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The Development of Hepatic Sinusoids in Mouse Embryos

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The Development of Hepatic Sinusoids in Mouse Embryos 86 Erika Awata, Akina Chiba, Chisato Yui and Shigeki Hirano 形態・機能 第 11 巻第 2 号 <Original> The Development of Hepatic Sinusoids in Mouse Embryos Erika Awata1), Akina Chiba2)*, Chisato Yui1) and Shigeki Hirano1) 1) ‌Department of Medical Technology, Graduate School of Health Sciences, Niigata University, Niigata, Japan 2) ‌Division of Gross Anatomy and Morphogenesis, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan (Received:25 May 2012, Accepted:23 August 2012) Abstract The development of hepatic sinusoids is only partially understood. This study investigated the development of hepatic sinusoids in order to clarify the formation process of sinusoidal endothelium by focusing on mouse tissue during a period of active liver hematopoiesis (E11-E16) using hematoxylin and eosin staining on paraffin-embedded liver sections, and toluidine blue staining on epoxy resin- embedded semi-thin sections. Flat cells lining the luminal surface of hepatic sinusoids were identified as endothelial cells with CD-146 immunohistochemical staining. We observed that developing sinusoids had partially naked walls that were not lined by flat cells, and from that hematopoietic cells and/or hepatic cells protruded into the sinusoidal lumen. In addition, CD-146 positive round cells scattering among hematopoietic cells and hepatic cells were observed. These observations suggest that hepatic sinusoids do not arise from the sprouting of intrahepatic capillary vessels but appear to be formed by CD-146 positive endothelial progenitor cells. Key words fetal mouse liver; sinusoid development; endothelial progenitor cells; CD-146 Introduction vascular system in liver, especially its sinusoidal Most liver functions, including the synthesis development, is poorly understood. and excretion of bile, the storage and supply of As the liver develops, intrahepatic capillary energy, and the metabolism and detoxification vessels that are directly connected to the ductus of various substances, arise gradually during venosus1, 2) can be observed in the primitive liver development. These functions occur in hepatic anlage. The vascular system of the liver anlage lobules in three distinct groups of the vascular is then distinguished as a vessel connecting the system (the afferent interlobular vessels via right and left vitelline veins, with sinusoids the porta hepatis, sinusoids of each lobe, developing among them. Therefore, it is thought and efferent veins connected to the inferior that one source of the vascular system in vena cava). However, the development of the liver is vitelline veins. It is unlikely, however, whether all vascular sets are derived from the 3) intrahepatic capillary vessels. Yokoyama et al. Corresponding author : Akina Chiba, Ph.D. demonstrated that the long-term survival of Division of Gross Anatomy and Morphogenesis, Niigata University Graduate School of Medical and Dental hepatocytes was dependent on a network of blood Sciences, 757 Asahimachi-dori 1-chome, Chuo-ku, Niigata, Niigata 951-8510, Japan vessels that developed before transplantation Tel: +81-25-227-2048 into the host. These blood vessels contributed to Fax: +81-25-227-0752 E-mail: [email protected] supplying hepatocytes with nutrients but did not 2013 年３月 The development of hepatic sinusoids 87 result, themselves, in sinusoidal development. Histology and immunohistochemical staining Sudo et al.4), who constructed a microfluidic Liver sections were prepared for either platform to analyze angiogenesis in 3D cultures immunohistochemistry or hematoxylin of rat primary hepatocytes, showed that these and eosin (H-E) staining. Anti-albumin microvascular networks did not contribute to immunohistochemical techniques were used to sinusoid formation. Chiba et al.5), observing a identify hepatoblasts and hepatocytes in the hematopoietic cell mass that was enveloped liver anlage. Paraffin-embedded liver sections by endothelial cells in the regenerating liver from E11.5, E12, E13 and E15 embryos were on the chorioallantoic membrane of chick pre-incubated with normal rabbit blocking embryos, suggested that the spaces occupied serum for 20 minutes and incubated overnight by the hematopoietic cell mass gave rise to with anti-mouse albumin in 0.01M PBS (Bethyl sinusoids. Sherer6) indicated that the endothelial Laboratories, Montgomery, TX, USA) at 4°C in lining of sinusoids in the developing quail’s a refrigerator. Biotinylated anti-goat IgG (H+L) liver transplanted onto a chick chorioallantoic (Vector Laboratories, Burlingame, CA, USA) membrane was formed by quail cells. Pérez- was used as the secondary antibody, followed Pomares et al.7) suggested that endothelial cells by Vectorstain ABC Kit (Vector Laboratories). of sinusoids were derived from mesothelial cells. Visualization of immuno-complexes was Taken together, these reports indicate that performed by incubation with diaminobenzidine, sinusoids develop from endothelial progenitor and sections were lightly counterstained with cells rather than intrahepatic capillary vessels. hematoxylin. Hepatic sinusoids are unique vessels, that To reveal the presence of endothelial cells of is, they are constructed from fenestrated sinusoids, CD-146 immunohistochemical staining endothelial cells with no basal lamina. Therefore, of E12, E13 and E15 samples was performed. the developmental mechanisms giving rise to CD-146 is a cell adhesion molecule localized at hepatic sinusoids may be distinct from those of the endothelial junction of the whole vascular other blood vessels. system8, 9). We examined several endothelial In the present study, in order to elucidate cell markers, and adopted CD-146 that showed the origin of sinusoids, we detail the endothelial the most intense reaction on the endothelial formation of the mouse liver at a developmental cells of the mouse embryonic livers. Paraffin stage in which hematopoiesis is in progress. and cryostat sections were pre-incubated with normal goat serum at room temperature for at Materials and methods least 30 minutes and incubated overnight with Pregnant mice (C57BL/6), purchased from anti-CD-146 antibody (Calbiochem, Frankfurt, Japan SLC Inc. (Shizuoka, Japan), were used. Germany) at 4°C in a refrigerator. Sections The presence of vaginal plaques was taken were then incubated with ImmPRESS reagent to represent embryonic day zero (E0). As (Calbiochem, Frankfurt, Germany) and anti- hematopoiesis started at E10 and reached a mouse IgG (Vector Laboratories) at room peak at E13, the mice were sacrificed under temperature for 30 minutes. Diaminobenzidine intraperitoneal anesthesia with pentobarbital was then used as a chromogen. The livers of sodium on days E9.5, 10, 10.25, 10.5, 11, newborn and adult mice were used as controls 11.25, 11.5, 12, 13 and 15, and the fetuses (data not shown). were collected. Fetal liver samples were fixed with 10% formaldehyde in 0.01M phosphate- Semi-thin sections buffered saline (PBS; pH 7.3). Because the livers To observe the discontinuity of endothelial of E9.5-E13 embryos were extremely small, cells on the walls of sinusoidal spaces, E11 and the entire thoracoabdominal region, including E12 livers were fixed with 2.5% glutaraldehyde the liver anlage, was dissected en bloc under a in 0.01M PBS for 3 hours, and then post-fixed stereomicroscope and immediately fixed. For with 1% osmium tetraoxide in 0.01M PBS for 2 cryostat sections, samples were immersed in 30% hours. The tissues were dehydrated through a sucrose at 4°C in a refrigerator. Other samples graded series of ethanols, placed in propylene were embedded in paraffin. oxide twice, and embedded in epoxy resin (Quetol 812). Serial semi-thin sections (1 μm) were cut 88 Erika Awata, Akina Chiba, Chisato Yui and Shigeki Hirano 形態・機能 第 11 巻第 2 号 with a diamond knife and stained with toluidine blue for light microscopic observation. Results Hepatoblasts and hepatic cells of the fetal livers were stained with H&E and immunostained with anti-albumin antibody (Fig.1). At E11, intrahepatic capillary vessels could already be seen as a relatively wide space (Fig.1, a-1) that had a direct connection to the ductus venosus (refer Kingsbury et al.2)). Thereafter, the primitive sinusoidal spaces diminished (Fig.1, b-1, c-1). Some primitive sinusoids were observed as having a smooth Fig. 2 Light photomicrograph of resin-embedded wall that was lined by flat cells sharing an semi-thin section of liver at E12. asterisk: The denuded position of the hepatic cells and hematopoietic cells into the sinusoid. arrowheads: the endothelial cells lining the wall of the sinusoid. arrows: Large round endothelial progenitor cell spreading their cytoplasmic processes along the wall of the sinusoid. (scale bar 50 μm) irregular wall and having no epithelial lining from which hematopoietic cells and hepatic cells were denuded (Fig.1d). At E11 and E12, hepatic cells were polygonal in shape and gathered together to form a network of branched-cell cords (Fig.1, a-2, b-2). The wide spaces of the mesh were filled with albumin-negative cells (most likely hematopoietic cells), which had spherical outlines and a large round nucleus. Thereafter, the liver anlage grew rapidly, increasing the number of hepatic cells, while the size of the mesh decreased. By contrast, the hematopoietic cells decreased in number (Fig.1c, e). Fig. 1 Light photomicrographs stained with H&E To confirm the denudation of hepatocytes and (left column) and anti-albumin (right column) in hematopoietic cells into the sinusoidal space the developing liver. (Fig.1d),
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