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Neurobiology of Chemical Communication


Title:Influence of Cat Odor on Reproductive Behavior and Physiology in the House Mouse: (Mus Musculus)
Author(s):Voznessenskaya VV;
Address:"Department of Molecular Medicine University of Padova Padova, Italy"
Journal Title:Neurobiology of Chemical Communication
Year:2014
Volume:
Issue:
Page Number: -
DOI:
ISSN/ISBN:978-1-4665-5341-5
Abstract:"Closely related Mus species Mus musculus and Mus domesticus are the most popular objects in the study of mammalian chemical communication. The understanding of pheromone influences on mammalian behavior has advanced dramatically since the term 'pheromone' was introduced. The major advances in recent years have been based mainly on a single species-the mouse (laboratory form of Mus musculus domesticus). Genetic technologies have revealed a surprisingly large repertoire of chemosensory receptors in mice that potentially detect pheromones (Brennan 2010). However, interspecies chemical communication in the house mouse remains the least investigated area. Use of the laboratory inbred strains of mice makes understanding of the behavioral effects elicited by chemical signals from other species even more complicated. Predator-prey relationships provide an excellent model for the study of interspecies chemical communication. Small mammals in general are frequently at risk to be caught by mammalian, avian, or reptilian predators. In turn their prey species developed a variety of specific adaptations to facilitate recognition, avoidance, and defense against predators. Such antipredator behavioral systems are critical for survival (see review Apfelbach et al. 2005). Chemosensory detection is a very important aspect for predator avoidance strategy for many mammals including the house mouse. Odors from carnivores may elicit fear-induced stereotypic behaviors, change activity patterns and feeding rate, and affect the neuroendocrine system, reproductive behavior, and reproductive output in potential prey (Apfelbach et al. 2005; Dielenberg and McGregor 2001; Harvell 1990; Hayes 2008; Hayes et al. 2006; Kats and Dill 1998; Muller-Schwarze 2006). A number of studies (see Table 14.1) showed effects of odors derived from different predators on behavior and physiology of the house mouse. It implies the existence of shared signal properties through a number of predator species. This idea about generalized 'leitmotif' of predator odors was suggested even much earlier (Stoddart 1980). The idea about the existence of a common carnivore signal was experimentally tested for the first time by Nolte et al. (1994). Manipulations with predator diet as well as chemical removal from carnivore urine of the sulfurous compounds and amines revealed their key role in the effects of coyote urine (Canis latrans) on feeding rates in wild living Mus domesticus (Nolte et al. 1994). Berton et al. (1998) also demonstrated that the diet of a cat strongly affects the behavior of mice towards its feces. Using similar chemical manipulations with cat urine (Felis catus) and manipulating with the diet of urine donors, it has been shown that sulfurous compounds and amines are critical for reproductive inhibitory effects of the cat urine in rodents (Voznessenskaya et al. 2002). Another study (Fendt 2006) indicates that only exposure to urine of canids and felids but not of herbivores induces defensive behavior in laboratory rats (Fendt 2006). The term 'kairomone' was widely adopted to name predator chemical signals: 'kairomones, such as those that elicit fear behavior, are cues transmitted between species that selectively disadvantage the signaler and advantage the receiver' (Wyatt 2003). In search of the molecular nature of kairomones, Papes et al. (2010) isolated the salient molecules from two species (rat and cat) using a combination of behavioral assays in naive laboratory mice, calcium imaging and c-Fos induction. The defensive behavior-promoting activity released by other animals is encoded by species-specific proteins belonging to the major urinary protein (MUP) family, homologs of aggression-promoting mouse pheromones and mediated through the vomeronasal organ (VNO) (Papes et al. 2010). The trace-amine-associated receptors (TAARs) form a specific family of G protein-coupled receptors in vertebrates that was initially considered to be neurotransmitter receptors before it was discovered that mouse TAARs function as chemosensory receptors in the olfactory epithelium (Liberles and Buck 2006). Discovery of a new function of TAARs stimulated the search for the potential ligands. More recent studies (Liberles 2009) showed that ligands for mouse TAARs include a number of volatile amines, several of which are natural constituents of mouse urine. One chemical, 2-phenylethylamine, is reported to be enriched in the urine of stressed animals, and two others, trimethylamine and isoamylamine, are enriched in male versus female urine. These findings raised the possibility that some TAARs are pheromone receptors (Liberles 2009). Further studies (Ferrero et al. 2011) revealed that 2-phenylethylamine is a key component of a predator odor blend that triggers hardwired aversion circuits in the rodent brain. Neurons expressing TAARs project to discrete glomeruli predominantly localized to a confined bulb region (Johnson et al. 2012). TAARs expression involves different regulatory logic than OR expression. Moreover, the epigenetic signature of OR gene choice is absent from TAAR genes. The unique molecular and anatomical features of the TAAR neurons suggest that they constitute a distinct olfactory subsystem (Johnson et al. 2012). Initially 2-phenylethylamine was purified from bobcat urine; quantitative HPLC analysis across 38 mammalian species indicated enriched 2-phenylethylamine production by numerous carnivores. Rats and mice avoid a 2-phenylethylamine odor source; enzymatic depletion of 2-phenylethylamine from a carnivore odor showed that it is required for full avoidance behavior (Ferrero et al. 2011). This study clearly demonstrated that rodent olfactory sensory neurons have the capacity for recognizing interspecies odors. Findings of universal carnivore signals may explain why potential prey respond to odors from allopatric predators with which they do not have evolutionary links and never encountered in their lives, on one hand. On the other hand, the ability of predator odors to produce profound effects on the behavior of prey in general and especially on the reproductive behavior and neuroendocrine system is associated with natural predators only, which suggests an essential role of the evolutionary link between signaling predator and potential prey. First of all, it means that potential prey (in our case, mice) are able to distinguish predator species on a chemosensory basis. Numerous studies (Table 14.1) support this observation (also see review in Apfelbach et al. 2005). It raises a question about the multicompound nature of the kairomones as well as about the existence of species-specific predator chemical cues. One of the most specialized predators toward the house mouse is the domestic cat Felis catus. A long history of coexistence in the same environments led to the development of mutual adaptations at the genetic level. These two species provide a perfect model for the study of innate responses to predator odors. Felinine is a unique sulfur-containing amino acid found in the urine of domestic cats (Rutherfurd et al. 2002). Sulfur-containing volatile compounds 3-mercapto-3-methyl-1-butanol, 3-mercapto-3-methylbutyl formate, 3-methyl-3-methylthio-1-butanol, and 3-methyl-3-(2-methyl-disulfanyl)-1-butanol are identified as species-specific odorants and candidates of felinine derivatives from the cat urine. The levels of these compounds were found to be sex- and age-dependent (Miyazaki et al. 2006a, b). These cat-specific volatile compounds may represent pheromones used as territorial markers for conspecific recognition or reproductive purposes by mature cats (Miyazaki et al. 2008). Species-specific compounds may be used also by other species to recognize potential predators and their physiological status. We now present evidence to support bioactivity of L-felinine and its derivates with the house mouse (Mus musculus)"
Keywords:neuroscience;
Notes:"engMucignat-Caretta, Carla Voznessenskaya, Vera V Review Book Chapter"

 
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