Biomaterials Translational ›› 2024, Vol. 5 ›› Issue (4): 337-354.doi: 10.12336/biomatertransl.2024.04.002
• REVIEW • Previous Articles Next Articles
Yongtao Wang1,2, Yan Hou1, Tian Hao3, Marta Garcia-Contreras3, Guoping Li3, Dragos Cretoiu4,5, Junjie Xiao1,2,*()
Received:
2024-08-14
Revised:
2024-09-08
Accepted:
2024-10-08
Online:
2024-11-14
Published:
2024-12-28
Contact:
Junjie Xiao, junjiexiao@shu.edu.cn.Wang, Y.; Hou, Y.; Hao, T.; Garcia-Contreras, M.; Li, G.; Cretoiu, D.; Xiao, J. Model construction and clinical therapeutic potential of engineered cardiac organoids for cardiovascular diseases. Biomater Transl. 2024, 5(4), 337-354.
Figure 1. Overview of cardiac organoid construction technologies, including co-culture, aggregation, scaffolds and geometries. 3D: three–dimensional; CMs: cardiomyocyte; dECM: decellularised extracellular matrix; ECs: endothelial cell. Created with Microsoft PowerPoint 2010.
Figure 2. Spontaneous self–assembly (aggregation) of cardiac cells in appropriate states is used to form cardiac organoids. (A) Cell viability of hiPSC–cardiomyocytes at days 15 and 35. Scale bars: 200 μm. (B) Aggregate size of hiPSC–cardiomyocytes at days 15 and 35. (C) Immunofluorescence analysis of hiPSC–cardiomyocytes (from plated 3D aggregates) for cTnT (red). Scale bar: 30 μm. A–C are reprinted from Correia et al.44 Copyright 2017, Wiley Periodicals, Inc. (D) Schematic (top), bright–field (middle), and fluorescence (bottom) images demonstrating, (i) MSC spheroid aspiration in a media reservoir, (ii) spheroid transfer into a self–healing support hydrogel (FITC–labelled), and (iii) spheroid deposition within the support hydrogel through removal of vacuum from the micropipette tip. (E) Reversible interactions between guest (adamantane, blue) and host (β–cyclodextrin, orange) modified hyaluronic acid of the support hydrogel (containing FITC–microparticles). Scale bars: 250 μm. D, and E are reprinted from Daly et al.47 (F) A schematic diagram of the protocol used to differentiate TNNT2+ cardiomyocytes in embryoid bodies. Reprinted from Lewis–Israeli et al.48 3D: three–dimensional; BMP4: bone morphogenetic protein 4; CHIR99021: a canonical Wnt pathway activator; cTnT: Troponin T; EB: embryoid body; FDA: fluorescein diacetate; FITC: fluorescein isothiocyanate; HOECHST: Hoechst 33342; ins: insulin; ns: not significant; PI: propidium iodide; PSC: pluripotent stem cell; RPMI: RPMI 1640 medium; TNNT2: troponin T2.
Figure 3. Decellularised ECM scaffolds for cardiac organoids. (A) Schematic illustration of heart decellularisation process. (B) Representative images demonstrating the workflow of decellularised ECM scaffolds. (C) H&E and Masson’s trichrome staining of native tissue and decellularised ECM scaffolds. Scale bars: 100 μm. (D) Quantitative DNA measurements. (E) Infarct region with cardiomyocytes (green) and CFs (magenta). Scale bar: 200 μm. Reprinted from Basara et al.81 CF: cardiac fibroblast; ECM: extracellular matrix; H&E: haematoxylin & eosin; iCM: induced pluripotent stem cell derived cardiomyocyte.
Figure 4. Hydrogel–based heart chips for cardiac organoids. (A) Flowchart for describing the main steps of the organoid–chip hydrogels. (B) Calcein AM and EthD–1 staining of cardiac organoids (20× original magnification). Scale bar: 400 μm. (C) Viability ratio of the organoids. Reprinted from Moshksayan et al.102 AM: Calcein AM; DOX: doxorubicin; EthD–1: ethidium homodimer–1.
Figure 5. Geometries of cardiac organoids. (A) The bioprinting setup. (B) A schematic showing the process of spheroid traversal across the yield–stress gel and media compartment. (C) A step–by–step illustration of the process. Scale bars: 1 mm. Reprinted from Ayan et al.114
Figure 6. Regulation of cardiac organoids in cardiac maturation and development. (A) Flow cytometry histogram from hiPSC–cardiomyocytes after differentiation. (B) Photo of a 7 mm × 7 mm hiPSC–cardiomyocyte–derived tissue patch (human “cardiopatch”). (C) Cross–sectional confocal image of 3–week–old cardiopatch demonstrating several layers of densely packed SAA+ hiPSC–cardiomyocytes (C1) surrounded by a layer of Vim+ fibroblasts (C2). Scale bars: 25 μm (B), 5 mm (C), 50 μm (C1, C2). (D) Representative images of ctrl (7 mm × 7 mm), Mega (15 mm × 15 mm) and Giga (36 mm × 36 mm) cardiopatches. Scale bar: 1 cm. (E, F) Representative confocal images of Giga cardiopatches stained for Cx43 and SAA, as seen in confocal cross–sections (E) or in the XY plane in the middle of the patch (F). Scale bars: 20 μm (E), 10 μm (F). (G) Representative activation maps of ctrl, Mega, and Giga cardiopatches following point stimulation from bottom right corner (pulse sign). Reprinted from Shadrin et al.138 ctrl: control; Cx43: connexin–43; DAPI: 4′,6–diamidino–2–phenylindole; hiPSC: human induced pluripotent stem cell; SAA: sarcomeric α–actinin; Vim: vimentin.
Figure 7. Cardiac organoids are used to regulate high–throughput drug screening for drug discovery and analysis. Created with BioRender.com. Functional cardiac organoids are further developed to explore the molecular mechanisms of drug screening. Drug screening in human PSC–cardiac organoids can identify pro–proliferative compounds.152 A high–throughput bioengineered human cardiac organoid platform has been fabricated to provide contractile cardiac tissue with biological properties similar to native heart tissues. Additionally, functional drug screening of 105 small molecules with pro–regenerative potential was performed. High–throughput proteomics in cardiac organoids can reveal synergistic stimuli of the mevalonate pathway and a cell–cycle network by pro–proliferative compounds. The assessment of doxorubicin toxicity is evaluated using human cardiac organoids for drug cardiotoxicity.153 Both traditional 2D monolayer cell models and 3D animal models have shown limitations and cannot fully mimic human heart physiology or pathology. A human cardiac organoid model promoting directed differentiation of human embryonic SCs is successfully created through 3D self–organised structures, capturing the biological characteristics and functions of heart tissue. This cardiac organoid model can recapitulate early myocardial development stages and accurately characterise the cardiotoxic damage caused by anticancer drug doxorubicin, including clinical cardiac injury and cardiac function indicators, cell apoptosis, inflammation and fibrosis. Cardiac organoid models are extensively used to evaluate drug cardiotoxicity, opening new avenues for drug screening and discovery.154
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