Differentiation of the segmented tubular nephron and excretory duct during lamprey metamorphosis

Abstract

The tubular portion of the adult lamprey nephron differentiates into various morphologically distinct segments during the seven stages of metamorphosis. At stage 1, a rudimentary nephron unit (RNU) originates from a nephrogenic mass attached to the peritoneum and elongates to become associated at its distal end with the archinephric (excretory) duct. The rapidly dividing cells show little sign of differentiation. Separation of the RNU from the peritoneum in stage 2 is first accompanied by widening of lateral intercellular spaces and then eventually by the formation of a small lumen at the proximal end. Cells surrounding a portion of this lumen show early signs of ciliogenesis and hence are located in the position of the presumptive neck segment. The distal end of the stage 2 RNU contains an electron-dense material in an enlarged intercellular space and the cells make non-junctional contact with the archinephric duct. The larval cells of the latter structure are either lost during degeneration and desquamation or are transformed into adult cells. By the end of stage 3 replication of basal bodies and formation of cilia has resulted in the appearance of a ciliated neck segment while numerous microvilli extending into a narrow lumen mark the position of the proximal segment. Furthermore, most of the distal portion of the newly formed tubule possesses a lumen containing a compact mass of material likely secreted by the cells during lumen formation. This presumptive distal segment terminates in the transforming epithelium of the archinephric duct as a presumptive connecting or collecting segment. Fully differentiated neck and proximal segments are present in stage 4 with the latter having a complete apparatus for endocytosis but the distal segment shows only early signs of differentiation of the smooth tubular network. This network appears to arise as an expanded surface area of the plasma membrane. Stage 5 is characterized by elongation of the proximal portion of the tubule, expansion of the tubular network in distal cells, and the identification of a collecting segment. The last two stages show no further major differentiation of the segments. The early differentiation of tubular segments in the adult lamprey nephron likely reflects the immediate physiological needs of this organism as the larval kidney undergoes regression. The potential of the developing kidney of adult lampreys as a source of information on morphogenesis of microvilli, the endocytotic apparatus, mitochondria, and a smooth tubular network is discussed. It appears that the archinephric duct and non-nephrogenic mesenchyme may play some role in tubulogenesis in lampreys.