Immunity in lamprey. I. Production of haemolytic and haemagglutinating antibody to sheep red blood cells in Japanese lampreys.
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The haematopoietic supraneural organ of adult, sexually immature river lampreys (Lampetra fluviatilis [L.] Gray) with particular reference to azurophil leucocytes.
The haematopoietic tissue in the supraneural organ of the freshwater river lamprey (Lampetra fluviatilis L. Gray) was studied in sexually immature animals. Besides erythro- and granulopoietic elements, macrophages, reticular cells, fibroblasts and glycogen-rich fat cells were seen. Developing granulocytes of the lamprey contain one type of azurophil granules originating from small cytoplasmic (Golgi) vesicles. The lamprey's azurophil granulocytes seem to be homologous with those of fishes. However, the granulocytes of fishes, studied thus far, show granules with only one type of inclusion, whereas in lamprey the granulocyte inclusions are variable in size and shape. Thus, lamprey granulocytes are, in this respect, reminiscent of similar cells of higher vertebrates. The PAS and alkaline phosphatase reactions, common markers of vertebrate neutrophil leucocytes, are very weak in the haematopoietic tissue granulocytes of the lamprey, and intense in the blood cells of the same animal. Lamprey granulocytes, similarly to the granulocytes of Chondrostei and Elasmobranchiata, do not stain with peroxidase, naphthol-AS-D-chloroacetate esterase and sudan black B. The haematopoietic tissue contains a relatively high number of degenerated granulocytes.
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Comparative study of the monoamine neuron system in the spinal cord of the lamprey and hagfish.
Spinal cords of the lamprey and hagfish were fluorescence histochemically and electron microscopically examined. Ventrally to the central canal of both cyclostomes, yellow fluorescence bound to small to medium sized neurons was observed. In the lamprey only, weakly blue-green fluorescent subependymal cells were seen just beneath the central canal. In the ventral floor of their spinal cord, yellow fluorescent varicosities were observed; their density was much higher in the lamprey than in the hagfish. The lateral surface of the hagfish spinal cord was marginated by a chain of yellow fluorescent varicosities. The yellow fluorescence was microspectrofluorometrically identified as fluorescence due to 5-HT. Electron microscopically, the 5-HT neurons contained many large dense-core vesicles. The 5-HT varicosities or terminals seen in the ventral zone of both cyclostomes possessed the large dense-core vesicles and small clear synaptic vesicles, which appeared as small dense-core vesicles after KMnO4 fixation. The terminal of the lamprey was nakedly situated on the ventral surface, while that of the hagfish was always covered by the superficial glial layer. This finding seems to favor the view that lamprey and hagfish should be divided into two different classes.
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[Composition and structure of the chief gangliosides in the brain of the lamprey Lampetra fluviatilis].
It has been shown that 4-sphingenine is the main sphingoid in lamprey brain gangliosides. Saturated and monoenoic fatty acids were found to predominate, the main fatty acids in the lamprey brain are presented by stearic (43-49% of total fatty acids) and oleic ones. N-acetylneuraminic acid is the only sialic acid found in gangliosides from the lamprey brain. Other components of ganglioside molecules are glucose, galactose and N-acetylgalactosamine. Two main lamprey brain gangliosides which constitute more than 90% of lipid-bound sialic acid, were found to be trisialogangliosides. It was shown that both gangliosides have the following structure in their molecules: (formula see text). They differ in the position of two other sialic acid residues. Data on lamprey brain gangliosides in the literature are practically absent. The data obtained in the present study confirmed the conclusions on changes in the hydrophobic part of ganglioside molecule in evolution of vertebrates and made it possible to define more exactly the molecular evolution of ganglioside carbohydrate component.
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Projections of lamprey spinal neurons determined by the retrograde axonal transport of horseradish peroxidase.
The spinal cords of larval sea lampreys (Petromyzon marinus) and adult river lampreys (Ichthyomyzon unicuspis) were injected with horseradish peroxidase through a transection 1 cm caudal to the last gill. Some animals also had a spinal hemisection 1 cm caudal to the injection. After recovery periods of 1 to 52 days, the spinal cords were treated with diaminobenzidene and hydrogen peroxide, and the projections of various cell types determined in wholemount slides. From these observations the following conclusions were drawn. Most dorsal cells (primary sensory cells) are bipolar with a long rostral projection and a short caudal projection of no more than 5-10 mm. Both processes travel in the ipsilateral dorsal column. Their peripheral processes enter the dorsal roots as branches of their central axons. Some dorsal cells send processes out three or more dorsal roots both rostral and caudal to the cell body. Myotomal motoneurons have characteristic locations in the medial gray column and send prominent transversely oriented dendrites into the lateral columns. A few motoneurons are unusually large. In addition to giant interneurons the majority of smaller rostrally projecting interneurons also have decussating axons. A recently described cell type, the oblique bipolar cell, appears to have an exclusively crossed rostral projection. Although most edge cells project rostrally, as many as 20% may have a caudal projection or both rostral and caudal projections. Edge cells project equally to the ipsilateral and contralateral spinal hemicord, but their processes do not extend more than about 18 mm in sea lamprey larvae and 37 mm in adult river lampreys. Lateral cells project exclusively to the ipsilateral caudal hemicord. A few cells which resemble lateral cells in location and in possessing large lateral dendrites, project rostrally. However, these have atypical morphologic features which probably distinguish them from true lateral cells. Thus far, regardless of cell type, all decussating axons seem to pass ventral to the central canal, while decussating medial dendrites pass dorsally.
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[Isolation and several properties of the glyceraldehyde-3-phosphate dehydrogenase from the muscles of the lamprey Lampetra fluviatillis].
Procedure for isolation of electrophoretically homogeneous, crystalline glyceraldehyde-3-phosphate dehydrogenase from lamprey muscles is described. Amino acid composition of the enzyme was investigated and compared with that of the same dehydrogenase from other sources. With respect to its secondary structure and kinetic parameters, the lamprey enzyme does not significantly differ from those of other animals. Activation energy for the lamprey enzyme is lower than for the same enzyme from endothermic animasl. "Temperature modulation" of Michaelis constant described in the literature, was not confirmed for the lamprey enzyme in the range of physiological pH values.
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[Fatty acids of the cerebrosides (1-beta-glycosylceramides) and sulfatides (sulfoglycosylceramides) of the brain of the river lamprey Lampetra fluviatilis].
The analysis of the fatty acids of cerebrosides and sulfatides from the brain of the lamprey L. fluviatilis has been carried out. Only normal fatty acids were revealed by TLC of total methyl esters of the fatty acid of cerebrosides and sulfatides. The hydroxy fatty acids are apparently absent. The composition of the normal fatty acids of cerebrosides and sulfatides is very similar. TLC revealed fatty acids containing from 14 to 27 C mainly saturated and small amount of monoenes. The fatty acid pattern of cerebrosides and sulfatides from lamprey brain resembles that from the brain of other vertebrates. The peculiarity of the fatty acid composition of these glycolipids in the lamprey brain is the high proportion of short chain (C14--C18) saturated acids, especially of palmitic acid. The fatty acid composition of cerebrosides and sulfatides from lamprey brain which does not contain myelin is rather similar to that of mammalian brain in early development before the onset of myelination.
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Divergence of Leptin Receptor and Interleukin-6 Receptor Subunit b in Early Vertebrate Evolution and Physiological Insights from the Sea Lamprey.
Current knowledge of class-I cytokine receptors comes primarily from studies in jawed vertebrates (gnathostomes), and their origin and evolution remain unresolved. In this study, we identified a leptin receptor-like sequence (LepRL) and three interleukin-6 receptor subunit b-like sequences (IL6RBL) from a jawless vertebrate (cyclostome), the sea lamprey (Petromyzon marinus). Based on structural, phylogenetic, and syntenic analyses, we deduced that these lamprey receptors are likely distinct ohnologs to gnathostome LepR and IL6RB-related receptors, respectively, that arose in the two rounds of vertebrate whole-genome duplication (1R and 2R). Notably, lamprey LepRL likely originated from a different 1R progenitor than the one giving rise to gnathostome LepR during cyclostome hexaploidization. Differential patterns in mRNA expression of LepRL and IL6RBLs were observed among adult tissues, during larval metamorphosis, and in response to juvenile feeding. Feeding stimulated hepatic expression of LepRL and IL6RBL (namely, IL6RBL1) mRNAs in correlation with upregulation of insulin-like growth factor mRNA, whereas brain LepRL and IL6RBL1 mRNA expression was correlated positively with neuropeptide Y but inversely with intestinal content in fed juveniles. Notably, these observations along with immunolocalization of LepRL in the hypothalamus suggest a role of leptin signaling in regulating energy balance that is conserved among vertebrates. Additionally, seawater exposure stimulated branchial LepRL expression coincident with increased expression of ion transporters in ionocytes, indicating a role of leptin signaling in osmoregulation. These findings provide new insight into the early evolution of class-I cytokine receptors and reveal diverse functions of the leptin signaling system in jawless vertebrate.
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[Autoradiographic and histochemical study of the intestinal epithelium of the Baltic lamprey].
The intestinal epithelium of the Baltic lamprey and its larva was studied. Glandular cells and absorbing cells simultaneously capable to synthesize polysaccharides were found histochemically in the composition of the epithelial layer. The cranial zone where glandular cells analogous to the cells of the pancreas were concentrated was revealed in the medial intestine of the larva. The rest of the intestine was devoid of specialized glandular cells. Using H3-thymidine as a precursor it was shown that in the cranial zone of the intestine the cambial cells were scattered diffusely throughout the whole epithelial layer and in other portions of the medial intestine the cambial zone was distinctly seen in the lateral portions of the intestine (the area of the fornix) where labelled nuclei were formed and mitoses took place. After injection of H3-thymidine poor incorporation of the isotope was found in the nuclei of solitary cells of some adult lampreys going to spawning. Uneven incorporation of S35-methyonine, used as a precursor, in the epithelium of the intestine and the liver of the adult lamprey was shown.
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Development of the renal corpuscle during metamorphosis in the lamprey.
The renal corpuscle of the adult lamprey, Petromyzon marinus L., is formed during the programmed period of metamorphosis. Development is initiated early in this metamorphic period and is marked by the synchronous formation and growth of rudimentary nephron units (RNU) from longitudinal cord of nephrogenictissue extending from the posterior tip of the degenerating larval kidney to the cloaca and connected to the peritoneal epithelium. Detachment of the RNU from the peritoneum involves autolysis and cell death and is accompanied by their branching into five or six hexagonally-arranged nephrons which radiate from the original point of attachment. Differentiation of the epithelial cells at the proximal ends of the nephrons is preceded by the widening of lateral intercellular spaces, the formation of tubular lumina (primitive urinary spaces), the loss of apical cell junctions, and the development of a capillary network with its associated mesangium. With the extension of the capillaries and mesangium between the proximal ends of adjacent undifferentiated nephrons, visceral epithelial cells (podocytes), with long cell processes (trabeculae) and slit membranes, make their appearance. The urinary spaces resulting from this form of development are lined by the epithelium of the dilated ends of the nephrons (nephric capsules). The cells of these capsules differentiate mainly into podocytes, but a few parietal cells connect to the draining tubule. This method of development explains the unique form of the renal corpuscle in the adult lamprey. Despite the type of morphogenesis, this renal corpuscle possesses the fine-structural features seen in the renal corpuscles of other vertebrates.
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Fine structure of the liver in the larval lamprey, Petromyzon marinus L.; hepatocytes and sinusoids.
The ultrastructure of hepatocytes, bile canaliculi, and hepatic sinusoids of the larval lamprey, Petromyzon marinus, was examined using thin-sectioned and freeze-fractured tissues. The liver is a "tubular gland" with hepatocytes arranged in a tubular fashion around large bile canaliculi. Hepatocytes are roughly conical in shape, with their tapered apices facing a bile canalicular lumen. They possess extensive rough and smooth endoplasmic reticulum, a well-developed Golgi complex, abundant mitochondria, and varying numbers of large secondary lysosomes. Both secondary lysosomes and the Golgi complex are concentrated in the apical or peribiliary cytoplasm, indicating a possible role in bile secretion. The apical surfaces of the hepatocytes bear numerous elongate microvilli and occasional cilia, which project into the bile canaliculi. The hepatocytes are joined, apically, by junctional complexes composed of zonulae occludentes and adhaerentes. In freeze-fracture, the zonulae occludentes are of variable apicobasal depth and consist of honeycomb-like meshworks of fibrils. Spaces of variable width frequently appear in the P-face grooves, indicating that the zonulae occludentes are "leaky." Numerous communicating (gap) junctions join the hepatocytes laterally. Varying numbers of lateral microvilli project into the intercellular spaces and, basally, the plasma membrane is deeply infolded, resulting in the formation of apparently interdigitating basal processes resting upon a thin basal lamina. Sinusoids are composed of both a heavily-fenestrated, continuous endothelium, and phagocytic reticulo-endothelial (Kupffer) cells. Depsite the difference in arrangement of their hepatocytes, the mammalian and lamprey livers show similar ultrastructural features.
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The hypothalamo-hypophysial system of the lamprey, Lampetra fluviatilis L. III. High-resolution radioautography of monoaminergic structures in neurohemal regions.
The distribution of monoaminergic structures was studied in the proximal neurosecretory contact region and neurohypophysis of the lamprey by light and electron microscopic radioautography. Only weak radioautographic reactions were found in the proximal neurosecretory contact region 1 h after injection of 3H-dopamine. High-resolution radioautography revealed some labeled neurosecretory terminals mainly in contact with the basement membrane of the connective tissue layer separating the proximal neurosecretory contact region from the hypophysial pars distalis. The number of silver grains as well as the number of neurosecretory terminals marked by the presence of labeled dopamine was much higher in the neurohypophysis of the same species. In the latter, labeled neurosecretory terminals were found in contact with the connective tissue layer containing blood vessels of the general circulation. Some neurosecretory terminals make synaptoid contacts with tanycyte perikarya and their basal processes. According to their ultrastructure and the size of their granules, the labeled neurosecretory terminals are identical with the B type terminals described in both neurohemal regions (transmission electron microscopy). No labeled neurosecretory terminals were observed in the proximal neurosecretory contact region and the neurohypophysis of lampreys treated with the serotonin precursor, 3H-5-hydroxytryptophan.
5-Hydroxytryptophan↗
Characterization of the myoglobin of the lamprey Petromyzon marinus.
Myoglobin has been identified in the myocardium of the lamprey Petromyzon marinus, one of the most primitive of all vertebrates. This protein was isolated by ammonium sulphate fractionation and purified by successive chromatography on Ultrogel AcA 54, DEAE-Sephadex and CM-23 cellulose. The molecule differs substantially from the monomeric hemoglobins found in the lamprey as evidenced by its elution profile on DEAE-Sephadex and the fingerprint pattern of its enzymically-produced peptides. The functional significance of this protein in Agnatha is discussed.
Amino Acid Sequence↗
Variability in maps of identified neurons in the sea lamprey spinal cord examined by a wholemount technique.
A technique is described for preparing toluidine blue-stained wholemounts of lamprey spinal cords. By this technique virtually all the neurons in the spinal cord can be studied with respect to their soma size and shape, their primary dendrites, and sometimes secondary dendrites and proximal portions of the axon. Several cell types previously studied physiologically and described by others in cross section are described in wholemounts. These are dorsal cells, giant interneurons, edge cells and lateral cells. In addition, several unique cell types are noted in wholemount which were previously unremarked upon. These include obliquely oriented bipolar cells, trident-shaped cells located mostly in the rostral two-thirds of the spinal gray column, and small neurons with cell bodies in the dorsal and ventral axon tracts. Edge cells, which had previously been described as having large cell bodies close to the lateral edge of the lateral axon tracts with large medially oriented dendrites, are shown to be quite heterogeneous in size, location of soma and dendritic tree configuration. By use of the wholemount technique, 4 spinal cords of large sea lamprey larvae, close to transformation, were mapped for lateral cells, giant interneurons and dorsal cells. Considerable variability was noted in numbers and locations of these cells. The possible significance of this finding for the development of the vertebrate nervous system is discussed.
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Estimates of cable parameters in lamprey spinal cord neurones.
1. Two micro-electrodes were used to penetrate giant interneurones in the isolated lamprey spinal cord. A brief (50--100 microsec) current pulse was applied to one electrode while the other recorded the voltage transient response. 2. A formal analysis of the voltage transient was achieved by the simplifying reduction of each neurone. Somas were treated as a parallel combination of resistance and capacitance. Dendrite trees were reduced to an equivalent cylinder (Rall, 1959). 3. The voltage transients were analysed according to the procedure suggested by Jack & Redman (1971b) to estimate the cable parameters governing the passive propagation of transmembrane potentials. Membrane time constant (tau m), dendritic to soma conductance ratio (rho 00), and electrotonic length (L) of the equivalent cylinder were estimated from these data. 4. In thirty-two interneurones it was possible to determine the membrane time constant, but rho 00 and L were determined in only twenty-two. 5. For the twenty-two neurones in which all cable parameters were estimated, the electrotonic length of the equivalent cylinder was similar to that found for cat spinal motoneurones (1--2 space constants). 6. Simulations of the voltage transient using the Rall model of the motoneurone as developed by Jack & Redman (1971b) resulted in a voltage response which closely ditted the experimental data. 7. These results suggest that the Rall model of the motoneurone accurately describes the propagation of passive transmembrane potentials in lamprey spinal cord neurones. It is further concluded that the time constant for soma and dendritic membrane is similar in these neurones.
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Effect of vasotocin on plasma free fatty acid level in the migrating anadromous sea lamprey.
The effect of injections of arginine vasotocin (AVT) on plasma free fatty acid (FFA) levels was studied in anadromous sea lampreys collected in the St. John River, New Brunswick, during their upstream spawning migration. Plasma FFA was significantly higher in lampreys injected with a single dose of 1 000 mU vasotocin/kg body weight than in those receiving only the vehicle solution, the difference being the greater at 90 than at 30 min post-injection. The significance of AVT in migration is discussed.
Acclimatization↗
[Biosynthesis of thyroglobulin in an adult lamprey, Lampetra planeri (Bloch)].
Thyroglobuline (Tg) biosynthesis has been studied in an adult fresh water lamprey Lampetra planeri (Bloch), by injection in coelomic cavity or by in vitro incorporation in follicles of branchial region of various radioactive labels: 125I-, 3H-leucine, 3H-mannose, 3H-galactose, N-acetyl mannosamine and 3H-N-acetylglucosamine. Labelling by all theses substances, present in Tg of mammals, proceeds efficiently in two hours. It has been demonstrated that the cyclostome studied synthetizes a 18 S iodinated glycoprotein analogous to Tg of higher vertebrates by its molecular size. It contains all the same hexose and N-acetyl derivatives of these in its sugar moiety and the same iodinated aminoacids. Purified 18 S Tg of the lamprey has been prepared; it is very poor in iodine (127I) and has a very low T3 and T4 content.
Acetylglucosamine↗
[Biosynthesis of thyroglobulin in the endostyle of larva (ammocoetes) of a fresh water lamprey, Lampetra planeri B1].
The biosynthesis of thyroglobulin (Tg) in larva of a fresh-water lamprey, Lampetra planeri B1. has been established. This glycoprotein presents the same characters as in thyroid follicles of adult lampreys, as shown by its 18-19 S sedimentation coefficient and by the incorporation (in vivo and in vitro experiments of 4, 12, 72 h) of 125I, 3H-leucine and 3H-galactose. 3-8 S fractions and a 12 S monomer are the precursors of the 18-19 S protein. Total I % of Tg is very low (0.002 %) ; about 5 % of 125I are present in thyroid hormones (T3 and T4) in the 125I-labeled protein. The biosynthesis of 18-19 S Tg proceeds in larvs before the morphological differentiation of thyroid cells and follicles after metamorphosis. However, the biosynthesis of this protein is much slower in the endostyle of larvs, in which a primitive mechanism of storage is poorly efficient, compared to the accumulation of Tg in the colloid of the follicles of adults.
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