Journal of Cardiovascular Development and Disease

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17 pages, 4898 KiB

Open AccessArticle

A Heterozygous Mutation in Cardiac Troponin T Promotes Ca²⁺ Dysregulation and Adult Cardiomyopathy in Zebrafish

by Sarah M. Kamel, Charlotte D. Koopman, Fabian Kruse, Sven Willekers, Sonja Chocron and Jeroen Bakkers

J. Cardiovasc. Dev. Dis. 2021, 8(4), 46; https://doi.org/10.3390/jcdd8040046 - 20 Apr 2021

Cited by 7 | Viewed by 4211

Abstract

Cardiomyopathies are a group of heterogeneous diseases that affect the muscles of the heart, leading to early morbidity and mortality in young and adults. Genetic forms of cardiomyopathy are caused predominantly by mutations in structural components of the cardiomyocyte sarcomeres, the contractile units [...] Read more.

Cardiomyopathies are a group of heterogeneous diseases that affect the muscles of the heart, leading to early morbidity and mortality in young and adults. Genetic forms of cardiomyopathy are caused predominantly by mutations in structural components of the cardiomyocyte sarcomeres, the contractile units of the heart, which includes cardiac Troponin T (TnT). Here, we generated mutations with CRISPR/Cas9 technology in the zebrafish tnnt2a gene, encoding cardiac TnT, at a mutational “hotspot” site to establish a zebrafish model for genetic cardiomyopathies. We found that a heterozygous tnnt2a mutation deleting Arginine at position 94 and Lysine at position 95 of TnT causes progressive cardiac structural changes resulting in heart failure. The cardiac remodeling is presented by an enlarged atrium, decreased ventricle size, increased myocardial stress as well as increased fibrosis. As early as five days post fertilization, larvae carrying the TnT RK94del mutation display diastolic dysfunction and impaired calcium dynamics related to increased Ca²⁺ sensitivity. In conclusion, adult zebrafish with a heterozygous TnT-RK94del mutation develop cardiomyopathy as seen in patients with TnT mutations and therefore represent a promising model to study disease mechanisms and to screen for putative therapeutic compounds. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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13 pages, 3921 KiB

Open AccessArticle

Persistent Ventricle Partitioning in the Adult Zebrafish Heart

by Catherine Pfefferli, Hannah R. Moran, Anastasia Felker, Christian Mosimann and Anna Jaźwińska

J. Cardiovasc. Dev. Dis. 2021, 8(4), 41; https://doi.org/10.3390/jcdd8040041 - 9 Apr 2021

Cited by 3 | Viewed by 3783

Abstract

The vertebrate heart integrates cells from the early-differentiating first heart field (FHF) and the later-differentiating second heart field (SHF), both emerging from the lateral plate mesoderm. In mammals, this process forms the basis for the development of the left and right ventricle chambers [...] Read more.

The vertebrate heart integrates cells from the early-differentiating first heart field (FHF) and the later-differentiating second heart field (SHF), both emerging from the lateral plate mesoderm. In mammals, this process forms the basis for the development of the left and right ventricle chambers and subsequent chamber septation. The single ventricle-forming zebrafish heart also integrates FHF and SHF lineages during embryogenesis, yet the contributions of these two myocardial lineages to the adult zebrafish heart remain incompletely understood. Here, we characterize the myocardial labeling of FHF descendants in both the developing and adult zebrafish ventricle. Expanding previous findings, late gastrulation-stage labeling using drl-driven CreERT2 recombinase with a myocardium-specific, myl7-controlled, loxP reporter results in the predominant labeling of FHF-derived outer curvature and the right side of the embryonic ventricle. Raised to adulthood, such lineage-labeled hearts retain broad areas of FHF cardiomyocytes in a region of the ventricle that is positioned at the opposite side to the atrium and encompasses the apex. Our data add to the increasing evidence for a persisting cell-based compartmentalization of the adult zebrafish ventricle even in the absence of any physical boundary. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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17 pages, 9955 KiB

Open AccessEditor’s ChoiceArticle

Cauterization as a Simple Method for Regeneration Studies in the Zebrafish Heart

by Papa K. Van Dyck, Natasha Hockaden, Emma C. Nelson, Alyssa R. Koch, Kamil L. Hester, Neil Pillai, Gabrielle C. Coffing, Alan R. Burns and Pascal J. Lafontant

J. Cardiovasc. Dev. Dis. 2020, 7(4), 41; https://doi.org/10.3390/jcdd7040041 - 3 Oct 2020

Cited by 6 | Viewed by 5097

Abstract

In the last two decades, the zebrafish has emerged as an important model species for heart regeneration studies. Various approaches to model loss of cardiac myocytes and myocardial infarction in the zebrafish have been devised, and have included resection, genetic ablation, and cryoinjury. [...] Read more.

In the last two decades, the zebrafish has emerged as an important model species for heart regeneration studies. Various approaches to model loss of cardiac myocytes and myocardial infarction in the zebrafish have been devised, and have included resection, genetic ablation, and cryoinjury. However, to date, the response of the zebrafish ventricle to cautery injury has not been reported. Here, we describe a simple and reproducible method using cautery injury via a modified nichrome inoculating needle as a probe to model myocardial infarction in the zebrafish ventricle. Using light and electron microscopy, we show that cardiac cautery injury is attended by significant inflammatory cell infiltration, accumulation of collagen in the injured area, and the reconstitution of the ventricular myocardium. Additionally, we document the ablation of cardiac nerve fibers, and report that the re-innervation of the injured zebrafish ventricle is protracted, compared to other repair processes that accompany the regeneration of the cauterized ventricle. Taken together, our study demonstrates that cautery injury is a simple and effective means for generating necrotic tissue and eliciting a remodeling and regenerative response in the zebrafish heart. This approach may serve as an important tool in the methods toolbox for regeneration studies in the zebrafish. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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Review

Jump to: Research

12 pages, 1123 KiB

Open AccessReview

Getting to the Heart of Left–Right Asymmetry: Contributions from the Zebrafish Model

by Kelly A. Smith and Veronica Uribe

J. Cardiovasc. Dev. Dis. 2021, 8(6), 64; https://doi.org/10.3390/jcdd8060064 - 4 Jun 2021

Cited by 6 | Viewed by 3901

Abstract

The heart is laterally asymmetric. Not only is it positioned on the left side of the body but the organ itself is asymmetric. This patterning occurs across scales: at the organism level, through left–right axis patterning; at the organ level, where the heart [...] Read more.

The heart is laterally asymmetric. Not only is it positioned on the left side of the body but the organ itself is asymmetric. This patterning occurs across scales: at the organism level, through left–right axis patterning; at the organ level, where the heart itself exhibits left–right asymmetry; at the cellular level, where gene expression, deposition of matrix and proteins and cell behaviour are asymmetric; and at the molecular level, with chirality of molecules. Defective left–right patterning has dire consequences on multiple organs; however, mortality and morbidity arising from disrupted laterality is usually attributed to complex cardiac defects, bringing into focus the particulars of left–right patterning of the heart. Laterality defects impact how the heart integrates and connects with neighbouring organs, but the anatomy of the heart is also affected because of its asymmetry. Genetic studies have demonstrated that cardiac asymmetry is influenced by left–right axis patterning and yet the heart also possesses intrinsic laterality, reinforcing the patterning of this organ. These inputs into cardiac patterning are established at the very onset of left–right patterning (formation of the left–right organiser) and continue through propagation of left–right signals across animal axes, asymmetric differentiation of the cardiac fields, lateralised tube formation and asymmetric looping morphogenesis. In this review, we will discuss how left–right asymmetry is established and how that influences subsequent asymmetric development of the early embryonic heart. In keeping with the theme of this issue, we will focus on advancements made through studies using the zebrafish model and describe how its use has contributed considerable knowledge to our understanding of the patterning of the heart. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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24 pages, 2297 KiB

Open AccessFeature PaperEditor’s ChoiceReview

The Zebrafish Cardiac Endothelial Cell—Roles in Development and Regeneration

by Vanessa Lowe, Laura Wisniewski and Caroline Pellet-Many

J. Cardiovasc. Dev. Dis. 2021, 8(5), 49; https://doi.org/10.3390/jcdd8050049 - 1 May 2021

Cited by 12 | Viewed by 6690

Abstract

In zebrafish, the spatiotemporal development of the vascular system is well described due to its stereotypical nature. However, the cellular and molecular mechanisms orchestrating post-embryonic vascular development, the maintenance of vascular homeostasis, or how coronary vessels integrate into the growing heart are less [...] Read more.

In zebrafish, the spatiotemporal development of the vascular system is well described due to its stereotypical nature. However, the cellular and molecular mechanisms orchestrating post-embryonic vascular development, the maintenance of vascular homeostasis, or how coronary vessels integrate into the growing heart are less well studied. In the context of cardiac regeneration, the central cellular mechanism by which the heart regenerates a fully functional myocardium relies on the proliferation of pre-existing cardiomyocytes; the epicardium and the endocardium are also known to play key roles in the regenerative process. Remarkably, revascularisation of the injured tissue occurs within a few hours after cardiac damage, thus generating a vascular network acting as a scaffold for the regenerating myocardium. The activation of the endocardium leads to the secretion of cytokines, further supporting the proliferation of the cardiomyocytes. Although epicardium, endocardium, and myocardium interact with each other to orchestrate heart development and regeneration, in this review, we focus on recent advances in the understanding of the development of the endocardium and the coronary vasculature in zebrafish as well as their pivotal roles in the heart regeneration process. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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14 pages, 753 KiB

Open AccessReview

Zebrafish as a New Tool in Heart Preservation Research

by Luciana Da Silveira Cavalcante and Shannon N. Tessier

J. Cardiovasc. Dev. Dis. 2021, 8(4), 39; https://doi.org/10.3390/jcdd8040039 - 8 Apr 2021

Cited by 4 | Viewed by 2787

Abstract

Heart transplantation became a reality at the end of the 1960s as a life-saving option for patients with end-stage heart failure. Static cold storage (SCS) at 4–6 °C has remained the standard for heart preservation for decades. However, SCS only allows for short-term [...] Read more.

Heart transplantation became a reality at the end of the 1960s as a life-saving option for patients with end-stage heart failure. Static cold storage (SCS) at 4–6 °C has remained the standard for heart preservation for decades. However, SCS only allows for short-term storage that precludes optimal matching programs, requires emergency surgeries, and results in the unnecessary discard of organs. Among the alternatives seeking to extend ex vivo lifespan and mitigate the shortage of organs are sub-zero or machine perfusion modalities. Sub-zero approaches aim to prolong cold ischemia tolerance by deepening metabolic stasis, while machine perfusion aims to support metabolism through the continuous delivery of oxygen and nutrients. Each of these approaches hold promise; however, complex barriers must be overcome before their potential can be fully realized. We suggest that one barrier facing all experimental efforts to extend ex vivo lifespan are limited research tools. Mammalian models are usually the first choice due to translational aspects, yet experimentation can be restricted by expertise, time, and resources. Instead, there are instances when smaller vertebrate models, like the zebrafish, could fill critical experimental gaps in the field. Taken together, this review provides a summary of the current gold standard for heart preservation as well as new technologies in ex vivo lifespan extension. Furthermore, we describe how existing tools in zebrafish research, including isolated organ, cell specific and functional assays, as well as molecular tools, could complement and elevate heart preservation research. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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14 pages, 1241 KiB

Open AccessReview

The Lymphatic System in Zebrafish Heart Development, Regeneration and Disease Modeling

by Xidi Feng, Stanislao Travisano, Caroline A. Pearson, Ching-Ling Lien and Michael R. M. Harrison

J. Cardiovasc. Dev. Dis. 2021, 8(2), 21; https://doi.org/10.3390/jcdd8020021 - 19 Feb 2021

Cited by 8 | Viewed by 5117

Abstract

Heart disease remains the single largest cause of death in developed countries, and novel therapeutic interventions are desperately needed to alleviate this growing burden. The cardiac lymphatic system is the long-overlooked counterpart of the coronary blood vasculature, but its important roles in homeostasis [...] Read more.

Heart disease remains the single largest cause of death in developed countries, and novel therapeutic interventions are desperately needed to alleviate this growing burden. The cardiac lymphatic system is the long-overlooked counterpart of the coronary blood vasculature, but its important roles in homeostasis and disease are becoming increasingly apparent. Recently, the cardiac lymphatic vasculature in zebrafish has been described and its role in supporting the potent regenerative response of zebrafish heart tissue investigated. In this review, we discuss these findings in the wider context of lymphatic development, evolution and the promise of this system to open new therapeutic avenues to treat myocardial infarction and other cardiopathologies. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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22 pages, 16990 KiB

Open AccessEditor’s ChoiceReview

From Stripes to a Beating Heart: Early Cardiac Development in Zebrafish

by Cassie L. Kemmler, Fréderike W. Riemslagh, Hannah R. Moran and Christian Mosimann

J. Cardiovasc. Dev. Dis. 2021, 8(2), 17; https://doi.org/10.3390/jcdd8020017 - 10 Feb 2021

Cited by 19 | Viewed by 7764

Abstract

The heart is the first functional organ to form during vertebrate development. Congenital heart defects are the most common type of human birth defect, many originating as anomalies in early heart development. The zebrafish model provides an accessible vertebrate system to study early [...] Read more.

The heart is the first functional organ to form during vertebrate development. Congenital heart defects are the most common type of human birth defect, many originating as anomalies in early heart development. The zebrafish model provides an accessible vertebrate system to study early heart morphogenesis and to gain new insights into the mechanisms of congenital disease. Although composed of only two chambers compared with the four-chambered mammalian heart, the zebrafish heart integrates the core processes and cellular lineages central to cardiac development across vertebrates. The rapid, translucent development of zebrafish is amenable to in vivo imaging and genetic lineage tracing techniques, providing versatile tools to study heart field migration and myocardial progenitor addition and differentiation. Combining transgenic reporters with rapid genome engineering via CRISPR-Cas9 allows for functional testing of candidate genes associated with congenital heart defects and the discovery of molecular causes leading to observed phenotypes. Here, we summarize key insights gained through zebrafish studies into the early patterning of uncommitted lateral plate mesoderm into cardiac progenitors and their regulation. We review the central genetic mechanisms, available tools, and approaches for modeling congenital heart anomalies in the zebrafish as a representative vertebrate model. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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17 pages, 1155 KiB

Open AccessEditor’s ChoiceReview

Atrial and Sinoatrial Node Development in the Zebrafish Heart

by Kendall E. Martin and Joshua S. Waxman

J. Cardiovasc. Dev. Dis. 2021, 8(2), 15; https://doi.org/10.3390/jcdd8020015 - 9 Feb 2021

Cited by 13 | Viewed by 4549

Abstract

Proper development and function of the vertebrate heart is vital for embryonic and postnatal life. Many congenital heart defects in humans are associated with disruption of genes that direct the formation or maintenance of atrial and pacemaker cardiomyocytes at the venous pole of [...] Read more.

Proper development and function of the vertebrate heart is vital for embryonic and postnatal life. Many congenital heart defects in humans are associated with disruption of genes that direct the formation or maintenance of atrial and pacemaker cardiomyocytes at the venous pole of the heart. Zebrafish are an outstanding model for studying vertebrate cardiogenesis, due to the conservation of molecular mechanisms underlying early heart development, external development, and ease of genetic manipulation. Here, we discuss early developmental mechanisms that instruct appropriate formation of the venous pole in zebrafish embryos. We primarily focus on signals that determine atrial chamber size and the specialized pacemaker cells of the sinoatrial node through directing proper specification and differentiation, as well as contemporary insights into the plasticity and maintenance of cardiomyocyte identity in embryonic zebrafish hearts. Finally, we integrate how these insights into zebrafish cardiogenesis can serve as models for human atrial defects and arrhythmias. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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14 pages, 3828 KiB

Open AccessFeature PaperEditor’s ChoiceReview

Pathways Regulating Establishment and Maintenance of Cardiac Chamber Identity in Zebrafish

by Yao Yao, Amanda N. Marra and Deborah Yelon

J. Cardiovasc. Dev. Dis. 2021, 8(2), 13; https://doi.org/10.3390/jcdd8020013 - 29 Jan 2021

Cited by 7 | Viewed by 3777

Abstract

The vertebrate heart is comprised of two types of chambers—ventricles and atria—that have unique morphological and physiological properties. Effective cardiac function depends upon the distinct characteristics of ventricular and atrial cardiomyocytes, raising interest in the genetic pathways that regulate chamber-specific traits. Chamber identity [...] Read more.

The vertebrate heart is comprised of two types of chambers—ventricles and atria—that have unique morphological and physiological properties. Effective cardiac function depends upon the distinct characteristics of ventricular and atrial cardiomyocytes, raising interest in the genetic pathways that regulate chamber-specific traits. Chamber identity seems to be specified in the early embryo by signals that establish ventricular and atrial progenitor populations and trigger distinct differentiation pathways. Intriguingly, chamber-specific features appear to require active reinforcement, even after myocardial differentiation is underway, suggesting plasticity of chamber identity within the developing heart. Here, we review the utility of the zebrafish as a model organism for studying the mechanisms that establish and maintain cardiac chamber identity. By combining genetic and embryological approaches, work in zebrafish has revealed multiple players with potent influences on chamber fate specification and commitment. Going forward, analysis of cardiomyocyte identity at the single-cell level is likely to yield a high-resolution understanding of the pathways that link the relevant players together, and these insights will have the potential to inform future strategies in cardiac tissue engineering. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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18 pages, 1632 KiB

Open AccessFeature PaperEditor’s ChoiceReview

Mechanisms of TTNtv-Related Dilated Cardiomyopathy: Insights from Zebrafish Models

by Celine F. Santiago, Inken G. Huttner and Diane Fatkin

J. Cardiovasc. Dev. Dis. 2021, 8(2), 10; https://doi.org/10.3390/jcdd8020010 - 25 Jan 2021

Cited by 13 | Viewed by 5883

Abstract

Dilated cardiomyopathy (DCM) is a common heart muscle disorder characterized by ventricular dilation and contractile dysfunction that is associated with significant morbidity and mortality. New insights into disease mechanisms and strategies for treatment and prevention are urgently needed. Truncating variants in the TTN [...] Read more.

Dilated cardiomyopathy (DCM) is a common heart muscle disorder characterized by ventricular dilation and contractile dysfunction that is associated with significant morbidity and mortality. New insights into disease mechanisms and strategies for treatment and prevention are urgently needed. Truncating variants in the TTN gene, which encodes the giant sarcomeric protein titin (TTNtv), are the most common genetic cause of DCM, but exactly how TTNtv promote cardiomyocyte dysfunction is not known. Although rodent models have been widely used to investigate titin biology, they have had limited utility for TTNtv-related DCM. In recent years, zebrafish (Danio rerio) have emerged as a powerful alternative model system for studying titin function in the healthy and diseased heart. Optically transparent embryonic zebrafish models have demonstrated key roles of titin in sarcomere assembly and cardiac development. The increasing availability of sophisticated imaging tools for assessment of heart function in adult zebrafish has revolutionized the field and opened new opportunities for modelling human genetic disorders. Genetically modified zebrafish that carry a human A-band TTNtv have now been generated and shown to spontaneously develop DCM with age. This zebrafish model will be a valuable resource for elucidating the phenotype modifying effects of genetic and environmental factors, and for exploring new drug therapies. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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12 pages, 574 KiB

Open AccessReview

Zebrafish Models of Cancer Therapy-Induced Cardiovascular Toxicity

by Sarah Lane, Luis Alberto More and Aarti Asnani

J. Cardiovasc. Dev. Dis. 2021, 8(2), 8; https://doi.org/10.3390/jcdd8020008 - 22 Jan 2021

Cited by 8 | Viewed by 3260

Abstract

Purpose of review: Both traditional and novel cancer therapies can cause cardiovascular toxicity in patients. In vivo models integrating both cardiovascular and cancer phenotypes allow for the study of on- and off-target mechanisms of toxicity arising from these agents. The zebrafish is the [...] Read more.

Purpose of review: Both traditional and novel cancer therapies can cause cardiovascular toxicity in patients. In vivo models integrating both cardiovascular and cancer phenotypes allow for the study of on- and off-target mechanisms of toxicity arising from these agents. The zebrafish is the optimal whole organism model to screen for cardiotoxicity in a high throughput manner, while simultaneously assessing the role of cardiotoxicity pathways on the cancer therapy’s antitumor effect. Here we highlight established zebrafish models of human cardiovascular disease and cancer, the unique advantages of zebrafish to study mechanisms of cancer therapy-associated cardiovascular toxicity, and finally, important limitations to consider when using the zebrafish to study toxicity. Recent findings: Cancer therapy-associated cardiovascular toxicities range from cardiomyopathy with traditional agents to arrhythmias and thrombotic complications associated with newer targeted therapies. The zebrafish can be used to identify novel therapeutic strategies that selectively protect the heart from cancer therapy without affecting antitumor activity. Advances in genome editing technology have enabled the creation of several transgenic zebrafish lines valuable to the study of cardiovascular and cancer pathophysiology. Summary: The high degree of genetic conservation between zebrafish and humans, as well as the ability to recapitulate cardiotoxic phenotypes observed in patients with cancer, make the zebrafish an effective model to study cancer therapy-associated cardiovascular toxicity. Though this model provides several key benefits over existing in vitro and in vivo models, limitations of the zebrafish model include the early developmental stage required for most high-throughput applications. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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18 pages, 2075 KiB

Open AccessEditor’s ChoiceReview

Unlocking the Secrets of the Regenerating Fish Heart: Comparing Regenerative Models to Shed Light on Successful Regeneration

by Helen G. Potts, William T. Stockdale and Mathilda T. M. Mommersteeg

J. Cardiovasc. Dev. Dis. 2021, 8(1), 4; https://doi.org/10.3390/jcdd8010004 - 16 Jan 2021

Cited by 9 | Viewed by 6586

Abstract

The adult human heart cannot repair itself after injury and, instead, forms a permanent fibrotic scar that impairs cardiac function and can lead to incurable heart failure. The zebrafish, amongst other organisms, has been extensively studied for its innate capacity to repair its [...] Read more.

The adult human heart cannot repair itself after injury and, instead, forms a permanent fibrotic scar that impairs cardiac function and can lead to incurable heart failure. The zebrafish, amongst other organisms, has been extensively studied for its innate capacity to repair its heart after injury. Understanding the signals that govern successful regeneration in models such as the zebrafish will lead to the development of effective therapies that can stimulate endogenous repair in humans. To date, many studies have investigated cardiac regeneration using a reverse genetics candidate gene approach. However, this approach is limited in its ability to unbiasedly identify novel genes and signalling pathways that are essential to successful regeneration. In contrast, drawing comparisons between different models of regeneration enables unbiased screens to be performed, identifying signals that have not previously been linked to regeneration. Here, we will review in detail what has been learnt from the comparative approach, highlighting the techniques used and how these studies have influenced the field. We will also discuss what further comparisons would enhance our knowledge of successful regeneration and scarring. Finally, we focus on the Astyanax mexicanus, an intraspecies comparative fish model that holds great promise for revealing the secrets of the regenerating heart. Full article

(This article belongs to the Special Issue Zebrafish Heart Development, Regeneration, and Disease Modelling)

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