Divergent Pathways of Ammonia and Urea Production and Excretion during the Life Cycle of the Sea Lamprey.

Little is known about nitrogenous waste (N waste) handling and excretion () during the complex life cycle of the sea lamprey (), an extant jawless fish that undergoes a complete metamorphosis from a filter-feeding larva (ammocoete) into a parasitic juvenile that feeds on the blood of larger, jawed fishes. Here, we investigate the ammonia- and urea-handling profiles of sea lampreys before, during, and after metamorphosis. The rates of ammonia excretion () and urea excretion () significantly decreased after the onset of metamorphosis, with the lowest rates observed during midmetamorphosis.

Thyroid hormone and retinoid X receptor function and expression during sea lamprey (Petromyzon marinus) metamorphosis.

Sea lampreys (Petromyzon marinus) are members of the ancient class Agnatha and undergo a metamorphosis that transforms blind, sedentary, filter-feeding larvae into free-swimming, parasitic juveniles. Thyroid hormones (THs) appear to be important for lamprey metamorphosis, however, serum TH concentrations are elevated in the larval phase, decline rapidly during early metamorphosis and remain low until metamorphosis is complete; these TH fluctuations are contrary to those of other metamorphosing vertebrates. Moreover, thyroid hormone synthesis inhibitors (goitrogens) induce precocious metamorphosis and exogenous TH treatments disrupt natural metamorphosis in P.

The influence of acclimation temperature on the lipid composition of the larval lamprey, Petromyzon marinus, depends on tissue and lipid class.

This study was designed to examine the effect of thermal acclimation on the lipid composition of fat depot organs the liver and kidneys of larval sea lamprey, Petromyzon marinus. We found that 21 °C-acclimated larvae possessed lower total lipid amounts in the liver (39% lower) and kidneys (30% lower) than 13 °C-acclimated larvae. Relatively lower lipid contents in the liver and kidneys of 21 °C-acclimated lamprey primarily resulted from a reduction in stored lipid reserve, triacylglycerol, but not the structural lipid, phospholipid.

Cholangiocyte apoptosis is an early event during induced metamorphosis in the sea lamprey, Petromyzon marinus L.

Background: Research in biliary atresia has been hindered by lack of a suitable animal model. Lampreys are primitive vertebrates with distinct larval and adult life cycle stages. During metamorphosis the biliary system of the larval lamprey disappears.

Identity and distribution of immunoreactive adenohypophysial cells in the pituitary during the life cycle of sea lampreys, Petromyzon marinus.

Adrenocorticotropin (ACTH), melanotropins (MSHs), growth hormone (GH) and gonadotropin (GTH) have been identified or cloned from the pituitary gland of sea lampreys (Petromyzon marinus). The present study was designed to gain insights into the functional significance of these hormones through a description of changes in the occurrence and distribution of cells immunoreactive to their antibodies at several different stages of the sea lamprey life cycle. ACTH-like cells and MSH-like cells were distributed in the rostral pars distalis and the pars intermedia, respectively, throughout the life cycle from ammocoetes (larvae) to pre-spawning adults.

What is metamorphosis?

Metamorphosis (Gr. meta- "change" + morphe "form") as a biological process is generally attributed to a subset of animals: most famously insects and amphibians, but some fish and many marine invertebrates as well. We held a symposium at the 2006 Society for Integrative and Comparative Biology (SICB) annual meeting in Orlando, FL (USA) to discuss metamorphosis in a comparative context.

Shifting patterns of nitrogen excretion and amino acid catabolism capacity during the life cycle of the sea lamprey (Petromyzon marinus).

The jawless fish, the sea lamprey (Petromyzon marinus), spends part of its life as a burrow-dwelling, suspension-feeding larva (ammocoete) before undergoing a metamorphosis into a free swimming, parasitic juvenile that feeds on the blood of fishes. We predicted that animals in this juvenile, parasitic stage have a great capacity for catabolizing amino acids when large quantities of protein-rich blood are ingested. The sixfold to 20-fold greater ammonia excretion rates (J(Amm)) in postmetamorphic (nonfeeding) and parasitic lampreys compared with ammocoetes suggested that basal rates of amino acid catabolism increased following metamorphosis.

Cloning of stanniocalcin (STC) cDNAs of divergent teleost species: Monomeric STC supports monophyly of the ancient teleosts, the osteoglossomorphs.

Molecular cloning of teleost stanniocalcin (STC) cDNAs was undertaken in two species of order Osteoglossiformes of subdivision Osteoglossomorpha and one species of each of orders Cypriniformes and Perciformes within the subdivision Euteleostei. The elephantnose (Gnathonemus petersii) and the butterflyfish (Pantadon buchholzi) are basal teleosts in different osteoglossiforme suborders yet their 218 amino acid (aa) mature hormones, from prehormones of 249 and 251aa, respectively, have only 10 cysteine residues. A substitution for cysteine at the intermonomeric disulfide linkage site, implies that their STCs exist as monomeric peptides, as is the case with STC from another osteoglossormorph, arawana [Amemiya, Y.

The fish endocrine pancreas: review, new data, and future research directions in ontogeny and phylogeny.

The literature on the ontogeny and phylogeny of the endocrine pancreas of ray-finned fishes is summarized since the latest review in fish [Youson, J.H., Al-Mahrouki, A.

Patterns of proopiomelanotropin and proopiocortin gene expression and of immunohistochemistry for gonadotropin-releasing hormones (lGnRH-I and III) during the life cycle of a nonparasitic lamprey: relationship to this adult life history type.

There are two adult life history types among lamprey species, nonparasitic and parasitic, with the former commencing the final interval of sexual maturation immediately after metamorphosis. There are no extensive studies that directly compare hormone profiles during the life cycles of nonparasitic and parasitic lamprey species, yet such data may explain differences in development, reproductive maturation, and feeding status. The present study uses immunohistochemistry to show the life cycle profiles for gonadotropin-releasing hormones (GnRH-I and -III) in the brain of the nonparasitic species, the American brook lamprey, Lampetra appendix, for comparison with the extensive, published, immunohistochemical data on these hormones in the parasitic species, the sea lamprey, Petromyzon marinus.

Expression of neuropeptide Y family peptides in the brain and gut during stages of the life cycle of a parasitic lamprey (Petromyzon marinus) and a nonparasitic lamprey (Ichthyomyzon gagei).

The long-term objective of our research is to show that internal factors may be key to triggering metamorphosis and directing the life history types in lampreys (parasitism versus nonparasitism). Since neuropeptide Y family peptides are key players in the endocrine-mediated feeding and reproductive events in mammals, a role for these peptides in the control of feeding behavior and development can be predicted for lampreys. We have investigated the expression pattern of these peptides in the brain and in the gut during different stages of the life cycle of the parasitic lamprey, Petromyzon marinus, and the nonparasitic lamprey, Ichthyomyzon gagei.

Trends in the evolution of the proenkephalin and prodynorphin genes in gnathostomes.

The opioid/orphanin gene family provides a model system for analyzing the outcomes of genome duplication events. Recent studies on the proenkephalin gene provide additional evidence that the organizational plan for this gene has been conserved throughout the extensive radiation of the gnathostome vertebrates. However, an analysis of the amino acid sequence of proenkephalin from the zebrafish, Danio rerio, suggests that novel forms of this opioid precursor may be evolving in teleosts.

Lamprey parasitism of sharks and teleosts: high capacity urea excretion in an extant vertebrate relic.

We observed 10 sea lampreys (Petromyzon marinus) parasitizing basking sharks (Cetorhinus maximus), the world's second largest fish, in the Bay of Fundy. Due to the high concentrations of urea in the blood and tissues of ureosmotic elasmobranchs, we hypothesized that sea lampreys would have mechanisms to eliminate co-ingested urea while feeding on basking sharks. Post-removal urea excretion rates (J(Urea)) in two lampreys, removed from separate sharks by divers, were initially 450 ( approximately 9000 micromol N kg-1 h-1) and 75 times ( approximately 1500 micromol N kg-1 h-1) greater than basal (non-feeding) rates ( approximately 20 micromol N kg-1 h-1).

Primary structure of stanniocalcin in two basal Actinopterygii.

The primary structure of stanniocalcin (STC), the principal product of the corpuscles of Stannius (CS) in ray-finned fishes, was deduced from STC cDNA clones for two species of holostean, the gar, Lepisosteus osseus and the bowfin, Amia calva. Overlapping partial cDNA clones were amplified by polymerase chain reaction (PCR) from single-strand cDNA of the CS. Excluding the poly(A) tail, the cDNAs of 1863 base pairs [bp] (gar) and 914 bp (bowfin) contained the 5' untranslated region followed by the coding region and the 3' untranslated region.

Response by the corpuscles of Stannius to hypotensive stimuli in three divergent ray-finned fishes (Amia calva, Anguilla rostrata, and Catastomus commersoni): cardiovascular and morphological changes.

In accordance with their vital role in cardiovascular physiology () corpuscles of Stannius (CS) from two teleosts and an holostean species showed marked and consistent degranulation and exocytotic responses to hypotensive stimuli. In eels (Anguilla rostrata LeSueur) acute blood withdrawal (hypovolemic hypotension) was followed by a prompt decrease in cardiac output (CO) and dorsal aortic pressure (P(DA)), a compensatory tachycardic response and an increase in systemic vascular resistance (R(SYS)). Isovolemic hypotension induced by papaverine i.

Effect of alloxan and insulin immunoneutralization on circulating thyroid hormone levels in larval landlocked sea lampreys, petromyzon marinus.

The effects of alloxan, an insulin (INS)-secreting cell toxin, and INS immunoneutralization on circulating levels of thyroid hormones (thyroxine, T(4); triiodothyronine, T(3)) were examined in larval landlocked sea lampreys, Petromyzon marinus. Animals were injected intraperitoneally with either (Experiment 1) saline (0.6%) or alloxan (20 or 200 microg/g body weight), or with (Experiment 2) normal rabbit serum or anti-lamprey INS.

Cloning of a functional vitamin D receptor from the lamprey (Petromyzon marinus), an ancient vertebrate lacking a calcified skeleton and teeth.

The nuclear vitamin D receptor (VDR) mediates the actions of its 1,25-dihydroxyvitamin D(3) ligand to control gene expression in terrestrial vertebrates. Prominent functions of VDR-regulated genes are to promote intestinal absorption of calcium and phosphate for bone mineralization and to potentiate the hair cycle in mammals. We report the cloning of VDR from Petromyzon marinus, an unexpected finding because lampreys lack mineralized tissues and hair.

Identification of growth hormone in the sea lamprey, an extant representative of a group of the most ancient vertebrates.

GH was identified in the sea lamprey, an extant representative of a group of the most ancient vertebrates, the Agnatha. A putative GH-cDNA was cloned from the pituitary by RT-PCR. The entire coding region comprised an open-reading frame of 203 amino acids (aa).

KClO(4) inhibits thyroidal activity in the larval lamprey endostyle in vitro.

An in vitro experimental system was devised to assess the direct effects of the goitrogen, potassium perchlorate (KClO(4)), on radioiodide uptake and organification by the larval lamprey endostyle. Organification refers to the incorporation of iodide into lamprey thyroglobulin (Tg). Histological and biochemical evidence indicated that endostyles were viable at the termination of a 4h in vitro incubation.

Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution.

It has been proposed that two events of duplication of the entire genome occurred early in vertebrate history (2R hypothesis). Several phylogenetic studies with a few gene families (mostly Hox genes and proteins from the MHC) have tried to confirm these polyploidization events. However, data from a single locus cannot explain the evolutionary history of a complete genome.

Stanniocalcin from an ancient teleost: a monomeric form of the hormone and a possible extracorpuscular distribution.

Stanniocalcin (STC) is a homodimeric glycoprotein hormone implicated in calcium and phosphate regulation in both teleost fish and mammals. In the present study, immunostaining with salmon STC antiserum demonstrated that STC cells were localized in both the corpuscles of Stannius (CS) and in specific cells of the distal renal tubules of the silver arawana, Osteoglossum bicirrhosum, an ancient ray-finned fish (actinoptergian) and basal teleost (Order Osteoglossiforme). The morphology of these STC-immunoreactive kidney cells was similar to renal 'chloride' (mitochondrial-rich) cells.

Differences in the fatty acid composition of larvae and metamorphosing sea lampreys, Petromyzon marinus.

This study was designed to evaluate biochemical changes in the fatty acid (FA) compositions of selected lipid depot (kidney and liver) and absorption (intestine) organs in larvae and metamorphosing sea lamprey, Petromyzon marinus. Palmitic or stearic acids were generally the predominant saturated fatty acids (SFA) before and during metamorphosis, but the greatest proportion of myristic acid occurred in renal triacylglycerol (TG). Monoenes, dienes, and polyenes consist mainly of 16:1, 18:1, and 20:1, 18:2 and 20:2omega6, and 18:4omega3, respectively.

The endocrine cells in the gastroenteropancreatic system of the bowfin, Amia calva L.: an immunohistochemical, ultrastructural, and immunocytochemical analysis.

The gastroenteropancreatic (GEP) endocrine system of bowfin (Amia calva) was described using light and electron microscopy and immunological methods. The islet organ (endocrine pancreas) consists of diffusely scattered, mostly small islets and isolated patches of cells among and within the exocrine acini. The islets are composed of abundant, centrally located B cells immunoreactive to bovine and lamprey insulin antisera and D cells showing a widespread distribution and specificity to somatostatin antibodies.

Proteins immunoreactive with antibody against a human leptin fragment are found in serum and tissues of the sea lamprey, Petromyzon marinus L.

An affinity-purified, polyclonal antibody raised against a peptide corresponding to amino acids 137-156 at the carboxy terminus of human leptin (16 kD) was used to search for immunoreactive protein(s) in the lamprey, Petromyzon marinus. Immunoblots of serum from different phases of the life cycle showed the presence of a 65-kD immunoreactive protein in the larvae and all stages of metamorphosis but not in feeding juvenile and upstream migrant adults. Extracts of tissues known to store fat were also examined using the same antibody.

Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes.

Metamorphosis is a developmental strategy used by only a small number of extant fishes and little is known about its phylogenetic development during the evolution history of this large group of vertebrates. The present report provides a putative evolutionary history of metamorphosis in the lamprey, an extant agnathan with direct descendancy from some of the oldest known vertebrates. The study reviews recent data on the role of the thyroid gland and its hormones in metamorphosis, summarizes some recent views on the evolution of the endostyle/follicular thyroid in lampreys, and provides new data on the content of two gonadotropin-releasing hormones (GnRH-I and -III) in brain during goitrogen-stimulated, precocious metamorphosis.