Jørgen Gomme

Recycling ofd-glucose in collagenous cuticle: A means of nutrient conservation?

SummaryTransport by an epithelium, possessing an accumulating, saturable transport system in the apical membrane as well as a finite Fick permeability to the transported solute, was considered in the steady state in the case of zerocis concentration, and in the presence of a peripheral diffusion resistance in a layer apposing thecis face of the tissue (unstirred solution or structural coating). Under suitable conditions, the combination of peripheral diffusion resistance and accumulating epithelial transport may lead to recycling of solute at thecis face of the epithelium. This causes a decrease of the effective permeability to diffusionaltrans-cis flow across the tissue. The phenomenon is discussed in terms of epidermald-glucose transport by the integument of aquatic animals with a collagenous cuticle, such as the seawater-acclimated polychaete wormNereis diversicolor. The recycling phenomenon may be of significance to other epithelia with the function of maintaining large concentration gradients of permeating substances.

d-Glucose transport across the apical membrane of the surface epithelium inNereis diversicolor

SummaryEpidermald-glucose transport was investigatedin vivo in the brackishwater polychaete wormNereis diversicolor. Transfer across the apical membrane is rate-limiting tod-glucose uptake, but the cuticle and/or mucus presents some resistance tod-glucose diffusion between bulk solution and transporting membrane. Maximald-glucose influx is about 10−12 mol sec−1 per cm2 of apical plasmalemma. Under natural conditions (∼1 μm d-glucose in the medium), backflux from the epidermal transport pool is negligible, but a significant paracellular outflux may occur.d-glucose influx across the apical membrane is Na+-dependent and completely inhibitable by phlorizin and harmaline; phloretin is less effective, and cytochalasin B has no effect. Influx is moderately depressed by KCN and iodoacetate. α-methyl-d-glucopyranoside is an effective substitute ofd-glucose in transport. Animals acclimated to a low salinity, in which epidermal salt transport takes place, show a marked decrease ofd-glucose transport capacity. On transfer of animals from a high to a low salinity, or vice versa, the corresponding change of influx occurs after a time-lag of at least an hour. Permeability of the epidermis to simple diffusion ofd-glucose is 8×10−8 cm sec−1 (on basis of gross epidermal area).

Transport of exogenous organic substances by invertebrate integuments: the field revisited.

The notion that some marine invertebrates can use integumental uptake of organic compounds as a nutritional supplement dates back to the late 19th and early 20th centuries. This article provides a brief overview of more than a century’s research, as it relates to significant stages in the development of experimental methods and concepts of general physiology. Emphasis is placed on changing paradigms and on the interplay between this specialized field of investigation and the mainstream of physiological thought. The present status of the field is summarized. The general consensus is challenged on the basis of previously published and new data from the author’s laboratory. Particular emphasis is placed on data pointing toward an ultra-rapid turnover of amino acids in part of the epidermal space of the polychaete worm Nereis diversicolor. It is suggested that intra-epidermal L-alanine is compartmentalized metabolically or physically, and the consequences of this proposition are discussed in view of the general concepts of secondary active transport and intracellular isosmotic regulation. Future studies in this area of comparative physiology should concentrate not only on the molecular characteristics of the transporter proteins, but also on the way their function is integrated in the cellular physiology of the transporting cells. J. Exp. Zool. 289:254–265, 2001.

Specificity of d-glucose transport by the apical membrane of Nereis diversicolor epidermis

(1) The specificity of d-[6-3H]glucose influx by a Na+-dependent and phlorizin-sensitive transport system in the apical epidermal membrane of the polychaete worm, Nereis diversicolor, was investigated in vivo. (2) The inhibitory effect of eleven d-glucose analogues on d-[6-3H]glucose influx from a 5 μM external concentration was recorded. The inhibitors (each tested at 5, 50, 500 and 5000 μM) were selected to illuminate the configurational requirements for interaction with the d-glucose transport system. (3) The following compounds were found to be significant inhibitors: methyl α-d-glucoside, methyl β-d-glucoside, d-galactose, 3-O-methyl-d-glucose, 2-deoxy-d-glucose, d-xylose, myo-inositol, β-d-fructose; the effect was graded according to inhibitor concentration. l-Glucose also inhibited d-glucose influx but to the same extent at all four concentrations tested, suggesting transport site heterogeneity. d-Mannose and l-arabinose did not inhibit influx. (4) The most potent inhibitor, methyl-α-d-glucoside, was itself a substrate, and its transport was inhibited by phlorizin and d-glucose, as well as by substitution of Na+ in the incubation medium with Li+ or choline+. (5) We conclude that the specificity of the Na+-dependent d-glucose transporter in the apical epidermal membrane of Nereis is similar to that in the apical membrane of vertebrate small intestinal and proximal tubular epithelium, and in the tapeworm integument.

Permeability and Epidermal Transport

Annelids occur in a variety of aquatic and terrestrial habitats. Most species, particularly among the polychaetes, are marine osmoconformers, in which the integument takes little or no part in creating an extracellular ionic milieu different from the ambient one. Integumentary permeability and transport processes may be involved, however, in other phenomena, including the passive changes and ensuing regulation of body volume under a fluctuating external salinity. A few species penetrate into brackish-waters, and in some of these the integument plays a decisive part in hyperosmotic regulation of the extracellular fluid. The same applies to those forms, notably among oligochaetes and leeches, which thrive in freshwater or water-logged soils. At least in certain cases, ion transport across the body surface appears to be linked to nitrogen excretion as well as to the regulation of the acid-base status of the internal fluids, and hence indirectly to respiration. Not only the exchange of inorganic materials, but also the transport of nutrients by the epidermis depends on the osmoregulatory state of the animal. Some annelids have adopted a terrestrial way of life and have acquired the ability to evade desiccation and to regain liquid water efficiently across the body surface to compensate for evaporative losses. With regard to respiration, soils and litters, the typical terrestrial habitats, normally maintain quite high oxygen and low carbon dioxide tensions, which lessens the problem of diffusive integumental gas exchange. Conditions are different in aquatic habitats, primarily due to the limited solubility of oxygen; in addition, many aquatic annelids live in sediments under extremely oxygen-poor conditions, and often with a high level of total carbon dioxide.

Problems of interpreting integumental D-glucose fluxes by the integument of Schistosoma.

1. The parasitic trematode Schistosoma mansoni can take up glucose across its surface at a rate three times higher than the glucose uptake by the mucosal border of the rabbit ileum. 2. Washout of tritiated polyethylene glycol (M Wt 4000) indicated that it was being lost through the integument and that the gut contribution is very small. 3. There is a peripheral diffusion resistance that will profoundly influence any transepidermal solute transfer.