Spatiotemporal and anatomical analyses of P2X receptor-mediated neuronal and glial processing of sensory signals in the rat dorsal horn

Pain

Volumn 152, Issue 9, 2011, Pages 2085-2097

  Aoyama, Ryoma ^a   Okada, Yasumasa ^a   Yokota, Shigefumi ^b   Yasui, Yutaka ^c   Fukuda, Kentaro ^a   Shinozaki, Yoshio ^a   Yoshida, Hideaki ^a   Nakamura, Masaya ^a   Chiba, Kazuhiro ^a   Yasui, Yukihiko ^b   Kato, Fusao ^c   Toyama, Yoshiaki ^a  

^a KEIO UNIVERSITY   (Japan)

^b SHIMANE UNIVERSITY   (Japan)

^c JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Astrocyte; Immunohistochemistry; Nociception; Spinal cord; Voltage imaging; Whole cell patch recording

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; POSTSYNAPTIC RECEPTOR; PROTEIN S100B; PURINERGIC P2X RECEPTOR; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DORSAL ROOT; FEMALE; GLIA CELL; GRAY MATTER; IMMUNOHISTOCHEMISTRY; LOW TEMPERATURE; MALE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROPIL; NONHUMAN; PERIKARYON; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SENSORY SYSTEM ELECTROPHYSIOLOGY; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION; TEMPERATURE DEPENDENCE; WHITE MATTER;

ANIMALS; BRAIN CHEMISTRY; FEMALE; MALE; NEUROGLIA; NEURONS; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; RECEPTORS, PURINERGIC P2X1; RECEPTORS, PURINERGIC P2X3; RECEPTORS, PURINERGIC P2X5; RECEPTORS, PURINERGIC P2X7; SENSORY RECEPTOR CELLS; SPINAL CORD; TIME FACTORS;

EID: 80051788754     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.05.014     Document Type: Article

References (76)

1. C.M. Anderson, J.P. Bergher, and R.A. Swanson ATP-induced ATP release from astrocytes J Neurochem 88 2004 246 256 (Pubitemid 38030227)
2. R. Aoyama, Y. Okada, K. Fukuda, H. Yoshida, M. Nakamura, K. Chiba, and Y. Toyama Effect of extracellular ATP on the neuronal network function of the rat spinal cord dorsal horn Neurosci Res 50 2004 64
3. R. Bardoni, A. Ghirri, M. Zonta, C. Betelli, G. Vitale, V. Ruggieri, M. Sandrini, and G. Carmignoto Glutamate-mediated astrocyte-to-neuron signalling in the rat dorsal horn J Physiol 588 2010 831 846
4. R. Bardoni, P.A. Goldstein, C.J. Lee, J.G. Gu, and A.B. MacDermott ATP P2X receptors mediate fast synaptic transmission in the dorsal horn of the rat spinal cord J Neurosci 17 1997 5297 5304
5. D.N. Bowser, and B.S. Khakh ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks J Neurosci 24 2004 8606 8620 (Pubitemid 39313783)
6. 3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor Mol Cell Neurosci 12 1998 256 268 (Pubitemid 28536078)
7. A. Brusco, L.A. Gomez, E.M. López, P. Tagliaferro, and J.P. Saavedra Relationship between glial organization and the establishment of nerve tracts in rat spinal cord Int J Neurosci 82 1995 25 31
8. G. Burnstock Physiology and pathophysiology of purinergic neurotransmission Physiol Rev 87 2007 659 797 (Pubitemid 47084682)
9. G. Burnstock Purines and sensory nerves Handb Exp Pharmacol 194 2009 333 392
10. M. Chen, and J.G. Gu A P2X receptor-mediated nociceptive afferent pathway to lamina I of the spinal cord Mol Pain 1 2005 4
11. B.A. Chizh, and P. Illes P2X receptors and nociception Pharmacol Rev 53 2001 553 568 (Pubitemid 33138210)
12. 7 receptors and downstream signaling pathways in long-term potentiation of spinal nociceptive responses Brain Behav Immun 24 2010 1176 1189
13. 7-dependent release of interleukin-1β and nociception in the spinal cord following lipopolysaccharide J Neurosci 30 2010 573 582
14. 6 receptors and the distribution and properties of an extended family of ATP-gated ion channels J Neurosci 16 1996 2495 2507 (Pubitemid 26124346)
15. R. D'Mello, and A.H. Dickenson Spinal cord mechanisms of pain Br J Anaesth 101 2008 8 16 (Pubitemid 351881902)
16. 2+ wave propagation in dorsal spinal cord astrocytes J Neurosci 20 2000 2800 2808 (Pubitemid 30220304)
17. T. Fellin, J.Y. Sul, M. D'Ascenzo, H. Takano, O. Pascual, and P.G. Haydon Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP Novartis Found Symp 276 2006 208 217
18. R.D. Fields Oligodendrocytes changing the rules: action potentials in glia and oligodendrocytes controlling action potentials Neuroscientist 14 2008 540 543
19. R.D. Fields, and G. Burnstock Purinergic signalling in neuron-glia interactions Nat Rev Neurosci 7 2006 423 436 (Pubitemid 44012283)
20. F. Fonnum, A. Johnsen, and B. Hassel Use of fluorocitrate and fluoroacetate in the study of brain metabolism Glia 21 1997 106 113 (Pubitemid 27389646)
21. Y. Fujiki, S. Yokota, Y. Okada, Y. Oku, F. Miwakeichi, Y. Tamura, and M. Ishiguro A standardization method of voltage-imaging data that enables to average and compare spatio-temporal neuronal activities obtained from different samples Neurosci Res 68 2010 e66
22. K. Fukuda, Y. Okada, H. Yoshida, R. Aoyama, M. Nakamura, K. Chiba, and Y. Toyama Ischemia-induced disturbance of neural network function in the rat spinal cord analyzed by voltage-imaging Neuroscience 140 2006 1453 1465 (Pubitemid 43928282)
23. R.E. Fyffe, and E.R. Perl Is ATP a central synaptic mediator for certain primary afferent fibers from mammalian skin? Proc Natl Acad Sci USA 81 1984 6890 6893 (Pubitemid 15221027)
24. 4 receptors and p38 MAPK in microglia Glia 57 2009 583 591
25. J.G. Gu, R. Bardoni, P.C. Magherini, and A.B. MacDermott Effects of the P2-purinoceptor antagonists suramin and pyridoxal-phosphate-6-azophenyl- 2′,4′-disulfonic acid on glutamatergic synaptic transmission in rat dorsal horn neurons of the spinal cord Neurosci Lett 253 1998 167 170 (Pubitemid 28442589)
26. J.G. Gu, and A.B. MacDermott Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses Nature 389 1997 749 753 (Pubitemid 27458964)
27. P.B. Guthrie, J. Knappenberger, M. Segal, M.V.L. Bennett, A.C. Charles, and S.B. Kater ATP released from astrocytes mediates glial calcium waves J Neurosci 19 1999 520 528 (Pubitemid 29036003)
28. N. Hamilton, S. Vayro, R. Wigley, and A.M. Butt Axons and astrocytes release ATP and glutamate to evoke calcium signals in NG2-glia Glia 58 2010 66 79
29. S. Hugel, and R. Schlichter Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons J Neurosci 20 2000 2121 2130 (Pubitemid 30230064)
30. S. Hülsmann, H. Straub, D.W. Richter, and E.J. Speckmann Blockade of astrocytes causes stimulation-induced depolarization as revealed by voltage sensitive dyes in mouse brainstem slices Exp Brain Res 150 2003 117 121 (Pubitemid 36543151)
31. H. Ikeda, M. Tsuda, K. Inoue, and K. Murase Long-term potentiation of neuronal excitation by neuron-glia interactions in the rat spinal dorsal horn Eur J Neurosci 25 2007 1297 1306 (Pubitemid 46568758)
32. R. Ikeda, Y. Takahashi, K. Inoue, and F. Kato NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain Pain 127 2007 161 172 (Pubitemid 44959439)
33. K. Inoue, F. Kato, and M. Tsuda The modulation of synaptic transmission by the glial purinergic system Open Neurosci J 4 2010 84 92
34. C.E. Jahr, and T.M. Jessell ATP excites a subpopulation of rat dorsal horn neurones Nature 304 1983 730 733 (Pubitemid 13037719)
35. Y.H. Jo, and R. Schlichter Synaptic corelease of ATP and GABA in cultured spinal neurons Nat Neurosci 2 1999 241 245 (Pubitemid 30491294)
36. 2 receptor subunit of the ATP-gated ion channels in the rat central nervous system J Comp Neurol 407 1999 11 32 (Pubitemid 29161990)
37. F. Kato, and E. Shigetomi Distinct modulation of evoked and spontaneous EPSCs by purinoceptors in the nucleus tractus solitarii of the rat J Physiol 530 2001 469 486 (Pubitemid 32162334)
38. A. Kawai, Y. Okada, K. Mckenhoff, and P. Scheid Theophylline and hypoxic ventilatory response in the rat isolated brainstem-spinal cord Respir Physiol 100 1995 25 32
39. Y. Kawamura, S. Manita, T. Nakamura, M. Inoue, Y. Kudo, and H. Miyakawa Glutamate release increases during mossy-CA3 LTP but not during Schaffer-CA1 LTP Eur J Neurosci 19 2004 1591 1600 (Pubitemid 38437921)
40. H. Kettenmann, K.H. Backus, and M. Schachner Aspartate, glutamate and gamma-aminobutyric acid depolarize cultured astrocytes Neurosci Lett 52 1984 25 29 (Pubitemid 15179720)
41. K. Kobayashi, T. Fukuoka, H. Yamanaka, Y. Dai, K. Obata, A. Tokunaga, and K. Noguchi Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord J Comp Neurol 498 2006 443 454 (Pubitemid 44232686)
42. S. Kojima, T. Nakamura, T. Nidaira, K. Nakamura, N. Ooashi, E. Ito, K. Watase, K. Tanaka, K. Wada, Y. Kudo, and H. Miyakawa Optical detection of synaptically induced glutamate transport in hippocampal slices J Neurosci 19 1999 2580 2588 (Pubitemid 29162406)
43. G. Lambrecht Agonists and antagonists acting at P2X receptors: selectivity profiles and functional implications Naunyn Schmiedebergs Arch Pharmacol 362 2000 340 350
44. K.T. Lê, P. Villeneuve, A.R. Ramjaun, P.S. McPherson, A. Beaudet, and P. Séguéla Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors Neuroscience 83 1998 177 190 (Pubitemid 28068048)
45. P. Li, A.A. Calejesan, and M. Zhuo ATP P2x receptors and sensory synaptic transmission between primary afferent fibers and spinal dorsal horn neurons in rats J Neurophysiol 80 1998 3356 3360 (Pubitemid 29029260)
46. J. Li, and E.R. Perl ATP modulation of synaptic transmission in the spinal substantia gelatinosa J Neurosci 15 1995 3357 3365
47. 7 receptor-mediated phosphoinositide 3-kinase signaling J Neurochem 113 2010 213 227
48. A.P. Lozier, and J.J. Kendig Long-term potentiation in an isolated peripheral nerve-spinal cord preparation J Neurophysiol 74 1995 1001 1009
49. N.S. Magoski, and W. Walz Ionic dependence of a P2-purinoceptor mediated depolarization of cultured astrocytes J Neurosci Res 32 1992 530 538
50. C. Molander, Q. Xu, C. Rivero-Melian, and G. Grant Cytoarchitectonic organization of the spinal cord in the rat: II. The cervical and upper thoracic cord J Comp Neurol 289 1989 375 385 (Pubitemid 19277915)
51. T. Nakagawa, K. Wakamatsu, N. Zhang, S. Maeda, M. Minami, M. Satoh, and S. Kaneko Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance Neuroscience 147 2007 445 455 (Pubitemid 46907446)
52. I. Nakamura, Y. Ohta, and O. Kemmotsu Characterization of adenosine receptors mediating spinal sensory transmission related to nociceptive information in the rat Anesthesiology 87 1997 577 584 (Pubitemid 27433007)
53. T. Nakatsuka, and J.G. Gu ATP P2X receptor-mediated enhancement of glutamate release and evoked EPSCs in dorsal horn neurons of the rat spinal cord J Neurosci 21 2001 6522 6531 (Pubitemid 32781096)
54. T. Nakatsuka, and J.G. Gu P2X purinoceptors and sensory transmission Pflügers Arch 452 2006 598 607 (Pubitemid 44015094)
55. W. Nörenberg, and P. Illes Neuronal P2X receptors: localisation and functional properties Naunyn Schmiedebergs Arch Pharmacol 362 2000 324 339
56. Y. Okada, H. Masumiya, Y. Tamura, and Y. Oku Respiratory and metabolic acidosis differentially affect the respiratory neuronal network in the ventral medulla of neonatal rats Eur J Neurosci 26 2007 2834 2843 (Pubitemid 350115510)
57. Y. Oku, H. Masumiya, and Y. Okada Postnatal developmental changes in activation profiles of the respiratory neuronal network in the rat ventral medulla J Physiol 585 2007 175 186 (Pubitemid 350131111)
58. G. Paxinos, I. Törk, L.H. Tecott, and K.L. Valentino Atlas of the developing rat brain 1991 Academic Press San Diego
59. J.S. Rhee, Z.M. Wang, J. Nabekura, K. Inoue, and N. Akaike ATP facilitates spontaneous glycinergic IPSC frequency at dissociated rat dorsal horn interneuron synapses J Physiol 524 2000 471 483 (Pubitemid 30229512)
60. M.W. Salter, Y. De Koninck, and J.L. Henry Physiological roles for adenosine and ATP in synaptic transmission in the spinal dorsal horn Prog Neurobiol 41 1993 125 156 (Pubitemid 23152303)
61. M.W. Salter, and J.L. Hicks ATP-evoked increases in intracellular calcium in neurons and glia from the dorsal spinal cord J Neurosci 14 1994 1563 1575 (Pubitemid 24080006)
62. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network J Neurosci 24 2004 3125 3135 (Pubitemid 38405760)
63. H. Shiokawa, T. Nakatsuka, H. Furue, M. Tsuda, T. Katafuchi, K. Inoue, and M. Yoshimura Direct excitation of deep dorsal horn neurones in the rat spinal cord by the activation of postsynaptic P2X receptors J Physiol 573 2006 753 763 (Pubitemid 43842515)
64. A and cationic P2X ionotropic receptors of rat dorsal root ganglion neurons J Neurosci 21 2001 4958 4968 (Pubitemid 32622921)
65. G.G. Somjen Evoked sustained focal potentials and membrane potential of neurons and of unresponsive cells of the spinal cord J Neurophysiol 33 1970 562 582
66. 2+ signaling J Neurosci 26 2006 1378 1385 (Pubitemid 43237008)
67. 2/3 receptor signaling in capsaicin-insensitive primary afferent neurons J Neurosci 20 2000 RC90
68. 4 receptors induced in spinal microglia gate tactile allodynia after nerve injury Nature 424 2003 778 783 (Pubitemid 37021707)
69. A. Verkhratsky, O.A. Krishtal, and G. Burnstock Purinoceptors on neuroglia Mol Neurobiol 39 2009 190 208
70. 3 receptor subunits in rat and monkey sensory neurons and their central terminals Neuropharmacology 36 1997 1229 1242 (Pubitemid 27465611)
71. 3 is expressed by DRG neurons that terminate in inner lamina II Eur J Neurosci 10 1998 3470 3478 (Pubitemid 29074138)
72. Z. Xiang, X. Bo, and G. Burnstock Localization of ATP-gated P2X receptor immunoreactivity in rat sensory and sympathetic ganglia Neurosci Lett 256 1998 105 108 (Pubitemid 28529708)
73. D.K. Yi, and G.A. Barr Formalin-induced c-fos expression in the spinal cord of fetal rats Pain 73 1997 347 354 (Pubitemid 28021838)
74. S. Yokota, T. Tsumori, T. Oka, S. Nakamura, and Y. Yasui GABAergic neurons in the ventrolateral subnucleus of the nucleus tractus solitarius are in contact with Kölliker-Fuse nucleus neurons projecting to the rostral ventral respiratory group and phrenic nucleus in the rat Brain Res 1228 2008 113 126
75. H. Yoshida, Y. Okada, H. Maruiwa, K. Fukuda, M. Nakamura, K. Chiba, and Y. Toyama Synaptic blockade plays a major role in the neural disturbance of experimental spinal cord compression J Neurotrauma 20 2003 1365 1376 (Pubitemid 38018372)
76. 1 receptor in astroglia-to-neuron signaling at dorsal spinal cord J Neurosci Res 87 2009 2667 2676