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Relationship Between Morphogenetic Activity and Metabolic Stability of Insect Juvenile Hormone Analogues*

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Relationship Between Morphogenetic Activity and Metabolic Stability of Insect Juvenile Hormone Analogues* 7. Insect Physiol., 1972, Vol. 18, pp. 2019 to 2028. Pergamon Press. Printed in Great Britain RELATIONSHIP BETWEEN MORPHOGENETIC ACTIVITY AND METABOLIC STABILITY OF INSECT JUVENILE HORMONE ANALOGUES* GUNDA REDDY and A. KRISHNAKUMARAN Department of Biology, Marquette University, Milwaukee, Wisconsin, 53233 (Received 3 March 1972) Abstract-The relationship between morphogenetic activity and metabolic stability of natural Cecropia juvenile hormone and some of its synthetic anal- ogues (methylenedioxyphenoxy, chlorophenoxy analogues, and ethyl-3,7,11- trimethyldodeca-2,4-dienoate) was studied in Tenebn’o pupae by parabiosis and in Galleria larvae by determination of the time course of decay of injected hor- mones. Parabiosis of dihomojuvenate or methylenedioxyphenoxy analogue treated Tenebrio pupae to fresh pupae 6 days after application of the hormone showed that the natural hormone but not the analogue was metabolized during the S-day period. Determination of the persistence of juvenile hormonal agents injected into O-day-old Gulleriu last instar larvae revealed that the natural hormone was in- activated much more rapidly when compared to methylenedioxyphenoxy, chlorophenoxy, and ethyl-3,7,11-trimethyldodeca-2,4-dienoate analogues. The significance of the positive correlation between greater stability and higher activity of juvenile hormone analogues is discussed. INTRODUCTION THE DETERMINATIONof the structures of the two Cecropia juvenile hormones, methyl-12,14-dihomojuvenate (methyl-lo-epoxy-7-ethyl-3,11-dimethyl-2,6-tri- decadienoate) (R~~LLERet al., 1967), and methyl-1Zhomojuvenate (methyl-lo- epoxy-3,7,11-trimethyl-2,6-tridecadienoate) (MEYER et al., 1968) was followed by the synthesis of several other analogues with juvenile hormone activity (BOWERS, 1969; WIGGLESWORTH,1969; SLLMA et al., 1970; SCHWARTZet al,, 1970; PALLOS et al., 1971; CRUICK~HANKand PALMERE,1971; STAAL et uZ., 1971). In several bioassays including the Tenebrio bioassay, some of the synthetic JH analogues showed higher morphogenetic activity than the natural Cecropia hormones. Two such potent analogues were the methylenedioxyphenoxy derivative of 12,14- dihomojuvenate (BOWERS, 1969) and ethyl-3,7,1 l-trimethyldodeca-2,4-dienoate, a compound lacking epoxide moiety (STAAL et al., 1971). These compounds were about 100-fold as active as methyl-12,14-dihomojuvenate in Tmebrio and/or GuZZeriubioassays (BOWERS,1969; STAALet al., 1971). The greater potency of hormonal analogues is a phenomenon well known to mammalian endocrinologists (ERCOLI and FALCONI, 1967) and was shown to be + This research is supported by N.S.F. research grant No. G.B. 19629. 2019 66 2020 GUNDAREDDY ANDA. KRISHNAKUMARAN true of insect moulting hormones (OHTAKI and WILLIAMS, 1970). Greater potency of a hormonal analogue can be accounted for either by its stereo chemical structure that is more suited for its function in a cell or by its greater metabolic stability. The higher activity of the analogues of mammalian gonadal hormones and of ecdysones was shown to stem from greater resistance of the analogues to enzymatic degra- dation (cf. STEELMANand HIRSCHMANN,1967). One consequence of this resistance to degradation is that the half life of the analogue was higher than that of the true hormone. Since a knowledge of the physiological basis of the higher activity of JH analogues is important for the proper utilization of these chemicals as insecticides, we sought to determine whether higher activity of the more potent JH analogues is a consequence of their greater stability in the test animal. Our study indicates that the more potent JH analogues are stable and persist longer in Tenebrio pupae and GuZZe-rialarvae than the natural hormone. MATERIALS AND METHODS Experimental animals Larvae of the wax moth, Galleria mellonella, were reared in the laboratory according to standard procedures (BECK, 1960; KRISHNAKUMARAN,1972). Newly ecdysed last instar (seventh instar) larvae, recognized by the size of the head capsule, weight (BECK, 1960), and dark pigmentation of the integument, were collected and maintained in plastic Petri dishes with ample food. Under these culture conditions, the seventh instar plus pharate pupa lasts about 9 days, of which the last 2 days represent the pharate pupal stage. In all the experiments reported here only seventh instar larvae were used and the term larva is used in the text to denote this stage. Mature larvae of Tmebrio molitor were purchased from bait dealers and main- tained in the laboratory at 25°C and 70% r.h. Fresh pupae less than 6 hr old, were used in these studies. Chemicals Cecropia juvenile hormone, methyl-la, 14-dihomojuvenate (Roller com- pound), methylenedioxyphenoxy (Bowers’ compound), and chlorophenoxy derivatives of juvenile hormone were generously supplied by Messrs. Hoffmann La Roche, Inc., Nutley, N. J. Ethyl-3,7,1 l-trimethyldodeca-2,4-dienoate was kindly supplied by Dr. J. B. Siddall of Zoecon Corp., Palo Alto, California. These compounds were mixed cis, tram isomers and were 99 per cent pure. As the dihomojuvenate was a mixture of isomers it was only about one-fifth as active as a sample of pure hormone kindly supplied by Professor Andre S. Meyer of Case Western Reserve University. Experimental methods Two different methods were used to determine the persistence or decay of JH and its analogues. ACTIVITY AND METABOLIC STABILITY OF JUVRNILE HORMONES 2021 In the first method, JH treated Tenebrio pupae were parabiosed with untreated pupae, 5 days after topical application of the hormone. Application of about 0.5 pg of Bowers’ compound or 6 pg of dihomojuvenate produced a more or less perfect second pupa. Five days after application of the hormonal agent a second pupal cuticle was formed but the second pupa never extricated itself from the old cuticle. These second pupae were tail-to-tail parabiosed to fresh Tenebrio pupae following the surgical methods outlined for parabiosis of Saturniid pupae (SCHNEIDERMAN, 1966). The parabiosed pupae (usually both the partners) deposited a new cuticle 6 to 8 days after parabiosis (Fig. 1). The nature of the cuticle deposited by the parabiosed pupae reflected the level of the persistent JH activity at the time of the parabiosis. If the parabiosed partners deposited a cuticle with pupal features, it was indicative of the persistence of the JH applied to one of the partners 6 days prior to the parabiosis. The absence of pupal characters in the parabionts at this apolysis was suggestive of the decay of the applied hormonal agent. Furthermore, quanti- tative estimation of the persistent JH activity was based on the morphological features of the cuticle of the parabionts and scoring them according to the pro- cedures described by BOWERSand THOMPSON(1963). The second method consisted of injection of a known quantity of the test chemical into a freshly ecdysed O-day-old (10 to 12 hr old) seventh stadium Galleria larva and the determination of the persistent hormonal activity, at successive time intervals. For this purpose we injected a known quantity (because of differences in the morphogenetic potency of the various juvenile hormone analogues the amount of the test chemical injected into each larva was varied; Cecropia hormone was injected at a dose of 25 pg/larva, while methylenedioxyphenoxy and chlorophenoxy analogues were injected at a dose of 5 pg/larva, ethyl-trimethyl-dodeca-dienoate was applied at a dose of 2 ,ug/larva) of the test chemical in 1~1 of peanut oil into each larva and at different time intervals after injection (0, 4, 8, 24, 48, and 72 hr) the larvae were frozen, homogenized in diethyl ether, and extracted in soxhlet for 3 hr. The lipid extract was washed according to the procedures described by GILBERT and SCHNEIDERMAN(1961) and assayed for morphogenetic activity in Tenebrio pupae (ROSE et al., 1968). Since the amount of lipid extracted at each stage was different, the amount of hormone applied to each Tenebrio pupa was adjusted to give equivalent concentration based on per mg of the lipid extracted. The scoring system was slightly modified from that of Bowers, in that the range of the score was 0 to 5 with increments of 0.5. The percentage of pupae that retained pupal features together with the individual scores of the pupae reflected the recovered JH activity. The JH activity recovered at 0 hr was regarded as 100 per cent of the injected hormone; and based on this the percentage recovered hormonal activity at different time intervals was calculated. To determine the efficiency of the extraction procedures we added a known quantity of the Cecropia hormone (12,14-dihomojuvenate) to a homogenate of the Galleria larvae prior to extraction. These studies revealed that the recovery of the hormone was slightly over the amount added, which was attributed to the fact that there is some endogenous JH in these larvae at this stage. Lipid extracts from 2022 GUNDAREDDY ANDA. KRISHNAKUMARAN peanut oil-injected controls showed no juvenilizing effect in the Tenebrio bioassay, although some morphogenetic effect was noticed in the more sensitive Gulleria wax test (SCHNEIDERMANet al., 1965). Thus we are measuring in these bioassays not only the persistent injected hormonal analogue but also the endogenous JH of the larvae. As our studies revealed that GaZZeria larval lipids do not have syner- gistic or inhibitory effects on the activity of the hormonal agents tested and because the endogenous hormone was undetectable in Tenebrio bioassay we believe that our data are valid reflections of the half life of the synthetic hormones in the larval milieu. RESULTS Inactivation of juvenile hormones in Tenebrio pupae The results reported in Table 1 show that all the Tenebrio pupae grafted to second pupae obtained by application of 6 pg of methyl-12,14-dihomojuvenate developed into adults with no pupal characters. This clearly shows that natural JH (6 pg) applied to the pupae was inactivated in the 5 days that elapsed from the time of application of hormone to the time of parabiosis.
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