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Early Development of the Human Mesonephros

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Early Development of the Human Mesonephros View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Anat Embryol (2005) 209: 439–447 DOI 10.1007/s00429-005-0460-3 ORIGINAL ARTICLE K. S. Ludwig Æ L. Landmann Early development of the human mesonephros Accepted: 11 February 2005 / Published online: 25 May 2005 Ó Springer-Verlag 2005 Abstract The mesonephrogenic cord disintegrates into approximately 35–40 provesicular cell masses which are Introduction in close contact with the mesonephric (Wolffian) duct (WD) on their lateral side. Here, the epithelium of the The development of the nephron in the mesonephros is WD is columnar and shares a common basal lamina reported in textbooks of embryology (Fischel 1929; with the provesicular cell masses. This in turn gives rise Hamilton et al. 1972; Starck 1975; Moore 1980; to a sickle-shaped pseudostratified epithelium. The O’Rahilly and Mu¨ller 1996) according to the mode concavity of the sickle is filled by spherical cells, the outlined by Felix (1911): the mesonephric cord generates transition of which into the surrounding connective tis- provesicular cell masses that become vesicles. Cells sue is continuous. The sickle is transformed into a dis- growing from the vesicles fuse with the mesonephric tillation flask and becomes separated from the (Wolffian) duct (WD) and, after acquisition of a lumen, mesonephric duct while the spherical cells maintain a become tubules whereas the vesicle becomes the cor- connection to it by a—for the time being—solid outlet puscle of the nephron. pipe. The columnar epithelium of the mesonephric duct Felix (1911) does not report details on the develop- becomes a multilayered cone, whose surface is in contact ment of the nephron, nor does he provide illustrations. with the outlet tube. Shortly after, a continuous lumen is He just states that ‘‘the anlagen appear suddenly’’ formed in the cone and the outlet pipe which is delimited (p. 779). In a schematic graph (Fig. 561) he compiles the by cells becoming columnar and forming a basal lamina. steps leading from a vesicle to a nephron. His view is The epithelial anlage of the nephron is clearly separated based on his knowledge of comparative embryology, from the surrounding mesenchyma by these processes. and on his belief in the ‘‘biogenetic basic law’’ (Haeckel The flask eventually becomes a corpusculum, the outlet 1903), even in modified form. He, therefore, claims pipe a secretory (proximal) as well as collecting tubule, (Felix 1911) to have identified ureters of the meso- and the cone of the mesonephric duct a mesoureter. The nephros (or better mesoureters) which sprout from the various sections display differentially differentiated epi- WD and collect caudal tubules of the mesonephros. thelia that are clearly distinct from each other. The Since Felix (1911), nobody has cared to reexamine the mesoureter behaves differently during differentiation of early development of the mesonephros. Therefore, we epi- and paragenitale: in the epigenitale, it is short and took another look into the nephrons of the mesonephros runs into the collecting tubules of the nephrons at the in order to investigate the presence of mesoureters. lateral side of the convolved tubules, whereas a long mesoureter crosses the dorsal side of the convolved tu- bules and joins the corresponding collecting tubules at Materials and methods the far end of the mesonephros in the paragenitale. Our examination is based on all serial sections of human Keywords Nephron Æ Mesonephros Æ Mesoureter Æ embryos and early fetal stages of the collection of the Wolffian duct Æ Embryology Department of Anatomy, University of Basel. Stages 15 through 23 and the early fetal stages are listed in Ludwig K. S. Ludwig (&) Æ L. Landmann (1993). The additional embryos used in this study com- Department of Anatomy, University of Basel, prising stages 11 through 14 as well as some older stages Pestalozzistr. 20, 4056 Basel, Switzerland E-mail: [email protected] useful for this examination are listed in Table 1. Tel.: +41-61-2673920 Digital micrographs of sections from embryo Fax: +41-61-2673959 10.12.1952 (29 mm CRL) were used for reconstruction. 440 Using the AutoAligner module of the Imaris software c package (Bitplane AG, Zurich, Switzerland), images Fig. 1 Embryo 28.7.59, 4.5 mm CRL (stage 13), ·360. a Section of were aligned with the ureter of the metanephros as a the most caudal provesicular cell mass of the mesonephros generated by the nephrogenic cord. Close to the Wolffian landmark, and truncated along the epithelial surface (mesonephric) duct (WD) the cells are densely packed; at the yielding reconstructions of the luminal space. After dorsal side the texture is less dense and forms a continuous processing with a Gaussian filter in order to soften sin- transition into the surrounding connective tissue. The WD forms a gular section-induced irregularities, each corpuscle and palisade consisting of columnar cells with a basal lamina at the side its associated tubule were reconstructed separately by of the mesonephrogenic cell mass. The palisade forms the boundary of the straight section of the semicircular lumen, whereas the surface rendering in the IsoSurface module of Imaris. curved section consists of a non-stratified, cuboidal epithelium. Co Finally, the color-coded reconstructions were joined into coelom, Vc cardinal vein. b This section shows the 4th and 5th a singular data set. provesicular cell masses counted from the caudal side. The 5th mass consists of densely packed columnar cells on the side of the WD while cells on the dorsal side are rather spherical. Here too, no sharp boundary against the mesenchyma is present. The palisade of Results the WD has become a cone sharing a common basal lamina with the adjacent provesicular cell mass (arrowhead). c Section display- In a stage 12 embryo (appr. 3–5 mm CRL), we found 31 ing the prospective nephrons 9, 10 and 11 (counted from caudal). The 9th anlage shows the so-called vesicular stage with the flask of anlagen of developing nephrons. While the cranial the distillery apparatus. Its lumen is delimited by a pseudostratified nephrons are already in the vesicle stage, the meso- columnar epithelium. As demonstrated by the 10th anlage, the flask nephric cord persists in the caudal region. Stage 13 continues into the outlet tube consisting of densely packed cells and embryos (appr. 4–6 mm CRL) show several nephrons in apposed to the conus of the WD. Right in the center of the cone, a canaliculus has been formed in situ (arrowhead) which extends in an early developmental stage in the caudal part of the the draining tube. A short stalk generated by the conus of the mesonephros. A caudal provesicular cell mass that has mesonephric duct (asterisk) supports the draining tube (arrow). The been generated from the mesonephric cord consists of 11th nephron shows that the cells become columnar and are densely and irregularly packed small cells without a lu- arranged concentrically around the canaliculus. There is still no men (Fig. 1a). Dorsally it cannot be separated from the distinct boundary between nephrons and connective tissue. Arrowhead points to the transition between mesoureter and adjacent dorsal tissue but it makes contact with the draining tubule. d The 13th prospective nephron and the mesonephric duct (Wolffian duct=WD) on its lateral mesoureter display a distinct basal lamina (arrowhead) separating side (Fig. 1a). The semicircular lumen of the WD faces epithelial components from connective tissue the lateral side with its convex half. While the cells of its lateral wall are cuboidal, those of the medial wall form a become the nephron are small, circular and arranged columnar palisade (Fig. 1a) that is separated from the irregularly. They cannot be separated unambiguously adjacent mesonephrogenic tissue by a basal lamina. from the dorsally adjacent tissue. A small, rapidly The lumen of the WD is round or oval in the intervals expanding lumen becomes visible in the region of the between the provesicular cell masses and consists en- columnar cells (Fig. 1c). This makes the anlage similar tirely of cuboidal cells. With proliferation of the meso- to a distillation flask: the flask which is reflected by a nephrogenic tissue, the cells adjacent to the WD become vesicle in cross sections (Fig. 1c, 9) is formed by columnar and interact with a basal lamina, which is columnar cells that are arranged concentrically around common for both structures in the area of contact the lumen form. The dorsally apposed round cells form (Fig. 1b). On the dorsal side, the cells that eventually the outlet pipe which bends strongly to the dorsolateral Table 1 Embryos used in this study listed by stage of Stage Designation of CRL Sex Direction of Thickness Stain Notes development (according to embryo (mm) sectioning of sectioning O’Rahilly et al. 1981) (lm) 11 NN 3–4 Transversal 10 Coch.-Alaun 12 Br. 1934 3.6 Frontal 8 Coch.-Alaun 13 Embryo 28.7.54 A 4–5 Transversal 6 Azan Twins Embryo 28.7.54 A 4–5 Transversal 6 Azan Twins Egli 4.1.50 5–6 Transversal 6 Azan 14 Pfy. 1 7 Sagittal 10 Coch.-Alaun Ve 1 7 Sagittal 10 Azan F.Sp. 43 7 Transversal 6 Azan 15 Embryo 17.5.1951 8 Frontal 6 Azan 16 Egli 13.1.1951 9 Transversal 6 Azan 18 MJSp. 8.11.1940 15 f Transversal 6 Azan 20 Sellheim 17.1.1945 20 m Transversal 8 Azan MJSp. 17.11.1948 20 f Frontal 6 Azan 23 Embryo 10.12.1952 29 m Transversal 7 Azan Embryo Mensch 30 f Transversal 7 Azan Early fetal stages Riehen 1948 40 f Transversal 8 Azan Embryo 22.10.1952 40 m Transversal 8 Azan 441 side and joins the WD (Fig.
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