The role of the "sensory neuron membrane protein 1" (SNMP1) in olfactory signal detection in insects
Sensory and Behavioural Biology
Molecular Biology and Physiology of Neurons and Glial Cells
Final Report Abstract
Studies in holometabolous insects, mainly Drosophila melanogaster and moth species, have indicated a crucial role of the „Sensory neuron membrane protein 1“ in the sensitive reception of pheromones by specialized olfactory sensory neurons (OSNs) in sensilla on the antenna. In OSNs, SNMP1 is indicated to act as co-receptor of certain odorant receptors. In contrast, its function in hemimetabolous insects and its possible relevance for the detection of general odorants, released in example from food sources, was unclear. By applying a CRISPR/Cas9- generated SNMP1 knockout line of the desert locust Schistocerca gregaria, we could demonstrate for the first time the essential role of SNMP1 for proper pheromone detection and appropriate pheromone-induced behaviour in a hemimetabolous insect. In the absence of SNMP1, OSNs in the antenna showed significantly reduced responses to the aromatic “courtship inhibition pheromone” phenylacetonitrile (PAN). In consequence, this led to a reduced PAN-induced activity of projection neurons in the antennal lobe of the brain. Moreover, we found a clear impairment of the PAN-controlled courtship behaviour in SNMP1 mutants. Further studies with pheromones and general odorants suggest a functional specialisation of SNMP1 for aromatic compounds and indicated a decisive role of the protein also in the detection of certain general odorants. Contrary to what was known before the project start, our immunohistochemical studies with subtype specific antibodies revealed that in S. gregaria SNMP1 is localized not only in the dendrites of certain OSNs, but instead is also present in the microvilli of „support cells“ (SCs). Similar Studies for the SNMP2-subtype, however, substantiated a selective expression restricted to the microvilli membrane of SCs. Since SCs control the composition of the sensillum lymph (SL) surrounding the dendrites of OSNs and because SNMP types belong to the CD36 family of receptors and transporters, a role of SC-expressed SNMPs in the physiologically crucial removal of inactivation products of odorants from the SL has been suggested. To test this hypothesis, we analysed the SNMP2 of the lepidopteran species Heliothis virescens und Bombyx mori, where pheromone components are inactivated to the corresponding fatty acids. Using a fluorescent fatty acid analogue (FFA) in cell culture studies, we could show for the first time an SNMP2-mediated cellular uptake. In addition, studies on antenna demonstrated that SNMP2-expressing SCs are able to take up the FFA from the SL. In summary, our finding in S. gregaria indicate a dual function of SNMP1 in certain insects. Accordingly, SNMP1 is of crucial importance in OSNs for the sensitive detection of certain pheromones and general odorants. In addition, SNMP1 is indicated to have a role in SCs and might also be involved in the physiologically important „clearance” of the sensillum lymph, similar to what we demonstrated for the first time for a SNMP2-subtype.
Publications
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Targeting the role of “Sensory Neuron Membrane Proteins” in insect olfaction – insights from expression patterns. European Symposium for Insect Taste and Olfaction (16th ESITO), Villasimius, Italy. (Poster).
Cassau. S., Jiang, X., Blankenburg, S., Pregitzer, P., Lemke, R.S., Breer, H., Fleischer, J. & Krieger, J.
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The role of SNMPs in insect olfaction. Cell and Tissue Research, 383(1), 21-33.
Cassau, Sina & Krieger, Jürgen
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Molecular mechanisms of pheromone detection. Insect Pheromone Biochemistry and Molecular Biology, 355-413. Elsevier.
Fleischer, Jörg & Krieger, Jürgen
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Sensory neuron membrane proteins (SNMPs) indicate distinct roles in olfactory signal detection in insects. XXVI International Congress of Entomology (ICE), Helsinki, Finnland. (Poster).
Cassau, S., Sander, D., Karcher, T., Laue, M., Hause, G., Breer, H. & Krieger, J.
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The Sensilla-Specific Expression and Subcellular Localization of SNMP1 and SNMP2 Reveal Novel Insights into Their Roles in the Antenna of the Desert Locust Schistocerca gregaria. Insects, 13(7), 579.
Cassau, Sina; Sander, Doreen; Karcher, Thomas; Laue, Michael; Hause, Gerd; Breer, Heinz & Krieger, Jürgen
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Exploring the role of sensory neuron membrane proteins in moth and locust olfaction. European Symposium for Insect Taste and Olfaction (18th ESITO), Villasimius, Italy. (Invited talk).
Krieger, J.
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SNMP1 is critical for sensitive pheromone detection and pheromone-controlled behaviors in the desert locust Schistocerca gregaria. 15th Göttingen Meeting of the German Neuroscience Society, Göttingen, Germany. (Poster).
Lehmann, J., Libnow, J., Khosravian, M., Chang, H., Knaden, M., Hansson, B.S., Krieger, J. & Fleischer, J.
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Targeting the role of “Sensory Neuron Membrane Proteins” in moth and locust olfaction. MPI for Chemical Ecology, Jena, Germany. (Invited talk).
Krieger, J.
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The role of SNMP2 in the olfactory system of moths. 15th Göttingen Meeting of the German Neuroscience Society, Göttingen, Germany. (Poster)
Cassau, S. & Krieger J.
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The sensilla-specific expression and subcellular localization of SNMP1 and SNMP2 reveal rovel rnsights into their roles in the antenna of the desert docust Schistocerca gregaria. 15th Göttingen Meeting of the German Neuroscience Society, Göttingen, Germany. (Poster).
Krieger, J., Sander, D., Degen, A., Karcher, T., Krüger, S., Laue, M., Hause, G., Breer, H. & Cassau, S.
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The specific expression patterns of sensory neuron membrane proteins are retained throughout the development of the desert locust Schistocerca gregaria. Current Research in Insect Science, 3, 100053.
Cassau, Sina; Degen, Angelina; Krüger, Stephanie & Krieger, Jürgen
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Evidence for a role of SNMP2 and antennal support cells in sensillum lymph clearance processes of moth pheromone-responsive sensilla. Insect Biochemistry and Molecular Biology, 164, 104046.
Cassau, Sina & Krieger, Jürgen
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SNMP1 is critical for sensitive detection of the desert locust aromatic courtship inhibition pheromone phenylacetonitrile. BMC Biology, 22(1).
Lehmann, Joris; Günzel, Yannick; Khosravian, Maryam; Cassau, Sina; Kraus, Susanne; Libnow, Johanna S.; Chang, Hetan; Hansson, Bill S.; Breer, Heinz; Couzin-Fuchs, Einat; Fleischer, Joerg & Krieger, Jürgen
