Structure and development of nephridia in Annelida and related taxa

Two different kinds of filtration nephridia, protonephridia and metanephridia, are described in Polychaeta. During ontogenesis protonephridia generally precede metanephridia. While the latter are segmentally arranged, protonephridia are characteristic for the larva and are the first nephridial structure formed during ontogenesis. There is strong evidence that both organs depend on the same information and that their specific structure depends on the way in which the coelom is formed and which final expansion it gains. While metanephridia are regarded to be homologous throughout the polychaetes, protonephridia seem to have evolved in several lineages. Some of the protonephridia closely resemble less differentiated stages of metanephridial development, so that protonephridial evolution can be explained by truncation of the metanephridial development. Nevertheless, structural details are large enough to allow us to expect information on the polychaete evolution if the database on polychaete nephridia increases. A comparison of the polychaete metanephridia with those of the Clitellata and Sipuncula reveals some surprising details. In Clitellata the structure of the funnel is quite uniform in microdrilid oligochaetous Clitellata and resembles that of the aeolosomatids. Like the nephridia in the polychaete taxa Sabellida and Terebellida, those of the Sipunucla possess podocytes covering the coelomic side of the duct.     

THE FUNCTIONAL ORGANIZATION OF FILTRATION NEPHRIDIA

(1) Based on the classical studies of Goodrich, protonephridia are believed to be phylogenetic antecedents of metanephridia. It is argued here that the primary factor determining the type of nephridium expressed is body size rather than phylogenetic status. (2) The proposed model defines a nephridium functionally and predicts two general configurations for filtration nephridia in animals. (3) Application of the model to metanephridial and protonephridial systems indicates differences in the sites of ultrafiltration and mechanisms of pressure generation. (4) Metanephridial systems function by muscle-mediated filtration of vascular fluid into a coelomic space before modification by an excretory duct. (5) Protonephridial systems function by cilia-mediated filtration of extracellular fluid into the lumen of a protonephridial terminal cell before modification in an adjoining duct. (6) The model predicts a correlation between animals with blood vessels and metanephridia, and animals without blood vessels and protonephridia. The correlation is shown to be nearly perfect. (7) Exceptions to the model are discussed. (8) Original experimental evidence is given for the permeability of the protonephridial terminal cell to iron dextran and its reabsorption by the protonephridial duct in the polychaete, Glycera dibranchiata. (9) Experimental data for proto- and metanephridial systems are summarized and shown to support the proposed model. (10) The ultrastructure of the exceptional amphioxus ‘protonephridium’ is reviewed and original data are presented. Its organization is structurally and perhaps functionally intermediate between proto- and metanephridial systems. (11) An original ultrastructural comparison is made of monociliated nitration cells in a size range of larval invertebrates from five phyla. Filtration cells that are structurally intermediate between protonephridial solenocytes and metanephridial podocytes are noted in larvae intermediate in body size between the two extremes. The comparative data suggest that (i) podocytes and solenocytes are homologous cells and (ii) that body size is correlated with which of the two designs is expressed. (12) The fates of larval podocytes are followed through metamorphosis in three species. The results confirm the equivalence of podocytes and solenocytes as suggested by the comparative analysis. They further indicate that which morph is expressed is a function of body design factors discussed in the model. (13) Protonephridia are believed to be primitive to metanephridia because they occur in presumably primitive animals and in ontogenetic stages of many animals with metanephridia as adults. It is suggested here that the distribution of protonephridia is related to small body size and the lack of blood vessels, regardless of phylogenetic status. The occurrence of protonephridia in the larvae of species with metanephridia as adults is explained similarly as a function of the small larval size and lack of blood vessels.     

Ultrastructure and significance of the transitory nephridia in Erpobdella octoculata (Hirudinea, Annelida)

In early developmental stages of Erpobdella octoculata two pairs of transitory nephridia occur which degenerate during the formation of the body segments. Because in the ground pattern of Annelida the first nephridia formed during ontogenesis are protonephridia, it can be assumed that the transitory nephridia of E. octoculata are homologous to the larval protonephridia (head kidneys) of Polychaeta. To test this hypothesis two cryptolarvae of E. octoculata were investigated ultrastructurally. Both pairs of transitory nephridia are serially arranged to either side of the midgut vestigium. Each organ consists of a coiled duct that opens separately to the exterior by an intraepidermal nephridiopore cell. The duct is percellular and formed by seventeen cells. Adluminal adherens and septate junctions connect all duct cells; the most proximal duct cell completely encloses the terminal end of the duct lumen. A filtration structure characteristic for protonephridia is lacking. Additionally, the entire organ lacks an inner ciliation. Morphologically and ultrastructurally the transitory nephridia of E. octoculata show far reaching congruencies with the segmental metanephridia in different species of the Hirudinea. These congruencies support the assumption that formation of transitory nephridia and definitive metanephridia in Hirudinea depends on the same genetic information. The same inherited information is assumed to cause the development of larval head kidneys and subsequently formed nephridia in different species of the Polychaeta. Thus, the presumed identical fate of a segmentally repeated nephridial anlage supports the hypothesis of a homology between the transitory nephridia in Hirudinea species and the protonephridial head kidneys in the ground pattern of the Polychaeta. We, therefore, assume that functional constraints lead to a modification of the protonephridial head kidneys in Hirudinea and explain ultrastructural differences between the transitory nephridia in Hirudinea and the protonephridia in Polychaeta. Accepted: 11 December 2000     

Ultrastructure of the crayfish antennal gland revealed by scanning and transmission electron microscopy combined with ultrasonic microdissection

The antennal gland of the crayfish Pacifasticus leniusculus was studied using standard techniques for scanning electron microscopy as well as newer procedures for ultrasonic microdissection. To clarify relationships in the nephron tubule, transmission electron microscopy was employed. The coelomosac contains elongated cells (podocytes) displaying microvilli and extensive apical blebbing. A smooth basal lamina lines the blood space that furnishes hemolymph to the coelomosac. The labyrinth consists of tall columnar cells displaying apical microvilli, numerous blebs that seem to represent an expansion of apical plasma membrane, and lateral interdigitations. The nephron tubule consists of two distinctly different areas: a proximal region of flattened cells with extensive intercellular fusions, and a distal segment of separate, dome-shaped cells. Despite many similarities between the crayfish kidney and the vertebrate nephron, there are striking differences. The amount of surface blebbing that occurs in the coelomosac and labyrinth far exceeds that of the vertebrate nephron and may reflect its importance in the function of the crayfish kidney. The cells of the coelomosac are taller than are the vertebrate podocytes and possess less obvious arms and pedicels. In addition, the proximal segment of the nephron tubule is notable for its intercellular fusions, which are not present in the vertebrate nephron. Although the function of the intercellular fusions is unknown, they may play a role in cellular communication or the redistribution of fluids or electrolytes between cells.     

Protonephridia in the larvae of the paleonemertean species Carinoma mutabilis (Carinomidae,Nemertea) and Cephalothrix (Procephalothrix) filiformis (Cephalothricidae,Nemertea)

During spiralian development, the first pair of nephridia forms anterior to the mouth. Each organ consists of a few cells, which is characteristic for spiralian larvae. In nemerteans, one of the unambiguously spiralian taxa, so far protonephridia, has been reported only in advanced pilidium larvae, where they likely persist as juvenile and adult nephridia. These organs have not been recorded in larvae of the basally branching nemertean taxa. In search for these organs, we examined the ultrastructure of pelagic planuliform larvae of the palaeonemerteans Carinoma mutabilis and Cephalothrix (Procephalothrix) filiformis. In both species, a pair of protonephridia is located at the level of the stomodaeum. Each protonephridium of C. mutabilis consists of two terminal cells, two duct cells and one nephropore cell, while that of C. filiformis consists of three terminal cells, three duct cells and one nephropore cell. In C. mutabilis and in C. filiformis, all terminal cells contribute to forming a compound filtration structure. In both species, the protonephridia seem to develop subepidermally, since in C. filiformis, the nephropore cells pierce the larval epidermis and in C. mutabilis, the nephropores are initially covered by the binucleated multiciliated trophoblast cells. On the fifth day, these cells degenerate, so that the protonephridium becomes functional. The occurrence of protonephridia in the larvae of both paleonemertean species is in accordance with the hypothesis that a common ancestor of Nemertea and Trochozoa had a larval stage with a pair of protonephridia. This does not contradict previous hypotheses on placing the Nemertea as an ingroup of the Trochozoa or Spiralia (= Lophotrochozoa). Whether these protonephridia are restricted to the larval phase or whether they are transformed into the adult protonephridia, like those of the pilidium larva, remains to be answered.     

Ultrastructure of the Protonephridium in Acteonemertes bathamae Pantin (Rhynchocoela: Enopla: Hoplonemertini)

The protonephridial system consists of terminal cell, protonephridial capillary, protonephridial tubule and efferent duct. The terminal cell is an elongated, thin-walled, fenestrated basket containing a ciliary flame circumscribed by a palisade of straight microvilli. The filtration area is confined to the terminal cell and consists of slits bridged by a filtration membrane. The cilia, as well as the microvilli, projects into the proximal bell-shaped part of the thin-walled protonephridial capillary. The terminal cells are often found in pairs connected to the same capillary, which has a very narrow lumen. The proximal part of the thick-walled, convoluted protonephridial tubule is ciliated and shows characteristic foldings of the luminal plasma membrane and numerous small vesicles in the cytoplasm. The cells of the following, non-ciliated part of the tubule have interdigitating lateral surfaces and the bases deeply invaginated to form compartments with numerous mitochondria; in the cytoplasm are many large vesicles, possibly containing lipid droplets, and small amounts of glycogen. The distal protonephridial tubule resembles various epithelia with an osmoregulatory function, including the vertebrate nephron.     

Morphology of the kidney in larvae of Bufo viridis (Amphibia, Anura, Bufonidae)

This study deals primarily with the morphology and ultrastructure of the pronephros in the green toad Bufo viridis during prometamorphosis when the pronephros and the developing mesonephros function simultaneously. Furthermore, the mesonephros was studied during pro- and postmetamorphosis with emphasis on the distal segments of the nephron. The paired kidneys consist of two cranial pronephroi immediately behind the gill region and two more caudal elongated mesonephroi. Each pronephros consists of a single convoluted tubule which opens into the coelom via three nephrostomes. This tubule is divided into three ciliated tubules, three proximal tubule branches, a common proximal tubule and a distal tubule, which in turn continues into the nephric duct. No intermediate segment is present. The length of the pronephric tubule is 12 mm, including the three branches of the ciliated tubules and proximal tubules. Primary urine is formed upon filtration from an external glomerulus, which is a convoluted capillary lined by podocytes, a specialization of the coelomic epithelium. From the coelom the filtrate is swept into the ciliated tubules. In the collecting duct system of the developing mesonephric nephron epithelial cells with conspicuous, apical osmiophilic granules appear in larvae of 9-10 mm. Heterocellularity of mixed intercalated (mitochondria rich) cells and principal cells is observed in the collecting duct system and nephric duct from a larval body length of 14 mm. As the proliferation of mitochondria-rich cells proceeds, the osmiophilic granules disappear and are completely absent from the adult amphibian mesonephros.     

Protonephridia and Metanephridia - their relation within the Bilateria

Two different kinds of nephridia occur within the Bilateria, protonephridia closed up by a terminal cell and metanephridia opening into the coelomic cavity. Both initially filter and subsequently modify intercellular fluids. Whereas metanephridia are strictly correlated to a coelom, proto-nephria occur in acoelomate as well as in coelomate organisms. Protonephridia of different bilaterian taxa correspond to each other in several structural features. Therefore, it is hypothesized that protonephridia are homologous organs throughout the Bilateria. They must have evolved once as one pair of monociliated organs orinatinng from the ectoderm and consistin of one terminal, one duct and one nephropore cell In the ground pattern of the Bilateria the cilium of the terminal cell has only one rootlet and is surrounded by resumably eight strengthened and elongated microvilli. Cilium and microvilli extend into the hollow cyinder of the terminal cell, which is oriented distally and is attached to the adjacent duct cell by desmosomes. This cylinder is perforated by clefts and represents the supporting structure of the filtration barrier consisting of extracellular matrix. In the Annelida and Phoronida, the metanehridia at the postlarval stages are ontogenetically preceded by protonephridia in the larva, but far reaching structural and developmental differ ences exist between the metanephridia of both. In horonids the rotonephrdial duct of the larva is retained in the postlarva and acquires a coelothelially derived funnel, whereas in annelids the metanephridia are uniform organs orihating from a solid anlage, which is a repetition of the protonehridial anlage of the larva. The differences contradict a homology of the metanephridia in Annegda and Phoronida. We therefore have to conclude that metanephridia must have evolved indeendently, at least two times. The comparative analysis of nephridia in the Bilateria allows the following hyothesis: Pro tonephridia were evolved in a monohasic acoelomate organism in the stem fineage of the Bilateria. During the evolution of biphasic life cycles consisting of an acoelomate larva and a coelomate adult, the information about the differentiation of protonephridia has been preserved in the early acoelomate developmental (larval) stages. During postlarval development and the formation of a coelom the protonephridia have either been retained or modified into meta nephridia. Accordin to the differences between the metanehridia of phoronids and annelids, we emphasize that. tiere is no possibility to trace back all bilaterian taxa with a coelom to a common stem species.     

Structure and development of the nephridia of Tomopteris helgolandica (Annelida)

 Nephridial diversity is high in Phyllodocida (Annelida) and ranges from protonephridia to metanephridia. The nephridia of Tomopteris helgolandica (Tomopteridae) can be characterized as metanephridia which bear a multiciliated solenocyte. This cell is medially apposed to the proximal part of the nephridial duct and bears several cilia, each of which is surrounded by a ring of 13 microvilli. An extracellular matrix connects the microvilli and thus leads to the impression of a tube surrounding the central cilium. Each tube separately enters a subjacent duct cell and the cilia extend into a cup-shaped compartment within the duct cell. This compartment is not connected to the duct. The funnel consists of eight multiciliated cells and is connected to the nephridial duct, which initially runs intercellularly and later percellularly. The last duct cell bears a neck-like process which pierces the subepidermal basal membrane and is connected to epidermal cells forming a small invagination, the nephropore. The nephridia of T. helgolandica develop from a band of cells and all structural components are differentiated at an early developmental stage. Further development is characterized by enlargment of the funnel, ciliogenesis in the solenocyte, merging of different sections of the duct and, finally, the formation of the nephropore. An evaluation of the nephridia of T. helgolandica leads to the hypothesis that the nephridial diversity in Phyllodocida can be explained by the retainment of different stages in the transition of protonephridia into metanephridia; this is caused by the formation of a ciliated funnel at different ontogenetic stages. Although the protonephridia in Phyllodocida are regarded as primary nephridial organs, protonephridia are also presumed to have evolved secondarily in progenetic interstitial species of the Annelida by an incomplete differentiation of the nephridial anlage. Accepted: 18 December 1996     

Ultrastructure of the Protonephridia in the Dorvilleid Polychaete Apodotrocha progenerans (Annelida)

The achaetous dorvilleid polychaete Apodotrocha progenerans Westheide & Riser, 1983, possesses several pairs of segmentally arranged protonephridia. They consist of a blindly ending terminal cell and three tubule (emission) cells. The terminal cell is a flame bulb with unusual filtration area consisting of interdigitated pedicel-like projections. Each cell has its own tuft of flagella; and the emission channel is intracellular. The tube-shaped 'seamless' cells are slotted into each other like water-pipes.     

Histochemical detection of sugar residues in the chick embryo mesonephros with lectin-horseradish peroxidase conjugates

Fragments of mesonephros were taken from chick embryos and studied from the 4th to the 21st day of incubation. A battery of seven different horseradish peroxidase-labelled lectins was used to study the distribution of carbohydrate residues in glycoconjugates along the mesonephric nephron during the period of excretory activity and the period of involution. ConA and WGA reacted at every site of the nephron thus showing the ubiquitous presence of alpha-D-mannose and N-acetyl-D-glucosamine. SBA was a good marker of the proximal tubule. Other lectins, such as PNA and LTA, reacted only for a short time at some sites during the considered period of incubation. The presence of sialic acid was detected in the podocytes, capillary wall and mesangial cells. From the 10th-11th day of incubation changes were noted in the proximal tubule as shown by PNA reactivity. This may be significant as regards the exact stage of incubation during which the involution of mesonephros begins.     

Ultrastructure and relationship between protonephridia and metanephridia in Phoronis muelleri (Phoronida)

Summary The actinotrocha of Phoronis muelleri has one pair of ectodermally derived, monociliated protonephridia. The duct runs mainly between the epidermis and the lining of the hyposphere coelom, pierces the septum and extends into the blastocoel. The proximal part is branched and closed up by terminal complexes consisting of two morphologically different cells which both serve filtration. During metamorphosis, the terminal complexes and the branches of the duct are cast off. The cells degenerate, pass into the remaining duct and are endocytosed by the duct cells. After metamorphosis the remaining part of the protonephridial duct is U-shaped, blindly closed and borders on the prospective lophophoral vessel. In a later stage the duct receives a ciliated funnel, which consists of monociliated epithelio-muscle cells and is a derivative of the lining of the metacoel. Thus, a part of the protonephridial duct of the larva and the whole metanephridial duct of the adult are identical. Aspects of a possible homology between phoronid nephridia and such organs in other bilaterians are discussed.     

Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

ABSTRACT: BACKGROUND: Two types of excretory systems, protonephridia and metanephridial systems are common among bilaterians. The homology of protonephridia of lophotrochozoan taxa has been widely accepted. In contrast, the homology of metanephridial systems -- including coelomic cavities as functional units -- among taxa as well as the homology between the two excretory systems is a matter of ongoing discussion. This particularly concerns the molluscan kidneys, which are mostly regarded as being derived convergently to the metanephridia of e.g. annelids because of different ontogenetic origin. A reinvestigation of nephrogenesis in polyplacophorans, which carry many primitive traits within molluscs, could shed light on these questions. RESULTS: The metanephridial system of Lepidochitona corrugata develops rapidly in the early juvenile phase. It is formed from a coelomic anlage that soon achieves endothelial organization. The pericardium and heart are formed from the central portion of the anlage. The nephridial components are formed by outgrowth from lateral differentiations of the anlage. Simultaneously with formation of the heart, podocytes appear in the atrial wall of the pericardium. In addition, renopericardial ducts, kidneys and efferent nephroducts, all showing downstream ciliation towards the internal lumen, become differentiated (specimen length: 0.62 mm). Further development consists of elongation of the kidney and reinforcement of filtration and reabsorptive structures. CONCLUSIONS: During development and in fully formed condition the metanephridial system of Lepidochitona corrugata shares many detailed traits (cellular and overall organization) with the protonephridia of the same species. Accordingly, we suggest a serial homology of various cell types and between the two excretory systems and the organs as a whole. The formation of the metanephridial system varies significantly within Mollusca, thus the mode of formation cannot be used as a homology criterion. Because of similarities in overall organization, we conclude that the molluscan metanephridial system is homologous with that of the annelids not only at the cellular but also at the organ level.     

Organization of the pronephric kidney revealed by large-scale gene expression mapping

Background

The pronephros, the simplest form of a vertebrate excretory organ, has recently become an important model of vertebrate kidney organogenesis. Here, we elucidated the nephron organization of the Xenopus pronephros and determined the similarities in segmentation with the metanephros, the adult kidney of mammals.

Results

We performed large-scale gene expression mapping of terminal differentiation markers to identify gene expression patterns that define distinct domains of the pronephric kidney. We analyzed the expression of over 240 genes, which included members of the solute carrier, claudin, and aquaporin gene families, as well as selected ion channels. The obtained expression patterns were deposited in the searchable European Renal Genome Project Xenopus Gene Expression Database. We found that 112 genes exhibited highly regionalized expression patterns that were adequate to define the segmental organization of the pronephric nephron. Eight functionally distinct domains were discovered that shared significant analogies in gene expression with the mammalian metanephric nephron. We therefore propose a new nomenclature, which is in line with the mammalian one. The Xenopus pronephric nephron is composed of four basic domains: proximal tubule, intermediate tubule, distal tubule, and connecting tubule. Each tubule may be further subdivided into distinct segments. Finally, we also provide compelling evidence that the expression of key genes underlying inherited renal diseases in humans has been evolutionarily conserved down to the level of the pronephric kidney.

Conclusion

The present study validates the Xenopus pronephros as a genuine model that may be used to elucidate the molecular basis of nephron segmentation and human renal disease.     

The larval nephridia of the brackish-water polychaete,Nereis diversicolor

The larval nephridia of the brackish-water polychaete Nereis diversicolor are described for the first time, and have been studied to determine if their times of development and structural characteristics are consistent with a role in the osmotic regulation of the larva. As shown in serial paraffin sections and by interference-contrast optics, the nephridia of the three-setiger larva consist of a single pair of very large metanephridia, arising in the 3rd larval setiger, but with their elongated terminal ducts and coiled ciliated tubules pushed forward into the 2nd setiger; their open metanephrostomes and anterior anchoring filaments lie dorsal to the 2nd set of setae. In contrast, the definitive or juvenile metanephridia, arising in the 4th and subsequently formed setigerous segments, have short terminal ducts and coiled ciliated tubules confined to the segments on which their external nephropores open; their nephrostomes are ventrally located and open into the rear of the next anterior segment. These findings are in contrast to the claims of Edouard Meyer (1887), who described two pairs of closed protonephridia in the 2nd and 3rd larval setigers of Perinereis cultrifera. Although it is not excluded that the single larval pair of metanephridia of N. diversicolor may arise as protonephridia, Meyer's claim of two pairs of larval protonephridia was an observational error. The larval nephridia of the marine Platynereis dumerilii resemble in form, but are considerably smaller than, those of N. diversicolor. It is concluded that the hypertrophied pair of larval metanephridia of N. diversicolor is an evolutionary adaptation to existence in habitats of low and unpredictably varying salinity. Their development occurs irrespective of the prevailing salinity; hence, it must be genetically determined.     

Cell junctions in the renal tubule of a fresh-water teleost,Salmo gairdneri Rich.

Summary Cell junctions in the renal tubule of the fresh-water rainbow trout were studied with thin-section and freeze-fracture techniques. Gap junctions were restricted to the proximal tubule, which is consistent with other vertebrate classes. Segments I and II of the proximal tubule and the collecting tubule/collecting duct system exhibited a well-developed zonula occludens with anastomosing strands. The distal segment showed a narrow zonula occludens composed of few parallel strands. The structure of the occluding junctions along the renal tubule of this teleost displays several similarities with the pattern of the zonulae occludentes in the amphibian and the mammalian nephron. From these observations, in conjunction with available data from other vertebrate classes, it can be concluded that in the proximal tubule the development of a deep and complex zonula occludens is a general feature of cold-blooded vertebrates.     

扩张莫尼茨绦虫(绦虫纲:圆叶目)的原肾管及原肾管概念的评述

本研究应用透射电子显微镜研究了扩张莫尼茨绦虫原肾管的细胞学特征 ,莫尼茨绦虫原肾管的焰茎球为一个过滤器结构 ,类似于“挡河坝”样构造 ,此构造由端细胞和近管细胞外突形成的肋条 (或称杆 )相互交错排列而成。肋条之间由细胞外物质构成的“膜”结构连接 ,过滤作用通过该“膜”发生。焰细胞与近管细胞交界处有裂缝或孔与细胞外的结缔组织 (实质组织 )相通 ;原肾管的毛细排泄管细胞质索之间没有隔状联结 ;毛细排泄管及排泄管的管腔内有大量珠状微绒毛突起以增加表面积。从扩张莫尼茨绦虫及其它一些无脊椎动物原肾管的研究结果表明 ,原原肾管概念将焰细胞作为封闭的盲端已不再合适 ,需要进行修订 ,建议修订为 :原肾管是一种焰细胞系统 ,通常由焰细胞、管细胞和肾孔细胞组成 ,焰茎球作为过滤装置与周围的结缔组织 (实质组织 )有或没有裂缝 (孔 )相通