Glutamate- and GABA-mediated neuron-satellite cell interaction in nodose ganglia as revealed by intracellular calcium imaging

Histochemistry and Cell Biology

Volumn 134, Issue 1, 2010, Pages 13-22

  Shoji, Yuko ^a   Yamaguchi Yamada, Misuzu ^a   Yamamoto, Yoshio ^a  

^a IWATE UNIVERSITY   (Japan)

Author keywords

GABA; Glutamate; Nodose ganglion; Satellite cell; Sensory neuron

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; BICUCULLINE; CALCIUM ION; GENE PRODUCT; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL INTERACTION; CELL ISOLATION; CELL STRUCTURE; CONTROLLED STUDY; GLIA CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVE CELL; NERVE CELL STIMULATION; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SATELLITE CELL; SCANNING ELECTRON MICROSCOPY; SENSORY NERVE CONDUCTION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, SCANNING; NEURONS; NODOSE GANGLION; RATS; RATS, WISTAR; SATELLITE CELLS, PERINEURONAL;

EID: 77954215391     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-010-0711-0     Document Type: Article

References (49)

1. FJ Alvarez B Taylor-Blake REW Fyffe AL De Blas AR Light 1996 Distribution of immunoreactivity for the beta 2 and beta 3 subunits of the GABAA receptor in the mammalian spinal cord J Comp Neurol 365 392 412 10.1002/(SICI)1096- 9861(19960212)365:3<392::AID-CNE5>3.0.CO;2-# 1:CAS:528:DyaK28Xhs1Slsrw%3D 8822178
2. H Arumuga JV Denisova RL Neve RA Corriveau AB Belousov 2008 Use of calcium imaging for analysis of neuronal gap junction coupling Neurosci Lett 445 26 30 10.1016/j.neulet.2008.08.075
3. P Barbaresi G Gazzanelli M Malatesta 2001 γ-Aminobutyric acid transporters in the cat periaqueductal gray: a light and electron microscopic immunocytochemical study J Comp Neurol 429 337 354 10.1002/1096-9861(20000108) 429:2<337::AID-CNE12>3.0.CO;2-Z 1:CAS:528:DC%2BD3cXptVags7k%3D 11116224
4. UV Berger MS Hediger 2000 Distribution of the glutamate transporters GLAST and GLT-1 in rat circumventricular organs, meninges, and dorsal root ganglia J Comp Neurol 421 385 399 10.1002/(SICI)1096-9861(20000605)421:3<385: :AID-CNE7>3.0.CO;2-S 1:CAS:528:DC%2BD3cXjtlKlt7k%3D 10813794 (Pubitemid 30253401)
5. KN Browning D Mendelowitz 2002 Musings on the wanderer: what's new in our understanding of vago-vagal reflexes? II. Integration of afferent signaling from the viscera by the nodose ganglia Am J Physiol Gastrointest Liver Physiol 284 G8 G14
6. B Canning N Mori SB Mazzone 2006 Vagal afferent nerves regulating the cough reflex Respir Physiol 152 223 242
7. SM Carlton GL Hargett 2007 Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells J Comp Neurol 501 780 789 10.1002/cne.21285 1:CAS:528:DC%2BD2sXltFWgsL8%3D 17299761
8. VA Carozzi A Canta N Oggioni C Ceresa P Marmiroli J Konvalinka C Zoia M Bossi C Ferrarese G Tredici G Cavaletti 2008 Expression and distribution of 'high affinity' glutamate transporters GLT1, GLAST, EAAC1 and of GCPII in the rat peripheral nervous system J Anat 213 539 546 19014361
9. S Ceruti M Fumagalli G Villa C Verderio MP Abbracchio 2008 Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures Cell Calcium 43 576 590 10.1016/j.ceca.2007.10.003 1:CAS:528: DC%2BD1cXlvF2rtb8%3D 18031810 (Pubitemid 351663988)
10. I Chambille O Rampin 2002 AMPA glutamatergic receptor-immunoreactive subunits are expressed in lumbosacral neurons of the spinal cords and neurons of the dorsal root and pelvic ganglia controlling pelvic functions in the rat Brain Res 933 66 80 10.1016/S0006-8993(02)02309-0 1:CAS:528:DC%2BD38XisV2lsb0%3D 11929637 (Pubitemid 34258536)
11. A Charles 1998 Intercellular calcium waves in glia Glia 24 39 49 10.1002/(SICI)1098-1136(199809)24:1<39::AID-GLIA5>3.0.CO;2-W 1:STN:280:DyaK1czmsFyntw%3D%3D 9700488 (Pubitemid 28370211)
12. Y Chen X Zhang C Wang G-W Li Y Gu L-YM Huang 2008 Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons Proc Natl Acad Sci USA 105 16773 16778 10.1073/pnas.0801793105 1:CAS:528:DC%2BD1cXhtlers73F 18946042
13. PJ Conn J-P Pin 1997 Pharmacology and functions of metabotropic glutamate receptors Annu Rev Pharmacol Toxicol 37 205 237 10.1146/annurev.pharmtox.37.1. 205 1:CAS:528:DyaK2sXisl2ktr0%3D 9131252
14. 5 metabotropic glutamate receptor activation in neonatal rat cultured dorsal root ganglia neurons Neuropharmacol 39 621 630 10.1016/S0028-3908(99)00167-7 1:CAS:528:DC%2BD3cXhtFWqsrc%3D (Pubitemid 30089312)
15. K Czaja RC Ritter GA Burns 2006 N-Methyl-d-asparate receptor subunit phenotypes of vagal afferent neurons in nodose ganglia of the rat J Comp Neurol 496 877 885 10.1002/cne.20955 1:CAS:528:DC%2BD28Xlt1Kmt7g%3D 16628619
16. T Fellin 2009 Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity J Neurochem 108 533 544 10.1111/j.1471-4159.2008.05830.x 1:CAS:528:DC%2BD1MXhvFGhsLs%3D 19187090
17. EL Fletcher MJ Clark JB Furness 2002 Neuronal and glial localization of GABA transporter immunoreactivity in the myenteric plexus Cell Tissue Res 308 339 346 10.1007/s00441-002-0566-3 1:CAS:528:DC%2BD38Xks1Srsrg%3D 12107427 (Pubitemid 34666960)
18. RD Foreman C Qin 2009 Neuromodulation of cardiac pain and cerebral vasculature: neural mechanisms Cleve Clin J Med 76 S75 S79 10.3949/ccjm.76.s2.15 19376989
19. PB Guthrie J Knappenberger M Segal MV Bennett AC Charles SB Kater 1999 ATP released from astrocytes mediates glial calcium waves J Neurosci 19 520 528 1:CAS:528:DyaK1MXltlagsA%3D%3D 9880572
20. M Hanani 2005 Satellite glial cells in sensory ganglia: from form to function Brain Res Rev 48 457 476 10.1016/j.brainresrev.2004.09.001 1:CAS:528:DC%2BD2MXks1Cksrk%3D 15914252 (Pubitemid 40725401)
21. H Hayasaki Y Sohma K Kanbara K Maemura T Kubota M Watanabe 2006 A local GABAergic system within rat trigeminal ganglion cells Eur J Neurosci 23 745 757 10.1111/j.1460-9568.2006.04602.x 1:STN:280:DC%2BD287gtVanug%3D%3D 16487155
22. T-Y Huang V Belzer M Hanani 2010 Gap junctions in dorsal root ganglia: possible contribution to visceral pain Eur J Pain 14 49e1 49e11 10.1016/j.ejpain.2009.02.005
23. D Julius AI Basbaum 2001 Molecular mechanisms of nociception Nature 413 203 210 10.1038/35093019 1:CAS:528:DC%2BD3MXntVyjsr0%3D 11557989 (Pubitemid 32867885)
24. M Kato-Negishi K Muramoto M Kawahara R Hosoda Y Kuroda M Ichikawa 2003 Bicuculline induces synapse formation on primary cultured accessory olfactory bulb neurons Eur J Neurosci 18 1343 1352 10.1046/j.1460-9568.2003.02901.x 14511315 (Pubitemid 37215090)
25. 2+ oscillations: involvement of ATP release in astrocytes FEBS J 277 286 292 10.1111/j.1742-4658. 2009.07438.x 1:CAS:528:DC%2BC3cXptVWjtQ%3D%3D 19895581
26. S Koizumi K Fujishita M Tsuda Y Shigemoto-Mogami K Inoue 2003 Dynamic inhibition of excitatory synaptic transmission by astrocyte-derived ATP in hippocampal cultures Proc Natl Acad Sci USA 100 11023 11028 10.1073/pnas. 1834448100 1:CAS:528:DC%2BD3sXnslynurY%3D 12958212 (Pubitemid 37140146)
27. EB Malarkey V Parpura 2008 Mechanisms of glutamate release from astrocytes Neurochem Int 52 142 154 10.1016/j.neuint.2007.06.005 1:CAS:528:DC%2BD2sXhsVCjt7fK 17669556 (Pubitemid 350235693)
28. S Matsuda J Desaki J Aburaya M Sakanaka 1997 Perikaryal projections of developing spinal ganglion neurons in the chick demonstrated by scanning electron microscopy Anat Embryol 195 137 146 10.1007/s004290050032 1:STN:280:DyaK2s7pslKrtQ%3D%3D 9045983 (Pubitemid 27087056)
29. A Minelli S DeBiasi NC Brecha LV Zuccarello F Conti 1996 GAT-3, a high-affinity GABA plasma membrane transporter, is localized to astrocytic processes, and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex J Neurosci 16 6255 6264 1:CAS:528:DyaK28Xntlegsb8%3D 8815906
30. E Pannese M Ledda V Conte P Procacci 1990 The perikaryal projections of rabbit spinal ganglion neurons. A comparison of thin section reconstructions and scanning microscopy views Anat Embryol 181 427 432 10.1007/BF02433789 1:STN:280:DyaK3czitV2msg%3D%3D 2372130 (Pubitemid 20312814)
31. E Pannese M Ledda V Conte P Procacci S Matsuda 1990 Scanning electron-microscope observations of the perikaryal projections of rabbit spinal ganglion neurons after enzymatic removal of connective tissue and satellite cells Cell Tissue Res 260 167 173 10.1007/BF00297502 1:STN:280: DyaK3c3lsVOrtw%3D%3D 2160330
32. E Pannese M Ledda PS Cherkas TY Huang M Hanani 2003 Satellite cell reactions to axon injury of sensory ganglion neurons: increase in number of gap junctions and formation of bridges connecting previously separate perineuronal sheaths Anat Embryol 206 337 347 1:STN:280:DC%2BD3s7nvVCntg%3D%3D 12698360
33. V Parpura PG Haydon 2000 Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons Proc Natl Acad Sci USA 97 8629 8634 10.1073/pnas.97.15.8629 1:CAS:528:DC%2BD3cXlt1GnsL8%3D 10900020 (Pubitemid 30639724)
34. V Parpura F Liu KS Jeftinija PG Haydon SD Jeftinija 1995 Neuroligand-evoked calcium-dependent release of excitatory amino acid from Schwann cells J Neurosci 15 5831 5839 1:CAS:528:DyaK2MXnsVOrtL8%3D 7643223
35. L Pasti T Pozzan G Carmignoto 1995 Long-lasting changes of calcium oscillations in astrocytes J Biol Chem 270 15203 15210 10.1074/jbc.270.25.15203 1:CAS:528:DyaK2MXmsFKqt7g%3D 7797504
36. J-P Pin J Bockaert 1989 Two distinct mechanisms, differentially affected by excitatory amino acids, trigger GABA release from fetal mouse striatal neurons in primary culture J Neurosci 9 648 656 1:CAS:528:DyaL1MXht12itLs%3D 2918382
37. N Schaffar H Rao JP Kessler A Jean 1997 Immunohistochemical detection of glutamate in rat vagal sensory neurons Brain Res 778 302 308 10.1016/S0006-8993(97)01058-5 1:CAS:528:DyaK2sXnvFGls78%3D 9459547 (Pubitemid 28037410)
38. JA Slattery JA Page CL Dorian SM Brierley LA Blackshaw 2006 Potentiation of mouse vagal afferent mechanosensitivity by ionotropic and metabotropic glutamate receptors J Physiol 577 295 306 10.1113/jphysiol.2006.117762 1:CAS:528:DC%2BD28Xht1yqsL3N 16945965 (Pubitemid 44698256)
39. E Sokolova A Nistri R Giniatullin 2001 Negative cross talk between anionic GABAA and cationic P2X ionotropic receptors of rat dorsal root ganglion neurons J Neurosci 21 4958 4968 1:CAS:528:DC%2BD3MXkvFSkurY%3D 11438571
40. II Stoyanova 2004 γ-Aminobutiric acid immunostaining in trigeminal, nodose and spinal ganglia of the cat Acta Histochem 106 309 314 15350813
41. AN van den Pol 1992 Calcium excitability and oscillations in suprachiasmatic nucleus neuron and glia in vitro J Neurosci 12 2648 2664 1351936
42. A Verkhratsky F Kirchhoff 2007 Glutamate-mediated neuronal-glial transmission J Anat 210 651 660 10.1111/j.1469-7580.2007.00734.x 1:CAS:528:DC%2BD2sXotFymurs%3D 17504269 (Pubitemid 46851000)
43. JP Vit PT Ohara C Sundberg B Rubi P Maechler C Liu M Puntel P Lowenstein M Castro L Jasmin 2009 Adenovector GAD65 gene delivery into the rat trigeminal ganglion produces orofacial analgesia Mol Pain 5 42 10.1186/1744-8069-5-42 19656360
44. M Weick PS Cherkas W Härtig T Pannicke O Uckermann A Bringmann M Tal A Reichenbach M Hanani 2003 P2 receptors in satellite glial cells in trigeminal ganglia of mice Neuroscience 120 969 977 10.1016/S0306-4522(03)00388-9 1:CAS:528:DC%2BD3sXmt1WrsL0%3D 12927203 (Pubitemid 36966649)
45. H Willcockson J Valtschanoff 2008 AMPA and NMDA glutamate receptors are found in both peptidergic and non-peptidergic primary afferent neurons in the rat Cell Tissue Res 334 17 23 10.1007/s00441-008-0662-0 1:CAS:528: DC%2BD1cXhtFSnu7bL 18679721
46. Y Xiao JA Richter JH Hurley 2008 Release of glutamate and CGRP from trigeminal ganglion neurons: role of calcium channels and 5-HT1 receptor signaling Mol Pain 4 21 10.1186/1744-8069-4-12 (Pubitemid 351622384)
47. J Xu H Peng N Kang Z Zhao JH-C Lin PK Stanton J Kang 2007 Glutamate-induced exocytosis of glutamate from astrocytes J Biol Chem 282 24185 24197 10.1074/jbc.M700452200 1:CAS:528:DC%2BD2sXoslOntbY%3D 17584743 (Pubitemid 47328058)
48. 2+ oscillation in hippocampal astrocytes during metabotropic glutamate receptor activation J Pharmacol Sci 97 212 218 10.1254/jphs.FP0040722 1:CAS:528:DC%2BD2MXhvFKlsbY%3D 15684567 (Pubitemid 40410261)
49. X Zhang Y Chen C Wang L-YM Huang 2007 Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia Proc Natl Acad Sci USA 104 9864 9869 10.1073/pnas.0611048104 1:CAS:528: DC%2BD2sXmsFSmtr0%3D 17525149 (Pubitemid 47175357)