Abstract
Using in vivo confocal Ca2+ imaging, we investigated whether oral application of kokumi substances elicits responses in trigeminal somatosensory ganglion neurons of the mouse. Our results show that 100 μM γEVG (γ-Glu-Val-Gly), a potent kokumi stimulus, evokes responses in a very small fraction (0.6%) of neurons in area V3 (oral sensory field) of the trigeminal ganglion. By comparison, cooled artificial saliva elicited thermal-evoked responses in >7% of V3 trigeminal ganglion neurons. γEVG-evoked responses were small and quite variable, with latencies ranging from 2 to over 200 s. Co-application of the calcium-sensing receptor (CaSR) inhibitor NPS-2143 significantly decreased γEVG-evoked activity. Furthermore, we show that four additional kokumi substances evoked responses in mouse trigeminal ganglion neurons. All neurons responding to kokumi compounds were small cells, with mean diameters below 20 μm. In summary, our data show that certain physiological and pharmacological properties of responses to kokumi compounds can be recorded from sensory neurons in the trigeminal ganglion of living mice. Thus, sensory neurons in the somatosensory trigeminal ganglia may transmit signals from the oral cavity to the central nervous system to generate the texture perceptions that are part of the enigmatic sensations evoked by kokumi substances.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Amino Y, Nakazawa M, Kaneko M, Miyaki T, Miyamura N, Maruyama Y, Eto Y (2016) Structure–CaSR–activity relation of Kokumi γ-glutamyl peptides. Chem Farm Bull 64(8):1181–1189
Brown EM, MacLeod RJ (2001) Extracellular calcium sensing and extracellular calcium signaling. Physiol Rev 81:239–297
Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378
Dunkel A, Koster J, Hofmann T (2007) Molecular and sensory characterization of gamma-glutamyl peptides as key contributors to the kokumi taste of edible beans (Phaseolus vulgaris L.). J Agric Food Chem 55:6712–6719
Heyeraas KJ, Haug SR, Bukoski RD et al (2008) Identification of a Ca2+-sensing receptor in rat trigeminal ganglia, sensory axons, and tooth dental pulp. Calcif Tissue Int 82:57
Kim YS, Chu Y, Han L, Li M, Li Z, LaVinka PC, Sun S et al (2014) Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron 81(4):873–887
Kuroda M, Miyamura N (2015) Mechanism of the perception of “kokumi” substances and the sensory characteristics of the “kokumi” peptide, γ-Glu-Val-Gly. Flavor 4:11
Leijon, S, Breza, JM, Berger, M, Maruyama, Y, Chaudhari N, Roper SD (2016) In vivo imaging of trigeminal ganglion neuron responses to γEVG, capsaicin, allyl isothiocyanate (AITC), and menthol in mice. Abstract presented at ISOT 2016, Yokohama, Japan
Leijon SCM, Neves AF, Breza JM, Simon SA, Chaudhari N, Roper SD (2019) Oral thermosensing by murine trigeminal neurons: modulation by capsaicin, menthol, and mustard oil. J Physiol. In press 597:2045
Maruyama Y, Yasuda R, Kuroda M, Eto Y (2012) Kokumi. Substances, enhancers of basic tastes, induce responses in calcium-sensing receptor expressing taste cells. PLoS One 7(4):e34489. https://doi.org/10.1371/journal.pone.0034489
Nguyen MQ, Wu Y, Bonilla LS, von Buchholtz LJ, Ryba NJP (2017) Diversity amongst trigeminal neurons revealed by high throughput single cell sequencing. PLoS One 12(9):e0185543
Ohsu T, Amino Y, Nagasaki H, Yamanaka T, Takeshita S, Hatanaka MY, Miyamura N, Eto Y (2010) Involvement of the calcium-sensing receptor in human taste perception. J Biol Chem 285(2):1016–1022
Sollars SI, Hill DL (2005) In vivo recordings from rat geniculate ganglia: taste response properties of individual greater superficial petrosal and chorda tympani neurones. J Physiol 564(3):877–893
Ueda Y, Sakaguchi M, Hirayama K, Miyajima R, Kimizuka A (1990) Characteristic flavor constituents in water extract of garlic. Agric Biol Chem 54:163–169
Wang M, Yao Y, Kuang D, Hampson D (2006) Activation of family C G-protein-coupled receptors by the tripeptide glutathione. J Biol Chem 281:8864–8870
Wu A, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2015) Breadth of tuning in taste afferent neurons varies with stimulus strength. Nat Commun 6:8171
Yarmolinsky DA, Peng Y, Pogorzala LA, Rutlin M, Hoon MA, Zuker CS (2016) Coding and plasticity in the mammalian thermosensory system. Neuron 92(5):1079–1092
Acknowledgments
This work was supported by grants from Ajinomoto Co., Inc., and the USA National Institutes of Health: NIDCD R01DC014420 (SR, NC) and NIDCR/NCI R21DE027237 (SR). The authors thank Dr. Ajay Dhaka, University of Washington, for the generous donation of tissue used to produce Fig. 9.13.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Leijon, S.C.M., Chaudhari, N., Roper, S.D. (2019). Mouse Trigeminal Neurons Respond to Kokumi Substances. In: Nishimura, T., Kuroda, M. (eds) Koku in Food Science and Physiology. Springer, Singapore. https://doi.org/10.1007/978-981-13-8453-0_9
Download citation
DOI: https://doi.org/10.1007/978-981-13-8453-0_9
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-8452-3
Online ISBN: 978-981-13-8453-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)