Skip to main content
Top
Published in: Heart and Vessels 6/2021

01-06-2021 | Original Article

Continuous measurement of surface electrical potentials from transplanted cardiomyocyte tissue derived from human-induced pluripotent stem cells under physiological conditions in vivo

Authors: Hiroshi Goto, Hyoe Komae, Hidekazu Sekine, Jun Homma, Sunghoon Lee, Tomoyuki Yokota, Katsuhisa Matsuura, Takao Someya, Minoru Ono, Tatsuya Shimizu

Published in: Heart and Vessels | Issue 6/2021

Login to get access

Abstract

Recording the electrical potentials of bioengineered cardiac tissue after transplantation would help to monitor the maturation of the tissue and detect adverse events such as arrhythmia. However, a few studies have reported the measurement of myocardial tissue potentials in vivo under physiological conditions. In this study, human-induced pluripotent stem cell-derived cardiomyocyte (hiPSCM) sheets were stacked and ectopically transplanted into the subcutaneous tissue of rats for culture in vivo. Three months after transplantation, a flexible nanomesh sensor was implanted onto the hiPSCM tissue to record its surface electrical potentials under physiological conditions, i.e., without the need for anesthetic agents that might adversely affect cardiomyocyte function. The nanomesh sensor was able to record electrical potentials in non-sedated, ambulating animals for up to 48 h. When compared with recordings made with conventional needle electrodes in anesthetized animals, the waveforms obtained with the nanomesh sensor showed less dispersion of waveform interval and waveform duration. However, waveform amplitude tended to show greater dispersion for the nanomesh sensor than for the needle electrodes, possibly due to motion artifacts produced by movements of the animal or local tissue changes in response to surgical implantation of the sensor. The implantable nanomesh sensor utilized in this study potentially could be used for long-term monitoring of bioengineered myocardial tissue in vivo under physiological conditions.
Literature
1.
go back to reference Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676CrossRef Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676CrossRef
2.
go back to reference Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872CrossRef Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872CrossRef
3.
go back to reference Protze SI, Lee JH, Keller GM (2019) Human pluripotent stem cell-derived cardiovascular cells: from developmental biology to therapeutic applications. Cell Stem Cell 25:311–327CrossRef Protze SI, Lee JH, Keller GM (2019) Human pluripotent stem cell-derived cardiovascular cells: from developmental biology to therapeutic applications. Cell Stem Cell 25:311–327CrossRef
4.
go back to reference Matsuura K, Wada M, Shimizu T, Haraguchi Y, Sato F, Sugiyama K, Konishi K, Shiba Y, Ichikawa H, Tachibana A, Ikeda U, Yamato M, Hagiwara N, Okano T (2012) Creation of human cardiac cell sheets using pluripotent stem cells. Biochem Biophys Res Commun 425:321–327CrossRef Matsuura K, Wada M, Shimizu T, Haraguchi Y, Sato F, Sugiyama K, Konishi K, Shiba Y, Ichikawa H, Tachibana A, Ikeda U, Yamato M, Hagiwara N, Okano T (2012) Creation of human cardiac cell sheets using pluripotent stem cells. Biochem Biophys Res Commun 425:321–327CrossRef
5.
go back to reference Seta H, Matsuura K, Sekine H, Yamazaki K, Shimizu T (2017) Tubular cardiac tissues derived from human induced pluripotent stem cells generate pulse pressure in vivo. Sci Rep 7:45499CrossRef Seta H, Matsuura K, Sekine H, Yamazaki K, Shimizu T (2017) Tubular cardiac tissues derived from human induced pluripotent stem cells generate pulse pressure in vivo. Sci Rep 7:45499CrossRef
6.
go back to reference Komae H, Sekine H, Dobashi I, Matsuura K, Ono M, Okano T, Shimizu T (2017) Three-dimensional functional human myocardial tissues fabricated from induced pluripotent stem cells. J Tissue Eng Regen Med 11:926–935CrossRef Komae H, Sekine H, Dobashi I, Matsuura K, Ono M, Okano T, Shimizu T (2017) Three-dimensional functional human myocardial tissues fabricated from induced pluripotent stem cells. J Tissue Eng Regen Med 11:926–935CrossRef
7.
go back to reference Masuda N, Sekine H, Niinami H, Shimizu T (2020) Engineering of functional cardiac tubes by stepwise transplantation of cardiac cell sheets onto intestinal mesentery. Heart Vessels 35:859–867CrossRef Masuda N, Sekine H, Niinami H, Shimizu T (2020) Engineering of functional cardiac tubes by stepwise transplantation of cardiac cell sheets onto intestinal mesentery. Heart Vessels 35:859–867CrossRef
8.
go back to reference Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ, Mahoney WM, Van Biber B, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem HP, Laflamme MA, Murry CE (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510:273–277CrossRef Chong JJ, Yang X, Don CW, Minami E, Liu YW, Weyers JJ, Mahoney WM, Van Biber B, Cook SM, Palpant NJ, Gantz JA, Fugate JA, Muskheli V, Gough GM, Vogel KW, Astley CA, Hotchkiss CE, Baldessari A, Pabon L, Reinecke H, Gill EA, Nelson V, Kiem HP, Laflamme MA, Murry CE (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510:273–277CrossRef
9.
go back to reference Miyagawa S, Fukushima S, Imanishi Y, Kawamura T, Mochizuki-Oda N, Masuda S, Sawa Y (2016) Building a new treatment for heart failure—transplantation of induced pluripotent stem cell-derived cells into the heart. Curr Gene Ther 16:5–13CrossRef Miyagawa S, Fukushima S, Imanishi Y, Kawamura T, Mochizuki-Oda N, Masuda S, Sawa Y (2016) Building a new treatment for heart failure—transplantation of induced pluripotent stem cell-derived cells into the heart. Curr Gene Ther 16:5–13CrossRef
10.
go back to reference Sekitani T, Yokota T, Kuribara K, Kaltenbrunner M, Fukushima T, Inoue Y, Sekino M, Isoyama T, Abe Y, Onodera H, Someya T (2016) Ultraflexible organic amplifier with biocompatible gel electrodes. Nat Commun 7:11425CrossRef Sekitani T, Yokota T, Kuribara K, Kaltenbrunner M, Fukushima T, Inoue Y, Sekino M, Isoyama T, Abe Y, Onodera H, Someya T (2016) Ultraflexible organic amplifier with biocompatible gel electrodes. Nat Commun 7:11425CrossRef
11.
go back to reference Constantinescu G, Jeong JW, Li X, Scott DK, Jang KI, Chung HJ, Rogers JA, Rieger J (2016) Epidermal electronics for electromyography: an application to swallowing therapy. Med Eng Phys 38:807–812CrossRef Constantinescu G, Jeong JW, Li X, Scott DK, Jang KI, Chung HJ, Rogers JA, Rieger J (2016) Epidermal electronics for electromyography: an application to swallowing therapy. Med Eng Phys 38:807–812CrossRef
12.
go back to reference Dai X, Zhou W, Gao T, Liu J, Lieber CM (2016) Three-dimensional mapping and regulation of action potential propagation in nanoelectronics-innervated tissues. Nat Nanotech 11:776–782CrossRef Dai X, Zhou W, Gao T, Liu J, Lieber CM (2016) Three-dimensional mapping and regulation of action potential propagation in nanoelectronics-innervated tissues. Nat Nanotech 11:776–782CrossRef
13.
go back to reference Xu L, Gutbrod SR, Ma Y, Petrossians A, Liu Y, Webb RC, Fan JA, Yang Z, Xu R, Whalen JJ 3rd, Weiland JD, Huang Y, Efimov IR, Rogers JA (2015) Materials and fractal designs for 3D multifunctional integumentary membranes with capabilities in cardiac electrotherapy. Adv Mater 27:1731–1737CrossRef Xu L, Gutbrod SR, Ma Y, Petrossians A, Liu Y, Webb RC, Fan JA, Yang Z, Xu R, Whalen JJ 3rd, Weiland JD, Huang Y, Efimov IR, Rogers JA (2015) Materials and fractal designs for 3D multifunctional integumentary membranes with capabilities in cardiac electrotherapy. Adv Mater 27:1731–1737CrossRef
14.
go back to reference Feiner R, Engel L, Fleischer S, Malki M, Gal I, Shapira A, Shacham-Diamand Y, Dvir T (2016) Engineered hybrid cardiac patches with multifunctional electronics for online monitoring and regulation of tissue function. Nat Mater 15:679–685CrossRef Feiner R, Engel L, Fleischer S, Malki M, Gal I, Shapira A, Shacham-Diamand Y, Dvir T (2016) Engineered hybrid cardiac patches with multifunctional electronics for online monitoring and regulation of tissue function. Nat Mater 15:679–685CrossRef
15.
go back to reference Morikawa Y, Yamagiwa S, Sawahata H, Numano R, Koida K, Ishida M, Kawano T (2018) Ultrastretchable kirigami bioprobes. Adv Healthc Mater 7:1701100CrossRef Morikawa Y, Yamagiwa S, Sawahata H, Numano R, Koida K, Ishida M, Kawano T (2018) Ultrastretchable kirigami bioprobes. Adv Healthc Mater 7:1701100CrossRef
16.
go back to reference Minev IR, Musienko P, Hirsch A, Barraud Q, Wenger N, Moraud EM, Gandar J, Capogrosso M, Milekovic T, Asboth L, Torres RF, Vachicouras N, Liu Q, Pavlova N, Duis S, Larmagnac A, Vörös J, Micera S, Suo Z, Courtine G, Lacour SP (2015) Biomaterials. Electronic dura mater for long-term multimodal neural interfaces. Science 347:159–163CrossRef Minev IR, Musienko P, Hirsch A, Barraud Q, Wenger N, Moraud EM, Gandar J, Capogrosso M, Milekovic T, Asboth L, Torres RF, Vachicouras N, Liu Q, Pavlova N, Duis S, Larmagnac A, Vörös J, Micera S, Suo Z, Courtine G, Lacour SP (2015) Biomaterials. Electronic dura mater for long-term multimodal neural interfaces. Science 347:159–163CrossRef
17.
go back to reference Kozai TD, Langhals NB, Patel PR, Deng X, Zhang H, Smith KL, Lahann J, Kotov NA, Kipke DR (2012) Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat Mater 11:1065–1073CrossRef Kozai TD, Langhals NB, Patel PR, Deng X, Zhang H, Smith KL, Lahann J, Kotov NA, Kipke DR (2012) Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat Mater 11:1065–1073CrossRef
18.
go back to reference Tsukada YT, Tokita M, Murata H, Hirasawa Y, Yodogawa K, Iwasaki YK, Asai K, Shimizu W, Kasai N, Nakashima H, Tsukada S (2019) Validation of wearable textile electrodes for ECG monitoring. Heart Vessels 34:1203–1211CrossRef Tsukada YT, Tokita M, Murata H, Hirasawa Y, Yodogawa K, Iwasaki YK, Asai K, Shimizu W, Kasai N, Nakashima H, Tsukada S (2019) Validation of wearable textile electrodes for ECG monitoring. Heart Vessels 34:1203–1211CrossRef
19.
go back to reference Lee S, Sasaki D, Kim D, Mori M, Yokota T, Lee H, Park S, Fukuda K, Sekino M, Matsuura K, Shimizu T, Someya T (2019) Ultrasoft electronics to monitor dynamically pulsing cardiomyocytes. Nat Nanotechnol 14:156–160CrossRef Lee S, Sasaki D, Kim D, Mori M, Yokota T, Lee H, Park S, Fukuda K, Sekino M, Matsuura K, Shimizu T, Someya T (2019) Ultrasoft electronics to monitor dynamically pulsing cardiomyocytes. Nat Nanotechnol 14:156–160CrossRef
20.
go back to reference Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K, Kikuchi A, Umezu M, Okano T (2002) Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90:e40-48CrossRef Shimizu T, Yamato M, Isoi Y, Akutsu T, Setomaru T, Abe K, Kikuchi A, Umezu M, Okano T (2002) Fabrication of pulsatile cardiac tissue grafts using a novel 3-dimensional cell sheet manipulation technique and temperature-responsive cell culture surfaces. Circ Res 90:e40-48CrossRef
21.
go back to reference Ohashi K, Yokoyama T, Yamato M, Kuge H, Kanehiro H, Tsutsumi M, Amanuma T, Iwata H, Yang J, Okano T, Nakajima Y (2007) Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med 13:880–885CrossRef Ohashi K, Yokoyama T, Yamato M, Kuge H, Kanehiro H, Tsutsumi M, Amanuma T, Iwata H, Yang J, Okano T, Nakajima Y (2007) Engineering functional two- and three-dimensional liver systems in vivo using hepatic tissue sheets. Nat Med 13:880–885CrossRef
22.
go back to reference Shimizu H, Ohashi K, Utoh R, Ise K, Gotoh M, Yamato M, Okano T (2009) Bioengineering of a functional sheet of islet cells for the treatment of diabetes mellitus. Biomaterials 30:5943–5949CrossRef Shimizu H, Ohashi K, Utoh R, Ise K, Gotoh M, Yamato M, Okano T (2009) Bioengineering of a functional sheet of islet cells for the treatment of diabetes mellitus. Biomaterials 30:5943–5949CrossRef
23.
go back to reference Sawa Y, Yoshikawa Y, Toda K, Fukushima S, Yamazaki K, Ono M, Sakata Y, Hagiwara N, Kinugawa K, Miyagawa S (2015) Safety and efficacy of autologous skeletal myoblast sheets (TCD-51073) for the treatment of severe chronic heart failure due to ischemic heart disease. Circ J 79:991–999CrossRef Sawa Y, Yoshikawa Y, Toda K, Fukushima S, Yamazaki K, Ono M, Sakata Y, Hagiwara N, Kinugawa K, Miyagawa S (2015) Safety and efficacy of autologous skeletal myoblast sheets (TCD-51073) for the treatment of severe chronic heart failure due to ischemic heart disease. Circ J 79:991–999CrossRef
24.
go back to reference Memon IA, Sawa Y, Fukushima N, Matsumiya G, Miyagawa S, Taketani S, Sakakida SK, Kondoh H, Aleshin AN, Shimizu T, Okano T, Matsuda H (2005) Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 130:1333–1341CrossRef Memon IA, Sawa Y, Fukushima N, Matsumiya G, Miyagawa S, Taketani S, Sakakida SK, Kondoh H, Aleshin AN, Shimizu T, Okano T, Matsuda H (2005) Repair of impaired myocardium by means of implantation of engineered autologous myoblast sheets. J Thorac Cardiovasc Surg 130:1333–1341CrossRef
Metadata
Title
Continuous measurement of surface electrical potentials from transplanted cardiomyocyte tissue derived from human-induced pluripotent stem cells under physiological conditions in vivo
Authors
Hiroshi Goto
Hyoe Komae
Hidekazu Sekine
Jun Homma
Sunghoon Lee
Tomoyuki Yokota
Katsuhisa Matsuura
Takao Someya
Minoru Ono
Tatsuya Shimizu
Publication date
01-06-2021
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 6/2021
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-021-01824-z

Other articles of this Issue 6/2021

Heart and Vessels 6/2021 Go to the issue