Calcitonin gene-related peptide reduces taste-evoked ATP secretion from mouse taste buds

Journal of Neuroscience

Volumn 35, Issue 37, 2015, Pages 12714-12724

  Huang, Anthony Y ^a,b   Wu, Sandy Y ^a  

^a Department of Anatomy ^*  (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ATP; Biosensors; Ca2+ imaging; CGRP; Serotonin; Taste

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCITONIN GENE RELATED PEPTIDE; CALCIUM ION; PHOSPHOLIPASE C; SEROTONIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; 1-(6-((3-METHOXYESTRA-1,3,5(10)-TRIEN-17-YL)AMINO)HEXYL)-1H-PYRROLE-2,5-DIONE; 2 PYRROLIDONE DERIVATIVE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; ESTRANE DERIVATIVE; PRESYNAPTIC RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ENZYME ACTIVATION; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TASTE; TASTE BUD; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; HAMSTER; MOLECULAR GENETICS; PARACRINE SIGNALING; PHYSIOLOGY; SECRETION (PROCESS); SENSORY NERVE;

ADENOSINE TRIPHOSPHATE; AFFERENT PATHWAYS; AMINO ACID SEQUENCE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM SIGNALING; CHO CELLS; CRICETINAE; CRICETULUS; ESTRENES; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PARACRINE COMMUNICATION; PYRROLIDINONES; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; RECEPTORS, PRESYNAPTIC; SEROTONIN; TASTE BUDS;

EID: 84941776797     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0100-15.2015     Document Type: Article

References (78)

1. Arulmani U, Maassenvandenbrink A, Villalón CM, Saxena PR (2004) Calcitonin gene-related peptide and its role in migraine pathophysiology. Eur J Pharmacol 500:315–330. CrossRef Medline
2. Astbäck J, Arvidson K, Johansson O (1997) An immunohistochemical screening of neurochemical markers in fungiform papillae and taste buds of the anterior rat tongue. Arch Oral Biol 42:137–147. CrossRef Medline
3. Berg KA, Clarke WP, Sailstad C, Saltzman A, Maayani S (1994) Signal transduction differences between 5-hydroxytryptamine type 2A and type 2C receptor systems. Mol Pharmacol 46:477–484. Medline
4. Bo X, Alavi A, Xiang Z, Oglesby I, Ford A, Burnstock G (1999) Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 10:1107–1111. CrossRef Medline
5. Bullock CM, Wookey P, Bennett A, Mobasheri A, Dickerson I, Kelly S (2014) Peripheral calcitonin gene-related peptide receptor activation and mechanical sensitization of the joint in rat models of osteoarthritis pain. Arthritis Rheumatol 66:2188–2200. CrossRef Medline
6. Cao Y, Zhao FL, Kolli T, Hivley R, Herness S (2009) GABA expression in the mammalian taste bud functions as a route of inhibitory cell-to-cell communication. Proc Natl Acad SciU S A 106:4006–4011. CrossRef Medline
7. Cardell LO, Uddman R, Edvinsson L (1994) Low plasma concentrations of VIP and elevated levels of other neuropeptides during exacerbations of asthma. Eur Respir J 7:2169–2173. CrossRef Medline
8. Ceruti S, Villa G, Fumagalli M, Colombo L, Magni G, Zanardelli M, Fabbretti E, Verderio C, van den Maagdenberg AM, Nistri A, Abbracchio MP (2011) Calcitonin gene-related peptide-mediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2.1 Knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci 31:3638–3649. CrossRef Medline
9. Chang RB, Waters H, Liman ER (2010) A proton current drives action po tentials in genetically identified sour taste cells. Proc Natl Acad Sci U S A 107:22320–22325. CrossRef Medline
10. Chaudhari N, Roper SD (2010) The cell biology of taste. J Cell Biol 190: 285–296. CrossRef Medline
11. 2+-dependent modulation of ATP-gated P2X receptors in nociceptors. Neuropharmacology 36:1303–1308. CrossRef Medline
12. Crescimanno C, Merigo F, Bernardi P, Osculati F, Sbarbati A (2004) Neurochemistry of the gustatory subgemmal plexus. Chem Senses 29: 537–546. CrossRef Medline
13. DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, Chaudhari N (2006) Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci 26:3971–3980. CrossRef Medline
14. Dickerson IM (2013) Role of CGRP-receptor component protein (RCP) in CLR/RAMPfunction. Curr Protein Pept Sci 14:407–415. CrossRef Medline
15. Drissi H, Lasmoles F, Le Mellay V, Marie PJ, Lieberherr M (1998) Activation of phospholipase C-beta1 via Galphaq/11 during calcium mobilization by calcitonin gene-related peptide. J Biol Chem 273:20168–20174. CrossRef Medline
16. Dvoryanchikov G, Tomchik SM, Chaudhari N (2007) Biogenic amine synthesis and uptake in rodent taste buds. J Comp Neurol 505:302–313. CrossRef Medline
17. Dvoryanchikov G, Huang YA, Barro-Soria R, Chaudhari N, Roper SD (2011) GABA, its receptors, and GABAergic inhibition in mouse taste buds. J Neurosci 31:5782–5791. CrossRef Medline
18. Finger TE (1986) Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallate papilla of the rat. Chem Senses 11:135–144. CrossRef
19. Finger TE, Simon SA (2002) The cell biology of lingual epithelia. In: The neurobiology of taste and smell (Finger TE, Silver WL, Restrepo D, eds), pp 287–314. New York: Wiley.
20. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310:1495–1499. CrossRef Medline
21. Grant J (2012) Tachykinins stimulate a subset of mouse taste cells. PLoS One 7:e31697. CrossRef Medline
22. Green BG (2012) Chemesthesis and the chemical senses as components of a “chemofensor complex.” Chem Senses 37:201–206. CrossRef
23. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440–3450. Medline
24. Hay DL, Poyner DR, Smith DM (2003) Desensitisation of adrenomedullin and CGRP receptors. Regul Pept 112:139–145. CrossRef Medline
25. Hayakawa T, Kuwahara S, Maeda S, Tanaka K, Seki M (2010) Calcitonin gene-related peptide immunoreactive neurons innervating the soft palate, the root of tongue, and the pharynx in the superior glossopharyngeal ganglion of the rat. J Chem Neuroanat 39:221–227. CrossRef Medline
26. Hayakawa T, Kuwahara-Otani S, Maeda S, Tanaka K, Seki M (2014) Calcitonin gene-related peptide immunoreactive sensory neurons in the vagal and glossopharyngeal ganglia innervating the larynx of the rat. J Chem Neuroanat 55:18–23. CrossRef Medline
27. He ML, Koshimizu TA, Tomić M, Stojilkovic SS (2002) Purinergic P2X2 receptor desensitization depends on coupling between ectodomain and C-terminal domain. Mol Pharmacol 62:1187–1197. CrossRef Medline
28. Heath TP, Melichar JK, Nutt DJ, Donaldson LF (2006) Human taste thresholds are modulated by serotonin and noradrenaline. J Neurosci 26: 12664–12671. CrossRef Medline
29. + current in rat taste receptor cells. Neuroreport 8:3257–3261. CrossRef Medline
30. Herness S, Zhao FL (2009) The neuropeptides CCK and NPY and the changing view of cell-to-cell communication in the taste bud. Physiol Behav 97:581–591. CrossRef Medline
31. Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739–768. CrossRef Medline
32. Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Tränkner D, Ryba NJ, Zuker CS (2006) The cells and logic for mammalian sour taste detection. Nature 442:934–938. CrossRef Medline
33. Huang YA, Maruyama Y, Roper SD (2008a) Norepinephrine is coreleased with serotonin in mouse taste buds. J Neurosci 28:13088–13093. CrossRef Medline
34. Huang YA, Maruyama Y, Stimac R, Roper SD (2008b) Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol 586: 2903–2912. CrossRef Medline
35. Huang YA, Dando R, Roper SD (2009) Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J Neurosci 29:13909–13918. CrossRef Medline
36. Huang YA, Pereira E, Roper SD (2011a) Acid stimulation (sour taste) elicits GABA and serotonin release from mouse taste cells. PLoS One 6:e25471. CrossRef Medline
37. Huang YA, Stone LM, Pereira E, Yang R, Kinnamon JC, Dvoryanchikov G, Chaudhari N, Finger TE, Kinnamon SC, Roper SD (2011b) Knocking out P2X receptors reduces transmitter secretion in taste buds. J Neurosci 31:13654–13661. CrossRef Medline
38. Huang YA, Grant J, Roper S (2012) Glutamate may be an efferent transmitter that elicits inhibition in mouse taste buds. PLoS One 7:e30662. CrossRef Medline
39. Huang YJ, Wu YH, Lu KS (2003) Immunoelectron microscopic studies on protein gene product 9.5 and calcitonin gene-related peptide in vallate taste cells and related nerves in the guinea pig. Microsc Res Tech 62:383–395. CrossRef Medline
40. Huang YJ, Maruyama Y, Lu KS, Pereira E, Plonsky I, Baur JE, Wu D, Roper SD (2005) Mouse taste buds use serotonin as a neurotransmitter. J Neurosci 25:843–847. CrossRef Medline
41. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (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. CrossRef Medline
42. Ishida Y, Ugawa S, Ueda T, Murakami S, Shimada S (2002) Vanilloid receptor subtype-1 (VR1) is specifically localized to taste papillae. Brain Res Mol Brain Res 107:17–22. CrossRef Medline
43. Ishida Y, Ugawa S, Ueda T, Yamada T, Shibata Y, Hondoh A, Inoue K, Yu Y, Shimada S (2009) P2X(2)-and P2X(3)-positive fibers in fungiform papillae originate from the chorda tympani but not the trigeminal nerve in rats and mice. J Comp Neurol 514:131–144. CrossRef Medline
44. Jaber L, Zhao FL, Kolli T, Herness S (2014) A physiologic role for serotonergic transmission in adult rat taste buds. PLoS One 9:e112152. CrossRef Medline
45. Juaneda C, Dumont Y, Quirion R (2000) The molecular pharmacology of CGRP and related peptide receptor subtypes. Trends Pharmacol Sci 21: 432–438. CrossRef Medline
46. Kaya N, Shen T, Lu SG, Zhao FL, Herness S (2004) A paracrine signaling role for serotonin in rat taste buds: expression and localization of serotonin receptor subtypes. Am J Physiol Regul Integr Comp Physiol 286: R649–R658. CrossRef Medline
47. Kelman L (2004) Osmophobia and taste abnormality in migraineurs: a tertiary care study. Headache 44:1019–1023. CrossRef Medline
48. Maggi CA, Meli A (1988) The sensory-efferent function of capsaicinsensitive sensory neurons. Gen Pharmacol 19:1–43. CrossRef Medline
49. 2+ responses in cultured astrocytes and in Bergmann glial cells from cerebellar slices. Eur J Neurosci 28:2213–2220. CrossRef Medline
50. Murata Y, Yasuo T, Yoshida R, Obata K, Yanagawa Y, Margolskee RF, Ninomiya Y (2010) Action potential-enhanced ATP release from taste cells through hemichannels. J Neurophysiol 104:896–901. CrossRef Medline
51. Murayama N (1988) Interaction among different sensory units within a single fungiform papilla in the frog tongue. J Gen Physiol 91:685–701. CrossRef Medline
52. Nagai T, Kim DJ, Delay RJ, Roper SD (1996) Neuromodulation of transduction and signal processing in the end organs of taste. Chem Senses 21: 353–365. CrossRef Medline
53. Nagy JI, Goedert M, Hunt SP, Bond A (1982) The nature of the substance P-containing nerve fibres in taste papillae of the rat tongue. Neuroscience 7:3137–3151. CrossRef Medline
54. Nishimoto T, Akai M, Inagaki S, Shiosaka S, Shimizu Y, Yamamoto K, Senba E, Sakanaka M, Takatsuki K, Hara Y, Takagi H, Matsuzaki T, Kawai Y, Tohyama M (1982) On the distribution and origins of substance P in the papillae of the rat tongue: an experimental and immunohistochemical study. J Comp Neurol 207:85–92. CrossRef Medline
55. Oka Y, Butnaru M, von Buchholtz L, Ryba NJ, Zuker CS (2013) High salt recruits aversive taste pathways. Nature 494:472–475. CrossRef Medline
56. Pokabla MJ, Dickerson IM, Papka RE (2002) Calcitonin gene-related peptide-receptor component protein expression in the uterine cervix, lumbosacral spinal cord, and dorsal root ganglia. Peptides 23:507–514. CrossRef Medline
57. Prado MA, Evans-Bain B, Oliver KR, Dickerson IM (2001) The role of the CGRP-receptor component protein (RCP) in adrenomedullin receptor signal transduction. Peptides 22:1773–1781. CrossRef Medline
58. Reich A, Orda A, Wiśnicka B, Szepietowski JC (2007) Plasma concentration of selected neuropeptides in patients suffering from psoriasis. Exp Dermatol 16:421–428. CrossRef Medline
59. Rettinger J, Schmalzing G (2004) Desensitization masks nanomolar potency of ATP for the P2X1 receptor. J Biol Chem 279:6426–6433. CrossRef Medline
60. Riddle DR, Hughes SE, Belczynski CR, DeSibour CL, Oakley B (1990) Inhibitory interactions among rodent taste axons. Brain Res 533:113–124. CrossRef Medline
61. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS (2007) Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBOJ 26:657–667. CrossRef Medline
62. Roper SD (1989) The cell biology of vertebrate taste receptors. Annu Rev Neurosci 12:329–353. CrossRef Medline
63. Roper SD (2014) TRPs in taste and chemesthesis. Handb Exp Pharmacol 223:827–871. CrossRef Medline
64. Rosenblatt MI, Dahl GP, Dickerson IM (2000) Characterization and localization of the rabbit ocular calcitonin gene-related peptide (CGRP)-receptor component protein (RCP). Invest Ophthalmol Vis Sci 41: 1159–1167. Medline
65. Sardi C, Zambusi L, Finardi A, Ruffini F, Tolun AA, Dickerson IM, Righi M, Zacchetti D, Grohovaz F, Provini L, Furlan R, Morara S (2014) Involvement of calcitonin gene-related peptide and receptor component protein in experimental autoimmune encephalomyelitis. J Neuroimmunol 271: 18–29. CrossRef Medline
66. Silverman JD, Kruger L (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J Comp Neurol 280:303–330. CrossRef Medline
67. Silverman JD, Kruger L (1990) Analysis of taste bud innervation based on glycoconjugate and peptide neuronal markers. J Comp Neurol 292: 575–584. CrossRef Medline
68. Simon SA, Liu L, Erickson RP (2003) Neuropeptides modulate rat chorda tympani responses. Am J Physiol Regul Integr Comp Physiol 284: R1494–R1505. CrossRef Medline
69. Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, Adrien L, Zhao H, Leung S, Abernethy M, Koppel J, Davies P, Civan MM, Chaudhari N, Matsumoto I, Hellekant G, Tordoff MG, Marambaud P, Foskett JK (2013) CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 495:223–226. CrossRef Medline
70. Vandenbeuch A, Pillias AM, Faurion A (2004) Modulation of taste peripheral signal through interpapillar inhibition in hamsters. Neurosci Lett 358:137–141. CrossRef Medline
71. Vandenbeuch A, Tizzano M, Anderson CB, Stone LM, Goldberg D, Kinnamon SC (2010) Evidence for a role of glutamate as an efferent transmitter in taste buds. BMC Neurosci 11:77. CrossRef Medline
72. Vandenbeuch A, Anderson CB, Parnes J, Enjyoji K, Robson SC, Finger TE, Kinnamon SC (2013) Role of the ectonucleotidase NTPDase2 in taste bud function. Proc Natl Acad Sci U S A 110:14789–14794. CrossRef Medline
73. Vandenbeuch A, Larson ED, Anderson CB, Smith SA, Ford AP, Finger TE, Kinnamon SC (2015) Postsynaptic P2X3-containing receptors in gustatory nerve fibres mediate responses to all taste qualities in mice. J Physiol 593:1113–1125. CrossRef Medline
74. Vandewauw I, Owsianik G, Voets T (2013) Systematic and quantitative mRNA expression analysis of TRP channel genes at the single trigeminal and dorsal root ganglion level in mouse. BMC Neurosci 14:21. CrossRef Medline
75. Walker CS, Conner AC, Poyner DR, Hay DL (2010) Regulation of signal transduction by calcitonin gene-related peptide receptors. Trends Pharmacol Sci 31:476–483. CrossRef Medline
76. Wang Y, Erickson RP, Simon SA (1995) Modulation of rat chorda tympani nerve activity by lingual nerve stimulation. J Neurophysiol 73:1468–1483. Medline
77. Willis WD Jr (1999) Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 124:395–421. CrossRef Medline
78. Yamasaki H, Kubota Y, Takagi H, Tohyama M (1984) Immunoelectronmicroscopic study on the fine structure of substance-P-containing fibers in the taste buds of the rat. J Comp Neurol 227:380–392. CrossRef Medline