Abstract

Mammalian olfaction depends on chemosensory neurons of the main olfactory epithelia (MOE), and/or of the accessory olfactory epithelia in the vomeronasal organ (VNO). Thus, we have generated the VNO and MOE transcriptomes and the nasal cavity proteome of the house mouse, Mus musculus musculus. Both transcriptomes had low levels of sexual dimorphisms, while the soluble proteome of the nasal cavity revealed high levels of sexual dimorphism similar to that previously reported in tears and saliva. Due to low levels of sexual dimorphism in the olfactory receptors in MOE and VNO, the sex-specific sensing seems less likely to be dependent on receptor repertoires. However, olfaction may also depend on a continuous removal of background compounds from the sites of detection. Odorant binding proteins (OBPs) are thought to be involved in this process and in our study Obp transcripts were most expressed along other lipocalins (e.g., Lcn13, Lcn14) and antimicrobial proteins. At the level of proteome, OBPs were highly abundant with only few being sexually dimorphic. We have, however, detected the major urinary proteins MUP4 and MUP5 in males and females and the male-biased central/group-B MUPs that were thought to be abundant mainly in the urine. The exocrine gland-secreted peptides ESP1 and ESP22 were male-biased but not male-specific in the nose. For the first time, we demonstrate that the expression of nasal lipocalins correlates with antimicrobial proteins thus suggesting that their individual variation may be linked to evolvable mechanisms that regulate natural microbiota and pathogens that regularly enter the body along the ‘eyes-nose-oral cavity’ axis.

Highlights

  • Chemical communication of the house mouse is mediated by the production of sexbiased major urinary proteins (MUP) from the lipocalin family, that due to their betabarrel structure are able to protect and transport volatile pheromones in their hydrophobic pockets (Zidek et al, 1999; Timm et al, 2001; Sharrow et al, 2002, 2003)

  • The signal-containing secretions such as urine and saliva yield strain-specific responses at the accessory olfactory bulb (Kahan and Ben-Shaul, 2016) and specific responses by females to both saliva and vaginal secretions depending on their estrous phase (Ben-Shaul et al, 2010).These responses yield differential sensory representations in the medial amygdala (Bergan et al, 2014), and are responsible for physiological and behavioral effects in the receiver such as estrus induction and synchronization described elsewhere (Jemiolo et al, 1986, 1989; Jemiolo and Novotny, 1994; Ma et al, 1999; Novotny et al, 1999a,b; Sam et al, 2001)

  • We identified a mixture of two normal distributions within the n-binomial distribution of our data, and for statistical analysis, we only tested differences between males and females for those genes that have on average more than four reads (MOE) or five reads (VNO)

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Summary

Introduction

Chemical communication of the house mouse is mediated by the production of sexbiased major urinary proteins (MUP) from the lipocalin family, that due to their betabarrel structure are able to protect and transport volatile pheromones in their hydrophobic pockets (Zidek et al, 1999; Timm et al, 2001; Sharrow et al, 2002, 2003). The Olfactory Transcriptome and Proteome of the House Mouse These receptors are differentially excitable under different pH (Cichy et al, 2015). It has been shown that the olfactory transcriptomes are only minimally different between males and females in C57BL mice (Ibarra-Soria et al, 2014). Individual variation in olfactory receptors is environmentally modulated (Ibarra-Soria et al, 2017) and their expression differences between Mus musculus musculus and M. m. Other genes with inter-individual variation – mainly from the lipocalin family – highly expressed in nasal tissues (Shiao et al, 2012; Ibarra-Soria et al, 2014; Stopkova et al, 2016) – may have roles in olfaction. We used wild-derived mice which in general may have natural variation in the expression of proteins and which may reveal particular expression dependencies that have not yet been detected in the laboratory mouse

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