Thyroid hormone deposition in avian eggs and effects on embryonic development

Thyroid Hormone Deposition in Avian Eggs and Effects on Embryonic Development1

F M. ANNE MCNABB2 AND C. MORGAN WILSON3

SYNOPSIS. Studies to date indicate that thyroid hormones are present in the eggs of chickens and quail and that those hormones are primarily in the yolk. Quail hens deposit thyroid hormones into eggs in proportion to their own thyroid status, but appear to show some regulation of this process. Indirect studies suggest that thyroid hormones are transferred into oocytes bound to lipoproteins and transthyretin, both of which are taken up by receptor-mediated processes. Thyroid hormones bound to yolk lipoproteins may enter embryos with yolk that is taken up by non-specific endocytosis or they may be transported into the embryo by specific carriers. To date most of these ideas about thyroid hormone transport into egg yolk and from egg yolk into embryos have not been investigated directly. In quail, very high T^sup 4^ content of eggs is associated with accelerated differentiation and growth of embryonic pelvic cartilage, a thyroid hormone-responsive tissue. We evaluate these effects on embryonic tissues and the changes in yolk hormone content during incubation in relation to the timing of thyroid development and studies of the capability for tissue responses to thyroid hormones during early embryonic life.

INTRODUCTION

Thyroid hormones are known to play important roles in the differentiation and maturation of specific tissues throughout the vertebrate classes. However, until recently most studies of the developmental effects of thyroid hormones in birds and mammals focused on the posthatching/postnatal effects of hormones produced by the thyroid gland of the developing young. Consequently, relatively little is known about maternal hormone effects during early embryonic development in higher vertebrates. In mammals, early work indicated that thyroid hormones did not cross the placenta readily and that the developing embryo/fetus was thus isolated from the potential effects of maternal thyroid hormones (reviews, Fisher et al., 1977; Roti et al., 1983). However, in the late 1980s a number of studies appeared that began to change this picture. These studies found that small amounts of thyroid hormones do cross the placenta in rats and that some aspects of early development in this altricial species are dependent on maternal hormones for the development of critical tissues like the central nervous system (Morreale de Escobar et al., 1985, 1988, 1989).

Concurrent with the studies cited above, evidence of hormone deposition in eggs of a number of species began to change the picture of maternal contributions of oviparous vertebrates to development of their young while in ovo. The range of maternal regulatory factors deposited in eggs may include mRNAs which result in translation of specific proteins critical to the developing embryo, a variety of specific growth-promoting hormones, growth factors and other regulatory peptides, and lipophilic hormones such as steroids, retinoic acid and thyroid hormones (reviews, Brown and Bern, 1989; de Pablo, 1989; Gilbert,1988). These regulatory factors can play important roles in the differentiation, maturation and growth of embryonic tissues and in the posthatching development of young.

One of the most difficult issues to address in studies of hormones and other regulatory factors in eggs is the relative role(s) of maternal hormones stored in eggs vs. embryonically-produced hormones in regulating embryonic development. In birds, two examples where maternal hormones have been shown to be important in embryonic development are (1) the studies of de Pablo (1989) showing the effects of growth promoting hormones in very early embryos and (2) the work of Schwabl (1993) showing that differences in maternal testosterone stored in eggs affects the degree of aggressiveness of nestling behavior.

THYROID HORMONE CONTENT AND ITS REGULATION IN AVIAN EGGS

Thyroid hormone content of eggs

Thyroid hormones of maternal origin have been measured in eggs of two galliform species, chickens (Hilfer and Searls, 1980; Sechman and Bobeck, 1988; Prati et al., 1992) and Japanese quail (Wilson and McNabb, 1997). The yolk thyroid hormone concentrations measured by the last three of these studies are in agreement (concentrations of about 4-6 ng T^sub 4^/g and 1.5-2.5 ng T^sub 3^/g of yolk). These studies extracted/separated thyroid hormones and measured them by radioimmunoassay (RIA). In contrast, Hilfer and Searls, who attempted to measure hormones in unextracted yolk directly by radioimmunoassay, reported hormone concentrations 2-4 fold higher than the other studies. It seems likely that their values were inflated due to lipid interference with antibody binding in the RIAs, and it should be noted that no information about validation of their assays was provided.

Most of the thyroid hormone content of avian eggs is in the yolk; 95.0% of T^sub 4^ and 99.8% of T^sub 3^ in chickens (Prati et al., 1992); 78.6-95.6% of T^sub 4^ and 75.7-84.1% of T3 in quail (Wilson and McNabb, 1997). In quail eggs, the albumen contains low concentrations of T^sub 4^ (~1 ng/g) and T^sub 3^ (