Microanatomy and ultrastructure of the kidney of the African lungfish Protopterus dolloi

Abstract

The Dipnoi (lungfishes) have developed true lungs, having the ability to take oxygen from both the gills and the lungs. During the tropical dry season, many lungfish estivate on land, breathing only air. The estivation period is accompanied by profound functional modifications, including the suppression of urine. Thus, the lungfish kidney must be designed to cope with these dramatic cyclic changes in renal function. We study here the microanatomy and the structure of the kidney of the African lungfish Protopterus dolloi, maintained under controlled freshwater conditions. Chemical microdissection, light microscopy, and scanning and transmission electron microscopy have been used. The nephrons of P. dolloi are composed of a renal corpuscle (RC) and of a renal tubule that appears divided into five morphologically distinct segments: neck segment (NS), proximal tubule (PT), intermediate segment (IS), distal tubule (DT), and collecting tubule (CT). Paired CTs abut into a collecting duct, the latter emptying into an archinephric duct. The RCs lie in the mid-zone of the kidney, between the PTs and the convoluted DTs. The spatial distribution of these elements allows recognition of a kidney zonation. The RCs group into clusters (3-4 RCs per cluster) that are supplied by a single arteriole surrounded by pericytes. Each cluster appears to represent a functional unit with a common hemodynamic regulatory mechanism. The major processes of the podocytes form flattened networks that appear to constitute an integrated system due to the presence of gap junctions. The existence of mesangial cells with large cell processes, and of mesangial cells with a dendritic appearance, suggests a complex functional role (contractile and phagocytic) for the mesangium. The NS and the IS are the narrowest nephron segments, formed only by multiciliated cells. The PT and the DT can be subdivided, based on the tubular morphology and on cell composition, into portions I and II: PTI is formed only by brush border (BB) cells, while PTII contains BB and multiciliated cells. The DTI is formed by segment-specific cells, while the DTII contains segment-specific and a small number of flask cells. The CT contains principal and flask cells in a 5:1 ratio. The flask cells adopt two different configurations (with a narrow canaliculus or with a large cavity). The main goal of this study was to disclose specific kidney features that could be related to function, phylogeny, and habitat. In addition, the present results constitute the basis for a study of the morphologic changes that should occur in the kidney of P. dolloi during estivation. © 2006 Wiley-Liss, Inc.