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Title: The cytology of the pronephros of lampreys
Author: Bowen, Peter C.
Awarding Body: University of Oxford
Current Institution: University of Oxford
Date of Award: 1969
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The cytology of the pronephros of the three species of lamprey larvae, Lamnetra planeri. L. fluviatilis and Petromyzon marinus, at the pronephric stage of excretion and during its subsequent degeneration, has been investigated with the optical and electron microscopes. The pronephros is a paired, segmental organ located in the cardiac region, each pronephros consisting of two functional units: a single large glomus and an aggregation of 3-8 tubules. Ultrastructurally, both have been found to be strikingly similar to their homologues in opisthonephric, mesonephric and metanephric kidneys. The principal dissimilarities between the functional lamprey pronephros and the kidneys of the higher vertebrates are, in general, due to the less complex structure and arrangement of the cells and the tissue of the pronephros. The glomus is composed of the usual three cell types found in all vertebrate glomeruli, although in the glomus they exhibit a less complex internal structure. There is no juxtaglomerular apparatus in the glomar artery, which arises from the dorsal aorta. Multiple filtration slit membranes are found between the foot processes of the epithelium, and the endothelial fenestrae lack membranes. There is no Bowman's capsule. Filtrate from the glomus passes into the coelom and coelomic fluid is collected by ciliated nephrostomes which lead to the tubular portion, which is enveloped by the anterior cardinal vein. The nephrostome is composed of an external funnel and a short, internal neck leading to the proximal tubule, which is the longest of the tubular sections and divided into two segments. The proximal tubule is connected to the shortar distal tubule by a abort, undifferentiated intermediate segment. Each pronephros is drained by a duct which empties into the cloaca. The fine structure of the proximal and distal tubules, while exhibiting minor differences, is almost identical to the homologous tubules of the mammalian metanephros, but the tubules do not display the greater degree of subdivision found in other vertebrates, particularly mammals. The ultrastructure of the pronephric duct is vary similar to that of the preceding distal tubule. Degeneration of the glomus begins in the latter part of the first year in all species. The capillaries become occluded with a dense, amorphous material and cellular material derived from proliferating endothelial and mesangial cells. The axial portion of the glomus increases is volume by further mesangial proliferation, and numerous reticular and collagenous fibres are deposited in the mesangial matrix. In the year before metamorphosis, the endothelial and mesangial cells begin to appear necrotic, but the epithelial cells are unaffected, and the glomus does not disappear entirely until metamorphosis. The tubules begin to atrophy in the first year, the proximal tubules of the most anterior segments being the first to show signs of degeneration. Lycosome-like bodies appear in the cytoplasm, many cells rupture and the lumens become blocked with cellular debris and subsequently with invading macrophages. This occlusion is followed by a swelling of the tubules, phagocytic invasion increases, the swollen tubules collapse and the remaining nephric cells are resorbed. The distal tubules and the tubules of the posterior segments follow in sequence, and by the last year of larval life all traces of the tubules have disappeared, except the nephrostomes which, although slightly altered, continue to function, passing coelomic fluid into the anterior cardinal vein. The pronephric duct usually persists in the undifferentiated region behind the pronephros, and can often be traced to the cardiac region in the adult. The changes which occur with age, and the death and resorption of the cells of the pronephros, are shown to have several points of similarity with changes which occur with increasing age and pathological conditions in mammalian kidneys. The only interspecific difference found between pronephroi of the three species studied occurs in the tine of onset and the rate of tubular degeneration. In L. planeri, atrophy begins earlier and is completed sooner than in P. marinus; onset and completion of tubular degeneration in L. fluviatilis appears to be intermediate to the other two species. The possible reasons for this difference are discussed in relation to the life history of lampreys, and it is concluded that earlier and faster degeneration of the tubules is related to the trend towards neoteny in L. planeri. Primary experimental evidence shows that the pronephros is capable of responding to changes in the osmotic pressure of the environment by adapting certain features of the tubular structure, principally the degree of lateral and basal interdigitation and the size of the intercellular spaces, to facilitate increased or decreased water resorption. The ultrastructure of the pronephros is discussed in relation to the ultrastructure of other kidneys, and pronephric function is considered, both by reference to the experimental results and by extrapolation from ultrastructural and functional studies of the kidneys of higher vertebrates. This investigation shows that although there are minor differences the essential ultrastructural similarity between the pronephros and the opisthonephros, mesonephros and metanephros suggests that the former should not be regarded as the ancestral excretory organ of vertebrates. On the contrary, the evidence presented here indicates that the regions of the vertebrate excretory system are serially homologous. Support is thus given to the holonephric theory of the evolution of the kidney in vertebrates.
Supervisor: Not available Sponsor: Not available
Qualification Name: Thesis (Ph.D.) Qualification Level: Doctoral
EThOS ID:  DOI: Not available