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The claudin family of proteins are integral components of tight junctions and are responsible for determining the ion specificity and permeability of paracellular transport within epithelial and endothelial cell layers. Studies in human, mouse, Xenopus, and zebrafish have shown that only a limited number of claudins are expressed in endothelial cells. Here, we report the expression pattern of Claudin-5 during chick development. Between HH stage 4 and 6 Claudin-5 expression was observed exclusively in extraembryonic tissue. Claudin-5 expression was not observed in the embryo until HH stage 8, coincident with the onset of embryonic vascularization. Claudin-5 expression was maintained in the developing vasculature in the embryonic and extraembryonic tissue throughout organogenesis (HH stage 19-35), including the vasculature of the ectoderm and of organs derived from the mesoderm and endoderm lineages. These data describe a conserved expression pattern for Claudin-5 in the endothelial tight junction barrier and is the first report of the onset of Claudin-5 expression in a vertebrate embryo.
Fig. 1. Phylogenetic analyses showing the relationship of chick Claudin-5 to human, mouse, and Xenopus Claudin-5. (A) Alignment of chick Claudin-5 with vertebrate orthologs. Transmembrane domains (TM), extracellular loops (ECL) 1 and 2, and the C-terminal tail (C-TERM) are underlined below the sequence. Asterisks indicate conserved (identical) amino acids and boxes indicate functionally defined residues. (B) Phylogenetic tree showing the relationship of chick Claudin-5 with mouse, human, and Xenopus orthologs using chick Claudin-2 as an outgroup. Bootstrapping values are indicated on the tree nodes.
Fig. 2. Claudin-5 expression from gastrulation to HH 16. (A–A′) Dorsal view of a gastrulation stage (HH stage 4) embryo and a higher magnification of the boxed region showing expression in the area opaca. (A′) Transverse section from (A). (B–B′) Dorsal view of a HH stage 6 embryo; higher magnification of the boxed region is shown in (B′). (C–C′) Expression of Claudin-5 in a HH stage 8 embryo. White arrowhead indicates vasculature in the embryonic region. Black arrowheads indicate blood islands, which are shown at a higher magnification in (C′). (D) Ventral view of a HH stage 12 embryo. (E–G) Transverse sections through a HH stage 12 embryo at the position indicated by the dashed lines in (D). (H) Transverse section through endothelial tubes in the extraembryonic tissue of a HH stage 12 embryo. (I) Claudin-5 expression in the vitelline arteries (black arrowheads) and vascular capillaries (white arrows) in the extraembryonic tissue of a HH stage 16 embryo. Abbreviations: ao, area opaca; da, dorsal aorta; e, endocardium; ec, ectoderm; en, endoderm; hf, head fold; hy, hypoblast; ph, pharynx; so, somite. Scale bars represent 0.1 mm.
Fig. 3. Expression of Claudin-5 from HH stage 19–24. (A–F) Expression of Claudin-5 in the vasculature of a HH stage 19 embryo. Asterisks indicated trapped probe. (B) Higher magnification of intersomitic vessels. (C and D) Transverse section through a HH 19 ventricle; the box indicates the region shown at a higher magnification in (D). (E) Expression in the omphalomesenteric artery and (F) vasculature of the developing gut. (G–U) Expression of Claudin-5 in a HH stage 24 embryo. (H) Higher magnification of the intersomitic vessels and surface vasculature. (I) Transverse section showing expression in the vasculature surrounding the neural tube and dorsal root ganglia, and in the aorta. (J) Whole mount view of the vasculature of the brain. (K) Coronal section through the brain; boxes outline regions shown at higher magnifications in (L), (N), and (O). (M) Expression in the choroid plexus. (P) Section through the somites of a HH stage 24 embryo. Arrowheads indicate expression in the intersomitic vessels. (Q) Expression of Claudin-5 in the otic vesicle and (R) vasculature around the lung bud. (S) Transverse section showing expression in the limb, surrounding the gut, and in the tail bud. (T) Claudin-5 expression in the vasculature of the gizzard and liver. (U) Expression in the atria, ventricle, and endocardial cushions of the heart. The dashed box outlines the ventricletrabeculae shown at a higher magnification inset. Arrowheads indicate vasculature along the body wall. Abbreviations: at, atria; da, dorsal aorta; cp, choroid plexus; drg, dorsal root ganglion; ec, endocardial cushion; g, gut; gz, gizzard; li, limb; liv, liver; lu, lung bud; nt, neural tube; no, notochord; omp, omphalomesenteric artery; ot, otic vesicle; so, somite; tb, tailbud; v, ventricle. Scale bars represent 0.1 mm.
Fig. 4. Expression of Claudin-5 in vasculature of ectodermal, mesodermal and endodermal organs. (A–A′) Expression of Claudin-5 in short feather buds and (B–B′) long feather buds in an HH stage 35 embryo. Sagittal sections through the bud are shown in (A′) and (B′). (C) Claudin-5 expression in the skinvasculature. (D and E) Claudin-5 expression in a HH stage 30 heart. The boxed region is shown at a higher magnification in (E). (F) Expression in the mesonephric kidney, gonad, and (G) metanephric kidney. (H–I) Expression in whole (H and I) and transverse sections (H′ and I′) of HH stage 30 and HH stage 35 lungs. (J) Claudin-5 expression in the vasculature overlying the gut and (K) intestine and pancreas of a HH stage 35 embryo. (L) Transverse section through the intestine of a HH stage 35 embryo. Abbreviations: go, gonad; gz, gizzard; int, intestine; ms, mesonephric kidney; pa, pancreas; pv, proventriculus; st, stomach. Scale bars represent 0.1 mm.
