Evolution of marsupial and other vertebrate thyroxine-binding plasma proteins

Abstract

Binding of radioactive thyroxine to proteins in the plasma of vertebrates was studied by electrophoresis followed by autoradiography. Albumin was found to be a thyroxine carrier in the blood of all studied fish, amphibians, reptiles, monotremes, marsupials, eutherians (placental mammals), and birds. Thyroxine binding to transthyretin was detected in the blood of eutherians, diprotodont marsupials, and birds, but not in blood from fish, toads, reptiles, monotremes, and Australian polyprotodont marsupials. Globulins binding thyroxine were only observed in the plasma of some mammals. Apparently, albumin is the phylogenetically oldest thyroxine carrier in vertebrate blood. Transthyretin gene expression in the liver developed in parallel, and independently, in the evolutionary lineages leading to eutherians, to diprotodont marsupials, and to birds. In contrast, high transthyretin mRNA levels, strong synthesis, and secretion of transthyretin in choroid plexus from reptiles and birds indicate that transthyretin gene expression in the choroid plexus evolved much earlier than in the liver, probably at the stage of the stem reptiles. NH2-terminal sequence analysis suggests a change of transthyretin pre-mRNA splicing during evolution.

Evolution of the Thyroid Hormone-Binding Protein, Transthyretin

“…There are relatively few studies of thyroid hormone-binding proteins in lower vertebrates. Moreover the results from such studies appear contradictory (Larsson et al, 1985;Richardson et al, 1994;Tanabe et al, 1969). In one study radiolabelled T 4 was incubated with plasma from adult reptiles, amphibia, and fish and the resulting products were subsequently fractionated by SDS-PAGE followed by autoradiography.…”

“…In one study radiolabelled T 4 was incubated with plasma from adult reptiles, amphibia, and fish and the resulting products were subsequently fractionated by SDS-PAGE followed by autoradiography. Only one protein, ALB, bound the radiolabeled T 4 (Richardson et al, 1994) and it has been proposed that this protein is the principal thyroid hormone-binding protein in the blood of such organisms. The identification in salmon of thyroid hormone-binding proteins with characteristics similar to transthyretin (Larsson et al, 1985) and the recent isolation of TTR and its cDNA from amphibian tadpoles before the metamorphic climax (Rana catesbeiana, Yamauchi et al, 1993Yamauchi et al, , 1998 and from the teleost fishes sea bream Power, 1996, 1999) and masu salmon (Oncorhychus masu) prior to smoltification (Yamauchi et al, 1999) suggest that it may also have a role in transporting TH in these species.…”

“…Since in teleost fish and amphibia, TTR appears to have a higher affinity for T 3 than for T 4 (Yamauchi et al, 1993(Yamauchi et al, , 1999, the contradictory observations mentioned earlier may be explained by suggesting that albumin may be the principal T 4 -binding protein and TTR the principal T 3 -binding protein. The relative importance of these two thyroid hormone-binding proteins at different stages of the life cycle of different organisms remains to be determined, particularly as earlier studies were carried out with plasma samples from adult teleost fish (Richardson et al, 1994) while more recent studies have been carried out with samples from juvenile teleost fish Power, 1996, 1999;Yamauchi et al, 1993Yamauchi et al, , 1998Yamauchi et al, , 1999. The identification of TTR in fish other than teleosts and the characterisation of its function will be important in defining its role in TH transport in fish.…”

“…TTR has a fairly restricted gene expression, being demonstrated principally in the liver and choroid plexus of rat Fung et al, 1988;Schreiber et al, 1990), human (Dickson and Schreiber, 1986), sheep (Schreiber et al, 1990), pig , and chicken (Southwell et al, 1991) and in the liver of marsupials (Richardson et al, 1994). In two reptiles, the turtle (Trachemys scripta) and lizard (Tiliqua rugosa), TTR is present in the brain but little or no expression has been detected in the liver (Achen et al, 1993;Richardson et al, 1997).…”

“…Existing models of TTR evolution are largely based on results of binding studies of radiolabelled T 4 with blood plasma from adult representatives of most vertebrate groups, of SDS-PAGE of the secretory products from the choroid plexus, or of Northern blotting of various tissues (Harms et al, 1991;Richardson et al, 1994;Schreiber et al, 1993). Such studies demonstrated T 4 binding to TTR in the plasma of all birds, eutherian mammals, and adult diprotodont marsupials (which includes kangeroos and opossums) and the absence of such binding in monotremes, polyprotodont marsupials, reptiles, amphibians, and fish (Chang et al, 1999;Richardson et al, 1994Richardson et al, , 1997Schreiber and Richardson, 1997).…”