Immunocytochemical analysis of P2X2 in rat circumvallate taste buds

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Yang, Ruibiao ^a,b   Montoya, Alana ^a,b   Bond, Amanda ^a,b   Walton, Jenna ^a,b   Kinnamon, John C ^a,b  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; IONOTROPIC RECEPTOR; PHENYLENEDIAMINE; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; SEROTONIN; SYNTAXIN 1;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BITTER TASTE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOGOLD ELECTRON MICROSCOPY; MALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SWEETNESS; SYNAPTIC TRANSMISSION; TASTE BUD;

5-HYDROXYTRYPTOPHAN; ANIMALS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NERVE FIBERS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X2; SEROTONIN; SYNAPSES; SYNTAXIN 1; TASTE BUDS;

EID: 84861337308     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-51     Document Type: Article

References (64)

1. Kinnamon JC, Sherman TA, Roper SD. Ultrastructure of mouse vallate taste buds: III. Patterns of synaptic connectivity. J Comp Neurol 1988, 270:1-10. 10.1002/cne.902700102, 3372731.
2. Kinnamon JC, Taylor BJ, Delay RJ, Roper SD. Ultrastructure of mouse vallate taste buds. I. Taste cells and their associated synapses. J Comp Neurol 1985, 235:48-60. 10.1002/cne.902350105, 3989005.
3. Kinnamon JC, Yang R. Ultrastructure of Taste Buds, In: " The Senses: A Comprehensive Reference" G. Beachamp (ed.). Elsevier (New York) 2007,
4. Pumplin DW, Yu C, Smith DV. Light and dark cells of rat vallate taste buds are morphologically distinct cell types. J Comp Neurol 1997, 378:389-410. 10.1002/(SICI)1096-9861(19970217)378:3<389::AID-CNE7>3.0.CO;2-#, 9034899.
5. Smith DV, Klevitsky R, Akeson RA, Shipley MT. Taste bud expression of human blood group antigens. J Comp Neurol 1994, 343:130-142. 10.1002/cne.903430110, 8027431.
6. Ohmura S, Horimoto S, Fujita K. Lectin cytochemistry of the dark granules in the type 1 cells of Syrian hamster circumvallate taste buds. Arch Oral Biol 1989, 34(3):161-166. 10.1016/0003-9969(89)90003-4, 2818266.
7. Bartel DL, Sullivan SL, Lavoie EG, Sévigny J, Finger TE. Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol 2006, 497(1):1-12. 10.1002/cne.20954, 2212711, 16680780.
8. Vlajkovic SM, Wang CJ, Soeller C, Zimmemann H, Thome PR, Housley GD. Activation-dependent trafficking of NTPDase2 in Chinese hamster ovary cells. Int J Biochem Cell Biol 2007, 39(4):810-817. 10.1016/j.biocel.2007.01.003, 17307380.
9. Vandenbeuch A, Clapp TR, Kinnamon SC. Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci 2008, 9:1. 10.1186/1471-2202-9-1, 2235881, 18171468.
10. Clapp TR, Stone LM, Margolskee RF, Kinnamon SC. Immunocytochemical evidence for co-expression of type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci 2001, 2:6. 10.1186/1471-2202-2-6, 31433, 11346454.
11. Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC. Morphological characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol 2004, 468:311-321. 10.1002/cne.10963, 14681927.
12. Boughter JD, Pumplin DW, Yu C, Christy RC, Smith DV. Differential expression of alpha-gustducin in taste bud populations of the rat and hamster. J Neurosci 1997, 17(8):2852-2858.
13. Yang R, Tabata S, Crowley HH, Margolskee RF, Kinnamon JC. Ultrastructural localization of gustducin immunoreactivity in microvilli of type II taste cells in the rat. J Comp Neurol 2000, 425:139-151. 10.1002/1096-9861(20000911)425:1<139::AID-CNE12>3.0.CO;2-#, 10940948.
14. Tizzano M, Dvoryanchikov G, Barrows JK, Kim S, Chaudhari N, Finger TE. Expression of Galpha14 in sweet-transducing taste cells of the posterior tongue. BMC Neurosci 2008, 9:110. 10.1186/1471-2202-9-110, 2596171, 19014514.
15. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol 2006, 4:7. 10.1186/1741-7007-4-7, 1444931, 16573824.
16. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310(5753):1495-1499. 10.1126/science.1118435, 16322458.
17. Lindemann B. Chemoreception: tyasting the sweet and bitter. Curr Biol 1996, 6:1234-1237. 10.1016/S0960-9822(96)00704-X, 8939555.
18. Yang R, Crowley HH, Rock ME, Kinnamon JC. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol 2000, 424:205-215. 10.1002/1096-9861(20000821)424:2<205::AID-CNE2>3.0.CO;2-F, 10906698.
19. Murray RG. The ultrastructure of taste buds. The ultrastructure of sensory organs 1973, 1-81. Amsterdam: North Holland Pub Co., Friedemann I.
20. Roper SD. Cell communication in taste buds. Cell Mol Life Sci 2006, 63(13):1494-1500. 10.1007/s00018-006-6112-9, 16732426.
21. Roper SD. Signal transduction and information processing in mammalian taste buds. Pflugers Arch 2007, 454(5):759-776. 10.1007/s00424-007-0247-x, 17468883.
22. Asano-Miyoshi M, Hamamichi R, Emori Y. Synaptophysin as a probable component of neurotransmission occurring in taste receptor cells. J Mol Histol 2009, 40(1):59-70. 10.1007/s10735-009-9214-5, 19253017.
23. DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, Chaudhari N. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci 2006, 26(15):3971-3980. 10.1523/JNEUROSCI.0515-06.2006, 16611813.
24. Kim D-J, Roper SD. Localization of serotonin in taste buds: a comparative study of four vertebrates. J Comp Neurol 1995, 353:364-370. 10.1002/cne.903530304, 7751436.
25. Takeda M, Suzuki Y, Obara N, Nagai Y. Neural cell adhesion molecule of taste buds. J Electron Microsc (Tokyo) 1992, 41(5):375-380.
26. Yang R, Cristi CL, Kinnamon JC. Synaptobrevin-2-like immunoreactivity is associated with vesicles at synapses in rat circumvallate taste buds. J Comp Neurol 2004, 471:59-71. 10.1002/cne.20021, 14983476.
27. Yang R, Ma H, Thomas SM, Kinnamon JC. Immunocytochemical analysis of syntaxin-1 in rat circumvallate taste buds. J Comp Neurol 2007, 502(6):883-893. 10.1002/cne.21317, 17447252.
28. Yee CL, Yang R, Böttger B, Finger TE, Kinnamon J. " Type III" cells of rat taste buds: Immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol 2001, 440:97-108. 10.1002/cne.1372, 11745610.
29. Huang YA, Dando R, Roper SD. Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J Neurosci 2009, 29(44):13909-13918. 10.1523/JNEUROSCI.2351-09.2009, 2821712, 19890001.
30. Huang YJ, Maruyama Y, Lu KS, Pereira E, Plonsky I, Baur JE, Wu D, Roper SD. Mouse taste buds use serotonin as a neurotransmitter. J Neurosci 2005, 25(4):843-847. 10.1523/JNEUROSCI.4446-04.2005, 15673664.
31. Huang YA, Maruyama Y, Roper SD. Norepinephrine is coreleased with serotonin in mouse taste buds. J Neurosci 2008, 28(49):13088-13093. 10.1523/JNEUROSCI.4187-08.2008, 3331792, 19052199.
32. Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Tränkner D, Ryba NJ, Zuker CS. The cells and logic for mammalian sour taste detection. Nature 2006, 442(7105):934-938. 10.1038/nature05084, 1571047, 16929298.
33. Kataoka S, Yang R, Ishimaru Y, Matsunami H, Sévigny J, Kinnamon JC, Finger TE. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses 2008, 33(3):243-254. 2642677, 18156604.
34. Kinnamon SC, Margolskee RF. Mechanisms of taste transduction. Curr Opin Neuobiol 1996, 6(4):506-513.
35. Margolskee RF. Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 2002, 277(1):1-4.
36. Wong GT, Gannon KS, Margolskee RF. Transduction of bitter and sweet taste by gustducin. Nature 1996, 381(6585):796-800. 10.1038/381796a0, 8657284.
37. Burnstock G. The past present and future of purine nucleotides as signaling molecules. Neuropharmacology 1997, 36:1127-1139. 10.1016/S0028-3908(97)00125-1, 9364468.
38. Burnstock G. P2X2 receptors in sensory neurons. Br J Anaesth 2000, 84(4):476-488. 10.1093/oxfordjournals.bja.a013473, 10823099.
39. Burnstock G. Purinergic P2 receptors as target for novel analgesics. Pharmacol Therap 2006, 110:433-454.
40. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 1998, 50(3):413-492.
41. Bo X, Alavi A, Xiang Z, Oglesby I, Ford A, Burnstock G. Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 1999, 10(5):1107-1111. 10.1097/00001756-199904060-00037, 10321492.
42. Ishida Y, Ugawa S, Ueda T, Yamada T, Shibata Y, Hondoh A, Inoue K, Yu Y, Shimada S. 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 2009, 514(2):131-144. 10.1002/cne.22000, 19266560.
43. Kataoka S, Toyono T, Seta Y, Toyoshima K. Expression of ATP-gated P2X3 receptors in rat gustatory papillae and taste buds. Arch Histol Cytol 2006, 69(4):281-288. 10.1679/aohc.69.281, 17287582.
44. Eddy MC, Eschle BK, Barrows J, Hallock RM, Finger TE, Delay ER. Double P2X2/P2X3 purinergic receptor knockout mice do not taste NaCI or the artificial sweetener SC45647. Chem Senses 2009, 34(9):789-297. 10.1093/chemse/bjp068, 2762055, 19833661.
45. Hallock RM, Tatangelo M, Barrows J, Finger TE. Residual chemosensory capabilities in double P2X2/P2X3 purinergic receptor null mice: intraoral or postingestive detection?. Chem Senses 2009, 34(9):799-808. 10.1093/chemse/bjp069, 2762056, 19833662.
46. Staikopoulos V, Sessle BJ, Furness JB, Jennings EA. Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons. Neuroscience 2007, 144(1):208-216. 10.1016/j.neuroscience.2006.09.035, 1861813, 17110047.
47. Hayato R, Ohtubo Y, Yoshii K. Functional expression of ionotropic purinergic receptors on mouse taste bud cells. J Physiol 2007, 584(2):473-488. 10.1113/jphysiol.2007.138370, 2277161, 17702819.
48. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 2007, 104(15):6436-6441. 10.1073/pnas.0611280104, 1851090, 17389364.
49. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 2007, 26(3):657-667. 10.1038/sj.emboj.7601526, 1794384, 17235286.
50. Green DE, Baum H. Energy and the Mitochondrion 1970, New York: Academic.
51. Korman EF, Addink ADF, Wakabayashi T, Green DE. A unified model of mitochondrial morphology. Bioenergetics 1970, 1:9-32.
52. Royer SM, Kinnamon JC. Ultrastructure of mouse foliate taste buds: synaptic and nonsynaptic interactions between taste cells and nerve fibers. J Comp Neurol 1988, 270(1):11-24. 10.1002/cne.902700103, 3372732.
53. William CH, Vail WJ, Harris RA, Caldwell M, Green DE, Valdivia E. Conformational basis of energy transduction in membrane systems. VIII. Configurational changes of mitochondria in situ and in vitro. Bioenergetics 1970, 1:147-180.
54. Huang YA, Stone LM, Pereira E, Yang R, Kinnamon JC, Dvoryanchikov G, Chaudhari N, Finger TE, Kinnamon SC, Roper SD. Knocking out P2X receptors reduces transmitter secretion in taste buds. J Neurosci 2011, 31(38):13654-13661. 10.1523/JNEUROSCI.3356-11.2011, 3188419, 21940456.
55. Ma H, Yang R, Thomas SM, Kinnamon JC. Qualitative and quantitative differences between taste buds of the rat and mouse. BMC Neuroscience 2007, 8:49. 10.1186/1471-2202-8-49, 1931605, 17610722.
56. Yang R, Bond A, Thomas S, Kinnamon JC. Pannexin-1 and connexin-43 immunoreactivity in rodent taste buds. Chem Senses 2010, 35(7):531-A79.
57. Gilkerson RW, Sellker JM, Capaldi RA. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett 2003, 546(2-3):355-358.
58. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 2004, 64(3):985-993. 10.1158/0008-5472.CAN-03-1101, 14871829.
59. Hajnóczky G, Csordás G, Krishnamurthy R, Szalai G. Mitochondrial calcium signaling driven by the IP3 receptor. J Bioenerg Biomembr 2000, 32(1):15-25. 10.1023/A:1005504210587, 11768758.
60. Hawkins BJ, Solt LA, Chowdhury I, Kazi AS, Abird MR, Aird WC, May MJ, Foskett JK, Madesh M. G protein-coupled receptor Ca2 + -linked mitochondrial reactive oxygen species are essential for endothelial/leukocyte adherence. Mol Cell Biol 2007, 27(21):7582-7593. 10.1128/MCB.00493-07, 2169045, 17724077.
61. Hisatsune C, Yasumatsu K, Takahashi-Iwanaga H, Ogawa N, Kuroda Y, Yoshida R, Ninomiya Y, Mikoshiba K. Abnomal taste perception in mice lacking the type 3 inositol 1,4,5-trisphosphate receptor. J Bio Chem 2007, 282(51):37225-37231.
62. Inoue A, Obata K, Akagawa K. Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen HPC-1. J Biol Chem 1992, 267(15):10613-10619.
63. Wei XY, Liu JP, Zhao CH, Ju G, Wong-Riley MT, Liu YY. Expressions of 5-HT/5-HT(2A) receptors and phospho-protein kinase C theta in the pre-Bötzinger complex in normal and chronic intermittent hypoxic rats. Neuroscience 2010, 168(1):61-73. 10.1016/j.neuroscience.2010.03.023, 20303395.
64. Crowley HH, Kinnamon JC. Transmission electron microscopy of gustatory epithelium. Experimental cell biology of taste and olfaction: current techniques and protocols 1995, 105-114. Boca Raton: CRC Press, Spielman AI, Brand JG.