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The modes of action of juvenile hormones: some questions we

ought to ask

K.G. Davey

*

Department of Biology, York University, Toronto, Ontario, Canada M3J 1P3

Received 31 October 1999; received in revised form 31 December 1999; accepted 25 January 2000

Abstract

This paper argues that the current dogma that juvenile hormones are structurally unique and constitute a family of derivatives of farnesoic acid which are produced by the corpus allatum (CA), secreted into the hemolymph, frequently transported by binding proteins, enter cells by diffusion across the cell membrane and there the products of the CA interact in some way with the genome, probably via nuclear receptors of the steroid superfamily, may not be tenable. It does so by examining the following questions. How many JHs are there? Are there other sources of JH in insects? Are there non-farnesoids with JH activity in insects? How does JH get into cells? Is the product of the CA the effective hormone? How many modes of action are there? How many receptors are there? 2000 Elsevier Science Ltd. All rights reserved.

Keywords:Juvenile hormone; Thyroid hormones; Receptors; Reproduction; Vitellogenesis; Metamorphosis

1. Introduction

Scientists toiling in any discipline are subject to a shared view of that field, which amounts to a commonly held set of assumptions that direct the thinking in that field. We who work in insect endocrinology have inherited a view from the pioneers of our subject about how juvenile hormone might effect its manifold actions. This view has its origins in the notion that “insects pro-vide unrivalled material for physiological study” (Wigglesworth, 1976), and that insects, being simpler organisms, ought to be able to illuminate physiology in general. We have perhaps translated that into a convic-tion that the endocrinology of insects is simpler, but we are beginning to glimpse a complexity of action which rivals that of mammalian endocrine action. Moreover, we are convinced, I suspect, that insects really are likely to be models for more complex organisms, and that the wealth of information accumulated about the action of hormones in more complex organisms will be broadly applicable to the JH field. It is not my objective to

chal-* Tel.:+1-416-736-2100 (ext. 3304); fax:+1-416-736-5698. E-mail address:davey@yorku.ca (K.G. Davey).

0965-1748/00/$ - see front matter2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 5 - 1 7 4 8 ( 0 0 ) 0 0 0 3 7 - 0

lenge this specific assumption, for that has already been done to a degree (Jones, 1995).

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2. The questions

2.1. How many JHs are there?

In some sense, the answer to this question depends on how JH is defined. If we are restrictive and define JH as a farnesoid secreted by the CA, then the list is man-ageable but growing. We are all familiar with the series from JH 0 to JH III with the addition of JHB3 and methyl farnesoate (see Riddiford, 1994 for details). To this list must be added two new products of the CA, both hydroxy derivatives of JH III (Darrouzet et al., 1997). At least one of these hydroxy derivatives has biological activity in theTenebriowax test. More extensive assay-ing of the activity of such compounds needs to be done. JH acid now appears to have some endocrine functions. In isolated prepupal abdomens of Manduca sexta, vitel-logenin transcripts are absent. Once the abdomens have been switched to pupal commitment by injection of 20-hydroxyecdysone, they require a further injection of JH II acid in order to become competent to produce vitellog-enin transcripts in response to a further injection of methoprene. JH III acid, or other precursors of JH, will not substitute for JH II acid (Ismail et al., 1998). Ver-son’s gland in M. sexta becomes committed to secrete pupal proteins early in the last larval instar before the first small commitment peak of ecdysteroid. In a recent paper, Ismail et al. (2000) show that commitment in Ver-son’s gland depends both on a very low titre of ecdys-teroid and on JH II acid.

Waiting in the wings for elucidation is the juvenile hormone of Hemiptera. This has been known for a very long time to be different from the JH of other orders, but the structure has been a matter of controversy. It is not worth reviewing the very long history of attempts to identify the hormone, but there is recent evidence that may be useful. The membranes of follicle cells of Rhod-nius prolixusbind JH I, but not JH II or JH III (Ilenchuk and Davey, 1987), suggesting that the hormone might be a form of JH I. Indeed, JH I has been identified from the hemolymph of the bean bug, Riptortus claveatus

(Numata et al., 1992), although Kotaki (1993) was unable to detect JH I as being released from the CA of this species in vitro. Kotaki (1996) has examined the JH-active compounds secreted in vitro by the CA of a stink bug; the most active has a mobility in thin layer chroma-tography different from any known JH. Given the econ-omic importance of this order, we ought to know more about its JH.

A glimpse of the complexity which may be emerging is provided by studies on the control of vitellogenesis in the blowfly Phormia regina. In this insect, the CA secretes JHB3, JH III and methyl farnesoate in a parti-cular ratio. While each of the hormones can support vit-ellogenesis on its own, the administration of the natural cocktail is better than any of the compounds alone or in

some other ratio (Yin et al., 1995). These observations raise a number of interesting questions, but they make it clear that it may not always be helpful to think ofthe

juvenile hormone of a particular species when a number of related compounds may be acting in concert to govern a particular function. Of course, it is never clear when applying compounds to intact insects whether these com-pounds are altered in some way before reaching their target receptors (see below).

2.2. Are there other sources of JH in insects?

Once more this depends on the definition of JH. If JH is defined as a farnesoid secreted by the CA, then the answer is no. But there are clearly other sources of active farnesoids in some insects. JH I was originally isolated from the abdomens of male pupae ofHyalophora cecro-pia (Williams, 1956). The JH is synthesised by male accessory glands from JH acid secreted by the CA (Peter et al., 1981). The amounts synthesised and stored are substantial, and are transferred to the female (Shirk et al., 1980). The synthesis of JH by accessory glands is not confined to Lepidoptera. The male accessory glands of mosquitoes synthesise JH I and III as well as JHB3 and methyl farnesoate, but not from JH acid. The syn-thesis in this case is from acetate (Borovsky et al., 1994a), raising the question of whether other tissues might also constitute a source of the hormone. InAedes, the ovary synthesises JH III from farnesoic acid (Borovsky et al., 1994b). If physiologically active farne-soids are secreted by tissues other than the CA, then questions need to be raised about the interpretation of results based primarily on allatectomy. If a function dis-appears upon allatectomy, it is probably safe to conclude that it is JH-dependent. But if a function persists, it may not be safe to conclude that it is JH-independent. Do our assumptions about when JH is required for egg pro-duction in mosquitoes need some further consideration?

2.3. Are there non-farnesoids with JH activity in insects?

It has been known for many years that ecdysteroids from the ovary fulfil many of the functions of JH in adult females. While JH is known to stimulate the synthesis of vitellogenin in many insects (Wyatt and Davey, 1996), ovarian ecdysteroids have this function in mosquitoes and some other Diptera (Hagedorn, 1983). While we may have originally viewed such an arrangement as spe-cific to Diptera, that view is no longer tenable, for Girar-die and GirarGirar-die (1996) have shown quite clearly that ovarian ecdysteroid functions as a gonadotropin, inducing vitellogenin synthesis in the fat body of

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it not possible that JH and ecdysone might be operating at the same site and in the same way to induce vitellog-enesis? Do these observations have anything to tell us about receptors for JH? There are some species for which it is known that ecdysone is without any influence on vitellogenin synthesis. Thus in Rhodnius females, which contain ecdysteroids from the ovary only after the peak of vitellogenesis is achieved, early treatment with doses of ecdysone large enough to induce cuticle depo-sition has no effect on vitellogenin synthesis (Wang, 1991).

There have also been persistent reports of peptides mimicking JH. The mechanism of at least one of these is indirect, acting to limit the synthesis of JH esterase (Hayakawa, 1992), a process which is known to be directly stimulated by JH (Venkataraman et al., 1994; Feng et al., 1999). The action of some of the other pep-tide mimics seems less certain. In Rhodnius, for example, an uncharacterised neuropeptide from the brain (Barker and Davey, 1983) and JH I (Gold and Davey, 1989) both have the capacity to stimulate protein syn-thesis in the male accessory gland in vitro. There are also several reports of peptides stimulating the synthesis of vitellogenin. The most recent involvesLocustaovary maturating parsin, which, in addition to its action on vit-ellogenin synthesis via an ecdysiotropic action on the ovary (Girardie and Girardie, 1996), may also act directly on the fat body (Girardie et al., 1998). In the case of the direct action on the fat body it is probably the C terminal end of the peptide which is active, the N-terminal portion being the ecdysiotropin. In this case, the peptide did not directly stimulate vitellogenin syn-thesis, but sustained it, either by reducing turnover or enhancing the translation of mRNA. Several peptides have either stimulatory or inhibitory effects on vitellog-enin synthesis, but where the action of these peptides has been characterised, it is evident that they act at the level of translation, whereas JH acts on transcription (see Wyatt and Davey, 1996 for a fuller discussion). Never-theless, some closer examination of these actions might be illuminating in terms of the precise mode of action of JH, and a knowledge of their effects serves to empha-sise the complexity of the events in which JH is interven-ing.

The thyroid hormones, long known to influence vari-ous processes in insects, have recently been shown to be rather precise mimics of the action of JH on follicle cells of the insect ovary. Thus, they stimulate cell shrinkage and patency, T3 (39,3,5-triiodo thyronine) binds to the same receptor on locust follicle cells as JH III (Davey and Gordon, 1996; Kim et al., 1999), and T3 is taken up by follicle cells by receptor mediated endocytosis, apparently via the JH receptor (Davey, 2000). These observations raise a number of interesting possibilities, not the least of which is the functional significance of thyroid hormones in insects (Davey, 2000). At least as

interesting are the clues that it might present to us in terms of our search for JH receptors. While the nuclear receptor mechanisms for thyroid hormones are well known, the membrane receptors are not at all well characterised (McNabb, 1992). The origin of the thyroid hormones in locusts appears to be the food (Davey, 2000), and this raises an obvious question about sup-plementary sources of JH in other insects.

2.4. Is the product of the CA the effective hormone?

It has been an implicit assumption underlying most of our work that the product of the CA intervenes in development and physiology unchanged, and that any metabolites are less active breakdown products. A little reflection, however, will reveal that this is unlikely on a priori grounds. Thus, ecdysone is well known to be processed into the more active 20-hydroxy-ecdysone, and thyroxine, the principal product of the thyroid gland, is deiodinated in the liver and other tissues to yield the much more active T3.

Processing of an inactive product of the CA, JH acid, to a more active form, JH I, by male accessory glands, is, as made clear above, already established. In addition, perhaps the most provocative paper presented at JH VI revealed that fat body and ovary, but not other tissues of locusts, processed injected labelled JH into unknown compounds (Couillaud et al., 1996). The fact that there are tissue specific metabolites raises questions about the function of such metabolites. They may simply be degra-dation products, but equally, as is well known in ver-tebrates, such products may contribute additional and significant biological activity (Robel and Baulieu, 1994). We would be wise to be alert to the possibility of such processing.

2.5. How does JH get into cells?

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by receptor-mediated endocytosis has been lurking in the background for many years (Szego, 1984).

In vertebrates, the thyroid hormones are taken up by receptor-mediated endocytosis (Di Liegro et al., 1987). I have recently shown that rhodamine conjugated T3 enters the follicle cells of locusts by receptor-mediated endocytosis, via a receptor which appears to be the mem-brane receptor for JH (Davey, 2000). These observations may or may not indicate that JH is also taken up by endocytosis. The functional significance of such a mech-anism remains obscure. For T3, it is clear that the uptake results in the conversion of T3 to a much more active molecule, but whether this is a functionally important phenomenon remains to be explored. The entire process may be artifactual, induced by an attempt on the part of the cell to eliminate the T3 rather than capitalise on its presence. Or, it may be simply a matter of the normal turnover of the receptor.

Nevertheless, there is at least the possibility that JH may be selectively accumulated by the cell. If this should prove to be the case, there are several potential conse-quences. Perhaps the most intriguing is the possibility that the concentration of hormone inside selected target cells may be considerably higher than the concentration in the hemolymph. This might expand the range of potential receptors to proteins with a somewhat lower affinity for the hormone than is customarily thought to be required.

At least one study has been conducted on JH uptake into cells. Mitsui et al. (1979) placed pieces of epidermis fromM. sextain medium containing [3H]JH I and

meas-ured the time course of uptake into epidermis. From the data in the paper it is possible to calculate the concen-tration inside the cell at equilibrium, and it appears that the cells accumulate JH to a level 10 times that in the medium.

2.6. How many modes of action are there?

This is obviously a complex question, for JH is among the most pleiotropic of hormones. The notion of an acti-vation or priming action, by which a target cell is pre-pared to respond to a later regulative action of the hor-mone was first hinted at more than 25 years ago (Pratt and Davey, 1972), and the first experimental evidence for the phenomenon was provided for the patency response of the follicle cells by Abu-Hakima and Davey (1975), who showed that follicles ofRhodniuswhich had developed in the absence of JH were not able to respond to JH by becoming patent. This was later shown to be the result of a failure to develop the JH membrane recep-tor and possibly the special JH-responsive isoform of Na+/K+ ATPase (Ilenchuk and Davey, 1987). The con-cept was later expanded to include the notion that the activation might be independent of the regulative func-tion, as in the case of the stimulation of vitellogenin

syn-thesis by ecdysone in flies, which requires a prior exposure of fat body to JH (Davey, 1994). The concept has been developed to include a wide variety of effects (Wyatt and Davey, 1996). Is priming really a distinct mode of action from regulation? The fact that priming by JH is sometimes followed by regulation by a different hormone supports this notion, although we have no clear idea about the mechanism. Perhaps the synthesis of receptors is involved. While there is no doubt that the distinction between priming and regulation is useful in conceptual terms, there is perhaps less certainty about its utility in thinking about receptors (see below).

Another dichotomy has arisen between membrane effects and nuclear effects. There is no doubt that there are effects of JH which are mediated by or even occur entirely within the cell membrane. We are moving towards a more complete description of the events in the membrane of follicle cells. We had earlier shown that JH binds to a membrane protein and by a cascade involv-ing the activation of protein kinase C, a 100 kDa protein is phosphorylated (see Wyatt and Davey, 1996 or Davey, 1996 for detailed references). It is now clear that the 100 kDa peptide is theα-subunit of the Na+/K+ATPase, and, moreover, high resolution gels reveal that there are two isoforms of theα-subunit, one of which is preferentially phosphorylated in the presence of JH (Davari, 1999). The involvement of other signalling elements such as a G protein, phospholipase C and diacylglycerol between the receptor and protein kinase C remains hypothetical. This is not a complete description of the events mediated by the membrane receptor, for the development of pat-ency involves a good deal more than the shrinkage of the cell: there are changes in the cytoskeleton and rearrangements of cell junctions (Davey, 1996).

There have been suggestions of other membrane receptors governing the synthesis of proteins in male accessory glands. Yamomoto et al. (1988) produced evi-dence suggesting that the in vitro stimulation of protein synthesis by JH in male accessory glands ofDrosophila

required both Ca++and protein kinase C. There has been some preliminary evidence of binding of a photoaffinity analogue of JH III to membranes of fat body and brain of Locusta(Sevala et al., 1995).

There may be other modes of action in addition to those at the membrane and in the nucleus. There are several reports of cytosolic binding proteins (see Wyatt and Davey, 1996 for detailed references), but there has been no function attached to the binding. Whether these represent functional receptors remains to be seen. Most current models of JH action assume the existence of a cytosolic binding protein in order to transport the JH to the nucleus.

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acti-vation of protein kinase C (Bigger and Laufer, 1999), but the initial action is apparently cytosolic, since the juvenoids were capable of directly activating purified cytosolic kinase C rather than acting to stimulate mem-brane bound kinase C. The concentrations necessary to achieve these results were an order of magnitude larger than what is normally regarded as physiological, but once the possibility of accumulation of JH by target cells has been raised, these concerns may not be so great.

There is also the possibility that JH might affect mito-chondria directly. The various attempts to demonstrate a direct effect have been reviewed, and we concluded that the definitive experiments necessary to examine the question have yet to be done (Wyatt and Davey, 1996). Given the parallels between JH and the thyroid hor-mones, it would be useful to do such experiments. Thy-roid hormones have been known for some time to stimu-late mitochondrial respiration, but that has always been assumed to be an indirect effect. Recently, however, there have been clear reports that 3,5-diiodothyronine can increase the metabolism of isolated mitochondria at doses in the low nanomolar range (Leary et al., 1996).

However, it is that group of effects which involve some interaction with the genome which are central to the action of JH. It is clear that the priming or activating actions are likely to be of this type, and they can only complicate the design and interpretation of experiments. The regulatory actions of JH that proceed via the nucleus are of two broad types. There are those that require an interaction with ecdysone, and those that are the result of independent action.

The requirement for ecdysone is clearest and most complete in the metamorphic actions of JH, for JH actions can only be expressed in the context of moulting controlled by ecdysone. This is a system of growing complexity. There is no doubt that one of the functions of JH in metamorphosis involves preventing the ecdy-sone-controlled switch in developmental pathway from larval to adult as made clear by Riddiford (1996). This will involve some interaction between ecdysone and JH, and given the timing of the switch, the strategy of docu-menting the effects of JH on the earliest ecdysone-con-trolled events (e.g. Hiruma et al., 1999; Zhou et al., 1998) is likely to be productive. It is, however, likely that there will also be connections between the actions of JH and ecdysone not only in terms of its action on metamorphosis, but also in its action on vitellogenin syn-thesis. The involvement of both JH and ecdysone in the control of vitellogenin synthesis is now clear in a number of species (see above).

Given the requirement for ecdysone, the discovery that JH binds to USP (Jones and Sharp, 1997) is pro-vocative. There are several unusual aspects to this bind-ing. First the affinity of USP for JH is in the high micromolar range. While this is unusual, until it is clear what the intracellular concentrations of JH might be, we

ought not to eliminate the possibility on these grounds alone. The finding by Hiruma et al. (1999) that JH down regulates at least one form of USP casts some doubt on the significance of the binding, since ligands normally increase the expression of their receptors. The facts that some farnesoids bind to FXR, an orphan receptor of ver-tebrates and that FXR has a high degree of homology to EcR is also intriguing, although JH III and methop-rene failed to activate FXR (Forman et al., 1995). Simi-larly, methoprene acid has been shown to bind to RXR, which is the homologue of USP, although once more JH II and other JH active compounds did not (Harmon et al., 1995).

There is thus a good deal of evidence to suggest that one of the nuclear actions of JH is closely associated with the way in which ecdysone exerts its effects, and may interact in some way with the ecdysone receptor complex. But what of the other nuclear actions which do not involve ecdysone? A conceptual model for the way in which JH might induce the synthesis of a parti-cular protein (in this case vitellogenin) has been presented by Wyatt and Davey (1996), who emphasise that the model is speculative and highly simplified. Per-haps the most useful system for studying the action of JH, leading perhaps to the identification of some of the molecular events within the nucleus, is the stimulation of JH esterase synthesis. This is under study in at least two laboratories (Venkataraman et al., 1994; Feng et al., 1999). One system involves a cell line, and thus the tim-ing of events can be precisely measured. The JH esterase begins to appear within about 30 min of the adminis-tration of JH: there is no sign of a lag or priming phase. In addition, no other hormones are needed (Feng et al., 1999). Does this represent a mode of action which is distinct from that which requires the joint action of ecdy-sone? That question remains open. In addition, our pre-occupation with the status quo actions of JH during development ought not to blind us to the large body of evidence, based on simple and clear experiments, that JH may also encourage the appearance of larval charac-ters rather than simply suppress the appearance of adult characters (Wigglesworth, 1970). As is made clear by Jones (1995), there are some larval developmental events which JH appears to stimulate.

Once the presumed nuclear receptor(s) have been acti-vated, there is a myriad of downstream events which can come into play ranging from the production of an exportable protein to the proliferation of neuroblasts, for which polyamine synthesis appears to be an essential step in the transduction pathway (Cayre et al., 1997).

2.7. How many receptors are there?

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range of receptors. However, it is worth remembering that many steroids are equally pleiotropic, and that a var-iety of events are affected as the result of interaction with a single receptor type. We have generally assumed that membrane receptors for JH are likely to be entirely different molecules from nuclear receptors, and even cytosolic receptors must surely argue for more than one type of receptor. Nuclear receptors with their DNA bind-ing domains and zinc fbind-ingers are unlikely to be compat-ible with membrane receptors with their transmembrane domains. In addition observations such as those outlined above concerning the requirement for JH B3, JH III and methyl farnesoate in specific proportions for normal vit-ellogenin synthesis in blowflies (Yin et al., 1995) might be regarded as a powerful argument for a galaxy of receptors.

However, vertebrate steroids also have membrane effects (Wehling, 1997). While rather few of the mem-brane receptors have been characterised, a recent study shows that transfecting cDNA for nuclear estrogen receptors into hamster ovary cells results in a single tran-script and expression of the receptor in both membrane and nuclear fractions of the cell. The membrane-bound receptors were functional as determined by their ability to stimulate adenyl cyclase and inositol phosphate pro-duction via associated G proteins (Razandi et al., 1999). The nuclear receptors do not possess transmembrane domains. This is not definitive evidence, but it is an encouraging sign.

3. Conclusion

What can be drawn from this highly idiosyncratic tour of the landscape? I hope that it is clear that the dogma with which I began the tour is not so tenable as we may have thought: we ought to be more alert to alternative views. The view that insects, given their simplicity, are likely to illuminate the physiology and development of higher taxa also seems less viable in this specific field. If anything, it is vertebrate endocrinology which is illuminating insect endocrinology. The essential task remains the identification of one or more receptor mol-ecules for JH, a difficult and frustrating one because of the very high non-specific binding involved. While we ought not to be guided too heavily by the rapid pace of events in vertebrate endocrinology, there are some close parallels, particularly with the thyroid hormones.

Acknowledgements

I am grateful to the Karlson Foundation, who sup-ported the preparation of this paper and enabled my attendance at JH VII. Research in my laboratory is

sup-ported by the Natural Sciences and Engineering Research Council of Canada.

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