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PLOS ONE  2013 

Ryanodine Receptors Selectively Interact with L Type Calcium Channels in Mouse Taste Cells

DOI: 10.1371/journal.pone.0068174

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Abstract:

Introduction We reported that ryanodine receptors are expressed in two different types of mammalian peripheral taste receptor cells: Type II and Type III cells. Type II cells lack voltage-gated calcium channels (VGCCs) and chemical synapses. In these cells, ryanodine receptors contribute to the taste-evoked calcium signals that are initiated by opening inositol trisphosphate receptors located on internal calcium stores. In Type III cells that do have VGCCs and chemical synapses, ryanodine receptors contribute to the depolarization-dependent calcium influx. Methodology/Principal Findings The goal of this study was to establish if there was selectivity in the type of VGCC that is associated with the ryanodine receptor in the Type III taste cells or if the ryanodine receptor opens irrespective of the calcium channels involved. We also wished to determine if the ryanodine receptors and VGCCs require a physical linkage to interact or are simply functionally associated with each other. Using calcium imaging and pharmacological inhibitors, we found that ryanodine receptors are selectively associated with L type VGCCs but likely not through a physical linkage. Conclusions/Significance Taste cells are able to undergo calcium induced calcium release through ryanodine receptors to increase the initial calcium influx signal and provide a larger calcium response than would otherwise occur when L type channels are activated in Type III taste cells.

References

[1]  Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS (2006) The receptors and cells for mammalian taste. Nature 444: 288–294.
[2]  Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, et al. (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112: 293–301.
[3]  Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, et al. (2003) The receptors for mammalian sweet and umami taste. Cell 115: 255–266.
[4]  Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC (2004) Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol 468: 311–321.
[5]  Medler KF, Margolskee RF, Kinnamon SC (2003) Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci 23: 2608–2617.
[6]  Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, et al. (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310: 1495–1499.
[7]  Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, et al. (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci U S A 104: 6436–6441.
[8]  Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, et al. (2007) Afferent neurotransmission mediated by hemichannels in mammalian taste cells. Embo J 26: 657–667.
[9]  DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, et al. (2006) Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci 26: 3971–3980.
[10]  Richter TA, Caicedo A, Roper SD (2003) Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J Physiol 547: 475–483.
[11]  Huang YA, Maruyama Y, Roper SD (2008) Norepinephrine is coreleased with serotonin in mouse taste buds. J Neurosci 28: 13088–13093.
[12]  Huang YJ, Maruyama Y, Lu KS, Pereira E, Plonsky I, et al. (2005) Mouse taste buds use serotonin as a neurotransmitter. J Neurosci 25: 843–847.
[13]  Rebello MR, Medler KF (2010) Ryanodine receptors selectively contribute to the formation of taste-evoked calcium signals in mouse taste cells. Eur J Neurosci 32: 1825–1835.
[14]  De Crescenzo V, Fogarty KE, Lefkowitz JJ, Bellve KD, Zvaritch E, et al. (2012) Type 1 ryanodine receptor knock-in mutation causing central core disease of skeletal muscle also displays a neuronal phenotype. Proc Natl Acad Sci U S A 109: 610–615.
[15]  De Crescenzo V, Fogarty KE, Zhuge R, Tuft RA, Lifshitz LM, et al. (2006) Dihydropyridine receptors and type 1 ryanodine receptors constitute the molecular machinery for voltage-induced Ca2+ release in nerve terminals. J Neurosci 26: 7565–7574.
[16]  Ouardouz M, Nikolaeva MA, Coderre E, Zamponi GW, McRory JE, et al. (2003) Depolarization-induced Ca2+ release in ischemic spinal cord white matter involves L-type Ca2+ channel activation of ryanodine receptors. Neuron 40: 53–63.
[17]  Berrout J, Isokawa M (2009) Homeostatic and stimulus-induced coupling of the L-type Ca2+ channel to the ryanodine receptor in the hippocampal neuron in slices. Cell Calcium 46: 30–38.
[18]  Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2: a003996.
[19]  Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440–3450.
[20]  Tomchik SM, Berg S, Kim JW, Chaudhari N, Roper SD (2007) Breadth of tuning and taste coding in mammalian taste buds. J Neurosci 27: 10840–10848.
[21]  Vandenbeuch A, Zorec R, Kinnamon SC (2010) Capacitance measurements of regulated exocytosis in mouse taste cells. J Neurosci 30: 14695–14701.
[22]  Zucchi R, Ronca-Testoni S (1997) The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states. Pharmacol Rev 49: 1–51.
[23]  Behe P, DeSimone JA, Avenet P, Lindemann B (1990) Membrane currents in taste cells of the rat fungiform papilla. Evidence for two types of Ca currents and inhibition of K currents by saccharin. J Gen Physiol 96: 1061–1084.
[24]  Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83: 117–161.
[25]  Roberts CD, Dvoryanchikov G, Roper SD, Chaudhari N (2009) Interaction between the second messengers cAMP and Ca2+ in mouse presynaptic taste cells. J Physiol 587: 1657–1668.
[26]  Mouton J, Marty I, Villaz M, Feltz A, Maulet Y (2001) Molecular interaction of dihydropyridine receptors with type-1 ryanodine receptors in rat brain. Biochem J 354: 597–603.
[27]  Kim S, Yun HM, Baik JH, Chung KC, Nah SY, et al. (2007) Functional interaction of neuronal Cav1.3 L-type calcium channel with ryanodine receptor type 2 in the rat hippocampus. J Biol Chem 282: 32877–32889.
[28]  Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325: 717–720.
[29]  De Crescenzo V, ZhuGe R, Velazquez-Marrero C, Lifshitz LM, Custer E, et al. (2004) Ca2+ syntillas, miniature Ca2+ release events in terminals of hypothalamic neurons, are increased in frequency by depolarization in the absence of Ca2+ influx. J Neurosci 24: 1226–1235.
[30]  McNally JM, De Crescenzo V, Fogarty KE, Walsh JV, Lemos JR (2009) Individual calcium syntillas do not trigger spontaneous exocytosis from nerve terminals of the neurohypophysis. J Neurosci 29: 14120–14126.
[31]  ZhuGe R, DeCrescenzo V, Sorrentino V, Lai FA, Tuft RA, et al. (2006) Syntillas release Ca2+ at a site different from the microdomain where exocytosis occurs in mouse chromaffin cells. Biophys J 90: 2027–2037.
[32]  Ouyang K, Zheng H, Qin X, Zhang C, Yang D, et al. (2005) Ca2+ sparks and secretion in dorsal root ganglion neurons. Proc Natl Acad Sci U S A 102: 12259–12264.
[33]  Lefkowitz JJ, Fogarty KE, Lifshitz LM, Bellve KD, Tuft RA, et al. (2009) Suppression of Ca2+ syntillas increases spontaneous exocytosis in mouse adrenal chromaffin cells. J Gen Physiol 134: 267–280.
[34]  Sun XH, Protasi F, Takahashi M, Takeshima H, Ferguson DG, et al. (1995) Molecular architecture of membranes involved in excitation-contraction coupling of cardiac muscle. J Cell Biol 129: 659–671.
[35]  Clapham DE (1995) Calcium signaling. Cell 80: 259–268.
[36]  Berridge MJ (1998) Neuronal calcium signaling. Neuron 21: 13–26.
[37]  Neher E (1998) Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20: 389–399.
[38]  Gilkey JC, Jaffe LF, Ridgway EB, Reynolds GT (1978) A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol 76: 448–466.
[39]  Wier WG, Egan TM, Lopez-Lopez JR, Balke CW (1994) Local control of excitation-contraction coupling in rat heart cells. J Physiol 474: 463–471.
[40]  Wier WG, Balke CW (1999) Ca(2+) release mechanisms, Ca(2+) sparks, and local control of excitation-contraction coupling in normal heart muscle. Circ Res 85: 770–776.
[41]  Ouyang K, Wu C, Cheng H (2005) Ca(2+)-induced Ca(2+) release in sensory neurons: low gain amplification confers intrinsic stability. J Biol Chem 280: 15898–15902.
[42]  Krizaj D, Bao JX, Schmitz Y, Witkovsky P, Copenhagen DR (1999) Caffeine-sensitive calcium stores regulate synaptic transmission from retinal rod photoreceptors. J Neurosci 19: 7249–7261.
[43]  Cadetti L, Bryson EJ, Ciccone CA, Rabl K, Thoreson WB (2006) Calcium-induced calcium release in rod photoreceptor terminals boosts synaptic transmission during maintained depolarization. Eur J Neurosci 23: 2983–2990.
[44]  Babai N, Morgans CW, Thoreson WB (2010) Calcium-induced calcium release contributes to synaptic release from mouse rod photoreceptors. Neuroscience 165: 1447–1456.
[45]  Kennedy HJ, Meech RW (2002) Fast Ca2+ signals at mouse inner hair cell synapse: a role for Ca2+-induced Ca2+ release. J Physiol 539: 15–23.

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