title: Compartmentalized cGMP Responses of Olfactory Sensory Neurons inCaenorhabditis elegans.
abstract: Cyclic guanosine monophosphate (cGMP) plays a crucial role as a second messenger in the regulation of sensory signal transduction in many organisms. In AWC olfactory sensory neurons ofCaenorhabditis elegans, cGMP also has essential and distinctive functions in olfactory sensation and adaptation. According to molecular genetic studies, when nematodes are exposed to odorants, a decrease in cGMP regulates cGMP-gated channels for olfactory sensation. Conversely, for olfactory adaptation, an increase in cGMP activates protein kinase G to modulate cellular physiological functions. Although these opposing cGMP responses in single neurons may occur at the same time, it is unclear how cGMP actually behaves in AWC sensory neurons. A hypothetical explanation for opposing cGMP responses is region-specific behaviors in AWC: for odor sensation, cGMP levels in cilia could decrease, whereas odor adaptation is mediated by increased cGMP levels in soma. Therefore, we visualized intracellular cGMP in AWC with a genetically encoded cGMP indicator, cGi500, and examined spatiotemporal cGMP responses in AWC neurons. The cGMP imaging showed that, after odor exposure, cGMP levels in AWC cilia decreased transiently, whereas levels in dendrites and soma gradually increased. These region-specific responses indicated that the cGMP responses in AWC neurons are explicitly compartmentalized. In addition, we performed Ca2+imaging to examine the relationship between cGMP and Ca2+These results suggested that AWC sensory neurons are in fact analogous to vertebrate photoreceptor neurons.SIGNIFICANCE STATEMENTCyclic guanosine monophosphate (cGMP) plays crucial roles in the regulation of sensory signal transduction in many animals. In AWC olfactory sensory neurons ofCaenorhabditis elegans, cGMP also has essential and distinctive functions involving olfactory sensation and adaptation. Here, we visualized intracellular cGMP in AWC neurons with a genetically encoded cGMP indicator and examined how these different functions could be regulated by the same second messenger in single neurons. cGMP imaging showed that, after odor application, cGMP levels in cilia decreased transiently, whereas levels in dendrites and soma gradually increased. These region-specific responses indicated that the responses in AWC neurons are explicitly compartmentalized. In addition, by combining cGMP and Ca2+imaging, we observed that AWC neurons are analogous to vertebrate photoreceptor neurons.
authors.affiliation: Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Yokohama, Kanagawa 223-8522, Japan.
authors.forename: Hisashi
authors.initials: H
authors.lastname: Shidara
authors.affiliation: Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Yokohama, Kanagawa 223-8522, Japan.
authors.forename: Kohji
authors.identifier: 0000-0003-4614-7473
authors.initials: K
authors.lastname: Hotta
authors.affiliation: Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Yokohama, Kanagawa 223-8522, Japan oka@bio.keio.ac.jp.
authors.forename: Kotaro
authors.initials: K
authors.lastname: Oka
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D006152:Cyclic GMP / Q000235:genetics / Q000378:metabolism*; D009812:Odorants; D018034:Olfactory Receptor Neurons / Q000187:drug effects / Q000378:metabolism*; D011984:Sensory Receptor Cells / Q000187:drug effects / Q000378:metabolism*; D012903:Smell / Q000187:drug effects / Q000502:physiology
chemical_list: D029742:Caenorhabditis elegans Proteins; D006152:Cyclic GMP
keywords: C. elegans; cGMP imaging; compartment; sensory neuron