Essential Role of the Main Olfactory System in Social Recognition of Major Histocompatibility Complex Peptide Ligands

Spehr, Marc; Kelliher, Kevin R.; Li, Xiaohong; Boehm, Thomas; Leinders‐Zufall, Trese; Zufall, Frank

doi:10.1523/jneurosci.4939-05.2006

Cited by 276 publications

(212 citation statements)

References 45 publications

(73 reference statements)

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“…Genotype discrimination via these peptides could be evolutionarily advantageous in a variety of processes ranging from assortative and disassortative mating to sympatric speciation. Importantly, SAV peptides will provide a signature of genomic individuality also in species lacking MUP polymorphism (for example, M. macedonicus) and, because peptides can additionally be detected by the main olfactory epithelium 22 , they may even play a role in species lacking a VNO. Despite all the differences in urinary peptides, one should be aware that, when comparing two given strains of M. musculus, most urinary peptides are shared (for example, our MS analyses showed that at least 70% of peptides identified in B6 mice were also present in BALB/c mice).…”

Section: Discussionmentioning

confidence: 99%

“…This immunological signature must be interpreted by the olfactory system. It is now well established that, in freely behaving mice, nonvolatile peptides gain access to sensory neurons of both the main olfactory system and the VNO during behavioural situations involving direct physical contact 21,22 , that such peptides are powerful ligands for subsets of vomeronasal and olfactory sensory neurons [21][22][23][24][25] (VSNs and OSNs, respectively), that they induce brain activity downstream from the sensory neurons in vivo 26 , and that synthetic MHC peptide ligands can be discriminated in social preference tests 22 and influence social learning and reproductive function in the context of the Bruce effect test 21 . However, it is important to note that there is also considerable evidence for the use of MHC-independent, individual identity signatures in mice in specific behavioural contexts 27,28 (but see the discussion in Ruff et al 29 ).…”

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confidence: 99%

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Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons

et al. 2013

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Selected groups of peptides, including those that are presented by major histocompatibility complex (MHC) proteins, have been proposed to transmit information to the olfactory system of vertebrates via their ability to stimulate chemosensory neurons. However, the lack of knowledge about such peptides in natural sources accessible for nasal recognition has been a major barrier for this hypothesis. Here we analyse urinary peptides from selected mouse strains with respect to genotype-related individual differences. We discover many abundant peptides with single amino-acid variations corresponding to genomic differences. The polymorphism of major urinary proteins is reflected by variations in prominent urinary peptides. We also demonstrate an MHC-dependent peptide (SIINFEKL) occurring at very low concentrations in mouse urine. Chemoreceptive neurons in the vomeronasal organ detect and discriminate single amino-acid variation peptides as well as SIINFEKL. Hence, urinary peptides represent a real-time sampling of the expressed genome available for chemosensory assessment by other individuals.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons

et al. 2013

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“…According to Wysocki et al (1980), the vomeronasal organ (VNO), but not the olfactory epithelium (with few exceptions, see Spehr et al, 2006), is able to detect non-volatile chemicals in the environment. Therefore, irrespective of the existence of volatile sexually attractive male pheromones, non-volatile male pheromones are detected by the VNO of females in which they elicit attraction and other behavioural responses.…”

Section: A Volatile Male Sexual Pheromones: Chemical Species and Thementioning

confidence: 99%

From sexual attraction to maternal aggression: When pheromones change their behavioural significance

Martín‐Sánchez

McLean

Beynon

et al. 2015

Hormones and Behavior

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From sexual attraction to maternal aggression: When pheromones change their behavioural significance, Hormones and Behavior (2014), doi: 10.1016/j.yhbeh.2014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT2 AbstractThis paper reviews the role of chemosignals in the socio-sexual interactions of female mice, and reports two experiments testing the role of pup-derived chemosignals and the male sexual pheromone darcin in inducing and promoting maternal aggression. Female mice are attracted to urine-borne male pheromones. Volatile and non-volatile urine fractions have been proposed to contain olfactory and vomeronasal pheromones. In particular, the male-specific major urinary protein (MUP) MUP20, darcin, has been shown to be rewarding and attractive to females. Non-urinary male chemosignals, such as the lacrimal protein ESP1, promote lordosis in female mice, but its attractive properties are still to be tested. There is evidence indicating that ESP1 and MUPs are detected by vomeronasal type 2 receptors (V2R).When a female mouse becomes pregnant, she undergoes dramatic changes in her physiology and behaviour. She builds a nest for her pups and takes care of them. Dams also defend the nest against conspecific intruders, attacking especially gonadally intact males. Maternal behaviour is dependent on a functional olfactory system, thus suggesting a role of chemosignals in the development of maternal behaviour. Our first experiment demonstrates, however, that pup chemosignals are not sufficient to induce maternal aggression in virgin females. In addition, it is known that vomeronasal stimuli are needed for maternal aggression.Since MUPs (and other molecules) are able to promote intermale aggression, in our second experiment we test if the attractive MUP darcin also promotes attacks on castrated male intruders by lactating dams. Our findings demonstrate that the same chemosignal, darcin, promotes attraction or aggression according to female reproductive state.

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“…These functions were seen as being the exclusive domain of each sensory system, however as discussed above it is not only non-volatile compounds that act as pheromones in mammals [6], and recent evidence suggests that while there are functional differences between the two systems, there is also overlap between the two olfactory systems in their roles in pheromone detection. Both the VNO and MOE have recently been shown to respond to certain volatile odours [87] while MOE sensory neurons have also been shown to be activated by involatile peptides which were previously thought to be detected solely through the VNO [78]. These data indicate that the two olfactory systems do not operate in mutually exclusive sensory domains, however the majority of pheromonal effects in mammals are still thought to be mediated via the VNO [11] and it is only the MOE that has both the appropriate morphology and the complexity of sensory receptor to act as a chemosensor for general airborne odours.…”

Section: Pheromone Detectionmentioning

confidence: 99%

“…Recent electrophysiological work has shown that the volatile male mouse pheromone (methylthio)methanethiol clear responses in the MOB of female mice, indicating that the main olfactory system may mediate the attraction of females to this pheromone in mice [59]. Some pheromonal signals may also be processed in parallel by the two olfactory systems, as calcium imaging studies with nasal tissue slices have shown that there are sensory neurons that respond to MHC peptides in both the VNO and the MOE [78]. Evidence at both the behavioural and cellular level shows that some pheromones are detected by the MOE and processed by the main olfactory system leading to increasing questioning of the view that pheromonal communication in mammals is the exclusive preserve of the vomeronasal system [6].…”

Section: The Main Olfactory System and Pheromonesmentioning

confidence: 99%

The evolution of pheromonal communication

Swaney

Keverne

2009

Behavioural Brain Research

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Small-brained rodents have been the principle focus for pheromonal research and have provided comprehensive insights into the chemosensory mechanisms that underpin pheromonal communication and the hugely important roles that pheromones play in behavioural regulation. However, pheromonal communication does not start or end with the mouse and the rat, and work in amphibians reveals much about the likely evolutionary origins of the chemosensory systems that mediate pheromonal effects. The dual olfactory organs (the main olfactory epithelium and the vomeronasal organ), their receptors and their separate projection pathways appear to have ancient evolutionary origins, appearing in the aquatic ancestors of all tetrapods during the Devonian period and so pre-dating the transition to land. While the vomeronasal organ has long been considered an exclusively pheromonal organ, accumulating evidence indicates that it is not the sole channel for the transduction of pheromonal information and that both olfactory systems have been co-opted for the detection of different pheromone signals over the course of evolution. This has also led to great diversity in the vomeronasal and olfactory receptor families, with enormous levels of gene diversity and inactivation of genes in different species. Finally, the evolution of trichromacy as well as huge increases in social complexity have minimised the role of pheromones in the lives of primates, leading to the total inactivation of the vomeronasal system in catarrhine primates while the brain increased in size and behaviour became emancipated from hormonal regulation.

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Essential Role of the Main Olfactory System in Social Recognition of Major Histocompatibility Complex Peptide Ligands

Abstract: Genes of the major histocompatibility complex (MHC),

Cited by 276 publications

References 45 publications

Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons

Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons

From sexual attraction to maternal aggression: When pheromones change their behavioural significance

The evolution of pheromonal communication

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