Odorant-binding proteins in canine anal sac glands indicate an evolutionarily conserved role in mammalian chemical communication

Janssenswillen, Sunita; Roelants, Kim; Carpentier, Sébastien; Rooster, H. de; Metzemaekers, Mieke; Vanschoenwinkel, Bram; Proost, Paul; Bossuyt, Franky

doi:10.1186/s12862-021-01910-w

Cited by 7 publications

(3 citation statements)

References 110 publications

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“…This indicates that changes in microbiota structure do not affect the composition of all compounds, but rather convey different information by changing the species and abundance of some specific compounds, which agrees with previous research in laboratory mouse urine-marks ( SimeoneZomer et al, 2009 ). These specific compounds are not just volatile fatty acids but also include some sterols and fatty acid esters, which corresponds to the general symbiotic hypothesis for animal chemical communication ( Whittaker et al, 2016 ; Drea, 2020 ; Janssenswillen et al, 2021 ; Mazorra-Alonso et al, 2021 ).…”

Section: Discussionmentioning

confidence: 86%

Symbiotic microbiota and odor ensure mating in time for giant pandas

Zheng²,

Guo

et al. 2022

Front. Microbiol.

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To achieve reproduction, male solitary mammals need to locate females using chemical communication with high levels of precision. In the case of giant pandas, the total estrus period of females was usually 15 days each year, however, successful mating activity is finished within 3 days from respective home range. The mating pattern of giant pandas, where multiple males compete for each female requires females employ efficient systems to communicate their estrus phases. To verifying whether the scent secretions of giant pandas changes by gender and estrus progression, the microbiota and compounds in 29 anogenital gland samples from 14 individuals during estrus were analyzed by 16S rRNA sequencing and GC-MS. We show that the microbiota communities covary by gender with 4 particular compounds of scent secretions. Among 597 genera, 34 were identified as biomarkers that could be used to distinguish between different estrus phases. By bacterial-compounds co-analysis, 3 fatty ester acids and squalene compounds covaried with the development of estrus in the bacterial communities of female giant pandas. This study helps clarify how a large, solitary mammal expresses accurate information to improve the likelihood of successful reproduction by changing the composition of microbiota and odor compounds of anogenital glands during estrus.

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Section: Discussionmentioning

confidence: 86%

Symbiotic microbiota and odor ensure mating in time for giant pandas

Zheng²,

Guo

et al. 2022

Front. Microbiol.

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“…Odorant binding proteins (OBPs) belonging to the lipocalin superfamily can be found both in the main and additional olfactory systems [65], but they also were identified in the glands responsible for the secretion of chemical signals, such as the canine anal sac glands [66]. OBPs are closely homologous to the pheromone carrier proteins (such as allergen Can f 4).…”

Section: Discussionmentioning

confidence: 99%

Urinary Proteins of Female Domestic Dog (Canis familiaris) during Ovarian Cycle

Woszczyło

Pasikowski²,

Sankarganesh

et al. 2023

Veterinary Sciences

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The presence and identity of non-volatile chemical signals remain elusive in canines. In this study, we aim to evaluate the urinary proteins of female domestic dogs in the estrus and anestrus phases to evidence the presence of non-volatile chemical signals and to elucidate their identities. We collected urine samples from eight female dogs in the estrus and anestrus phases. A total of 240 proteins were identified in the urine samples using liquid chromatography–mass spectrometry (LC–MS analysis). The comparison of the proteins revealed a significant difference between the estrus and anestrus urine. We identified proteins belonging to the lipocalin family of canines (beta-lactoglobulin-1 and beta-lactoglobulin-2, P33685 and P33686, respectively), one of whose function was the transport of pheromones and which was present only in the estrus urine samples. Moreover, proteins such as Clusterin (CLU), Liver-expressed antimicrobial peptide 2 (LEAP2), and Proenkephalin (PENK) were more abundant in the estrus urine when compared to the anestrus urine. LEAP2 was recently described as a ghrelin receptor antagonist and implicated in regulating food intake and body weight in humans and mice. Proenkephalin, a polypeptide hormone cleaved into opioid peptides, was also recognized as a candidate to determine kidney function. As of yet, none of these have played a role in chemical communication. Clusterin, an extracellular chaperone protecting from protein aggregation implicated in stress-induced cell apoptosis, is a plausible candidate in chemical communication, which is a claim that needs to be ascertained further. Data are available via ProteomeXchange with the identifier PXD040418.

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“…When compared with insect OBPs, the function of vertebrate OBPs remains less well understood; however, evidence suggests that these proteins might also be involved in scent markings. For instance, three OBPs were identified in the anal sac gland of dogs ( Canis lupus familiaris ) and are involved in the signal release and nasal mucosa reception of scent secretions [24]. Similarly, rodent urine also contains a class of lipocalins that play a key role in individual recognition [25].…”

Section: Introductionmentioning

confidence: 99%

Muscone-specific olfactory protein reveals the putative scent-marking pheromone in the Sunda pangolin (Manis javanica)

Yu,

Meng,

et al. 2024

Preprint

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The Sunda pangolin (Manis javanica) is a burrowing and nocturnal animal, and they have poor vision, thus, intraspecies communication relies on olfaction, such as mating, warning, and scent-marking. However, the intraspecies pheromone in pangolins remains unknown. In this study, all the odorant-binding proteins in Sunda pangolins were functionally expressed, and they were screened against a panel of 32 volatiles that were derived from the pangolin’s urine, feces, and anal gland secretions. Reverse chemical ecology identified thatM. javanicaodorant-binding protein 3 (MjavOBP3) possesses the highest binding affinity to muscone. A subsequent behavior-tracking assay showed that only males can sense muscone; thus, we hypothesize that muscone is a male-specific scent-marking pheromone. Meanwhile, the structural study showed that Tyr117 contributes the most to muscone’s binding, which was further validated by site-directed mutagenesis. The findings clarify the scent-marking mechanism in pangolins, and muscone could potentially be used to support the monitoring and conservation of this endangered animal.Author SummaryThe Sunda pangolin is an endangered mammal that is native to Southeast Asia and is threatened due to its economic value. They are cave-living and nocturnal, poor vision; thus, their intraspecies communication is highly reliant on olfaction. Although they are generally solitary, they have been observed to have some social aspects in the wild, such as breeding and territorial behaviors, which are mediated by scents. However, no previous study has investigated the type of pheromones and how they are detected. Using the reverse chemical ecology approach, MjavOBP3 was found to bind to muscone with high affinity, and behavior-tracking assay was performed under well-controlled artificial rearing conditions, which showed only male pangolins can recognize muscone, suggesting its potential male-specific pheromone role.

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Odorant-binding proteins in canine anal sac glands indicate an evolutionarily conserved role in mammalian chemical communication

Cited by 7 publications

References 110 publications

Symbiotic microbiota and odor ensure mating in time for giant pandas

Symbiotic microbiota and odor ensure mating in time for giant pandas

Urinary Proteins of Female Domestic Dog (Canis familiaris) during Ovarian Cycle

Muscone-specific olfactory protein reveals the putative scent-marking pheromone in the Sunda pangolin (Manis javanica)

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