Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework

Dominic E. Fullenkamp; Woo Youl Maeng; Seyong Oh; Haiwen Luan; Kyung Su Kim; Ivana A. Chychula; Jin Tae Kim; Jae Young Yoo; Cory W. Holgren; Alexis R. Demonbreun; Sharon Ann George; Binjie Li; Yaching Hsu; Gooyoon Chung; Jeongmin Yoo; Jahyun Koo; Yoonseok Park; Igor Rudolf Efimov; Elizabeth M McNally; John A. Rogers

doi:10.1126/sciadv.ado7089

Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework

Dominic E. Fullenkamp, Woo Youl Maeng, Seyong Oh, Haiwen Luan, Kyung Su Kim, Ivana A. Chychula, Jin Tae Kim, Jae Young Yoo, Cory W. Holgren, Alexis R. Demonbreun, Sharon Ann George, Binjie Li, Yaching Hsu, Gooyoon Chung, Jeongmin Yoo, Jahyun Koo, Yoonseok Park^*, Igor Rudolf Efimov^*, Elizabeth M McNally^*, John A. Rogers^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

Engineered heart tissues (EHTs) generated from human induced pluripotent stem cell–derived cardiomyocytes (hiPSC-CMs) represent powerful platforms for human cardiac research, especially in drug testing and disease modeling. Here, we report a flexible, three-dimensional electronic framework that enables real-time, spatiotemporal analysis of electrophysiologic and mechanical signals in EHTs under physiological loading conditions for dynamic, noninvasive, longer-term assessments. These electromechanically monitored EHTs support multisite measurements throughout the tissue under baseline conditions and in response to stimuli. Demonstrations include uses in tracking physiological responses to pharmacologically active agents and in capturing electrophysiological characteristics of reentrant arrhythmias. This platform facilitates precise analysis of signal location and conduction velocity in human cardiomyocyte tissues, as the basis for a broad range of advanced cardiovascular studies.

Original language	English (US)
Article number	eado7089
Journal	Science Advances
Volume	10
Issue number	37
DOIs	https://doi.org/10.1126/sciadv.ado7089
State	Published - Sep 13 2024

Funding

D.E.F., I.R.E., and E.M.M. are CZ Biohub Chicago Investigators. This work is supported by the Querrey-Simpson Institute for Bioelectronics at Northwestern University and funding by NIH HL168758, NIH HL128075, NIH K08HL 163392, NIH HL167813, and Leducq Foundation. Y.P. acknowledges support by National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (RS-2023-00211261) and Korea Institute of Science and Technology (KIST) through 2E32960 and the Basic Science Research Capacity Enhancement Project through Korea Basic Science Institute (National Research Facilities and Equipment Center) grant funded by the Ministry of Education (grant no. 2019R1A6C1010052). S.O. acknowledges support by National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2021R1C1C2010180). K.S.K and J.K acknowledge support by Ministry of Health & Welfare, Republic of Korea (HI22C0467) and National Research Foundation of Korea (NRF) grant funded by the Korea government (MIST) (RS-2024-00345402). This work made use of the Northwestern University Micro/nano Fabrication facility (NUFAB) of Northwestern University\u2019s Atomic and Nanoscale Characterization Experimental (NUANCE) Center, which has received support from the SHyNE Resource (NSF ECCS-2025633), the INN, and Northwestern\u2019s MRSEC program (NSF DMR-1720139). Acknowledgments: d.e.F., i.R.e., and e.M.M. are cZ Biohub chicago investigators. Funding: this work is supported by the Querrey-Simpson institute for Bioelectronics at northwestern University and funding by nih hl168758, nih hl128075, nih K08hl 163392, nih hl167813, and leducq Foundation. Y.P. acknowledges support by national Research Foundation of Korea (nRF) grant funded by the Korea government (MSit) (RS-2023-00211261) and Korea institute of Science and technology (KiSt) through 2e32960 and the Basic Science Research capacity enhancement Project through Korea Basic Science institute (national Research Facilities and equipment center) grant funded by the Ministry of education (grant no. 2019R1A6c1010052). S.O. acknowledges support by national Research Foundation of Korea (nRF) grant funded by the Korea government (MSit) (2021R1c1c2010180). K.S.K and J.K acknowledge support by Ministry of health & Welfare, Republic of Korea (hi22c0467) and national Research Foundation of Korea (nRF) grant funded by the Korea government (MiSt) (RS-2024-00345402). this work made use of the northwestern University Micro/nano Fabrication facility (nUFAB) of northwestern University\u2019s Atomic and nanoscale characterization experimental (nUAnce) center, which has received support from the Shyne Resource (nSF eccS-2025633), the inn, and northwestern\u2019s MRSec program (nSF dMR-1720139). Author contributions: d.e.F.: conceptualization, methodology, writing\u2013review and editing, and writing\u2013original draft; W.-Y.M.: methodology, software, validation, data analysis, engineering investigation, visualization, data curation, writing\u2013review and editing, and writing\u2013original draft; S.O.: conceptualization, methodology, software, data analysis, engineering investigation, writing\u2013review and editing; h.l.: theoretical simulation and software; K.S.K.: methodology, software, validation, data analysis, and writing\u2013review and editing; i.A.c.: methodology and investigation; J.-t.K.: data analysis and investigation; J.-Y.Y.: data analysis and visualization; c.W.h.: methodology; A.R.d.: methodology; S.G.: methodology; B.l.: methodology; Y.h.: methodology; G.c.: visualization; J.Y.: visualization; J.K.: writing\u2013review and editing; Y.P.: conceptualization, methodology, engineering investigation, writing\u2013 review and editing; i.R.e.: conceptualization and writing\u2013review and editing; e.M.M.: conceptualization, project administration, supervision, writing\u2013review and editing, and writing\u2013original draft; J.A.R.: conceptualization, project administration, supervision, writing\u2013review and editing, and writing\u2013original draft. Competing interests: the other authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.

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Fullenkamp, D. E., Maeng, W. Y., Oh, S., Luan, H., Kim, K. S., Chychula, I. A., Kim, J. T., Yoo, J. Y., Holgren, C. W., Demonbreun, A. R., George, S. A., Li, B., Hsu, Y., Chung, G., Yoo, J., Koo, J., Park, Y., Efimov, I. R., McNally, E. M., & Rogers, J. A. (2024). Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework. Science Advances, 10(37), Article eado7089. https://doi.org/10.1126/sciadv.ado7089

@article{187878061ad349359daadcf00d404bd0,

title = "Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework",

abstract = "Engineered heart tissues (EHTs) generated from human induced pluripotent stem cell–derived cardiomyocytes (hiPSC-CMs) represent powerful platforms for human cardiac research, especially in drug testing and disease modeling. Here, we report a flexible, three-dimensional electronic framework that enables real-time, spatiotemporal analysis of electrophysiologic and mechanical signals in EHTs under physiological loading conditions for dynamic, noninvasive, longer-term assessments. These electromechanically monitored EHTs support multisite measurements throughout the tissue under baseline conditions and in response to stimuli. Demonstrations include uses in tracking physiological responses to pharmacologically active agents and in capturing electrophysiological characteristics of reentrant arrhythmias. This platform facilitates precise analysis of signal location and conduction velocity in human cardiomyocyte tissues, as the basis for a broad range of advanced cardiovascular studies.",

author = "Fullenkamp, {Dominic E.} and Maeng, {Woo Youl} and Seyong Oh and Haiwen Luan and Kim, {Kyung Su} and Chychula, {Ivana A.} and Kim, {Jin Tae} and Yoo, {Jae Young} and Holgren, {Cory W.} and Demonbreun, {Alexis R.} and George, {Sharon Ann} and Binjie Li and Yaching Hsu and Gooyoon Chung and Jeongmin Yoo and Jahyun Koo and Yoonseok Park and Efimov, {Igor Rudolf} and McNally, {Elizabeth M} and Rogers, {John A.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2024 The Authors",

year = "2024",

month = sep,

day = "13",

doi = "10.1126/sciadv.ado7089",

language = "English (US)",

volume = "10",

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Fullenkamp, DE, Maeng, WY, Oh, S, Luan, H, Kim, KS, Chychula, IA, Kim, JT, Yoo, JY, Holgren, CW, Demonbreun, AR, George, SA, Li, B, Hsu, Y, Chung, G, Yoo, J, Koo, J, Park, Y, Efimov, IR , McNally, EM & Rogers, JA 2024, 'Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework', Science Advances, vol. 10, no. 37, eado7089. https://doi.org/10.1126/sciadv.ado7089

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T1 - Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework

AU - Fullenkamp, Dominic E.

AU - Maeng, Woo Youl

AU - Oh, Seyong

AU - Luan, Haiwen

AU - Kim, Kyung Su

AU - Chychula, Ivana A.

AU - Kim, Jin Tae

AU - Yoo, Jae Young

AU - Holgren, Cory W.

AU - Demonbreun, Alexis R.

AU - George, Sharon Ann

AU - Li, Binjie

AU - Hsu, Yaching

AU - Chung, Gooyoon

AU - Yoo, Jeongmin

AU - Koo, Jahyun

AU - Park, Yoonseok

AU - Efimov, Igor Rudolf

AU - McNally, Elizabeth M

AU - Rogers, John A.

PY - 2024/9/13

Y1 - 2024/9/13

N2 - Engineered heart tissues (EHTs) generated from human induced pluripotent stem cell–derived cardiomyocytes (hiPSC-CMs) represent powerful platforms for human cardiac research, especially in drug testing and disease modeling. Here, we report a flexible, three-dimensional electronic framework that enables real-time, spatiotemporal analysis of electrophysiologic and mechanical signals in EHTs under physiological loading conditions for dynamic, noninvasive, longer-term assessments. These electromechanically monitored EHTs support multisite measurements throughout the tissue under baseline conditions and in response to stimuli. Demonstrations include uses in tracking physiological responses to pharmacologically active agents and in capturing electrophysiological characteristics of reentrant arrhythmias. This platform facilitates precise analysis of signal location and conduction velocity in human cardiomyocyte tissues, as the basis for a broad range of advanced cardiovascular studies.

AB - Engineered heart tissues (EHTs) generated from human induced pluripotent stem cell–derived cardiomyocytes (hiPSC-CMs) represent powerful platforms for human cardiac research, especially in drug testing and disease modeling. Here, we report a flexible, three-dimensional electronic framework that enables real-time, spatiotemporal analysis of electrophysiologic and mechanical signals in EHTs under physiological loading conditions for dynamic, noninvasive, longer-term assessments. These electromechanically monitored EHTs support multisite measurements throughout the tissue under baseline conditions and in response to stimuli. Demonstrations include uses in tracking physiological responses to pharmacologically active agents and in capturing electrophysiological characteristics of reentrant arrhythmias. This platform facilitates precise analysis of signal location and conduction velocity in human cardiomyocyte tissues, as the basis for a broad range of advanced cardiovascular studies.

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Simultaneous electromechanical monitoring in engineered heart tissues using a mesoscale framework

Abstract

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