한국동물생명공학회지 (Journal of Animal Reproduction and Biotechnology)

  • 제37권2호
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  • Pages.67-79
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  • 2022
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  • 2671-4639(pISSN)
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  • 2671-4663(eISSN)
한국동물생명공학회 (The Korean Society of Animal Reproduction and Biotechnology)
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In vitro maturation of human pluripotent stem cell-derived cardiomyocyte: A promising approach for cell therapy

  • 투고 : 2022.06.06
  • 심사 : 2022.06.20
  • 발행 : 2022.06.30
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초록

Currently, there is no treatment to reverse or cure heart failure caused by ischemic heart disease and myocardial infarction despite the remarkable advances in modern medicine. In addition, there is a lack of evidence regarding the existence of stem cells involved in the proliferation and regeneration of cardiomyocytes in adult hearts. As an alternative solution to overcome this problem, protocols for differentiating human pluripotent stem cell (hPSC) into cardiomyocyte have been established, which further led to the development of cell therapy in major leading countries in this field. Recently, clinical studies have confirmed the safety of hPSC-derived cardiac progenitor cells (CPCs). Although several institutions have shown progress in their research on cell therapy using hPSC-derived cardiomyocytes, the functions of cardiomyocytes used for transplantation remain to be those of immature cardiomyocytes, which poses a risk of graft-induced arrhythmias in the early stage of transplantation. Over the last decade, research aimed at achieving maturation of immature cardiomyocytes, showing same characteristics as those of mature cardiomyocytes, has been actively conducted using various approaches at leading research institutes worldwide. However, challenges remain in technological development for effective generation of mature cardiomyocytes with the same properties as those present in the adult hearts. Therefore, in this review, we provide an overview of the technological development status for maturation methods of hPSC-derived cardiomyocytes and present a direction for future development of maturation techniques.

키워드

과제정보

We thanks to Prof. Seong-Woo Choi of Dongguk University College of Medicine, Na-Kyeong Park of Seoul National University College of Medicine, Dr. Seok-Yun Jung and Mi-Jeong Kim of Stem Cell Research Institute, T&R Biofab Co. Ltd, Republic of Korea for their insightful comments on this manuscript.

참고문헌

  1. Abbasi J. 2022. The COVID heart-one year after SARS-CoV-2 infection, patients have an array of increased cardiovascular risks. JAMA 327:1113-1114. https://doi.org/10.1001/jama.2022.2411
  2. Bedada FB, Chan SS, Metzger SK, Zhang L, Zhang J, Garry DJ, Kamp TJ, Kyba M, Metzger JM. 2014. Acquisition of a quantitative, stoichiometrically conserved ratiometric marker of maturation status in stem cell-derived cardiac myocytes. Stem Cell Reports 3:594-605. https://doi.org/10.1016/j.stemcr.2014.07.012
  3. Birket MJ, Ribeiro MC, Kosmidis G, Ward D, Leitoguinho AR, van de Pol V, Dambrot C, Devalla HD, Davis RP, Mastroberardino PG, Atsma DE, Passier R, Mummery CL. 2015. Contractile defect caused by mutation in MYBPC3 revealed under conditions optimized for human PSC-cardiomyocyte function. Cell Rep. 13:733-745. https://doi.org/10.1016/j.celrep.2015.09.025
  4. Bulatovic I, Mansson-Broberg A, Sylven C, Grinnemo KH. 2016. Human fetal cardiac progenitors: the role of stem cells and progenitors in the fetal and adult heart. Best Pract. Res. Clin. Obstet. Gynaecol. 31:58-68. https://doi.org/10.1016/j.bpobgyn.2015.08.008
  5. Burridge PW, Holmstrom A, Wu JC. 2015. Chemically defined culture and cardiomyocyte differentiation of human pluripotent stem cells. Curr. Protoc. Hum. Genet. 87:21.3.1-21.3.15.
  6. Choi SW, Shin JS, Park SJ, Jung E, Park YG, Lee J, Kim SJ, Park HJ, Lee JH, Park SM, Moon SH, Ban K, Go YY. 2020. Antiviral activity and safety of remdesivir against SARS-CoV-2 infection in human pluripotent stem cell-derived cardiomyocytes. Antiviral Res. 184:104955. https://doi.org/10.1016/j.antiviral.2020.104955
  7. Correia C, Koshkin A, Duarte P, Hu D, Carido M, Sebastiao MJ, Gomes-Alves P, Elliott DA, Domian IJ, Teixeira AP, Alves PM, Serra M. 2018. 3D aggregate culture improves metabolic maturation of human pluripotent stem cell derived cardiomyocytes. Biotechnol. Bioeng. 115:630-644. https://doi.org/10.1002/bit.26504
  8. Correia C, Koshkin A, Duarte P, Hu D, Teixeira A, Domian I, Serra M, Alves PM. 2017. Distinct carbon sources affect structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Sci. Rep. 7:8590. https://doi.org/10.1038/s41598-017-08713-4
  9. Cyganek L, Tiburcy M, Sekeres K, Gerstenberg K, Bohnenberger H, Lenz C, Henze S, Stauske M, Salinas G, Zimmermann WH, Hasenfuss G, Guan K. 2018. Deep phenotyping of human induced pluripotent stem cell-derived atrial and ventricular cardiomyocytes. JCI Insight 3:e99941. https://doi.org/10.1172/jci.insight.99941
  10. de Lange WJ, Farrell ET, Kreitzer CR, Jacobs DR, Lang D, Glukhov AV, Ralphe JC. 2021. Human iPSC-engineered cardiac tissue platform faithfully models important cardiac physiology. Am. J. Physiol. Heart Circ. Physiol. 320:H1670-H1686. https://doi.org/10.1152/ajpheart.00941.2020
  11. Denning C, Borgdorff V, Crutchley J, Firth KS, George V, Kalra S, Kondrashov A, Hoang MD, Mosqueira D, Patel A, Prodanov L, Rajamohan D, Skarnes WC, Smith JG, Young LE. 2016. Cardiomyocytes from human pluripotent stem cells: from laboratory curiosity to industrial biomedical platform. Biochim. Biophys. Acta 1863(7 Pt B):1728-1748. https://doi.org/10.1016/j.bbamcr.2015.10.014
  12. Dunn KK, Reichardt IM, Simmons AD, Jin G, Floy ME, Hoon KM, Palecek SP. 2019. Coculture of endothelial cells with human pluripotent stem cell-derived cardiac progenitors reveals a differentiation stage-specific enhancement of cardiomyocyte maturation. Biotechnol. J. 14:e1800725.
  13. Eisner DA, Caldwell JL, Kistamas K, Trafford AW. 2017. Calcium and excitation-contraction coupling in the heart. Circ. Res. 121:181-195. https://doi.org/10.1161/CIRCRESAHA.117.310230
  14. Feric NT and Radisic M. 2016. Maturing human pluripotent stem cell-derived cardiomyocytes in human engineered cardiac tissues. Adv. Drug Deliv. Rev. 96:110-134. https://doi.org/10.1016/j.addr.2015.04.019
  15. Fukushima H, Yoshioka M, Kawatou M, Lopez-Davila V, Takeda M, Kanda Y, Sekino Y, Yoshida Y, Yamashita JK. 2020. Specific induction and long-term maintenance of high purity ventricular cardiomyocytes from human induced pluripotent stem cells. PLoS One 15:e0241287. https://doi.org/10.1371/journal.pone.0241287
  16. Galdos FX, Guo Y, Paige SL, VanDusen NJ, Wu SM, Pu WT. 2017. Cardiac regeneration: lessons from development. Circ. Res. 120:941-959. https://doi.org/10.1161/CIRCRESAHA.116.309040
  17. Goversen B, van der Heyden MAG, van Veen TAB, de Boer TP. 2018. The immature electrophysiological phenotype of iPSC-CMs still hampers in vitro drug screening: special focus on IK1. Pharmacol. Ther. 183:127-136. https://doi.org/10.1016/j.pharmthera.2017.10.001
  18. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, Hermiller JB Jr, Reisman MA, Schaer GL, Sherman W. 2009. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J. Am. Coll. Cardiol. 54:2277-2286. https://doi.org/10.1016/j.jacc.2009.06.055
  19. Hirose K, Payumo AY, Cutie S, Hoang A, Zhang H, Guyot R, Lunn D, Bigley RB, Yu H, Wang J, Smith M, Gillett E, Muroy SE, Schmid T, Wilson E, Field KA, Reeder DM, Maden M, Yartsev MM, Wolfgang MJ, Grutzner F, Scanlan TS, Szweda LI, Buffenstein R, Hu G, Flamant F, Olgin JE, Huang GN. 2019. Evidence for hormonal control of heart regenerative capacity during endothermy acquisition. Science 364:184-188. https://doi.org/10.1126/science.aar2038
  20. Hwang HS, Kryshtal DO, Feaster TK, Sanchez-Freire V, Zhang J, Kamp TJ, Hong CC, Wu JC, Knollmann BC. 2015. Comparable calcium handling of human iPSC-derived cardiomyocytes generated by multiple laboratories. J. Mol. Cell. Cardiol. 85:79-88. https://doi.org/10.1016/j.yjmcc.2015.05.003
  21. Ivashchenko CY, Pipes GC, Lozinskaya IM, Lin Z, Xiaoping X, Needle S, Grygielko ET, Hu E, Toomey JR, Lepore JJ, Willette RN. 2013. Human-induced pluripotent stem cell-derived cardiomyocytes exhibit temporal changes in phenotype. Am. J. Physiol. Heart Circ. Physiol. 305:H913-H922. https://doi.org/10.1152/ajpheart.00819.2012
  22. Jeevaratnam K, Chadda KR, Huang CL, Camm AJ. 2018. Cardiac potassium channels: physiological insights for targeted therapy. J. Cardiovasc. Pharmacol. Ther. 23:119-129. https://doi.org/10.1177/1074248417729880
  23. Kamakura T, Makiyama T, Sasaki K, Yoshida Y, Wuriyanghai Y, Chen J, Hattori T, Ohno S, Kita T, Horie M, Yamanaka S, Kimura T. 2013. Ultrastructural maturation of human-induced pluripotent stem cell-derived cardiomyocytes in a long-term culture. Circ. J. 77:1307-1314. https://doi.org/10.1253/circj.CJ-12-0987
  24. Karakikes I, Ameen M, Termglinchan V, Wu JC. 2015. Human induced pluripotent stem cell-derived cardiomyocytes: insights into molecular, cellular, and functional phenotypes. Circ. Res. 117:80-88. https://doi.org/10.1161/CIRCRESAHA.117.305365
  25. Kashiyama N, Miyagawa S, Fukushima S, Kawamura T, Kawamura A, Yoshida S, Eiraku S, Harada A, Matsunaga K, Watabe T, Toda K, Hatazawa J, Sawa Y. 2019. MHC-mismatched allotransplantation of induced pluripotent stem cell-derived cardiomyocyte sheets to improve cardiac function in a primate ischemic cardiomyopathy model. Transplantation 103:1582-1590. https://doi.org/10.1097/tp.0000000000002765
  26. Katrukha IA. 2013. Human cardiac troponin complex. Structure and functions. Biochemistry (Mosc.) 78:1447-1465. https://doi.org/10.1134/S0006297913130063
  27. Kawaguchi S, Soma Y, Nakajima K, Kanazawa H, Tohyama S, Tabei R, Hirano A, Handa N, Yamada Y, Okuda S, Hishikawa S, Teratani T, Kunita S, Kishino Y, Okada M, Tanosaki S, Someya S, Morita Y, Tani H, Kawai Y, Yamazaki M, Ito A, Shibata R, Murohara T, Tabata Y, Kobayashi E, Shimizu H, Fukuda K, Fujita J. 2021. Intramyocardial transplantation of human iPS cell-derived cardiac spheroids improves cardiac function in heart failure animals. JACC Basic Transl. Sci. 6: 239-254. https://doi.org/10.1016/j.jacbts.2020.11.017
  28. Koivumaki JT, Naumenko N, Tuomainen T, Takalo J, Oksanen M, Puttonen KA, Lehtonen S, Kuusisto J, Laakso M, Koistinaho J, Tavi P. 2018. Structural immaturity of human iPSC-derived cardiomyocytes: in silico investigation of effects on function and disease modeling. Front. Physiol. 9:80. https://doi.org/10.3389/fphys.2018.00080
  29. Lasher RA, Pahnke AQ, Johnson JM, Sachse FB, Hitchcock RW. 2012. Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype. J. Tissue Eng. 3:2041731412455354. https://doi.org/10.1177/2041731412455354
  30. Lin ZC, McGuire AF, Burridge PW, Matsa E, Lou HY, Wu JC, Cui B. 2017. Accurate nanoelectrode recording of human pluripotent stem cell-derived cardiomyocytes for assaying drugs and modeling disease. Microsyst. Nanoeng. 3:16080. https://doi.org/10.1038/micronano.2016.80
  31. Liu J, Laksman Z, Backx PH. 2016. The electrophysiological development of cardiomyocytes. Adv. Drug Deliv. Rev. 96:253-273. https://doi.org/10.1016/j.addr.2015.12.023
  32. Lundy SD, Zhu WZ, Regnier M, Laflamme MA. 2013. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev. 22:1991-2002. https://doi.org/10.1089/scd.2012.0490
  33. Menasche P, Vanneaux V, Hagege A, Bel A, Cholley B, Parouchev A, Cacciapuoti I, Al-Daccak R, Benhamouda N, Blons H, Agbulut O, Tosca L, Trouvin JH, Fabreguettes JR, Bellamy V, Charron D, Tartour E, Tachdjian G, Desnos M, Larghero J. 2018. Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction. J. Am. Coll. Cardiol. 71:429-438. https://doi.org/10.1016/j.jacc.2017.11.047
  34. Park SJ, Kim H, Lee S, Kim J, Jung TH, Choi SW, Park BW, Kang SW, Elliott DA, Stanley EG, Elefanty AG, Ban K, Park HJ, Moon SH. 2022. Effect and application of cryopreserved three-dimensional microcardiac spheroids in myocardial infarction therapy. Clin. Transl. Med. 12:e721.
  35. Park SJ, Kim RY, Park BW, Lee S, Choi SW, Park JH, Choi JJ, Kim SW, Jang J, Cho DW, Chung HM, Moon SH, Ban K, Park HJ. 2019. Dual stem cell therapy synergistically improves cardiac function and vascular regeneration following myocardial infarction. Nat. Commun. 10:3123. https://doi.org/10.1038/s41467-019-11091-2
  36. Piquereau J and Ventura-Clapier R. 2018. Maturation of cardiac energy metabolism during perinatal development. Front. Physiol. 9:959. https://doi.org/10.3389/fphys.2018.00959
  37. Romagnuolo R, Masoudpour H, Porta-Sanchez A, Qiang B, Barry J, Laskary A, Qi X, Masse S, Magtibay K, Kawajiri H, Wu J, Valdman Sadikov T, Rothberg J, Panchalingam KM, Titus E, Li RK, Zandstra PW, Wright GA, Nanthakumar K, Ghugre NR, Keller G, Laflamme MA. 2019. Human embryonic stem cell-derived cardiomyocytes regenerate the infarcted pig heart but induce ventricular tachyarrhythmias. Stem Cell Reports 12:967-981. https://doi.org/10.1016/j.stemcr.2019.04.005
  38. Ruan JL, Tulloch NL, Razumova MV, Saiget M, Muskheli V, Pabon L, Reinecke H, Regnier M, Murry CE. 2016. Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation 134:1557-1567. https://doi.org/10.1161/CIRCULATIONAHA.114.014998
  39. Sharifi M, Buzatu D, Harris S, Wilkes J. 2017. Development of models for predicting Torsade de Pointes cardiac arrhythmias using perceptron neural networks. BMC Bioinformatics 18(Suppl 14):497. https://doi.org/10.1186/s12859-017-1895-2
  40. 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. 2016. Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature 538:388-391. https://doi.org/10.1038/nature19815
  41. Shinozawa T, Imahashi K, Sawada H, Furukawa H, Takami K. 2012. Determination of appropriate stage of human-induced pluripotent stem cell-derived cardiomyocytes for drug screening and pharmacological evaluation in vitro. J. Biomol. Screen. 17:1192-1203. https://doi.org/10.1177/1087057112449864
  42. Talman V and Kivela R. 2018. Cardiomyocyte-endothelial cell interactions in cardiac remodeling and regeneration. Front. Cardiovasc. Med. 5:101. https://doi.org/10.3389/fcvm.2018.00101
  43. Tveito A, Lines GT, Edwards AG, Maleckar MM, Michailova A, Hake J, McCulloch A. 2012. Slow Calcium-Depolarization-Calcium waves may initiate fast local depolarization waves in ventricular tissue. Prog. Biophys. Mol. Biol. 110:295-304. https://doi.org/10.1016/j.pbiomolbio.2012.07.005
  44. Varzideh F, Mahmoudi E, Pahlavan S. 2019. Coculture with noncardiac cells promoted maturation of human stem cell-derived cardiomyocyte microtissues. J. Cell. Biochem. 120: 16681-16691. https://doi.org/10.1002/jcb.28926
  45. Veerman CC, Mengarelli I, Lodder EM, Kosmidis G, Bellin M, Zhang M, Dittmann S, Guan K, Wilde AAM, Schulze-Bahr E, Greber B, Bezzina CR, Verkerk AO. 2017. Switch from fetal to adult SCN5A isoform in human induced pluripotent stem cell-derived cardiomyocytes unmasks the cellular phenotype of a conduction disease-causing mutation. J. Am. Heart Assoc. 6:e005135. https://doi.org/10.1161/JAHA.116.005135
  46. Yang X, Pabon L, Murry CE. 2014a. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ. Res. 114:511-523. https://doi.org/10.1161/CIRCRESAHA.114.300558
  47. Yang X, Rodriguez M, Pabon L, Fischer KA, Reinecke H, Regnier M, Sniadecki NJ, Ruohola-Baker H, Murry CE. 2014b. Tri-iodo-l-thyronine promotes the maturation of human cardiomyocytes-derived from induced pluripotent stem cells. J. Mol. Cell. Cardiol. 72:296-304. https://doi.org/10.1016/j.yjmcc.2014.04.005
  48. Yoshida S, Miyagawa S, Fukushima S, Kawamura T, Kashiyama N, Ohashi F, Toyofuku T, Toda K, Sawa Y. 2018. Maturation of human induced pluripotent stem cell-derived cardiomyocytes by soluble factors from human mesenchymal stem cells. Mol. Ther. 26:2681-2695. https://doi.org/10.1016/j.ymthe.2018.08.012
  49. Youm JB. 2016. Electrophysiological properties and calcium handling of embryonic stem cell-derived cardiomyocytes. Integr. Med. Res. 5:3-10. https://doi.org/10.1016/j.imr.2015.12.007
  50. Yu Y, Qin N, Lu XA, Li J, Han X, Ni X, Ye L, Shen Z, Chen W, Zhao ZA, Lei W, Hu S. 2019. Human embryonic stem cellderived cardiomyocyte therapy in mouse permanent ischemia and ischemia-reperfusion models. Stem Cell Res. Ther. 10:167. https://doi.org/10.1186/s13287-019-1271-4
  51. Zhang P, Su J, Mende U. 2012. Cross talk between cardiac myocytes and fibroblasts: from multiscale investigative approaches to mechanisms and functional consequences. Am. J. Physiol. Heart Circ. Physiol. 303:H1385-H1396. https://doi.org/10.1152/ajpheart.01167.2011
  52. Zhao Z, Lan H, El-Battrawy I, Li X, Buljubasic F, Sattler K, Yucel G, Lang S, Tiburcy M, Zimmermann WH, Cyganek L, Utikal J, Wieland T, Borggrefe M, Zhou XB, Akin I. 2018. Ion channel expression and characterization in human induced pluripotent stem cell-derived cardiomyocytes. Stem Cells Int. 2018: 6067096. https://doi.org/10.1155/2018/6067096