Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages

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JOURNAL ARTICLES

Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages

DY Stainier, BM Weinstein, HW Detrich, LI Zon and MC Fishman
Cardiovascular Research Center, Massachusetts General Hospital, Charlestown 02129, USA.

Endothelial and hematopoietic cells appear synchronously on the extra-embryonic membranes of amniotes in structures known as blood islands. This observation has led to the suggestion that these two ventral lineages share a common progenitor. Recently, we have shown in the zebrafish, Danio rerio, that a single cell in the ventral marginal zone of the early blastula can give rise to both endothelial and blood cells as well as to other mesodermal cells (Stainier, D. Y. R., Lee, R. K. and Fishman, M. C. (1993). Development 119, 31-40; Lee, R. K. K., Stainier, D. Y. R., Weinstein, B. M. and Fishman, M. C. (1994). Development 120, 3361-3366). Here we describe a zebrafish mutation, cloche, that affects both the endothelial and hematopoietic lineages at a very early stage. The endocardium, the endothelial lining of the heart, is missing in mutant embryos. This deletion is selective as evidenced by the presence of other endothelial cells, for example those lining the main vessels of the trunk. Early cardiac morphogenesis proceeds normally even in the absence of the endocardium. The myocardial cells form a tube that is demarcated into chambers, beats rhythmically, but exhibits a reduced contractility. This functional deficit is likely due to the absence of the endocardial cells, although it may be a direct effect of the mutation on the myocardial cells. Cell transplantation studies reveal that the endothelial defect, i.e. the endocardial deletion, is a cell-autonomous lesion, consistent with the possibility that cloche is part of a signal transduction pathway. In addition, the number of blood cells is greatly reduced in cloche mutants and the hematopoietic tissues show no expression of GATA-1 or GATA-2, two key hematopoietic transcription factors that are first expressed during early embryogenesis. These results show that cloche is involved in the genesis and early diversification of the endothelial and blood lineages, possibly by affecting a common progenitor cell population.

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				M. Gering, Y. Yamada, T. H. Rabbitts, and R. K. Patient Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1 Development, December 22, 2003; 130(25): 6187 - 6199. [Abstract] [Full Text] [PDF]

				M. Walmsley, A. Ciau-Uitz, and R. Patient Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus Development, March 14, 2003; 129(24): 5683 - 5695. [Abstract] [Full Text] [PDF]

				M. L. Kalev-Zylinska, J. A. Horsfield, M. V. C. Flores, J. H. Postlethwait, M. R. Vitas, A. M. Baas, P. S. Crosier, and K. E. Crosier Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis Development, March 6, 2003; 129(8): 2015 - 2030. [Abstract] [Full Text] [PDF]

				S. Childs, J.-N. Chen, D. M. Garrity, and M. C. Fishman Patterning of angiogenesis in the zebrafish embryo Development, March 4, 2003; 129(4): 973 - 982. [Abstract] [Full Text] [PDF]

				D. L. Brutsaert Cardiac Endothelial-Myocardial Signaling: Its Role in Cardiac Growth, Contractile Performance, and Rhythmicity Physiol Rev, January 1, 2003; 83(1): 59 - 115. [Abstract] [Full Text] [PDF]

				J. M. Spitsbergen and M. L. Kent The State of the Art of the Zebrafish Model for Toxicology and Toxicologic Pathology Research--Advantages and Current Limitations Toxicol Pathol, January 1, 2003; 31(1_suppl): 62 - 87. [Abstract] [PDF]

				S. J. Pratt, A. Drejer, H. Foott, B. Barut, A. Brownlie, J. Postlethwait, Y. Kato, M. Yamamoto, and L. I. Zon Isolation and characterization of zebrafish NFE2 Physiol Genomics, October 29, 2002; 11(2): 91 - 98. [Abstract] [Full Text] [PDF]