Combinatorial Coexpression of Neural and Immune Multigene Families in Mouse Vomeronasal Sensory Neurons

Ishii, Takeshi; Hirota, Junji; Mombaerts, Peter

doi:10.1016/s0960-9822(03)00092-7

Cited by 167 publications

(141 citation statements)

References 34 publications

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“…Others (Loconto et al, 2003) and we (Ishii et al, 2003) have shown that V2R ϩ VSNs express another multigene family, termed H2-Mv, representing nonclassical class I genes of the Mhc. Each of the nine H2-Mv genes is expressed in a subset of VSNs; individual VSNs can coexpress multiple H2-Mv genes.…”

Section: Introductionmentioning

confidence: 85%

Expression of Nonclassical Class I Major Histocompatibility Genes Defines a Tripartite Organization of the Mouse Vomeronasal System

Ishii¹,

Mombaerts²

2008

J. Neurosci.

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Section: Introductionmentioning

confidence: 85%

Expression of Nonclassical Class I Major Histocompatibility Genes Defines a Tripartite Organization of the Mouse Vomeronasal System

Ishii¹,

Mombaerts²

2008

J. Neurosci.

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“…To study whether M10 and ESP families coevolve with V2Rs, we examined these families in each of the 11 vertebrates studied here. In addition to the six previously described mouse M10 genes (Ishii et al 2003;Loconto et al 2003), we identified four M10 genes in the rat. Furthermore, nine intact and 11 disrupted mouse ESP genes and five intact and three disrupted rat ESP genes were identified.…”

Section: Evolution Of Protein Families That Interact With V2rsmentioning

confidence: 98%

“…Neurons expressing V1Rs and V2Rs project to the anterior and posterior accessory olfactory bulb, respectively, where they form multiple glomeruli in spatially conserved domains (Dulac and Torello 2003). Second, most V2Rs, but not V1Rs, are coexpressed with M10 and M1 families of Major-Histocompatibility-Complex (MHC) class Ib molecules (Ishii et al 2003;Loconto et al 2003;Silvotti et al 2005). It appears that M10 proteins function as escort molecules in the transport of V2Rs (with the exception of V2R2) to the cell membrane of vomeronasal sensory neurons (Loconto et al 2003;Silvotti et al 2005).…”

mentioning

confidence: 99%

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

Shi¹,

Zhang²

2007

Genome Res.

202

235

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Two evolutionarily unrelated superfamilies of G-protein coupled receptors, V1Rs and V2Rs, bind pheromones and "ordinary" odorants to initiate vomeronasal chemical senses in vertebrates, which play important roles in many aspects of an organism's daily life such as mating, territoriality, and foraging. To study the macroevolution of vomeronasal sensitivity, we identified all V1R and V2R genes from the genome sequences of 11 vertebrates. Our analysis suggests the presence of multiple V1R and V2R genes in the common ancestor of teleost fish and tetrapods and reveals an exceptionally large among-species variation in the sizes of these gene repertoires. Interestingly, the ratio of the number of intact V1R genes to that of V2R genes increased by ∼50-fold as land vertebrates evolved from aquatic vertebrates. A similar increase was found for the ratio of the number of class II odorant receptor (OR) genes to that of class I genes, but not in other vertebrate gene families. Because V1Rs and class II ORs have been suggested to bind to small airborne chemicals, whereas V2Rs and class I ORs recognize water-soluble molecules, these increases reflect a rare case of adaptation to terrestrial life at the gene family level. Several gene families known to function in concert with V2Rs in the mouse are absent outside rodents, indicating rapid changes of interactions between vomeronasal receptors and their molecular partners. Taken together, our results demonstrate the exceptional evolutionary fluidity of vomeronasal receptors, making them excellent targets for studying the molecular basis of physiological and behavioral diversity and adaptation.[Supplemental material is available online at www.genome.org.]Olfaction, or nasal chemoreception, plays a critical role in the daily life of vertebrates. The nasal cavity of most air-breathing vertebrates contains two distinct olfactory tissues/organs: the main olfactory epithelium (MOE) and the vomeronasal organ (VNO) (Dulac and Torello 2003). MOE-mediated olfaction and VNO-mediated olfaction use completely different receptors and signal transduction pathways, and excite different regions of the brain (Dulac and Torello 2003). It was initially thought that MOE and VNO have distinct functions, as MOE detects "ordinary" odorants whereas VNO is specialized for detecting pheromones (Dulac 1997;Buck 2000). This view is changing, as several studies suggested that the MOE can also detect pheromones, whereas the VNO can also detect ordinary odorants (Sam et al. 2001;Boehm et al. 2005;Mandiyan et al. 2005;Yoon et al. 2005;Baxi et al. 2006). Here, pheromones refer to a loosely defined class of chemicals that are emitted and sensed by individuals of the same species to elicit sexual/social behaviors and physiological changes. Examples of pheromone-related behaviors and physiological changes include individual recognition, induction of early puberty, block of pregnancy, and male-male aggression (Keverne 1999).The molecular biology of vertebrate olfaction is best understood in the laboratory mouse Mus m...

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“…A third mutant showing reduced V2R sensitivity renders results consistent with the idea that these receptors are involved in detecting chemosignals that promote aggression. Thus, as discussed above, a subpopulation of the basal, V2R-expressing cells of the vomeronasal epithelium co-express nine nonclassical class I major histocompatibility complex (MHC) genes, termed H2-Mv (Ishii et al, 2003).…”

Section: Role Of the Vomeronasal And Olfactory Epithelia On Aggressionmentioning

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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Combinatorial Coexpression of Neural and Immune Multigene Families in Mouse Vomeronasal Sensory Neurons

Cited by 167 publications

References 34 publications

Expression of Nonclassical Class I Major Histocompatibility Genes Defines a Tripartite Organization of the Mouse Vomeronasal System

Expression of Nonclassical Class I Major Histocompatibility Genes Defines a Tripartite Organization of the Mouse Vomeronasal System

Comparative genomic analysis identifies an evolutionary shift of vomeronasal receptor gene repertoires in the vertebrate transition from water to land

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

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