Abstract
Blood circulation is essential for the maintenance of life. It starts from the early embryonic stage and continues throughout the entire lifetime. However, it remains unclear how the circulation of blood starts in early development. This chapter introduces an active mechanism involving the primitive erythroblasts for the onset of blood circulation by monitoring fluorescently labeled blood precursors and blood vessels in transgenic zebrafish. The earliest erythroblasts are generated in the extravascular region and enter into the vascular tube by interacting with the endothelial cells. They continue to adhere to the vascular lumen and are not released into the bloodstream soon after the invasion. ADAM8, a membrane-bound metalloprotease expressed in the erythroblasts, mediates the onset of blood circulation by an abrogation of blood–vessel contact. In adam8-depleted embryos, the erythroid cells fail to detach from the vascular lumen and stagnate. Biochemical assay indicates that ADAM8 is an active protease that cleaves the membrane-anchored cell adhesion molecules such as PSGL-1. These findings suggest that the primitive erythroblasts have a cell autonomous function in regulating the timing of the onset of blood circulation.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Arribas J, Coodly L, Vollmer P et al (1996) Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J Biol Chem 271:11376–11382
Bertrand JY, Chi NC, Santoso B et al (2010) Haematopoietic stem cells derive directly from aortic endothelium during development. Nature (Lond) 464:108–111
Boisset JC, van Cappellen W, Andrieu-Soler C et al (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature (Lond) 464:116–120
Davidson AJ, Zon LI (2004) The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis. Oncogene 23:7233–7246
De Luca M, Dunlop LC, Andrews RK (1995) A novel cobra venom metalloproteinase, mocarhagin, cleaves a 10-amino acid peptide from the mature N terminus of P-selectin glycoprotein ligand receptor, PSGL-1, and abolishes P-selectin binding. J Biol Chem 270:26734–26737
Edwards DR, Handsley MM, Pennington CJ (2008) The ADAM metalloproteinases. Mol Aspects Med 29:258–289
Gómez-Gaviro M, Domínguez-Luis M, Canchado J et al (2007) Expression and regulation of the metalloproteinase ADAM-8 during human neutrophil pathophysiological activation and its catalytic activity on L-selectin shedding. J Immunol 178:8053–8063
Herbert SP, Huisken J, Kim TN et al (2009) Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 326:294–298
Iida A, Sakaguchi K, Sato K et al (2010) Metalloprotease-dependent onset of blood circulation in zebrafish. Curr Biol 20:1110–1116
Jin SW, Beis D, Mitchell T et al (2005) Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development (Camb) 132:5199–209
Jones EA, Crotty D, Kulesa PM et al (2002) Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture. Genesis 34:228–235
Kelly K, Hutchinson G, Nebenius-Oosthuizen D et al (2005) Metalloprotease-disintegrin ADAM8: expression analysis and targeted deletion in mice. Dev Dyn 232:221–231
Kissa K, Herbomel P (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature (Lond) 464:112–115
Kitaguchi T, Kawakami K, Kawahara A (2009) Transcriptional regulation of a myeloid-lineage specific gene lysozyme C during zebrafish myelopoiesis. Mech Dev 126:314–323
Kumar A, Villani MP, Patel UK et al (1999) Recombinant soluble form of PSGL-1 accelerates thrombolysis and prevents reocclusion in a porcine model. Circulation 99:1363–136
Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318
Ley K, Laudanna C, Cybulsky MI et al (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678–689
Lichtenthaler SF, Dominguez DI, Westmeyer GG et al (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J Biol Chem 278:48713–48719
Lucitti JL, Jones EAV, Huang C et al (2007) Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development (Camb) 134:3317–3326
McEver RP, Cummings RD (1997) Perspectives series: cell adhesion in vascular biology. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 100:485–491
McGrath KE, Koniski AD, Malik J et al (2003) Circulation is established in a stepwise pattern in the mammalian embryo. Blood 101:1669–1676
Moss ML, Rasmussen FH (2007) Fluorescent substrates for the proteinases ADAM17, ADAM10, ADAM8, and ADAM12 useful for highthroughput inhibitor screening. Anal Biochem 366:144–148
Palis J, Robertson S, Kennedy M et al (1999) Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development (Camb) 126:5073–5084
Schulz B, Pruessmeyer J, Maretzky T et al (2008) ADAM10 regulates endothelial permeability and T-Cell transmigration by proteolysis of vascular endothelial cadherin. Circ Res 102:1192–1201
The FANTOM Consortium (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Japan
About this chapter
Cite this chapter
Iida, A. (2014). Primitive Erythroblast Cell Autonomously Regulates the Timing of Blood Circulation Onset via a Control of Adherence to Endothelium. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_14
Download citation
DOI: https://doi.org/10.1007/978-4-431-54634-4_14
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-54633-7
Online ISBN: 978-4-431-54634-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)