Advances in the construction of cardiac microtissues and its repair of infarcted hearts

doi:10.3877/cma.j.issn.2095-1221.2022.04.005

Abstract

Abstract:

Myocardial infarction (MI) and resulting heart failure (HF) are the leading causes of mortality worldwide. Current therapeutic approaches cannot compensate for irreversible loss of cardiomyocytes and damage of cardiocontractile myocardial that is hardly regenerated. Due to the integration of recent advances in stem cell biology, materials science, and engineering, cardiac microtissues (CMTs) provide a new direction and hope for cardiac regenerative medicine. This concise review summarized main research advances in the construction and application of CMTs for the repair of infarcted hearts, focusing on the construction strategy of CMTs, the transplantation approaches and effects in the promtion of cardial repair. The challenges for the translational applications of the CMTs in myocardial repair and regeneration were discussed too.

Key words: Myocardial infarction, Pluripotent stem cells, Cardiomyocytes, Microtissues

Minxia Ke, Huangtian Yang. Advances in the construction of cardiac microtissues and its repair of infarcted hearts[J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2022, 12(04): 224-229.

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References 67

1	Anderson JL, Morrow DA. Acute myocardial infarction[J]. N Engl J Med, 2017, 376(21):2053-2064.
2	Shah KS, Kittleson MM, Kobashigawa JA. Updates on heart transplantation[J]. Curr Heart Fail Rep, 2019, 16(5):150-156.
3	Frigerio M. Left ventricular assist device: indication, timing, and management[J]. Heart Fail Clin, 2021, 17(4):619-634.
4	Bolli R, Solankhi M, Tang XL, et al. Cell therapy in patients with heart failure: a comprehensive review and emerging concepts[J]. Cardiovasc Res, 2022, 118(4):951-976.
5	Zhu K, Wu Q, Ni C, et al. Lack of remuscularization following transplantation of human embryonic stem cell-derived cardiovascular progenitor cells in infarcted nonhuman primates[J]. Circ Res, 2018, 122(7):958-969.
6	Li Q, Wang J, Wu Q, et al. Perspective on human pluripotent stem cell-derived cardiomyocytes in heart disease modeling and repair[J]. Stem Cells Transl Med, 2020, 9(10):1121-1128.
7	Garbern JC, Lee RT. Heart regeneration: 20 years of progress and renewed optimism[J]. Dev Cell, 2022, 57(4):424-439.
8	Wu Q, Wang J, Tan WLW, et al. Extracellular vesicles from human embryonic stem cell-derived cardiovascular progenitor cells promote cardiac infarct healing through reducing cardiomyocyte death and promoting angiogenesis[J]. Cell Death Dis, 2020, 11(5):354.
9	Patino-Guerrero A, Veldhuizen J, Zhu W, et al. Three-dimensional scaffold-free microtissues engineered for cardiac repair[J]. J Mater Chem B, 2020, 8(34):7571-7590.
10	Boheler KR, Meli AC, Yang HT. Special issue on recent progress with hPSC-derived cardiovascular cells for organoids, engineered myocardium, drug discovery, disease models, and therapy[J]. Pflugers Arch, 2021, 473(7):983-988.
11	Bergmann O, Zdunek S, Felker A, et al. Dynamics of cell generation and turnover in the human heart[J]. Cell, 2015, 161(7):1566-1575.
12	Pinto AR, Ilinykh A, Ivey MJ, et al. Revisiting cardiac cellular composition[J]. Circ Res, 2016, 118(3):400-409.
13	Cao N, Liang H, Huang J, et al. Highly efficient induction and long-term maintenance of multipotent cardiovascular progenitors from human pluripotent stem cells under defined conditions[J]. Cell Res, 2013, 23(9):1119-1132.
14	Burridge PW, Matsa E, Shukla P, et al. Chemically defined generation of human cardiomyocytes[J]. Nat Methods, 2014, 11(8):855-860.
15	Patsch C, Challet-Meylan L, Thoma EC, et al. Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells[J]. Nat Cell Biol, 2015, 17(8):994-1003.
16	Bao X, Lian X, Qian T, et al. Directed differentiation and long-term maintenance of epicardial cells derived from human pluripotent stem cells under fully defined conditions[J]. Nat Protoc, 2017, 12(9):1890-1900.
17	Luo XL, Zhang P, Liu X, et al. Myosin light chain 2 marks differentiating ventricular cardiomyocytes derived from human embryonic stem cells[J]. Pflugers Arch, 2021, 473(7):991-1007.
18	Giacomelli E, Meraviglia V, Campostrini G, et al. Human-iPSC-derived cardiac stromal cells enhance maturation in 3D cardiac microtissues and reveal non-cardiomyocyte contributions to heart disease[J]. Cell Stem Cell, 2020, 26(6):862-879.e11.
19	Campostrini G, Meraviglia V, Giacomelli E, et al. Generation, functional analysis and applications of isogenic three-dimensional self-aggregating cardiac microtissues from human pluripotent stem cells[J]. Nat Protoc, 2021, 16(4):2213-2256.
20	Liu Y, Zhang Y, Mei T, et al. hESCs-derived early vascular cell spheroids for cardiac tissue vascular engineering and myocardial infarction treatment[J]. Adv Sci (Weinh), 2022, 9(9):e2104299. doi: 10.1002/advs.202104299.
21	Bargehr J, Ong LP, Colzani M, et al. Epicardial cells derived from human embryonic stem cells augment cardiomyocyte-driven heart regeneration[J]. Nat Biotechnol, 2019, 37(8):895-906.
22	Gao L, Gregorich ZR, Zhu W, et al. Large cardiac muscle patches engineered from human induced-pluripotent stem cell-derived cardiac cells improve recovery from myocardial infarction in swine[J]. Circulation, 2018, 137(16):1712-1730.
23	Cho S, Lee C, Skylar-Scott MA, et al. Reconstructing the heart using iPSCs: engineering strategies and applications[J]. J Mol Cell Cardiol, 2021, 157:56-65.
24	Wendel JS, Ye L, Tao R, et al. Functional effects of a tissue-engineered cardiac patch from human induced pluripotent stem cell-derived cardiomyocytes in a rat infarct model[J]. Stem Cells Transl Med, 2015, 4(11):1324-1332.
25	Querdel E, Reinsch M, Castro L, et al. Human engineered heart tissue patches remuscularize the injured heart in a dose-dependent manner[J]. Circulation, 2021, 143(20):1991-2006.
26	Kaiser NJ, Kant RJ, Minor AJ, et al. Optimizing blended collagen-fibrin hydrogels for cardiac tissue engineering with human iPSC-derived cardiomyocytes[J]. ACS Biomater Sci Eng, 2019, 5(2):887-899.
27	Riegler J, Tiburcy M, Ebert A, et al. Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model[J]. Circ Res, 2015, 117(8):720-730.
28	Qin X, Riegler J, Tiburcy M, et al. Magnetic resonance imaging of cardiac strain pattern following transplantation of human tissue engineered heart muscles[J]. Circ Cardiovasc Imaging, 2016, 9(11):e004731. doi: 10.1161/CIRCIMAGING.116.004731.
29	Tsui JH, Ostrovsky-Snider NA, Yama DMP, et al. Conductive silk-polypyrrole composite scaffolds with bioinspirednanotopographic cues for cardiac tissue engineering[J]. J Mater Chem B, 2018, 6(44):7185-7196.
30	Liang Y, Mitriashkin A, Lim TT, et al. Conductive polypyrrole-encapsulated silk fibroin fibers for cardiac tissue engineering[J]. Biomaterials, 2021, 276:121008. doi: 10.1016/j.biomaterials.2021.121008.
31	Bouhrira N, Galie PA, Janmey PA. Hyaluronan disrupts cardiomyocyte organization within 3D fibrin-based hydrogels[J]. Biophys J, 2019, 116(7):1340-1347.
32	Saporito F, Sandri G, Bonferoni MC, et al. Electrospun gelatin(-)chondroitin sulfate scaffolds loaded with platelet lysate promote immature cardiomyocyte proliferation[J]. Polymers (Basel), 2018, 10(2):208. doi: 10.3390/polym10020208.
33	Chu X, Wang M, Qiu X, et al. Strategies for constructing pluripotent stem cell- and progenitor cell-derived three-dimensional cardiac micro-tissues[J]. J Biomed Mater Res A, 2022, 110(2):488-503.
34	Maiullari F, Costantini M, Milan M, et al. A multi-cellular 3D bioprinting approach for vascularized heart tissue engineering based on HUVECs and iPSC-derived cardiomyocytes[J]. Sci Rep, 2018, 8(1):13532. doi: 10.1038/s41598-018-31848-x.
35	Chen Y, Wang J, Shen B, et al. Engineering a freestanding biomimetic cardiac patch using biodegradable poly (lactic-co-glycolic acid) (PLGA) and human embryonic stem cell-derived ventricular cardiomyocytes (hESC-VCMs)[J]. Macromol Biosci, 2015, 15(3):426-436.
36	Brazhkina O, Park JH, Park HJ, et al. Designing a 3D printing based auxetic cardiac patch with hiPSC-CMs for heart repair[J]. J Cardiovasc Dev Dis, 2021, 8(12):172. doi: 10.3390/jcdd8120172.
37	Wu Y, Wang L, Guo B, et al. Interwoven aligned conductive nanofiber yarn/hydrogel composite scaffolds for engineered 3D cardiac anisotropy[J]. ACS Nano, 2017, 11(6):5646-5659.
38	Tan Y, Richards D, Xu R, et al. Silicon nanowire-induced maturation of cardiomyocytes derived from human induced pluripotent stem cells[J]. Nano Lett, 2015, 15(5):2765-2772.
39	Richards DJ, Tan Y, Coyle R, et al. Nanowires and electrical stimulation synergistically improve functions of hiPSC cardiac spheroids[J]. Nano Lett, 2016, 16(7):4670-4678.
40	Baei P, Hosseini M, Baharvand H, et al. Electrically conductive materials for in vitro cardiac microtissue engineering[J]. J Biomed Mater Res A, 2020, 108(5):1203-1213.
41	Campostrini G, Windt LM, van Meer BJ, et al. Cardiac tissues from stem cells: new routes to maturation and cardiac regeneration[J]. Circ Res, 2021, 128(6):775-801.
42	Yu D, Wang X, Ye L. Cardiac tissue engineering for the treatment of myocardial infarction[J]. J Cardiovasc Dev Dis, 2021, 8(11):153. doi: 10.3390/jcdd8110153.
43	Majid QA, Fricker ATR, Gregory DA, et al. Natural biomaterials for cardiac tissue engineering: a highly biocompatible solution[J]. Front Cardiovasc Med, 2020, 7:554597. doi: 10.3389/fcvm.2020.554597.
44	Sharma V, Dash SK, Govarthanan K, et al. Recent advances in cardiac tissue engineering for the management of myocardium infarction[J]. Cells, 2021, 10(10):2538. doi: 10.3390/cells10102538.
45	Esmaeili H, Patino-Guerrero A, Hasany M, et al. Electroconductive biomaterials for cardiac tissue engineering[J]. Acta Biomater, 2022, 139:118-140.
46	Li J, Hu S, Zhu D, et al. All roads lead to rome (the heart): cell retention and outcomes from various delivery routes of cell therapy products to the heart[J]. J Am Heart Assoc, 2021, 10(8):e020402. doi: 10.1161/JAHA.120.020402.
47	Tabei R, Kawaguchi S, Kanazawa H, et al. Development of a transplant injection device for optimal distribution and retention of human induced pluripotent stem cellderivedcardiomyocytes[J]. J Heart Lung Transplant, 2019, 38(2):203-214.
48	Kawaguchi S, Soma Y, Nakajima K, et al. Intramyocardial transplantation of human iPS cell-derived cardiac spheroids improves cardiac function in heart failure animals[J]. JACC Basic Transl Sci, 2021, 6(3):239-254.
49	Sahito RGA, Sheng X, Maass M, et al. In vitro grown micro-tissues for cardiac cell replacement therapy in vivo[J]. Cell Physiol Biochem, 2019, 52(6):1309-1324.
50	Mitsutake Y, Pyun WB, Rouy D, et al. Improvement of local cell delivery using helix transendocardial delivery catheter in a porcine heart[J]. Int Heart J, 2017, 58(3):435-440.
51	Miyagawa S, Kainuma S, Kawamura T, et al. Transplantation of iPSC-derived cardiomyocyte patches for ischemic cardiomyopathy[J]. med Rxiv, 2022:21268295. DOI:10.1101/2021.12.27.21268295
52	Weinberger F, Breckwoldt K, Pecha S, et al. Cardiac repair in guinea pigs with human engineered heart tissue from induced pluripotent stem cells[J]. Sci Transl Med, 2016, 8(363):363ra148. doi: 10.1126/scitranslmed.aaf8781.
53	Gao L, Kupfer ME, Jung JP, et al. Myocardial tissue engineering with cells derived from human-induced pluripotent stem cells and a native-like, high-resolution, 3-dimensionally printed scaffold[J]. Circ Res, 2017, 120(8):1318-1325.
54	Munarin F, Kant RJ, Rupert CE, et al. Engineered human myocardium with local release of angiogenic proteins improves vascularization and cardiac function in injured rat hearts[J]. Biomaterials, 2020, 251:120033. doi: 10.1016/j.biomaterials.2020.120033.
55	Ye L, Chang YH, Xiong Q, et al. Cardiac repair in a porcine model of acute myocardial infarction with human induced pluripotent stem cell-derived cardiovascular cells[J]. Cell Stem Cell, 2014, 15(6):750-761.
56	Li J, Minami I, Shiozaki M, et al. Human pluripotent stem cell-derived cardiac tissue-like constructs for repairing the infarcted myocardium[J]. Stem Cell Reports, 2017, 9(5):1546-1559.
57	Noor N, Shapira A, Edri R, et al. 3D printing of personalized thick and perfusable cardiac patches and hearts[J]. Adv Sci (Weinh), 2019, 6(11):1900344. doi: 10.1002/advs.201900344.
58	van der Meer AD, Orlova VV, ten Dijke P, et al. Three-dimensional co-cultures of human endothelial cells and embryonic stem cell-derived pericytes inside a microfluidic device[J]. Lab Chip, 2013, 13(18):3562-3568.
59	Shen MJ. The cardiac autonomic nervous system: an introduction[J]. Herzschrittmacherther Elektrophysiol, 2021, 32(3):295-301.
60	Nicolas-Avila JA, Lechuga-Vieco AV, Esteban-Martinez L, et al. A network of macrophages supports mitochondrial homeostasis in the heart[J]. Cell, 2020, 183(1):94-109.e23.
61	Hulsmans M, Clauss S, Xiao L, et al. Macrophages facilitate electrical conduction in the heart[J]. Cell, 2017, 169(3):510-522.e20.
62	Li Y, Feng J, Song S, et al. gp130 controls cardiomyocyte proliferation and heart regeneration[J]. Circulation, 2020, 142(10):967-982.
63	Rusinkevich V, Huang Y, Chen ZY, et al. Temporal dynamics of immune response following prolonged myocardial ischemia/reperfusion with and without cyclosporine A[J]. ActaPharmacol Sin, 2019, 40(9):1168-1183.
64	Deuse T, Hu X, Gravina A, et al. Hypoimmunogenic derivatives of induced pluripotent stem cells evade immune rejection in fully immunocompetent allogeneic recipients[J]. Nat Biotechnol, 2019, 37(3):252-258.
65	Deuse T, Tediashvili G, Hu X, et al. Hypoimmune induced pluripotent stem cell-derived cell therapeutics treat cardiovascular and pulmonary diseases in immunocompetent allogeneic mice[J]. Proc Natl Acad Sci U S A, 2021, 118(28):e2022091118. doi: 10.1073/pnas.2022091118.
66	Buikema JW, Lee S, Goodyer WR, et al. Wnt activation and reduced cell-cell contact synergistically induce massive expansion of functional human iPSC-derived cardiomyocytes[J]. Cell Stem Cell, 2020, 27(1):50-63.e55.
67	Finklea FB, Tian Y, Kerscher P, et al. Engineered cardiac tissue microsphere production through direct differentiation of hydrogel-encapsulated human pluripotent stem cells[J]. Biomaterials, 2021, 274:120818. doi: 10.1016/j.biomaterials.2021.120818.

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