Functional characterization of the vertebrate primary ureter: Structure and ion transport mechanisms of the pronephric duct in axolotl larvae (Amphibia)

Abstract

BackgroundThree kidney systems appear during vertebrate development: the pronephroi, mesonephroi and metanephroi. The pronephric duct is the first or primary ureter of these kidney systems. Its role as a key player in the induction of nephrogenic mesenchyme is well established. Here we investigate whether the duct is involved in urine modification using larvae of the freshwater amphibian Ambystoma mexicanum (axolotl) as model.ResultsWe investigated structural as well as physiological properties of the pronephric duct. The key elements of our methodology were: using histology, light and transmission electron microscopy as well as confocal laser scanning microscopy on fixed tissue and applying the microperfusion technique on isolated pronephric ducts in combination with single cell microelectrode impalements. Our data show that the fully differentiated pronephric duct is composed of a single layered epithelium consisting of one cell type comparable to the principal cell of the renal collecting duct system. The cells are characterized by a prominent basolateral labyrinth and a relatively smooth apical surface with one central cilium. Cellular impalements demonstrate the presence of apical Na+ and K+ conductances, as well as a large K+ conductance in the basolateral cell membrane. Immunolabeling experiments indicate heavy expression of Na+/K+-ATPase in the basolateral labyrinth.ConclusionsWe propose that the pronephric duct is important for the subsequent modification of urine produced by the pronephros. Our results indicate that it reabsorbs sodium and secretes potassium via channels present in the apical cell membrane with the driving force for ion movement provided by the Na+/K+ pump. This is to our knowledge the first characterization of the pronephric duct, the precursor of the collecting duct system, which provides a model of cell structure and basic mechanisms for ion transport. Such information may be important in understanding the evolution of vertebrate kidney systems and human diseases associated with congenital malformations.

The testicular sperm ducts and genital kidney of male Ambystoma maculatum (Amphibia, Urodela, Ambystomatidae)

“…Electron dense bodies like those found in the distal convoluted tubule genital kidney nephron are also found in the collecting tubule. We found no evidence of intercalated cells ultrastructurally, a similar finding to the lack of intercalated cells in the collecting duct system of larval A. mexicanum (Haugan et al, 2010). Whereas the collecting tubule empties into a collecting duct that hypertrophies due to the synthesis of secretions during the mating season in the pelvic kidney of A. maculatum (Siegel et al, 2010), no such duct exists in the genital kidney nephrons, and thus, the collecting tubule communicates directly with the Wolffian duct.…”

Conserved and novel functions of programmed cellular senescence during vertebrate development

“…S1 " type="url"/> ), the stage at which the axolotl pronephros is no longer functional and begins to degenerate ( Haugan et al, 2010 ). This is in agreement with previous observations of marked decreases in pronephric tubule volume at the onset of degeneration ( Haugan et al, 2010 ). The structural collapse of the pronephric tubules was accompanied by a marked recruitment of macrophages/monocytes ( …”

Embryonic development of kidneys in viviparous Typhlonectes compressicauda (Amphibia, Gymnophiona)

“…The ablation of pronephroi in larvae of several anuran species provokes an important oedema followed by death (CAMBAR, 1947), which suggests that these first kidneys are functional at least during a part of larval development. In larval Ambystoma mexicanum, HAUGAN et al (2010) proposed that pronephroi were important for modification of urine. In Bufo viridis, each pronephros is a single convoluted tubule open into the coelomic cavity through three nephrostomes (MØBJERG et al, 2000), and urine is formed by filtration from an external glomerulus.…”