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 of , 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 Ca imaging to examine the relationship between cGMP and Ca These results suggested that AWC sensory neurons are in fact analogous to vertebrate photoreceptor neurons. Cyclic guanosine monophosphate (cGMP) plays crucial roles in the regulation of sensory signal transduction in many animals. In AWC olfactory sensory neurons of , 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 Ca imaging, we observed that AWC neurons are analogous to vertebrate photoreceptor neurons.

cGMP dynamics underlie thermosensation in C. elegans

“…These results are consistent with the sensory ending-specific localization of GCYs Nguyen et al, 2014) and the fact that the laser-axotomized AFD sensory ending but not AFD soma changes Ca2+ level in response to temperature stimuli (Clark et al, 2006). Compartmentalized cGMP dynamics are also observed in olfactory sensory neuron AWC (Shidara et al, 2017) and O2-sensing neuron PQR (Couto et al, 2013).…”

The Input-Output Relationship of AIY Interneurons in Caenorhabditis elegans in Noisy Environment

“…The glutamate input to AIY decreased following odor application and transiently increased following odor removal, in a deterministic manner (Figure 2C). These responses to odor correspond to the responses of sensory neurons (Chalasani et al., 2007, Shidara et al., 2017). Although there were deterministic changes in glutamate input, large Ca 2+ spikes were observed even without odor, and often at the onset of odor stimulation, as reported previously (Chalasani et al., 2007).…”

Using a Robust and Sensitive GFP-Based cGMP Sensor for Real-Time Imaging in Intact Caenorhabditis elegans

“…, calcium sensors and fluorescent markers for organelles). In the olfactory neuron AWC, this FRET-based sensor showed cilia-compartmentalized cGMP dynamics in response to odorants (Shidara et al 2017). Additionally, Couto et al (2013) found that, in the oxygen-sensing neuron PQR, simultaneous imaging of the cGMP sensor with a calcium sensor in response to a 7–21% increase in oxygen revealed that a decrease in cGMP correlated with an increase in calcium.…”