Comparison of Caenorhabditis elegans NLP peptides with arthropod neuropeptides

Husson, Steven; Lindemans, Marleen; Janssen, Tom; Schoofs, Liliane

doi:10.1016/j.pt.2008.12.009

Cited by 17 publications

(8 citation statements)

References 71 publications

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“…The beetle Tribolium castaneum is the exception as it lacks both AST-A and the receptors [ 51 – 53 ]. In contrast, in the nematode, Caenorhabditis elegans , an orthologue of the insect AST-ARs was characterised ( npr-9 ) [ 39 ], and two putative AST-A peptide encoding genes ( nlp-5 and nlp-6 ) were also identified [ 41 , 54 , 55 ]. All the studies of AST-A to date suggest that its role in feeding behaviour emerged early during its evolution and have probably been maintained during the Ecdysozoa radiation [ 14 , 22 , 25 ].…”

Section: Introductionmentioning

confidence: 99%

Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes

et al. 2015

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Allatostatin type A receptors (AST-ARs) are a group of G-protein coupled receptors activated by members of the FGL-amide (AST-A) peptide family that inhibit food intake and development in arthropods. Despite their physiological importance the evolution of the AST-A system is poorly described and relatively few receptors have been isolated and functionally characterised in insects. The present study provides a comprehensive analysis of the origin and comparative evolution of the AST-A system. To determine how evolution and feeding modified the function of AST-AR the duplicate receptors in Anopheles mosquitoes, were characterised. Phylogeny and gene synteny suggested that invertebrate AST-A receptors and peptide genes shared a common evolutionary origin with KISS/GAL receptors and ligands. AST-ARs and KISSR emerged from a common gene ancestor after the divergence of GALRs in the bilaterian genome. In arthropods, the AST-A system evolved through lineage-specific events and the maintenance of two receptors in the flies and mosquitoes (Diptera) was the result of a gene duplication event. Speciation of Anopheles mosquitoes affected receptor gene organisation and characterisation of AST-AR duplicates (GPRALS1 and 2) revealed that in common with other insects, the mosquito receptors were activated by insect AST-A peptides and the iCa2+-signalling pathway was stimulated. GPRALS1 and 2 were expressed mainly in mosquito midgut and ovaries and transcript abundance of both receptors was modified by feeding. A blood meal strongly up-regulated expression of both GPRALS in the midgut (p < 0.05) compared to glucose fed females. Based on the results we hypothesise that the AST-A system in insects shared a common origin with the vertebrate KISS system and may also share a common function as an integrator of metabolism and reproduction. Highlights: AST-A and KISS/GAL receptors and ligands shared common ancestry prior to the protostome-deuterostome divergence. Phylogeny and gene synteny revealed that AST-AR and KISSR emerged after GALR gene divergence. AST-AR genes were present in the hemichordates but were lost from the chordates. In protostomes, AST-ARs persisted and evolved through lineage-specific events and duplicated in the arthropod radiation. Diptera acquired and maintained functionally divergent duplicate AST-AR genes.

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Section: Introductionmentioning

confidence: 99%

Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes

et al. 2015

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“…Neuropeptides and their receptors offer promising candidates for the regulation of various behaviors and changes in physiology. The Caenorhabditis elegans genome sequence has allowed the identification of 109 putative neuropeptide genes encoding precursors that may be processed to Ϸ250 neuropeptides (1)(2)(3). These neuropeptides are grouped into three families: FMRFamide-related peptides (f lp), insulin-like peptides (ins), and neuropeptide-like-peptides (nlps).…”

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confidence: 99%

A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues

Bendena

Boudreau

Papanicolaou

et al. 2008

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

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Movement inCaenorhabditis elegans is the result of sensory cues creating stimulatory and inhibitory output from sensory neurons. Four interneurons (AIA, AIB, AIY, and AIZ) are the primary recipients of this information that is further processed en route to motor neurons and muscle contraction. C. elegans has >1,000 G proteincoupled receptors (GPCRs), and their contribution to sensory-based movement is largely undefined. We show that an allatostatin/ galanin-like GPCR (NPR-9) is found exclusively in the paired AIB interneuron. AIB interneurons are associated with local search/ pivoting behavior. npr-9 mutants display an increased local search/ pivoting that impairs their ability to roam and travel long distances on food. With impaired roaming behavior on food npr-9 mutants accumulate more intestinal fat as compared with wild type. Overexpression of NPR-9 resulted in a gain-of-function phenotype that exhibits enhanced forward movement with lost pivoting behavior off food. As such the animal travels a great distance off food, creating arcs to return to food. These findings indicate that NPR-9 has inhibitory effects on the AIB interneuron to regulate foraging behavior, which, in turn, may affect metabolic rate and lipid storage.neuropeptide receptor ͉ nerve transmission ͉ foraging ͉ glutamate receptor ͉ interneuron A major challenge in neurobiology is to understand the control of behavior at the molecular level. Neuropeptides and their receptors offer promising candidates for the regulation of various behaviors and changes in physiology. The Caenorhabditis elegans genome sequence has allowed the identification of 109 putative neuropeptide genes encoding precursors that may be processed to Ϸ250 neuropeptides (1-3). These neuropeptides are grouped into three families: FMRFamide-related peptides (f lp), insulin-like peptides (ins), and neuropeptide-like-peptides (nlps). C. elegans expresses Ͼ1,000 orphan G protein-coupled receptors (GPCRs). More than 50 GPCRs resemble known receptors for known neuropeptide families based on phylogenetic comparisons with known vertebrate GPCRs (4). Of these GPCRs, based on sequence identity, C. elegans gene ZK455.3 expresses an nlp receptor, NPR-9, that is most similar to insect allatostatin/ mammalian galanin receptors (5-8). Allatostatins are a family of neuropeptides that share a conserved C-terminal sequence -Tyr/PheXaaPheGlyLeu-NH 2 and are widespread throughout the invertebrate lineage (9, 10). In insects, allatostatins regulate numerous physiological functions, including inhibition of juvenile hormone biosynthesis (11, 12), inhibition of muscle contraction (13), myoendocrine regulation (14, 15), neuromodulation (16), and regulation of enzymatic activities (17) and ecdysis (18). Similarly, mammalian galanin modulates a wide variety of processes that range from neurotransmission, nociception, feeding and metabolism, energy and osmotic homeostasis and learning and memory (19). We report that NPR-9 is uniquely localized in interneuron AIB to negatively regulate a variety of inputs th...

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“…Compared with traditional histology-based approaches, these techniques enable enhanced specificity and sensitivity through the use of antibodiesfor example, for the detection of the specific psychostimulant neuropeptide cocaine-and amphetamine-regulated transcript peptide (CART) . Antibodies can theoretically also be raised against virtually any peptide; however, many invertebrate neuropeptide genes encode more than one biologically active peptide that show high structural similarity to each other, leading to antibody cross-reactivity (Husson et al, 2009;McVeigh et al, 2009;Rowe and Elphick, 2012). Generation of N-terminally directed antisera, which can readily distinguish between peptides with highly similar C-terminal motifs, can help overcome cross reactivity issues (Atkinson et al, 2016).…”

Section: Methods For Neuropeptide Localizationmentioning

confidence: 99%

“…Infrared (IR) spectroscopy has successfully been used to provide a quantitative estimate of secondary structural elements. When analyzed by IR spectroscopy, peptides demonstrate characteristic peaks for different folding patterns, including α-helices, β-sheets and turns, as has been characterized in human Peptide YY neuropeptide Secher et al, 2016;Gade et al, 2016;Glover et al, 2015 In silico prediction Predicts sequences and structure from precursor protein and gene sequences Christie, 2014;Wong et al, 2016;Bigot et al, 2014 NMR Gives information into conformations and folding patterns Robinson et al, 2016;Xie et al, 2015;Kaiser et al, 2015 Spectroscopy Uses characteristic peaks to identify folding patterns Hegefeld et al, 2011;Schneider et al, 2016 X-ray crystallography Characterizes key structural sites with high spatial resolution Hassler et al, 2014;Yin et al, 2014 Localization Immuno assays Enables localization for virtually any peptide using antibodies Singh et al, 2016;Husson et al, 2009;Rowe and Elphick, 2012 In situ hybridization Target-specific expression mapping of neuropeptideencoding genes Levsky and Singer, 2003;Qian and Lloyd, 2003;Atkinson et al, 2016 Promotor::reporter Each technique described has the potential to provide deep insight into neuropeptide biology, and often provide complementary information to other techniques. Several key references are indicated for each that demonstrate current trends in the field.…”

Section: Western Blottingmentioning

confidence: 99%

New techniques, applications and perspectives in neuropeptide research

DeLaney

Buchberger

Atkinson

et al. 2018

Journal of Experimental Biology

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Neuropeptides are one of the most diverse classes of signaling molecules and have attracted great interest over the years owing to their roles in regulation of a wide range of physiological processes. However, there are unique challenges associated with neuropeptide studies stemming from the highly variable molecular sizes of the peptides, low concentrations, high degree of structural diversity and large number of isoforms. As a result, much effort has been focused on developing new techniques for studying neuropeptides, as well as novel applications directed towards learning more about these endogenous peptides. The areas of importance for neuropeptide studies include structure, localization within tissues, interaction with their receptors, including ion channels, and physiological function. Here, we discuss these aspects and the associated techniques, focusing on technologies that have demonstrated potential in advancing the field in recent years. Most identification and structural information has been gained by mass spectrometry, either alone or with confirmations from other techniques, such as nuclear magnetic resonance spectroscopy and other spectroscopic tools. While mass spectrometry and bioinformatic tools have proven to be the most powerful for large-scale analyses, they still rely heavily on complementary methods for confirmation. Localization within tissues, for example, can be probed by mass spectrometry imaging, immunohistochemistry and radioimmunoassays. Functional information has been gained primarily from behavioral studies coupled with tissue-specific assays, electrophysiology, mass spectrometry and optogenetic tools. Concerning the receptors for neuropeptides, the discovery of ion channels that are directly gated by neuropeptides opens up the possibility of developing a new generation of tools for neuroscience, which could be used to monitor neuropeptide release or to specifically change the membrane potential of neurons. It is expected that future neuropeptide research will involve the integration of complementary bioanalytical technologies and functional assays.

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Comparison of Caenorhabditis elegans NLP peptides with arthropod neuropeptides

Cited by 17 publications

References 71 publications

Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes

Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes

A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues

New techniques, applications and perspectives in neuropeptide research

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