Insect Biochemistry and Molecular Biology 30 2000 877–884 www.elsevier.comlocateibmb
Do thyroid hormones function in insects?
K.G. Davey
Department of Biology, York University, Toronto, Ont. M3J 1P3, Canada Received 31 October 1999; received in revised form 31 December 1999; accepted 23 January 2000
Abstract
Earlier work demonstrated that phenoxy–phenyl compounds such as fenoxycarb and thyroxine mimicked the effects of JH III in causing a reduction in volume of the follicle cells of Locusta migratoria. While these compounds were only moderately effective,
a derivative of thyroxine, 3,3 9,5-triiodothyronine T3 was as effective as JH III, and T3 has been shown to bind to the same
membrane receptor and activate the same pathway as JH III. The current paper shows that other thyroxine derivatives vary in activity. 3,3
9,59-Triiodothyronine reverse T3 is inactive. 3,5-Diiodothyronine T2 is more active than JH III, while its relatives iodines at 3
9,59 or at 3,39 are inactive. When follicles are exposed in vitro to rhodamine conjugated T3, the fluorescent compound can be seen to enter the cells and accumulate there: this process is inhibited by cycloheximide or by a temperature of 0
° C. The
accumulation is antagonised by JH III but not JH I which does not bind to the JH III membrane receptor and by an antiserum raised against the putative membrane receptor protein. The action of T3, but not T2, is inhibited by 6-n-propyl-2-thiouracil or by
aurothioglucose, both known to inhibit deiodinases. The activity of T3, but not of T2, increases with time of exposure to the follicle cells. These facts suggest that T3 enters the cells by receptor mediated endocytosis and is converted to a more active compound.
Immunoreactivity to T3, but not thyroxine, can be detected in the haemolymph of locusts, and the titre varies slightly with the gonotrophic cycle. The food shows immunoreactivity for both thyroxine and T3. These findings suggest that thyroid hormones are
ingested by locusts and have the potential to be used as hormonal signals in the control of egg production.
2000 Elsevier Science
Ltd. All rights reserved.
Keywords: Juvenile hormone; Receptors; Thyroid hormones; Endocytosis; Deiodinase
1. Introduction
While the thyroid hormones are customarily regarded as vertebrate hormones, evidence is accumulating that
derivatives of thyroxine may have a role to play in the development of a variety of invertebrates. Eales 1997,
in a provocative review, has argued that derivatives of thyroxine, originating in the food of many invertebrates,
may function in the control of development as vitamins. In insects, feeding 3,5,3
9,59-tetraiodothyronine T4 to silkworms, has a number of effects on silk production
and reproductive function, which were interpreted as indirect, acting perhaps via ecdysone Thagaraja et al.
1991, 1993. Others have documented a variety of long lasting effects of a single injection of T4 into larvae of
Bombyx mori or Antherea mylitta, including protein and
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2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 5 - 1 7 4 8 0 0 0 0 0 6 1 - 8
nucleic acid
and glycogen
content of
fat body
Chaudhuri et al. 1986, 1992; Chaudhuri et al., 1987a,b, protein and nucleic acid turnover Reddy et al., 1994a,b,
haemolymph amino acid content Reddy et al., 1994c and ion-specific ATPases Reddy et al. 1994d, 1996. T4
also stimulates the release of triglycerides and fatty acids from the fat body of Hyalophora cecropia in vitro
Bhakthan and Gilbert, 1968.
In most insects, the vitellogenin gains access to the oocyte surface via spaces between the cells of the fol-
licular epithelium, and in many species, the appearance of these open spaces is governed by JH. The follicle cells
respond to JH by shrinking and by altering the cytoskele- ton and the distribution of septate junctions, resulting in
the appearance of large lateral spaces between the cells Davey, 1996. These effects are mediated by a mem-
brane receptor Sevala et al., 1995. The effect of JH on cell volume involves the activation of Na
+
K
+
ATPase Davey, 1996.
The thyroid hormones and other phenoxyphenyl com-
878 K.G. Davey Insect Biochemistry and Molecular Biology 30 2000 877–884
pounds such as fenoxycarb mimic these effects. We have shown that both T4 and particularly 3
9,3,5-triiodothyron- ine T3, when applied to follicle cells of locusts in vitro,
induce the same rapid reduction in cell volume as JH III, and this effect is inhibited by ouabain, implicating
Na
+
K
+
ATPase Davey and Gordon, 1996. More recently, we have shown that T3 also mimics the action
of JH I in causing both a reduction in volume and an increase in patency in the follicle cells of Rhodnius pro-
lixus. Moreover, the effects of T3 on the follicle cells of L. migratoria appear to be mediated by the same recep-
tor as JH III. The effect on follicle cell volume is blocked by incubation in an antibody raised against the 35 kDa
binding protein for JH III, T3 shows specific and satu- rable binding to membrane preparations of follicle cells,
and JH III will compete for these binding sites Kim et al., 1999.
In this paper, I further explore the effects of deriva- tives of thyroxine on follicle cells, and examine the
occurrence and probable origin in locusts of immunore- active thyroxine derivatives.
2. Materials and methods
