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Allatostatins in Gryllus Bimaculatus Eur. J. Entorno!. 96: 267-274, 1999 ISSN 1210-5759 Allatostatins inGryllus bimaculatus (Ensifera: Gryllidae): New structures and physiological properties* M atthias W. LORENZ’, R oland KELLNER2 and K laus H. HOFFMANN1 'Department of Animal Ecology 1, University of Bayreuth, 95440 Bayreuth, Germany; e-mail:[email protected] 2Biomed Fo/GBT, Merck KGaA, 64271 Darmstadt, Germany Key words. Allatostatin, juvenile hormone, farnesol, peptide sequence, cricket,Gryllus bimaculatus, Gryllidae Abstract. Four peptides with allatostatic activity were isolated from brains of the Mediterranean field cricket, Gryllus bimaculatus. Three of them (Grb-AST A3: AGMYSFGL-NH2; Grb-AST A4: SRPFGFGL-NH2; Grb-AST A5: GPDHRFAFGL-NH2) belong to the wide-spread family of Y/FXFGL/I-amide peptides, the fourth (Grb-AST B5: AWDQLRPGW-NH2) is a member of the W2W9- amide family of neuropeptides. All of these peptides are potent inhibitors of juvenile hormone (JH) biosynthesis by cricket corpora allata in vitro, causing 50% inhibition of JH biosynthesis at 0.4-3 x 10~8 M. The two peptides Grb-AST A5 and Grb-AST B5 have virtually the same potency and efficacy in inhibiting JH biosynthesis in vitro. No synergistic effect of the two peptide families with respect to the inhibition of JH biosynthesis could be observed. Peptides of both families decrease the accumulation of methylfarneso- ate, the direct precursor of JH, within CA that have been incubated in farnesol-rich medium. This suggests an involvement of these ASTs in the late steps of JH biosynthesis. INTRODUCTION tion of vitellogenin release from the periovaric fat body of Development and reproduction of insects are regulated the German cockroach,Blattella germánica (Martín et ah, to a large extent by juvenile hormone (JH) and ecdyster­ 1996) and the inhibition of myogenic contractions of the oids (Hardie, 1995; Hoffmann & Lorenz, 1997). During foregut (Duve et ah, 1995), the hindgut (Duve et ah, the last decade, interest has focused on the isolation, puri­ 1996), and the oviduct (Schoofs et ah, 1997). Further­ fication and identification of factors that regulate the bio­ more, they can act as antimyotropins (Hertel & Penzlin, synthesis and release of these glandular hormones, since 1992; Lange et ah, 1995). it is hoped that such compounds may help in designing In addition to the Y/FXFGL/I-amide allatostatins (A- safer and more specific insecticides (Couillaud & Peype- allatostatins, Lorenz et ah, 1995a) a fourth group of alla­ lut, 1995; Hoffmann & Lorenz, 1998). Factors that stimu­ tostatic neuropeptides, members of the W2W9-amide late (allatotropins) or inhibit (allatostatins) the activity of peptide family, has been found in brain extracts of the the JH-producing corpora allata (CA) have been isolated cricket Gryllus bimaculatus (Lorenz et ah, 1995b). These from a variety of insects (for review see Gade et al., 1997; peptides have been designated B-allatostatins or W2W9- Hoffmann et ah, 1999). The allatoregulating peptides can amide allatostatins and are closely related to myoinhibit- be classified into four groups. The first two groups are an ing peptides isolated from Locusta migratoria (Schoofs et allatotropin (Mas-AT) isolated from the tobacco horn- ah, 1991) and M. sexta (Blackburn et ah, 1995). Members worm, Manduca sexta (Kataoka et ah, 1989) and an alla­ of this peptide family have also been found in brain ex­ tostatin (Mas-AST), isolated from the same species (Kra­ tracts of the Indian stick insect Carausius morosus (Lo­ mer et ah, 1991), that both seem to act as allatoregulators renz et ah, 1998a). However, their allatostatic function only in lepidopterans (Weaver et ah, 1998). seems to be restricted to crickets (Lorenz et ah, 1997a). In The third and most prominent group of allatoregulating addition to their myoinhibiting function in locusts and neuropeptides is the Y/FXFGL/I-amide allatostatin (AST) moths and their allatostatic effect on cricket CA, they superfamily, originally isolated from brains of the Hawai­ were shown to inhibit ovarian ecdysteroid biosynthesis in ian beetle roach, Diploptera punctata (Woodhead et ah, crickets (Lorenz et ah, 1997b) and they are capable of af­ 1989). Although these peptides have been isolated from fecting JH-, ecdysteroid-, and vitellogenin-titres in vivo various cockroaches (Belles et ah, 1994; Weaver et ah, when injected into adult crickets (Lorenz et ah, 1998b). 1994), flies (Duve et ah, 1993), mosquitoes (Veenstra et In the present study, we report the isolation and identi­ ah, 1997), crickets (Lorenz et ah, 1995a), locusts (Vee- fication of additional members of both the Y/FXFGL/I- laert et ah, 1996), and moths (Davis et ah, 1997; Duve et amide and the W2W9-amide allatostatin family from ah, 1997a, b), they seem to inhibit JH biosynthesis only in cricket brains, and on one of their possible target sites cockroaches and crickets. However, additional functions within the pathway leading to the formation of JH III. of this peptide family have been found, such as the inhibi­ * This paper is based on a lecture presented at the 6th European Congress of Entomology held in České Budějovice, Czech Repub­ lic, August 1998. 267 MATERIAL AND METHODS ments to obtain maximally stimulated CA. In order to investi­ gate effects of allatostatins under such stimulated conditions, the Insects and tissue dissection CA were preincubated in radioactive medium without farnesol, Mediterranean field crickets Gryllus bimaculatus de Geer transferred into medium with 200 pM farnesol for the 1st incu­ (Ensifera: Gryllidae) were reared as described (Lorenz et al., bation and transferred again after 2 h, this time into medium ei­ 1997b). Brains were dissected from 2-4 day-old virgin females, ther containing 200 pM farnesol alone (control) or 200 pM immediately transferred into ice-cold extraction medium farnesol plus the allatostatins to be tested (in concentrations of (methanol/water/acetic acid, 100/10/1, v/v/v), and stored at 10~'° to 10^ M). After the second incubation period the glands -75°C. Single CA from 3 day-old virgin females were used to were transferred into 20 pi of HPLC-grade water. Medium and test chromatographic fractions for allatoregulating activity and glands were then extracted separately with isooctane. The isooc­ to generate dose-response curves with the synthetic peptides. tane phase from the extracted medium containing JH III that had Single CA from 1 day-old unpaired adult males were used in the been released into the medium was directly pipetted into 2.5 ml experiments employing farnesol. of scintillation cocktail Rotiszint 11 (Roth, Karlsruhe, Radiochemical assay for allatostatic activity Germany). The isooctane phase from the CA extract that con­ tained unreleased JH III that had been produced by the CA, as Juvenile hormone biosynthesis and the effects of chroma­ well as the immediate JH III precursor, methylfarnesoate (MF), tographic fractions and synthetic peptides on CA activity were was subjected to thin-layer chromatography on Silica gel 60 F254 determined by the rapid partition assay (Feyereisen & Tobe, plates (Merck, Darmstadt, Germany) using xylol : ethylacetate 1981) as described (Lorenz et al., 1997b). In the standard ex­ (80/20, v/v) as the solvent system. Unlabelled JH III (Fluka, periments, single CA were preincubated in radioactive medium Neu-Ulm, Germany) that had been added to the extract served to allow the precursor (L-[methyl-l4C]methionine) to equilibrate as a tracer to identify the JH III band. MF was identified on the with the endogenous methionine within the glands, resulting in basis of its Rf-value. Bands were visualised by uv-illumination consistent rates of JH biosynthesis during the following incuba­ at 254 nm and scraped into 3 ml of scintillation cocktail Rotisz­ tions. After 90 min, the CA were transferred to fresh radioactive int 2211 (Roth). Samples were measured using a TriCarb 2100 medium without any additives and incubated for 120 min (first TR liquid scintillation counter (Canberra Packard, Frankfurt, incubation) to establish basal rates of JH release. Then, the CA Germany). were transferred for the second incubation (120 min) either to fresh radioactive medium without any additions (controls) or to Tissue extraction and peptide purification medium containing the HPLC fractions/synthetic peptides to be Extraction and SEP-PAK purification of the brain material tested. Incubations were stopped by removing the glands from were carried out as described (Lorenz et al., 1995b). Since only the medium. Inhibition of CA activity was calculated as the per­ the 40% acetonitrile (MeCN) SEP-PAK fraction showed consis­ centage change in JH release between the first and the second tent allatostatic activity, this fraction was chosen for further pu­ incubation. rification by a four step reversed-phase high performance liquid In some experiments, the glands were incubated in medium chromatography (HPLC) procedure. The first HPLC step was containing the allatostatins to be tested without preincubation. carried out on a Shimadzu HPLC system (LC-9A V2.2 HPLC The CA were repeatedly transferred in hourly or two-hour inter­ pump; SPD-6A UV-VIS detector, set to 215 nm; FCV-9AL low- vals into fresh medium containing allatostatins; the total incuba­ pressure flow control valve; DGU-2A helium degassing unit; tion time in the presence of allatostatins was 5 h in these experi­ Shimadzu Europa GmbH, Duisburg, Germany), the other HPLC ments. Then the CA were repeatedly transferred into medium steps were carried out on a Jasco series 900 high-pressure gradi­ without allatostatins in hourly intervals to follow the recoveryent HPLC system (Jasco, Groß-Umstadt, Germany), consisting from inhibition. of two pumps PU-980, an on-line degasser DG-980-50, a vari­ Farnesol, a late precursor of JH biosynthesis that stimulates able wavelength UV-detector UV-975 (set to 214 nm), a column the last steps of JH formation was employed in some experi­ thermostat Jet-stream Peltier (set to 25°C), and a Rheodyne T able 1.
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