Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo

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Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo

DY Stainier, B Fouquet, JN Chen, KS Warren, BM Weinstein, SE Meiler, MA Mohideen, SC Neuhauss, L Solnica-Krezel, AF Schier, F Zwartkruis, DL Stemple, J Malicki, W Driever and MC Fishman
Cardiovascular Research Center, Massachusetts General Hospital, Charlestown 02129, USA.

As part of a large-scale mutagenesis screen of the zebrafish genome, we have identified 58 mutations that affect the formation and function of the cardiovascular system. The cardiovascular system is particularly amenable for screening in the transparent zebrafish embryo because the heart and blood vessels are prominent and their function easily examined. We have classified the mutations affecting the heart into those that affect primarily either morphogenesis or function. Nine mutations clearly disrupt the formation of the heart. cloche deletes the endocardium. In cloche mutants, the myocardial layer forms in the absence of the endocardium but is dysmorphic and exhibits a weak contractility. Two loci, miles apart and bonnie and clyde, play a critical role in the fusion of the bilateral tubular primordia. Three mutations lead to an abnormally large heart and one to the formation of a diminutive, dysmorphic heart. We have found no mutation that deletes the myocardial cells altogether, but one, pandora, appears to eliminate the ventricle selectively. Seven mutations interfere with vascular integrity, as indicated by hemorrhage at particular sites. In terms of cardiac function, one large group exhibits a weak beat. In this group, five loci affect both chambers and seven a specific chamber (the atrium or ventricle). For example, the weak atrium mutation exhibits an atrium that becomes silent but has a normally beating ventricle. Seven mutations affect the rhythm of the heart causing, for example, a slow rate, a fibrillating pattern or an apparent block to conduction. In several other mutants, regurgitation of blood flow from ventricle to atrium is the most prominent abnormality, due either to the absence of valves or to poor coordination between the chambers with regard to the timing of contraction. The mutations identified in this screen point to discrete and critical steps in the formation and function of the heart and vasculature.
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				B. Meder, C. Laufer, D. Hassel, S. Just, S. Marquart, B. Vogel, A. Hess, M. C. Fishman, H. A. Katus, and W. Rottbauer A Single Serine in the Carboxyl Terminus of Cardiac Essential Myosin Light Chain-1 Controls Cardiomyocyte Contractility In Vivo Circ. Res., March 13, 2009; 104(5): 650 - 659. [Abstract] [Full Text] [PDF]

				A. Bukrinsky, K. J. P. Griffin, Y. Zhao, S. Lin, and U. Banerjee Essential role of spi-1-like (spi-1l) in zebrafish myeloid cell differentiation Blood, February 26, 2009; 113(9): 2038 - 2046. [Abstract] [Full Text] [PDF]

				W. Mu, W. Wang, and J. C. Schimenti An Allelic Series Uncovers Novel Roles of the BRCT Domain-Containing Protein PTIP in Mouse Embryonic Vascular Development Mol. Cell. Biol., October 15, 2008; 28(20): 6439 - 6451. [Abstract] [Full Text] [PDF]

				V. Mehta, R. E. Peterson, and W. Heideman 2,3,7,8-Tetrachlorodibenzo-p-dioxin Exposure Prevents Cardiac Valve Formation in Developing Zebrafish Toxicol. Sci., August 1, 2008; 104(2): 303 - 311. [Abstract] [Full Text] [PDF]

				M. Yamashita, N. Mizusawa, M. Hojo, and T. Yabu Extensive apoptosis and abnormal morphogenesis in pro-caspase-3 transgenic zebrafish during development J. Exp. Biol., June 15, 2008; 211(12): 1874 - 1881. [Abstract] [Full Text] [PDF]

				J.-W. Xiong, Q. Yu, J. Zhang, and J. D. Mably An Acyltransferase Controls the Generation of Hematopoietic and Endothelial Lineages in Zebrafish Circ. Res., May 9, 2008; 102(9): 1057 - 1064. [Abstract] [Full Text] [PDF]

				N. Sultana, K. Nag, K. Hoshijima, D. W. Laird, A. Kawakami, and S. Hirose Zebrafish early cardiac connexin, Cx36.7/Ecx, regulates myofibril orientation and heart morphogenesis by establishing Nkx2.5 expression PNAS, March 25, 2008; 105(12): 4763 - 4768. [Abstract] [Full Text] [PDF]

				D. Hassel, E. P. Scholz, N. Trano, O. Friedrich, S. Just, B. Meder, D. L. Weiss, E. Zitron, S. Marquart, B. Vogel, et al. Deficient Zebrafish Ether-a-Go-Go-Related Gene Channel Gating Causes Short-QT Syndrome in Zebrafish Reggae Mutants Circulation, February 19, 2008; 117(7): 866 - 875. [Abstract] [Full Text] [PDF]

				C. V. Esguerra, L. Nelles, L. Vermeire, A. Ibrahimi, A. D. Crawford, R. Derua, E. Janssens, E. Waelkens, P. Carmeliet, D. Collen, et al. Ttrap is an essential modulator of Smad3-dependent Nodal signaling during zebrafish gastrulation and left-right axis determination Development, December 15, 2007; 134(24): 4381 - 4393. [Abstract] [Full Text] [PDF]

				C. Wang, P. W. Faloon, Z. Tan, Y. Lv, P. Zhang, Y. Ge, H. Deng, and J.-W. Xiong Mouse lysocardiolipin acyltransferase controls the development of hematopoietic and endothelial lineages during in vitro embryonic stem-cell differentiation Blood, November 15, 2007; 110(10): 3601 - 3609. [Abstract] [Full Text] [PDF]

				J. Liu, S. D. Fraser, P. W. Faloon, E. L. Rollins, J. Vom Berg, O. Starovic-Subota, A. L. Laliberte, J.-N. Chen, F. C. Serluca, and S. J. Childs A betaPix Pak2a signaling pathway regulates cerebral vascular stability in zebrafish PNAS, August 28, 2007; 104(35): 13990 - 13995. [Abstract] [Full Text] [PDF]

				D. A. Buchner, F. Su, J. S. Yamaoka, M. Kamei, J. A. Shavit, L. K. Barthel, B. McGee, J. D. Amigo, S. Kim, A. W. Hanosh, et al. From the Cover: pak2a mutations cause cerebral hemorrhage in redhead zebrafish PNAS, August 28, 2007; 104(35): 13996 - 14001. [Abstract] [Full Text] [PDF]

				R. Knoll, R. Postel, J. Wang, R. Kratzner, G. Hennecke, A. M. Vacaru, P. Vakeel, C. Schubert, K. Murthy, B. K. Rana, et al. Laminin-{alpha}4 and Integrin-Linked Kinase Mutations Cause Human Cardiomyopathy Via Simultaneous Defects in Cardiomyocytes and Endothelial Cells Circulation, July 31, 2007; 116(5): 515 - 525. [Abstract] [Full Text] [PDF]

				R. Arnaout, T. Ferrer, J. Huisken, K. Spitzer, D. Y. R. Stainier, M. Tristani-Firouzi, and N. C. Chi Zebrafish model for human long QT syndrome PNAS, July 3, 2007; 104(27): 11316 - 11321. [Abstract] [Full Text] [PDF]

				Y.-X. Wang, L.-X. Qian, D. Liu, L.-L. Yao, Q. Jiang, Z. Yu, Y.-H. Gui, T. P. Zhong, and H.-Y. Song Bone morphogenetic protein-2 acts upstream of myocyte-specific enhancer factor 2a to control embryonic cardiac contractility Cardiovasc Res, May 1, 2007; 74(2): 290 - 303. [Abstract] [Full Text] [PDF]

				T. Sakaguchi, Y. Kikuchi, A. Kuroiwa, H. Takeda, and D. Y. R. Stainier The yolk syncytial layer regulates myocardial migration by influencing extracellular matrix assembly in zebrafish Development, October 15, 2006; 133(20): 4063 - 4072. [Abstract] [Full Text] [PDF]

				E. E. Hamm, D. E. Voth, and J. D. Ballard Identification of Clostridium difficile toxin B cardiotoxicity using a zebrafish embryo model of intoxication PNAS, September 19, 2006; 103(38): 14176 - 14181. [Abstract] [Full Text] [PDF]

				G. Bendig, M. Grimmler, I. G. Huttner, G. Wessels, T. Dahme, S. Just, N. Trano, H. A. Katus, M. C. Fishman, and W. Rottbauer Integrin-linked kinase, a novel component of the cardiac mechanical stretch sensor, controls contractility in the zebrafish heart Genes & Dev., September 1, 2006; 20(17): 2361 - 2372. [Abstract] [Full Text] [PDF]

				J. D. Mably, L. P. Chuang, F. C. Serluca, M.-A. P. K. Mohideen, J.-N. Chen, and M. C. Fishman santa and valentine pattern concentric growth of cardiac myocardium in the zebrafish Development, August 15, 2006; 133(16): 3139 - 3146. [Abstract] [Full Text] [PDF]

				W. Rottbauer, G. Wessels, T. Dahme, S. Just, N. Trano, D. Hassel, C. G. Burns, H. A. Katus, and M. C. Fishman Cardiac Myosin Light Chain-2: A Novel Essential Component of Thick-Myofilament Assembly and Contractility of the Heart Circ. Res., August 4, 2006; 99(3): 323 - 331. [Abstract] [Full Text] [PDF]

				D. J. Milan, A. C. Giokas, F. C. Serluca, R. T. Peterson, and C. A. MacRae Notch1b and neuregulin are required for specification of central cardiac conduction tissue Development, March 15, 2006; 133(6): 1125 - 1132. [Abstract] [Full Text] [PDF]

				F. C. Serluca and M. C. Fishman Big, bad hearts: From flies to man. PNAS, March 14, 2006; 103(11): 3947 - 3948. [Full Text] [PDF]

				A. D. Langenbacher, Y. Dong, X. Shu, J. Choi, D. A. Nicoll, J. I. Goldhaber, K. D. Philipson, and J.-N. Chen Mutation in sodium-calcium exchanger 1 (NCX1) causes cardiac fibrillation in zebrafish PNAS, December 6, 2005; 102(49): 17699 - 17704. [Abstract] [Full Text] [PDF]

				H. Roest Crollius and J. Weissenbach Fish genomics and biology Genome Res., December 1, 2005; 15(12): 1675 - 1682. [Abstract] [Full Text] [PDF]

				S.-W. Jin, D. Beis, T. Mitchell, J.-N. Chen, and D. Y. R. Stainier Cellular and molecular analyses of vascular tube and lumen formation in zebrafish Development, December 1, 2005; 132(23): 5199 - 5209. [Abstract] [Full Text] [PDF]

				J.E. Ferguson III, R. W. Kelley, and C. Patterson Mechanisms of Endothelial Differentiation in Embryonic Vasculogenesis Arterioscler Thromb Vasc Biol, November 1, 2005; 25(11): 2246 - 2254. [Abstract] [Full Text] [PDF]

				D. Beis, T. Bartman, S.-W. Jin, I. C. Scott, L. A. D'Amico, E. A. Ober, H. Verkade, J. Frantsve, H. A. Field, A. Wehman, et al. Genetic and cellular analyses of zebrafish atrioventricular cushion and valve development Development, September 15, 2005; 132(18): 4193 - 4204. [Abstract] [Full Text] [PDF]

				S. Sumanas, T. Jorniak, and S. Lin Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants Blood, July 15, 2005; 106(2): 534 - 541. [Abstract] [Full Text] [PDF]