Jonathan's interest for insects and ants in particular started in childhood. He began studying olfaction during his M.Sc. with Dr. Patricia Nagnan-Le Meillour at INRA in Versailles France (1998). After getting his Ph.D. in the laboratory of Prof. Richard Vogt on the development and evolution of insect olfactory systems (2004), he joined Prof. Laurence Zwiebel's group at Vanderbilt University to study mosquito odorant receptors (2008). The function of mosquito odorant receptors and the molecular mechanism of insect repellent action led him to the laboratory of Dr. Joseph Dickens at the USDA near Washington DC. In 2014, Jonathan joined the Department of Entomology at the Hebrew University of Jerusalem to study the neurobiology of insect olfaction. Supervisors: Dr. Patricia Nagnan-Le Meillour, Prof. Richard G. Vogt, Dr. Joseph Dickens, and Prof. Laurence J. Zwiebel Phone: +972 (0)89489865 Address: The Robert H. Smith Faculty of Agriculture, Food and Environment
Olfaction is a key insect adaptation to a wide range of habitats. In the last thirty years, the d... more Olfaction is a key insect adaptation to a wide range of habitats. In the last thirty years, the detection of octenol by blood-feeding insects has been primarily understood in the context of animal host-seeking. The recent discovery of a conserved octenol receptor gene in the strictly nectar-feeding elephant mosquito Toxorhynchites amboinensis (TaOr8) suggests a different biological role. Here, we show that TaOR8 is a functional ortholog of its counterparts in blood-feeding mosquitoes displaying selectivity towards the (R)-enantiomer of octenol and susceptibility to the insect repellent DEET. These findings suggest that while the function of OR8 has been maintained throughout mosquito evolution, the context in which this receptor is operating has diverged in blood and nectar-feeding mosquitoes. The molecular mechanisms by which insects detect odor cues involve many gene families of which odorant receptors (Ors) play a major role 1. The interactions between ORs and their ligands (biochemical function) and the ecological contexts in which these interactions take place are fascinating relationships to be explored. With the exception of pheromone receptors, whose roles are well understood, there is little knowledge of how insects detect and process specific olfactory cues that are important to their life histories.
BackgroundDEET, 2-undecanone (2-U), IR3535 and Picaridin are widely used as insect repellents to ... more BackgroundDEET, 2-undecanone (2-U), IR3535 and Picaridin are widely used as insect repellents to prevent interactions between humans and many arthropods including mosquitoes. Their molecular action has only recently been studied, yielding seemingly contradictory theories including odorant-dependent inhibitory and odorant-independent excitatory activities on insect olfactory sensory neurons (OSNs) and odorant receptor proteins (ORs).Methodology/Principal FindingsHere we characterize the action of these repellents
The modulation of insect behavior for the purpose of controlling the spread of infectious disease... more The modulation of insect behavior for the purpose of controlling the spread of infectious diseases has been the task of a few insect repellents for which the mechanistic modes of action on odorant receptors (ORs) are unclear. Here, we study the effects of the repellents DEET and IR3535, and a novel OR co-receptor (Orco) agonist on odorant-evoked currents in Xenopus oocytes expressing two subtypes of Aedes aegypti ORs (AaORs). We show that DEET and IR3535 behave as insurmountable antagonists of ORs, and that modulation of OR activity is not restricted to antagonism and agonism, but also includes synergism. This knowledge of the molecular mechanisms underlying OR blockade, activation and hyperactivation will be fundamental to the development of novel strategies for the control of mosquito behavior.
Olfactory signaling is a crucial component in the life history of insects. The development of pre... more Olfactory signaling is a crucial component in the life history of insects. The development of precise and parallel mechanisms to analyze the tremendous amount of chemical information from the environment and other sources has been essential to their evolutionary success. Considerable progress has been made in the study of insect olfaction fueled by bioinformatics- based utilization of genomics along with rapid advances in functional analyses. Here we review recent progress in our rapidly emerging understanding of insect peripheral sensory reception and signal transduction. These studies reveal that the nearly unlimited chemical space insects encounter is covered by distinct chemosensory receptor repertoires that are generally derived by species-specific, rapid gene gain and loss, reflecting the evolutionary consequences of adaptation to meet their specific biological needs. While diverse molecular mechanisms have been put forth, often in the context of controversial models, the characterization of the ubiquitous, highly conserved and insect-specific Orco odorant receptor co-receptor has opened the door to the design and development of novel insect control methods to target agricultural pests, disease vectors and even nuisance insects.
A small cDNA library was constructed from antennae of 100 adult male Aedes aegypti yellow fever m... more A small cDNA library was constructed from antennae of 100 adult male Aedes aegypti yellow fever mosquitoes. Sequencing of 80 clones identified 49 unique gene products, including a member of the Odorant Binding Protein family (Aaeg-OBP10), a homologue of Takeout (Aaeg-TO), and transposable elements of the LINE, SINE and MITE classes. Aaeg-OBP10 encodes a 140 amino acid protein including a predicted 25 amino acid signal peptide. Aaeg-OBP10 expression was adult male enriched, increased with adult age, and greatest in antennae and wings but also present in maxillary palps, proboscis and leg. Aaeg-OBP10 is a likely orthologue of Agam-OBP10 of the malaria mosquito Anopheles gambiae and shares significant similarity with members of the OBP56 gene cluster of Drosophila melanogaster. These OBP genes may represent a unified class of OBPs with unique roles in chemodetection; the expression pattern of Aaeg-OBP10 suggests it may play a role in adult male chemosensory behavior. Aaeg-TO encodes a 248 amino acid protein including a predicted 22 amino acid signal peptide. Aaeg-TO is homologous with the circadian/feeding regulated D. melanogaster Takeout protein (Dmel-TO) and a subclass of Juvenile Hormone Binding Proteins (JHBP) characterized by Moling from Manduca sexta; both Dmel-TO and Moling are sensitive to feeding, suggesting Aaeg-TO might regulate the antennal response to food, host or pheromonal odors in a JH sensitive manner. Aaeg-TO was used to identify 25 D. melanogaster and 13 A. gambiae homologues by Blast analysis suggesting these may comprise a relatively large class of protein involved in the hormonal regulation of behavior.
The olfactory-driven blood-feeding behaviour of female Aedes aegypti mosquitoes is the primary tr... more The olfactory-driven blood-feeding behaviour of female Aedes aegypti mosquitoes is the primary transmission mechanism by which the arboviruses causing dengue and yellow fevers affect over 40 million individuals worldwide. Bioinformatics analysis has been used to identify 131 putative odourant receptors from the A. aegypti genome that are likely to function in chemosensory perception in this mosquito. Comparison with the Anopheles gambiae olfactory subgenome demonstrates significant divergence of the odourant receptors that reflects a high degree of evolutionary activity potentially resulting from their critical roles during the mosquito life cycle. Expression analyses in the larval and adult olfactory chemosensory organs reveal that the ratio of odourant receptors to antennal glomeruli is not necessarily one to one in mosquitoes.
Olfaction is a key insect adaptation to a wide range of habitats. In the last thirty years, the d... more Olfaction is a key insect adaptation to a wide range of habitats. In the last thirty years, the detection of octenol by blood-feeding insects has been primarily understood in the context of animal host-seeking. The recent discovery of a conserved octenol receptor gene in the strictly nectar-feeding elephant mosquito Toxorhynchites amboinensis (TaOr8) suggests a different biological role. Here, we show that TaOR8 is a functional ortholog of its counterparts in blood-feeding mosquitoes displaying selectivity towards the (R)-enantiomer of octenol and susceptibility to the insect repellent DEET. These findings suggest that while the function of OR8 has been maintained throughout mosquito evolution, the context in which this receptor is operating has diverged in blood and nectar-feeding mosquitoes. The molecular mechanisms by which insects detect odor cues involve many gene families of which odorant receptors (Ors) play a major role 1. The interactions between ORs and their ligands (biochemical function) and the ecological contexts in which these interactions take place are fascinating relationships to be explored. With the exception of pheromone receptors, whose roles are well understood, there is little knowledge of how insects detect and process specific olfactory cues that are important to their life histories.
BackgroundDEET, 2-undecanone (2-U), IR3535 and Picaridin are widely used as insect repellents to ... more BackgroundDEET, 2-undecanone (2-U), IR3535 and Picaridin are widely used as insect repellents to prevent interactions between humans and many arthropods including mosquitoes. Their molecular action has only recently been studied, yielding seemingly contradictory theories including odorant-dependent inhibitory and odorant-independent excitatory activities on insect olfactory sensory neurons (OSNs) and odorant receptor proteins (ORs).Methodology/Principal FindingsHere we characterize the action of these repellents
The modulation of insect behavior for the purpose of controlling the spread of infectious disease... more The modulation of insect behavior for the purpose of controlling the spread of infectious diseases has been the task of a few insect repellents for which the mechanistic modes of action on odorant receptors (ORs) are unclear. Here, we study the effects of the repellents DEET and IR3535, and a novel OR co-receptor (Orco) agonist on odorant-evoked currents in Xenopus oocytes expressing two subtypes of Aedes aegypti ORs (AaORs). We show that DEET and IR3535 behave as insurmountable antagonists of ORs, and that modulation of OR activity is not restricted to antagonism and agonism, but also includes synergism. This knowledge of the molecular mechanisms underlying OR blockade, activation and hyperactivation will be fundamental to the development of novel strategies for the control of mosquito behavior.
Olfactory signaling is a crucial component in the life history of insects. The development of pre... more Olfactory signaling is a crucial component in the life history of insects. The development of precise and parallel mechanisms to analyze the tremendous amount of chemical information from the environment and other sources has been essential to their evolutionary success. Considerable progress has been made in the study of insect olfaction fueled by bioinformatics- based utilization of genomics along with rapid advances in functional analyses. Here we review recent progress in our rapidly emerging understanding of insect peripheral sensory reception and signal transduction. These studies reveal that the nearly unlimited chemical space insects encounter is covered by distinct chemosensory receptor repertoires that are generally derived by species-specific, rapid gene gain and loss, reflecting the evolutionary consequences of adaptation to meet their specific biological needs. While diverse molecular mechanisms have been put forth, often in the context of controversial models, the characterization of the ubiquitous, highly conserved and insect-specific Orco odorant receptor co-receptor has opened the door to the design and development of novel insect control methods to target agricultural pests, disease vectors and even nuisance insects.
A small cDNA library was constructed from antennae of 100 adult male Aedes aegypti yellow fever m... more A small cDNA library was constructed from antennae of 100 adult male Aedes aegypti yellow fever mosquitoes. Sequencing of 80 clones identified 49 unique gene products, including a member of the Odorant Binding Protein family (Aaeg-OBP10), a homologue of Takeout (Aaeg-TO), and transposable elements of the LINE, SINE and MITE classes. Aaeg-OBP10 encodes a 140 amino acid protein including a predicted 25 amino acid signal peptide. Aaeg-OBP10 expression was adult male enriched, increased with adult age, and greatest in antennae and wings but also present in maxillary palps, proboscis and leg. Aaeg-OBP10 is a likely orthologue of Agam-OBP10 of the malaria mosquito Anopheles gambiae and shares significant similarity with members of the OBP56 gene cluster of Drosophila melanogaster. These OBP genes may represent a unified class of OBPs with unique roles in chemodetection; the expression pattern of Aaeg-OBP10 suggests it may play a role in adult male chemosensory behavior. Aaeg-TO encodes a 248 amino acid protein including a predicted 22 amino acid signal peptide. Aaeg-TO is homologous with the circadian/feeding regulated D. melanogaster Takeout protein (Dmel-TO) and a subclass of Juvenile Hormone Binding Proteins (JHBP) characterized by Moling from Manduca sexta; both Dmel-TO and Moling are sensitive to feeding, suggesting Aaeg-TO might regulate the antennal response to food, host or pheromonal odors in a JH sensitive manner. Aaeg-TO was used to identify 25 D. melanogaster and 13 A. gambiae homologues by Blast analysis suggesting these may comprise a relatively large class of protein involved in the hormonal regulation of behavior.
The olfactory-driven blood-feeding behaviour of female Aedes aegypti mosquitoes is the primary tr... more The olfactory-driven blood-feeding behaviour of female Aedes aegypti mosquitoes is the primary transmission mechanism by which the arboviruses causing dengue and yellow fevers affect over 40 million individuals worldwide. Bioinformatics analysis has been used to identify 131 putative odourant receptors from the A. aegypti genome that are likely to function in chemosensory perception in this mosquito. Comparison with the Anopheles gambiae olfactory subgenome demonstrates significant divergence of the odourant receptors that reflects a high degree of evolutionary activity potentially resulting from their critical roles during the mosquito life cycle. Expression analyses in the larval and adult olfactory chemosensory organs reveal that the ratio of odourant receptors to antennal glomeruli is not necessarily one to one in mosquitoes.
Uploads