Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis

Abstract

All olfactory receptors identified in teleost fish are expressed in a single sensory surface, whereas mammalian olfactory receptor gene families segregate into different olfactory organs, chief among them the main olfactory epithelium expressing ORs and TAARs, and the vomeronasal organ expressing V1Rs and V2Rs. A transitional stage is embodied by amphibians, with their vomeronasal organ expressing more ‘modern’, later diverging V2Rs, whereas more ‘ancient’, earlier diverging V2Rs are expressed in the main olfactory epithelium. During metamorphosis, the main olfactory epithelium of Xenopus tadpoles transforms into an air-filled cavity (principal cavity, air nose), whereas a newly formed cavity (middle cavity) takes over the function of a water nose. We report here that larval expression of ancient V2Rs is gradually lost from the main olfactory epithelium as it transforms into the air nose. Concomitantly, ancient v2r gene expression begins to appear in the basal layers of the newly forming water nose. We observe the same transition for responses to amino acid odorants, consistent with the hypothesis that amino acid responses may be mediated by V2R receptors.

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References

  1. 1.

    Korsching SI (2016) Aquatic olfaction. In: Zufall F, Munger SD (eds) Chemosensory transduction: the detection of odors, tastes, and other chemostimuli, Academic Press, Elsevier, Amsterdam, Netherland, pp 82–100

  2. 2.

    Reiss JO, Eisthen HL (2008) Comparative anatomy and physiology of chemical senses in amphibians. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold. Adaptations in secondarily aquatic vertebrates, University of California Press, Berkeley, CA, USA, pp 43–63

  3. 3.

    Hansen A, Reiss JO, Gentry CL, Burd GD (1998) Ultrastructure of the olfactory organ in the clawed frog, Xenopus laevis, during larval development and metamorphosis. J Comp Neurol 398:273–288. doi:10.1002/(SICI)1096-9861(19980824)398:2<273:AID-CNE8>3.0.CO;2-Y

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Dittrich K, Kuttler J, Hassenklöver T, Manzini I (2016) Metamorphic remodeling of the olfactory organ of the African clawed frog, Xenopus laevis. J Comp Neurol 524:986–998. doi:10.1002/cne.23887

    Article  PubMed  Google Scholar 

  5. 5.

    Higgs DM, Burd GD (2001) Neuronal turnover in the Xenopus laevis olfactory epithelium during metamorphosis. J Comp Neurol 433:124–130

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Syed AS, Sansone A, Nadler W et al (2013) Ancestral amphibian v2rs are expressed in the main olfactory epithelium. Proc Natl Acad Sci USA 110:7714–7719. doi:10.1073/pnas.1302088110/-/DCSupplemental

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Sansone A, Syed AS, Tantalaki E et al (2014) Trpc2 is expressed in two olfactory subsystems, the main and the vomeronasal system of larval Xenopus laevis. J Exp Biol 217:2235–2238. doi:10.1242/jeb.103465

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Hara T (2006) Feeding behaviour in some teleosts is triggered by single amino acids through olfaction. J Fish Biol 68:810–825

    CAS  Article  Google Scholar 

  9. 9.

    Manzini I, Brase C, Chen T-W, Schild D (2007) Response profiles to amino acid odorants of olfactory glomeruli in larval Xenopus laevis. J Physiol 581:567–579

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Gliem S, Syed AS, Sansone A et al (2013) Bimodal processing of olfactory information in an amphibian nose: odor responses segregate into a medial and a lateral stream. Cell Mol Life Sci 70:1965–1984. doi:10.1007/s00018-012-1226-8

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Zielinski BS, Hara T (2007) Olfaction. In: Hara T, Zielinski BS (eds) Fish physiology: sensory systems neuroscience, vol. 25. Academic Press, Elsevier, Amsterdam, Netherland, pp 1–44

  12. 12.

    Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). Garland Publishing Inc, New York

    Google Scholar 

  13. 13.

    Hassenklöver T, Kurtanska S, Bartoszek I et al (2008) Nucleotide-induced Ca2+ signaling in sustentacular supporting cells of the olfactory epithelium. Glia 56:1614–1624

    Article  PubMed  Google Scholar 

  14. 14.

    Junek S, Chen T-W, Alevra M, Schild D (2009) Activity correlation imaging: visualizing function and structure of neuronal populations. Biophys J 96:3801–3809. doi:10.1016/j.bpj.2008.12.3962

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Etkin W (1932) Growth and resorption phenomena in anuran metamorphosis. Physiol Zool 5:275–300

    Article  Google Scholar 

  16. 16.

    Mezler M, Konzelmann S, Freitag J et al (1999) Expression of olfactory receptors during development in Xenopus laevis. J Exp Biol 202:365–376

    CAS  PubMed  Google Scholar 

  17. 17.

    Liberles SD (2014) Mammalian pheromones. Annu Rev Physiol 76:151–175. doi:10.1146/annurev-physiol-021113-170334

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Sato Y, Miyasaka N, Yoshihara Y (2005) Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish. J Neurosci 25:4889–4897. doi:10.1523/JNEUROSCI.0679-05.2005

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Sansone A, Hassenklöver T, Syed AS et al (2014) Phospholipase C and diacylglycerol mediate olfactory responses to amino acids in the main olfactory epithelium of an amphibian. PLoS One 9:e87721

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Hansen A, Rolen SH, Anderson K et al (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23:9328–9339

    CAS  PubMed  Google Scholar 

  21. 21.

    Freitag J, Krieger J, Strotmann J, Breer H (1995) Two classes of olfactory receptors in Xenopus laevis. Neuron 15:1383–1392. doi:10.1016/0896-6273(95)90016-0

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Niimura Y, Nei M (2005) Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc Natl Acad Sci USA 102:6039–6044. doi:10.1073/pnas.0501922102

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Niimura Y (2012) Olfactory receptor multigene family in vertebrates: from the viewpoint of evolutionary genomics. Curr Genomics 13:103–114. doi:10.2174/138920212799860706

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Mezler M, Fleischer J, Breer H (2001) Characteristic features and ligand specificity of the two olfactory receptor classes from Xenopus laevis. J Exp Biol 204:2987–2997

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by DFG Grants 4113/3-1 (I.M.), KO1046/10-1 (S. I. K.), Schwerpunktprogramm 1392 (I. M. and S. I. K.), Cluster of Excellence and DFG Research Center Nanoscale Microscopy and Molecular Physiology of the Brain (I. M.), and German Ministry of Research and Education (BMBF), Grant Number: 1364480 (I. M.).

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Correspondence to Sigrun I. Korsching.

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Syed, A.S., Sansone, A., Hassenklöver, T. et al. Coordinated shift of olfactory amino acid responses and V2R expression to an amphibian water nose during metamorphosis. Cell. Mol. Life Sci. 74, 1711–1719 (2017). https://doi.org/10.1007/s00018-016-2437-1

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Keywords

  • Metamorphosis
  • Olfactory receptors
  • Evolution
  • V2R family
  • Calcium imaging
  • Amino acid odorants