Pheromone Transduction in Moths

Abstract

Calling female moths attract their mates late at night with intermittent release of a species-specific sex-pheromone blend. Mean frequency of pheromone filaments encodes distance to the calling female. In their zig-zagging upwind search male moths encounter turbulent pheromone blend filaments at highly variable concentrations and frequencies. The male moth antennae are delicately designed to detect and distinguish even traces of these sex pheromones amongst the abundance of other odors. Its olfactory receptor neurons sense even single pheromone molecules and track intermittent pheromone filaments of highly variable frequencies up to about 30 Hz over a wide concentration range. In the hawkmoth Manduca sexta brief, weak pheromone stimuli as encountered during flight are detected via a metabotropic PLCβ-dependent signal transduction cascade which leads to transient changes in intracellular Ca2+ concentrations. Strong or long pheromone stimuli, which are possibly perceived in direct contact with the female, activate receptor-guanylyl cyclases causing long-term adaptation. In addition, depending on endogenous rhythms of the moth's physiological state, hormones such as the stress hormone octopamine modulate second messenger levels in sensory neurons. High octopamine levels during the activity phase maximize temporal resolution cAMP-dependently as a prerequisite to mate location. Thus, I suggest that sliding adjustment of odor response threshold and kinetics is based upon relative concentration ratios of intracellular Ca2+ and cyclic nucleotide levels which gate different ion channels synergistically. In addition, I propose a new hypothesis for the cyclic nucleotide-dependent ion channel formed by insect olfactory receptor/coreceptor complexes. Instead of being employed for an ionotropic mechanism of odor detection it is proposed to control subthreshold membrane potential oscillation of sensory neurons, as a basis for temporal encoding of odors.

Olfaction in insects

“…The MGC is marked in gray, while the various"ordinary glomeruli" are marked in different colors. trophysiological, and genetic investigations carried out in the last 20 years also suggest the existence of a G-protein-mediated metabotropic mechanism in pheromone signal transduction: in this context, studies on various moth species support a pheromone-activated IP 3 signal cascade in pheromone-sensitive OSNs [39,52]. A corresponding model which attempts to combine experimental findings obtained to date (.…”

“…Alternatively, it has been proposed that binding of the PBP-pheromone complex to SNMP reverses an inhibition of the pheromone receptor (PR x )-Orco complex, thus triggering an influx of cations into the cell [24]. D Several lines of evidence indicate a G-protein-mediated pathway in pheromone recognition [52]. Receptor activation could thus activate a phospholipase C (PLCβ) via a G q -protein, which converts phosphoinositol-(4,5)-biphosphate (PIP 2 ) into inositol trisphosphate (IP 3 ) and diacylglycerol (DAG).…”

“…3D) proposes that the binding of a pheromone molecule to a specific pheromone receptor mediates the activation of a G-protein and, subsequently, a phospholipase C (PLC); this enzyme catalyzes the hydrolysis of phosphatidyl-4,5-bisphosphate to yield inositol trisphosphate (IP 3 ) and diacylglycerol (DAG). IP 3 then opens a calcium (Ca 2+ )-selective ion channel, which in turn"gates" further non-selective cation channels via the calcium influx [52]. How the expression of the cAMP-activatable Orco channel in pheromone-responsive OSNs is reconcilable with this signal transduction cascade remains as yet unclear.…”

Deterrence of feeding in Rhodnius prolixus (Hemiptera: Reduviidae) after treatment of antennae with a nitric oxide donor

“…Decreases in sensitivity of the sensory system may be due to changes in the permeability of ion channels, mainly by increases in the intracellular Ca ++ concentration. Increase in intracellular Ca ++ is usually caused by the activation of CNG Ca ++ channels (Stengl, 2010). Broillet & Firestein (1997) describe a Ca ++ channel directly activated by NO in rats.…”

The spatial and temporal patterns of odors sampled by lobsters and crabs in a turbulent plume

“…There are marked similarities in the neural olfactory pathways in different phyla (reviewed by Hildebrand and Shepherd, 1997;Ache and Young, 2005;Wilson, 2008;Su et al, 2009), and temporal patterns of neuron activity play a role in olfactory coding in many types of animal (reviewed by Laurent et al, 2001;Stengl, 2010;Junek et al, 2010). Thus, the temporal patterns of active sampling (sniffing) of the odor environment by an olfactory organ can influence the brain's response to odors (reviewed by Ache and Young, 2005;Wilson, 2008), and temporal properties of the stimuli used in neurobiological experiments can affect olfactory coding (e.g.…”