P2X receptors, sensory neurons and pain

Current Medicinal Chemistry

Volumn 22, Issue 7, 2015, Pages 845-850

  Bele, Tanja ^a   Fabbretti, Elsa ^a  

^a UNIVERSITY OF NOVA GORICA   (Slovenia)

Author keywords

Adenosine triphosphate; ATP; Hyperalgesia; Nociception; Purinergic signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; MICRORNA; PURINERGIC P2X RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; UNTRANSLATED RNA;

ACCESSORY CELL; ARTICLE; CALCIUM CELL LEVEL; CENTRAL NERVOUS SYSTEM SENSITIZATION; CHRONIC PAIN; DISEASE COURSE; ENZYME DEGRADATION; GENE EXPRESSION; HUMAN; MOLECULAR DYNAMICS; NERVE CELL; NOCICEPTION; NONHUMAN; PAIN; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DISEASE PROGRESSION; HUMANS; PAIN; RECEPTORS, PURINERGIC P2X; SENSORY RECEPTOR CELLS;

EID: 84926453299     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666141011195351     Document Type: Article

References (84)

1. D'Mello, R.; Dickenson, A.H. Spinal cord mechanisms of pain. Br. J. Anaesth., 2008, 101, 8-16
2. Woolf, C.J.; Salter, M.W. Neuronal plasticity: increasing the gain in pain. Science, 2000, 288(5472), 1765-1769
3. Giniatullin, R.; Nistri, A.; Fabbretti, E. Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF. Mol. Neurobiol., 2008, 37, 83-90
4. Harrington A.W.; Ginty, D.D. Long-distance retrograde neurotrophic factor signalling in neurons. Nat. Rev. Neurosci., 2013, 14(3), 177-187
5. Villa, G.; Ceruti, S.; Zanardelli, M.; Magni, G.; Jasmin, L.; Ohara, P.T.; Abbracchio, M.P. Temporomandibular joint inflammation activates glial and immune cells in both the trigeminal ganglia and in the spinal trigeminal nucleus. Mol. Pain., 2010, 6, 89
6. Franceschini, A.; Vilotti, S.; Ferrari, M.D.; van den Maagdenberg, A.M.; Nistri, A.; Fabbretti, E. TNFa levels and macrophages expression reflect an inflammatory potential of trigeminal ganglia in a mouse model of familial hemiplegic migraine. PLoS One, 2013, 8(1), e52394
7. Ohara, P.T.; Vit, J.P.; Bhargava, A.; Romero, M.; Sundberg, C.; Charles, A.C.; Jasmin, L. Gliopathic pain: when satellite glial cells go bad. Neuroscientist, 2009, 15, 450-463
8. Takeda, M.; Takahashi, M.; Matsumoto, S. Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neurosci. Biobehav. Rev., 2009, 33(6), 784-792
9. Ceruti, S.; Fumagalli, M.; Villa, G.; Verderio, C.; Abbracchio, M.P. Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium, 2008, 43(6), 576-590
10. Tsuda, M.; Toyomitsu, E.; Komatsu, T.; Masuda, T.; Kunifusa, E.; Nasu-Tada, K.; Koizumi, S.; Yamamoto, K.; Ando, J.; Inoue, K. Fibronectin/integrin system is involved in P2X4 receptor upregulation in the spinal cord and neuropathic pain after nerve injury. Glia, 2008, 56(5), 579-585
11. Rozanski, G.M.; Li, Q.; Stanley, E.F. Transglial transmission at the dorsal root ganglion sandwich synapse: glial cell to postsynaptic neuron communication. Eur. J. Neurosci., 2013, 37(8), 1221-1228
12. Fabbretti, E. ATP P2X3 receptors and neuronal sensitization. Front. Cell Neurosci., 2013, 7, 236
13. Shu, X.; Mendell, L.M. Acute sensitization by NGF of the response of small-diameter sensory neurons to capsaicin. J. Neurophysiol., 2001, 86, 2931-2938
14. Clark, A.K.; Old, E.A.; Malcangio, M. Neuropathic pain and cytokines: current perspectives. J. Pain Res., 2013, 6, 803-814
15. Ceruti, S.; Villa, G.; Fumagalli, M.; Colombo, L.; Magni, G.; Zanardelli, M.; Fabbretti, E.; Verderio, C.; van den Maagdenberg, A.M.; Nistri, A.; Abbracchio, M.P. Calcitonin gene-related peptidemediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2.1 Knock-in mice: implications for basic mechanisms of migraine pain. J. Neurosci., 2011, 31(10), 3638-3649
16. Jakobsson, P.J. Pain: how macrophages mediate inflammatory pain via ATP signaling. Nat. Rev. Rheumatol., 2010, 6, 679-681
17. Hamilton, S.G.; Warburton, J.; Bhattacharjee, A.; Ward, J.; McMahon, S.B. ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain, 2000, 123, 1238-1246
18. Holton, F.A.; Holton, P. The possibility that ATP is a transmitter at sensory nerve endings. J. Physiol., 1953, 119, 50-51
19. Bardoni, R.; Goldstein, P.A.; Lee, C.J.; Gu, J.G.; MacDermott, A.B. ATP P2X receptors mediate fast synaptic transmission in the dorsal horn of the rat spinal cord. J. Neurosci., 1997, 17, 5297-5304
20. Corriden, R.; Insel, P.A. Basal release of ATP: an autocrineparacrine mechanism for cell regulation. Sci. Signal., 2010, 3(104), re1
21. Novak, I. Purinergic signaling in epithelial ion transport: regulation of secretion and absorption. Acta. Physiol., 2011, 202, 501-522
22. Bleehen T., Keele C.A., Observations on the algogenic actions of adenosine compounds on the human blister base preparation. Pain. 1977, 3, 367-377.
23. Bleehen, T.; Keele, C.A. Observations on the algogenic actions of adenosine compounds on the human blister base preparation. Pain, 1977, 3, 367-377, [23] Jahr, C.E.; Jessell, T.M. ATP excites a subpopulation of rat dorsal horn neurones. Nature, 1983, 304, 730-733
24. Hilliges, M.; Weidner, C.; Schmelz, M.; Schmidt, R.; Ørstavik, K.; TorebjÖrk, E.; Handwerker, H. ATP responses in human C nociceptors. Pain, 2002, 98, 59-68
25. Gu, J.G.; MacDermott, A.B. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature, 1997, 389, 749-753
26. Pankratov, Y.; Lalo, U.; Verkhratsky, A.; North, R.A. Vesicular release of ATP at central synapses. Pflugers Arch., 2006, 452(5), 589-597
27. Burnstock, G. Purinergic signalling and disorders of the central nervous system. Nat. Rev. Drug Discov., 2008, 7(7), 575-590
28. Khakh, B.S.; North, R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature, 2006, 442, 527-532
29. Lewis, C.; Neidhart, S.; Holy, C.; North, R.A.; Buell, G.; Surprenant, A. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature, 1995, 377, 432-435
30. Kaan, T.K.; Yip, P.K.; Patel, S.; Davies, M.; Marchand, F.; Cockayne, D.A.; Nunn, P.A.; Dickenson, A.H.; Ford, A.P.; Zhong, Y.; Malcangio, M.; McMahon, S.B. Systemic blockade of P2X3 and P2X2/3 receptors attenuates bone cancer pain behaviour in rats. Brain, 2010, 133(9), 2549-2564
31. D'Arco, M.; Giniatullin, R.; Simonetti, M.; Fabbro, A.; Nair, A.; Nistri, A.; Fabbretti, E. Neutralization of nerve growth factor induces plasticity of ATP-sensitive P2X3 receptors of nociceptive trigeminal ganglion neurons. J. Neurosci., 2007, 27, 8190-8201
32. Xu, G.Y.; Huang, L.Y. Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. J. Neurosci., 2002, 22, 93-102
33. Vulchanova, L.; Riedl, M.S.; Shuster, S.J.; Buell, G.; Surprenant, A.; North, R.A.; Elde, R. Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology, 1997, 36, 1229-1242
34. Sokolova, E.; Skorinkin, A.; Moiseev, I.; Agrachev, A.; Nistri, A.; Giniatullin, R. Experimental and modeling studies of desensitization of P2X3 receptors. Mol. Pharmacol., 2006, 70(1), 373-382
35. Nair, A.; Simonetti, M.; Birsa, N.; Ferrari, M.D.; van den Maagdenberg, A.M.; Giniatullin, R.; Nistri, A.; Fabbretti, E. Familial hemiplegic migraine Ca(v)2.1 channel mutation R192Q enhances ATP-gated P2X3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol. Pain, 2010, 6, 48
36. Liu, X.J.; Gingrich, J.R.; Vargas-Caballero, M.; Dong, Y.N.; Sengar, A.; Beggs, S.; Wang, S.H.; Ding, H.K.; Frankland, P.W.; Salter, M.W. Treatment of inflammatory and neuropathic pain by uncoupling Src from the NMDA receptor complex. Nat. Med., 2008, 14(12), 1325-1332
37. D'Arco, M.; Giniatullin, R.; Leone, V.; Carloni, P.; Birsa, N.; Nair, A.; Nistri, A.; Fabbretti, E. The C-terminal Src inhibitory kinase (Csk)-mediated tyrosine phosphorylation is a novel molecular mechanism to limit P2X3 receptor function in mouse sensory neurons. J. Biol. Chem., 2009, 284(32), 21393-21401
38. Sundukova, M.; Vilotti, S.; Abbate, R.; Fabbretti, E.; Nistri, A. Functional differences between ATP-gated human and rat P2X3 receptors are caused by critical residues of the intracellular Cterminal domain. J. Neurochem., 2012, 122(3), 557-567
39. Coddou, C.; Yan, Z.; Obsil, T.; Huidobro-Toro, J.P.; Stojilkovic, S.S. Activation and regulation of purinergic P2X receptor channels. Pharmacol. Rev., 2011, 63(3), 641-683
40. Di Virgilio, F.; Ceruti, S.; Bramanti P., Abbracchio, M.P. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci., 2009, 32(2), 79-87
41. Dubyak, G.R. P2X7 receptor regulation of non-classical secretion from immune effector cells. Cell. Microbiol., 2012, 14(11), 1697-1706
42. Donnelly-Roberts, D.L.; Namovic, M.T.; Han, P.; Jarvis, M.F. Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br. J. Pharmacol., 2009, 157(7), 1203-1214
43. Rokic, M.B.; Stojilkovic, S.S. Two open states of P2X receptor channels. Front. Cell Neurosci., 2013, 7, 215
44. Yan, Z.; Li, S.; Liang, Z.; Tomic, M.; Stojilkovic, S.S. The P2X7 receptor channel pore dilates under physiological ion conditions. J. Gen. Physiol., 2008, 132(5), 563-573
45. Khakh, B.S.; North, R.A. Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron, 2012, 76(1), 51-69
46. Karatas, H.; Erdener, S.E.; Gursoy-Ozdemir, Y.; Lule, S.; Eren- Kocak, E.; Sen Z.D.; Sen, Z.D.; Dalkara, T. Spreading depression triggers headache by activating neuronal panx1 channels. Science, 2013, 339, 1092-1095
47. Li, S.; Tomic, M.; Stojilkovic, S.S. Characterization of novel Pannexin 1 isoforms from rat pituitary cells and their association with ATP-gated P2X channels. Gen. Comp. Endocrinol., 2011, 174(2), 202-210
48. Tsuda, M.; Kuboyama, K.; Inoue, T.; Nagata, K.; Tozaki-Saitoh, H.; Inoue, K. Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays. Mol. Pain, 2009, 5, 28
49. Masuda, T.; Iwamoto, S.; Yoshinaga, R.; Tozaki-Saitoh, H.; Nishiyama, A.; Mak, T.W.; Tamura, T.; Tsuda, M.; Inoue, K. Transcription factor IRF5 drives P2X4R(+)-reactive microglia gating neuropathic pain. Nat. Commun., 2014, 5, 3771
50. Masuda, T.; Tsuda, M.; Yoshinaga, R.; Tozaki-Saitoh, H.; Ozato, K.; Tamura, T.; Inoue, K. IRF8 Is a Critical Transcription Factor for Transforming Microglia into a Reactive Phenotype. Cell. Rep., 2012, 1, 334-340
51. Coull, J.A.; Beggs, S.; Boudreau, D.; Boivin, D.; Tsuda, M.; Inoue, K.; Gravel, C.; Salter, M.W.; De Koninck, Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature, 2005, 438, 1017-1021
52. Trang, T.; Beggs, S.; Wan, X.; Salter, M.W. P2X4-receptormediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci., 2009, 29(11), 3518-3528
53. Boumechache, M.; Masin, M.; Edwardson, J.M.; Górecki, D.C.; Murrell-Lagnado, R. Analysis of assembly and trafficking of native P2X4 and P2X7 receptor complexes in rodent immune cells. J. Biol. Chem., 2009, 284(20), 13446-13454
54. McDonald, M.K.; Tian, Y.; Qureshi, R.A.; Gormley, M.; Ertel, A.; Gao, R.; Lopez, E.A.; Alexander, G.M.; Sacan, A.; Fortina, P.; Ajit, S.K. Functional significance of macrophage-derived exosomes in inflammation and pain. Pain, 2014 [Epub ahead of print]
55. Souslova, V.; Cesare, P.; Ding, Y.; Akopian, A.N.; Stanfa, L.; Suzuki, R.; Carpenter, K.; Dickenson, A.; Boyce, S.; Hill, R.; Nebenuis- Oosthuizen, D.; Smith, A.J.; Kidd, E.J.; Wood, J.N. Warmcoding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature, 2000, 407(6807), 1015-1017
56. Barclay, J.; Patel, S.; Dorn, G.; Wotherspoon, G.; Moffatt, S.; Eunson, L.; Abdel'al, S.; Natt, F.; Hall, J.; Winter, J.; Bevan, S.; Wishart, W.; Fox, A.; Ganju, P. Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J. Neurosci., 2002, 22(18), 8139-8147
57. Cockayne, D.A.; Hamilton, S.G.; Zhu, Q.M.; Dunn, P.M.; Zhong, Y.; Novakovic, S.; Malmberg, A.B.,; Cain, G.; Berson, A.; Kassotakis, L.; Hedley, L.; Lachnit, W.G.; Burnstock, G.; McMahon, S.B.; Ford, A.P. Urinary bladder hyporeflexia and reduced painrelated behaviour in P2X3-deficient mice. Nature, 2000, 407, 1011-1015
58. Hansen, R.R.; Nielsen, C.K.; Nasser, A.; Thomsen, S.I.; Eghorn, L.F.; Pham, Y.; Schulenburg, C.; Syberg, S.; Ding, M.; Stojilkovic, S.S.; Jorgensen, N.R.; Heegaard, A.M. P2X7 receptor-deficient mice are susceptible to bone cancer pain. Pain, 2011, 152(8), 1766-1776
59. Hullugundi SK, Ansuini A, Ferrari MD, van den Maagdenberg AM, Nistri A. A hyperexcitability phenotype in mouse trigeminal sensory neurons expressing the R192Q Cacna1a missense mutation of familial hemiplegic migraine type-1. Neuroscience, 2014, 266, 244-254
60. Vilotti, S.; Marchenkova, A.; Ntamati, N.; Nistri, A. B-type natriuretic peptide-induced delayed modulation of TRPV1 and P2X3 receptors of mouse trigeminal sensory neurons. PLoS One, 2013, 8(11), e81138
61. Vacca, F.; Giustizieri, M.; Ciotti, M.T.; Mercuri, N.B.; Volonté, C. Rapid constitutive and ligand-activated endocytic trafficking of P2X receptor. J. Neurochem., 2009, 109(4), 1031-1041
62. Gnanasekaran, A.; Sundukova, M.; van den Maagdenberg, A.M.; Fabbretti, E.; Nistri, A. Lipid rafts control P2X3 receptor distribution and function in trigeminal sensory neurons of a transgenic migraine mouse model. Mol. Pain., 2011, 7, 77-90
63. Chen, X.Q.; Wang, B.; Wu, C.; Pan, J.; Yuan, B.; Su, Y.Y.; Jiang, X.Y.; Zhang, X., Bao, L. Endosome-mediated retrograde axonal transport of P2X3 receptor signals in primary sensory neurons. Cell Res., 2012, 22(4), 677-696
64. Chen, X.Q.; Zhu, J.X.; Wang, Y.; Zhang, X.; Bao, L. CaMKIIa and caveolin-1 cooperate to drive ATP-induced membrane delivery of the P2X3 receptor. J. Mol. Cell Biol., 2014, 6(2), 140-153
65. Hattori, M.; Gouaux, E. Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature, 2012, 485(7397), 207-212
66. Kim, M.; Jiang, L.H.; Wilson, H.L.; North, R.A.; Surprenant, A. Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J., 2001, 20(22), 6347-6358
67. Volonté, C.; Burnstock, G. P2X3 receptor: a novel 'CASKade' of signaling? J. Neurochem., 2013, 126(1), 1-3
68. Gnanasekaran, A.; Sundukova, M.; Hullugundi, S.; Birsa, N.; Bianchini, G.; Hsueh, Y.P.; Nistri, A.; Fabbretti, E. Calcium/ calmodulin-dependent serine protein kinase (CASK) is a new intracellular modulator of P2X3 receptors. J. Neurochem., 2013, 126(1), 102-112
69. Gnanasekaran, A.; Bele, T.; Hullugundi, S.; Simonetti, M.; Ferrari, M.D.; van den Maagdenberg, A.M.; Nistri, A.; Fabbretti, E. Mutated CaV2.1 channels dysregulate CASK/P2X3 signaling in mouse trigeminal sensory neurons of R192Q Cacna1a knock-in mice. Mol. Pain, 2013, 9, 62-68
70. Fountain, S.J.; North, R.A. A C-terminal lysine that controls human P2X4 receptor desensitization. J. Biol. Chem., 2006, 281(22), 15044-15049
71. Bernier, L.P.; Ase, A.R.; Séguéla, P. Post-translational regulation of P2X receptor channels: modulation by phospholipids. Front. Cell Neurosci., 2013, 7, 226
72. Roberts, J.A.; Bottrill, A.R.; Mistry, S.; Evans, R.J. Mass spectrometry analysis of human P2X1 receptors; insight into phosphorylation, modelling and conformational changes. J. Neurochem., 2012, 123(5), 725-735
73. Alewine, C.; Olsen, O.; Wade, J.B.; Welling, P.A. TIP-1 has PDZ scaffold antagonist activity. Mol. Biol. Cell., 2006, 17(10), 4200-4211
74. Márquez-Rosado, L.; Singh, D.; Rincón-Arano, H.; Solan, J.L.; Lampe, P.D. CASK (LIN2) interacts with Cx43 in wounded skin and their coexpression affects cell migration. J. Cell. Sci., 2012, 125(Pt 3), 695-702
75. Zordan, M.A.; Massironi, M.; Ducato, M.G.; Te Kronnie, G.; Costa, R.; Reggiani, C.; Chagneau, C.; Martin, J.R.; Megighian, A. Drosophila CAKI/CMG protein, a homolog of human CASK, is essential for regulation of neurotransmitter vesicle release. J. Neurophysiol., 2005, 94(2), 1074-1083
76. Gillespie, J.M.; Hodge, J.J. CASK regulates CaMKII autophosphorylation in neuronal growth, calcium signaling, and learning. Front. Mol. Neurosci., 2013, 6, 27
77. Atasoy, D.; Schoch, S.; Ho, A.; Nadasy, K.A.; Liu, X.; Zhang, W.; Mukherjee, K.; Nosyreva, E.D.;Fernandez-Chacon, R.; Missler, M.; Kavalali, E.T.; Südhof, T.C. Deletion of CASK in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. U S A, 2007, 104(7), 2525-2530
78. Jeyifous, O.; Waites, C.L.; Specht, C.G.; Fujisawa, S.; Schubert, M.; Lin, E.I.; Marshall, J.; Aoki, C.; de Silva, T.; Montgomery, J.M.; Garner, C.C.; Green, W.N. SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat. Neurosci., 2009, 12(8), 1011-1019
79. Hsueh, YP. The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem., 2006, 13(16), 1915-1927
80. Kuner, R. Central mechanisms of pathological pain. Nat. Med., 2010, 16, 1258-1266
81. Fabbretti. E.; D'Arco, M.; Fabbro, A.; Simonetti, M.; Nistri, A.; Giniatullin, R. Delayed upregulation of ATP P2X3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J. Neurosci., 2006, 26, 6163-6171
82. Simonetti, M.; Giniatullin, R.; Fabbretti, E. Mechanisms mediating the enhanced gene transcription of P2X3 receptor by calcitonin gene-related peptide in trigeminal sensory neurons. J. Biol. Chem., 2008, 283(27), 18743-18752
83. Zhao, J.; Lee, M.C.; Momin, A.; Cendan, C.M.; Shepherd, S.T.; Baker, M.D.; Asante, C.; Bee, L.; Bethry, A.; Perkins, J.R.; Nassar, M.A.; Abrahamsen, B.; Dickenson, A.; Cobb, B.S.; Merkenschlager, M.; Wood, J.N. Small RNAs control sodium channel expression, nociceptor excitability, and pain thresholds. J. Neurosci., 2010, 30(32), 10860-10871
84. Lutz, B.M.; Bekker, A.; Tao, Y.X. Noncoding RNAs: New Players in Chronic Pain. Anesthesiology, 2014, 121(2), 409-417.