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      Microscale grooves regulate maturation development of hPSC‐CMs by the transient receptor potential channels (TRP channels)

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          Abstract

          The use of human pluripotent stem cell‐derived cardiomyocytes (hPSC‐CMs) is limited in drug discovery and cardiac disease mechanism studies due to cell immaturity. Micro‐scaled grooves can promote the maturation of cardiomyocytes by aligning them in order, but the mechanism of cardiomyocytes alignment has not been studied. From the level of calcium activity, gene expression and cell morphology, we verified that the W20H5 grooves can effectively promote the maturation of cardiomyocytes. The transient receptor potential channels (TRP channels) also play an important role in the maturation and development of cardiomyocytes. These findings support the engineered hPSC‐CMs as a powerful model to study cardiac disease mechanism and partly mimic the myocardial morphological development. The important role of the TRP channels in the maturation and development of myocardium is first revealed.

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          Advanced maturation of human cardiac tissue grown from pluripotent stem cells

          Kacey Ronaldson-Bouchard, Stephen Ma, Keith Yeager … (2018)
          Cardiac tissues generated from human induced pluripotent stem (iPS) cells can serve as platforms for patient-specific studies of physiology and disease 1–6 . The predictive power of these models remains limited by their immature state 1,2,5,6 . We show that this fundamental limitation could be overcome if cardiac tissues are formed from early iPS-derived cardiomyocytes (iPS-CM), soon after the initiation of spontaneous contractions, and subjected to physical conditioning of an increasing intensity. After only 4 weeks of culture, these tissues displayed adult-like gene expression profiles, remarkably organized ultrastructure, physiologic sarcomere length (2.2 μm) and density of mitochondria (30%), the presence of transverse tubules (t-tubules), oxidative metabolism, positive force-frequency relationship, and functional calcium handling for all iPS cell lines studied. Electromechanical properties developed more slowly and did not achieve the stage of maturity seen in adult human myocardium. Tissue maturity was necessary for achieving physiologic responses to isoproterenol and recapitulating pathological hypertrophy, in support of the utility of this tissue model for studies of cardiac development and disease.
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            Human induced pluripotent stem cell-derived cardiomyocytes: insights into molecular, cellular, and functional phenotypes.

            Ioannis Karakikes, Mohamed Ameen, Vittavat Termglinchan … (2015)
            Disease models are essential for understanding cardiovascular disease pathogenesis and developing new therapeutics. The human induced pluripotent stem cell (iPSC) technology has generated significant enthusiasm for its potential application in basic and translational cardiac research. Patient-specific iPSC-derived cardiomyocytes offer an attractive experimental platform to model cardiovascular diseases, study the earliest stages of human development, accelerate predictive drug toxicology tests, and advance potential regenerative therapies. Harnessing the power of iPSC-derived cardiomyocytes could eliminate confounding species-specific and interpersonal variations and ultimately pave the way for the development of personalized medicine for cardiovascular diseases. However, the predictive power of iPSC-derived cardiomyocytes as a valuable model is contingent on comprehensive and rigorous molecular and functional characterization.
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              Biowire: a new platform for maturation of human pluripotent stem cell derived cardiomyocytes

              Sara Nunes, Jason W. Miklas, Jie Liu … (2013)
              Directed differentiation protocols enable derivation of cardiomyocytes from human pluripotent stem cells (hPSC) and permit engineering of human myocardium in vitro. However, hPSC-derived cardiomyocytes are reflective of very early human development, limiting their utility in the generation of in vitro models of mature myocardium. Here, we developed a new platform that combines three-dimensional cell cultivation in a microfabricated system with electrical stimulation to mature hPSC-derived cardiac tissues. We utilized quantitative structural, molecular and electrophysiological analyses to elucidate the responses of immature human myocardium to electrical stimulation and pacing. We demonstrated that the engineered platform allowed for the generation of 3-dimensional, aligned cardiac tissues (biowires) with frequent striations. Biowires submitted to electrical stimulation markedly increased myofibril ultrastructural organization, displayed elevated conduction velocity and altered both the electrophysiological and Ca2+ handling properties versus non-stimulated controls. These changes were in agreement with cardiomyocyte maturation and were dependent on the stimulation rate.
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                Author and article information

                Contributors
                Hongfeng Jiang: hfjiang@ccmu.edu.cn
                Feng Lan:
                ORCID: https://orcid.org/0000-0002-9038-4014
                fenglan@ccmu.edu.cn
                Journal
                Journal ID (nlm-ta): J Cell Mol Med
                Journal ID (iso-abbrev): J Cell Mol Med
                Journal ID (doi): 10.1111/(ISSN)1582-4934
                Journal ID (publisher-id): JCMM
                Title: Journal of Cellular and Molecular Medicine
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Print): 1582-1838
                ISSN (Electronic): 1582-4934
                Publication date (Electronic): 10 March 2021
                Publication date (Print): April 2021
                Volume: 25
                Issue: 7 ( doiID: 10.1111/jcmm.v25.7 )
                Pages: 3469-3483
                Affiliations
                [ 1 ] Beijing Lab for Cardiovascular Precision Medicine Anzhen Hospital Capital Medical University Beijing China
                [ 2 ] State Key Laboratory of Stem Cell and Reproductive Biology Institute of Zoology Chinese Academy of Sciences Beijing China
                [ 3 ] University of Chinese Academy of Sciences Beijing China
                [ 4 ] Department of Biomedical Engineering School of Medicine Tsinghua University Beijing China
                [ 5 ] Department of Cardiology Peking University Third Hospital Beijing China
                [ 6 ] State Key Laboratory of Chemical Resource Engineering Beijing Laboratory of Biomedical Materials Beijing Advanced Innovation Center for Soft Matter Science and Engineering Beijing University of Chemical Technology Beijing China
                [ 7 ] Key Laboratory of Remodeling‐Related Cardiovascular Diseases Ministry of Education Beijing Anzhen Hospital Capital Medical University Beijing China
                Author notes
                [*] [* ] Correspondence

                Hongfeng Jiang, Key Laboratory of Remodeling‐Related Cardiovascular Diseases, Ministry of Education, Beijing Anzhen Hospital, Capital Medical University, Beijing 100029, China.

                Email: hfjiang@ 123456ccmu.edu.cn

                Feng Lan, Beijing Lab for Cardiovascular Precision Medicine, Anzhen Hospital, Capital Medical University, 2 Anzhen Road, Chaoyang District, Beijing 100029, China.

                Email: fenglan@ 123456ccmu.edu.cn

                Author information
                https://orcid.org/0000-0002-9038-4014
                Article
                Publisher ID: JCMM16429
                DOI: 10.1111/jcmm.16429
                PMC ID: 8034460
                PubMed ID: 33689230
                SO-VID: fe5f0a83-f58f-48da-aacd-12c15662b5b0
                Copyright © © 2021 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date revision received : 07 February 2021
                Date received : 10 October 2020
                Date accepted : 09 February 2021
                Page count
                Figures: 6, Tables: 0, Pages: 15, Words: 8478
                Funding
                Funded by: Beijing Natural Science Foundation , open-funder-registry 10.13039/501100005089;
                Award ID: Z190013
                Funded by: Beijing Nova Program , open-funder-registry 10.13039/501100005090;
                Award ID: Z181100006218086
                Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;
                Award ID: 81970205
                Funded by: Non‐profit Central Research Institute Fund of Chinese Academy of Medical Sciences
                Award ID: 2019PT320026
                Categories
                Subject: Original Article
                Subject: Original Articles
                Custom metadata
                source-schema-version-number 2.0
                cover-date April 2021
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.1 mode:remove_FC converted:09.04.2021

                ScienceOpen disciplines: Molecular medicine
                Keywords: hpsc‐cms,maturation,microtopography,topographic cues,trp channels
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: hpsc‐cms, maturation, microtopography, topographic cues, trp channels

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