TY - JOUR A1 - Scheiner, Ricarda A1 - Reim, Tina A1 - Sovik, Eirik A1 - Entler, Brian V. A1 - Barron, Andrew B. A1 - Thamm, Markus T1 - Learning, gustatory responsiveness and tyramine differences across nurse and forager honeybees JF - The journal of experimental biology N2 - Honeybees are well known for their complex division of labor. Each bee sequentially performs a series of social tasks during its life. The changes in social task performance are linked to gross differences in behavior and physiology. We tested whether honeybees performing different social tasks (nursing versus foraging) would differ in their gustatory responsiveness and associative learning behavior in addition to their daily tasks in the colony. Further, we investigated the role of the biogenic amine tyramine and its receptors in the behavior of nurse bees and foragers. Tyramine is an important insect neurotransmitter, which has long been neglected in behavioral studies as it was believed to only act as the metabolic precursor of the better-known amine octopamine. With the increasing number of characterized tyramine receptors in diverse insects, we need to understand the functions of tyramine on its own account. Our findings suggest an important role for tyramine and its two receptors in regulating honeybee gustatory responsiveness, social organization and learning behavior. Foragers, which were more responsive to gustatory stimuli than nurse bees and performed better in appetitive learning, also differed from nurse bees in their tyramine brain titers and in the mRNA expression of a tyramine receptor in the brain. Pharmacological activation of tyramine receptors increased gustatory responsiveness of nurse bees and foragers and improved appetitive learning in nurse bees. These data suggest that a large part of the behavioral differences between honeybees may be directly linked to tyramine signaling in the brain. KW - Biogenic amines KW - Nurse bee KW - Apis mellifera KW - PER KW - Proboscis extension response Y1 - 2017 U6 - https://doi.org/10.1242/jeb.152496 SN - 0022-0949 SN - 1477-9145 VL - 220 SP - 1443 EP - 1450 PB - Company of Biologists Limited CY - Cambridge ER - TY - JOUR A1 - Thamm, Markus A1 - Scholl, Christina A1 - Reim, Tina A1 - Gruebel, Kornelia A1 - Moeller, Karin A1 - Rossler, Wolfgang A1 - Scheiner, Ricarda T1 - Neuronal distribution of tyramine and the tyramine receptor AmTAR1 in the honeybee brain JF - The journal of comparative neurology N2 - Tyramine is an important neurotransmitter, neuromodulator, and neurohormone in insects. In honeybees, it is assumed to have functions in modulating sensory responsiveness and controlling motor behavior. Tyramine can bind to two characterized receptors in honeybees, both of which are coupled to intracellular cAMP pathways. How tyramine acts on neuronal, cellular and circuit levels is unclear. We investigated the spatial brain expression of the tyramine receptor AmTAR1 using a specific antibody. This antibody detects a membrane protein of the expected molecular weight in western blot analysis. In honeybee brains, it labels different structures which process sensory information. Labeling along the antennal nerve, in projections of the dorsal lobe and in the gnathal ganglion suggest that tyramine receptors are involved in modulating gustatory and tactile perception. Furthermore, the ellipsoid body of the central complex and giant synapses in the lateral complex show AmTAR1-like immunoreactivity (AmTAR1-IR), suggesting a role of this receptor in modulating sky-compass information and/or higher sensor-motor control. Additionally, intense signals derive from the mushroom bodies, higher-order integration centers for olfactory, visual, gustatory and tactile information. To investigate whether AmTAR1-expressing brain structures are in vicinity to tyramine releasing sites, a specific tyramine antibody was applied. Tyramine-like labeling was observed in AmTAR1-IR positive structures, although it was sometimes weak and we did not always find a direct match of ligand and receptor. Moreover, tyramine-like immunoreactivity was also found in brain regions without AmTAR1-IR (optic lobes, antennal lobes), indicating that other tyramine-specific receptors may be expressed there. KW - antibody KW - biogenic amines KW - G-protein coupled receptor KW - honeybee KW - tyramine Y1 - 2017 U6 - https://doi.org/10.1002/cne.24228 SN - 0021-9967 SN - 1096-9861 VL - 525 SP - 2615 EP - 2631 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Scheiner, Ricarda A1 - Kulikovskaja, Leonora A1 - Thamm, Markus T1 - The honey bee tyramine receptor AmTYR1 and division of foraging labour JF - The journal of experimental biology N2 - Honey bees display a fascinating division of labour among foragers. While some bees solely collect pollen, others only collect nectar. It is assumed that individual differences in sensory response thresholds are at the basis of this division of labour. Biogenic amines and their receptors are important candidates for regulating the division of labour, because they can modulate sensory response thresholds. Here, we investigated the role of the honey bee tyramine receptor AmTYR1 in regulating the division of foraging labour. We report differential splicing of the Amtyr1 gene and show differential gene expression of one isoform in the suboesophageal ganglion of pollen and nectar foragers. This ganglion mediates gustatory inputs. These findings imply a role for the honey bee tyramine receptor in regulating the division of foraging labour, possibly through the suboesophageal ganglion. KW - Splicing KW - Tyramine KW - Gene expression KW - Pollen KW - Nectar KW - Biogenic amines Y1 - 2014 U6 - https://doi.org/10.1242/jeb.098475 SN - 0022-0949 SN - 1477-9145 VL - 217 IS - 8 SP - 1215 EP - 1217 PB - Company of Biologists Limited CY - Cambridge ER - TY - JOUR A1 - Thamm, Markus A1 - Scheiner, Ricarda T1 - PKG in honey bees: spatial expression, amfor gene expression, sucrose responsiveness, and division of labor JF - The journal of comparative neurology N2 - Division of labor is a hallmark of social insects. In honey bees, division of labor involves transition of female workers from one task to the next. The most distinct tasks are nursing (providing food for the brood) and foraging (collecting pollen and nectar). The brain mechanisms regulating this form of behavioral plasticity have largely remained elusive. Recently, it was suggested that division of labor is based on nutrition-associated signaling pathways. One highly conserved gene associated with food-related behavior across species is the foraging gene, which encodes a cyclic guanosine monophosphate (cGMP)-dependent protein kinase (PKG). Our analysis of this gene reveals the presence of alternative splicing in the honey bee. One isoform is expressed in the brain. Expression of this isoform is most pronounced in the mushroom bodies, the subesophageal ganglion, and the corpora allata. Division of labor and sucrose responsiveness in honey bees correlate significantly with foraging gene expression in distinct brain regions. Activating PKG selectively increases sucrose responsiveness in nurse bees to the level of foragers, whereas the same treatment does not affect responsiveness to light. These findings demonstrate a direct link between PKG signaling in distinct brain areas and division of labor. Furthermore, they demonstrate that the difference in sensory responsiveness between nurse bees and foragers can be compensated for by activating PKG. Our findings on the function of PKG in regulating specific sensory responsiveness and social organization offer valuable indications for the function of the cGMP/PKG pathway in many other insects and vertebrates. J. Comp. Neurol. 522:1786-1799, 2014. (c) 2013 Wiley Periodicals, Inc. KW - protein kinase G KW - cyclic GMP KW - division of labor KW - sucrose responsiveness Y1 - 2014 U6 - https://doi.org/10.1002/cne.23500 SN - 0021-9967 SN - 1096-9861 VL - 522 IS - 8 SP - 1786 EP - 1799 PB - Wiley-Blackwell CY - Hoboken ER - TY - JOUR A1 - Reim, Tina A1 - Thamm, Markus A1 - Rolke, Daniel A1 - Blenau, Wolfgang A1 - Scheiner, Ricarda T1 - Suitability of three common reference genes for quantitative real-time PCR in honey bees JF - Apidologie : a quality journal in bee science N2 - Honey bees are important model organisms for neurobiology, because they display a large array of behaviors. To link behavior with individual gene function, quantitative polymerase chain reaction is frequently used. Comparing gene expression of different individuals requires data normalization using adequate reference genes. These should ideally be expressed stably throughout lifetime. Unfortunately, this is frequently not the case. We studied how well three commonly used reference genes are suited for this purpose and measured gene expression in the brains of honey bees differing in age and social role. Although rpl32 is used most frequently, it only remains stable in expression between newly emerged bees, nurse-aged bees, and pollen foragers but shows a peak at the age of 12 days. The genes gapdh and ef1 alpha-f1, in contrast, are expressed stably in the brain throughout all age groups except newly emerged bees. According to stability software, gapdh was expressed most stably, followed by rpl32 and ef1 alpha-f1. KW - gene expression KW - quantitative PCR KW - reference gene KW - stability program KW - Apis mellifera Y1 - 2013 U6 - https://doi.org/10.1007/s13592-012-0184-3 SN - 0044-8435 VL - 44 IS - 3 SP - 342 EP - 350 PB - Springer CY - Paris ER - TY - JOUR A1 - Thamm, Markus A1 - Rolke, Daniel A1 - Jordan, Nadine A1 - Balfanz, Sabine A1 - Schiffer, Christian A1 - Baumann, Arnd A1 - Blenau, Wolfgang T1 - Function and distribution of 5-HT2 receptors in the honeybee (apis mellifera) JF - PLoS one N2 - Background: Serotonin plays a pivotal role in regulating and modulating physiological and behavioral processes in both vertebrates and invertebrates. In the honeybee (Apis mellifera), serotonin has been implicated in division of labor, visual processing, and learning processes. Here, we present the cloning, heterologous expression, and detailed functional and pharmacological characterization of two honeybee 5-HT2 receptors. Methods: Honeybee 5-HT2 receptor cDNAs were amplified from brain cDNA. Recombinant cell lines were established constitutively expressing receptor variants. Pharmacological properties of the receptors were investigated by Ca2+ imaging experiments. Quantitative PCR was applied to explore the expression patterns of receptor mRNAs. Results: The honeybee 5-HT2 receptor class consists of two subtypes, Am5-HT2 alpha and Am5-HT2 beta. Each receptor gene also gives rise to alternatively spliced mRNAs that possibly code for truncated receptors. Only activation of the full-length receptors with serotonin caused an increase in the intracellular Ca2+ concentration. The effect was mimicked by the agonists 5-methoxytryptamine and 8-OH-DPAT at low micromolar concentrations. Receptor activities were blocked by established 5-HT receptor antagonists such as clozapine, methiothepin, or mianserin. High transcript numbers were detected in exocrine glands suggesting that 5-HT2 receptors participate in secretory processes in the honeybee. Conclusions: This study marks the first molecular and pharmacological characterization of two 5-HT2 receptor subtypes in the same insect species. The results presented should facilitate further attempts to unravel central and peripheral effects of serotonin mediated by these receptors. Y1 - 2013 U6 - https://doi.org/10.1371/journal.pone.0082407 SN - 1932-6203 VL - 8 IS - 12 PB - PLoS CY - San Fransisco ER - TY - JOUR A1 - Thamm, Markus A1 - Balfanz, Sabine A1 - Scheiner, Richarda A1 - Baumann, Arnd A1 - Blenau, Wolfgang T1 - Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior N2 - Serotonin plays a key role in modulating various physiological and behavioral processes in both protostomes and deuterostomes. The vast majority of serotonin receptors belong to the superfamily of G-protein-coupled receptors. We report the cloning of a cDNA from the honeybee (Am5-ht1A) sharing high similarity with members of the 5-HT1 receptor class. Activation of Am5-HT1A by serotonin inhibited the production of cAMP in a dose-dependent manner (EC50 = 16.9 nM). Am5-HT1A was highly expressed in brain regions known to be involved in visual information processing. Using in vivo pharmacology, we could demonstrate that Am5-HT1A receptor ligands had a strong impact on the phototactic behavior of individual bees. The data presented here mark the first comprehensive study-from gene to behavior-of a 5-HT1A receptor in the honeybee, paving the way for the eventual elucidation of additional roles of this receptor subtype in the physiology and behavior of this social insect. Y1 - 2010 UR - http://www.springerlink.com/content/101193 U6 - https://doi.org/10.1007/s00018-010-0350-6 SN - 1420-682X ER - TY - JOUR A1 - Thamm, Markus A1 - Schmidt, Stephanie L. A1 - Bernhard, Detlef T1 - Insights into the phylogeny of the genus stentor (heterotrichea, ciliophora) with special emphasis on the evolution of the macronucleus based on SSU rDNA data N2 - Representatives of the genus Stentor (Stentoridae, Heterotrichea) are striking ciliates in environmental water samples because of their size (up to 4 mm) and their trumpet-like shape. Important for species identification are the following main characteristics: (1) the presence or absence of endosymbiotic algae (zoochlorellae); (2) the colour of the pigmented cortical granules, and (3) the shape of the macronucleus. The complete small subunit rDNA (SSU rDNA) of 19 further representatives of the genus Stentor was sequenced to examine the phylogenetic relationships within this genus and to determine the taxonomic value of these main characteristics. The detailed phylogenetic analyses yielded a separation of all species possessing a single compact macronucleus from those species with an "elongated" macronucleus (moniliform or vermiform). The data also indicate that the uptake of algae as well as the loss of pigmentation happened independently in different lineages. Furthermore, a high level of intraspecific variation within several species was found. Thus, S. muelleri and S. (sp.) cf. katashimai appear to represent distinct species and S. multiformis is composed of a species complex. Y1 - 2010 UR - http://www1.nencki.gov.pl/ap-archive.htm SN - 0065-1583 ER -