The sensory neurone membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system

Abstract

Male moths detect female-released sex pheromones with extraordinary sensitivity. The remarkable sensory ability is based on a cooperative interplay of pheromone binding proteins in the lymph of hair-like sensilla trichodea and pheromone receptors in the dendrites of sensory neurones. Here we examined whether in Heliothis virescens the so-called 'sensory neurone membrane protein 1' (SNMP1) may contribute to responsiveness to the pheromone component, (Z)-11-hexadecenal (Z11-16:Ald). By means of immunohistochemistry and in situ hybridization we demonstrated that SNMP1 is in fact present in cells expressing the Z11-16:Ald receptor HR13 and the dendrites of sensory neurones. To assess a possible function of SNMP1 we monitored the responsiveness of cell lines that expressed HR13 alone or the combination SNMP1/HR13 to stimulation with Z11-16:Ald by calcium imaging. It was found that SNMP1/HR13 cells were 1000-fold more sensitive to pheromone stimulation compared with HR13 cells. In contrast, cells that expressed HR13 and the non-neuronal SNMP2-type showed no change in pheromone sensitivity. Overall, our reconstitution experiments demonstrate that the presence of SNMP1 significantly increases the HR13-based responsiveness of cells to Z11-16:Ald, suggesting that SNMP1 also contributes to the response of the antennal neurones and thus to the remarkable sensitivity of the pheromone detection system.

Novel cell-based odorant sensor elements based on insect odorant receptors

“…odorant receptors, soluble proteins (odorant binding proteins: OBP, pheromone binding proteins: PBP), and sensory neuron membrane proteins (SNMP) are thought to be involved in sensitive odorant detection in insects (Benton et al, 2007;GrosseWilde et al, 2007;Jin et al, 2008). Most recently, it was suggested that the application of these biological molecules possibly increase the sensitivity of heterologous cells expressing insect odorant receptors (Pregitzer et al, 2014). Thus, by utilizing the functions of these biological molecules, we could enhance the sensitivity of cell-based odorant sensor elements established in this study.…”

A Sex Pheromone Receptor in the Hessian Fly Mayetiola destructor (Diptera, Cecidomyiidae)

“…In addition to pheromone receptors, SNMP1, which shows widespread conservation among insects (Rogers et al, 1997; Nichols and Vogt, 2008; Andersson et al, 2013; Jiang et al, 2016), is important for pheromone reception in both D. melanogaster and moths (Benton et al, 2007; Li et al, 2014; Pregitzer et al, 2014). Three non-mutually exclusive effects of SNMP1 on pheromone reception have been observed, namely (i) that SNMP1 is required for pheromone response (Benton et al, 2007), (ii) that it provides a more rapid onset and especially offset of response (Li et al, 2014), or (iii) that it increases the sensitivity of pheromone detection (Pregitzer et al, 2014).…”

“…OSN responses to pheromone components may also require the presence of certain sensory neuron membrane proteins (SNMPs), which are integral membrane proteins related to scavenger proteins of the CD36 family (Benton et al, 2007; Jin et al, 2008; Nichols and Vogt, 2008). SNMP1 affects responses of pheromone receptors in Drosophila melanogaster and moths, but its role in pheromone reception at the molecular level is just beginning to be unraveled (Benton et al, 2007; Li et al, 2014; Pregitzer et al, 2014; Gomez-Diaz et al, 2016). Rapid advances in next-generation sequencing techniques have resulted in an accelerating number of insect species for which sequences of ORs and other proteins involved in chemoreception have been identified (Montagné et al, 2015).…”

“…This effect was demonstrated for both the DmelOr67d receptor for cVA in vivo , and the Bombyx mori (Lepidoptera) PR for bombykol using Xenopus oocytes (Li et al, 2014). Also, SNMP1 has been shown to increase the sensitivity of a PR (HR13) from Heliothis virescens (Lepidoptera) in Human Embryonic Kidney (HEK) 293 cells (Pregitzer et al, 2014). …”

Identification of candidate chemosensory genes in the antennal transcriptome of Tenebrio molitor (Coleoptera: Tenebrionidae)

“…The SNMP1 subfamily is located on the membrane of pheromone-sensitive OSNs and is coexpressed with pheromone receptors, whereas the SNMP2 subfamily is expressed in the supporting cells surrounding the pheromonesensitive OSNs (Forstner et al, 2008). In the fruit fly Drosophila melanogaster and the moth Heliothis virescens, SNMP1 is essential for the detection of the pheromones 11-cis-vaccenyl acetate (cVA) and (Z)-11-hexadecenal, respectively (Benton et al, 2007;Jin et al, 2008;Pregitzer et al, 2014). However, the function of SNMP2 is still poorly understood.…”