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Webster, S.G, Keller, R. & Dircksen, H. 2012. the CHH Superfamily Of

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Webster, S.G, Keller, R. & Dircksen, H. 2012. the CHH Superfamily Of General and Comparative Endocrinology 175 (2012) 217–233 Contents lists available at SciVerse ScienceDirect General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen Review The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction ⇑ Simon George Webster a, , Rainer Keller b, Heinrich Dircksen c a School of Biological Sciences, Bangor University, LL57 2UW Bangor, UK b Institute for Molecular Biomedicine (LIMES-Institute), University of Bonn, D-53115 Bonn, Germany c Department of Zoology, Stockholm University, S-106 91 Stockholm, Sweden article info abstract Article history: Apart from providing an up-to-date review of the literature, considerable emphasis was placed in this Received 27 October 2011 article on the historical development of the field of ‘‘crustacean eyestalk hormones’’. A role of the neuro- Accepted 21 November 2011 secretory eyestalk structures of crustaceans in endocrine regulation was recognized about 80 years ago, Available online 29 November 2011 but it took another half a century until the first peptide hormones were identified. Following the identi- fication of crustacean hyperglycaemic hormone (CHH) and moult-inhibiting hormone (MIH), a large Keywords: number of homologous peptides have been identified to this date. They comprise a family of multifunc- Crustacean hyperglycaemic hormone tional peptides which can be divided, according to sequences and precursor structure, into two subfam- superfamily ilies, type-I and -II. Recent results on peptide sequences, structure of genes and precursors are described Gene Transcript and peptide structures here. The best studied biological activities include metabolic control, moulting, gonad maturation, ionic Localization and expression and osmotic regulation and methyl farnesoate synthesis in mandibular glands. Accordingly, the names Biological activities CHH, MIH, and GIH/VIH (gonad/vitellogenesis-inhibiting hormone), MOIH (mandibular organ-inhibiting Signal transduction and receptors hormone) were coined. The identification of ITP (ion transport peptide) in insects showed, for the first time, that CHH-family peptides are not restricted to crustaceans, and data mining has recently inferred their occurrence in other ecdysozoan clades as well. The long-held tenet of exclusive association with the eyestalk X-organ-sinus gland tract has been challenged by the finding of several extra nervous system sites of expression of CHH-family peptides. Concerning mode of action and the question of target tissues, second messenger mechanisms are discussed, as well as binding sites and receptors. Future challenges are highlighted. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction stalk (ES). He identified the sinus gland (SG) as a neurohaemal structure, i.e. as an aggregation of terminals of a cluster of neuro- Crustacean endocrinology began with the discovery, by Koller secretory perikarya that are located in the medulla terminalis [111,112], that colour change in shrimp is caused by blood-borne (MT). This cluster was named the X-organ (XO). For references factors which originated from tissues in the eyestalk. Hanström on the early history see Fingerman [70]. [85,86] provided the morphological basis by describing the anat- During an investigation of a possible hormonal control of carbo- omy of neurosecretory structures in the optic ganglia of the eye- hydrate metabolism in crustaceans, Abramowitz et al. [1] found in 1944 that injection of ES extracts into blue crabs, Callinectes sapi- dus, elicited a dramatic hyperglycaemia. The factor proved to be Abbreviations: AG, androgenic gland; CHH, crustacean hyperglycaemic hor- mone; CPRP, crustacean hyperglycaemic hormone precursor-related peptide; DA, very potent (0.001 ES equivalents giving a significant response), dopamine; ES, eyestalk; GC, guanylyl cyclase; GIH, gonad-inhibiting hormone; heat stable, highly concentrated in the SG, and was named a ‘‘dia- GPCR, G-protein coupled receptor; 5-HT, 5-hydroxy-tryptamine; IBMX, isobutylm- betogenic factor’’. In the course of further studies, this was eventu- ethylxanthine; ITP, ion transport peptide; IPRP, ion transport precursor-related ally replaced by the name crustacean hyperglycaemic hormone peptide; MF, methyl farnesoate; MIH, moult-inhibiting hormone; MO, mandibular organ; MOIH, mandibular organ-inhibiting hormone; NO, nitric oxide; PO, pericar- (CHH). A CHH isolated from the SG of the shore crab, Carcinus mae- dial organ; RIA, radioimmunoassay; SG, sinus gland; TR-FIA, time resolved- nas, was the first to be fully characterized [98]. This was directly fluoroimmunoassay; VIH, vitellogenesis-inhibiting hormone; XO-SG, X-organ-sinus followed by the report of the amino acid sequence of a peptide gland; YO, Y-organ. ⇑ from Homarus americanus [27] which proved to be very similar Corresponding author. Fax: +44 (0)1248 370731/371644. to that of Carcinus-CHH in terms of molecular size (72 amino acids) E-mail addresses: [email protected] (S.G. Webster), [email protected] (R. Keller), [email protected] (H. Dircksen). and sequence identity (61% identical residues). Particularly 0016-6480/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2011.11.035 218 S.G. Webster et al. / General and Comparative Endocrinology 175 (2012) 217–233 interesting was the observation that the Homarus-peptide exhib- been demonstrated in Homarus and crayfish species ited both CHH and moult-inhibiting hormone (MIH) activity. This [17,18,205,240]. With regard to biological activities, several novel key finding presaged two aspects of the structure and function of ones have more recently been added to the early recognized roles CHH and homologous peptides: (1) they are multifunctional hor- in the regulation of carbohydrate metabolism (CHH), secretagogue mones and, (2) they often display overlapping biological activities. action on the hepatopancreas, inhibition of moulting (MIH) and go- From C. maenas, a second peptide was soon fully identified [231], nad maturation (GIH/VIH). These comprise: the inhibition of which had distinct moult inhibiting, but no hyperglycaemic activ- methyl farnesoate secretion (MOIH activity) [137,227], water up- ity. MIH had certain structural features which set it apart from Car- take during ecdysis [36], and ionic and osmotic regulation [206]. cinus-CHH, notwithstanding basic similarities in the amino acid These results once again underscore the pleiotropic activities of sequence. After a few more sequences became available, a new CHH-superfamily peptides. Much further work is, however, needed peptide family emerged. Moreover, the CHHs from Carcinus and to elucidate the details and mechanisms of action, at the organ and Homarus on the one hand, and Carcinus MIH and another MIH-re- cellular level, which underlie the variety of biological effects. It is lated peptide from Homarus, VIH [231,235] on the other hand, safe to predict that more biological activities will eventually be could be considered prototypes of two subgroups of this family discovered. [99]. The entire grouping is now usually referred to as the CHH- Finally, an increasing number of studies have established that superfamily. For the two subfamilies, the terms type-I (CHH sensu CHH-superfamily peptides are not confined to neural tissues, par- stricto and ion transport peptides, ITPs) and type-II peptides (MIH ticularly the XO-SG system and the pericardial organs, but are also, and vitellogenesis-inhibiting hormones, VIHs) have been intro- unexpectedly and surprisingly, expressed in non-neural tissues duced [118]. Differences in the gene and precursor structures and organs. A particularly intriguing example is the transient firmly support this division (see below). appearance of secretory CHH-cells (paraneurons) in the fore- and During the last two decades, a remarkable upsurge of interest hindgut epithelium of C. maenas during premoult [36] (see below). has resulted in the identification of approximately 80 family Apart from the attempt to summarize the current state of members from about 40 crustacean species [232], increasingly less knowledge, it has been our aim to show how the field of CHH- by peptide sequencing, but by conceptual translation from cDNAs superfamily peptide research has developed and expanded during or in silico mining of transcriptomes and genomes. All of these the last twenty plus years. The different topics briefly outlined in (with perhaps one exception) can unequivocally be placed in one this introduction will be covered in some detail in this review of the two subfamilies. A remarkable feature from a historical point (For other recent reviews see: [15,23,43,118,200,232]). of view is the fact that putative hormones that had long been postulated from classical ablation and replacement experiments, have now all been identified as members of a common peptide 2. Structures of genes, derived precursors and peptides family. The moult-inhibiting hormone (MIH) was postulated more than 100 years ago by the observation [242], many times repeated, Members of the CHH-superfamily are grouped into type-I (CHH/ of precocious moulting after ES ablation. About 70 years ago, it was ITP) and type-II (MIH, MOIH, VIH/GIH) peptides based on their pre- found that ES ablation resulted in accelerated maturation of the cursor and primary structures [118]. With regard to their gene gonads [173], which led to the postulate of a gonad-inhibiting structures, there are at present no clear-cut
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