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A Potential Insect Growth Regulator: Synthesis and Bioactivity of an Allatostatin Mimic

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A Potential Insect Growth Regulator: Synthesis and Bioactivity of an Allatostatin Mimic Peptides 30 (2009) 1249–1253 Contents lists available at ScienceDirect Peptides journal homepage: www.elsevier.com/locate/peptides A potential insect growth regulator: Synthesis and bioactivity of an allatostatin mimic Zhen-peng Kai a,b, Juan Huang a, Stephen S. Tobe b,*, Xin-ling Yang a a Department of Applied Chemistry, College of Science, China Agricultural University, Beijing, 100193, PR China b Department of Cell and Systems Biology, University of Toronto, 25 Harbord St., Toronto, ON, Canada M5S 3G5 ARTICLE INFO ABSTRACT Article history: Insect growth regulators play an important role in Integrated Pest Management systems. Cockroach- Received 18 February 2009 type allatostatins (FGLamides) (ASTs), which are a family of basic peptides first isolated from brains of Received in revised form 15 March 2009 Diploptera punctata were originally discovered on the basis of their ability to inhibit the production of Accepted 17 March 2009 juvenile hormone by the corpora allata. For this reason, the ASTs can be regarded as possible IGR Available online 26 March 2009 candidates for pest control although the absence of effect in vivo, rapid degradation and high production costs of the natural peptides preclude their use in pest management. However, we have synthesized a Keywords: new AST mimic, H17, from the pentapeptide C-terminal active core of the AST. This mimic is able to Allatostatin significantly inhibit the biosynthesis of JH by cockroach CA in vitro (IC value: 12 nM) and in vivo IGR 50 Juvenile hormone following injection (IC50 value: 33 nM). H17 also shows a highly significant inhibition of JH production in Biosynthesis topical cuticular assays in vivo. Our results suggest that H17 has potential as an IGR for cockroach Cockroach control. Peptidomimetic ß 2009 Elsevier Inc. All rights reserved. 1. Introduction allatostatin receptors and elicits inhibition of JH production [4,9]. Garside et al. [3] studied the effects of injection of Dippu- Insect growth regulators (IGRs) are compounds that can AST 5 or Dippu-AST 6 analogs on rates of JH biosynthesis in vitro regulate the growth of insect pests and play an important role and on basal oocyte growth of mated female cockroaches, D. in Integrated Pest Management systems. As commercial IGRs have punctata. These authors found several peptidomimetics that some shortcomings such as the slowness of insecticidal activity, inhibited JH biosynthesis and oocyte growth significantly although pest resistance and limitations in their application, it has become the effects of injection were monitored only at one specific age. necessary to develop new IGRs that have new structures and new Piulachs et al. [8] also synthesized Dippu-AST 5 analogs that can targets to address these problems. inhibit JH biosynthesis and vitellogenin production by the fat body Cockroach-type (FGLa) allatostatins (ASTs) are a family of basic of the cockroach Blattella germanica. All the analogs were designed peptides first isolated from brains of Diploptera punctata that were with Dippu-AST 5 and Dippu-AST 6 as the lead compounds and originally found to inhibit the production of juvenile hormone (JH) both are octapeptides. In the present study, for purposes of by the corpora allata (CA) [13]. ASTs are potent inhibitors of JH potential application, we have focused on pentapeptide active core biosynthesis in cockroaches [5] and they therefore represent mimics, to reduce the production cost. potential leads for the discovery of new IGRs. However, ASTs also Our approach to the design of pseudopeptide analogs differs have some shortcomings such as lack of effect in vivo, rapid from those of Piulachs et al. [8] and Garside et al. [3], by focusing on degradation in vivo, and high production cost [3,7]. These issues the active core region and by making simple substitutions in this preclude the use of ASTs themselves in pest management. region to reduce costs of synthesis. Piulachs et al. [8], for example, Previous structure–activity studies demonstrated that the C- altered the nature of the peptide bond, thereby reducing the terminal pentapeptide Y/FXFGL-NH2 is the ‘active core’ region of susceptibility of the bond to hydrolysis. However, these com- the cockroach-type ASTs; this region probably binds to the pounds involved modifications outside the core region targeted in the present work and are considerably more difficult to synthesize. Other substitutions were made outside of the core region, which * Corresponding author. Tel.: +1 416 978 3517; fax: +1 416 978 3522. differs from our focus. Nachman et al. [7] and Garside et al. [3] E-mail addresses: [email protected] (S.S. Tobe), [email protected] replaced Phe-Gly residues in the pentapeptide with unnatural (X.-l. Yang). amino acids to reduce degradation by endoproteases, whereas in 0196-9781/$ – see front matter ß 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.peptides.2009.03.010 1250 Z.-p. Kai et al. / Peptides 30 (2009) 1249–1253 Fig. 1. Synthesis of H17. Reagents and conditions: (a) (E)-3-(4-nitrophenyl)acrylic acid, HBTU, HOBt, DIEA, DMF, room temperature, 3 h; (b) TFA, 5% phenol, 2.5% thioanisole, 5% water, room temp, 2 h. The crude peptide was purified on a C18 reversed-phase column with a flow rate of 1 mL/min using acetonitrile/water (80:20) containing 0.06% TFA as an ion-pairing reagent. UV detection was at 215 nm. The structure of H17 was confirmed by the presence of the following molecular ions using an 1100 series LC/MSD Trap (VL) (Agilent Technologies, USA). H17: 589.3 (calc. MNa+: 589.6). our research, the Tyr/Phe in the pentapeptide was replaced by (E)- 2.3. Bioassays 3-(4-nitrophenyl)acrylic acid to prevent degradation by amino- peptidases. This new AST mimic (H17) has potent effects in vitro 2.3.1. In vitro assays and in vivo on the inhibition of JH biosynthesis in the cockroach. All radiochemical assays for JH biosynthesis were performed This disruption in JH biosynthesis in the present study appears to using individual pairs of CA from day 7 mated females. Compounds be reflected in attenuated basal oocyte growth. were dissolved in medium 199 for assay as described previously [14,15]. Compounds were used in the bioassay on the same day 2. Methods that the samples were prepared. The solutions were discarded at the end of each day. Rates of JH release were determined using 2.1. Synthesis of peptidomimetic H17 the modified in vitro radiochemical assay [14,15]. This assay measures the incorporation of the radiolabeled S-methyl moiety of GFGL with resin was synthesized from Rink Amide-AM resin radiolabeled methionine into JH III in the final step of biosynthesis using the standard Fmoc/tBu chemistry and HBTU/HOBt (O- by CA maintained in vitro. CA were incubated for 3 h in 100 mLof Benzotriazole-N,N,N0,N0-tetramethyl-uronium-hexafluoro-phos- medium 199 (GIBCO, 1.3 mM Ca2+, 2% Ficoll, methionine-free) phate/1-hydroxybenzotriazole anhydrate) protocol [1].Incoming containing L[14C-S-methyl] methionine (40 mM, specific radio- amino acids were activated with HOBt, HBTU and DIEA in DMF for activity 1.48–2.03 GBq/mmol (Amersham)). Samples were 5 min, and couplings were run for 2 h. Removal of the N-terminal extracted and JH release determined. Each data point on the Fmoc group from the residues was accomplished with 20% dose–response figure represents replicate incubations of 10–27 piperidine in DMF for 20 min. experimental CA compared to control CA (i.e. no analog added). H17:(E)-3-(4-nitrophenyl)acrylic acid was coupled to the GFGLwithresinwithHOBt,HBTUandDIEAinDMFfor3hat 2.3.2. In vivo assays room temperature (Fig. 1). The peptide was cleaved from the resin with TFA containing 5% phenol, 2.5% thioanisole and 5% 2.3.2.1. Injection. H17 was dissolved in DMSO and then diluted to a water for 2 h. The crude peptide was purified on a C18 reversed- final DMSO concentration of 0.3% in H2O (stock final concentration phase column with a flow rate of 1 mL/min using acetonitrile/ of H17 was 10 mM). Injections were administered using a 26 gauge water (80:20) containing 0.06% TFA as an ion-pairing reagent. 10 mL Hamilton syringe. The needle was inserted into the UV detection was at 215 nm. The structure of H17 was membranous joint between the coxa and femur on the metathor- confirmed by the presence of the following molecular ions acic leg. Control insects were similarly injected, but with 5 mLof using an 1100 series LC/MSD Trap (VL) (Agilent Technologies, double distilled water. Five mLofH17 (at concentrations ranging USA). H17: 589.3 (calc. MNa+: 589.6). between 10 mM and 1 nM, serially diluted in H2O from the stock) (E)-3-(4-Nitrophenyl)acrylic acid was prepared using the were injected into D. punctata females at day 1, and animals were method of Sun et al. [12]. Rink Amide-AM resin (0.52 mmol/g assayed for JH biosynthesis at day 3 as described (see Section substitution), HOBt, HBTU, DIEA (N,N0-diisopropyl ethylamine), 2.3.1). All injections were administered to non-anesthetized mated TFA (trifluoroacetic acid) and Fmoc-protected amino acids were female D. punctata. Assuming a hemolymph volume of 50 mL for purchased from GL Biochem (Shanghai) Ltd. HPLC grade DMF (N,N- day 1 adult female D. punctata [6], the final concentrations of the dimethyl-formamide), DCM (dichloromethane) and acetonitrile were purchased from DIMA Technology Inc. (USA). Thioanisole, Table 1 99% was purchased from ACROS, USA. Age at oviposition following treatment with H17a,b. Age (days) Number of animals ovipositing 2.2. Animals Controlsc Injection Topical applicationd Newly emerged mated female D. punctata (day 0) were 7 24 (100%) 24 (100%) 0 isolated from stock cultures.
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