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Mass spectrometry-driven discovery of neuropeptides mediating nictation behavior of nematodes

ABSTRACT: Very little is known about the genetic modulation of nictation, a host-finding strategy used by infective juveniles of many pathogenic nematodes, as well as a phoretic strategy of Caenorhabditis elegans dauers. We here use a mass spectrometry-driven approach to find neuropeptides involved in the modulation of this behavior. We identified 126 neuropeptides in infective juveniles of the commercially relevant entomopathogenic nematode Steinernema carpocapsae, 75 of which have orthologs in the model organism C. elegans. To prioritize candidates for causality testing in light of the stage-restricted nictation behavior, we developed quantitative peptidomic assays and carried out targeted proteomic measurements that allows comparing neuropeptide levels at different C. elegans life stages. Our results show that virtually all 164 quantified neuropeptides are more abundant in dauers compared to L3 juveniles. Even so, not all are relevant to nictation, and we identify the neuropeptide genes flp-7 and flp-11 as novel regulators of nictation.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Steinernema Carpocapsae

TISSUE(S): Whole Body

SUBMITTER: Sven Van Bael

LAB HEAD: Liesbet Temmerman

PROVIDER: PXD034629 | Pride | 2022-12-08

REPOSITORIES: Pride

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			Action	DRS
	SC_13.mgf	Mgf
	SC_13.raw	Raw
	SC_13_peptides_1_1_0.mzid.gz	Mzid
	SC_2.mgf	Mgf
	SC_2.raw	Raw

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Global analysis of neuropeptides in cestodes identifies Attachin, a SIFamide homolog, as a stimulant of parasite motility and attachment

Project description:Many anthelmintics target the neuromuscular system, in particular by interfering with signalling mediated by classical neurotransmitters. Although peptidergic signalling has been proposed as a target of novel anthelmintics, current knowledge of the neuropeptide complement of many helminths is still limited, especially for parasitic flatworms (cestodes, trematodes and monogeneans). In this work, we have characterised the neuropeptide complement of the model cestode Hymenolepis microstoma. Peptidomic characterization of adults of H. microstoma validated many of the neuropeptide precursor (npp) genes previously predicted in silico, and identified novel neuropeptides that are conserved in parasitic flatworms. Most neuropeptides from parasitic flatworms lack significant similarity to those from other animals, confirming the uniqueness of their peptidergic signalling. Analysis of gene expression of ten npp genes by in situ hybridization confirmed that all of them are expressed in the nervous system and identified cryptic features, including the first evidence of dorsoventral asymmetry, as well as a new population of peripheral neurosecretory cells that appears to be conserved in the trematode Schistosoma mansoni. Finally, we characterised in greater detail Attachin, an experimentally validated SIFamide homolog. Although its expression is largely restricted to the longitudinal nerve cords and cerebral commissure in H. microstoma, it shows widespread expression in the larval nervous system of Echinococcus multilocularis and Mesocestoides corti. Exogenous addition of a peptide corresponding to the highly conserved C-terminus of Attachin stimulated motility and attachment of M. corti larvae. Altogether, this work provides a robust experimental foothold for the characterization of peptidergic signalling in parasitic flatworms.

2022-06-13 | PXD033611 | Pride

Mass spectrometric evidence for neuropeptide-amidating enzymes in C. elegans

Project description:Neuropeptides constitute a vast and functionally diverse family of neurochemical signaling molecules, and are widely involved in the regulation of various physiological processes. The nematode C. elegans is well-suited for the study of neuropeptide biochemistry and function, as neuropeptide biosynthesis enzymes are not essential for C. elegans viability. This permits the study of neuropeptide biosynthesis in mutants lacking certain neuropeptide-processing enzymes. Mass spectrometry has been used to study the effects of proprotein convertase and carboxypeptidase mutations on proteolytic processing of neuropeptide precursors and on the peptidome in C. elegans. However, the enzymes required for the last step in the production of many bioactive peptides – the carboxyterminal amidation reaction – have not been characterized in this manner. Here, we describe three genes that encode homologs of neuropeptide amidation enzymes in C. elegans and used tandem LC-MS to compare neuropeptides in wild-type animals with those in newly generated mutants for these putative amidation enzymes. We report that mutants lacking both a functional peptidylglycine α-hydroxylating monooxygenase (PHM) and a peptidylglycine α-amidating monooxygenase (PAM) had a severely altered neuropeptide profile and also a decreased number of offspring. Interestingly, single mutants of the amidation enzymes still expressed some fully processed amidated neuropeptides, indicating the existence of a redundant amidation mechanism in C. elegans. In summary, the key steps in neuropeptide-processing in C. elegans seem to be executed by redundant enzymes, and loss of these enzymes severely affects brood size, supporting the need of amidated peptides for C. elegans reproduction.

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Neuropeptidomic Analysis of the Stick Insect, <i> Carausius morosus </i>

Project description:One of the most thoroughly studied insect species, with respect to locomotion behaviour, is the stick insect Carausius morosus. Although detailed information exists on premotor networks controlling walking, surprisingly little is known about neuropeptides, which are certainly involved in motor activity generation and modulation. So far, only few neuropeptides were identified from C. morosus or related stick insects. We performed a transcriptome analysis of the central nervous system to assemble and identify 65 neuropeptide and protein hormone precursors of C. morosus, including five novel putative neuropeptide precursors without clear homology to known neuropeptide precursors of other insects (Carausius neuropeptide-like precursor 1, HanSolin, PK-like1, PK-like2, RFLamide). Using Q Exactive Orbitrap and MALDI-TOF mass spectrometry, 277 peptides including 153 likely bioactive mature neuropeptides were confirmed. Peptidomics yielded a complete coverage for many of the neuropeptide propeptides and confirmed a surprisingly high number of heterozygous sequences. Few neuropeptide precursors commonly occurring in insects, including those of insect kinins and sulfakinins, could neither be found in the transcriptome data nor did peptidomics support their presence. The results of our study represent one of the most comprehensive peptidomic analyses on insects and provide the necessary input for subsequent experiments revealing neuropeptide function in greater detail.

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Genomics- and Peptidomics-Based Discovery of Conserved and Novel Neuropeptides in the American Cockroach

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Transcriptome analysis of N2 and flp-6 Caenorhabditis elegans at 25 °C

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Neuropeptide inactivation regulates egg-laying behavior to influence reproductive health in Caenorhabditis elegans

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