Regeneration of the heart: from molecular mechanisms to clinical therapeutics
Regeneration of the heart: from molecular mechanisms to clinical therapeutics
- MMR 2024年11卷第1期 页码：80-97
- Affiliations：
Beijing Key Laboratory of Precision Medicine of Coronary Atherosclerotic Disease, Beijing Institute of Heart Lung and Blood Vessel Disease, Clinical Center for Coronary Heart Disease, Department of Cardiology, Beijing Anzhen Hospital, Capital Medical University, Beijing 100029, China
- Author bio：
* azzyj12@163.com
- Funds：This work was supported by the Natural Science Foundation of Beijing, China(7214223;7212027);the Beijing Hospitals Authority Youth Programme(QML20210601);the Chinese Scholarship Council (CSC) scholarship(201706210415);the National Key Research and Development Program of China(2017YFC0908800);the Beijing Municipal Health Commission(PXM2020_026272_000002;PXM2020_026272_000014);the National Natural Science Foundation of China(82070293)
DOI：10.1186/s40779-023-00452-0
中图分类号：-
纸质出版：2024-02
- Accepted：
Scan QR Code
Regeneration of the heart: from molecular mechanisms to clinical therapeutics[J]. MMR, 2024,11(1):80-97.
Cite this article as: Guo QY, Yang JQ, Feng XX, Zhou YJ. Regeneration of the heart: from molecular mechanisms to clinical therapeutics. Mil Med Res. 2023;10(1):18.
Regeneration of the heart: from molecular mechanisms to clinical therapeutics[J]. MMR, 2024,11(1):80-97. DOI： 10.1186/s40779-023-00452-0.
Cite this article as: Guo QY, Yang JQ, Feng XX, Zhou YJ. Regeneration of the heart: from molecular mechanisms to clinical therapeutics. Mil Med Res. 2023;10(1):18. DOI： 10.1186/s40779-023-00452-0.
摘要
Abstract
Heart injury such as myocardial infarction leads to cardiomyocyte loss
fibrotic tissue deposition
and scar formation. These changes reduce cardiac contractility
resulting in heart failure
which causes a huge public health burden. Military personnel
compared with civilians
is exposed to more stress
a risk factor for heart diseases
making cardiovascular health management and treatment innovation an important topic for military medicine. So far
medical intervention can slow down cardiovascular disease progression
but not yet induce heart regeneration. In the past decades
studies have focused on mechanisms underlying the regenerative capability of the heart and applicable approaches to reverse heart injury. Insights have emerged from studies in animal models and early clinical trials. Clinical interventions show the potential to reduce scar formation and enhance cardiomyocyte proliferation that counteracts the pathogenesis of heart disease. In this review
we discuss the signaling events controlling the regeneration of heart tissue and summarize current therapeutic approaches to promote heart regeneration after injury.
关键词
Keywords
references
Zhang Y , Lin C , Liu M , Zhang W , Xun X , Wu J , et al . Burden and trend of cardiovascular diseases among people under 20 years in China, Western Pacific region, and the world: an analysis of the global burden of disease study in 2019 . Front Cardiovasc Med . 2023 ; 10 : 1067072 .
Virani SS , Alonso A , Aparicio HJ , Benjamin EJ , Bittencourt MS , Callaway CW , et al . Heart disease and stroke statistics-2021 update: a report from the American Heart Association . Circulation . 2021 ; 143 ( 8 ): e254 – 743 .
Pflanz S , Sonnek S . Work stress in the military: prevalence, causes, and relationship to emotional health . Mil Med . 2002 ; 167 ( 11 ): 877 – 82 .
Bustamante-Sánchez Á , Tornero-Aguilera JF , Fernández-Elías VE , Hormeño-Holgado AJ , Dalamitros AA , Clemente-Suárez VJ . Effect of stress on autonomic and cardiovascular systems in military population: a systematic review . Cardiol Res Pract . 2020 ; 2020 : 7986249 .
Steptoe A , Kivimäki M . Stress and cardiovascular disease . Nat Rev Cardiol . 2012 ; 9 ( 6 ): 360 – 70 .
Grósz A , Tóth E , Péter I . A 10-year follow-up of ischemic heart disease risk factors in military pilots . Mil Med . 2007 ; 172 ( 2 ): 214 – 9 .
Heidenreich PA , Sahay A , Kapoor JR , Pham MX , Massie B . Divergent trends in survival and readmission following a hospitalization for heart failure in the Veterans Affairs health care system 2002 to 2006 . J Am Coll Cardiol . 2010 ; 56 ( 5 ): 362 – 8 .
Mamas MA , Sperrin M , Watson MC , Coutts A , Wilde K , Burton C , et al . Do patients have worse outcomes in heart failure than in cancer? A primary care-based cohort study with 10-year follow-up in Scotland . Eur J Heart Fail . 2017 ; 19 ( 9 ): 1095 – 104 .
Benjamin EJ , Blaha MJ , Chiuve SE , Cushman M , Das SR , Deo R , et al . Heart disease and stroke statistics-2017 update: a report from the American Heart Association . Circulation . 2017 ; 135 ( 10 ): e146 – 603 .
Lawson CA , Zaccardi F , Squire I , Ling S , Davies MJ , Lam CSP , et al . 20-year trends in cause-specific heart failure outcomes by sex, socioeconomic status, and place of diagnosis: a population-based study . Lancet Public Health . 2019 ; 4 ( 8 ): e406 – 20 .
Bergmann O , Bhardwaj RD , Bernard S , Zdunek S , Barnabé-Heider F , Walsh S , et al . Evidence for cardiomyocyte renewal in humans . Science . 2009 ; 324 ( 5923 ): 98 – 102 .
Tenreiro MF , Louro AF , Alves PM , Serra M . Next generation of heart regenerative therapies: progress and promise of cardiac tissue engineering . NPJ Regen Med . 2021 ; 6 ( 1 ): 30 .
Curfman G . Stem cell therapy for heart failure: an unfulfilled promise? . JAMA . 2019 ; 321 ( 12 ): 1186 – 7 .
Zhang J , Bolli R , Garry DJ , Marbán E , Menasché P , Zimmermann WH , et al . Basic and translational research in cardiac repair and regeneration: JACC state-of-the-art review . J Am Coll Cardiol . 2021 ; 78 ( 21 ): 2092 – 105 .
Plackett B . Cells or drugs? The race to regenerate the heart . Nature . 2021 ; 594 ( 7862 ): S16 – 7 .
Tehzeeb J , Manzoor A , Ahmed MM . Is stem cell therapy an answer to heart failure: a literature search . Cureus . 2019 ; 11 ( 10 ): e5959 .
Poss KD , Wilson LG , Keating MT . Heart regeneration in zebrafish . Science . 2002 ; 298 ( 5601 ): 2188 – 90 .
Raya A , Koth CM , Büscher D , Kawakami Y , Itoh T , Raya RM , et al . Activation of Notch signaling pathway precedes heart regeneration in zebrafish . Proc Natl Acad Sci U S A . 2003 ; 100 Suppl 1 ( Suppl 1 ): 11889 – 95 .
Münch J , Grivas D , González-Rajal Á , Torregrosa-Carrión R , de la Pompa JL . Notch signalling restricts inflammation and serpine1 expression in the dynamic endocardium of the regenerating zebrafish heart . Development . 2017 ; 144 ( 8 ): 1425 – 40 .
Zhao L , Ben-Yair R , Burns CE , Burns CG . Endocardial Notch signaling promotes cardiomyocyte proliferation in the regenerating zebrafish heart through Wnt pathway antagonism . Cell Rep . 2019 ; 26 ( 3 ): 546 - 54.e5 .
Wang J , Karra R , Dickson AL , Poss KD . Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration . Dev Biol . 2013 ; 382 ( 2 ): 427 – 35 .
Kikuchi K , Holdway JE , Major RJ , Blum N , Dahn RD , Begemann G , et al . Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration . Dev Cell . 2011 ; 20 ( 3 ): 397 – 404 .
Bednarek D , González-Rosa JM , Guzmán-Martínez G , Gutiérrez-Gutiérrez Ó , Aguado T , Sánchez-Ferrer C , et al . Telomerase is essential for zebrafish heart regeneration . Cell Rep . 2015 ; 12 ( 10 ): 1691 – 703 .
Gemberling M , Karra R , Dickson AL , Poss KD . Nrg1 is an injury-induced cardiomyocyte mitogen for the endogenous heart regeneration program in zebrafish . Elife . 2015 ; 4 : e05871 .
Zhao L , Borikova AL , Ben-Yair R , Guner-Ataman B , Macrae CA , Lee RT , et al . Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration . Proc Natl Acad Sci USA . 2014 ; 111 ( 4 ): 1403 – 8 .
Pfefferli C , Jaźwińska A . The careg element reveals a common regulation of regeneration in the zebrafish myocardium and fin . Nat Commun . 2017 ; 8 : 15151 .
Gupta V , Poss KD . Clonally dominant cardiomyocytes direct heart morphogenesis . Nature . 2012 ; 484 ( 7395 ): 479 – 84 .
Cui M , Atmanli A , Morales MG , Tan W , Chen K , Xiao X , et al . Nrf1 promotes heart regeneration and repair by regulating proteostasis and redox balance . Nat Commun . 2021 ; 12 ( 1 ): 5270 .
Kachanova O , Lobov A , Malashicheva A . The role of the Notch signaling pathway in recovery of cardiac function after myocardial infarction . Int J Mol Sci . 2022 ; 23 ( 20 ): 12509 .
Ma J , Gu Y , Liu J , Song J , Zhou T , Jiang M , et al . Functional screening of congenital heart disease risk loci identifies 5 genes essential for heart development in zebrafish . Cell Mol Life Sci . 2022 ; 80 ( 1 ): 19 .
Heallen T , Morikawa Y , Leach J , Tao G , Willerson JT , Johnson RL , et al . Hippo signaling impedes adult heart regeneration . Development . 2013 ; 140 ( 23 ): 4683 – 90 .
Leach JP , Heallen T , Zhang M , Rahmani M , Morikawa Y , Hill MC , et al . Hippo pathway deficiency reverses systolic heart failure after infarction . Nature . 2017 ; 550 ( 7675 ): 260 – 4 .
Aharonov A , Shakked A , Umansky KB , Savidor A , Genzelinakh A , Kain D , et al . ERBB2 drives YAP activation and EMT-like processes during cardiac regeneration . Nat Cell Biol . 2020 ; 22 ( 11 ): 1346 – 56 .
Fernández-Ruiz I . ERBB2-YAP crosstalk mediates cardiac regeneration in mice . Nat Rev Cardiol . 2021 ; 18 ( 1 ): 4 .
Xin M , Kim Y , Sutherland LB , Murakami M , Qi X , Mcanally J , et al . Hippo pathway effector Yap promotes cardiac regeneration . Proc Natl Acad Sci U S A . 2013 ; 110 ( 34 ): 13839 – 44 .
Lin Z , von Gise A , Zhou P , Gu F , Ma Q , Jiang J , et al . Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model . Circ Res . 2014 ; 115 ( 3 ): 354 – 63 .
Eulalio A , Mano M , Dal Ferro M , Zentilin L , Sinagra G , Zacchigna S , et al . Functional screening identifies miRNAs inducing cardiac regeneration . Nature . 2012 ; 492 ( 7429 ): 376 – 81 .
Lesizza P , Prosdocimo G , Martinelli V , Sinagra G , Zacchigna S , Giacca M . Single-dose intracardiac injection of pro-regenerative microRNAs improves cardiac function after myocardial infarction . Circ Res . 2017 ; 120 ( 8 ): 1298 – 304 .
Gabisonia K , Prosdocimo G , Aquaro GD , Carlucci L , Zentilin L , Secco I , et al . MicroRNA therapy stimulates uncontrolled cardiac repair after myocardial infarction in pigs . Nature . 2019 ; 569 ( 7756 ): 418 – 22 .
Tao Y , Zhang H , Huang S , Pei L , Feng M , Zhao X , et al . miR-199a-3p promotes cardiomyocyte proliferation by inhibiting Cd151 expression . Biochem Biophys Res Commun . 2019 ; 516 ( 1 ): 28 – 36 .
Li Z , Song Y , Liu L , Hou N , An X , Zhan D , et al . miR-199a impairs autophagy and induces cardiac hypertrophy through mTOR activation . Cell Death Differ . 2017 ; 24 ( 7 ): 1205 – 13 .
Hashemi Gheinani A , Burkhard FC , Rehrauer H , Aquino Fournier C , Monastyrskaya K . microRNA miR-199a-5p regulates smooth muscle cell proliferation and morphology by targeting WNT2 signaling pathway . J Biol Chem . 2015 ; 290 ( 11 ): 7067 – 86 .
Huang W , Feng Y , Liang J , Yu H , Wang C , Wang B , et al . Loss of micro-RNA-128 promotes cardiomyocyte proliferation and heart regeneration . Nat Commun . 2018 ; 9 ( 1 ): 700 .
Porrello ER , Mahmoud AI , Simpson E , Johnson BA , Grinsfelder D , Canseco D , et al . Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family . Proc Natl Acad Sci U S A . 2013 ; 110 ( 1 ): 187 – 92 .
Valussi M , Besser J , Wystub-Lis K , Zukunft S , Richter M , Kubin T , et al . Repression of Osmr and Fgfr1 by miR-1/133a prevents cardiomyocyte dedifferentiation and cell cycle entry in the adult heart . Sci Adv . 2021 ; 7 ( 42 ): eabi6648 .
Huang S , Li X , Zheng H , Si X , Li B , Wei G , et al . Loss of super-enhancerregulated circRNA Nfix induces cardiac regeneration after myocardial infarction in adult mice . Circulation . 2019 ; 139 ( 25 ): 2857 – 76 .
Wang X , Ha T , Liu L , Hu Y , Kao R , Kalbfleisch J , et al . TLR3 mediates repair and regeneration of damaged neonatal heart through glycolysis dependent YAP1 regulated miR-152 expression . Cell Death Differ . 2018 ; 25 ( 5 ): 966 – 82 .
Yang YS , Liu MH , Yan ZW , Chen GQ , Huang Y . FAM122A is required for mesendodermal and cardiac differentiation of embryonic stem cells . Stem cells . 2023 ; sxad008 . https://doi.org/10.1093/stmcls/sxad008 https://doi.org/10.1093/stmcls/sxad008 .
Rigaud VOC , Hoy RC , Kurian J , Zarka C , Behanan M , Brosious I , et al . RNAbinding protein LIN28a regulates new myocyte formation in the heart through long noncoding RNA-H19 . Circulation . 2023 ; 147 ( 4 ): 324 – 37 .
Ye Z , Su Z , Xie S , Liu Y , Wang Y , Xu X , et al . Yap-lin28a axis targets let7-Wnt pathway to restore progenitors for initiating regeneration . Elife . 2020 ; 9 : e55771 .
Gamba L , Amin-Javaheri A , Kim J , Warburton D , Lien CL . Collagenolytic activity is associated with scar resolution in zebrafish hearts after cryoinjury . J Cardiovasc Dev Dis . 2017 ; 4 ( 1 ): 2 .
Beauchemin M , Smith A , Yin VP . Dynamic microRNA-101a and Fosab expression controls zebrafish heart regeneration . Development . 2015 ; 142 ( 23 ): 4026 – 37 .
Flinn MA , Jeffery BE , O’Meara CC , Link BA . Yap is required for scar formation but not myocyte proliferation during heart regeneration in zebrafish . Cardiovasc Res . 2019 ; 115 ( 3 ): 570 – 7 .
Simões FC , Cahill TJ , Kenyon A , Gavriouchkina D , Vieira JM , Sun X , et al . Macrophages directly contribute collagen to scar formation during zebrafish heart regeneration and mouse heart repair . Nat Commun . 2020 ; 11 ( 1 ): 600 .
Chablais F , Veit J , Rainer G , Jaźwińska A . The zebrafish heart regenerates after cryoinjury-induced myocardial infarction . BMC Dev Biol . 2011 ; 11 : 21 .
González-Rosa JM , Martín V , Peralta M , Torres M , Mercader N . Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish . Development . 2011 ; 138 ( 9 ): 1663 – 74 .
Bersell K , Arab S , Haring B , Kühn B . Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury . Cell . 2009 ; 138 ( 2 ): 257 – 70 .
D’Uva G , Aharonov A , Lauriola M , Kain D , Yahalom-Ronen Y , Carvalho S , et al . ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation . Nat Cell Biol . 2015 ; 17 ( 5 ): 627 – 38 .
de Preux Charles AS , Bise T , Baier F , Marro J , Jaźwińska A . Distinct effects of inflammation on preconditioning and regeneration of the adult zebrafish heart . Open Biol . 2016 ; 6 ( 7 ): 160102 .
Fang Y , Gupta V , Karra R , Holdway JE , Kikuchi K , Poss KD . Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration . Proc Natl Acad Sci U S A . 2013 ; 110 ( 33 ): 13416 – 21 .
Wen X , Jiao L , Tan H . MAPK/ERK pathway as a central regulator in vertebrate organ regeneration . Int J Mol Sci . 2022 ; 23 ( 3 ): 1464 .
Zhang D , Ning J , Ramprasath T , Yu C , Zheng X , Song P , et al . Kynurenine promotes neonatal heart regeneration by stimulating cardiomyocyte proliferation and cardiac angiogenesis . Nat Commun . 2022 ; 13 ( 1 ): 6371 .
Missinato MA , Saydmohammed M , Zuppo DA , Rao KS , Opie GW , Kühn B , et al . Dusp6 attenuates Ras/MAPK signaling to limit zebrafish heart regeneration . Development . 2018 ; 145 ( 5 ): dev157206 .
Zhou X , Zhang C , Wu X , Hu X , Zhang Y , Wang X , et al . Dusp6 deficiency attenuates neutrophil-mediated cardiac damage in the acute inflammatory phase of myocardial infarction . Nat Commun . 2022 ; 13 ( 1 ): 6672 .
Zhang Z , Chen Y , Zheng L , Du J , Wei S , Zhu X , et al . A DUSP6 inhibitor suppresses inflammatory cardiac remodeling and improves heart function after myocardial infarction . Dis Model Mech . 2023 ; 16 ( 5 ): dmm049662 .
Belviso I , Sacco AM , Cozzolino D , Nurzynska D , Di Meglio F , Castaldo C , et al . Cardiac-derived extracellular matrix: a decellularization protocol for heart regeneration . PLoS ONE . 2022 ; 17 ( 10 ): e0276224 .
Han L , Mich-Basso JD , Li Y , Ammanamanchi N , Xu J , Bargaje AP , et al . Changes in nuclear pore numbers control nuclear import and stress response of mouse hearts . Dev Cell . 2022 ; 57 ( 20 ): 2397 - 411.e9 .
Sogo T , Nakao S , Tsukamoto T , Ueyama T , Harada Y , Ihara D , et al . Canonical Wnt signaling activation by chimeric antigen receptors for efficient cardiac differentiation from mouse embryonic stem cells . Inflamm Regen . 2023 ; 43 ( 1 ): 11 .
Senyo SE , Steinhauser ML , Pizzimenti CL , Yang VK , Cai L , Wang M , et al . Mammalian heart renewal by pre-existing cardiomyocytes . Nature . 2013 ; 493 ( 7432 ): 433 – 6 .
Kimura W , Xiao F , Canseco DC , Muralidhar S , Thet S , Zhang HM , et al . Hypoxia fate mapping identifies cycling cardiomyocytes in the adult heart . Nature . 2015 ; 523 ( 7559 ): 226 – 30 .
Porrello ER , Mahmoud AI , Simpson E , Hill JA , Richardson JA , Olson EN , et al . Transient regenerative potential of the neonatal mouse heart . Science . 2011 ; 331 ( 6020 ): 1078 – 80 .
Orlic D , Kajstura J , Chimenti S , Jakoniuk I , Anderson SM , Li B , et al . Bone marrow cells regenerate infarcted myocardium . Nature . 2001 ; 410 ( 6829 ): 701 – 5 .
van Berlo JH , Kanisicak O , Maillet M , Vagnozzi RJ , Karch J , Lin SC , et al . C-kit + cells minimally contribute cardiomyocytes to the heart . Nature . 2014 ; 509 ( 7500 ): 337 – 41 .
Li J , Yang KY , Tam RCY , Chan VW , Lan HY , Hori S , et al . Regulatory T-cells regulate neonatal heart regeneration by potentiating cardiomyocyte proliferation in a paracrine manner . Theranostics . 2019 ; 9 ( 15 ): 4324 – 41 .
Li J , Liang C , Yang KY , Huang X , Han MY , Li X , et al . Specific ablation of CD4 + T-cells promotes heart regeneration in juvenile mice . Theranostics . 2020 ; 10 ( 18 ): 8018 – 35 .
Das S , Goldstone AB , Wang H , Farry J , D’Amato G , Paulsen MJ , et al . A unique collateral artery development program promotes neonatal heart regeneration . Cell . 2019 ; 176 ( 5 ): 1128 - 42.e18 .
Marín-Juez R , El-Sammak H , Helker CSM , Kamezaki A , Mullapuli ST , Bibli SI , et al . Coronary revascularization during heart regeneration is regulated by epicardial and endocardial cues and forms a scaffold for cardiomyocyte repopulation . Dev Cell . 2019 ; 51 ( 4 ): 503 - 15.e4 .
Marín-Juez R , Marass M , Gauvrit S , Rossi A , Lai SL , Materna SC , et al . Fast revascularization of the injured area is essential to support zebrafish heart regeneration . Proc Natl Acad Sci U S A . 2016 ; 113 ( 40 ): 11237 – 42 .
Wang L , Yu P , Zhou B , Song J , Li Z , Zhang M , et al . Single-cell reconstruction of the adult human heart during heart failure and recovery reveals the cellular landscape underlying cardiac function . Nat Cell Biol . 2020 ; 22 ( 1 ): 108 – 19 .
Jonsson MKB , Hartman RJG , Ackers-Johnson M , Tan WLW , Lim B , Van Veen TaB , et al . A transcriptomic and epigenomic comparison of fetal and adult human cardiac fibroblasts reveals novel key transcription factors in adult cardiac fibroblasts . JACC Basic Transl Sci . 2016 ; 1 ( 7 ): 590 – 602 .
Kaur H , Takefuji M , Ngai CY , Carvalho J , Bayer J , Wietelmann A , et al . Targeted ablation of periostin-expressing activated fibroblasts prevents adverse cardiac remodeling in mice . Circ Res . 2016 ; 118 ( 12 ): 1906 – 17 .
Sánchez-Iranzo H , Galardi-Castilla M , Sanz-Morejón A , González-Rosa JM , Costa R , Ernst A , et al . Transient fibrosis resolves via fibroblast inactivation in the regenerating zebrafish heart . Proc Natl Acad Sci U S A . 2018 ; 115 ( 16 ): 4188 – 93 .
Yuan P , Cheedipudi SM , Rouhi L , Fan S , Simon L , Zhao Z , et al . Single-cell RNA sequencing uncovers paracrine functions of the epicardial-derived cells in arrhythmogenic cardiomyopathy . Circulation . 2021 ; 143 ( 22 ): 2169 – 87 .
Xia H , Li X , Gao W , Fu X , Fang RH , Zhang L , et al . Tissue repair and regeneration with endogenous stem cells . Nat Rev Mater . 2018 ; 3 ( 7 ): 174 – 93 .
Bergmann O , Zdunek S , Felker A , Salehpour M , Alkass K , Bernard S , et al . Dynamics of cell generation and turnover in the human heart . Cell . 2015 ; 161 ( 7 ): 1566 – 75 .
Haubner BJ , Schneider J , Schweigmann U , Schuetz T , Dichtl W , Velik-Salchner C , et al . Functional recovery of a human neonatal heart after severe myocardial infarction . Circ Res . 2016 ; 118 ( 2 ): 216 – 21 .
Cesna S , Eicken A , Juenger H , Hess J . Successful treatment of a newborn with acute myocardial infarction on the first day of life . Pediatr Cardiol . 2013 ; 34 ( 8 ): 1868 – 70 .
Deutsch MA , Cleuziou J , Noebauer C , Eicken A , Vogt M , Hoerer J , et al . Successful management of neonatal myocardial infarction with ECMO and intracoronary r-tPA lysis . Congenit Heart Dis . 2014 ; 9 ( 5 ): E169 – 74 .
Farooqi KM , Sutton N , Weinstein S , Menegus M , Spindola-Franco H , Pass RH . Neonatal myocardial infarction: case report and review of the literature . Congenit Heart Dis . 2012 ; 7 ( 6 ): E97 – 102 .
Drenckhahn JD , Schwarz QP , Gray S , Laskowski A , Kiriazis H , Ming Z , et al . Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development . Dev Cell . 2008 ; 15 ( 4 ): 521 – 33 .
Darehzereshki A , Rubin N , Gamba L , Kim J , Fraser J , Huang Y , et al . Differential regenerative capacity of neonatal mouse hearts after cryoinjury . Dev Biol . 2015 ; 399 ( 1 ): 91 – 9 .
Haubner BJ , Adamowicz-Brice M , Khadayate S , Tiefenthaler V , Metzler B , Aitman T , et al . Complete cardiac regeneration in a mouse model of myocardial infarction . Aging . 2012 ; 4 ( 12 ): 966 – 77 .
Bryant DM , O’Meara CC , Ho NN , Gannon J , Cai L , Lee RT . A systematic analysis of neonatal mouse heart regeneration after apical resection . J Mol Cell Cardiol . 2015 ; 79 : 315 – 8 .
Konfino T , Landa N , Ben-Mordechai T , Leor J . The type of injury dictates the mode of repair in neonatal and adult heart . J Am Heart Assoc . 2015 ; 4 ( 1 ): e001320 .
González-Rosa JM , Burns CE , Burns CG . Zebrafish heart regeneration: 15 years of discoveries . Regeneration (Oxf) . 2017 ; 4 ( 3 ): 105 – 23 .
Wang J , Panáková D , Kikuchi K , Holdway JE , Gemberling M , Burris JS , et al . The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion . Development . 2011 ; 138 ( 16 ): 3421 – 30 .
Schultheiss HP , Fairweather D , Caforio ALP , Escher F , Hershberger RE , Lipshultz SE , et al . Dilated cardiomyopathy . Nat Rev Dis Primers . 2019 ; 5 ( 1 ): 32 .
Cao J , Poss KD . The epicardium as a hub for heart regeneration . Nat Rev Cardiol . 2018 ; 15 ( 10 ): 631 – 47 .
Schächinger V , Erbs S , Elsässer A , Haberbosch W , Hambrecht R , Hölschermann H , et al . Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction . N Engl J Med . 2006 ; 355 ( 12 ): 1210 – 21 .
Perin EC , Willerson JT , Pepine CJ , Henry TD , Ellis SG , Zhao DXM , et al . Effect of transendocardial delivery of autologous bone marrow mononuclear cells on functional capacity, left ventricular function, and perfusion in chronic heart failure: the FOCUS-CCTRN trial . JAMA . 2012 ; 307 ( 16 ): 1717 – 26 .
Sürder D , Manka R , Lo Cicero V , Moccetti T , Rufibach K , Soncin S , et al . Intracoronary injection of bone marrow-derived mononuclear cells early or late after acute myocardial infarction: effects on global left ventricular function . Circulation . 2013 ; 127 ( 19 ): 1968 – 79 .
Traverse JH , Henry TD , Pepine CJ , Willerson JT , Zhao DX , Ellis SG , et al . Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarction: the TIME randomized trial . JAMA . 2012 ; 308 ( 22 ): 2380 – 9 .
Menasché P , Alfieri O , Janssens S , Mckenna W , Reichenspurner H , Trinquart L , et al . The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation . Circulation . 2008 ; 117 ( 9 ): 1189 – 200 .
Fouts K , Fernandes B , Mal N , Liu J , Laurita KR . Electrophysiological consequence of skeletal myoblast transplantation in normal and infarcted canine myocardium . Heart Rhythm . 2006 ; 3 ( 4 ): 452 – 61 .
Dominguez MH , Krup AL , Muncie JM , Bruneau BG . Graded mesoderm assembly governs cell fate and morphogenesis of the early mammalian heart . Cell . 2023 ; 186 ( 3 ): 479 - 96.e23 .
Mummery C , Ward-Van Oostwaard D , Doevendans P , Spijker R , Van Den Brink S , Hassink R , et al . Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells . Circulation . 2003 ; 107 ( 21 ): 2733 – 40 .
Mummery CL , Zhang J , Ng ES , Elliott DA , Elefanty AG , Kamp TJ . Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview . Circ Res . 2012 ; 111 ( 3 ): 344 – 58 .
Shiba Y , Fernandes S , Zhu WZ , Filice D , Muskheli V , Kim J , et al . Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts . Nature . 2012 ; 489 ( 7415 ): 322 – 5 .
Chong JJH , Yang X , Don CW , Minami E , Liu YW , Weyers JJ , et al . Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts . Nature . 2014 ; 510 ( 7504 ): 273 – 7 .
Romagnuolo R , Masoudpour H , Porta-Sánchez A , Qiang B , Barry J , Laskary A , et al . Human embryonic stem cell-derived cardiomyocytes regenerate the infarcted pig heart but induce ventricular tachyarrhythmias . Stem Cell Rep . 2019 ; 12 ( 5 ): 967 – 81 .
Menasché P , Vanneaux V , Hagège A , Bel A , Cholley B , Parouchev A , et al . Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction . J Am Coll Cardiol . 2018 ; 71 ( 4 ): 429 – 38 .
Shiba Y , Gomibuchi T , Seto T , Wada Y , Ichimura H , Tanaka Y , et al . Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts . Nature . 2016 ; 538 ( 7625 ): 388 – 91 .
Kawamura M , Miyagawa S , Miki K , Saito A , Fukushima S , Higuchi T , et al . Feasibility, safety, and therapeutic efficacy of human induced pluripotent stem cell-derived cardiomyocyte sheets in a porcine ischemic cardiomyopathy model . Circulation . 2012 ; 126 ( 11 Suppl 1 ): S29 - 37 .
Hare JM , Fishman JE , Gerstenblith G , Difede Velazquez DL , Zambrano JP , Suncion VY , et al . Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial . JAMA . 2012 ; 308 ( 22 ): 2369 – 79 .
Mathiasen AB , Qayyum AA , Jørgensen E , Helqvist S , Fischer-Nielsen A , Kofoed KF , et al . Bone marrow-derived mesenchymal stromal cell treatment in patients with severe ischaemic heart failure: a randomized placebo-controlled trial (MSC-HF trial) . Eur Heart J . 2015 ; 36 ( 27 ): 1744 – 53 .
Bartolucci J , Verdugo FJ , González PL , Larrea RE , Abarzua E , Goset C , et al . Safety and efficacy of the intravenous infusion of umbilical cord mesenchymal stem cells in patients with heart failure: a phase 1/2 randomized controlled trial [RIMECARD Trial (Randomized Clinical Trial of Intravenous Infusion Umbilical Cord Mesenchymal Stem Cells on Cardiopathy)] . Circ Res . 2017 ; 121 ( 10 ): 1192 – 204 .
Bartunek J , Terzic A , Davison BA , Filippatos GS , Radovanovic S , Beleslin B , et al . Cardiopoietic cell therapy for advanced ischaemic heart failure: results at 39 weeks of the prospective, randomized, double blind, sham-controlled CHART-1 clinical trial . Eur Heart J . 2017 ; 38 ( 9 ): 648 – 60 .
Bartunek J , Terzic A , Davison BA , Behfar A , Sanz-Ruiz R , Wojakowski W , et al . Cardiopoietic stem cell therapy in ischaemic heart failure: longterm clinical outcomes . ESC Heart Fail . 2020 ; 7 ( 6 ): 3345 – 54 .
Yamada S , Bartunek J , Behfar A , Terzic A . Mass customized outlook for regenerative heart failure care . Int J Mol Sci . 2021 ; 22 ( 21 ): 11394 .
Bolli R , Mitrani RD , Hare JM , Pepine CJ , Perin EC , Willerson JT , et al . A phase Ⅱ study of autologous mesenchymal stromal cells and c-kit positive cardiac cells, alone or in combination, in patients with ischaemic heart failure: the CCTRN CONCERT-HF trial . Eur J Heart Fail . 2021 ; 23 ( 4 ): 661 – 74 .
Bolli R , Hare JM , March KL , Pepine CJ , Willerson JT , Perin EC , et al . Rationale and design of the CONCERT-HF trial (combination of mesenchymal and c-kit + cardiac stem cells as regenerative therapy for heart failure) . Circ Res . 2018 ; 122 ( 12 ): 1703 – 15 .
Gao LR , Pei XT , Ding QA , Chen Y , Zhang NK , Chen HY , et al . A critical challenge: dosage-related efficacy and acute complication intracoronary injection of autologous bone marrow mesenchymal stem cells in acute myocardial infarction . Int J Cardiol . 2013 ; 168 ( 4 ): 3191 – 9 .
Ward MR , Abadeh A , Connelly KA . Concise review: rational use of mesenchymal stem cells in the treatment of ischemic heart disease . Stem Cells Transl Med . 2018 ; 7 ( 7 ): 543 – 50 .
Antonitsis P , Ioannidou-Papagiannaki E , Kaidoglou A , Papakonstantinou C . In vitro cardiomyogenic differentiation of adult human bone marrow mesenchymal stem cells . The role of 5-azacytidine. Interact Cardiovasc Thorac Surg . 2007 ; 6 ( 5 ): 593 – 7 .
Silva GV , Litovsky S , Assad JAR , Sousa ALS , Martin BJ , Vela D , et al . Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model . Circulation . 2005 ; 111 ( 2 ): 150 – 6 .
Xu JY , Qian HY , Huang PS , Xu J , Xiong YY , Jiang WY , et al . Transplantation efficacy of autologous bone marrow mesenchymal stem cells combined with atorvastatin for acute myocardial infarction (TEAM-AMI): rationale and design of a randomized, double-blind, placebo-controlled, multi-center Phase Ⅱ TEAM-AMI trial . Regen Med . 2019 ; 14 ( 12 ): 1077 – 87 .
Vagnozzi RJ , Maillet M , Sargent MA , Khalil H , Johansen AKZ , Schwanekamp JA , et al . An acute immune response underlies the benefit of cardiac stem cell therapy . Nature . 2020 ; 577 ( 7790 ): 405 – 9 .
Bolli R , Tang XL , Guo Y , Li Q . After the storm: an objective appraisal of the efficacy of c-kit + cardiac progenitor cells in preclinical models of heart disease . Can J Physiol Pharmacol . 2021 ; 99 ( 2 ): 129 – 39 .
Bolli R , Solankhi M , Tang XL , Kahlon A . Cell therapy in patients with heart failure: a comprehensive review and emerging concepts . Cardiovasc Res . 2022 ; 118 ( 4 ): 951 – 76 .
Nakajima H , Ishikawa H , Yamamoto T , Chiba A , Fukui H , Sako K , et al . Endoderm-derived islet1-expressing cells differentiate into endothelial cells to function as the vascular HSPC niche in zebrafish . Dev Cell . 2023 ; 58 ( 3 ): 224 - 38.e7 .
Akbarzadeh A , Sobhani S , Soltani Khaboushan A , Kajbafzadeh AM . Whole-heart tissue engineering and cardiac patches: challenges and promises . Bioengineering (Basel) . 2023 ; 10 ( 1 ): 106 .
Diaz-Navarro R , Urrútia G , Cleland JG , Poloni D , Villagran F , Acosta-Dighero R , et al . Stem cell therapy for dilated cardiomyopathy . Cochrane Database Syst Rev . 2021 ; 7 ( 7 ): CD013433 .
Weiss JN . IMMNC-HF: IntraMyocardial injection of bone marrow mono-Nuclear cells in heart failure (HF) patients . In: Weiss JN , editor . Stem cell surgery trials in heart failure and diabetes: a concise guide . Cham : Springer International Publishing ; 2022 . p. 67 – 9 .
Borow KM , Yaroshinsky A , Greenberg B , Perin EC . Phase 3 DREAM-HF trial of mesenchymal precursor cells in chronic heart failure . Circ Res . 2019 ; 125 ( 3 ): 265 – 81 .
Yamada S , Jeon R , Garmany A , Behfar A , Terzic A . Screening for regenerative therapy responders in heart failure . Biomark Med . 2021 ; 15 ( 10 ): 775 – 83 .
Tripathi H , Domingues A , Donahue R , Cras A , Guerin CL , Gao E , et al . Combined transplantation of human MSCs and ECFCs improves cardiac function and decrease cardiomyocyte apoptosis after acute myocardial infarction . Stem Cell Rev Rep . 2023 ; 19 ( 2 ): 573 – 7 .
Spiroski AM , McCracken IR , Thomson A , Magalhaes-Pinto M , Lalwani MK , Newton KJ , et al . Human embryonic stem cell-derived endothelial cell product injection attenuates cardiac remodeling in myocardial infarction . Front Cardiovasc Med . 2022 ; 9 : 953211 .
Rolland L , Harrington A , Faucherre A , Abaroa JM , Gangatharan G , Gamba L , et al . The regenerative response of cardiac interstitial cells . J Mol Cell Biol . 2022 . mjac059 . https://doi.org/10.1093/jmcb/mjac0 59 https://doi.org/10.1093/jmcb/mjac0 59 .
Mohamed TMA , Ang YS , Radzinsky E , Zhou P , Huang Y , Elfenbein A , et al . Regulation of cell cycle to stimulate adult cardiomyocyte proliferation and cardiac regeneration . Cell . 2018 ; 173 ( 1 ): 104 - 16.e12 .
Liu S , Li K , Wagner Florencio L , Tang L , Heallen TR , Leach JP , et al . Gene therapy knockdown of Hippo signaling induces cardiomyocyte renewal in pigs after myocardial infarction . Sci Transl Med . 2021 ; 13 ( 600 ): eabd6892 .
Dang CV . MYC, metabolism, cell growth, and tumorigenesis . Cold Spring Harb Perspect Med . 2013 ; 3 ( 8 ): a014217 .
Bywater MJ , Burkhart DL , Straube J , Sabò A , Pendino V , Hudson JE , et al . Reactivation of Myc transcription in the mouse heart unlocks its proliferative capacity . Nat Commun . 2020 ; 11 ( 1 ): 1827 .
Chen Y , Lüttmann FF , Schoger E , Schöler HR , Zelarayán LC , Kim KP , et al . Reversible reprogramming of cardiomyocytes to a fetal state drives heart regeneration in mice . Science . 2021 ; 373 ( 6562 ): 1537 – 40 .
Polizzotti BD , Ganapathy B , Walsh S , Choudhury S , Ammanamanchi N , Bennett DG , et al . Neuregulin stimulation of cardiomyocyte regeneration in mice and human myocardium reveals a therapeutic window . Sci Transl Med . 2015 ; 7 ( 281 ): 281ra45 .
Lenihan DJ , Anderson SA , Lenneman CG , Brittain E , Muldowney JaS, 3rd , Mendes L , et al . A phase I, single ascending dose study of cimaglermin Alfa (neuregulin 1β3) in patients with systolic dysfunction and heart failure . JACC Basic Transl Sci . 2016 ; 1 ( 7 ): 576 – 86 .
Gao R , Zhang J , Cheng L , Wu X , Dong W , Yang X , et al . A phase Ⅱ, randomized, double-blind, multicenter, based on standard therapy, placebo-controlled study of the efficacy and safety of recombinant human neuregulin-1 in patients with chronic heart failure . J Am Coll Cardiol . 2010 ; 55 ( 18 ): 1907 – 14 .
Nguyen NUN , Canseco DC , Xiao F , Nakada Y , Li S , Lam NT , et al . A calcineurin-Hoxb13 axis regulates growth mode of mammalian cardiomyocytes . Nature . 2020 ; 582 ( 7811 ): 271 – 6 .
Mahmoud AI , Kocabas F , Muralidhar SA , Kimura W , Koura AS , Thet S , et al . Meis1 regulates postnatal cardiomyocyte cell cycle arrest . Nature . 2013 ; 497 ( 7448 ): 249 – 53 .
Pinto AR , Ilinykh A , Ivey MJ , Kuwabara JT , D’antoni ML , Debuque R , et al . Revisiting cardiac cellular composition . Circ Res . 2016 ; 118 ( 3 ): 400 – 9 .
Ieda M , Fu JD , Delgado-Olguin P , Vedantham V , Hayashi Y , Bruneau BG , et al . Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors . Cell . 2010 ; 142 ( 3 ): 375 – 86 .
Song K , Nam YJ , Luo X , Qi X , Tan W , Huang GN , et al . Heart repair by reprogramming non-myocytes with cardiac transcription factors . Nature . 2012 ; 485 ( 7400 ): 599 – 604 .
Abad M , Hashimoto H , Zhou H , Morales MG , Chen B , Bassel-Duby R , et al . Notch inhibition enhances cardiac reprogramming by increasing MEF2C transcriptional activity . Stem Cell Rep . 2017 ; 8 ( 3 ): 548 – 60 .
Zhou H , Morales MG , Hashimoto H , Dickson ME , Song K , Ye W , et al . ZNF281 enhances cardiac reprogramming by modulating cardiac and inflammatory gene expression . Genes Dev . 2017 ; 31 ( 17 ): 1770 – 83 .
Yamakawa H , Muraoka N , Miyamoto K , Sadahiro T , Isomi M , Haginiwa S , et al . Fibroblast growth factors and vascular endothelial growth factor promote cardiac reprogramming under defined conditions . Stem Cell Rep . 2015 ; 5 ( 6 ): 1128 – 42 .
Zhou H , Dickson ME , Kim MS , Bassel-Duby R , Olson EN . Akt1/protein kinase B enhances transcriptional reprogramming of fibroblasts to functional cardiomyocytes . Proc Natl Acad Sci U S A . 2015 ; 112 ( 38 ): 11864 – 9 .
Zhou Y , Wang L , Vaseghi HR , Liu Z , Lu R , Alimohamadi S , et al . Bmi1 is a key epigenetic barrier to direct cardiac reprogramming . Cell Stem Cell . 2016 ; 18 ( 3 ): 382 – 95 .
Mohamed TMA , Stone NR , Berry EC , Radzinsky E , Huang Y , Pratt K , et al . Chemical enhancement of in vitro and in vivo direct cardiac reprogramming . Circulation . 2017 ; 135 ( 10 ): 978 – 95 .
Wang L , Ma H , Huang P , Xie Y , Near D , Wang H , et al . Down-regulation of Beclin1 promotes direct cardiac reprogramming . Sci Transl Med . 2020 ; 12 ( 566 ): eaay7856 .
Jayawardena TM , Egemnazarov B , Finch EA , Zhang L , Payne JA , Pandya K , et al . MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes . Circ Res . 2012 ; 110 ( 11 ): 1465 – 73 .
Jayawardena TM , Finch EA , Zhang L , Zhang H , Hodgkinson CP , Pratt RE , et al . MicroRNA induced cardiac reprogramming in vivo : evidence for mature cardiac myocytes and improved cardiac function . Circ Res . 2015 ; 116 ( 3 ): 418 – 24 .
Lalit PA , Salick MR , Nelson DO , Squirrell JM , Shafer CM , Patel NG , et al . Lineage reprogramming of fibroblasts into proliferative induced cardiac progenitor cells by defined factors . Cell Stem Cell . 2016 ; 18 ( 3 ): 354 – 67 .
Tang Y , Aryal S , Geng X , Zhou X , Fast VG , Zhang J , et al . TBX20 improves contractility and mitochondrial function during direct human cardiac reprogramming . Circulation . 2022 ; 146 ( 20 ): 1518 – 36 .
Nam YJ , Song K , Luo X , Daniel E , Lambeth K , West K , et al . Reprogramming of human fibroblasts toward a cardiac fate . Proc Natl Acad Sci U S A . 2013 ; 110 ( 14 ): 5588 – 93 .
Paoletti C , Divieto C , Tarricone G , Di Meglio F , Nurzynska D , Chiono V . MicroRNA-mediated direct reprogramming of human adult fibroblasts toward cardiac phenotype . Front Bioeng Biotechnol . 2020 ; 8 ( 529 ): 529 .
Wada R , Muraoka N , Inagawa K , Yamakawa H , Miyamoto K , Sadahiro T , et al . Induction of human cardiomyocyte-like cells from fibroblasts by defined factors . Proc Natl Acad Sci U S A . 2013 ; 110 ( 31 ): 12667 – 72 .
Fu JD , Stone NR , Liu L , Spencer CI , Qian L , Hayashi Y , et al . Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state . Stem Cell Rep . 2013 ; 1 ( 3 ): 235 – 47 .
Islas JF , Liu Y , Weng KC , Robertson MJ , Zhang S , Prejusa A , et al . Transcription factors ETS2 and MESP1 transdifferentiate human dermal fibroblasts into cardiac progenitors . Proc Natl Acad Sci U S A . 2012 ; 109 ( 32 ): 13016 – 21 .
Nam YJ , Lubczyk C , Bhakta M , Zang T , Fernandez-Perez A , Mcanally J , et al . Induction of diverse cardiac cell types by reprogramming fibroblasts with cardiac transcription factors . Development . 2014 ; 141 ( 22 ): 4267 – 78 .
Tani H , Sadahiro T , Yamada Y , Isomi M , Yamakawa H , Fujita R , et al . Direct reprogramming improves cardiac function and reverses fibrosis in chronic myocardial infarction . Circulation . 2023 ; 147 ( 3 ): 223 – 38 .
Puente BN , Kimura W , Muralidhar SA , Moon J , Amatruda JF , Phelps KL , et al . The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response . Cell . 2014 ; 157 ( 3 ): 565 – 79 .
Nakada Y , Canseco DC , Thet S , Abdisalaam S , Asaithamby A , Santos CX , et al . Hypoxia induces heart regeneration in adult mice . Nature . 2017 ; 541 ( 7636 ): 222 – 7 .
Harada K , Friedman M , Lopez JJ , Wang SY , Li J , Prasad PV , et al . Vascular endothelial growth factor administration in chronic myocardial ischemia . Am J Physiol . 1996 ; 270 ( 5 Pt 2 ): H1791 – 802 .
House SL , Bolte C , Zhou M , Doetschman T , Klevitsky R , Newman G , et al . Cardiac-specific overexpression of fibroblast growth factor-2 protects against myocardial dysfunction and infarction in a murine model of low-flow ischemia . Circulation . 2003 ; 108 ( 25 ): 3140 – 8 .
Gyöngyösi M , Khorsand A , Zamini S , Sperker W , Strehblow C , Kastrup J , et al . NOGA-guided analysis of regional myocardial perfusion abnormalities treated with intramyocardial injections of plasmid encoding vascular endothelial growth factor A-165 in patients with chronic myocardial ischemia: subanalysis of the EUROINJECT-ONE multicenter double-blind randomized study . Circulation . 2005 ; 112 ( 9 Suppl ): I157 – 65 .
Simons M , Annex BH , Laham RJ , Kleiman N , Henry T , Dauerman H , et al . Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial . Circulation . 2002 ; 105 ( 7 ): 788 – 93 .
Zangi L , Lui KO , Von Gise A , Ma Q , Ebina W , Ptaszek LM , et al . Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction . Nat Biotechnol . 2013 ; 31 ( 10 ): 898 – 907 .
Boos F , Oo JA , Warwick T , Günther S , Izquierdo Ponce J , Lopez M , et al . The endothelial-enriched lncRNA LINC00607 mediates angiogenic function . Basic Res Cardiol . 2023 ; 118 ( 1 ): 5 .
Anttila V , Saraste A , Knuuti J , Hedman M , Jaakkola P , Laugwitz KL , et al . Direct intramyocardial injection of VEGF mRNA in patients undergoing coronary artery bypass grafting . Mol Ther . 2023 ; 31 ( 3 ): 866 – 74 .
Arora H , Lavin AC , Balkan W , Hare JM , White IA . Neuregulin-1, in a conducive milieu with Wnt/BMP/retinoic acid, prolongs the epicardial-mediated cardiac regeneration capacity of neonatal heart explants . J Stem Cells Regen Med . 2021 ; 17 ( 1 ): 18 – 27 .
Wasserman AH , Huang AR , Lewis-Israeli YR , Dooley MD , Mitchell AL , Venkatesan M , et al . Oxytocin promotes epicardial cell activation and heart regeneration after cardiac injury . Front Cell Dev Biol . 2022 ; 10 : 985298 .
Smart N , Risebro CA , Melville AAD , Moses K , Schwartz RJ , Chien KR , et al . Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization . Nature . 2007 ; 445 ( 7124 ): 177 – 82 .
Smart N , Bollini S , Dubé KN , Vieira JM , Zhou B , Davidson S , et al . De novo cardiomyocytes from within the activated adult heart after injury . Nature . 2011 ; 474 ( 7353 ): 640 – 4 .
Barile L , Lionetti V , Cervio E , Matteucci M , Gherghiceanu M , Popescu LM , et al . Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction . Cardiovasc Res . 2014 ; 103 ( 4 ): 530 – 41 .
Gladka MM , Johansen AKZ , van Kampen SJ , Peters MMC , Molenaar B , Versteeg D , et al . Thymosin β4 and prothymosin α promote cardiac regeneration post-ischemic injury in mice . Cardiovasc Res . 2022 . cvac155 . https://doi.org/10.1093/cvr/cvac155 https://doi.org/10.1093/cvr/cvac155 .
Colombo M , Raposo G , Théry C . Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles . Annu Rev Cell Dev Biol . 2014 ; 30 : 255 – 89 .
Gao L , Wang L , Wei Y , Krishnamurthy P , Walcott GP , Menasché P , et al . Exosomes secreted by hiPSC-derived cardiac cells improve recovery from myocardial infarction in swine . Sci Transl Med . 2020 ; 12 ( 561 ): eaay1318 . https://doi.org/10.1126/scitranslmed.aay1318 https://doi.org/10.1126/scitranslmed.aay1318 .
Saha P , Sharma S , Korutla L , Datla SR , Shoja-Taheri F , Mishra R , et al . Circulating exosomes derived from transplanted progenitor cells aid the functional recovery of ischemic myocardium . Sci Transl Med . 2019 ; 11 ( 493 ): eaau1168 .
Cai CL , Martin JC , Sun Y , Cui L , Wang L , Ouyang K , et al . A myocardial lineage derives from Tbx18 epicardial cells . Nature . 2008 ; 454 ( 7200 ): 104 – 8 .
Zhou B , Ma Q , Rajagopal S , Wu SM , Domian I , Rivera-Feliciano J , et al . Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart . Nature . 2008 ; 454 ( 7200 ): 109 – 13 .
Zhou B , Honor LB , He H , Ma Q , Oh JH , Butterfield C , et al . Adult mouse epicardium modulates myocardial injury by secreting paracrine factors . J Clin Invest . 2011 ; 121 ( 5 ): 1894 – 904 .
Arrell DK , Rosenow CS , Yamada S , Behfar A , Terzic A . Cardiopoietic stem cell therapy restores infarction-altered cardiac proteome . NPJ Regen Med . 2020 ; 5 : 5 .
de Abreu RC , Fernandes H , da Costa Martins PA , Sahoo S , Emanueli C , Ferreira L . Native and bioengineered extracellular vesicles for cardiovascular therapeutics . Nat Rev Cardiol . 2020 ; 17 ( 11 ): 685 – 97 .
Lim GB . An acellular artificial cardiac patch for myocardial repair . Nat Rev Cardiol . 2020 ; 17 ( 6 ): 323 .
Chow A , Stuckey DJ , Kidher E , Rocco M , Jabbour RJ , Mansfield CA , et al . Human induced pluripotent stem cell-derived cardiomyocyte encapsulating bioactive hydrogels improve rat heart function post myocardial infarction . Stem Cell Rep . 2017 ; 9 ( 5 ): 1415 – 22 .
Shafei S , Khanmohammadi M , Ghanbari H , Nooshabadi VT , Tafti SHA , Rabbani S , et al . Effectiveness of exosome mediated miR-126 and miR-146a delivery on cardiac tissue regeneration . Cell Tissue Res . 2022 ; 390 ( 1 ): 71 – 92 .
Sharma V , Manhas A , Gupta S , Dikshit M , Jagavelu K , Verma RS . Fabrication, characterization and in vivo assessment of cardiogel loaded chitosan patch for myocardial regeneration . Int J Biol Macromol . 2022 ; 222 ( Pt B ): 3045 – 56 .
Hu C , Liu W , Long L , Wang Z , Zhang W , He S , et al . Regeneration of infarcted hearts by myocardial infarction-responsive injectable hydrogels with combined anti-apoptosis, anti-inflammatory and proangiogenesis properties . Biomaterials . 2022 ; 290 : 121849 .
Grigorian-Shamagian L , Sanz-Ruiz R , Climent A , Badimon L , Barile L , Bolli R , et al . Insights into therapeutic products, preclinical research models, and clinical trials in cardiac regenerative and reparative medicine: where are we now and the way ahead. Current opinion paper of the ESC Working Group on Cardiovascular Regenerative and Reparative Medicine . Cardiovasc Res . 2021 ; 117 ( 6 ): 1428 – 33 .
Lovell-Badge R , Anthony E , Barker RA , Bubela T , Brivanlou AH , Carpenter M , et al . ISSCR guidelines for stem cell research and clinical translation: the 2021 update . Stem Cell Rep . 2021 ; 16 ( 6 ): 1398 – 408 .
Povsic TJ , Sanz-Ruiz R , Climent AM , Bolli R , Taylor DA , Gersh BJ , et al . Reparative cell therapy for the heart: critical internal appraisal of the field in response to recent controversies . ESC Heart Fail . 2021 ; 8 ( 3 ): 2306 – 9 .
Yamada S , Behfar A , Terzic A . Regenerative medicine clinical readiness . Regen Med . 2021 ; 16 ( 3 ): 309 – 22 .
Vermersch E , Jouve C , Hulot JS . CRISPR/Cas9 gene-editing strategies in cardiovascular cells . Cardiovasc Res . 2020 ; 116 ( 5 ): 894 – 907 .
Zhang Y , Karakikes I . Translating genomic insights into cardiovascular medicine: opportunities and challenges of CRISPR-Cas9 . Trends Cardiovasc Med . 2021 ; 31 ( 6 ): 341 – 8 .
Musunuru K . CRISPR and cardiovascular diseases . Cardiovasc Res . 2022 . cvac048 . https://doi.org/10.1093/cvr/cvac048 https://doi.org/10.1093/cvr/cvac048 .
Jiang L , Liang J , Huang W , Ma J , Park KH , Wu Z , et al . CRISPR activation of endogenous genes reprograms fibroblasts into cardiovascular progenitor cells for myocardial infarction therapy . Mol Ther . 2022 ; 30 ( 1 ): 54 – 74 .
Theodoris CV , Zhou P , Liu L , Zhang Y , Nishino T , Huang Y , et al . Network-based screen in iPSC-derived cells reveals therapeutic candidate for heart valve disease . Science . 2021 ; 371 ( 6530 ): eabd0724 .
Lin X , Liu Y , Liu S , Zhu X , Wu L , Zhu Y , et al . Nested epistasis enhancer networks for robust genome regulation . Science . 2022 ; 377 ( 6610 ): 1077 – 85 .
Sendra M , de Dios Hourcade J , Temiño S , Sarabia AJ , Ocaña OH , Domínguez JN , et al . Cre recombinase microinjection for single-cell tracing and localised gene targeting . Development . 2023 ; 150 ( 3 ): dev201206 . https://doi.org/10.1242/dev.201206 https://doi.org/10.1242/dev.201206 .
Assad H , Assad A , Kumar A . Recent developments in 3D bio-printing and its biomedical applications . Pharmaceutics . 2023 ; 15 ( 1 ): 255 .
0
浏览量
1
Downloads
0
CSCD
- 网络PDF下载
- Meta-XML下载
- BibTeX下载
- Endnote下载
- RefMan 下载
- NoteExpress下载
- NoteFirst下载
关联资源
相关文章
相关作者
相关机构
- 技术支持由北京北大方正电子有限公司提供 京ICP备09064830号-19
京公网安备11010802024621 - 本系统建议在Chrome、 IE9+ 以上版本浏览器阅读本站内容，360浏览器请切换至极速模式
- Cookies帮助我们提供服务并提供个性化体验。使用本网站，即表示您同意我们使用Cookies