Publications by authors named "Joachim Schachtner"

50 Publications

Metamorphic development of the olfactory system in the red flour beetle (Tribolium castaneum, HERBST).

BMC Biol 2021 07 30;19(1):155. Epub 2021 Jul 30.

Department of Biology, Animal Physiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, 35032, Marburg, Germany.

Background: Insects depend on their olfactory sense as a vital system. Olfactory cues are processed by a rather complex system and translated into various types of behavior. In holometabolous insects like the red flour beetle Tribolium castaneum, the nervous system typically undergoes considerable remodeling during metamorphosis. This process includes the integration of new neurons, as well as remodeling and elimination of larval neurons.

Results: We find that the sensory neurons of the larval antennae are reused in the adult antennae. Further, the larval antennal lobe gets transformed into its adult version. The beetle's larval antennal lobe is already glomerularly structured, but its glomeruli dissolve in the last larval stage. However, the axons of the olfactory sensory neurons remain within the antennal lobe volume. The glomeruli of the adult antennal lobe then form from mid-metamorphosis independently of the presence of a functional OR/Orco complex but mature dependent on the latter during a postmetamorphic phase.

Conclusions: We provide insights into the metamorphic development of the red flour beetle's olfactory system and compared it to data on Drosophila melanogaster, Manduca sexta, and Apis mellifera. The comparison revealed that some aspects, such as the formation of the antennal lobe's adult glomeruli at mid-metamorphosis, are common, while others like the development of sensory appendages or the role of Orco seemingly differ.
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http://dx.doi.org/10.1186/s12915-021-01055-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8323255PMC
July 2021

Adult neurogenesis in the mushroom bodies of red flour beetles (Tribolium castaneum, HERBST) is influenced by the olfactory environment.

Sci Rep 2020 01 23;10(1):1090. Epub 2020 Jan 23.

Philipps-University Marburg, Department of Biology, Animal Physiology, Karl-von-Frisch-Str. 8, 35032, Marburg, Germany.

Several studies showed adult persisting neurogenesis in insects, including the red flour beetle Tribolium castaneum, while it is absent in honeybees, carpenter ants, and vinegar flies. In our study, we focus on cell proliferation in the adult mushroom bodies of T. castaneum. We reliably labelled the progenies of the adult persisting mushroom body neuroblasts and determined the proliferation rate under several olfactory conditions within the first week after adult eclosion. We found at least two phases of Kenyon cell proliferation in the early adult beetle. Our results suggest that the generation of Kenyon cells during the first three days after adult eclosion is mainly genetically predetermined and a continuation of the developmental processes (nature), whereas from day four on proliferation seems to be mainly dependent on the odour environment (nurture). Considering that the mushroom bodies are linked to learning and memory, neurogenesis in the mushroom bodies is part of the remodelling of neuronal circuits leading to the adaption to the environment and optimization of behaviour.
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http://dx.doi.org/10.1038/s41598-020-57639-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6978414PMC
January 2020

Functional characterization of mosquito short neuropeptide F receptors.

Peptides 2018 05 14;103:31-39. Epub 2018 Mar 14.

Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, Sundsvägen 14, 23053, Alnarp, Sweden. Electronic address:

Mosquito blood feeding transiently inhibits sugar- and host seeking through neuropeptide signaling. Short neuropeptide F (sNPF) is one of the neuromodulators involved in this regulation. Here, we identified the genes for the sNPF precursor and the sNPF receptor in the southern house mosquito, Culex quinquefasciatus. Comparative analyses are made with the genes of the sNPF precursor and receptor from two other important vectors, Aedes aegypti and Anopheles coluzzii. We functionally characterized the receptors in all three species using endogenous neuropeptides, and quantified their transcript expression following a blood meal and a sugar meal. Our analysis reveals several Cx. quinquefasciatus-specific duplications of the sNPF-3 isoform on the sNPF precursor, which are not reflected in the precursors of the other two species. In contrast, the structure of the sNPF receptors is highly conserved within mosquitoes, and a putative ligand binding region is proposed and discussed. Reflecting the high structural conservation, the sNPF receptor sensitivity to endogenous sNPF isoforms is conserved across mosquito species. Using quantitative real time PCR, we demonstrate that transcript abundance of the sNPF receptor and precursor is regulated following feeding, only in Cx. quinquefasciatus. We discuss our findings in relation to previous work on sNPF signaling and its role in feeding regulation.
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http://dx.doi.org/10.1016/j.peptides.2018.03.009DOI Listing
May 2018

Mating-Induced Differential Peptidomics of Neuropeptides and Protein Hormones in Agrotis ipsilon Moths.

J Proteome Res 2018 04 28;17(4):1397-1414. Epub 2018 Feb 28.

Institut de Génétique, Environnement et Protection des Plantes (UMR IGEPP) , INRA , Agrocampus Ouest, rue Le Nôtre , 49054 Angers cedex 01 , France.

In many insects, mating induces drastic changes in male and female responses to sex pheromones or host-plant odors. In the male moth Agrotis ipsilon, mating induces a transient inhibition of behavioral and neuronal responses to the female sex pheromone. As neuropeptides and peptide hormones regulate most behavioral processes, we hypothesize that they could be involved in this mating-dependent olfactory plasticity. Here we used next-generation RNA sequencing and a combination of liquid chromatography, matrix assisted laser desorption ionization time-of-flight (MALDI-TOF) mass spectrometry, and direct tissue profiling to analyze the transcriptome and peptidome of different brain compartments in virgin and mated males and females of A. ipsilon. We identified 37 transcripts encoding putative neuropeptide precursors and 54 putative bioactive neuropeptides from 23 neuropeptide precursors (70 sequences in total, 25 neuropeptide precursors) in different areas of the central nervous system including the antennal lobes, the gnathal ganglion, and the corpora cardiaca-corpora allata complex. Comparisons between virgin and mated males and females revealed tissue-specific differences in peptide composition between sexes and according to physiological state. Mated males showed postmating differences in neuropeptide occurrence, which could participate in the mating-induced olfactory plasticity.
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http://dx.doi.org/10.1021/acs.jproteome.7b00779DOI Listing
April 2018

Feeding-induced changes in allatostatin-A and short neuropeptide F in the antennal lobes affect odor-mediated host seeking in the yellow fever mosquito, Aedes aegypti.

PLoS One 2017 22;12(11):e0188243. Epub 2017 Nov 22.

Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden.

Aedes aegypti is a model species in which the endogenous regulation of odor-mediated host seeking behavior has received some attention. Sugar feeding and host seeking in female A. aegypti are transiently inhibited following a blood meal. This inhibition is partially mediated by short neuropeptide F (sNPF). The paired antennal lobes (ALs), as the first processing centers for olfactory information, has been shown to play a significant role in the neuropeptidergic regulation of odor-mediated behaviors in insects. The expression of sNPF, along with other peptides in the ALs of A. aegypti, indicate parallel neuromodulatory systems that may affect olfactory processing. To identify neuropeptides involved in regulating the odor-mediated host seeking behavior in A. aegypti, we use a semi-quantitative neuropeptidomic analysis of single ALs to analyze changes in the levels of five individual neuropeptides in response to different feeding regimes. Our results show that the level of sNPF-2, allatostatin-A-5 (AstA-5) and neuropeptide-like precursor-1-5 (NPLP-1-5), but not of tachykinin-related-peptides and SIFamide (SIFa), in the AL of female mosquitoes, changes 24 h and 48 h post-blood meal, and are dependent on prior access to sugar. To assess the role of these neuropeptides in modulating host seeking behavior, when systemically injected individually, sNPF-2 and AstA-5 significantly reduced host seeking behavior. However, only the injection of the binary mixture of the two neuropeptides lead to a host seeking inhibition similar to that observed in blood fed females. We conclude that modulation of the odor mediated host seeking behavior of A. aegypti is likely regulated by a dual neuropeptidergic pathway acting in concert in the ALs.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0188243PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5699834PMC
December 2017

Functional characterization of the dual allatostatin-A receptors in mosquitoes.

Peptides 2018 01 16;99:44-55. Epub 2017 Nov 16.

Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, Sundsvägen 14, 230 53 Alnarp, Sweden. Electronic address:

The neuropeptide allatostatin-A (AstA) and its cognate receptors (AstARs) are involved in the modulation of feeding behavior, which in hematophagous insects includes the regulation of the disease vector-related behaviors, host seeking and blood feeding. In mosquitoes and other dipterans, there are two copies of AstAR, contrasting with the single copy found in other insects. In this study, we identified and cloned the dual AstAR system of two important disease vectors Aedes aegypti and Culex quinquefasciatus, and compared them with those previously described, including those in Anopheles coluzzii and Drosophila melanogaster. Phylogenetic analysis of the AstARs revealed that the mosquito AstAR1s has retained a similar amino acid sequence as the AstARs from non-dipteran insect species. Intron analysis revealed that the number of introns accumulated in the AstAR2s is similar to that in other insects, and that introns are conserved within the receptor types, but that only the final two introns are conserved across AstAR1s and 2s. We functionally characterized the dual AstARs in An. coluzzii, Ae. aegypti and Cx. quinquefasciatus by stably expressing the receptors in a Chinese hamster oocyte cell line (CHO) also stably expressing a promiscuous G-protein (G16), and challenged them with the endogenous isoforms of AstA from the three mosquito species. In the culicine mosquitoes, Ae. aegypti and Cx. quinquefasciatus, the AstARs demonstrated differential sensitivity to AstA, with the AstAR2s displaying a higher sensitivity than the AstAR1s, suggesting a divergence of functional roles for these AstARs. In contrast, both An. coluzzii AstARs demonstrated a similar sensitivity to the AstA ligands. We discuss our findings in the light of AstA acting as a regulator of blood feeding in mosquitoes. A better understanding of the regulation of host seeking and blood feeding in vector mosquitoes will lead to the rational development of novel approaches for vector control.
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http://dx.doi.org/10.1016/j.peptides.2017.10.016DOI Listing
January 2018

Distribution of tachykinin-related peptides in the brain of the tobacco budworm Heliothis virescens.

J Comp Neurol 2017 Dec 15;525(18):3918-3934. Epub 2017 Sep 15.

Department of Biology, Animal Physiology, Philipps University, Marburg, 35032, Germany.

Invertebrate tachykinin-related peptides (TKRPs) comprise a group of signaling molecules having sequence similarities to mammalian tachykinins. A growing body of evidence has demonstrated the presence of TKRPs in the central nervous system of insects. In this investigation, we used an antiserum against locustatachykinin-II to reveal the distribution pattern of these peptides in the brain of the moth Heliothis virescens. Immunolabeling was found throughout the brain of the heliothine moth. Most of the roughly 500 locustatachykinin-II immunoreactive cell bodies, that is, ca. 400, were located in the protocerebrum, whereas the rest was distributed in the deutocerebrum, tritocerebrum, and the gnathal ganglion. Abundant immunoreactive processes were located in the same regions. Labeled processes in the protocerebrum were especially localized in optic lobe, central body, lateral accessory lobe, superior protocerebrum, and lateral protocerebrum, while those in the deutocerebrum were present exclusively in the antennal lobe. In addition to brain interneurons, four pairs of median neurosecretory cells in the pars intercerebralis with terminal processes in the corpora cardiaca and aorta wall were immunostained. No sexual dimorphism in immunoreactivity was found. Comparing the data obtained here with findings from other insect species reveals considerable differences, suggesting species-specific roles of tachykinin-related peptides in insects.
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http://dx.doi.org/10.1002/cne.24310DOI Listing
December 2017

Variations on a Theme: Antennal Lobe Architecture across Coleoptera.

PLoS One 2016 14;11(12):e0166253. Epub 2016 Dec 14.

Department of Biology-Animal Physiology, Philipps-University Marburg, Marburg, Germany.

Beetles comprise about 400,000 described species, nearly one third of all known animal species. The enormous success of the order Coleoptera is reflected by a rich diversity of lifestyles, behaviors, morphological, and physiological adaptions. All these evolutionary adaptions that have been driven by a variety of parameters over the last about 300 million years, make the Coleoptera an ideal field to study the evolution of the brain on the interface between the basic bauplan of the insect brain and the adaptions that occurred. In the current study we concentrated on the paired antennal lobes (AL), the part of the brain that is typically responsible for the first processing of olfactory information collected from olfactory sensilla on antenna and mouthparts. We analyzed 63 beetle species from 22 different families and thus provide an extensive comparison of principal neuroarchitecture of the AL. On the examined anatomical level, we found a broad diversity including AL containing a wide range of glomeruli numbers reaching from 50 to 150 glomeruli and several species with numerous small glomeruli, resembling the microglomerular design described in acridid grasshoppers and diving beetles, and substructures within the glomeruli that have to date only been described for the small hive beetle, Aethina tumida. A first comparison of the various anatomical features of the AL with available descriptions of lifestyle and behaviors did so far not reveal useful correlations. In summary, the current study provides a solid basis for further studies to unravel mechanisms that are basic to evolutionary adaptions of the insect olfactory system.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0166253PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5156346PMC
July 2017

Morphological and Transcriptomic Analysis of a Beetle Chemosensory System Reveals a Gnathal Olfactory Center.

BMC Biol 2016 10 17;14(1):90. Epub 2016 Oct 17.

Department of Developmental Biology, Göttingen Center for Molecular Biosciences (GZMB), Georg-August-University Goettingen, Johann-Friedrich-Blumenbach-Institute of Zoology and Anthropology, Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Göttingen, Germany.

Background: The red flour beetle Tribolium castaneum is an emerging insect model organism representing the largest insect order, Coleoptera, which encompasses several serious agricultural and forest pests. Despite the ecological and economic importance of beetles, most insect olfaction studies have so far focused on dipteran, lepidopteran, or hymenopteran systems.

Results: Here, we present the first detailed morphological description of a coleopteran olfactory pathway in combination with genome-wide expression analysis of the relevant gene families involved in chemoreception. Our study revealed that besides the antennae, also the mouthparts are highly involved in olfaction and that their respective contribution is processed separately. In this beetle, olfactory sensory neurons from the mouthparts project to the lobus glomerulatus, a structure so far only characterized in hemimetabolous insects, as well as to a so far non-described unpaired glomerularly organized olfactory neuropil in the gnathal ganglion, which we term the gnathal olfactory center. The high number of functional odorant receptor genes expressed in the mouthparts also supports the importance of the maxillary and labial palps in olfaction of this beetle. Moreover, gustatory perception seems equally distributed between antenna and mouthparts, since the number of expressed gustatory receptors is similar for both organs.

Conclusions: Our analysis of the T. castaneum chemosensory system confirms that olfactory and gustatory perception are not organotopically separated to the antennae and mouthparts, respectively. The identification of additional olfactory processing centers, the lobus glomerulatus and the gnathal olfactory center, is in contrast to the current picture that in holometabolous insects all olfactory inputs allegedly converge in the antennal lobe. These findings indicate that Holometabola have evolved a wider variety of solutions to chemoreception than previously assumed.
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http://dx.doi.org/10.1186/s12915-016-0304-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5067906PMC
October 2016

The insect central complex as model for heterochronic brain development-background, concepts, and tools.

Dev Genes Evol 2016 06 7;226(3):209-19. Epub 2016 Apr 7.

Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach Institute, GZMB, CNMPB, Georg-August-University Göttingen, Göttingen Campus, Göttingen, Germany.

The adult insect brain is composed of neuropils present in most taxa. However, the relative size, shape, and developmental timing differ between species. This diversity of adult insect brain morphology has been extensively described while the genetic mechanisms of brain development are studied predominantly in Drosophila melanogaster. However, it has remained enigmatic what cellular and genetic mechanisms underlie the evolution of neuropil diversity or heterochronic development. In this perspective paper, we propose a novel approach to study these questions. We suggest using genome editing to mark homologous neural cells in the fly D. melanogaster, the beetle Tribolium castaneum, and the Mediterranean field cricket Gryllus bimaculatus to investigate developmental differences leading to brain diversification. One interesting aspect is the heterochrony observed in central complex development. Ancestrally, the central complex is formed during embryogenesis (as in Gryllus) but in Drosophila, it arises during late larval and metamorphic stages. In Tribolium, it forms partially during embryogenesis. Finally, we present tools for brain research in Tribolium including 3D reconstruction and immunohistochemistry data of first instar brains and the generation of transgenic brain imaging lines. Further, we characterize reporter lines labeling the mushroom bodies and reflecting the expression of the neuroblast marker gene Tc-asense, respectively.
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http://dx.doi.org/10.1007/s00427-016-0542-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4896989PMC
June 2016

Space Takes Time: Concentration Dependent Output Codes from Primary Olfactory Networks Rapidly Provide Additional Information at Defined Discrimination Thresholds.

Front Cell Neurosci 2015 14;9:515. Epub 2016 Jan 14.

Fachbereich Biologie, Philipps-Universität Marburg, Germany.

As odor concentration increases, primary olfactory network representations expand in spatial distribution, temporal complexity and duration. However, the direct relationship between concentration dependent odor representations and the psychophysical thresholds of detection and discrimination is poorly understood. This relationship is absolutely critical as thresholds signify transition points whereby representations become meaningful to the organism. Here, we matched stimulus protocols for psychophysical assays and intracellular recordings of antennal lobe (AL) projection neurons (PNs) in the moth Manduca sexta to directly compare psychophysical thresholds and the output representations they elicit. We first behaviorally identified odor detection and discrimination thresholds across an odor dilution series for a panel of structurally similar odors. We then characterized spatiotemporal spiking patterns across a population of individually filled and identified AL PNs in response to those odors at concentrations below, at, and above identified thresholds. Using spatial and spatiotemporal based analyses we observed that each stimulus produced unique representations, even at sub-threshold concentrations. Mean response latency did not decrease and the percent glomerular activation did not increase with concentration until undiluted odor. Furthermore, correlations between spatial patterns for odor decreased, but only significantly with undiluted odor. Using time-integrated Euclidean distance (ED) measures, we determined that added spatiotemporal information was present at the discrimination but not detection threshold. This added information was evidenced by an increase in integrated distance between the sub-detection and discrimination threshold concentrations (of the same odor) that was not present in comparison of the sub-detection and detection threshold. After consideration of delays for information to reach the AL we find that it takes ~120-140 ms for the AL to output identity information. Overall, these results demonstrate that as odor concentration increases, added information about odor identity is embedded in the spatiotemporal representation at the discrimination threshold.
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http://dx.doi.org/10.3389/fncel.2015.00515DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4712294PMC
February 2016

Novel antennal lobe substructures revealed in the small hive beetle Aethina tumida.

Cell Tissue Res 2016 Mar 24;363(3):679-92. Epub 2015 Oct 24.

Department of Biology, Animal Physiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, 35032, Marburg, Germany.

The small hive beetle, Aethina tumida, is an emerging pest of social bee colonies. A. tumida shows a specialized life style for which olfaction seems to play a crucial role. To better understand the olfactory system of the beetle, we used immunohistochemistry and 3-D reconstruction to analyze brain structures, especially the paired antennal lobes (AL), which represent the first integration centers for odor information in the insect brain. The basic neuroarchitecture of the A. tumida brain compares well to the typical beetle and insect brain. In comparison to other insects, the AL are relatively large in relationship to other brain areas, suggesting that olfaction is of major importance for the beetle. The AL of both sexes contain about 70 olfactory glomeruli with no obvious size differences of the glomeruli between sexes. Similar to all other insects including beetles, immunostaining with an antiserum against serotonin revealed a large cell that projects from one AL to the contralateral AL to densely innervate all glomeruli. Immunostaining with an antiserum against tachykinin-related peptides (TKRP) revealed hitherto unknown structures in the AL. Small TKRP-immunoreactive spherical substructures are in both sexes evenly distributed within all glomeruli. The source for these immunoreactive islets is very likely a group of about 80 local AL interneurons. We offer two hypotheses on the function of such structures.
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http://dx.doi.org/10.1007/s00441-015-2282-9DOI Listing
March 2016

Colocalization of allatotropin and tachykinin-related peptides with classical transmitters in physiologically distinct subtypes of olfactory local interneurons in the cockroach (Periplaneta americana).

J Comp Neurol 2015 Jul 2;523(10):1569-86. Epub 2015 Apr 2.

Biocenter, Institute for Zoology, and Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.

In the insect antennal lobe different types of local interneurons mediate complex excitatory and inhibitory interactions between the glomerular pathways to structure the spatiotemporal representation of odors. Mass spectrometric and immunohistochemical studies have shown that in local interneurons classical neurotransmitters are likely to colocalize with a variety of substances that can potentially act as cotransmitters or neuromodulators. In the antennal lobe of the cockroach Periplaneta americana, gamma-aminobutyric acid (GABA) has been identified as the potential inhibitory transmitter of spiking type I local interneurons, whereas acetylcholine is most likely the excitatory transmitter of nonspiking type IIa1 local interneurons. This study used whole-cell patch clamp recordings combined with single-cell labeling and immunohistochemistry to test if the GABAergic type I local interneurons and the cholinergic type IIa1 local interneurons express allatotropin and tachykinin-related neuropeptides (TKRPs). These are two of the most abundant types of peptides in the insect antennal lobe. GABA-like and choline acetyltransferase (ChAT)-like immunoreactivity were used as markers for GABAergic and cholinergic neurons, respectively. About 50% of the GABA-like immunoreactive (-lir) spiking type I local interneurons were allatotropin-lir, and ∼ 40% of these neurons were TKRP-lir. About 20% of nonspiking ChAT-lir type IIa1 local interneurons were TKRP-lir. Our results suggest that in subpopulations of GABAergic and cholinergic local interneurons, allatotropin and TKRPs might act as cotransmitters or neuromodulators. To unequivocally assign neurotransmitters, cotransmitters, and neuromodulators to identified classes of antennal lobe neurons is an important step to deepen our understanding of information processing in the insect olfactory system.
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http://dx.doi.org/10.1002/cne.23757DOI Listing
July 2015

Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions.

BMC Genomics 2014 Dec 18;15:1141. Epub 2014 Dec 18.

Department of Developmental Biology, Georg-August-University Goettingen, Johann-Friedrich-Blumenbach-Institute for Zoology and Anthropology, GZMB, Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, Goettingen 37077, Germany.

Background: Chemoreception is based on the senses of smell and taste that are crucial for animals to find new food sources, shelter, and mates. The initial step in olfaction involves the translocation of odorants from the periphery through the aqueous lymph of the olfactory sensilla to the odorant receptors most likely by chemosensory proteins (CSPs) or odorant binding proteins (OBPs).

Results: To better understand the roles of CSPs and OBPs in a coleopteran pest species, the red flour beetle Tribolium castaneum (Coleoptera, Tenebrionidae), we performed transcriptome analyses of male and female antennae, heads, mouthparts, legs, and bodies, which revealed that all 20 CSPs and 49 of the 50 previously annotated OBPs are transcribed. Only six of the 20 CSP are significantly transcriptionally enriched in the main chemosensory tissues (antenna and/or mouthparts), whereas of the OBPs all eight members of the antenna binding proteins II (ABPII) subgroup, 18 of the 20 classic OBP subgroup, the C + OBP, and only five of the 21 C-OBPs show increased chemosensory tissue expression. By MALDI-TOF-TOF MS protein fingerprinting, we confirmed three CSPs, four ABPIIs, three classic OBPs, and four C-OBPs in the antennae.

Conclusions: Most of the classic OBPs and all ABPIIs are likely involved in chemoreception. A few are also present in other tissues such as odoriferous glands and testes and may be involved in release or transfer of chemical signals. The majority of the CSPs as well as the C-OBPs are not enriched in antennae or mouthparts, suggesting a more general role in the transport of hydrophobic molecules.
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http://dx.doi.org/10.1186/1471-2164-15-1141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4377858PMC
December 2014

Neuropeptides in the antennal lobe of the yellow fever mosquito, Aedes aegypti.

J Comp Neurol 2014 Feb;522(3):592-608

Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, 230 53, Alnarp, Sweden.

For many insects, including mosquitoes, olfaction is the dominant modality regulating their behavioral repertoire. Many neurochemicals modulate olfactory information in the central nervous system, including the primary olfactory center of insects, the antennal lobe. The most diverse and versatile neurochemicals in the insect nervous system are found in the neuropeptides. In the present study, we analyzed neuropeptides in the antennal lobe of the yellow fever mosquito, Aedes aegypti, a major vector of arboviral diseases. Direct tissue profiling of the antennal lobe by matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) mass spectrometry indicated the presence of 28 mature products from 10 different neuropeptide genes. In addition, immunocytochemical techniques were used to describe the cellular location of the products of up to seven of these genes within the antennal lobe. Allatostatin A, allatotropin, SIFamide, FMRFamide-related peptides, short neuropeptide F, myoinhibitory peptide, and tachykinin-related peptides were found to be expressed in local interneurons and extrinsic neurons of the antennal lobe. Building on these results, we discuss the possible role of neuropeptide signaling in the antennal lobe of Ae. aegypti.
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http://dx.doi.org/10.1002/cne.23434DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4265797PMC
February 2014

Neuropeptidome of Tribolium castaneum antennal lobes and mushroom bodies.

J Comp Neurol 2014 Feb;522(2):337-57

Philipps-University Marburg, Department of Biology, Animal Physiology, 35043, Marburg, Germany.

Neuropeptides are a highly diverse group of signaling molecules that affect a broad range of biological processes in insects, including development, metabolism, behavior, and reproduction. In the central nervous system, neuropeptides are usually considered to act as neuromodulators and cotransmitters that modify the effect of "classical" transmitters at the synapse. The present study analyzes the neuropeptide repertoire of higher cerebral neuropils in the brain of the red flour beetle Tribolium castaneum. We focus on two integrative neuropils of the olfactory pathway, the antennal lobes and the mushroom bodies. Using the technique of direct peptide profiling by matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry, we demonstrate that these neuropils can be characterized by their specific neuropeptide expression profiles. Complementary immunohistological analyses of selected neuropeptides revealed neuropeptide distribution patterns within the antennal lobes and the mushroom bodies. Both approaches revealed consistent differences between the neuropils, underlining that direct peptide profiling by mass spectrometry is a fast and reliable method to identify neuropeptide content.
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http://dx.doi.org/10.1002/cne.23399DOI Listing
February 2014

Cockchafer larvae smell host root scents in soil.

PLoS One 2012 1;7(10):e45827. Epub 2012 Oct 1.

Forest Zoology and Forest Protection, Georg-August-Universität, Göttingen, Germany.

In many insect species olfaction is a key sensory modality. However, examination of the chemical ecology of insects has focussed up to now on insects living above ground. Evidence for behavioral responses to chemical cues in the soil other than CO(2) is scarce and the role played by olfaction in the process of finding host roots below ground is not yet understood. The question of whether soil-dwelling beetle larvae can smell their host plant roots has been under debate, but proof is as yet lacking that olfactory perception of volatile compounds released by damaged host plants, as is known for insects living above ground, occurs. Here we show that soil-dwelling larvae of Melolontha hippocastani are well equipped for olfactory perception and respond electrophysiologically and behaviorally to volatiles released by damaged host-plant roots. An olfactory apparatus consisting of pore plates at the antennae and about 70 glomeruli as primary olfactory processing units indicates a highly developed olfactory system. Damage induced host plant volatiles released by oak roots such as eucalyptol and anisol are detected by larval antennae down to 5 ppbv in soil air and elicit directed movement of the larvae in natural soil towards the odor source. Our results demonstrate that plant-root volatiles are likely to be perceived by the larval olfactory system and to guide soil-dwelling white grubs through the dark below ground to their host plants. Thus, to find below-ground host plants cockchafer larvae employ mechanisms that are similar to those employed by the adult beetles flying above ground, despite strikingly different physicochemical conditions in the soil.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0045827PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3462172PMC
February 2013

Neuropeptides in insect mushroom bodies.

Arthropod Struct Dev 2012 May 6;41(3):199-226. Epub 2012 Mar 6.

Philipps-University Marburg, Department of Biology, Animal Physiology, Marburg, Germany.

Owing to their experimental amenability, insect nervous systems continue to be in the foreground of investigations into information processing in - ostensibly - simple neuronal networks. Among the cerebral neuropil regions that hold a particular fascination for neurobiologists are the paired mushroom bodies, which, despite their function in other behavioral contexts, are most renowned for their role in learning and memory. The quest to understand the processes that underlie these capacities has been furthered by research focusing on unraveling neuroanatomical connections of the mushroom bodies and identifying key players that characterize the molecular machinery of mushroom body neurons. However, on a cellular level, communication between intrinsic and extrinsic mushroom body neurons still remains elusive. The present account aims to provide an overview on the repertoire of neuropeptides expressed in and utilized by mushroom body neurons. Existing data for a number of insect representatives is compiled and some open gaps in the record are filled by presenting additional original data.
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http://dx.doi.org/10.1016/j.asd.2012.02.005DOI Listing
May 2012

Seasonal leptin resistance is associated with impaired signalling via JAK2-STAT3 but not ERK, possibly mediated by reduced hypothalamic GRB2 protein.

J Comp Physiol B 2012 May 24;182(4):553-67. Epub 2011 Dec 24.

Department of Animal Physiology, Faculty of Biology, Philipps University Marburg, Marburg, Germany.

The Siberian hamster, Phodopus sungorus, undergoes a striking seasonal cycle of leptin sensitivity and body weight regulation, but the molecular mechanism and relevance to human leptin insensitivity are unknown. Here we show that nuclear translocation of phospho-STAT3 in the hypothalamus is rapidly stimulated by leptin to a greater extent in hamsters held in short-day length (SD) as compared to long-day length (LD). Intriguingly, effects of leptin on STAT3 appeared to be in part limited to nuclear translocation of phospho-STAT3 associated with the cell surface rather than phosphorylation of STAT3. The number of phospho-ERK cells within the hypothalamus was unaffected by either photoperiod or leptin. However, proximal to ERK phosphorylation, hypothalamic SH2-containing tyrosine phosphatase (SHP2) and the small growth factor receptor-binding protein (GRB2), which act as competitive negative modulators on binding of SOCS3 to leptin receptor (LRb)-associated Tyr⁹⁸⁵, were increased in SD compared to LD. Our findings suggest that activation of STAT3 by leptin may be dependent on interaction of stimulatory SHP2/GRB2 as well as inhibitory SOCS3 on the level of competitive binding to LRb-associated Tyr⁹⁸⁵. This hypothetical mechanism may represent the molecular identity of seasonally induced adjustments in leptin sensitivity and may be applied to investigating leptin sensitivity in other rodent models.
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http://dx.doi.org/10.1007/s00360-011-0637-4DOI Listing
May 2012

Toward a single-cell-based analysis of neuropeptide expression in Periplaneta americana antennal lobe neurons.

J Comp Neurol 2012 Mar;520(4):694-716

Cologne Biocenter, Institute for Zoology, University of Cologne, D- 50674 Cologne, Germany.

A multitude of potential neurotransmitters and neuromodulators, including peptides, have been detected in the antennal lobe (AL), the first synaptic relay of the central olfactory pathway in the insect brain. However, the functional role of neuropeptides in this system has yet to be revealed. An important prerequisite to understanding the role of neuropeptides is to match the functionally different cell types in the AL with their peptide profiles by using electrophysiological recordings combined with immunocytochemical studies and/or single-cell mass spectrometry. The olfactory system of Periplaneta americana is particularly well suited to accomplish this goal because several physiologically distinct neuron types can be unequivocally identified. With the aim to analyze the neuropeptide inventory of the P. americana AL, this study is an essential step in this direction. First, we systematically analyzed different parts of the AL by matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry to obtain the complete set of neuropeptides present. Altogether, 56 ion signals could be assigned to products of 10 neuropeptide genes (allatostatins A, B, C, SIFamide, allatotropin, FMRFamide-related peptides [myosuppressin, short neuropeptides F, extended FMRFamides], crustacean cardioactive peptide, tachykinin-related peptides). In a second step, a combination of immunocytochemistry and mass spectrometric profiling of defined AL compartments was used to reveal the spatial distribution of neuropeptide-containing cells. Finally, we demonstrated the feasibility of MALDI-TOF mass spectrometric profiling of single AL neurons, which is an important precondition for combining electrophysiology with peptide profiling at the single-cell level.
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http://dx.doi.org/10.1002/cne.22745DOI Listing
March 2012

Brain organization in Collembola (springtails).

Arthropod Struct Dev 2011 Jul 21;40(4):304-16. Epub 2011 Mar 21.

Department of Biology - Animal Physiology, Philipps-University Marburg, Karl-von-Frisch-Str. 8, D-35032 Marburg, Germany.

Arthropoda is comprised of four major taxa: Hexapoda, Crustacea, Myriapoda and Chelicerata. Although this classification is widely accepted, there is still some debate about the internal relationships of these groups. In particular, the phylogenetic position of Collembola remains enigmatic. Some molecular studies place Collembola into a close relationship to Protura and Diplura within the monophyletic Hexapoda, but this placement is not universally accepted, as Collembola is also regarded as either the sister group to Branchiopoda (a crustacean taxon) or to Pancrustacea (crustaceans + hexapods). To contribute to the current debate on the phylogenetic position of Collembola, we examined the brains in three collembolan species: Folsomia candida, Protaphorura armata and Tetrodontophora bielanensis, using antennal backfills, series of semi-thin sections, and immunostaining technique with several antisera, in conjunction with confocal laser scanning microscopy and three-dimensional reconstructions. We identified several neuroanatomical structures in the collembolan brain, including a fan-shaped central body showing a columnar organization, a protocerebral bridge, one pair of antennal lobes with 20-30 spheroidal glomeruli each, and a structure, which we interpret as a simply organized mushroom body. The results of our neuroanatomical study are consistent with the phylogenetic position of Collembola within the Hexapoda and do not contradict the hypothesis of a close relationship of Collembola, Protura and Diplura.
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http://dx.doi.org/10.1016/j.asd.2011.02.003DOI Listing
July 2011

Revisiting the anatomy of the central nervous system of a hemimetabolous model insect species: the pea aphid Acyrthosiphon pisum.

Cell Tissue Res 2011 Feb 18;343(2):343-55. Epub 2010 Dec 18.

Department of Biology - Animal Physiology, Philipps University Marburg, 35043, Marburg, Germany.

Aphids show a marked phenotypic plasticity, producing asexual or sexual and winged or wingless morphs depending on environmental conditions and season. We describe here the general structure of the brain of various morphs of the pea aphid Acyrthosiphon pisum. This is the first detailed anatomical study of the central nervous system of an aphid by immunocytochemistry (synapsin, serotonin, and several neuropeptides), ethyl-gallate staining, confocal laser scanning microscopy, and three-dimensional reconstructions. The study has revealed well-developed optic lobes composed of lamina, medulla, and lobula complex. Ocelli are only present in males and winged parthenogenetic females. The central complex is well-defined, with a central body divided into two parts, a protocerebral bridge, and affiliated lateral accessory lobes. The mushroom bodies are ill-defined, lacking calyces, and only being visualized by using an antiserum against the neuropeptide orcokinin. The antennal lobes contain poorly delineated glomeruli but can be clearly visualized by performing antennal backfills. On the basis of our detailed description of the brain of winged and wingless parthenogenetic A. pisum females, an anatomical map is now available that should improve our knowledge of the way that these structures are involved in the regulation of phenotypic plasticity.
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http://dx.doi.org/10.1007/s00441-010-1099-9DOI Listing
February 2011

Confocal laser scanning microscopy method for quantitative characterization of silica monolith morphology.

Anal Chem 2010 Aug;82(15):6569-75

Department of Chemistry, Philipps-Universität Marburg, Hans-Meerwein-Strasse, 35032 Marburg, Germany.

We present a fast, nondestructive, and quantitative approach to characterize the morphology of capillary silica-based monolithic columns by reconstruction from confocal laser scanning microscopy images. The method comprises column pretreatment, image acquisition, image processing, and statistical analysis of the image data. The received morphological data are chord length distributions for the bulk macropore space and skeleton of the silica monolith. The morphological information is shown to be comparable to that derived from transmission electron microscopy, but far easier to access. The approach is generally applicable to silica-based capillary columns, monolithic or particulate. It allows the rapid acquisition of hundreds of longitudinal and cross-sectional images in a single session, resolving a multitude of morphological details in the column.
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http://dx.doi.org/10.1021/ac100909tDOI Listing
August 2010

Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits.

J Comp Neurol 2010 Aug;518(16):3359-80

Department of Zoology, Stockholm University, S-10691, Stockholm, Sweden.

The fruitfly, Drosophila, is dependent on its olfactory sense in food search and reproduction. Processing of odorant information takes place in the antennal lobes, the primary olfactory center in the insect brain. Besides classical neurotransmitters, earlier studies have indicated the presence of a few neuropeptides in the olfactory system. In the present study we made an extensive analysis of the expression of neuropeptides in the Drosophila antennal lobes by direct profiling using matrix-assisted laser desorption/ionization-time-of-flight (MALDI-TOF) mass spectrometry and immunocytochemistry. Neuropeptides from seven different precursor genes were unambiguously identified and their localization in neurons was subsequently revealed by immunocytochemistry. These were short neuropeptide F, tachykinin related peptide, allatostatin A, myoinhibitory peptide, SIFamide, IPNamide, and myosuppressin. The neuropeptides were expressed in subsets of olfactory sensory cells and different populations of local interneurons and extrinsic (centrifugal) neurons. In some neuron types neuropeptides were colocalized with classical neurotransmitters. Our findings suggest a huge complexity in peptidergic signaling in different circuits of the antennal lobe.
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http://dx.doi.org/10.1002/cne.22405DOI Listing
August 2010

3D Standard Brain of the Red Flour Beetle Tribolium Castaneum: A Tool to Study Metamorphic Development and Adult Plasticity.

Front Syst Neurosci 2010 3;4. Epub 2010 Mar 3.

Department of Biology, Animal Physiology, Philipps-University Marburg Marburg, Germany.

The red flour beetle Tribolium castaneum is emerging as a further standard insect model beside Drosophila. Its genome is fully sequenced and it is susceptible for genetic manipulations including RNA-interference. We use this beetle to study adult brain development and plasticity primarily with respect to the olfactory system. In the current study, we provide 3D standard brain atlases of freshly eclosed adult female and male beetles (A0). The atlases include eight paired and three unpaired neuropils including antennal lobes (ALs), optic lobe neuropils, mushroom body calyces and pedunculi, and central complex. For each of the two standard brains, we averaged brain areas of 20 individual brains. Additionally, we characterized eight selected olfactory glomeruli from 10 A0 female and male beetles respectively, which we could unequivocally recognize from individual to individual owing to their size and typical position in the ALs. In summary, comparison of the averaged neuropil volumes revealed no sexual dimorphism in any of the reconstructed neuropils in A0 Tribolium brains. Both, the female and male 3D standard brain are also used for interspecies comparisons, and, importantly, will serve as future volumetric references after genetical manipulation especially regarding metamorphic development and adult plasticity.
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http://dx.doi.org/10.3389/neuro.06.003.2010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2845059PMC
July 2011

3D-Reconstructions and Virtual 4D-Visualization to Study Metamorphic Brain Development in the Sphinx Moth Manduca Sexta.

Front Syst Neurosci 2010 18;4. Epub 2010 Mar 18.

Department of Biology, Animal Physiology, Philipps-University Marburg Marburg, Germany.

DURING METAMORPHOSIS, THE TRANSITION FROM THE LARVA TO THE ADULT, THE INSECT BRAIN UNDERGOES CONSIDERABLE REMODELING: new neurons are integrated while larval neurons are remodeled or eliminated. One well acknowledged model to study metamorphic brain development is the sphinx moth Manduca sexta. To further understand mechanisms involved in the metamorphic transition of the brain we generated a 3D standard brain based on selected brain areas of adult females and 3D reconstructed the same areas during defined stages of pupal development. Selected brain areas include for example mushroom bodies, central complex, antennal- and optic lobes. With this approach we eventually want to quantify developmental changes in neuropilar architecture, but also quantify changes in the neuronal complement and monitor the development of selected neuronal populations. Furthermore, we used a modeling software (Cinema 4D) to create a virtual 4D brain, morphing through its developmental stages. Thus the didactical advantages of 3D visualization are expanded to better comprehend complex processes of neuropil formation and remodeling during development. To obtain datasets of the M. sexta brain areas, we stained whole brains with an antiserum against the synaptic vesicle protein synapsin. Such labeled brains were then scanned with a confocal laser scanning microscope and selected neuropils were reconstructed with the 3D software AMIRA 4.1.
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http://dx.doi.org/10.3389/fnsys.2010.00007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2845058PMC
July 2011

Discovery of a novel insect neuropeptide signaling system closely related to the insect adipokinetic hormone and corazonin hormonal systems.

J Biol Chem 2010 Apr 12;285(14):10736-47. Epub 2010 Jan 12.

Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.

Neuropeptides and their G protein-coupled receptors (GPCRs) play a central role in the physiology of insects. One large family of insect neuropeptides are the adipokinetic hormones (AKHs), which mobilize lipids and carbohydrates from the insect fat body. Other peptides are the corazonins that are structurally related to the AKHs but represent a different neuropeptide signaling system. We have previously cloned an orphan GPCR from the malaria mosquito Anopheles gambiae that was structurally intermediate between the A. gambiae AKH and corazonin GPCRs. Using functional expression of the receptor in cells in cell culture, we have now identified the ligand for this orphan receptor as being pQVTFSRDWNAamide, a neuropeptide that is structurally intermediate between AKH and corazonin and that we therefore named ACP (AKH/corazonin-related peptide). ACP does not activate the A. gambiae AKH and corazonin receptors and, vice versa, AKH and corazonin do not activate the ACP receptor, showing that the ACP/receptor couple is an independent and so far unknown peptidergic signaling system. Because ACP is structurally intermediate between AKH and corazonin and the ACP receptor between the AKH and corazonin receptors, this is a prominent example of receptor/ligand co-evolution, probably originating from receptor and ligand gene duplications followed by mutations and evolutionary selection, thereby yielding three independent hormonal systems. The ACP signaling system occurs in the mosquitoes A. gambiae, Aedes aegypti, and Culex pipiens (Diptera), the silkworm Bombyx mori (Lepidoptera), the red flour beetle Tribolium castaneum (Coleoptera), the parasitic wasp Nasonia vitripennis (Hymenoptera), and the bug Rhodnius prolixus (Hemiptera). However, the ACP system is not present in 12 Drosophila species (Diptera), the honeybee Apis mellifera (Hymenoptera), the pea aphid Acyrthosiphon pisum (Hemiptera), the body louse Pediculus humanus (Phthiraptera), and the crustacean Daphnia pulex, indicating that it has been lost several times during arthropod evolution. In particular, this frequent loss of hormonal systems is unique for arthropods compared with vertebrates.
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http://dx.doi.org/10.1074/jbc.M109.045369DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2856281PMC
April 2010

Direct peptide profiling of brain tissue by MALDI-TOF mass spectrometry.

Methods Mol Biol 2010 ;615:129-35

Department of Biology, Animal Physiology, Philipps-University, Marburg, Germany.

Direct MALDI-TOF mass spectrometric peptide profiling is increasingly used to analyze the peptide complement in the nervous system of a variety of invertebrate animals from leech to Aplysia and many arthropod species, especially insects and crustaceans. Here, we describe a protocol for direct peptide profiling of defined areas of the central nervous system of insects. With this method, one can routinely and reliably obtain neuropeptide signatures of selected brain areas from various insects.
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http://dx.doi.org/10.1007/978-1-60761-535-4_10DOI Listing
February 2010

Anisometric brain dimorphism revisited: Implementation of a volumetric 3D standard brain in Manduca sexta.

J Comp Neurol 2009 Nov;517(2):210-25

Department of Biology, Animal Physiology, Philipps-University, Marburg, Germany.

Lepidopterans like the giant sphinx moth Manduca sexta are known for their conspicuous sexual dimorphism in the olfactory system, which is especially pronounced in the antennae and in the antennal lobe, the primary integration center of odor information. Even minute scents of female pheromone are detected by male moths, facilitated by a huge array of pheromone receptors on their antennae. The associated neuropilar areas in the antennal lobe, the glomeruli, are enlarged in males and organized in the form of the so-called macroglomerular complex (MGC). In this study we searched for anatomical sexual dimorphism more downstream in the olfactory pathway and in other neuropil areas in the central brain. Based on freshly eclosed animals, we created a volumetric female and male standard brain and compared 30 separate neuropilar regions. Additionally, we labeled 10 female glomeruli that were homologous to previously quantitatively described male glomeruli including the MGC. In summary, the neuropil volumes reveal an isometric sexual dimorphism in M. sexta brains. This proportional size difference between male and female brain neuropils masks an anisometric or disproportional dimorphism, which is restricted to the sex-related glomeruli of the antennal lobes and neither mirrored in other normal glomeruli nor in higher brain centers like the calyces of the mushroom bodies. Both the female and male 3D standard brain are also used for interspecies comparisons, and may serve as future volumetric reference in pharmacological and behavioral experiments especially regarding development and adult plasticity. J. Comp. Neurol. 517:210-225, 2009. (c) 2009 Wiley-Liss, Inc.
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http://dx.doi.org/10.1002/cne.22150DOI Listing
November 2009

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

J Neurochem 2009 Nov 27;111(3):757-65. Epub 2009 Aug 27.

Institute of Zoology, Friedrich-Schiller, University of Jena, Jena, Germany.

By means of single-cell matrix assisted laser desorption/ionization time-of-flight mass spectrometry, we analysed neuropeptide expression in all FXPRLamide/pheromone biosynthesis activating neuropeptide synthesizing neurons of the adult tobacco hawk moth, Manduca sexta. Mass spectra clearly suggest a completely identical processing of the pheromone biosynthesis activating neuropeptide-precursor in the mandibular, maxillary and labial neuromeres of the subesophageal ganglion. Only in the pban-neurons of the labial neuromere, products of two neuropeptide genes, namely the pban-gene and the capa-gene, were detected. Both of these genes expressed, amongst others, sequence-related neuropeptides (extended WFGPRLamides). We speculate that the expression of the two neuropeptide genes is a plesiomorph character typical of moths. A detailed examination of the neuroanatomy and the peptidome of the (two) pban-neurons in the labial neuromere of moths with homologous neurons of different insects indicates a strong conservation of the function of this neuroendocrine system. In other insects, however, the labial neurons either express products of the fxprl-gene or products of the capa-gene. The processing of the respective genes is reduced to extended WFGPRLamides in each case and yields a unique peptidome in the labial cells. Thus, sequence-related messenger molecules are always produced in these cells and it seems that the respective neurons recruited different neuropeptide genes for this motif.
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http://dx.doi.org/10.1111/j.1471-4159.2009.06361.xDOI Listing
November 2009
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