P2X7 receptors in satellite glial cells mediate high functional expression of P2X3 receptors in immature dorsal root ganglion neurons

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Chen, Yong ^a   Li, Guangwen ^a   Huang, Li Yen M ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Abnormal pain; Development; Dorsal root ganglion; Neuron glia interactions; Nociception; P2X3 receptors; P2X7 receptors; P2X7R P2X3R inhibitory control; Postnatal immature rats; Purinergic signaling

Indexed keywords

PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X7 RECEPTOR;

ANALGESIA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; ENZYME REGULATION; GLIA CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SATELLITE CELL; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; AGING; ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; GANGLIA, SPINAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X3; RECEPTORS, PURINERGIC P2X7; SATELLITE CELLS, PERINEURONAL;

EID: 84856578213     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-9     Document Type: Article

References (45)

1. Huang TY, Cherkas PS, Rosenthal DW, Hanani M. Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Res 2005, 1036:42-49. 10.1016/j.brainres.2004.12.021, 15725400.
2. Pannese E, Ledda M, Cherkas PS, Huang TY, Hanani M. 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 (Berl) 2003, 206:337-347.
3. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Rev 2005, 48:457-476. 10.1016/j.brainresrev.2004.09.001, 15914252.
4. Zhang X, Chen Y, Wang C, Huang LY. Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci USA 2007, 104:9864-9869. 10.1073/pnas.0611048104, 1887586, 17525149.
5. Chen Y, Zhang X, Wang C, Li G, Gu Y, Huang LY. Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc Natl Acad Sci USA 2008, 105:16773-16778. 10.1073/pnas.0801793105, 2575495, 18946042.
6. Suadicani SO, Cherkas PS, Zuckerman J, Smith DN, Spray DC, Hanani M. Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biol 2010, 6:43-51. 10.1017/S1740925X09990408, 2897940, 19891813.
7. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002, 82:1013-1067.
8. Liu XJ, Salter MW. Purines and pain mechanisms: recent developments. Curr Opin Investig Drugs 2005, 6:65-75.
9. Nakatsuka T, Gu JG. P2X purinoceptors and sensory transmission. Pflugers Arch 2006, 452:598-607. 10.1007/s00424-006-0057-6, 16547751.
10. Engelman HS, MacDermott AB. Presynaptic ionotropic receptors and control of transmitter release. Nat Rev Neurosci 2004, 5:135-145. 10.1038/nrn1297, 14735116.
11. Bradbury EJ, Burnstock G, McMahon SB. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 1998, 12:256-268. 10.1006/mcne.1998.0719, 9828090.
12. Kobayashi K, Fukuoka T, Yamanaka H, Dai Y, Obata K, Tokunaga A, Noguchi K. Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J Comp Neurol 2005, 481:377-390. 10.1002/cne.20393, 15593340.
13. Zhang XF, Han P, Faltynek CR, Jarvis MF, Shieh CC. Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Res 2005, 1052:63-70. 10.1016/j.brainres.2005.06.022, 16005856.
14. Gu Y, Chen Y, Zhang X, Li GW, Wang C, Huang LY. Neuronal soma-satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors. Neuron Glia Biol 2010, 6:53-62. 10.1017/S1740925X10000116, 3120217, 20604979.
15. Souslova V, Cesare P, Ding Y, Akopian AN, Stanfa L, Suzuki R, Carpenter K, Dickenson A, Boyce S, Hill R, Nebenuis-Oosthuizen D, Smith AJ, Kidd EJ, Wood JN. Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 2000, 407:1015-1017. 10.1038/35039526, 11069182.
16. Cockayne DA, Dunn PM, Zhong Y, Rong W, Hamilton SG, Knight GE, Ruan HZ, Ma B, Yip P, Nunn P, McMahon SB, Burnstock G, Ford AP. P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 2005, 567:621-639. 10.1113/jphysiol.2005.088435, 1474198, 15961431.
17. Cook SP, Vulchanova L, Hargreaves KM, Elde R, McCleskey EW. Distinct ATP receptors on pain-sensing and stretch-sensing neurons. Nature 1997, 387:505-508. 10.1038/387505a0, 9168113.
18. Ando RD, Mehesz B, Gyires K, Illes P, Sperlagh B. A comparative analysis of the activity of ligands acting at P2X and P2Y receptor subtypes in models of neuropathic, acute and inflammatory pain. Br J Pharmacol 2010, 159:1106-1117. 10.1111/j.1476-5381.2009.00596.x, 2839268, 20136836.
19. Colomar A, Marty V, Medina C, Combe C, Parnet P, Amedee T. Maturation and release of interleukin-1beta by lipopolysaccharide-primed mouse Schwann cells require the stimulation of P2X7 receptors. J Biol Chem 2003, 278:30732-30740. 10.1074/jbc.M304534200, 12796490.
20. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CB, Casula MA, Yiangou Y, Birch R, Anand P, Buell GN. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396. 10.1016/j.pain.2005.01.002, 15777864.
21. McGaraughty S, Chu KL, Namovic MT, Donnelly-Roberts DL, Harris RR, Zhang XF, Shieh CC, Wismer CT, Zhu CZ, Gauvin DM, Fabiyi AC, Honore P, Gregg RJ, Kort ME, Nelson DW, Carroll WA, Marsh K, Faltynek CR, Jarvis MF. P2X7-related modulation of pathological nociception in rats. Neuroscience 2007, 146:1817-1828. 10.1016/j.neuroscience.2007.03.035, 17478048.
22. Cheung KK, Burnstock G. Localization of P2X3 receptors and coexpression with P2X2 receptors during rat embryonic neurogenesis. J Comp Neurol 2002, 443:368-382. 10.1002/cne.10123, 11807844.
23. Ruan HZ, Moules E, Burnstock G. Changes in P2X3 purinoceptors in sensory ganglia of the mouse during embryonic and postnatal development. Histochem Cell Biol 2004, 122:539-551. 10.1007/s00418-004-0714-9, 15549366.
24. Dunn PM, Gever J, Ruan HZ, Burnstock G. Developmental changes in heteromeric P2X(2/3) receptor expression in rat sympathetic ganglion neurons. Dev Dyn 2005, 234:505-511. 10.1002/dvdy.20466, 15973739.
25. Cheung KK, Chan WY, Burnstock G. Expression of P2X purinoceptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience 2005, 133:937-945. 10.1016/j.neuroscience.2005.03.032, 15964486.
26. Boldogkoi Z, Schutz B, Sallach J, Zimmer A. P2X(3) receptor expression at early stage of mouse embryogenesis. Mech Dev 2002, 118:255-260. 10.1016/S0925-4773(02)00280-0, 12351197.
27. Amir R, Devor M. Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience 2000, 95:189-195.
28. Fulton BP. Postnatal changes in conduction velocity and soma action potential parameters of rat dorsal root ganglion neurones. Neurosci Lett 1987, 73:125-130. 10.1016/0304-3940(87)90005-X, 3822244.
29. Stebbing MJ, McLachlan EM, Sah P. Are there functional P2X receptors on cell bodies in intact dorsal root ganglia of rats?. Neuroscience 1998, 86:1235-1244. 10.1016/S0306-4522(98)00127-4, 9697129.
30. Tan PH, Yang LC, Shih HC, Lan KC, Cheng JT. Gene knockdown with intrathecal siRNA of NMDA receptor NR2B subunit reduces formalin-induced nociception in the rat. Gene Ther 2005, 12:59-66. 10.1038/sj.gt.3302376, 15470478.
31. Hylden JL, Wilcox GL. Intrathecal morphine in mice: a new technique. Eur J Pharmacol 1980, 67:313-316. 10.1016/0014-2999(80)90515-4, 6893963.
32. Chen Y, Li GW, Wang C, Gu Y, Huang LY. Mechanisms underlying enhanced P2X receptor-mediated responses in the neuropathic pain state. Pain 2005, 119:38-48. 10.1016/j.pain.2005.09.007, 16298067.
33. Wang C, Gu Y, Li GW, Huang LY. A critical role of the cAMP sensor Epac in switching protein kinase signalling in prostaglandin E2-induced potentiation of P2X3 receptor currents in inflamed rats. J Physiol 2007, 584:191-203. 10.1113/jphysiol.2007.135616, 2277053, 17702820.
34. Lawson SN, Caddy KW, Biscoe TJ. Development of rat dorsal root ganglion neurones. Studies of cell birthdays and changes in mean cell diameter. Cell Tissue Res 1974, 153:399-413.
35. Bunge MB, Bunge RP, Peterson ER, Murray MR. A light and electron microscope study of long-term organized cultures of rat dorsal root ganglia. J Cell Biol 1967, 32:439-466. 10.1083/jcb.32.2.439, 2107246, 10976233.
36. Pannese E. The structure of the perineuronal sheath of satellite glial cells (SGCs) in sensory ganglia. Neuron Glia Biol 2010, 6:3-10. 10.1017/S1740925X10000037, 20604977.
37. Vulchanova L, Riedl MS, Shuster SJ, Stone LS, Hargreaves KM, Buell G, Surprenant A, North RA, Elde R. P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 1998, 10:3470-3478. 10.1046/j.1460-9568.1998.00355.x, 9824460.
38. Xiang Z, Bo X, Burnstock G. Localization of ATP-gated P2X receptor immunoreactivity in rat sensory and sympathetic ganglia. Neurosci Lett 1998, 256:105-108. 10.1016/S0304-3940(98)00774-5, 9853714.
39. Xiang Z, Burnstock G. Expression of P2X receptors on rat microglial cells during early development. GLIA 2005, 52:119-126. 10.1002/glia.20227, 15920729.
40. Xiang Z, Burnstock G. Changes in expression of P2X purinoceptors in rat cerebellum during postnatal development. Brain Res Dev Brain Res 2005, 156:147-157.
41. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci 2005, 6:507-520.
42. Ren K, Anseloni V, Zou SP, Wade EB, Novikova SI, Ennis M, Traub RJ, Gold MS, Dubner R, Lidow MS. Characterization of basal and re-inflammation-associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult. Pain 2004, 110:588-596. 10.1016/j.pain.2004.04.006, 15288399.
43. Anand P, Birch R. Restoration of sensory function and lack of long-term chronic pain syndromes after brachial plexus injury in human neonates. Brain 2002, 125:113-122. 10.1093/brain/awf017, 11834597.
44. Fitzgerald M, Walker SM. Infant pain management: a developmental neurobiological approach. Nat Clin Pract Neurol 2009, 5:35-50.
45. Xu GY, Huang LY. Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. J Neurosci 2002, 22:93-102.