Insect Juvenile Hormone Binding Protein Shows Ancestral Fold Present in Human Lipid-Binding Proteins

Kolodziejczyk, R.; Bujacz, G.; Jakób, Michał; Ożyhar, Andrzej; Jaskólski, Mariusz; Kochman, Marian

doi:10.1016/j.jmb.2008.01.026

Cited by 53 publications

(52 citation statements)

References 39 publications

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“…JH is important in caste differentiation in eusocial insects, including termites 12,52 . Haemolymph JH-binding proteins (JHBPs), which transport JH to its target tissues 53 , are reduced within the termites (21 to 33 genes) but significantly expanded in B. germanica (51 copies; P = 0018; Supplementary Table 6). Thirteen of the JHBP genes are overexpressed in adult females and only 8 in nymphs in B. germanica ( Fig.…”

Section: Nature Ecology and Evolutionmentioning

confidence: 99%

Hemimetabolous genomes reveal molecular basis of termite eusociality

et al. 2018

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E usociality, the reproductive division of labour with overlapping generations and cooperative brood care, is one of the major evolutionary transitions in biology 1 . Although rare, eusociality has been observed in a diverse range of organisms, including shrimps, mole rats and several insect lineages [2][3][4] . A particularly striking case of convergent evolution occurred within the holometabolous Hymenoptera and in the hemimetabolous termites (Isoptera), which are separated by over 350 Myr of evolution 5 . Termites evolved within the cockroaches around 150 Myr ago, towards the end of the Jurassic period 6,7 , about 50 Myr before the first bees and ants appeared 5 . Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed extensive research into the origins of eusociality within ants and bees [9][10][11] , a paucity of genomic data from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality in this hemimetabolous clade.The conditions under which eusociality arose differ greatly between the two groups. Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis. In termites, workers are immatures and only reproductive castes are adults 12 , while in Hymenoptera, adult workers and queens represent the primary division of labour. Moreover, termites are diploid and their colonies consist of both male and female workers, and usually a queen and king dominate reproduction. This is in contrast to the haplodiploid system found in Hymenoptera, in which all workers and dominant reproductives are female. It is therefore intriguing that strong similarities have evolved convergently within the termites and the hymenopterans, such as differentiated castes and a nest life with reproductive division of labour. The termites can be subdivided into wood-dwelling and foraging termites. The former belong to the lower termites and produce simple, small colonies with totipotent workers that can become reproductives. Foraging termites (some lower and all higher termites) form large, complex societies, in which worker castes can be irreversible 12 . For this reason, higher, but not lower, termites can be classed as superorganismal 13 . Similarly, within Hymenoptera, varying levels of eusociality exist.Here we provide insights into the molecular signatures of eusociality within the termites. We analysed the genomes of two lower and one higher termite species and compared them to the genome

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Section: Nature Ecology and Evolutionmentioning

confidence: 99%

Hemimetabolous genomes reveal molecular basis of termite eusociality

et al. 2018

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“…There are, however, two major differences between the families: a second disulfide bond in the JHBPs, not present in To; and the presence of two conserved C-terminal sequence motifs that are unique to the To family (2). Very recently, the structure of JHBP from the moth Galleria mellonella (GmJHBP) has been solved, revealing an unusual fold in which a highly curved antiparallel ␤-sheet wraps around a long ␣-helix (16). Although no direct evidence of ligand binding was obtained, two hydrophobic cavities were found within the protein, and it was hypothesized that one cavity binds JH.…”

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confidence: 99%

“…Although no direct evidence of ligand binding was obtained, two hydrophobic cavities were found within the protein, and it was hypothesized that one cavity binds JH. The presence of the second cavity was not anticipated, and its role remains unclear (16).…”

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confidence: 99%

Crystal Structure of Epiphyas postvittana Takeout 1 with Bound Ubiquinone Supports a Role as Ligand Carriers for Takeout Proteins in Insects

Hamiaux

Stanley

Greenwood

et al. 2009

Journal of Biological Chemistry

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Takeout (To) proteins are found exclusively in insects and have been proposed to have important roles in various aspects of their physiology and behavior. Limited sequence similarity with juvenile hormone-binding proteins (JHBPs), which specifically bind and transport juvenile hormones in Lepidoptera, suggested a role for To proteins in binding hydrophobic ligands. We present the first crystal structure of a To protein, EpTo1 from the light brown apple moth Epiphyas postvittana, solved in-house by the single-wavelength anomalous diffraction technique using sulfur anomalous dispersion, and refined to 1.3 Å resolution. EpTo1 adopts the unusual ␣/␤-wrap fold, seen only for JHBP and several mammalian lipid carrier proteins, a scaffold tailored for the binding and/or transport of hydrophobic ligands. EpTo1 has a 45 Å long, purely hydrophobic, internal tunnel that extends for the full length of the protein and accommodates a bound ligand. The latter was shown by mass spectrometry to be ubiquinone-8 and is probably derived from Escherichia coli. The structure provides the first direct experimental evidence that To proteins are ligand carriers; gives insights into the nature of endogenous ligand(s) of EpTo1; shows, by comparison with JHBP, a basis for different ligand specificities; and suggests a mechanism for the binding/release of ligands. Takeout (To) 3 family have been proposed to have important roles in various aspects of insect physiology and behavior and as such may represent novel targets for insect control strategies. The original member, To, was discovered in Drosophila melanogaster as a clock-regulated gene, acting as a molecular link between circadian rhythms and feeding behavior (1, 2). In addition, To expression is regulated by the somatic sex determination pathway and affects male courtship behavior (3, 4). To has a predicted secretion signal (1) and is secreted in the hemolymph of adult males (4). At least 80 To genes have now been identified from seven orders of insect, including 20 from D. melanogaster, but few have been characterized in any detail. Due to the localization and/or expression profiles of their transcripts, some are proposed to have roles in chemosensory perception (5-8), whereas others are thought to be involved in binding terpenoids (9), including juvenile hormones (JH) (10 -15). Members of theTo proteins share limited sequence similarity and a conserved N-terminal disulfide bond with juvenile hormone-binding proteins (JHBPs). These proteins specifically bind and transport JH to target tissues in the Lepidoptera, further suggesting a role for To proteins in binding hydrophobic ligands (2). There are, however, two major differences between the families: a second disulfide bond in the JHBPs, not present in To; and the presence of two conserved C-terminal sequence motifs that are unique to the To family (2). Very recently, the structure of JHBP from the moth Galleria mellonella (GmJHBP) has been solved, revealing an unusual fold in which a highly curved antiparallel ␤-sheet wraps around a...

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“…It regulates embryogenesis, development and eclosion, and stimulates sexual maturation in adults. 38 Two SNPs in the haemolymph JH binding protein CG15497 were strongly associated (P D 1.1 £ 10 ¡18 and P D 1.3 £ 10 ¡18 ) with pigmentation in the combined xQTL mapping analysis. These proteins are responsible for transporting JH from the corpora allata through the haemolymph to specific target tissues.…”

Section: Even More Candidate Genesmentioning

confidence: 90%