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Is the Regulation of Corpora Allata Activity Their Primary Function?*

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Is the Regulation of Corpora Allata Activity Their Primary Function?* REVIEW Eur. J. Entomol. 96: 255-266, 1999 ISSN 1210-5759 Allatostatins and allatotropins: Is the regulation of corpora allata activity their primary function?* K laus H. HOFFMANN, M artina MEYERING-VOS and M atthias W. LORENZ Tierökologie 1, Universität Bayreuth, D-95440 Bayreuth, Germany; e-mail: [email protected] Key words. Allatostatin, allatotropin, JH-biosynthesis, myotropic activity, immunocytochemistry, cDNA, prohormone gene sequences, second messenger, protostomes, Insecta, Crustacea Abstract. More than 60 neuropeptides that inhibit juvenile hormone synthesis by the corpora allata have been isolated from the brains of various insect species. Most of them are characterized by a common C-terminal pentapeptide sequence Y/FXFGL/l/V (alla­ tostatin A family, allatostatin superfamily). Besides the allatostatin A family, allatostatic neuropeptides belonging to other two pep­ tide families (W2W9-allatostatins or allatostatin B family; lepidopteran allatostatin) were reported. So far, only one allatotropin has been identified. Here we discuss latest literature on the multiplicity and multifunctionality of the allatoregulating neuropeptides, their physiological significance as well as their evolutionary conservation in structure and function. INTRODUCTION Since 1989, more than 60 neuropeptides that inhibit JH Development and reproduction of insects are regulated production by the CA in homologous or heterologous bio­ to a large extent by juvenile hormones (JH) and ecdyster- assays in vitro have been isolated from the brains of a few oids. During the larval stages, these hormones control insect species. Most of them are characterized by a com­ moulting and metamorphosis whereas in adult insects, mon C-terminal pentapeptide sequence Y/FXFGL/I-NH2 they are involved in the regulation of vitellogenesis in fe­ (Duve et al., 1997a; Gade et al., 1997; Veenstra et al., males and spermatogenesis and growth of the accessory 1997; Veelaert et al., 1998). The sequences of many more reproductive glands in males (Koeppe et al., 1985; allatostatins of the Y/FXFGL/I-NH 2 family were deduced Nijhout, 1994; Riddiford, 1994; Gade et al., 1997). Juve­ from prohormone gene sequences (Donly et al., 1993; nile hormones are synthesized and released from the cor­ Ding et al., 1995; East et al., 1996; Vanden Broeck et al., pora allata (CA) which are present in all insect stages. 1996; Veenstra et al., 1997; Belles et al., 1999). Besides Juvenile hormone III (C16-JH) is the predominant insect the Y/FXFGL/I-NH2 allatostatins (allatostatin A family, JH; the higher homologues (JH 0 ,1, II) are only produced allatostatin superfamily), allatostatic neuropeptides be­ in Lepidoptera. A new type of JH has been identified in longing to another two peptide families were reported higher dipterans, the JH III bisepoxide (JHB3) (Richard et (Kramer et al., 1991; Lorenz et al., 1995a). So far, only al., 1989). one allatotropin has been identified (Kataoka et al., Haemolymph JH levels may change dramatically over 1989). relatively short periods of time. The finite haemolymph or Allatostatins have been the subject of several reviews in tissue levels of JH are a balance between the rate at which which more extensive bibliographies can be found (Stay hormones are biosynthesized by the CA and the rate at et al., 1994a; Tobe et al., 1995; Bendena et al., 1997; which these molecules are metabolized or excreted. Al­ Weaver et al., 1998). In the present review we discuss lat­ though JH-degrading enzymes are known to play a role in est literature on the multiplicity and multifunctionality of determining physiological levels of JH, it is likely that the the allatostatins (and also of the one known allatotropin), overall control of tissue and haemolymph levels is more the physiological significance of such a variety of related intimately linked with changes in the rates of JH biosyn­ peptides, as well as their evolutionary conservation in thesis (Weaver et al., 1998). structure and function. During the last decade, interest has focused on factors NEUROPEPTIDES OF THE ALLATOSTATIN that regulate JH biosynthesis by the CA (Stay et al., SUPERFAMILY 1994a). Juvenile hormone biosynthesis is regulated by The name allatostatin was originally introduced to de­ both peptidergic and aminergic inputs (Rachinsky & fine unknown regulatory factors that inhibited JH biosyn­ Tobe, 1996). Depending upon the species and develop­ thesis in vitro by the CA of insects (Tobe, 1980). When ment stage, their signals may be either stimulatory or in­ these structures were isolated at first from brain extracts hibitory (allatotropins and allatostatins), and the signals of the cockroach Diploptera punctata (Woodhead et al., may reach the glands via the haemolymph or via nervous 1989; Pratt et al., 1989) and identified as neuropeptides, connections (Stay et al., 1994a). the term allatostatin was retained. Meanwhile, further * This paper is based on a lecture presented at the 6th European Congress of Entomology held in České Budějovice, Czech Repub­ lic, August 1998. 255 members of the allatostatin superfamily have been iso­ THE ALLATOSTATIN SUPERFAMILY GENES lated and identified from the cockroaches Periplaneta The amino acid sequence of the first allatostatin precur­ americana (Weaver et al., 1994) andBlattella germanica sor was deduced from a cDNA sequence derived from (Belles et ah, 1994), the cricket Gryllus bimaculatus (Lo­ mRNA isolated from the brain of virgin female D. punc­ renz et ah, 1995b), the locust Schistocerca gregaria (Vee- tata (Donly et ah, 1993). Specific primers designed laert et ah, 1996a), the stick insect Carausius morosus against sequences within the coding region of the D. (Lorenz et ah, 1998a), the blowfly Calliphora vomitoria punctata cDNA were subsequently used to amplify allato­ (Duve et ah, 1993), the mosquito Aedes aegypti (Veenstra statin specific DNA fragments by PCR from both P. et ah, 1997), the lepidopteran species Cydia pomonella, americana genomic DNA and brain-derived cDNA (Ding Helicoverpa armigera (Duve et ah, 1997a) and Manduca et ah, 1995). The pre-proallatostatins of D. punctata and sexta (Davis et ah, 1997), and the honeybee, Apis mellif- P. americana, two distantly related cockroach species, are era (Unnithan et ah, 1995; H. Kaatz, pers. commun.). In similar in sequence, in size and in organization. Each pre­ S. gregaria, one peptide (Scg-AST 1) ends with Val at the cursor is organized into domains beginning with a hydro- C-terminus and, therefore, the allatostatin superfamily phobic signal sequence domain followed by the allatosta­ should be named Y/FXFGL/I/V-NH 2 family. In flies, an­ tin peptides with associated sequence Gly-Lys/Arg-Arg other sub-group of the same peptide family ending C- required for a-amidation and endoproteolytic cleavage, terminally with Met-NLL instead of Leu/Ile/Val-NH2 was and four acidic spacer regions which interrupt the ar­ found (Duve et ah, 1993, 1994; 1995a). Three of the four rangement of peptides and probably serve to compensate known Met-callatostatins originate through post- the basic charge contribution of the cleavage sites. In ad­ translational modifications. [Hyp3] Met-callatostatin dition to the already purified peptide sequences, a number (Cav-AST 6) and [Hyp2] Met-callatostatin (Cav-AST 7) of other putative allatostatin-like peptides were discov­ are hydroxylated analogs of Cav-AST 5; the third one ered by analysing their precursors. The P. americana pre­ represents a truncated hexapeptide (Cav-AST 8), des Gly- cursor is cleaved into 14 different allatostatins, compared Pro Cav-AST 5. The post-translational modification of to 13 peptides that derived from the D. punctata prolyl hydroxylation may provide the peptides with a precursor. The difference in peptide number is the result higher resistance to enzymatic degradation. When using of a carboxyl-terminal substitution/deletion in the D. the allatostatins in the rapid partition assay for determina­ punctata counterpart to Pea-AST 12 which has destroyed tion of in vitro JH-release (Feyereisen & Tobe, 1981) in a the amidation signal that is required for biological activity homologous way, only in cockroaches and crickets a (Weaver et al., 1998). dose-dependent, rapid and reversible inhibition of JH- Further gene sequences of allastostatins have been re­ release was observed (Woodhead et ah, 1989; Pratt et ah, ported from the cockroaches Blattella germanica, Blatta 1991a; Belles et ah, 1994; Weaver et ah, 1994; Wood- orientalis, Supella longipalpa, and Blaberus craniifer head et ah, 1994; Lorenz et ah, 1995b). Structure activity (Bellés et al., 1999), the orthopteran Schistocerca gre­ studies of the cockroach and cricket allatostatins have garia (Vanden Broeck et al., 1996), the dipterans Calli­ shown that these peptides are capable of inhibiting JH III- phora vomitoria, Lucilia cuprina (East et al., 1996) and biosynthesis in CA, but with varying degrees of efficacy Aedes aegypti (Veenstra et al., 1997), and the lepidop­ (Lange et ah, 1995; Weaver et ah, 1998). In the two cock­ teran Helicoverpa armigera (in Duve et al., 1997a). The roach species, D. punctata and P. americana, there are precursors of all the cockroach species are similar in size, major differences in the sensitivity of the CA to the alla­ and the organisation of the allatostatins that they contain tostatins at different stages of development and particu­ (13 or 14, depending on the species) has been conserved. larly during the female reproductive cycle (Pratt et ah, The four acidic domains separate the individual func­ 1990, 1991b; Stay et ah, 1991; Weaver 1991; Fairbaim & tional peptides into five groups: peptides 1^1; 5-10; 11; Stay, 1995; Weaver et ah, 1995). Unnithan & Feyereisen 12 in the case of P. americana and B. orientalis', 13-14. (1995) demonstrated that the sensitivity to allatostatins The schistostatin precursor differs from that of cockroach can be experimentally manipulated (CA transplantation, pre-proallatostatins in size, in sequence, and in organisa­ CA denervation, ovariectomy) and suggest the existence tion. It contains 10 peptides that are interrupted only once of humoral factor(s) (from the ovary?) responsible to the by an acidic spacer (schistostatins 1—4 and 5-10).
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