668 K.G. Davey Insect Biochemistry and Molecular Biology 30 2000 663–669
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 fingers 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.
References
Abu-Hakima, R., Davey, K.G., 1975. Two actions of juvenile hormone on the follicle cells of Rhodnius prolixus. Can. J. Zool. 53,
1187–1188. Barker, J.F., Davey, K.G., 1983. A polypeptide from the brain and
corpus cardiacum of male Rhodnius prolixus which stimulates in vitro protein synthesis in the transparent accessory reproductive
gland. Insect Biochem. 13, 7–10. Bigger, W.J., Laufer, H., 1999. Settlement and metamorphosis of Capi-
tella larvae induced by juvenile hormone-active compounds is
mediated by protein kinase C and ion channels. Biol. Bull. 196, 187–198.
Borovsky, D., Carlson, D.A., Hancock, R.G., Rembold, H., Van Han- del, E., 1994a. De novo biosynthesis of juvenile hormone III and
I by the accessory glands of the male mosquito. Insect Biochem. Molec. Biol. 24, 437–444.
Borovsky, D., Carlson, D.A., Ujvary, I., Prestwich, G.D., 1994b. Biosynthesis of 10R-juvenile hormone III from farnesoic acid by
Aedes aegypti ovary. Arch. Insect Biochem. Physiol. 2, 75–90.
Cayre, M., Strambi, C., Charpin, P., Augier, R., Strambi, A., 1997. Specific requirement of putrescine for the mitogenic action of juv-
enile hormone on adult insect neuroblasts. Proc. Natl. Acad. Sci. USA 94, 8238–8242.
Couillaud, F., Debernard, S., Darrouzet, E., Rossignol, F., 1996. The hidden face of juvenile hormone metabolism in the African locust.
Arch. Insect Biochem. Physiol. 32, 387–397. Darrouzet, E., Mauchamp, B., Prestwich, G.D., Kerhoas, L., Ujvary,
I., Couillaud, F., 1997. Hydroxy juvenile hormones biosynthesized by locust corpora allata in vitro. Biochem. Biophys. Res. Comm.
240, 752–758. Davari, E.D., 1999. The effect of JH on isozymes of Na
+
K
+
-ATPase in ovarian follicles of Locusta migratoria. M.Sc. Thesis, York Uni-
versity, Toronto. Davey, K.G., 1994. Vitellogenesis in insects: putting the Diptera in
context. In: Davey, K.G., Peter, R.E., Tobe, S.S. Eds., Perpectives in Comparative Endocrinology. NRC Research Journals, Ottawa,
pp. 299–303. Davey, K.G., 1996. Hormonal control of the follicular epithelium dur-
ing vitellogenin uptake. Invert. Reprod. Dev. 30, 249–254. Davey, K.G., 2000. Do thyroid hormones function in insects? Insect
Biochem. Molec. Biol. in press. Davey, K.G., Gordon, D.R.B., 1996. Fenoxycarb and thyroid hormones
have JH-like effects on the follicle cells of Locusta migratoria in vitro. Arch. Insect Biochem. Physiol. 32, 613–622.
Di Liegro, I., Savettieri, G., Cestelli, A., 1987. Cellular mechanism of thyroid hormones. Differentiation 35, 165–175.
Feng, Q.L., Davey, K.G., Pang, A.S.D., Primavera, M., Ladd, T.R., Zheng, S.C., Sohi, S., Retnakaran, A., Palli, S.R., 1999. Spruce
budworm Choristoneura fumiferana juvenile hormone esterase: hormonal regulation, developmental expression and cDNA cloning.
Molec. Cell. Endocrinol. 148, 95–108. Forman, B.M., Goode, E., Chen, J., Oro, A.E., Bradley, D.J., Perlmann,
T., Noonan, D.J., Burka, L.T., McMorris, T., Lamph, W.W., Evans, R.M., Weinberger, C., 1995. Identification of a nuclear receptor
that is activated by farnesol metabolites. Cell 81, 687–693. Girardie, J., Girardie, A., 1996. Lom OMP, a putative ecdysiotropic
factor for the ovary in Locusta migratoria. J. Insect Physiol. 42, 215–221.
Girardie, J., Geoffre, S., Delbecqu, J.-P., Girardie, A., 1998. Argu- ments for two distinct gonadotropic activities triggered by different
669 K.G. Davey Insect Biochemistry and Molecular Biology 30 2000 663–669
domains of the ovary maturating parsin of Locust migratoria. J. Insect Physiol. 44, 1063–1072.
Gold, S.M.W., Davey, K.G., 1989. Juvenile hormone and protein syn- thesis in the transparent accessory gland of male Rhodnius prolixus.
Insect Biochem. 19, 139–143. Hagedorn, H.H., 1983. The role of ecdysone in adult insects. In:
Downer, R.G.H., Laufer, H. Eds. Endocrinology of insects. Alan R. Liss, New York, pp. 271–304.
Hayakawa, Y., 1992. A putative new juvenile peptide hormone in lepi- dopteran insects. Biochem. Biophys. Res. Comm. 185, 1141–1147.
Harmon, M.A., Boehm, M.F., Heyman, R.E., Mangelsdorf, D.J., 1995. Activation of mammalian retinoid X receptors by the insect growth
regulator methoprene. Proc. Natl. Acad. Sci. USA 92, 6157–6160. Hiruma, K., Shinoda, T., Malone, F., Riddiford, L.M., 1999. Juvenile
hormone modulates
20-hydroxyecdysone-inducible ecdysone
receptor and ultraspiracle gene expression in the tobacco hornworm, Manduca sexta. Dev. Genes Evol. 209, 18–30.
Ilenchuk, T.T., Davey, K.G., 1987. The development of responsiveness to juvenile hormone in the follicle cells of Rhodnius prolixus. Insect
Biochem. 17, 525–529. Ismail, S.M., Satyanarayama, K., Bradfield, J.Y., Dahm, K.H., Bhaska-
ran, G., 1998. Juvenile hormone acid: evidence for a hormonal function in induction of vitellogenin in larvae of Manduca sexta.
Arch. Insect Biochem. Physiol. 37, 305–314. Ismail, S.M., Goin, C., Muthumani, K., Kim, M., Dahm, K.H., Bhaska-
ran, G., 2000. Juvenile hormone acid and ecdysteroid together induce competence for metamorphosis of the Verson’s gland in
Manduca sexta . J. Insect Physiol. 46, 59–68.
Jones, G., 1995. Molecular mechanisms of action of juvenile hormone. Ann. Rev. Entomol. 40, 147–169.
Jones, G., Sharp, P.A., 1997. Ultraspiracle; an inverebrate nuclear receptor for juvenile hormones. Proc. Natl. Acad. Sci. USA 94,
13499–13503. Kim, Y., Davari, E., Sevala, V., Davey, K.G., 1999. Functional binding
of a vertebrate hormone, L-3,5,39-triodothyronine T
3
to insect fol- licle cell membranes. Insect Biochem. Molec. Biol. 29, 943–950.
Kotaki, T., 1993. Biosynthetic products by heteropteran corpora allata in vitro. Appl. Ent. Zool. 28, 242–245.
Kotaki, T., 1996. Evidence for a new juvenile hormone in a stink bug Plautia stali
. J. Insect Physiol. 42, 279–286. Leary, S.C., Barton, K.N., Ballantyne, J.S., 1996. Direct effects of
3,5,39 triiodothyronine and 3,5 diiodthyronine on mitochondrial metabolism in the goldfish Carassius auratus. Gen. Comp. Endoc-
rinol. 104, 61–66. Lomas, L.O., Gelman, D., Kaufamn, W.R., 1998. Ecdysteroid regu-
lation of salivary gland degeration in the ixodid tick, Amblyomma hebraeum
: a reconciliation of in vivo and in vitro observations. Gen. Comp. Endocrinol. 109, 200–211.
McNabb, F.M.A., 1992. Thyroid Hormones. Prentice-Hall, Englewood Cliffs, NJ.
Mitsui, T., Riddiford, L.M., Bellamy, G., 1979. Metabolism of juvenile hormone by the epidermis of the tobacco hornworm Manduca
sexta . Insect Biochem. 9, 637–643.
Numata, H., Numata, A., Takahashi, C., Nakagawa, Y., Iwatani, K., Takahashi, S., Miura, K., Chinzei, Y., 1992. Juvenile hormone I is
the principal juvenile hormone in a hemipteran insect, Riptortus clavatus
. Experientia 48, 606–610. Peter, M.G., Shirk, P.D., Dahm, K.H., Roller, H., 1981. On the speci-
ficity of juvenile hormone biosynthesis in the male cecropia moth. Z. Naturf. 36C, 579–585.
Pratt, G.E., Davey, K.G., 1972. The corpus allatum and oogenesis in Rhodnius prolixus
. I The effects of allatectomy. J. Exp. Biol. 56, 201–214.
Razandi, M., Pedram, A., Greene, G.L., Levin, E.R., 1999. Cell mem- brane and nuclear estrogen receptors ERs originate from a single
transcript: studies of ER alpha and ER beta expressed in chinese hamster ovary cells. Mol. Endocrinol. 13, 307–319.
Riddiford, L.M., 1994. Cellular and molecular actions of juvenile hor- mone. I. General considerations and premetamorphic actions. Adv.
Insect Physiol. 24, 213–274. Riddiford, L.M., 1996. Juvenile hormone: the status of the “status quo”
action. Arch. Insect Biochem. Physiol. 32, 271–286. Robel, P., Baulieu, E.E., 1994. Neurosteroids: biosynthesis and func-
tion. Trends Endo. Met. 5, 1-8.279–286. Sevala, V.L., Davey, K.G., Prestwich, G.D., 1995. Photoaffinity labe-
ling and characterization of a juvenile hormone binding protein in the membranes of follicle cells of Locusta migratoria. Insect
Biochem. Molec. Biol. 25, 267–273. Shirk, P.D., Bhaskaran, G., Roller, H., 1980. The transfer of juvenile
hormone from male to female during mating in the male Cecropia silkmoth. Experientia 36, 682–683.
Szego, C.M., 1984. Mechanisms of hormone action: parallels in recep- tor-mediated signal propagation for steroid and peptide effectors.
Life Sci. 35, 2383–2396. Venkatamaran, V., O’Mahony, P.J., Manzcak, M., Jones, G., 1994.
Regulation of juvenile hormone esterase gene transcription by juv- enile hormone. Dev. Gen. 15, 391–400.
Wang, Z., 1991. Studies on vitellogenesis of Rhodnius prolixus. Ph.D. Thesis, York University, Toronto.
Wehling, M., 1997. Specific, nongenomic actions of steroid hormones. Ann. Rev. Physiol. 59, 365–387.
Wigglesworth, V.B., 1970. Insect Hormones. Oliver and Boyd, Edin- burgh.
Wigglesworth, V.B., 1976. Insects and the Life of Man. Chapman and Hall, London.
Williams, C.M., 1956. The juvenile hormone of insects. Nature 178, 212–213.
Wyatt, G.R., Davey, K.G., 1996. Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects.
Adv. Insect Physiol. 26, 1–155. Yamomoto, K., Chadarevian, A., Pellegrini, M., 1988. Juvenile hor-
mone action mediated in male accessory glands of Drosophila by calcium and kinase C. Science 239, 916–919.
Yin, C.M., Zou, B.-X., Jiang, M., Li, M.-F., Qin, W., Potter, T.L., Stoffolano, J.G., 1995. Identification of juvenile hormone III bise-
poxide JHB3, juvenile hormone III and methyl farnesoate secreted by the corpus allatum of Phormia regina Meigen in vitro
and function of JHB3, either applied alone or as part of a juvenoid blend. J. Insect Physiol. 40, 283–292.
Zhou, B., Hiruma, K., Shinoda, T., Riddiford, L.M., 1998. Juvenile hormone prevents ecdysteroid-induced expression of broad com-
plex RNAs in the epidermis of the tobacco hornworm, Manduca sexta
. Dev. Biol. 203, 233–244.
