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Neural mechanisms of alarm pheromone signaling

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Molecules and Cells

Abstract

Alarm pheromones are important semiochemicals used by many animal species to alert conspecifics or other related species of impending danger. In this review, we describe recent developments in our understanding of the neural mechanisms underlying the ability of fruit flies, zebrafish and mice to mediate the detection of alarm pheromones. Specifically, alarm pheromones are detected in these species through specialized olfactory subsystems that are unique to the chemosensitive receptors, second messenger-signaling and physiology. Thus, the alarm pheromones appears to be detected by signaling mechanisms that are distinct from those seen in the canonical olfactory system.

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References

  • Blumberg, M.S., Efimova, I.V., and Alberts, J.R. (1992). Ultrasonic vocalizations by rat pups: the primary importance of ambient temperature and the thermal significance of contact comfort. Dev. Psychobiol. 25, 229–250.

    Article  PubMed  CAS  Google Scholar 

  • Braubach, O.R., Fine, A., and Croll, R.P. (2012). Distribution and functional organization of glomeruli in the olfactory bulbs of zebrafish (Danio rerio). J. Comp. Neurol. 520, 2317–2339- Spc2311.

    Article  PubMed  Google Scholar 

  • Brechbühl, J., Klaey, M., and Broillet, M.-C. (2008). Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science 321, 1092–1095.

    Article  PubMed  Google Scholar 

  • Breer, H., Fleischer, J., and Strotmann, J. (2006). The sense of smell: multiple olfactory subsystems. Cell. Mol. Life Sci. 63, 1465–1475.

    Article  PubMed  CAS  Google Scholar 

  • Brown, G.E., Adrian, J., James, C., Smyth, E., Leet, H., and Brennan, S. (2000). Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J. Chem. Ecol. 26, 139–154.

    Article  CAS  Google Scholar 

  • Carr, W.J., Martorano, R.D., and Krames, L. (1970). Responses of mice to odors associated with stress. J. Comp. Physiol. Psych. 71, 223–228.

    Article  CAS  Google Scholar 

  • de Bruyne, M., Foster, K., and Carlson, J.R. (2001). Odor coding in the Drosophila antenna. Neuron 30, 537–552.

    Article  PubMed  Google Scholar 

  • Dean, P., Redgrave, P., and Westby, G.W. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137–147.

    Article  PubMed  CAS  Google Scholar 

  • Dill, L.M., Fraser, A.H.G., and Roitberg, B.D. (1990). The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83, 473–478.

    Article  Google Scholar 

  • Faucher, C., Forstreuter, M., Hilker, M., and de Bruyne, M. (2006). Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J. Exp. Biol. 209, 2739–2748.

    Article  PubMed  CAS  Google Scholar 

  • Fleischer, J., and Breer, H. (2010). The Grueneberg ganglion: a novel sensory system in the nose. Histol. Histopathol. 25, 909–915.

    PubMed  Google Scholar 

  • Fleischer, J., Schwarzenbacher, K., Besser, S., Hass, N., and Breer, H. (2006). Olfactory receptors and signalling elements in the Grueneberg ganglion. J. Neurochem. 98, 543–554.

    Article  PubMed  CAS  Google Scholar 

  • Fleischer, J., Schwarzenbacher, K., and Breer, H. (2007). Expression of trace amine-associated receptors in the Grueneberg ganglion. Chem. Senses 32, 623–631.

    Article  PubMed  CAS  Google Scholar 

  • Fleischer, J., Mamasuew, K., and Breer, H. (2009). Expression of cGMP signaling elements in the Grueneberg ganglion. Histochem. Cell. Biol. 131, 75–88.

    Article  PubMed  CAS  Google Scholar 

  • Frisch, K. (1942). Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung. Z. Vergl. Physiol. 29, 46–145.

    Article  Google Scholar 

  • Gayoso, J., Castro, A., Anadón, R., and Manso, M.J. (2012). Crypt cells of the zebrafish Danio rerio mainly project to the dorsomedial glomerular field of the olfactory bulb. Chem. Senses 37, 357–369.

    Article  PubMed  CAS  Google Scholar 

  • Gruneberg, H. (1973). A ganglion probably belonging to the N. terminalis system in the nasal mucosa of the mouse. Z. Anat. Entwicklungsgesch 140, 39–52.

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez-Garcia, A.G., Contreras, C.M., Mendoza-Lopez, M.R., Garcia-Barradas, O., and Cruz-Sanchez, J.S. (2007). Urine from stressed rats increases immobility in receptor rats forced to swim: role of 2-heptanone. Physiol. Behav. 91, 166–172.

    Article  PubMed  CAS  Google Scholar 

  • Hamdaniel, H., and Doving, K.B. (2003). Sensitivity and selectivity of neurons in the medial region of the olfactory bulb to skin extract from conspecifics in crucian carp, Carassius carassius. Chem. Senses 28, 181–189.

    Article  Google Scholar 

  • Hansen, A., and Zeiske, E. (1998). The peripheral olfactory organ of the zebrafish, Danio rerio: an ultrastructural study. Chem. Senses 23, 39–48.

    Article  PubMed  CAS  Google Scholar 

  • Hansson, B.S., and Stensmyr, M.C. (2011). Evolution of insect olfaction. Neuron 72, 698–711.

    Article  PubMed  CAS  Google Scholar 

  • Hu, J., Zhong, C., Ding, C., Chi, Q., Walz, A., Mombaerts, P., Matsunami, H., and Luo, M. (2007). Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317, 953–957.

    Article  PubMed  CAS  Google Scholar 

  • Ishimoto, H., Takahashi, K., Ueda, R., and Tanimura, T. (2005). Gprotein gamma subunit 1 is required for sugar reception in Drosophila. EMBO J. 24, 3259–3265.

    Article  PubMed  CAS  Google Scholar 

  • Jones, W.D., Cayirlioglu, P., Kadow, I.G., and Vosshall, L.B. (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86–90.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, J.Y., Dahanukar, A., Weiss, L.A., and Carlson, J.R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. USA 104, 3574–3578.

    Article  PubMed  CAS  Google Scholar 

  • Leinders-Zufall, T., Cockerham, R.E., Michalakis, S., Biel, M., Garbers, D.L., Reed, R.R., Zufall, F., and Munger, S.D. (2007). Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc. Natl. Acad. Sci. USA 104, 14507–14512.

    Article  PubMed  CAS  Google Scholar 

  • Lighton, J.R. (1996). Discontinuous gas exchange in insects. Annu. Rev. Entomol. 41, 309–324.

    Article  PubMed  CAS  Google Scholar 

  • Liu, C.Y., Fraser, S.E., and Koos, D.S. (2009). Grueneberg ganglion olfactory subsystem employs a cGMP signaling pathway. J. Comp. Neurol. 516, 36–48.

    Article  PubMed  CAS  Google Scholar 

  • Mamasuew, K., Hofmann, N., Breer, H., and Fleischer, J. (2011). Grueneberg ganglion neurons are activated by a defined set of odorants. Chem. Senses 36, 271–282.

    Article  PubMed  CAS  Google Scholar 

  • Martini, S., Silvotti, L., Shirazi, A., Ryba, N.J., and Tirindelli, R. (2001). Co-expression of putative pheromone receptors in the sensory neurons of the vomeronasal organ. J. Neurosci. 21, 843–848.

    PubMed  CAS  Google Scholar 

  • Mathuru, A.S., Kibat, C., Cheong, W.F., Shui, G., Wenk, M.R., Friedrich, R.W., and Jesuthasan, S. (2012). Chondroitin fragments are odorants that trigger fear behavior in fish. Curr. Biol. 22, 538–544.

    Article  PubMed  CAS  Google Scholar 

  • Munger, S.D., Leinders-Zufall, T., and Zufall, F. (2009). Subsystem organization of the mammalian sense of smell. Annu. Rev. Physiol. 71, 115–140.

    Article  PubMed  CAS  Google Scholar 

  • Munger, S.D., Leinders-Zufall, T., McDougall, L.M., Cockerham, R. E., Schmid, A., Wandernoth, P., Wennemuth, G., Biel, M., Zufall, F., and Kelliher, K.R. (2010). An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Curr. Biol. 20, 1438–1444.

    Article  PubMed  CAS  Google Scholar 

  • Oka, Y., Saraiva, L.R., and Korsching, S.I. (2012). Crypt neurons express a single V1R-related ora gene. Chem. Senses 37, 219–227.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, S.R., and Wilson, R.I. (2008). Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956–960.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, S.R., Bhandawat, V., and Wilson, R.I. (2010). Divisive normalization in olfactory population codes. Neuron 66, 287–299.

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer, W. (1977). The distribution of fright reaction and alarm substance cells in fishes. Copeia 4, 653–665.

    Article  Google Scholar 

  • Pfeiffer, W., Riegelbauer, G., Meier, G., and Scheibler, B. (1985). Effect of hypoxanthine-3(N)-oxide and hypoxanthine-1(N)-oxide on central nervous excitation of the black tetraGymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J. Chem. Ecol. 11, 507–523.

    Article  CAS  Google Scholar 

  • Ralphs, J.R., and Benjamin, M. (1992). Chondroitin and keratan sul- phate in the epidermal club cells of teleosts. J. Fish Biol. 40, 473–475.

    Article  CAS  Google Scholar 

  • Root, C.M., Masuyama, K., Green, D.S., Enell, L.E., Nassel, D.R., Lee, C.H., and Wang, J.W. (2008). A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311–321.

    Article  PubMed  CAS  Google Scholar 

  • Rottman, S.J., and Snowdon, C.T. (1972). Demonstration and analysis of an alarm pheromone in mice. J. Comp. Physiol. Psych. 81, 483–490.

    Article  CAS  Google Scholar 

  • Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L.B., and Touhara, K. (2008). Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002–1006.

    Article  PubMed  CAS  Google Scholar 

  • Schmid, A., Pyrski, M., Biel, M., Leinders-Zufall, T., and Zufall, F. (2010). Grueneberg ganglion neurons are finely tuned cold sensors. J. Neurosci. 30, 7563–7568.

    Article  PubMed  CAS  Google Scholar 

  • Scott, K., Brady, R., Jr., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., and Axel, R. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661–673.

    Article  PubMed  CAS  Google Scholar 

  • Shanbhag, S.R., Müller, B., and Steinbrecht, R.A. (1999). Atlas of olfactory organs of Drosophila melanogaster: 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28, 377–397.

    Article  Google Scholar 

  • Smith, R.J.F. (1992). Alarm signals in fishes. Rev. Fish Biol. Fish. 2, 33–63.

    Article  Google Scholar 

  • Speedie, N., and Gerlai, R. (2008). Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav. Brain Res. 188, 168–177.

    Article  PubMed  CAS  Google Scholar 

  • Stensmyr, M.C., and Maderspacher, F. (2012). Pheromones: fish fear factor. Curr. Biol. 22, R183–186.

    Article  PubMed  CAS  Google Scholar 

  • Su, C.-Y., Menuz, K., and Carlson, J.R. (2009). Olfactory perception: receptors, cells, and circuits. Cell 139, 45–59.

    Article  PubMed  CAS  Google Scholar 

  • Suh, G.S.B., Wong, A.M., Hergarden, A.C., Wang, J.W., Simon, A.F., Benzer, S., Axel, R., and Anderson, D.J. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854–859.

    Article  PubMed  CAS  Google Scholar 

  • Turner, S.L., and Ray, A. (2009). Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461, 277–281.

    Article  PubMed  CAS  Google Scholar 

  • Ueno, K., Kohatsu, S., Clay, C., Forte, M., Isono, K., and Kidokoro, Y. (2006). Gsalpha is involved in sugar perception in Drosophila melanogaster. J. Neurosci. 26, 6143–6152.

    Article  PubMed  CAS  Google Scholar 

  • Verheggen, F.J., Haubruge, E., and Mescher, M.C. (2010). Alarm pheromones-chemical signaling in response to danger. Vitam. Horm. 83, 215–239.

    Article  PubMed  CAS  Google Scholar 

  • Vielma, A., Ardiles, A., Delgado, L., and Schmachtenberg, O. (2008). The elusive crypt olfactory receptor neuron: evidence for its stimulation by amino acids and cAMP pathway agonists. J. Exp. Biol. 211, 2417–2422.

    Article  PubMed  CAS  Google Scholar 

  • Wasserman, S., Salomon, A., and Frye, M.A. (2013). Drosophila tracks carbon dioxide in flight. Curr. Biol. pii: S0960-9822, 01511–01514.

    Google Scholar 

  • Wicher, D., Schafer, R., Bauernfeind, R., Stensmyr, M.C., Heller, R., Heinemann, S.H., and Hansson, B.S. (2008). Drosophila odorant receptors are both ligand-gated and cyclic-nucleotideactivated cation channels. Nature 452, 1007–1011.

    Article  PubMed  CAS  Google Scholar 

  • Yao, C.A., and Carlson, J.R. (2010). Role of G-proteins in odorsensing and CO2-sensing neurons in Drosophila. J. Neurosci. 30, 4562–4572.

    Article  PubMed  CAS  Google Scholar 

  • Yoshihara, Y. (2008). Molecular genetic dissection of the zebrafish olfactory system. Results Probl. Cell Differ. 47, 97–120.

    Google Scholar 

  • Zalaquett, C., and Thiessen, D. (1991). The effects of odors from stressed mice on conspecific behavior. Physiol. Behav. 50, 221–227.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Molecular Neurobiology Program, Skirball Institute of Biomolecular Medicine, Department of Cell Biology, New York University School of Medicine, New York, New York, 10016, USA

    Anders Enjin & Greg Seong-Bae Suh

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  1. Anders Enjin
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  2. Greg Seong-Bae Suh
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Correspondence to Anders Enjin or Greg Seong-Bae Suh.

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Enjin, A., Suh, G.SB. Neural mechanisms of alarm pheromone signaling. Mol Cells 35, 177–181 (2013). https://doi.org/10.1007/s10059-013-0056-3

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  • DOI: https://doi.org/10.1007/s10059-013-0056-3

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