From the Genome to the Proteome: Uncovering Peptides in the
            <i>Apis</i>
            Brain

Hummon, Amanda B.; Richmond, Timothy A.; Verleyen, Peter; Baggerman, Geert; Huybrechts, Jurgen; Ewing, Michael A.; Vierstraete, Evy; Rodriguez-Zas, Sandra L.; Schoofs, Liliane; Robinson, Gene E.; Sweedler, Jonathan V.

doi:10.1126/science.1124128

Cited by 289 publications

(303 citation statements)

References 18 publications

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“…The honey bee genome contains genes encoding two ILPs (AmIlp1 and AmIlp2), AKH (AmAkh), and the putative receptors for these peptides (AmInR1, AmInR2, and AmAkhR) (25)(26)(27). Several lines of evidence indicate a role for AmIlp1 as a functional insulin propeptide gene.…”

Section: Characterization Of Insulin-related Neuropeptide and Receptormentioning

confidence: 99%

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

Ament

Corona

Pollock

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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305

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It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes. Age-related division of labor in honey bee colonies, a highly derived behavioral system, involves the performance of different feeding-related tasks by different groups of individuals. Older bees acquire the colony's food by foraging for nectar and pollen, and the younger ''nurse'' bees feed larvae processed foods. The transition from hive work to foraging has been shown to be socially regulated and associated both with decreases in abdominal lipid stores and with increases in brain expression of genes implicated in feeding behavior in Drosophila melanogaster. Here we show that division of labor is influenced by a canonical regulator of food intake and energy balance in solitary species, the insulin/insulin-like growth factor signaling (IIS) pathway. Foragers had higher levels of IIS gene expression in the brain and abdomen than did nurses, despite their low lipid stores. These differences are likely nutritionally mediated because manipulations that induced low lipid stores in young bees also up-regulated these genes. Changes in IIS also causally influenced the timing of behavioral maturation: inhibition of the insulin-related target of rapamycin pathway delayed the onset of foraging in a seasonally dependent manner. In addition, pathway analyses of microarray data revealed that nurses and foragers differ in brain energy metabolism gene expression, but the differences are opposite predictions based on their insulin-signaling status. These results suggest that changes in the regulation of the IIS pathway are associated with social behavior.Apis mellifera ͉ behavioral maturation ͉ social insect ͉ nutrition ͉ foraging A n important problem in biology is to understand the molecular basis for complex behavior. It has been proposed that one route of behavioral evolution involves novel regulation of conserved genes (1). It is well established that orthologous sets of genes regulate the development of body plans across taxa (2), but this idea has only recently begun to be tested for behavior (3,4).Age-related division of labor in honey bee colonies involves the performance of different food-related tasks by different groups of individuals. Nurse bees feed brood for the first 1-2 weeks of adult life, process and store food for another week, and then shift to foraging for nectar and pollen at Ϸ2-3 weeks of age (5). This division of labor is socially regulated; bees speed up, slow down, or reverse their maturation in response to colony needs (6). Although the mechanics of foraging in honey bees are similar to food-gathering in solitary bees, there are fundamental differences. Honey bees forage to improve the fitness of the colony rather than their own; they collect food when their colony needs it. Honey bees feed on honey before exiting the hive to fuel their foraging flights, and most of the food obtained on a foraging trip is not for their own sustenance.We hypothesized that the regulation of honey bee behavioral mat...

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Section: Characterization Of Insulin-related Neuropeptide and Receptormentioning

confidence: 99%

Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies

Ament

Corona

Pollock

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

305

341

View full text Add to dashboard Cite

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“…pNPs have a signal peptide (SP) and enter the secretory apparatus where dedicated proteases cleave them at mono-or dibasic cleavage sites (12) and where the maturing peptides are often further modified (13). pNPs are ubiquitous in eumetazoans, and genomics and mass spectrometry revealed the full neuropeptide repertoire of several species (14)(15)(16)(17)(18)(19)(20). Given their wide occurrence in metazoans, and importance in neuronal regulation, a global pNP phylogeny would further our knowledge of nervous system evolution.…”

mentioning

confidence: 99%

Global view of the evolution and diversity of metazoan neuropeptide signaling

Jékely

2013

Proc. Natl. Acad. Sci. U.S.A.

386

651

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Neuropeptides are signaling molecules that commonly act via G protein-coupled receptors (GPCRs) and are generated in neurons by proneuropeptide (pNP) cleavage. Present in both cnidarians and bilaterians, neuropeptides represent an ancient and widespread mode of neuronal communication. Due to the inherent difficulties of analyzing highly diverse and repetitive pNPs, the relationships among different families are often elusive. Using similarity-based clustering and sensitive similarity searches, I obtained a global view of metazoan pNP diversity and evolution. Clustering revealed a large and diffuse network of sequences connected by significant sequence similarity encompassing one-quarter of all families. pNPs belonging to this cluster were also identified in the early-branching neuronless animal Trichoplax adhaerens. Clustering of neuropeptide GPCRs identified several orthology groups and allowed the reconstruction of the phyletic distribution of receptor families. GPCR phyletic distribution closely paralleled that of pNPs, indicating extensive conservation and long-term coevolution of receptor-ligand pairs. Receptor orthology and intermediate sequences also revealed the homology of pNPs so far considered unrelated, including allatotropin and orexin. These findings, together with the identification of deuterostome achatin and luqin and protostome opioid pNPs, extended the neuropeptide complement of the urbilaterian. Several pNPs were also identified from the hemichordate Saccoglossus kowalevskii and the cephalochordate Branchiostoma floridae, elucidating pNP evolution in deuterostomes. Receptor-ligand conservation also allowed ligand predictions for many uncharacterized GPCRs from nonmodel species. The reconstruction of the neuropeptide-signaling repertoire at deep nodes of the animal phylogeny allowed the formulation of a testable scenario of the evolution of animal neuroendocrine systems.Platynereis | proenkephalin | Petromyzon N europeptides are diverse neuron-secreted peptides with neuromodulatory, neurotransmitter, or hormonal functions. Most neuropeptides signal via G protein-coupled receptors (GPCRs) (1), with a few exceptions (2-8). As modulators of neuronal activity, neuropeptides contribute to the generation of different outputs from the same neuronal circuit in a context-dependent manner (9), or orchestrate complex motor programs (10). Many neuropeptides act as hormones and are released into the haemolymph by neurohemal organs, such as the vertebrate pituitary gland, or the insect corpora cardiaca (11). These peptide hormones regulate various aspects of physiology, including growth, metabolism, and reproduction. Active neuropeptides are generated from an inactive proneuropeptide (pNP) that contains a single or multiple copies of active peptides. Active peptides are commonly short, with only a few families adopting well-defined, but unrelated, folds (e.g., prolactin and glycoprotein hormones). pNPs have a signal peptide (SP) and enter the secretory apparatus where dedicated proteases cleave them at mono...

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“…In this respect, hugin may be part of a neuronal circuit involved not only in making a decision between feeding and not feeding, but also in making perhaps an even tougher decision: between feeding and mating. Chemically identified peptides [14][15][16][26][27][28] are boxed in red, the PRXa C-termini are boxed in blue. Peptide designations (see Roman numbers) refer to common peptide designations from M. sexta, H. zea, and D. melanogaster.…”

Section: Functional Implicationsmentioning

confidence: 99%