The functional unit of the taste system in mammals is the taste bud, which is a heterogeneous population of 50–80 different cells, including types I, II, and III taste cells. Apart from recognizing taste molecules, taste cells encode sensory information in the form of stimulus-dependent secretion of the afferent neurotransmitter stimulating the taste nerves. Afferent neurotransmission in type II taste cells has many characteristics setting them apart from other exteroreceptor cells operating in vertebrate sensory organs. Thus, type II cells use ATP as neurotransmitter, released via ATP-permeable ion channels. Although taste cells lack axons, type II cells are electrically excitable and the neurotransmitter secretion process is controlled by an action potential. We developed a mathematical model of ATP secretion through a potential-dependent ATP-permeable ion channel and analyzed the potential dependence of secretion in the steady-state case and on stimulation of the cell with pulses. The patterns of ATP secretion found here led to the conclusion that as compared with control of ATP release by a graduated receptor potential, the electrical excitability of taste cells widens the dynamic range of perceived taste stimuli and provides greater reliability of synaptic transmission and confers quantum properties upon it.
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S. D. Roper and N. Chaudhari, “Taste buds: cells, signals and synapses,” Nat. Rev. Neurosci., 18, 485–497 (2017).
Y. A. Huang, Y. Maruyama, R. Stimac, and S. D. Roper, “Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste,” J. Physiol., 586, 2903–2912 (2008).
Y. Oka, M. Butnaru, L. von Buchholtz, et al., “High salt recruits aversive taste pathways,” Nature, 494, 472–475 (2013).
J. Chandrashekar, M. A. Hoon, N. J. Ryba, and C. S. Zuker, “The receptors and cells for mammalian taste,” Nature, 444, 288–294 (2006).
M. Behrens and W. Meyerhof, “Vertebrate bitter taste receptors: Keys for survival in changing environments,” J. Agric. Food Chem., 66, 2204–2213 (2018).
Y. Zhang, M. A. Hoon, J. Chandrashekar, et al., “Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways,” Cell, 112, 293–301 (2003).
M. J. Berridge, “The inositol trisphosphate/calcium signaling pathway in health and disease,” Physiol. Rev., 96, 1261–1296 (2016).
T. R. Clapp, L. M. Stone, R. F. Margolskee, and S. C. Kinnamon, “Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction,” BMC Neurosci., 2, 6 (2001).
M. A. Miyoshi, K. Abe, and Y. Emori, “IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells,” Chem. Senses, 26, 259–265 (2001).
C. A. Perez, L. Huang, M. Rong, et al., “A transient receptor potential channel expressed in taste receptor cells,” Nat. Neurosci., 5, 1169–1176 (2002).
T. Hofmann, V. Chubanov, T. Gudermann, and C. Montell, “TRPM5 is a voltage-modulated and Ca2+-activated monovalent selective cation channel,” Curr. Biol., 13, 1153–1158 (2003).
N. Gao, M. Lu, F. Echeverri, et al., “Voltage-gated sodium channels in taste bud cells,” BMC Neurosci., 10, 20 (2009).
R. Yoshida, K. Sanematsu, N. Shigemura, et al., “Taste receptor cells responding with action potentials to taste stimuli and their molecular expression of taste related genes,” Chem. Senses, 30, Suppl. 1, i19–i20 (2005).
R. I. Wilson and Z. F. Mainen, “Early events in olfactory processing,” Annu. Rev. Neurosci., 29, 163–201 (2006).
G. Matthews and P. Fuchs, “The diverse roles of ribbon synapses in sensory neurotransmission,” Nat. Rev. Neurosci., 11, 812–822 (2010).
T. E. Finger, V. Danilova, J. Barrows, et al., “ATP signaling is crucial for communication from taste buds to gustatory nerves,” Science, 310, 1495–1499 (2005).
R. A. Romanov, O. A. Rogachevskaja, M. F. Bystrova, et al., “Afferent neurotransmission mediated by hemichannels in mammalian taste cells,” EMBO J., 26, 657–667 (2007).
R. A. Romanov, O. A. Rogachevskaja, A. A. Khokhlov, and S. S. Kolesnikov, “Voltage dependence of ATP secretion in mammalian taste cells,” J. Gen. Physiol., 132, 731–744 (2008).
A. Taruno, V. Vingtdeux, M. Ohmoto, et al., “CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes,” Nature, 495, 223–226 (2013).
Z. Ma, A. Taruno, M. Ohmoto, et al., “CALHM3 is essential for rapid ion channel-mediated purinergic neurotransmission of GPCRmediated tastes,” Neuron, 98, 547–561 (2018).
Z. Ma, J. E. Tanis, A. Taruno, and J. K. Foskett, “Calcium homeostasis modulator (CALHM) ion channels,” Pflügers Arch., 468, 395–403 (2016).
B. Hille, Ion Channels of Excitable Membranes, Sinauer Associates, Sunderland, Massachusetts, USA (2001), 3rd ed.
D. Gonzalez, J. M. Gomez-Hernandez, and L. C. Barrio, “Molecular basis of voltage dependence of connexin channels: An integrative appraisal,” Prog. Biophys. Mol. Biol, 94, 66–106 (2007).
F. Bezanilla, “The voltage sensor in voltage-dependent ion channels,” Physiol. Rev., 80, 555–592 (2000).
Z. Ma, A. P. Siebert, K. H. Cheung, et al., “Calcium homeostasis modulator 1 (CALHM1) is the pore-forming subunit of an ion channel that mediates extracellular Ca2+ regulation of neuronal excitability,” Proc. Natl. Acad. Sci. USA, 109, E1963–E1971 (2012).
R. A. Romanov, O. A. Rogachevskaja, M. F. Bystrova, and S. S. Kolesnikov, “Electrical excitability of taste cells. Mechanisms and possible physiological significance,” Biochemistry (Moscow) Supplement. Series A: Membrane and Cell Biology, 6, 169–185 (2012).
Z. Ma, W. T. Saung, and J. K. Foskett, “Action potentials and ion conductances in wild-type and CALHM1-knockout Type II taste cells,” J. Neurophysiol, 117, 1865–1876 (2017).
Z. Zhang, Z. Zhao, R. Margolskee, and E. Liman, “The transduction channel TRPM5 is gated by intracellular calcium in taste cells,” J. Neurosci., 27, 5777–5786 (2007).
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 106, No. 4, pp. 521–532, April, 2020.
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Kolesnikov, S.S. A Mathematical Model of ATP Secretion by Type II Taste Cells. Neurosci Behav Physi 51, 238–244 (2021). https://doi.org/10.1007/s11055-021-01062-w
- taste cells
- ATP secretion
- ATP-permeable channels
- mathematical modeling