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Lipoproteins from Plasma and Perivelline Fluid of the Apple Snail Pomacea Canaliculata Workshop

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Lipoproteins from Plasma and Perivelline Fluid of the Apple Snail Pomacea Canaliculata Workshop BIOCELL ISSN 0327 -9545 2002, 26(1): 111-118 PRINTED IN ARGENTINA Workshop: “Biology of Ampullariidae” Minireview Lipoproteins from plasma and perivelline fluid of the apple snail Pomacea canaliculata H. HERAS AND R.J. POLLERO Instituto de Investigaciones Bioquímicas de La Plata, INIBIOLP (CONICET- UNLP), Facultad de Medicina, UNLP, Calle 60 y 120, (1900) La Plata, Argentina. Key words: Lipoproteins; lipids; proteins, snail embryogenesis Introduction the phyllum Mollusca has received little attention. In fact, the lipoproteins of only one species of the classes Structural lipids, primarily phospholipids and ste- Bivalvia, Cephalopoda and Gastropoda were described rols, as well as energy-storage lipids such as up to date. In addition to the lipoproteins common to triacylglycerols are insoluble in water. In the aqueous males and females, there are female-specific lipopro- fluids of animals, they are carried as lipoproteins, com- teins, which appear in the hemolymph plasma during plexes of lipids bound to polypeptides. These water- vitellogenesis. They are similar to vitellins, the egg li- soluble lipoproteins can be separated into different poproteins that provide energy and nutrient for the de- classes, depending upon their hydrated densities. These veloping embryo. These egg storage molecules can also classes include very low density (VLDL), low density play a role in the growth and survival of larvae. Among (LDL), high density (HDL) and very high-density aquatic invertebrates, egg lipoproteins have been de- (VHDL) lipoproteins. The two first ones predominate scribed in crustaceans, sea urchins and molluscs (for a in the blood of vertebrates, while HDLs are the main review, see Lee, 1991). lipoproteins in invertebrate hemolymph. Lipid circula- The present review deals with the lipoproteins tion systems in invertebrates have been studied mainly present in hemolymph and perivitelline fluid of the snail in the phyla Arthropoda and Mollusca. In terrestrial in- Pomacea canaliculata, their lipid and protein composi- vertebrates, the mechanisms of lipid circulation are well tion, as well as their consumption during the embryo known in insects and comparatively less known in arach- development. This is the only Gastropoda species whose nids. The most studied group of aquatic invertebrates, plasma and egg lipoproteins were studied. Results are respect to lipoproteins, is the Crustacea and, in contrast, discussed comparatively with other invertebrates. Interorgan transport of lipids Address correspondence to: Dr. R.J. Pollero, INIBIOLP, Facultad Hemolymph of aquatic invertebrates usually has a de Medicina, UNLP, Calle 60 y 120, (1900) La Plata, ARGENTINA. Fax: (+54-221) 425 8988; E-mail: [email protected] low lipid content. The lipid concentration in P. Received on November 29, 2000. Accepted on November 13, 2001. Canaliculata plasma varies between 127 and 210 µg/ 112 H. HERAS and R.J. POLLERO ml and the values in hemocytes are within the range of Plasma lipoproteins 54 – 68 µg/ml hemolymph. The lipid content in hemolymph of P. canaliculata is very low when com- Labeled plasma of P. canaliculata was pared with that from other gastropods such as Planorbis ultracentrifuged in density gradients, fractionated, and corneus (Ottaviani, 1984) or Biomphalaria glabrata the total proteins, radioactivity and density were mea- (Fried et al., 1989). Nevertheless, values are similar to sured in isolated fractions. Fractions containing radio- those reported for plasma of bivalves living in the same activity and protein maxima, which indicated the oc- habitat (Pollero et al., 1985), which varies from 80 to currence of lipoproteins, were pooled and used to 260 µg/ml, and also for cephalopods (Heras and Pollero, analyze lipid and protein compositions, using radiochro- 1989). Variations in blood lipid composition in aquatic matographic and electrophoretic techniques, respec- invertebrates have been attributed to food intake and go- tively. nad maturity (Thompson, 1977). The scanty lipid con- On the basis of labeled cholesterol experiments, a centration in hemolymph of these invertebrates makes it cholesterol transporting HDL was detected, it was the rather difficult to study the mechanism of lipid trans- first lipoprotein reported for the gastropods (Pollero et port. This obstacle is overcome by using radioactive trac- al., 1992). Table I collect the lipid classes composition ers, so that plasma lipoproteins can be detected and their of this P.canaliculata plasma lipoprotein. The observa- relative importance in the transport of tracers or metabo- tion on the labeled-cholesterol transport system implies lites is determined. The low-lipid-content hemolymph of that the HDL transports the largest amount of this ste- P. canaliculata was labeled by in vivo injections of lipo- rol in the free form. Nevertheless, free sterol concen- somes containing 14C-cholesterol (Pollero et al., 1992) tration, as well as free fatty acids and triacylglycerols, or salts of 14C-palmitic acid (Garin and Pollero, 1995), reach moderate mass values in this plasma fraction, at different times of incubation, in order to investigate while phospholipids account for the highest percent- the possible occurrence of lipoproteins and their role and ages of the total lipids. Other lipids including a signifi- that of hemocytes in lipid transport. cant percentage of hydrocarbons, and small amounts of The hemolymphatic transport of lipids in associa- sterol esters, complete the lipid classes spectrum of this tion with hematic cells had been demonstrated for lipoprotein. triacylglycerol and cholesterol in a bivalve (Pollero et When the HDL is analyzed by electrophoresis un- al., 1985; Pollero, 1987; Pollero and Heras, 1989) and, der dissociating conditions, it shows a unique apoprotein as a secondary way of lipid transport in an octopus (Heras band with an apparent molecular weight of 70 kDa and Pollero, 1990). Nevertheless, such role of hemocytes (Garin, 1996). It points out a difference respect to the in lipid circulation does not seem to be important in P. HDL from O. tehuelchus, the other mollusc whose canaliculata, as it was demonstrated in experiments con- apolipoproteins were described. In octopus HDL three ducted in vivo. When 14C-cholesterol–containing lipo- polipeptides of 129, 230 and 340 kDa were detected, somes were injected into the snail foot and incubated, corresponding the last one to the monomer of hemocya- they were absorbed and incorporated into the hemolymph. nin. This observation suggested, for the first time, the The radioactivity was largely recovered in plasma and, in apoprotein role for this respiratory pigment (Heras and lesser amount, in the hemocytes. The low values of ra- Pollero, 1992), function of hemocyanin then corrobo- dioactivity found in hemocytes were attributed to a rated in arachnids (Cunningham and Pollero, 1996; plasma-cell interchange and not to any special function Cunningham et al., 1999). Nevertheless, hemocyanin’s of hematic cells in lipid transport (Pollero et al., 1992; role concerning the lipid transport in hemolymph of Garin and Pollero, 1995). This distribution of radioactiv- invertebrates cannot be generalised; upon the results ity among the hemolymph components indicates that the obtained in the P. canaliculata HDL, the role of interorgan transport of cholesterol is mostly performed hemocyanin as an apolipoprotein may be discarded. by plasma and, perhaps to a very lesser extent, by he- Protein/lipid ratio of P. canaliculata HDL, of about matic cells. A marked difference is shown between the 1.9, falls into the range presented by other HDLs from cholesterol transport in this snail and that of the bivalve different origins (Chapman, 1980). Concerning density Diplodon delodontus, where more than 40% of and lipid composition, the HDL from P. canaliculata hemolymphatic cholesterol circulates associated with may be compared with those HDLs isolated from the hemocytes (Pollero, 1987). We can conclude that the lipid bivalve D. Delodontus and from the cephalopod O. transport in P. canaliculata hemolymph is mostly per- Tehuelchus, the only molluscs whose lipoproteins were formed via plasma lipoproteins. characterized. Density of the snail HDL is higher than LIPOPROTEINS OF APPLE SNAIL 113 that of the clam and it is coincident with octopus HDL. lipoproteins, they have been also reported in some in- Each HDL differs in protein/lipid ratio, and perhaps this vertebrates. Lipoproteins ranging within density inter- explains the density differences. However, lipid and vals of 1.04 – 1.08 gr/ml, were isolated from the satur- protein compositions must also be considered. While niid silkmoth Hyalophora cecropia (Thomas and cholesterol and phospholipids are both the main lipid Gilbert, 1968), the clam D. Delodontus (Pollero and classes in clam and octopus HDLs, triacylglycerols are Heras, 1989) and O. tehuelchus (Heras and Pollero, significant components only in the clam. On the other 1990). In the housefly Musca domestica, the occur- hand, in the snail, phospholipids predominate, while rence of a lipoprotein tentatively identified as LDL was triacylglycerols contribute to a lesser extent. Such dif- also reported (Dwivedy and Bridges, 1973). LDL also ferences in lipid composition confer particular charac- appears during the flight of migratory insects when teristic to each lipoprotein and the same could be ex- diacylglicerol uptake by HDL lipophorin converts it to pected concerning the protein composition. The LDL lipophorin (Van der Horst et al.,
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