Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Heart Failure Reviews
Published in: Heart Failure Reviews 6/2016

01-11-2016

Zebrafish models of cardiovascular disease

Authors: Despina Bournele, Dimitris Beis

Published in: Heart Failure Reviews | Issue 6/2016

Login to get access

Abstract

Cardiovascular disease (CVD) is one of the leading causes of death worldwide. The most significant risk factors associated with the development of heart diseases include genetic and environmental factors such as hypertension, high blood cholesterol levels, diabetes, smoking, and obesity. Coronary artery disease accounts for the highest percentage of CVD deaths and stroke, cardiomyopathies, congenital heart diseases, heart valve defects and arrhythmias follow. The causes, prevention, and treatment of all forms of cardiovascular disease remain active fields of biomedical research, with hundreds of scientific studies published on a weekly basis. Generating animal models of cardiovascular diseases is the main approach used to understand the mechanism of pathogenesis and also design and test novel therapies. Here, we will focus on recent advances to finding the genetic cause and the molecular mechanisms of CVDs as well as novel drugs to treat them, using a small tropical freshwater fish native to Southeast Asia: the zebrafish (Danio rerio). Zebrafish emerged as a high-throughput but low-cost model organism that combines the advantages of forward and reverse genetics with phenotype-driven drug screenings. Noninvasive imaging allows in vivo analyses of cardiovascular phenotypes. Functional verification of candidate genes from genome-wide association studies has verified the role of several genes in the pathophysiology of CVDs. Also, zebrafish hearts maintain their ability to regenerate throughout their lifetime, providing novel insights to understand human cardiac regeneration.
Literature
1.
2.
Asakawa K, Kawakami K (2008) Targeted gene expression by the gal4-UAS system in zebrafish. Dev Growth Differ 50:391–399CrossRefPubMed
3.
Asimaki A, Kapoor S, Plovie E, Arndt K, Adams E, Liu Z, James C, Judge D, Calkins H, Churko J, Wu J, MacRae C, Kléber A, Saffitz J (2014) Identification of a new modulator of the intercalated disc in a zebrafish model of arrhythmogenic cardiomyopathy. Sci Trans Med 6:240ra74CrossRef
4.
Baker K, Warren K, Yellen G, Fishman M (1997) Defective “pacemaker” current (Ih) in a zebrafish mutant with a slow heart rate. Proc Natl Acad Sci USA 94:4554–4559CrossRefPubMedPubMedCentral
5.
Bamford RN, Roessler E, Burdine RD, Saplakoğlu U, De La Cruz J, Splitt M, Goodship JA, Towbin J, Bowers P, Ferrero GB, Marino B, Schier AF, Shen MM, Muenke M, Casey B (2000) Loss-of-function mutations in the EGF-CFC gene CFC1 are associated with human left-right laterality defects. Nat Genet 26:365–369CrossRefPubMed
6.
Barbazuk W, Korf I, Kadavi C, Heyen J, Tate S, Wun E, Bedell J, McPherson J, Johnson S (2000) The syntenic relationship of the zebrafish and human genomes. Genome Res 10:1351–1358CrossRefPubMedPubMedCentral
7.
Becker-Heck A, Zohn I, Okabe N, Pollock A, Lenhart K, Sullivan-Brown J, McSheene J, Loges N, Olbrich H, Haeffner K, Fliegauf M, Horvath J, Reinhardt R, Nielsen K, Marthin J, Baktai G, Anderson K, Geisler R, Niswander L, Omran H, Burdine R (2010) The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 43:79–84CrossRefPubMedPubMedCentral
8.
Becker T, Wullimann M, Becker C, Bernhardt R, Schachner M (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377:577–595CrossRefPubMed
9.
Beis D, Bartman T, Jin S, Scott I, D’Amico L, Ober E, Verkade H, Frantsve J, Field H, Wehman A, Baier H, Tallafuss A, Bally-Cuif L, Chen J, Stainier D, Jungblut B (2005) Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development. Development (Cambridge, England) 132:4193–4204CrossRef
10.
Beis D, Stainier D (2006) In vivo cell biology: following the zebrafish trend. Trends Cell Biol 16:105–112CrossRefPubMed
11.
Bögershausen N, Tsai I, Pohl E, Kiper P, Beleggia F, Percin E, Keupp K, Matchan A, Milz E, Alanay Y, Kayserili H, Liu Y, Banka S, Kranz A, Zenker M, Wieczorek D, Elcioglu N, Prontera P, Lyonnet S, Meitinger T, Stewart A, Donnai D, Strom T, Boduroglu K, Yigit G, Li Y, Katsanis N, Wollnik B (2015) RAP1-mediated MEK/ERK pathway defects in Kabuki syndrome. J Clin Investig 125:3585–3599CrossRefPubMedPubMedCentral
12.
Bonetti M, Paardekooper Overman J, Tessadori F, Noël E, Bakkers J, den Hertog J (2014) Noonan and LEOPARD syndrome Shp2 variants induce heart displacement defects in zebrafish. Development (Cambridge, England) 141:1961–1970CrossRef
13.
Boselli F, Vermot J (2015) Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart. Methods (San Diego, Calif) 94:129–134CrossRef
14.
Burns C, Milan D, Grande E, Rottbauer W, MacRae C, Fishman M (2006) High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat Chem Biol 1:263–264CrossRef
15.
16.
Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Nüsslein-Volhard C (1996) Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development (Cambridge, England) 123:293–302
17.
Chetaille P, Preuss C, Burkhard S, Côté JM, Houde C, Castilloux J, Piché J, Gosset N, Leclerc S, Wünnemann F, Thibeault M, Gagnon C, Galli A, Tuck E, Hickson GR, El Amine N, Boufaied I, Lemyre E, de Santa Barbara P, Faure S, Jonzon A, Cameron M, Dietz HC, Gallo-McFarlane E, Benson DW, Moreau C, Labuda D, FORGE Canada Consortium, Zhan SH, Shen Y, Jomphe M, Jones SJ, Bakkers J, Andelfinger G (2014) Mutations in SGOL1 cause a novel cohesinopathy affecting heart and gut rhythm. Nat Genet 46:1245–1249CrossRefPubMed
18.
Chi N, Shaw R, Jungblut B, Huisken J, Ferrer T, Arnaout R, Scott I, Beis D, Xiao T, Baier H, Jan L, Tristani-Firouzi M, Stainier D (2008) Genetic and physiologic dissection of the vertebrate cardiac conduction system. PLoS Biol 6(5):e109CrossRefPubMedPubMedCentral
19.
Choi W, Gemberling M, Wang J, Holdway J, Shen M, Karlstrom R, Poss K (2013) In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development (Cambridge, England) 140:660–666CrossRef
20.
Curado S, Anderson R, Jungblut B, Mumm J, Schroeter E, Stainier D (2007) Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn 236:1025–1035CrossRefPubMed
21.
Cutler C, Multani P, Robbins D, Kim HT, Le T, Hoggatt J, Pelus LM, Desponts C, Chen YB, Rezner B, Armand P, Koreth J, Glotzbecker B, Ho VT, Alyea E, Isom M, Kao G, Armant M, Silberstein L, Hu P, Soiffer RJ, Scadden DT, Ritz J, Goessling W, North TE, Mendlein J, Ballen K, Zon LI, Antin JH, Shoemaker DD (2013) Prostaglandin-modulated umbilical cord blood hematopoietic stem cell transplantation. Blood 122:3074–3081CrossRefPubMedPubMedCentral
22.
Davis E, Zhang Q, Liu Q, Diplas B, Davey L, Hartley J, Stoetzel C, Szymanska K, Ramaswami G, Logan C, Muzny D, Young A, Wheeler D, Cruz P, Morgan M, Lewis L, Cherukuri P, Maskeri B, Hansen N, Mullikin J, Blakesley R, Bouffard G, Comparative N, Gyapay G, Rieger S, Tönshoff B, Kern I, Soliman N, Neuhaus T, Swoboda K, Kayserili H, Gallagher T, Lewis R, Bergmann C, Otto E, Saunier S, Scambler P, Beales P, Gleeson J, Maher E, Attié-Bitach T, Dollfus H, Johnson C, Green E, Gibbs R, Hildebrandt F, Pierce E, Katsanis N (2011) TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum. Nat Genet 43:189–196CrossRefPubMedPubMedCentral
23.
Davison J, Akitake C, Goll M, Rhee J, Gosse N, Baier H, Halpern M, Leach S, Parsons M (2007) Transactivation from gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol 304:811–824CrossRefPubMedPubMedCentral
24.
Di Donato V, De Santis F, Auer T, Testa N, Sánchez-Iranzo H, Mercader N, Concordet JP, Del Bene F (2016) 2C-Cas9: a versatile tool for clonal analysis of gene function. Genome Res 26:681–692CrossRefPubMed
25.
Dina C, Bouatia-Naji N, Tucker N, Delling FN, Toomer K, Durst R, Perrocheau M, Fernandez-Friera L, Solis J, Le Tourneau T, Chen M-H, Probst V, Bosse Y, Pibarot P, Zelenika D, Lathrop M, Hercberg S, Roussel R, Benjamin EJ, Bonnet F, Lo SH, Dolmatova E, Simonet F, Lecointe S, Kyndt F, Redon R, Le Marec H, Froguel P, Ellinor PT, Vasan RS, Bruneval P, Markwald RR, Norris RA, Milan DJ, Slaugenhaupt SA, Levine RA, Schott J-J, Hagege AA, France MVP, Jeunemaitre X (2015) Genetic association analyses highlight biological pathways underlying mitral valve prolapse. Nat Genet 47:1206–1211CrossRefPubMedPubMedCentral
26.
Driever W, Solnica-Krezel L, Schier A, Neuhauss S, Malicki J, Stemple D, Stainier D, Zwartkruis F, Abdelilah S, Rangini Z, Belak J, Boggs C (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development (Cambridge, England) 123:37–46
27.
Eisen J, Smith J (2008) Controlling morpholino experiments: don’t stop making antisense. Development (Cambridge, England) 135:1735–1743CrossRef
28.
Fisher S, Grice E, Vinton R, Bessling S, McCallion A (2006) Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science (New York, NY) 312:276–279CrossRef
29.
Frangogiannis N (2006) The mechanistic basis of infarct healing. Antioxid Redox Signal 8:1907–1939CrossRefPubMed
30.
González-Rosa J, Martín V, Peralta M, Torres M, Mercader N (2011) Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development (Cambridge, England) 138:1663–1674CrossRef
31.
Haack T, Abdelilah-Seyfried S (2016) The force within: endocardial development, mechanotransduction and signalling during cardiac morphogenesis. Development (Cambridge, England) 143:373–386CrossRef
32.
Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang Y, Heisenberg CP, Kelsh RN, Furutani-Seiki M, Vogelsang E, Beuchle D, Schach U, Fabian C, Nüsslein-Volhard C (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development (Cambridge, England) 123:1–36
33.
Hoffman J, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39:1890–1900CrossRefPubMed
34.
Hwang W, Fu Y, Reyon D, Maeder M, Tsai S, Sander J, Peterson R, Yeh J, Joung J (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31:227–229CrossRefPubMedPubMedCentral
35.
Hyde AS, Farmer EL, Easley KE, van Lammeren K, Christoffels VM, Barycki JJ, Bakkers J, Simpson MA (2012) UDP-glucose dehydrogenase polymorphisms from patients with congenital heart valve defects disrupt enzyme stability and quaternary assembly. J Biol Chem 287:32708–32716CrossRefPubMedPubMedCentral
36.
Itou J, Oishi I, Kawakami H, Glass T, Richter J, Johnson A, Lund T (2012) Migration of cardiomyocytes is essential for heart regeneration in zebrafish. Development (Cambridge, England) 139:4133–4142CrossRef
37.
Jin S, Herzog W, Santoro M, Mitchell T, Frantsve J, Jungblut B, Beis D, Scott I, D’Amico L, Ober E, Verkade H, Field H, Chi N, Wehman A, Baier H, Stainier D (2007) A transgene-assisted genetic screen identifies essential regulators of vascular development in vertebrate embryos. Dev Biol 307:29–42CrossRefPubMedPubMedCentral
38.
Jopling C, Sleep E, Raya M, Martí M, Belmonte I (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464:606–609CrossRefPubMedPubMedCentral
39.
Kalogirou S, Malissovas N, Moro E, Argenton F, Stainier D, Beis D (2014) Intracardiac flow dynamics regulate atrioventricular valve morphogenesis. Cardiovasc Res 104:49–60CrossRefPubMedPubMedCentral
40.
41.
Kennedy MP, Omran H, Leigh MW, Dell S, Morgan L, Molina PL, Robinson BV, Minnix SL, Olbrich H, Severin T, Ahrens P, Lange L, Morillas HN, Noone PG, Zariwala MA, Knowles MR (2007) Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia. Circulation 115:2814–2821CrossRefPubMed
42.
Kikuchi K, Holdway J, Major R, Blum N, Dahn R, Begemann G, Poss K (2011) Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell 20:397–404CrossRefPubMedPubMedCentral
43.
Kikuchi K, Holdway J, Werdich A, Anderson R, Fang Y, Egnaczyk G, Evans T, Macrae C, Stainier D, Poss K (2010) Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464:601–605CrossRefPubMedPubMedCentral
44.
Kim J, Wu Q, Zhang Y, Wiens K, Huang Y, Rubin N, Shimada H, Handin R, Chao M, Tuan T, Starnes V, Lien C (2010) PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci USA 107:17206–17210CrossRefPubMedPubMedCentral
45.
Kodo K, Nishizawa T, Furutani M, Arai S, Ishihara K, Oda M, Makino S, Fukuda K, Takahashi T, Matsuoka R, Nakanishi T, Yamagishi H (2012) Genetic analysis of essential cardiac transcription factors in 256 patients with non-syndromic congenital heart defects. Circ J 76:1703–1711CrossRefPubMed
46.
Konantz M, Balci T, Hartwig U, Dellaire G, André M, Berman J, Lengerke C (2012) Zebrafish xenografts as a tool for in vivo studies on human cancer. Ann N Y Acad Sci 1266:124–137CrossRefPubMed
47.
Kroehne V, Freudenreich D, Hans S, Kaslin J, Brand M (2011) Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Development (Cambridge, England) 138:4831–4841CrossRef
48.
Lam S, Wu Y, Vega V, Miller L, Spitsbergen J, Tong Y, Zhan H, Govindarajan K, Lee S, Mathavan S, Murthy K, Buhler Liu E, Gong Z (2005) Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat Biotechnol 24:73–75CrossRefPubMed
49.
Langheinrich U, Vacun G, Wagner T (2003) Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol Appl Pharmacol 193:370–382CrossRefPubMed
50.
Lepilina A, Coon A, Kikuchi K, Holdway J, Roberts R, Burns C, Poss K (2006) A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127:607–619CrossRefPubMed
51.
Lessman C (2011) The developing zebrafish (Danio rerio): a vertebrate model for high-throughput screening of chemical libraries. Birth Defects Res Part C Embryo Today Rev 93:268–280CrossRef
52.
Loges N, Olbrich H, Becker-Heck A, Häffner K, Heer A, Reinhard C, Schmidts M, Kispert A, Zariwala M, Leigh M, Knowles Zentgraf H, Seithe H, Nürnberg G, Reinhardt R, Omran H (2009) Deletions and point mutations of LRRC50 cause primary ciliary dyskinesia due to dynein arm defects. Am J Hum Genet 85:883–889CrossRefPubMedPubMedCentral
53.
54.
Mellman K, Huisken J, Dinsmore C, Hoppe C, Stainier D (2012) Fibrillin-2b regulates endocardial morphogenesis in zebrafish. Dev Biol 372:111–119CrossRefPubMed
55.
Milan D, Peterson T, Ruskin J, Peterson R, MacRae C (2003) Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation 107:1355–1358CrossRefPubMed
56.
Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, O’Callaghan C, Blau H, Al Dabbagh M, Olbrich H, Beales PL, Yagi T, Mussaffi H, Chung EM, Omran H, Mitchell DR (2012) Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet 44:381–389CrossRefPubMedPubMedCentral
57.
Nasevicius A, Ekker S (2000) Effective targeted gene “knockdown” in zebrafish. Nat Genet 26:216–220CrossRefPubMed
58.
Noël E, Momenah T, Al-Dagriri K, Al-Suwaid A, Al-Shahrani S, Jiang H, Willekers S, Oostveen Y, Chocron S, Postma A, Bhuiyan Z, Bakkers J (2015) A Zebrafish loss-of-function model for human CFAP53 mutations reveals its specific role in Laterality organ function. Hum Mutat 37:194–200CrossRefPubMed
59.
North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang IH, Grosser T, Fitzgerald GA, Daley GQ, Orkin SH, Zon LI (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447:1007–1011CrossRefPubMedPubMedCentral
60.
Orr N, Arnaout R, Gula L, Spears D, Leong-Sit P, Li Q, Tarhuni W, Reischauer S, Chauhan V, Borkovich M, Uppal S, Adler A, Coughlin S, Stainier D, Gollob M (2016) A mutation in the atrial-specific myosin light chain gene (MYL4) causes familial atrial fibrillation. Nat Commun 7:11303CrossRefPubMedPubMedCentral
61.
Paige S, Thomas S, Stoick-Cooper C, Wang H, Maves L, Sandstrom R, Pabon L, Reinecke H, Pratt G, Keller G, Moon R, Stamatoyannopoulos J, Murry C (2012) A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 151:221–232CrossRefPubMedPubMedCentral
62.
Papakyriakou A, Kefalos P, Sarantis P, Tsiamantas C, Xanthopoulos K, Vourloumis D, Beis D (2014) A zebrafish in vivo phenotypic assay to identify 3-aminothiophene-2-carboxylic acid-based angiogenesis inhibitors. Assay Drug Dev Technol 12:527–535CrossRefPubMedPubMedCentral
63.
Pelster B, Burggren W (1996) Disruption of hemoglobin oxygen transport does not impact oxygen-dependent physiological processes in developing embryos of zebra fish (Danio rerio). Circ Res 79:358–362CrossRefPubMed
64.
Peterson R, Link B, Dowling J, Schreiber S (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci USA 97:12965–12969CrossRefPubMedPubMedCentral
65.
Peterson R, Macrae C (2011) Systematic approaches to toxicology in the zebrafish. Annu Rev Pharmacol Toxicol 52:433–453CrossRefPubMed
66.
Peterson R, Shaw S, Peterson T, Milan D, Zhong T, Schreiber S, MacRae C, Fishman M (2004) Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol 22:595–599CrossRefPubMed
67.
Porrello E, Mahmoud A, Simpson E, Hill J, Richardson J, Olson E, Sadek H (2011) Transient regenerative potential of the neonatal mouse heart. Science (New York, NY) 331:1078–1080CrossRef
68.
69.
Poss K, Wilson L, Keating M (2002) Heart regeneration in zebrafish. Science (New York, NY) 298:2188–2190CrossRef
70.
Postlethwait J, Yan Y, Gates M, Horne S, Amores A, Brownlie A, Donovan A, Egan E, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw B, Ransom D, Singer A, Thomson M, Abduljabbar T, Yelick P, Beier D, Joly J, Larhammar D, Rosa F, Westerfield M, Zon L, Johnson S, Talbot W (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Genet 18:345–349CrossRefPubMed
71.
Ramspacher C, Steed E, Boselli F, Ferreira R, Faggianelli N, Roth S, Spiegelhalter C, Messaddeq N, Trinh L, Liebling M, Chacko N, Tessadori F, Bakkers J, Laporte J, Hnia K, Vermot J (2015) Developmental alterations in heart Biomechanics and skeletal muscle function in desmin mutants suggest an early pathological root for desminopathies. Cell reports 11:1564–1576CrossRefPubMed
72.
Renz M, Otten C, Faurobert E, Rudolph F, Zhu Y, Boulday G, Duchene J, Mickoleit M, Dietrich A, Ramspacher C, Steed E, Manet-Dupé S, Benz A, Hassel D, Vermot J, Huisken J, Tournier-Lasserve E, Felbor U, Sure U, Albiges-Rizo C, Abdelilah-Seyfried S (2015) Regulation of β1 integrin-klf2-mediated angiogenesis by CCM proteins. Dev Cell 32:181–190CrossRefPubMed
73.
Rossi A, Kontarakis Z, Gerri C, Nolte H, Hölper S, Krüger M, Stainier D (2015) Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524:230–233CrossRefPubMed
74.
Santoro M (2014) Antiangiogenic cancer drug using the zebrafish model. Arterioscler Thromb Vasc Biol 34:1846–1853CrossRefPubMed
75.
Schnabel K, Wu C, Kurth T, Weidinger G (2011) Regeneration of cryoinjury induced necrotic heart lesions in zebrafish is associated with epicardial activation and cardiomyocyte proliferation. PLoS One 6:e18503CrossRefPubMedPubMedCentral
76.
Schulte E, Kousi M, Tan P, Tilch E, Knauf F, Lichtner P, Trenkwalder C, Högl B, Frauscher B, Berger K, Fietze I, Hornyak M, Oertel W, Bachmann C, Zimprich A, Peters A, Gieger C, Meitinger T, Müller-Myhsok B, Katsanis N, Winkelmann J (2014) Targeted resequencing and systematic in vivo functional testing identifies rare variants in MEIS1 as significant contributors to restless legs syndrome. Am J Hum Genet 95:85–95CrossRefPubMedPubMedCentral
77.
Schulte-Merker S, Stainier D (2014) Out with the old, in with the new: reassessing morpholino knockdowns in light of genome editing technology. Development (Cambridge, England) 141:3103–3104CrossRef
78.
Sehnert A, Huq A, Weinstein B, Walker C, Fishman M, Stainier D (2002) Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat Genet 31:106–110CrossRefPubMed
79.
Smith KA, Joziasse IC, Chocron S, van Dinther M, Guryev V, Verhoeven MC, Rehmann H, der van Smagt JJ, Doevendans PA, Cuppen E, Mulder BJ, Ten Dijke P, Bakkers J (2009) Dominant-negative ALK2 allele associates with congenital heart defects. Circulation 119:3062–3069CrossRefPubMed
80.
Stainier D, Fouquet B, Chen J, Warren K, Weinstein B, Meiler S, Mohideen M, Neuhauss S, Solnica-Krezel L, Schier A, Zwartkruis F, Stemple D, Malicki J, Driever W, Fishman M (1996) Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development (Cambridge, England) 123:285–292
81.
82.
Szeto D, Griffin K, Kimelman D (2002) HrT is required for cardiovascular development in zebrafish. Development (Cambridge, England) 129:5093–5101
83.
Tran T, Sneed B, Haider J, Blavo D, White A, Aiyejorun T, Baranowski T, Rubinstein A, Doan T, Dingledine R, Sandberg E (2007) Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Res 67:11386–11392CrossRefPubMed
84.
Vihtelic TS, Hyde DR (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44:289–307CrossRefPubMed
85.
86.
Wang J, Panáková D, Kikuchi K, Holdway JE, Gemberling M, Burris JS, Singh SP, Dickson AL, Lin Y-F, Sabeh KM, Werdich AA, Yelon D, MacRae CA, Poss KD (2011) The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138:3421–3430CrossRefPubMedPubMedCentral
87.
Wang X, Yu Q, Wu Q, Bu Y, Chang N, Yan S, Zhou X, Zhu X, Xiong J (2013) Genetic interaction between pku300 and fbn2b controls endocardial cell proliferation and valve development in zebrafish. J Cell Sci 126:1381–1391CrossRefPubMedPubMedCentral
88.
White R, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, Bourque C, Dovey M, Goessling W, Burns C, Zon L (2008) Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2:183–189CrossRefPubMedPubMedCentral
89.
Wu CC, Kruse F, Vasudevarao MD, Junker JP, Zebrowski DC, Fischer K, Noël ES, Grün D, Berezikov E, Engel FB, van Oudenaarden A, Weidinger G, Bakkers J (2016) Spatially resolved genome-wide transcriptional profiling identifies BMP signaling as essential regulator of zebrafish cardiomyocyte regeneration. Dev Cell 36:36–49CrossRefPubMed
90.
91.
Zareba W, Cygankiewicz I (2008) Long QT syndrome and short QT syndrome. Prog Cardiovasc Dis 51:264–278CrossRefPubMed
92.
Zebrowski D, Becker R, Engel F (2016) Towards regenerating the mammalian heart: challenges in evaluating experimentally induced adult mammalian cardiomyocyte proliferation. Am J Physiol Heart Circ Physiol 310(9):H1045–H1054CrossRefPubMed
93.
Zebrowski D, Vergarajauregui S, Wu C, Piatkowski T, Becker R, Leone M, Hirth S, Ricciardi F, Falk N, Giessl A, Just S, Braun T, Weidinger G, Engel F (2015) Developmental alterations in centrosome integrity contribute to the post-mitotic state of mammalian cardiomyocytes. Elife. doi:10.​7554/​eLife.​05563 PubMedPubMedCentral
94.
Zhao L, Borikova A, Ben-Yair R, Guner-Ataman B, MacRae C, Lee R, Burns C (2014) Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci USA 111:1403–1408CrossRefPubMedPubMedCentral
Metadata
Title
Zebrafish models of cardiovascular disease
Authors
Despina Bournele
Dimitris Beis
Publication date
01-11-2016
Publisher
Springer US
Published in
Heart Failure Reviews / Issue 6/2016
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI
https://doi.org/10.1007/s10741-016-9579-y

Other articles of this Issue 6/2016

Heart Failure Reviews 6/2016 Go to the issue

ReviewPaper

New strategies for improving stem cell therapy in ischemic heart disease

OriginalPaper

Myocardial transcription factors in diastolic dysfunction: clues for model systems and disease

OriginalPaper

Cognitive decline in heart failure

OriginalPaper

Personalised computational cardiology: Patient-specific modelling in cardiac mechanics and biomaterial injection therapies for myocardial infarction

OriginalPaper

Cardiac contractility modulation: a novel approach for the treatment of heart failure

OriginalPaper

Stem cells and diabetic cardiomyopathy: from pathology to therapy

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits