Expression of Kainate Glutamate Receptors in Type II Cells in Taste Buds of Rats

  • Lee, Sang-Bok (Department of Physiology and Neuroscience, College of Dentistry, Kangnung National University) ;
  • Lee, Cil-Han (Department of Physiology and Neuroscience, College of Dentistry, Kangnung National University) ;
  • Cho, Young-Kyung (Department of Physiology and Neuroscience, College of Dentistry, Kangnung National University) ;
  • Chung, Ki-Myung (Department of Physiology and Neuroscience, College of Dentistry, Kangnung National University) ;
  • Kim, Kyung-Nyun (Department of Physiology and Neuroscience, College of Dentistry, Kangnung National University)
  • Published : 2008.09.30

Abstract

Glutamate-induced cobalt uptake reveals non-NMDA glutamate receptors (GluRs) in rat taste bud cells. Previous studies suggest that glutamate-induced cobalt uptake in taste cells occurs mainly via kainate type GluRs. Cobaltstained cells were immunoreactive against GluR6 and KA1 subunits of GluRs. However, the functions of those type of receptors are not known yet. It is important question which types of taste cells are cobalt-stained when stimulated by glutamate and whether they express these kinds of GluRs. Circumvallate and foliate papilla of Sprague-Dawley rats (45-60 days old) were used. A cobalt-staining technique combined with immunohistochemistry against specific markers for taste bud cell types, such as blood group H antigen (BGH), $\alpha$-gustducin (Gus), or neural cell adhesion molecule (NCAM) was employed. We also performed double labeling of GluR6 or KA1 subunits of GluR with each specific marker for taste bud cell types. Lots of cobaltstained taste bud cells expressed Gus-like immunoreactivity, and subsets of the cobalt stained cells appeared NCAM- or BGH-like immunoreactivity. Stimulation with 1 mM glutamate significantly increased the number of cobaltstained cells in Gus-like immunoreactive cells, but not in NCAM- or BGH-like immunoreactive cells. In the double labeling experiments, GluR6 and KA1 subunits of GluRs were mainly expressed with Gus. These results suggest that kainate glutamate receptors preferentially expressed in type II taste bud cells in rat.

Keywords

References

  1. 김경년, 천상우.: 특수감각, 전국치과대학(원)생리학 교수 협의회 저 , 치의학을 위한 생리학 , pp 403-414, 대한나래 출판사, 서울, 2005
  2. Bigiani A.: Mouse taste cells with glialike membrane properties. J Neurophysiol. 2001; 85: 1552-1560 https://doi.org/10.1152/jn.2001.85.4.1552
  3. Boughter Jr JD, Pumplin DW, Yu C, Christy RC, and Smith DV.: Differential expression of alpha-gustducin in taste bud populations of the rat and hamster. J Neurosci. 1997; 17: 2852?2858
  4. Bowie D.: External anions and cations distinguish between AMPA and kainate receptor gating mechanisms.; J Physiol (London).;2002; 539:725-733 https://doi.org/10.1113/jphysiol.2001.013407
  5. Bradlley RM, King MS, Wang L, and Shu X.: Neurotransmitter and neuromodulator activity in the gustatory zone of the nucleustractus solitarius. Chem Sens. 1996; 21: 377-385 https://doi.org/10.1093/chemse/21.3.377
  6. Caicedo A, Kim KN, and Roper SD.: Glutamate-induced cobalt uptake reveals non-NMDA receptors in rat taste cells. J Comp Neurol. 2000; 417: 315-324 https://doi.org/10.1002/(SICI)1096-9861(20000214)417:3<315::AID-CNE5>3.0.CO;2-1
  7. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, and Henley JM.: Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature. 1993; 79: 78-816
  8. Chung KM, Chang JH, Park IW, Cho YK, Lee HS, and Kim KN.: Expression of AMPA and kainate receptor subunits in taste cells of rats. Int J Oral Biol. 2004; 29: 145-147
  9. Chung KM, Lee SB, Heur R, Cho YK, Lee CH, Jung HY, Chung SH, Lee SP, and Kim KN.: Glutamate-induced cobalt uptake elicited by kainate receptors in rat taste bud cells. Chem Senses. 2005; 30: 137-143 https://doi.org/10.1093/chemse/bji009
  10. DeFazio RA, Dvoryanchikov G,. Maruyama Y, Kim JW, Pereira E, Roper SD, and Chaudhari N.: Seperate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006; 26: 3971-3980 https://doi.org/10.1523/JNEUROSCI.0515-06.2006
  11. Dingledine R, and Conn PJ.: Peripheral Glutamate Receptors: molecular biology and role in taste sensation. J Nutr. 2000; 130: 1039S-1042S
  12. Farbmann AI.: Fine structure of taste bud. J Ultrastruct Res. 1965; 12: 328-350 https://doi.org/10.1016/S0022-5320(65)80103-4
  13. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, and Kinnamon SC.: ATP Signaling Is Crucial for Communication from Taste Buds to Gustatory Nerves. Science. 2005; 310: 1495-1499 https://doi.org/10.1126/science.1118435
  14. Herness MS, and Chen Y.: Serotonin inhibits calciumactivated $K^{+}$ current in rat taste recepter cells. NeuroReport. 1997; 8: 3527-3261 https://doi.org/10.1097/00001756-199711100-00022
  15. Herness MS, Zhao FL, Lu SG, Kaya N, Shen T, and Sun XD.: Adrenergic signaling between rat taste recepter cells. J Physiol (Lond). 2002; 543: 601-614 https://doi.org/10.1113/jphysiol.2002.020438
  16. Huang YJ, Maruyama Y, Lu KS, Pereira E, Plonsky I, Baur JE, Wu D, and Roper SD.: Mouse taste buds use serotonin as a neurotransmitter. J Neurosci. 2005; 25: 843-847 https://doi.org/10.1523/JNEUROSCI.4446-04.2005
  17. Jain S, and Roper SD.: Immunocytochemistry of GABA, glutamate, serotonin, and histamine in Necturus taste buds. J Comp Neurol. 1991; 307: 675-682 https://doi.org/10.1002/cne.903070412
  18. Kim KN, Caicedo A, and Roper SD.: Glutamate-induced cobalt uptake reveals non-NMDA recepters in developing rat taste buds. NeuroReport. 2001; 12: 1715-1718 https://doi.org/10.1097/00001756-200106130-00039
  19. Kim MW, Park HO, Pahng MS, Park SW, Kim SH, Jung JY, Jeong YJ, and Kim WJ.: Effect of GABA on the gustatory nucleus tractus solitarius in rats. Int J Oral Biol. 2005; 30: 91-98
  20. Lerma J.: Roles, and rules of kainate recepters in synaptic transmission. Nat Rev Neurosci. 2003; 4: 481-495 https://doi.org/10.1038/nrn1118
  21. Mayer ML.: Crystal structure of the GluR5 and GluR6 ligand binding cores: Molecular mechanisms underlying kainate receptor selectivity. Neuron. 2005; 45: 539-552 https://doi.org/10.1016/j.neuron.2005.01.031
  22. Murray RG.: The ultrastructure of taste buds. in The ultrastructure of taste organs. edited by Friedmann I, pp 1- 81, North Holland, Amsterdam, 1974
  23. Nagai T, Delay RJ, Welton J, and Roper SD.: Uptake and release of neurotransmitter candidates, [3H]serotonin, [3H]glutamate, and [3H]GABA, in taste buds of the mudpuppy, Nectrus maculosus. J Comp Neurol. 1998; 392: 199-208 https://doi.org/10.1002/(SICI)1096-9861(19980309)392:2<199::AID-CNE4>3.0.CO;2-Y
  24. Passafaro M, Nakagawa T, Sala C, and Sheng M.: GABAnergic neurotransmission in rat taste buds: immunocytochemical study for GABA and GABA transporter subtypes. Nature. 2003; 424: 677-681 https://doi.org/10.1038/nature01781
  25. Pruss RM, Akeson RL, Racke MM, and Wilburn JL.: Agonist activated cobalt uptake identifies divalent cation-permeable kainate receptors on neurons and glial cells. Neuron. 1991; 7: 509-518 https://doi.org/10.1016/0896-6273(91)90302-G
  26. Pumplin DW, Yu C, and Smith DV.: Light and dark cells of rat vallate taste buds are morphologically distinct cell types. J Comp Neurol. 1997; 378: 380?410
  27. Raphael Y, and Altschuler RA.: Structure and innervation of the cochlea. Brain Res Bull. 2003; 60: 397-422 https://doi.org/10.1016/S0361-9230(03)00047-9
  28. Roper SD.: The microphysiology of peripheral taste organs. J Neurosci. 1992; 12: 1127-1134 https://doi.org/10.1523/JNEUROSCI.12-04-01127.1992
  29. Roper SD.: Cell communication in taste buds. Cell Mol Life Sci. 2006; 63: 1494-1500 https://doi.org/10.1007/s00018-006-6112-9
  30. Song I, and Huganir RL.: Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 2002; 25: 578- 588 https://doi.org/10.1016/S0166-2236(02)02270-1
  31. Yang R, Crowley HH, Rock ME, and Kinnamon JC.: Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol. 2000; 424: 205-215 https://doi.org/10.1002/1096-9861(20000821)424:2<205::AID-CNE2>3.0.CO;2-F