.; Khan, E.A.; Khatab, K.; Kibria, G.M.A.; Kim, Y.J.; Kim, G.R.; Kimokoti, R.W.; Kisa, S.; Kisa, A.; Kivimäki, M.; Kolte, D.; Koolivand, A.; Korshunov, V.A.; Koulmane Laxminarayana, S.L.; Koyanagi, A.; Krishan, K.; Krishnamoorthy, V.; Kuate Defo, B.; Kucuk Bicer, B.; Kulkarni, V.; Kumar, G.A.; Kumar, N.; Kurmi, O.P.; Kusuma, D.; Kwan, G.F.; La Vecchia, C.; Lacey, B.; Lallukka, T.; Lan, Q.; Lasrado, S.; Lassi, Z.S.; Lauriola, P.; Lawrence, W.R.; Laxmaiah, A.; LeGrand, K.E.; Li, M-C.; Li, B.; Li, S.; Lim, S.S.; Lim, L-L.; Lin, H.; Lin, Z.; Lin, R-T.; Liu, X.; Lopez, A.D.; Lorkowski, S.; Lotufo, P.A.; Lugo, A.; M, N.K.; Madotto, F.; Mahmoudi, M.; Majeed, A.; Malekzadeh, R.; Malik, A.A.; Mamun, A.A.; Manafi, N.; Mansournia, M.A.; Mantovani, L.G.; Martini, S.; Mathur, M.R.; Mazzaglia, G.; Mehata, S.; Mehndiratta, M.M.; Meier, T.; Menezes, R.G.; Meretoja, A.; Mestrovic, T.; Miazgowski, B.; Miazgowski, T.; Michalek, I.M.; Miller, T.R.; Mirrakhimov, E.M.; Mirzaei, H.; Moazen, B.; Moghadaszadeh, M.; Mohammad, Y.; Mohammad, D.K.; Mohammed, S.; Mohammed, M.A.; Mokhayeri, Y.; Molokhia, M.; Montasir, A.A.; Moradi, G.; Moradzadeh, R.; Moraga, P.; Morawska, L.; Moreno Velásquez, I.; Morze, J.; Mubarik, S.; Muruet, W.; Musa, K.I.; Nagarajan, A.J.; Nalini, M.; Nangia, V.; Naqvi, A.A.; Narasimha Swamy, S.; Nascimento, B.R.; Nayak, V.C.; Nazari, J.; Nazarzadeh, M.; Negoi, R.I.; Neupane Kandel, S.; Nguyen, H.L.T.; Nixon, M.R.; Norrving, B.; Noubiap, J.J.; Nouthe, B.E.; Nowak, C.; Odukoya, O.O.; Ogbo, F.A.; Olagunju, A.T.; Orru, H.; Ortiz, A.; Ostroff, S.M.; Padubidri, J.R.; Palladino, R.; Pana, A.; Panda-Jonas, S.; Parekh, U.; Park, E-C.; Parvizi, M.; Pashazadeh Kan, F.; Patel, U.K.; Pathak, M.; Paudel, R.; Pepito, V.C.F.; Perianayagam, A.; Perico, N.; Pham, H.Q.; Pilgrim, T.; Piradov, M.A.; Pishgar, F.; Podder, V.; Polibin, R.V.; Pourshams, A.; Pribadi, D.R.A.; Rabiee, N.; Rabiee, M.; Radfar, A.; Rafiei, A.; Rahim, F.; Rahimi-Movaghar, V.; Ur Rahman, M.H.; Rahman, M.A.; Rahmani, A.M.; Rakovac, I.; Ram, P.; Ramalingam, S.; Rana, J.; Ranasinghe, P.; Rao, S.J.; Rathi, P.; Rawal, L.; Rawasia, W.F.; Rawassizadeh, R.; Remuzzi, G.; Renzaho, A.M.N.; Rezapour, A.; Riahi, S.M.; Roberts-Thomson, R.L.; Roever, L.; Rohloff, P.; Romoli, M.; Roshandel, G.; Rwegerera, G.M.; Saadatagah, S.; Saber-Ayad, M.M.; Sabour, S.; Sacco, S.; Sadeghi, M.; Saeedi Moghaddam, S.; Safari, S.; Sahebkar, A.; Salehi, S.; Salimzadeh, H.; Samaei, M.; Samy, A.M.; Santos, I.S.; Santric-Milicevic, M.M.; Sarrafzadegan, N.; Sarveazad, A.; Sathish, T.; Sawhney, M.; Saylan, M.; Schmidt, M.I.; Schutte, A.E.; Senthilkumaran, S.; Sepanlou, S.G.; Sha, F.; Shahabi, S.; Shahid, I.; Shaikh, M.A.; Shamali, M.; Shamsizadeh, M.; Shawon, M.S.R.; Sheikh, A.; Shigematsu, M.; Shin, M-J.; Shin, J.I.; Shiri, R.; Shiue, I.; Shuval, K.; Siabani, S.; Siddiqi, T.J.; Silva, D.A.S.; Singh, J.A.; Mtech, A.S.; Skryabin, V.Y.; Skryabina, A.A.; Soheili, A.; Spurlock, E.E.; Stockfelt, L.; Stortecky, S.; Stranges, S.; Suliankatchi Abdulkader, R.; Tadbiri, H.; Tadesse, E.G.; Tadesse, D.B.; Tajdini, M.; Tariqujjaman, M.; Teklehaimanot, B.F.; Temsah, M-H.; Tesema, A.K.; Thakur, B.; Thankappan, K.R.; Thapar, R.; Thrift, A.G.; Timalsina, B.; Tonelli, M.; Touvier, M.; Tovani-Palone, M.R.; Tripathi, A.; Tripathy, J.P.; Truelsen, T.C.; Tsegay, G.M.; Tsegaye, G.W.; Tsilimparis, N.; Tusa, B.S.; Tyrovolas, S.; Umapathi, K.K.; Unim, B.; Unnikrishnan, B.; Usman, M.S.; Vaduganathan, M.; Valdez, P.R.; Vasankari, T.J.; Velazquez, D.Z.; Venketasubramanian, N.; Vu, G.T.; Vujcic, I.S.; Waheed, Y.; Wang, Y.; Wang, F.; Wei, J.; Weintraub, R.G.; Weldemariam, A.H.; Westerman, R.; Winkler, A.S.; Wiysonge, C.S.; Wolfe, C.D.A.; Wubishet, B.L.; Xu, G.; Yadollahpour, A.; Yamagishi, K.; Yan, L.L.; Yandrapalli, S.; Yano, Y.; Yatsuya, H.; Yeheyis, T.Y.; Yeshaw, Y.; Yilgwan, C.S.; Yonemoto, N.; Yu, C.; Yusefzadeh, H.; Zachariah, G.; Zaman, S.B.; Zaman, M.S.; Zamanian, M.; Zand, R.; Zandifar, A.; Zarghi, A.; Zastrozhin, M.S.; Zastrozhina, A.; Zhang, Z-J.; Zhang, Y.; Zhang, W.; Zhong, C.; Zou, Z.; Zuniga, Y.M.H.; Murray, C.J.L.; Fuster, V. Global burden of cardiovascular diseases and risk factors, 1990-2019. J. Am. Coll. Cardiol., 2020, 76(25), 2982-3021.
[http://dx.doi.org/10.1016/j.jacc.2020.11.010] [PMID: 33309175]
[6]
Kerr, C.M.; Richards, D.; Menick, D.R.; Deleon-Pennell, K.Y.; Mei, Y. Multicellular human cardiac organoids transcriptomically model distinct tissue-level features of adult myocardium. Int. J. Mol. Sci., 2021, 22(16), 8482.
[http://dx.doi.org/10.3390/ijms22168482] [PMID: 34445185]
[7]
Valizadeh, A.; Asghari, S.; Mansouri, P.; Alemi, F.; Majidinia, M.; Mahmoodpoor, A.; Yousefi, B. The roles of signaling pathways in cardiac regeneration. Curr. Med. Chem., 2021, 29(12), 2142-2166.
[http://dx.doi.org/10.2174/0929867328666210914115411] [PMID: 34521319]
[8]
Blau, H.M.; Daley, G.Q. Stem cells in the treatment of disease. N. Engl. J. Med., 2019, 380(18), 1748-1760.
[http://dx.doi.org/10.1056/NEJMra1716145] [PMID: 31042827]
[9]
Shewale, B.; Dubois, N. Of form and function: Early cardiac morphogenesis across classical and emerging model systems. Semin. Cell Dev. Biol., 2021, 118, 107-118.
[http://dx.doi.org/10.1016/j.semcdb.2021.04.025] [PMID: 33994301]
[10]
Li, M.; Izpisua Belmonte, J.C. Organoids - preclinical models of human disease. N. Engl. J. Med., 2019, 380(6), 569-579.
[http://dx.doi.org/10.1056/NEJMra1806175] [PMID: 30726695]
[11]
Brassard, J.A.; Lutolf, M.P. Engineering stem cell self-organization to build better organoids. Cell Stem Cell, 2019, 24(6), 860-876.
[http://dx.doi.org/10.1016/j.stem.2019.05.005] [PMID: 31173716]
[12]
Sun, Y.; Ding, Q. Genome engineering of stem cell organoids for disease modeling. Protein Cell, 2017, 8(5), 315-327.
[http://dx.doi.org/10.1007/s13238-016-0368-0] [PMID: 28102490]
[13]
Garreta, E.; Kamm, R.D.; Chuva de Sousa Lopes, S.M.; Lancaster, M.A.; Weiss, R.; Trepat, X.; Hyun, I.; Montserrat, N. Rethinking organoid technology through bioengineering. Nat. Mater., 2021, 20(2), 145-155.
[http://dx.doi.org/10.1038/s41563-020-00804-4] [PMID: 33199860]
[14]
Lancaster, M.A.; Huch, M. Disease modelling in human organoids. Dis. Model. Mech., 2019, 12(7), dmm039347.
[http://dx.doi.org/10.1242/dmm.039347] [PMID: 31383635]
[15]
Streuli, C.H.; Bissell, M.J. Expression of extracellular matrix components is regulated by substratum. J. Cell Biol., 1990, 110(4), 1405-1415.
[http://dx.doi.org/10.1083/jcb.110.4.1405] [PMID: 2182652]
[16]
Fatehullah, A.; Tan, S.H.; Barker, N. Organoids as an in vitro model of human development and disease. Nat. Cell Biol., 2016, 18(3), 246-254.
[http://dx.doi.org/10.1038/ncb3312] [PMID: 26911908]
[17]
Clevers, H. Modeling development and disease with organoids. Cell, 2016, 165(7), 1586-1597.
[http://dx.doi.org/10.1016/j.cell.2016.05.082] [PMID: 27315476]
[18]
Srivastava, D. Modeling human cardiac chambers with organoids. N. Engl. J. Med., 2021, 385(9), 847-849.
[http://dx.doi.org/10.1056/NEJMcibr2108627] [PMID: 34437788]
[19]
Azar, J.; Bahmad, H.F.; Daher, D.; Moubarak, M.M.; Hadadeh, O.; Monzer, A.; Al Bitar, S.; Jamal, M.; Al-Sayegh, M.; Abou-Kheir, W. The use of stem cell-derived organoids in disease modeling: An update. Int. J. Mol. Sci., 2021, 22(14), 7667.
[http://dx.doi.org/10.3390/ijms22147667] [PMID: 34299287]
[20]
Giacomelli, E.; Meraviglia, V.; Campostrini, G.; Cochrane, A.; Cao, X.; van Helden, R.W.J.; Krotenberg Garcia, A.; Mircea, M.; Kostidis, S.; Davis, R.P.; van Meer, B.J.; Jost, C.R.; Koster, A.J.; Mei, H.; Míguez, D.G.; Mulder, A.A.; Ledesma-Terrón, M.; Pompilio, G.; Sala, L.; Salvatori, D.C.F.; Slieker, R.C.; Sommariva, E.; de Vries, A.A.F.; Giera, M.; Semrau, S.; Tertoolen, L.G.J.; Orlova, V.V.; Bellin, M.; Mummery, C.L. Human-iPSC-derived cardiac stromal cells enhance maturation in 3D cardiac microtissues and reveal non-cardiomyocyte contributions to heart disease. Cell Stem Cell, 2020, 26(6), 862-879.e11.
[http://dx.doi.org/10.1016/j.stem.2020.05.004] [PMID: 32459996]
[21]
de Lange, W.J.; Farrell, E.T.; Kreitzer, C.R.; Jacobs, D.R.; Lang, D.; Glukhov, A.V.; Ralphe, J.C. Human iPSC-engineered cardiac tissue platform faithfully models important cardiac physiology. Am. J. Physiol. Heart Circ. Physiol., 2021, 320(4), H1670-H1686.
[http://dx.doi.org/10.1152/ajpheart.00941.2020] [PMID: 33606581]
[22]
Lee, J.; Sutani, A.; Kaneko, R.; Takeuchi, J.; Sasano, T.; Kohda, T.; Ihara, K.; Takahashi, K.; Yamazoe, M.; Morio, T.; Furukawa, T.; Ishino, F. In vitro generation of functional murine heart organoids via FGF4 and extracellular matrix. Nat. Commun., 2020, 11(1), 4283.
[http://dx.doi.org/10.1038/s41467-020-18031-5] [PMID: 32883967]
[23]
Testa, G.; Di Benedetto, G.; Passaro, F. Advanced technologies to target cardiac cell fate plasticity for heart regeneration. Int. J. Mol. Sci., 2021, 22(17), 9517.
[http://dx.doi.org/10.3390/ijms22179517] [PMID: 34502423]
[24]
Seguret, M.; Vermersch, E.; Jouve, C.; Hulot, J.S. Cardiac organoids to model and heal heart failure and cardiomyopathies. Biomedicines, 2021, 9(5), 563.
[http://dx.doi.org/10.3390/biomedicines9050563] [PMID: 34069816]
[25]
Banerjee, I.; Fuseler, J.W.; Price, R.L.; Borg, T.K.; Baudino, T.A. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am. J. Physiol. Heart Circ. Physiol., 2007, 293(3), H1883-H1891.
[http://dx.doi.org/10.1152/ajpheart.00514.2007] [PMID: 17604329]
[26]
Bergmann, O.; Zdunek, S.; Felker, A.; Salehpour, M.; Alkass, K.; Bernard, S.; Sjostrom, S.L.; Szewczykowska, M.; Jackowska, T.; dos Remedios, C.; Malm, T.; Andrä, M.; Jashari, R.; Nyengaard, J.R.; Possnert, G.; Jovinge, S.; Druid, H.; Frisén, J. Dynamics of cell generation and turnover in the human heart. Cell, 2015, 161(7), 1566-1575.
[http://dx.doi.org/10.1016/j.cell.2015.05.026] [PMID: 26073943]
[27]
Zhou, P.; Pu, W.T. Recounting cardiac cellular composition. Circ. Res., 2016, 118(3), 368-370.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.308139] [PMID: 26846633]
[28]
Tirziu, D.; Giordano, F.J.; Simons, M. Cell communications in the heart. Circulation, 2010, 122(9), 928-937.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.847731] [PMID: 20805439]
[29]
Stevens, K.R.; Kreutziger, K.L.; Dupras, S.K.; Korte, F.S.; Regnier, M.; Muskheli, V.; Nourse, M.B.; Bendixen, K.; Reinecke, H.; Murry, C.E. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. USA, 2009, 106(39), 16568-16573.
[http://dx.doi.org/10.1073/pnas.0908381106] [PMID: 19805339]
[30]
Artegiani, B.; Hendriks, D.; Beumer, J.; Kok, R.; Zheng, X.; Joore, I.; Chuva de Sousa Lopes, S.; van Zon, J.; Tans, S.; Clevers, H. Fast and efficient generation of knock-in human organoids using homology-independent CRISPR- Cas9 precision genome editing. Nat. Cell Biol., 2020, 22(3), 321-331.
[http://dx.doi.org/10.1038/s41556-020-0472-5] [PMID: 32123335]
[31]
Shkumatov, A.; Baek, K.; Kong, H. Matrix rigidity-modulated cardiovascular organoid formation from embryoid bodies. PLoS One, 2014, 9(4), e94764.
[http://dx.doi.org/10.1371/journal.pone.0094764] [PMID: 24732893]
[32]
Hofbauer, P.; Jahnel, S.M.; Papai, N.; Giesshammer, M.; Deyett, A.; Schmidt, C.; Penc, M.; Tavernini, K.; Grdseloff, N.; Meledeth, C.; Ginistrelli, L.C.; Ctortecka, C.; Šalic, Š.; Novatchkova, M.; Mendjan, S. Cardioids reveal self-organizing principles of human cardiogenesis. Cell, 2021, 184(12), 3299-3317.e22.
[http://dx.doi.org/10.1016/j.cell.2021.04.034] [PMID: 34019794]
[33]
Gao, L.; Kupfer, M.E.; Jung, J.P.; Yang, L.; Zhang, P.; Da Sie, Y.; Tran, Q.; Ajeti, V.; Freeman, B.T.; Fast, V.G.; Campagnola, P.J.; Ogle, B.M.; 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(8), 1318-1325.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.310277] [PMID: 28069694]
[34]
Lind, J.U.; Busbee, T.A.; Valentine, A.D.; Pasqualini, F.S.; Yuan, H.; Yadid, M.; Park, S.J.; Kotikian, A.; Nesmith, A.P.; Campbell, P.H.; Vlassak, J.J.; Lewis, J.A.; Parker, K.K. Instrumented cardiac microphysiological devices via multimaterial three-dimensional printing. Nat. Mater., 2017, 16(3), 303-308.
[http://dx.doi.org/10.1038/nmat4782] [PMID: 27775708]
[35]
Ma, Z.; Wang, J.; Loskill, P.; Huebsch, N.; Koo, S.; Svedlund, F.L.; Marks, N.C.; Hua, E.W.; Grigoropoulos, C.P.; Conklin, B.R.; Healy, K.E. Self-organizing human cardiac microchambers mediated by geometric confinement. Nat. Commun., 2015, 6(1), 7413.
[http://dx.doi.org/10.1038/ncomms8413] [PMID: 26172574]
[36]
Hoang, P.; Wang, J.; Conklin, B.R.; Healy, K.E.; Ma, Z. Generation of spatial-patterned early-developing cardiac organoids using human pluripotent stem cells. Nat. Protoc., 2018, 13(4), 723-737.
[http://dx.doi.org/10.1038/nprot.2018.006] [PMID: 29543795]
[37]
Li, J.; Minami, I.; Shiozaki, M.; Yu, L.; Yajima, S.; Miyagawa, S.; Shiba, Y.; Morone, N.; Fukushima, S.; Yoshioka, M.; Li, S.; Qiao, J.; Li, X.; Wang, L.; Kotera, H.; Nakatsuji, N.; Sawa, Y.; Chen, Y.; Liu, L. Human pluripotent stem cell-derived cardiac tissue-like constructs for repairing the infarcted myocardium. Stem Cell Reports, 2017, 9(5), 1546-1559.
[http://dx.doi.org/10.1016/j.stemcr.2017.09.007] [PMID: 29107590]
[38]
Ong, C.S.; Fukunishi, T.; Zhang, H.; Huang, C.Y.; Nashed, A.; Blazeski, A.; DiSilvestre, D.; Vricella, L.; Conte, J.; Tung, L.; Tomaselli, G.F.; Hibino, N. Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci. Rep., 2017, 7(1), 4566.
[http://dx.doi.org/10.1038/s41598-017-05018-4] [PMID: 28676704]
[39]
Radisic, M.; Park, H.; Shing, H.; Consi, T.; Schoen, F.J.; Langer, R.; Freed, L.E.; Vunjak-Novakovic, G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. USA, 2004, 101(52), 18129-18134.
[http://dx.doi.org/10.1073/pnas.0407817101] [PMID: 15604141]
[40]
Thavandiran, N.; Dubois, N.; Mikryukov, A.; Massé, S.; Beca, B.; Simmons, C.A.; Deshpande, V.S.; McGarry, J.P.; Chen, C.S.; Nanthakumar, K.; Keller, G.M.; Radisic, M.; Zandstra, P.W. Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc. Natl. Acad. Sci. USA, 2013, 110(49), E4698-E4707.
[http://dx.doi.org/10.1073/pnas.1311120110] [PMID: 24255110]
[41]
Hirt, M.N.; Boeddinghaus, J.; Mitchell, A.; Schaaf, S.; Börnchen, C.; Müller, C.; Schulz, H.; Hubner, N.; Stenzig, J.; Stoehr, A.; Neuber, C.; Eder, A.; Luther, P.K.; Hansen, A.; Eschenhagen, T. Functional improvement and maturation of rat and human engineered heart tissue by chronic electrical stimulation. J. Mol. Cell. Cardiol., 2014, 74, 151-161.
[http://dx.doi.org/10.1016/j.yjmcc.2014.05.009] [PMID: 24852842]
[42]
Mihic, A.; Li, J.; Miyagi, Y.; Gagliardi, M.; Li, S.H.; Zu, J.; Weisel, R.D.; Keller, G.; Li, R.K. The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials, 2014, 35(9), 2798-2808.
[http://dx.doi.org/10.1016/j.biomaterials.2013.12.052] [PMID: 24424206]
[43]
Mills, R.J.; Titmarsh, D.M.; Koenig, X.; Parker, B.L.; Ryall, J.G.; Quaife-Ryan, G.A.; Voges, H.K.; Hodson, M.P.; Ferguson, C.; Drowley, L.; Plowright, A.T.; Needham, E.J.; Wang, Q.D.; Gregorevic, P.; Xin, M.; Thomas, W.G.; Parton, R.G.; Nielsen, L.K.; Launikonis, B.S.; James, D.E.; Elliott, D.A.; Porrello, E.R.; Hudson, J.E. Functional screening in human cardiac organoids reveals a metabolic mechanism for cardiomyocyte cell cycle arrest. Proc. Natl. Acad. Sci. USA, 2017, 114(40), E8372-E8381.
[http://dx.doi.org/10.1073/pnas.1707316114] [PMID: 28916735]
[44]
Voges, H.K.; Mills, R.J.; Elliott, D.A.; Parton, R.G.; Porrello, E.R.; Hudson, J.E. Development of a human cardiac organoid injury model reveals innate regenerative potential. Development, 2017, 144(6), 143966.
[http://dx.doi.org/10.1242/dev.143966] [PMID: 28174241]
[45]
Sun, X.; Nunes, S.S. Biowire platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Methods, 2016, 101, 21-26.
[http://dx.doi.org/10.1016/j.ymeth.2015.11.005] [PMID: 26546730]
[46]
Ronaldson-Bouchard, K.; Ma, S.P.; Yeager, K.; Chen, T.; Song, L.; Sirabella, D.; Morikawa, K.; Teles, D.; Yazawa, M.; Vunjak-Novakovic, G. Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature, 2018, 556(7700), 239-243.
[http://dx.doi.org/10.1038/s41586-018-0016-3] [PMID: 29618819]
[47]
Hofer, M.; Lutolf, M.P. Engineering organoids. Nat. Rev. Mater., 2021, 6(5), 402-420.
[http://dx.doi.org/10.1038/s41578-021-00279-y]
[48]
Marti-Figueroa, C.R.; Ashton, R.S. The case for applying tissue engineering methodologies to instruct human organoid morphogenesis. Acta Biomater., 2017, 54, 35-44.
[http://dx.doi.org/10.1016/j.actbio.2017.03.023] [PMID: 28315813]
[49]
Hendriks, D.; Clevers, H.; Artegiani, B. CRISPR-Cas tools and their application in genetic engineering of human stem cells and organoids. Cell Stem Cell, 2020, 27(5), 705-731.
[http://dx.doi.org/10.1016/j.stem.2020.10.014] [PMID: 33157047]
[50]
Driehuis, E.; Clevers, H. CRISPR/Cas 9 genome editing and its applications in organoids. Am. J. Physiol. Gastrointest. Liver Physiol., 2017, 312(3), G257-G265.
[http://dx.doi.org/10.1152/ajpgi.00410.2016] [PMID: 28126704]
[51]
Kitaguchi, T.; Moriyama, Y.; Taniguchi, T.; Ojima, A.; Ando, H.; Uda, T.; Otabe, K.; Oguchi, M.; Shimizu, S.; Saito, H.; Morita, M.; Toratani, A.; Asayama, M.; Yamamoto, W.; Matsumoto, E.; Saji, D.; Ohnaka, H.; Tanaka, K.; Washio, I.; Miyamoto, N. CSAHi study: Evaluation of multi-electrode array in combination with human iPS cell-derived cardiomyocytes to predict drug-induced QT prolongation and arrhythmia - Effects of 7 reference compounds at 10 facilities. J. Pharmacol. Toxicol. Methods, 2016, 78, 93-102.
[http://dx.doi.org/10.1016/j.vascn.2015.12.002] [PMID: 26657830]
[52]
Kawatou, M.; Masumoto, H.; Fukushima, H.; Morinaga, G.; Sakata, R.; Ashihara, T.; Yamashita, J.K. Modelling torsade de pointes arrhythmias in vitro in 3D human iPS cell-engineered heart tissue. Nat. Commun., 2017, 8(1), 1078.
[http://dx.doi.org/10.1038/s41467-017-01125-y] [PMID: 29057872]
[53]
Kim, D.S.; Choi, Y.W.; Shanmugasundaram, A.; Jeong, Y.J.; Park, J.; Oyunbaatar, N.E.; Kim, E.S.; Choi, M.; Lee, D.W. Highly durable crack sensor integrated with silicone rubber cantilever for measuring cardiac contractility. Nat. Commun., 2020, 11(1), 535.
[http://dx.doi.org/10.1038/s41467-019-14019-y] [PMID: 31988308]
[54]
Mills, R.; Hudson, J. An in vitro model of myocardial infarction. Nat. Biomed. Eng., 2020, 4(4), 366-367.
[http://dx.doi.org/10.1038/s41551-020-0550-9] [PMID: 32286510]
[55]
Virani, S.S.; Alonso, A.; Benjamin, E.J.; Bittencourt, M.S.; Callaway, C.W.; Carson, A.P.; Chamberlain, A.M.; Chang, A.R.; Cheng, S.; Delling, F.N.; Djousse, L.; Elkind, M.S.V.; Ferguson, J.F.; Fornage, M.; Khan, S.S.; Kissela, B.M.; Knutson, K.L.; Kwan, T.W.; Lackland, D.T.; Lewis, T.T.; Lichtman, J.H.; Longenecker, C.T.; Loop, M.S.; Lutsey, P.L.; Martin, S.S.; Matsushita, K.; Moran, A.E.; Mussolino, M.E.; Perak, A.M.; Rosamond, W.D.; Roth, G.A.; Sampson, U.K.A.; Satou, G.M.; Schroeder, E.B.; Shah, S.H.; Shay, C.M.; Spartano, N.L.; Stokes, A.; Tirschwell, D.L.; VanWagner, L.B.; Tsao, C.W. Heart Disease and Stroke Statistics-2020 Update: A Report From the American Heart Association. Circulation, 2020, 141(9), e139-e596.
[http://dx.doi.org/10.1161/CIR.0000000000000757] [PMID: 31992061]
[56]
Gheorghiade, M.; Larson, C.J.; Shah, S.J.; Greene, S.J.; Cleland, J.G.F.; Colucci, W.S.; Dunnmon, P.; Epstein, S.E.; Kim, R.J.; Parsey, R.V.; Stockbridge, N.; Carr, J.; Dinh, W.; Krahn, T.; Kramer, F.; Wahlander, K.; Deckelbaum, L.I.; Crandall, D.; Okada, S.; Senni, M.; Sikora, S.; Sabbah, H.N.; Butler, J. Developing new treatments for heart failure. Circ. Heart Fail., 2016, 9(5), e002727.
[http://dx.doi.org/10.1161/CIRCHEARTFAILURE.115.002727] [PMID: 27166246]
[57]
Fine, B.; Vunjak-Novakovic, G. Shortcomings of animal models and the rise of engineered human cardiac tissue. ACS Biomater. Sci. Eng., 2017, 3(9), 1884-1897.
[http://dx.doi.org/10.1021/acsbiomaterials.6b00662] [PMID: 33440547]
[58]
Kaye, D.M.; Krum, H. Drug discovery for heart failure: A new era or the end of the pipeline? Nat. Rev. Drug Discov., 2007, 6(2), 127-139.
[http://dx.doi.org/10.1038/nrd2219] [PMID: 17268484]
[59]
Richards, D.J.; Li, Y.; Kerr, C.M.; Yao, J.; Beeson, G.C.; Coyle, R.C.; Chen, X.; Jia, J.; Damon, B.; Wilson, R.; Starr Hazard, E.; Hardiman, G.; Menick, D.R.; Beeson, C.C.; Yao, H.; Ye, T.; Mei, Y. Human cardiac organoids for the modelling of myocardial infarction and drug cardiotoxicity. Nat. Biomed. Eng., 2020, 4(4), 446-462.
[http://dx.doi.org/10.1038/s41551-020-0539-4] [PMID: 32284552]
[60]
Ding, Y.; Wang, Y.; Zhang, W.; Jia, Q.; Wang, X.; Li, Y.; Lv, S.; Zhang, J. Roles of biomarkers in myocardial fibrosis. Aging Dis., 2020, 11(5), 1157-1174.
[http://dx.doi.org/10.14336/AD.2020.0604] [PMID: 33014530]
[61]
Stratton, M.S.; Bagchi, R.A.; Felisbino, M.B.; Hirsch, R.A.; Smith, H.E.; Riching, A.S.; Enyart, B.Y.; Koch, K.A.; Cavasin, M.A.; Alexanian, M.; Song, K.; Qi, J.; Lemieux, M.E.; Srivastava, D.; Lam, M.P.Y.; Haldar, S.M.; Lin, C.Y.; McKinsey, T.A. Dynamic chromatin targeting of BRD4 stimulates cardiac fibroblast activation. Circ. Res., 2019, 125(7), 662-677.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.315125] [PMID: 31409188]
[62]
Shinnawi, R.; Shaheen, N.; Huber, I.; Shiti, A.; Arbel, G.; Gepstein, A.; Ballan, N.; Setter, N.; Tijsen, A.J.; Borggrefe, M.; Gepstein, L. Modeling reentry in the short QT syndrome with human-induced pluripotent stem cell-derived cardiac cell sheets. J. Am. Coll. Cardiol., 2019, 73(18), 2310-2324.
[http://dx.doi.org/10.1016/j.jacc.2019.02.055] [PMID: 31072576]
[63]
Hulot, J.S. Modeling cardiac arrhythmias with organoids. J. Am. Coll. Cardiol., 2019, 73(18), 2325-2327.
[http://dx.doi.org/10.1016/j.jacc.2019.01.076] [PMID: 31072577]
[64]
Filippo Buono, M.; von Boehmer, L.; Strang, J.; Hoerstrup, S.P.; Emmert, M.Y.; Nugraha, B. Human cardiac organoids for modeling genetic cardiomyopathy. Cells, 2020, 9(7), E1733.
[http://dx.doi.org/10.3390/cells9071733] [PMID: 32698471]
[65]
Nugraha, B.; Buono, M.F.; Boehmer, L.; Hoerstrup, S.P.; Emmert, M.Y. Human cardiac organoids for disease modeling. Clin. Pharmacol. Ther., 2019, 105(1), 79-85.
[http://dx.doi.org/10.1002/cpt.1286] [PMID: 30415499]
[66]
Cashman, T.J.; Josowitz, R.; Johnson, B.V.; Gelb, B.D.; Costa, K.D. Human engineered cardiac tissues created using induced pluripotent stem cells reveal functional characteristics of BRAF-mediated hypertrophic cardiomyopathy. PLoS One, 2016, 11(1), e0146697.
[http://dx.doi.org/10.1371/journal.pone.0146697] [PMID: 26784941]
[67]
Wang, G.; McCain, M.L.; Yang, L.; He, A.; Pasqualini, F.S.; Agarwal, A.; Yuan, H.; Jiang, D.; Zhang, D.; Zangi, L.; Geva, J.; Roberts, A.E.; Ma, Q.; Ding, J.; Chen, J.; Wang, D.Z.; Li, K.; Wang, J.; Wanders, R.J.A.; Kulik, W.; Vaz, F.M.; Laflamme, M.A.; Murry, C.E.; Chien, K.R.; Kelley, R.I.; Church, G.M.; Parker, K.K.; Pu, W.T. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat. Med., 2014, 20(6), 616-623.
[http://dx.doi.org/10.1038/nm.3545] [PMID: 24813252]
[68]
Lan, F.; Lee, A.S.; Liang, P.; Sanchez-Freire, V.; Nguyen, P.K.; Wang, L.; Han, L.; Yen, M.; Wang, Y.; Sun, N.; Abilez, O.J.; Hu, S.; Ebert, A.D.; Navarrete, E.G.; Simmons, C.S.; Wheeler, M.; Pruitt, B.; Lewis, R.; Yamaguchi, Y.; Ashley, E.A.; Bers, D.M.; Robbins, R.C.; Longaker, M.T.; Wu, J.C. Abnormal calcium handling properties underlie familial hypertrophic cardiomyopathy pathology in patient-specific induced pluripotent stem cells. Cell Stem Cell, 2013, 12(1), 101-113.
[http://dx.doi.org/10.1016/j.stem.2012.10.010] [PMID: 23290139]
[69]
Hinson, J.T.; Chopra, A.; Nafissi, N.; Polacheck, W.J.; Benson, C.C.; Swist, S.; Gorham, J.; Yang, L.; Schafer, S.; Sheng, C.C.; Haghighi, A.; Homsy, J.; Hubner, N.; Church, G.; Cook, S.A.; Linke, W.A.; Chen, C.S.; Seidman, J.G.; Seidman, C.E. Titin mutations in iPS cells define sarcomere insufficiency as a cause of dilated cardiomyopathy. Science, 2015, 349(6251), 982-986.
[http://dx.doi.org/10.1126/science.aaa5458] [PMID: 26315439]
[70]
Kofron, C.M.; Kim, T.Y.; Munarin, F.; Soepriatna, A.H.; Kant, R.J.; Mende, U.; Choi, B.R.; Coulombe, K.L.K. A predictive in vitro risk assessment platform for pro-arrhythmic toxicity using human 3D cardiac microtissues. Sci. Rep., 2021, 11(1), 10228.
[http://dx.doi.org/10.1038/s41598-021-89478-9] [PMID: 33986332]
[71]
Zheng, P.P.; Li, J.; Kros, J.M. Breakthroughs in modern cancer therapy and elusive cardiotoxicity: Critical research-practice gaps, challenges, and insights. Med. Res. Rev., 2018, 38(1), 325-376.
[http://dx.doi.org/10.1002/med.21463] [PMID: 28862319]
[72]
Cappetta, D.; Rossi, F.; Piegari, E.; Quaini, F.; Berrino, L.; Urbanek, K.; De Angelis, A. Doxorubicin targets multiple players: A new view of an old problem. Pharmacol. Res., 2018, 127, 4-14.
[http://dx.doi.org/10.1016/j.phrs.2017.03.016] [PMID: 28336372]
[73]
Tai, W.; He, L.; Zhang, X.; Pu, J.; Voronin, D.; Jiang, S.; Zhou, Y.; Du, L. Characterization of the receptor-binding domain (RBD) of 2019 novel coronavirus: Implication for development of RBD protein as a viral attachment inhibitor and vaccine. Cell. Mol. Immunol., 2020, 17(6), 613-620.
[http://dx.doi.org/10.1038/s41423-020-0400-4] [PMID: 32203189]
[74]
Grimm, F.; Blanchette, A.; House, J.S.; Ferguson, K.; Hsieh, N.H.; Dalaijamts, C.; Wright, A.A.; Anson, B.; Wright, F.A.; Chiu, W.A.; Rusyn, I. A human population-based organotypic in vitro model for cardiotoxicity screening. Altern. Anim. Exp., 2018, 35(4), 441-452.
[http://dx.doi.org/10.14573/altex.1805301] [PMID: 29999168]
[75]
Gintant, G.; Burridge, P.; Gepstein, L.; Harding, S.; Herron, T.; Hong, C.; Jalife, J.; Wu, J.C. Use of human induced pluripotent stem cell-derived cardiomyocytes in preclinical cancer drug cardiotoxicity testing: A scientific statement from the American Heart Association. Circ. Res., 2019, 125(10), e75-e92.
[http://dx.doi.org/10.1161/RES.0000000000000291] [PMID: 31533542]
[76]
van den Berg, C.W.; Okawa, S.; Chuva de Sousa Lopes, S.M.; van Iperen, L.; Passier, R.; Braam, S.R.; Tertoolen, L.G.; del Sol, A.; Davis, R.P.; Mummery, C.L. Transcriptome of human foetal heart compared with cardiomyocytes from pluripotent stem cells. Development, 2015, 142(18), dev.123810.
[http://dx.doi.org/10.1242/dev.123810] [PMID: 26209647]
[77]
Rao, C.; Prodromakis, T.; Kolker, L.; Chaudhry, U.A.R.; Trantidou, T.; Sridhar, A.; Weekes, C.; Camelliti, P.; Harding, S.E.; Darzi, A.; Yacoub, M.H.; Athanasiou, T.; Terracciano, C.M. The effect of microgrooved culture substrates on calcium cycling of cardiac myocytes derived from human induced pluripotent stem cells. Biomaterials, 2013, 34(10), 2399-2411.
[http://dx.doi.org/10.1016/j.biomaterials.2012.11.055] [PMID: 23261219]
[78]
Herron, T.J.; Rocha, A.M.D.; Campbell, K.F.; Ponce-Balbuena, D.; Willis, B.C.; Guerrero-Serna, G.; Liu, Q.; Klos, M.; Musa, H.; Zarzoso, M.; Bizy, A.; Furness, J.; Anumonwo, J.; Mironov, S.; Jalife, J. Extracellular matrix-mediated maturation of human pluripotent stem cell-derived cardiac monolayer structure and electrophysiological function. Circ. Arrhythm. Electrophysiol., 2016, 9(4), e003638.
[http://dx.doi.org/10.1161/CIRCEP.113.003638] [PMID: 27069088]
[79]
Feaster, T.K.; Cadar, A.G.; Wang, L.; Williams, C.H.; Chun, Y.W.; Hempel, J.E.; Bloodworth, N.; Merryman, W.D.; Lim, C.C.; Wu, J.C.; Knollmann, B.C.; Hong, C.C. Matrigel Mattress. Circ. Res., 2015, 117(12), 995-1000.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.307580] [PMID: 26429802]
[80]
Nishiguchi, A.; Matsusaki, M.; Miyagawa, S.; Sawa, Y.; Akashi, M. Dynamic nano-interfaces enable harvesting of functional 3D-engineered tissues. Adv. Healthc. Mater., 2015, 4(8), 1164-1168.
[http://dx.doi.org/10.1002/adhm.201500065] [PMID: 25728509]
[81]
Takeda, M.; Miyagawa, S.; Fukushima, S.; Saito, A.; Ito, E.; Harada, A.; Matsuura, R.; Iseoka, H.; Sougawa, N.; Mochizuki-Oda, N.; Matsusaki, M.; Akashi, M.; Sawa, Y. Development of in vitro drug-induced cardiotoxicity assay by using three-dimensional cardiac tissues derived from human induced pluripotent stem cells. Tissue Eng. Part C Methods, 2018, 24(1), 56-67.
[http://dx.doi.org/10.1089/ten.tec.2017.0247] [PMID: 28967302]
[82]
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.; Field, L.J.; Keller, G.M. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature, 2008, 453(7194), 524-528.
[http://dx.doi.org/10.1038/nature06894] [PMID: 18432194]
[83]
Schulz, T.C.; Swistowska, A.M.; Liu, Y.; Swistowski, A.; Palmarini, G.; Brimble, S.N.; Sherrer, E.; Robins, A.J.; Rao, M.S.; Zeng, X. A large-scale proteomic analysis of human embryonic stem cells. BMC Genomics, 2007, 8(1), 478.
[http://dx.doi.org/10.1186/1471-2164-8-478] [PMID: 18162134]
[84]
Thomas, R.J.; Anderson, D.; Chandra, A.; Smith, N.M.; Young, L.E.; Williams, D.; Denning, C. Automated, scalable culture of human embryonic stem cells in feeder-free conditions. Biotechnol. Bioeng., 2009, 102(6), 1636-1644.
[http://dx.doi.org/10.1002/bit.22187] [PMID: 19062183]
[85]
Anderson, D.; Self, T.; Mellor, I.R.; Goh, G.; Hill, S.J.; Denning, C. Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol. Ther., 2007, 15(11), 2027-2036.
[http://dx.doi.org/10.1038/sj.mt.6300303] [PMID: 17895862]
[86]
Huber, I.; Itzhaki, I.; Caspi, O.; Arbel, G.; Tzukerman, M.; Gepstein, A.; Habib, M.; Yankelson, L.; Kehat, I.; Gepstein, L. Identification and selection of cardiomyocytes during human embryonic stem cell differentiation. FASEB J., 2007, 21(10), 2551-2563.
[http://dx.doi.org/10.1096/fj.05-5711com] [PMID: 17435178]
[87]
Mordwinkin, N.M.; Burridge, P.W.; Wu, J.C. A review of human pluripotent stem cell-derived cardiomyocytes for high-throughput drug discovery, cardiotoxicity screening, and publication standards. J. Cardiovasc. Transl. Res., 2013, 6(1), 22-30.
[http://dx.doi.org/10.1007/s12265-012-9423-2] [PMID: 23229562]
[88]
Rossi, G.; Manfrin, A.; Lutolf, M.P. Progress and potential in organoid research. Nat. Rev. Genet., 2018, 19(11), 671-687.
[http://dx.doi.org/10.1038/s41576-018-0051-9] [PMID: 30228295]
[89]
Liu, C.; Oikonomopoulos, A.; Sayed, N.; Wu, J.C. Modeling human diseases with induced pluripotent stem cells: From 2D to 3D and beyond. Development, 2018, 145(5), dev156166.
[http://dx.doi.org/10.1242/dev.156166] [PMID: 29519889]
[90]
Pham, M.T.; Pollock, K.M.; Rose, M.D.; Cary, W.A.; Stewart, H.R.; Zhou, P.; Nolta, J.A.; Waldau, B. Generation of human vascularized brain organoids. Neuroreport, 2018, 29(7), 588-593.
[http://dx.doi.org/10.1097/WNR.0000000000001014] [PMID: 29570159]
[91]
Kitsuka, T.; Itoh, M.; Amamoto, S.; Arai, K.; Oyama, J.; Node, K.; Toda, S.; Morita, S.; Nishida, T.; Nakayama, K. 2-Cl-C.OXT-A stimulates contraction through the suppression of phosphodiesterase activity in human induced pluripotent stem cell-derived cardiac organoids. PLoS One, 2019, 14(7), e0213114.
[http://dx.doi.org/10.1371/journal.pone.0213114] [PMID: 31295264]
[92]
Xiang, Y.; Tanaka, Y.; Patterson, B.; Kang, Y.J.; Govindaiah, G.; Roselaar, N.; Cakir, B.; Kim, K.Y.; Lombroso, A.P.; Hwang, S.M.; Zhong, M.; Stanley, E.G.; Elefanty, A.G.; Naegele, J.R.; Lee, S.H.; Weissman, S.M.; Park, I.H. Fusion of regionally specified hPSC-derived organoids models human brain development and interneuron migration. Cell Stem Cell, 2017, 21(3), 383-398.e7.
[http://dx.doi.org/10.1016/j.stem.2017.07.007] [PMID: 28757360]
[93]
Low, L.A.; Mummery, C.; Berridge, B.R.; Austin, C.P.; Tagle, D.A. Organs-on-chips: Into the next decade. Nat. Rev. Drug Discov., 2021, 20(5), 345-361.
[http://dx.doi.org/10.1038/s41573-020-0079-3] [PMID: 32913334]
[94]
Michl, J.; Park, K.C.; Swietach, P. Evidence-based guidelines for controlling pH in mammalian live-cell culture systems. Commun. Biol., 2019, 2(1), 144.
[http://dx.doi.org/10.1038/s42003-019-0393-7] [PMID: 31044169]
[95]
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.; O’Sullivan, C.; Collins, L.; Chen, Y.; Minami, E.; Gill, E.A.; Ueno, S.; Yuan, C.; Gold, J.; Murry, C.E. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol., 2007, 25(9), 1015-1024.
[http://dx.doi.org/10.1038/nbt1327] [PMID: 17721512]
[96]
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(7625), 388-391.
[http://dx.doi.org/10.1038/nature19815] [PMID: 27723741]
[97]
Rojas, S.V.; Kensah, G.; Rotaermel, A.; Baraki, H.; Kutschka, I.; Zweigerdt, R.; Martin, U.; Haverich, A.; Gruh, I.; Martens, A. Transplantation of purified iPSC-derived cardiomyocytes in myocardial infarction. PLoS One, 2017, 12(5), e0173222.
[http://dx.doi.org/10.1371/journal.pone.0173222] [PMID: 28493867]
[98]
Duelen, R.; Sampaolesi, M. Stem cell technology in cardiac regeneration: A pluripotent stem cell promise. EBioMedicine, 2017, 16, 30-40.
[http://dx.doi.org/10.1016/j.ebiom.2017.01.029] [PMID: 28169191]
[99]
Jackman, C.P.; Shadrin, I.Y.; Carlson, A.L.; Bursac, N. Human cardiac tissue engineering: From pluripotent stem cells to heart repair. Curr. Opin. Chem. Eng., 2015, 7, 57-64.
[http://dx.doi.org/10.1016/j.coche.2014.11.004] [PMID: 25599018]
[100]
Masumoto, H.; Ikuno, T.; Takeda, M.; Fukushima, H.; Marui, A.; Katayama, S.; Shimizu, T.; Ikeda, T.; Okano, T.; Sakata, R.; Yamashita, J.K. Human iPS cell-engineered cardiac tissue sheets with cardiomyocytes and vascular cells for cardiac regeneration. Sci. Rep., 2015, 4(1), 6716.
[http://dx.doi.org/10.1038/srep06716] [PMID: 25336194]
[101]
Zimmermann, W.H.; Didié, M.; Wasmeier, G.H.; Nixdorff, U.; Hess, A.; Melnychenko, I.; Boy, O.; Neuhuber, W.L.; Weyand, M.; Eschenhagen, T. Cardiac grafting of engineered heart tissue in syngenic rats. Circulation, 2002, 106(12 Suppl 1), I151-I157.
[http://dx.doi.org/10.1161/01.cir.0000032876.55215.10] [PMID: 12354725]
[102]
Zhao, S.; Agarwal, P.; Rao, W.; Huang, H.; Zhang, R.; Liu, Z.; Yu, J.; Weisleder, N.; Zhang, W.; He, X. Coaxial electrospray of liquid core-hydrogel shell microcapsules for encapsulation and miniaturized 3D culture of pluripotent stem cells. Integr. Biol., 2014, 6(9), 874-884.
[http://dx.doi.org/10.1039/c4ib00100a] [PMID: 25036382]
[103]
Zimmermann, W.H.; Melnychenko, I.; Wasmeier, G.; Didié, M.; Naito, H.; Nixdorff, U.; Hess, A.; Budinsky, L.; Brune, K.; Michaelis, B.; Dhein, S.; Schwoerer, A.; Ehmke, H.; Eschenhagen, T. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat. Med., 2006, 12(4), 452-458.
[http://dx.doi.org/10.1038/nm1394] [PMID: 16582915]
[104]
Riegler, J.; Tiburcy, M.; Ebert, A.; Tzatzalos, E.; Raaz, U.; Abilez, O.J.; Shen, Q.; Kooreman, N.G.; Neofytou, E.; Chen, V.C.; Wang, M.; Meyer, T.; Tsao, P.S.; Connolly, A.J.; Couture, L.A.; Gold, J.D.; Zimmermann, W.H.; Wu, J.C. Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ. Res., 2015, 117(8), 720-730.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306985] [PMID: 26291556]
[105]
Tiburcy, M.; Hudson, J.E.; Balfanz, P.; Schlick, S.; Meyer, T.; Chang Liao, M.L.; Levent, E.; Raad, F.; Zeidler, S.; Wingender, E.; Riegler, J.; Wang, M.; Gold, J.D.; Kehat, I.; Wettwer, E.; Ravens, U.; Dierickx, P.; van Laake, L.W.; Goumans, M.J.; Khadjeh, S.; Toischer, K.; Hasenfuss, G.; Couture, L.A.; Unger, A.; Linke, W.A.; Araki, T.; Neel, B.; Keller, G.; Gepstein, L.; Wu, J.C.; Zimmermann, W.H. Defined engineered human myocardium with advanced maturation for applications in heart failure modeling and repair. Circulation, 2017, 135(19), 1832-1847.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.024145] [PMID: 28167635]
[106]
Kola, I.; Landis, J. Can the pharmaceutical industry reduce attrition rates? Nat. Rev. Drug Discov., 2004, 3(8), 711-716.
[http://dx.doi.org/10.1038/nrd1470] [PMID: 15286737]
[107]
Pound, P.; Ebrahim, S.; Sandercock, P.; Bracken, M.B.; Roberts, I. Where is the evidence that animal research benefits humans? BMJ, 2004, 328(7438), 514-517.
[http://dx.doi.org/10.1136/bmj.328.7438.514] [PMID: 14988196]
[108]
Mathur, A.; Loskill, P.; Shao, K.; Huebsch, N.; Hong, S.; Marcus, S.G.; Marks, N.; Mandegar, M.; Conklin, B.R.; Lee, L.P.; Healy, K.E. Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep., 2015, 5(1), 8883.
[http://dx.doi.org/10.1038/srep08883] [PMID: 25748532]
[109]
Lee, E.K.; Tran, D.D.; Keung, W.; Chan, P.; Wong, G.; Chan, C.W.; Costa, K.D.; Li, R.A.; Khine, M. Machine learning of human pluripotent stem cell-derived engineered cardiac tissue contractility for automated drug classification. Stem Cell Reports, 2017, 9(5), 1560-1572.
[http://dx.doi.org/10.1016/j.stemcr.2017.09.008] [PMID: 29033305]
[110]
Agarwal, A.; Goss, J.A.; Cho, A.; McCain, M.L.; Parker, K.K. Microfluidic heart on a chip for higher throughput pharmacological studies. Lab Chip, 2013, 13(18), 3599-3608.
[http://dx.doi.org/10.1039/c3lc50350j] [PMID: 23807141]
[111]
Huebsch, N.; Loskill, P.; Deveshwar, N.; Spencer, C.I.; Judge, L.M.; Mandegar, M.A.; Fox, C.B.; Mohamed, T.M.; Ma, Z.; Mathur, A.; Sheehan, A.M.; Truong, A.; Saxton, M.; Yoo, J.; Srivastava, D.; Desai, T.A.; So, P.L.; Healy, K.E.; Conklin, B.R. Miniaturized iPS-cell-derived cardiac muscles for physiologically relevant drug response analyses. Sci. Rep., 2016, 6, 24726.
[http://dx.doi.org/10.1038/srep24726] [PMID: 27095412]
[112]
Itzhaki, I.; Maizels, L.; Huber, I.; Zwi-Dantsis, L.; Caspi, O.; Winterstern, A.; Feldman, O.; Gepstein, A.; Arbel, G.; Hammerman, H.; Boulos, M.; Gepstein, L. Modelling the long QT syndrome with induced pluripotent stem cells. Nature, 2011, 471(7337), 225-229.
[http://dx.doi.org/10.1038/nature09747] [PMID: 21240260]
[113]
Campostrini, G.; Meraviglia, V.; Giacomelli, E.; van Helden, R.W.J.; Yiangou, L.; Davis, R.P.; Bellin, M.; Orlova, V.V.; Mummery, C.L. Generation, functional analysis and applications of isogenic three-dimensional self-aggregating cardiac microtissues from human pluripotent stem cells. Nat. Protoc., 2021, 16(4), 2213-2256.
[http://dx.doi.org/10.1038/s41596-021-00497-2] [PMID: 33772245]
[114]
Yu, F.; Hunziker, W.; Choudhury, D. Engineering microfluidic organoid-on-a-chip platforms. Micromachines, 2019, 10(3), 165.
[http://dx.doi.org/10.3390/mi10030165] [PMID: 30818801]
[115]
Abulaiti, M.; Yalikun, Y.; Murata, K.; Sato, A.; Sami, M.M.; Sasaki, Y.; Fujiwara, Y.; Minatoya, K.; Shiba, Y.; Tanaka, Y.; Masumoto, H. Establishment of a heart-on-a-chip microdevice based on human iPS cells for the evaluation of human heart tissue function. Sci. Rep., 2020, 10(1), 19201.
[http://dx.doi.org/10.1038/s41598-020-76062-w] [PMID: 33154509]
[116]
Kupfer, M.E.; Lin, W.H.; Ravikumar, V.; Qiu, K.; Wang, L.; Gao, L.; Bhuiyan, D.B.; Lenz, M.; Ai, J.; Mahutga, R.R.; Townsend, D.; Zhang, J.; McAlpine, M.C.; Tolkacheva, E.G.; Ogle, B.M. In situ expansion, differentiation, and electromechanical coupling of human cardiac muscle in a 3D bioprinted, chambered organoid. Circ. Res., 2020, 127(2), 207-224.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.316155] [PMID: 32228120]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy