Selective potentiation of homomeric P2X2 ionotropic ATP receptors by a fast non-genomic action of progesterone

Neuropharmacology

Volumn 58, Issue 3, 2010, Pages 569-577

  De Roo, Mathias ^a   Boué Grabot, Eric ^b   Schlichter, Rémy ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Dorsal root ganglion; Purinoceptor; Sensory transmission; Spinal cord; Steroid

Indexed keywords

ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; PRASTERONE; PROGESTERONE; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; HORMONE ACTION; HUMAN; HUMAN CELL; NEUROTRANSMISSION; NEWBORN; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SPINAL GANGLION; XENOPUS LAEVIS;

ADENOSINE TRIPHOSPHATE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CELLS, CULTURED; DEHYDROEPIANDROSTERONE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; GANGLIA, SPINAL; HUMANS; MEMBRANE POTENTIALS; NEURONS; OOCYTES; PATCH-CLAMP TECHNIQUES; PROGESTERONE; PROGESTINS; PROTEIN SUBUNITS; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; TRANSFECTION; XENOPUS;

EID: 73449108016     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.12.002     Document Type: Article

References (48)

1. Baulieu E.E. Neurosteroids: a novel function of the brain. Psychoneuroendocrinology 23 (1998) 963-987
2. Belelli D., and Lambert J.J. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat. Rev. Neurosci. 6 (2005) 565-575
3. Bernier L.P., Ase A.R., Chevallier S., Blais D., Zhao Q., Boue-Grabot E., Logothetis D., and Seguela P. Phosphoinositides regulate P2X4 ATP-gated channels through direct interactions. J. Neurosci. 28 (2008) 12938-12945
4. Brenner R.M., and West N.B. Hormonal regulation of the reproductive tract in female mammals. Annu. Rev. Physiol. 37 (1975) 273-302
5. Burgard E.C., Niforatos W., van Biesen T., Lynch K.J., Touma E., Metzger R.E., Kowaluk E.A., and Jarvis M.F. P2X receptor-mediated ionic currents in dorsal root ganglion neurons. J. Neurophysiol. 82 (1999) 1590-1598
6. Burnstock G. P2X receptors in sensory neurones. Br. J. Anaesth. 84 (2000) 476-488
7. Cockayne D.A., Dunn P.M., Zhong Y., Rong W., Hamilton S.G., Knight G.E., Ruan H.Z., Ma B., Yip P., Nunn P., McMahon S.B., Burnstock G., and Ford A.P. 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. 567 (2005) 621-639
8. Codocedo J.F., Rodriguez F.E., and Huidobro-Toro J.P. Neurosteroids differentially modulate P2X ATP-gated channels through non-genomic interactions. J. Neurochem. 110 (2009) 734-744
9. Coirini H., Gouezou M., Liere P., Delespierre B., Pianos A., Eychenne B., Schumacher M., and Guennoun R. 3 Beta-hydroxysteroid dehydrogenase expression in rat spinal cord. Neuroscience 113 (2002) 883-891
10. Collo G., North R.A., Kawashima E., Merlo-Pich E., Neidhart S., Surprenant A., and Buell G. Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci. 16 (1996) 2495-2507
11. Compagnone N.A., and Mellon S.H. Neurosteroids: biosynthesis and function of these novel neuromodulators. Front. Neuroendocrinol. 21 (2000) 1-56
12. De Roo M., Rodeau J.L., and Schlichter R. Dehydroepiandrosterone potentiates native ionotropic ATP receptors containing the P2X2 subunit in rat sensory neurones. J. Physiol. 552 (2003) 59-71
13. Dunn P.M., Zhong Y., and Burnstock G. P2X receptors in peripheral neurons. Prog. Neurobiol. 65 (2001) 107-134
14. Egan T.M., and Khakh B.S. Contribution of calcium ions to P2X channel responses. J. Neurosci. 24 (2004) 3413-3420
15. Fujiwara Y., and Kubo Y. Regulation of the desensitization and ion selectivity of ATP-gated P2X2 channels by phosphoinositides. J. Physiol. 576 (2006) 135-149
16. Gu J.G., and MacDermott A.B. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389 (1997) 749-753
17. Hugel S., and Schlichter R. Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J. Neurosci. 20 (2000) 2121-2130
18. Jarvis M.F., and Khakh B.S. ATP-gated P2X cation-channels. Neuropharmacology 56 (2009) 208-215
19. Jiang L.H., Kim M., Spelta V., Bo X., Surprenant A., and North R.A. Subunit arrangement in P2X receptors. J. Neurosci. 23 (2003) 8903-8910
20. Jo Y.H., and Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat. Neurosci. 2 (1999) 241-245
21. Khakh B.S. Molecular physiology of P2X receptors and ATP signalling at synapses. Nat. Rev. Neurosci. 2 (2001) 165-174
22. Khakh B.S. ATP-gated P2X receptors on excitatory nerve terminals onto interneurons initiate a form of asynchronous glutamate release. Neuropharmacology 56 (2009) 216-222
23. Khakh B.S., Burnstock G., Kennedy C., King B.F., North R.A., Seguela P., Voigt M., and Humphrey P.P. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol. Rev. 53 (2001) 107-118
24. Khakh B.S., Gittermann D., Cockayne D.A., and Jones A. ATP modulation of excitatory synapses onto interneurons. J. Neurosci. 23 (2003) 7426-7437
25. Koenig H.L., Schumacher M., Ferzaz B., Thi A.N., Ressouches A., Guennoun R., Jung-Testas I., Robel P., Akwa Y., and Baulieu E.E. Progesterone synthesis and myelin formation by Schwann cells. Science 268 (1995) 1500-1503
26. Lewis C., Neidhart S., Holy C., North R.A., Buell G., and Surprenant A. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377 (1995) 432-435
27. Liu X.H., Zeng J.W., Zhao Y.D., Chen P.H., Xiao Z., and Ruan H.Z. Rapid inhibition of ATP-induced currents by corticosterone in rat dorsal root ganglion neurons. Pharmacology 82 (2008) 164-170
28. Ma B., Rong W., Dunn P.M., and Burnstock G. 17beta-estradiol attenuates alpha, beta-meATP-induced currents in rat dorsal root ganglion neurons. Life Sci. 76 (2005) 2547-2558
29. Nakatsuka T., Tsuzuki K., Ling J.X., Sonobe H., and Gu J.G. Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord. J. Neurophysiol. 89 (2003) 3243-3252
30. Nicke A., Baumert H.G., Rettinger J., Eichele A., Lambrecht G., Mutschler E., and Schmalzing G. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels. Embo J. 17 (1998) 3016-3028
31. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 82 (2002) 1013-1067
32. Pankratov Y.V., Lalo U.V., Dashkin A.N., and Krishtal A. Heterogeneity of the functional expression of P2X3 and P2X2/3 receptors in the primary nociceptive neurons of rat. Neurochem. Res. 26 (2001) 993-1000
33. Ralevic V., and Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50 (1998) 413-492
34. Rhee J.S., Wang Z.M., Nabekura J., Inoue K., and Akaike N. ATP facilitates spontaneous glycinergic IPSC frequency at dissociated rat dorsal horn interneuron synapses. J. Physiol. 524 Pt 2 (2000) 471-483
35. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci. 22 (1999) 410-416
36. Schlichter R., Keller A.F., De Roo M., Breton J.D., Inquimbert P., and Poisbeau P. Fast nongenomic effects of steroids on synaptic transmission and role of endogenous neurosteroids in spinal pain pathways. J. Mol. Neurosci. 28 (2006) 33-51
37. Slominski A., and Wortsman J. Neuroendocrinology of the skin. Endocr. Rev. 21 (2000) 457-487
38. Spelta V., Jiang L.H., Surprenant A., and North R.A. Kinetics of antagonist actions at rat P2X2/3 heteromeric receptors. Br. J. Pharmacol. 135 (2002) 1524-1530
39. Stoop R., Surprenant A., and North R.A. Different sensitivities to pH of ATP-induced currents at four cloned P2X receptors. J. Neurophysiol. 78 (1997) 1837-1840
40. Stoop R., Thomas S., Rassendren F., Kawashima E., Buell G., Surprenant A., and North R.A. Contribution of individual subunits to the multimeric P2X(2) receptor: estimates based on methanethiosulfonate block at T336C. Mol. Pharmacol. 56 (1999) 973-981
41. Torres G.E., Egan T.M., and Voigt M.M. Topological analysis of the ATP-gated ionotropic [correction of ionotrophic] P2X2 receptor subunit. FEBS Lett. 425 (1998) 19-23
42. Torres G.E., Egan T.M., and Voigt M.M. Hetero-oligomeric assembly of P2X receptor subunits. Specificities exist with regard to possible partners. J. Biol. Chem. 274 (1999) 6653-6659
43. Toulme E., Blais D., Leger C., Landry M., Garret M., Seguela P., and Boue-Grabot E. An intracellular motif of P2X(3) receptors is required for functional cross-talk with GABA(A) receptors in nociceptive DRG neurons. J. Neurochem. 102 (2007) 1357-1368
44. Vulchanova L., Riedl M.S., Shuster S.J., Buell G., Surprenant A., North R.A., and Elde R. Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36 (1997) 1229-1242
45. Wang C., Li G.W., and Huang L.Y. Prostaglandin E2 potentiation of P2X3 receptor mediated currents in dorsal root ganglion neurons. Mol. Pain 3 (2007) 22
46. Zhao Q., Logothetis D.E., and Seguela P. Regulation of ATP-gated P2X receptors by phosphoinositides. Pflugers Arch. 455 (2007) 181-185
47. Zhu Y., Bond J., and Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2237-2242
48. Zhu Y., Rice C.D., Pang Y., Pace M., and Thomas P. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2231-2236