The metabolic potential of hepatocytes and kidney tissue in the little skate, Raja erinacea

Abstract

Isolated hepatocytes from the little skate (Raja erinacea) are characterized by a general low metabolic activity, which can be explained by the benthic lifestyle of the animal. Of the substrates tested, alanine, serine, and leucine are equally good oxidative substrates, and the highest rates of gluconeogenesis are achieved with alanine and glycerol as carbon sources. In both respects, lactate is a relatively poor substrate, and this probably reflects the low abundance of this potential energy source in the skate, even after bouts of anaerobic exercise. The long chain fatty acid oleate and glycerol are poor oxidative substrates for the hepatocytes. Experiments with 3-mercaptopicolinate, an inhibitor for phosphoenolypyruvate carboxykinase (PEP CK), reveal that serine is funneled into gluconeogenesis through the serinetransaminase pathway, and PEP CK is bypassed. In vitro, the skate liver cells display the potential to synthesize and export ketone bodies from precursors such as leucine or oleate, whereas added P-hydroxybutyrate is poorly oxidized.The skate liver appears to be geared towards export of ketone bodies while at the same time conserving glycerol carbon for lipid synthesis. Supplied with precursors such as bicarbonate, glutamine, and aspartate, the cells synthesize urea at a rate of 0.85 fimol/g/hr at 10°C. /3-Hydroxybutyrate can accelerate the rate of urea synthesis, probably by increasing the intramitochondrial availability of ATP. Unlike any other vertebrate kidney, the tissue of the little skate appears to play no role in glucose synthesis. Skate kidney is characterized by an active oxidative metabolism and a broad substrate preference, with lactate, serine, alanine, and @-hydroxybutyrate serving as equally good oxidative fuels.Elasmobranch fishes possess a number of metabolic features that make this ancient group of vertebrates ideal objects of study for evolutionary biologists and comparative physiologists alike. These unique features include the specific synthesis and use of urea as an osmoregulatory agent (Smith, '361, the maintenance of trimethylamine-N-oxide (TMAO) as an important osmolyte (Pang et al., '77), and the apparent lack of albumin synthesis in many species (Sulya et al., '61). Furthermore, a variety of metabolic traits sets the elasmobranchs apart from most other vertebrates: Elasmobranchs are generally osmoconformers; they appear to regulate the concentration of blood glucose even more poorly than teleost fishes (deRoos et al., '85); their blood is almost devoid of free fatty acids (Plisetskaya, '80) Since our interests lie with the elucidation of liver cell metabolism in the lower vertebrates, with special emphasis on teleost fishes, we became interested in the elasmobranchs as a substantially different model Address reprint requests to Thomas P. Mommsen, who is now

Adaptation, constraint, and the function of the gluconeogenic pathway

“…The sea (raven has a low liver lactate dehydrogenase titer and apparently does not elevate plasma lactate even after exhaustive exercise (see Walsh et al 1985). Low lactate gluconeogenesis was also found for the little skate (Raja erinacea; Table 4; Mommsen and Moon 1987). There is generally a direct correlation between the rates of glucose and C 0 2 production from lactate in fish, with the sea raven and skate being exceptions Mommsen 1986).…”

“…Teleosts do not possess the enzymes for ketogenesis (Zammit and Newsholme 1979), and elasmobranch hepatocytes have higher ketogenic rates with leucine than oleate (Mommsen and Moon 1987). Alteruse of alternate fuels.…”

Metabolic actions of glucagon-family hormones in liver

“…Together, the results imply that a non-hepatic target tissue for GLU is responsible for this phenomenon. In line with its action in mammals, bovine GLU also activates unreagenesis in isolated skate hepatocytes (Mommsen and Moon 1987).…”

Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland

“…Our results are discussed in the context of the in vivo role of the gland and mechanisms of possible upregulation of enzyme activities. fatty oxidation were generally low, substrates such as oleate (and leucine for that matter) could support a net export of ketone bodies from the liver (Mommsen and Moon, 1987). Likewise, isolated liver mitochondria of dogfish shark (Squalus acanthias) had a great capacity to produce ketone bodies from acetate, palmitoyl-CoA, pyruvate and alanine (Anderson, 1990).…”