Conservation of the function counts: homologous neurons express sequence‐related neuropeptides that originate from different genes

Neupert, Susanne; Huetteroth, Wolf; Schachtner, Joachim; Predel, Reinhard

doi:10.1111/j.1471-4159.2009.06361.x

Cited by 19 publications

(10 citation statements)

References 34 publications

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“…Possibly within the Pancrustacea lineage, a gene duplication of this predecessor occurred which, in turn, might have a common ancestor with neuromedin U of vertebrates [20]. In insects, the pk gene is known by different names (e. g. pban of Lepidoptera, hugin of Drosophila ) but is always expressed in neurosecretory neurons of the SEG [5], [21]–[25] which is different from the major expression site of the capa gene. CAPA-PVKs and CAPA-PK (C-terminal WFGPRLamide) both have specific receptors [26], [27].…”

Section: Discussionmentioning

confidence: 99%

Identification and Expression of Capa Gene in the Fire Ant, Solenopsis invicta

et al. 2014

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Recent genome analyses suggested the absence of a number of neuropeptide genes in ants. One of the apparently missing genes was the capa gene. Capa gene expression in insects is typically associated with the neuroendocrine system of abdominal ganglia; mature CAPA peptides are known to regulate diuresis and visceral muscle contraction. The apparent absence of the capa gene raised questions about possible compensation of these functions. In this study, we re-examined this controversial issue and searched for a potentially unrecognized capa gene in the fire ant, Solenopsis invicta. We employed a combination of data mining and a traditional PCR-based strategy using degenerate primers designed from conserved amino acid sequences of insect capa genes. Our findings demonstrate that ants possess and express a capa gene. As shown by MALDI-TOF mass spectrometry, processed products of the S. invicta capa gene include three CAPA periviscerokinins and low amounts of a pyrokinin which does not have the C-terminal WFGPRLa motif typical of CAPA pyrokinins in other insects. The capa gene was found with two alternative transcripts in the CNS. Within the ventral nerve cord, two capa neurons were immunostained in abdominal neuromeres 2–5, respectively, and projected into ventrally located abdominal perisympathetic organs (PSOs), which are the major hormone release sites of abdominal ganglia. The ventral location of these PSOs is a characteristic feature and was also found in another ant, Atta sexdens.

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Section: Discussionmentioning

confidence: 99%

Identification and Expression of Capa Gene in the Fire Ant, Solenopsis invicta

et al. 2014

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“…Most reports about SCMS in insects focused on neurosecretory neurons producing peptide hormones (e.g., refs ,,− ). Such cells are regulated by the transcription factors dimmed and crytocephal which results in a large number of peptide-containing dense core vesicles and, hence, also a high concentration of neuropeptides in the somata.…”

Section: Results and Discussionmentioning

confidence: 99%

Analysis of Single Neurons by Perforated Patch Clamp Recordings and MALDI-TOF Mass Spectrometry

Neupert

Fusca

Kloppenburg

et al. 2018

ACS Chem. Neurosci.

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Single-cell mass spectrometry has become an established technique to study specific molecular properties such as the neuropeptide complement of identified neurons. Here, we describe a strategy to characterize, by MALDI-TOF mass spectrometry, neurochemical composition of neurons that were identified by their electrophysiological and neuroanatomical characteristics. The workflow for the first time combined perforated patch clamp recordings with dye loading by electroporation for electrophysiological and neuroanatomical characterization as well as chemical profiling of somata by MALDI-TOF mass spectrometry with subsequent immunohistochemistry. To develop our protocol, we used identified central olfactory neurons from the American cockroach Periplaneta americana. First, the combined approach was optimized using a relative homogeneous, well-characterized neuron population of uniglomerular projection neurons, which show acetylcholine esterase immunoreactivity. The general applicability of this approach was verified on local interneurons, which are a diverse neuron population expressing highly differentiated neuropeptidomes. Thus, this study shows that the newly established protocol is suitable to comprehensively analyze electrophysiological, neuroanatomical, and molecular properties of single neurons. We consider this approach an important step to foster single-cell analysis in a wide variety of neuron types.

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“…Sample preparation and immunostaining were performed as described in Neupert et al (2009). As the primary antiserum, we used a polyclonal anti-CAPA-PVK serum raised against Periplaneta americana periviscerokinin-2 in rabbit at a concentration of 1:4000 (kindly provided by Dr M. Eckert, Jena).…”

Section: Immunohistochemistrymentioning

confidence: 99%

Peptidomics-Based Phylogeny and Biogeography of Mantophasmatodea (Hexapoda)

et al. 2012

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The insect order Mantophasmatodea was described in 2002. Prior to that time, several generations of entomologists had assumed that all major insect taxa were known; thus, its description was a sensation for zoologists. Since then, a surprising abundance and species diversity of this taxon have been found, particularly in the winter rainfall region of South Africa. To learn more about the evolutionary lineages, speciation, and biogeography of Mantophasmatodea, we applied an unusual peptidomics approach. We collected specimens of almost all known and novel taxa of these insects, developed methods for immediate sample preparation in the field, introduced peptide mass fingerprints for the unambiguous identification of taxa, and subsequently analyzed the most extensive data set on peptide hormones ever compiled for insect taxa. To account for intraspecific variation, we analyzed several individuals per putative species. Increased taxon sampling was preferred over a further increase in the number of characters to optimize the accuracy of phylogenetic analyses. The large data set made it possible to test the validity of using neuropeptide sequences, which coevolve with their respective receptors, to analyze phylogenetic relationships among closely related taxa. Altogether, the data from 71 populations of Mantophasmatodea were sufficient to clearly separate the major clades of Mantophasmatodea, including previously undescribed taxa such as Pachyphasma, Striatophasma, and Austrophasmatidae gen. et sp. nov. "RV." The data confirm the monophyly of Austrophasmatidae and show a relatively recent and extensive radiation in the winter rainfall region of South Africa but also suggest that the species-level diversification of Namibian Mantophasma is less marked than previously thought. We discuss the biogeographical and ecological factors that may have resulted in different regional patterns of endemism and species diversity in Mantophasmatodea. The unique development of the neuroendocrine capa-neurons in the ventral nervous system is described as synapomorphy of Mantophasmatodea + Grylloblattodea and is a further argument for a close relationship between these insect taxa.

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Conservation of the function counts: homologous neurons express sequence‐related neuropeptides that originate from different genes

Cited by 19 publications

References 34 publications

Identification and Expression of Capa Gene in the Fire Ant, Solenopsis invicta

Identification and Expression of Capa Gene in the Fire Ant, Solenopsis invicta

Analysis of Single Neurons by Perforated Patch Clamp Recordings and MALDI-TOF Mass Spectrometry

Peptidomics-Based Phylogeny and Biogeography of Mantophasmatodea (Hexapoda)

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