Purinergic signalling: What is missing and needed next? The use of transgenic mice, crystallographic analysis and microRNA

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 6, 2012, Pages 751-767

  Volonte C ^a   Parisi, C ^a   Burnstock, G ^b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Ectonucleotidases; Extracellular adenosine; Extracellular ATP; Nervous system; Purinergic receptors; Purinergic signalling

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A2B RECEPTOR; ADENOSINE A3 RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CD39 ANTIGEN; MICRORNA; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y11 RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y4 RECEPTOR; PURINERGIC P2Y6 RECEPTOR; PURINERGIC RECEPTOR;

ALTERNATIVE RNA SPLICING; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; KNOCKOUT GENE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

ADENOSINE; ADENOSINE TRIPHOSPHATE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICRORNAS; NUCLEOTIDASES; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION;

EID: 84869014228     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152712803581146     Document Type: Review

References (119)

1. Burnstock, G. Purinergic nerves. Pharmacol. Rev., 1972, 24(3), 509-581.
2. Burnstock, G. Purinergic Signalling: its unpopular beginning, its acceptance and its exciting future. BioEssays, 2012, 34(3), 218-225.
3. Valera, S.; Talabot, F.; Evans, R.J.; Gos, A.; Antonarakis S.E.; Morris, M.A.; Buell, G.N. Characterization and chromosomal localization of a human P2X receptor from the urinary bladder. Recep. Chann, 1995, 3(4), 283-289.
4. Lynch, K.J.; Touma, E.; Niforatos, W.; Kage, K.L.; Bugard, E.C.; Van Biesen, T.; Kowaluk, E.A.; Jarvis M.F. Molecular and functional characterization of human P2X2 receptors. Mol. Pharmacol., 1999, 56(6), 1171-1181.
5. Garcia-Guzman, M.; Stühmer, W.; Soto, F. Molecular characterization and pharmacological properties of the human P2X3 purinoceptor. Brain Res. Mol. Brain Res., 1997, 47(1-2), 59-66.
6. Garcia-Guzman, M.; Soto, F.; Gomez-Hernandez, J.M.; Lund, P.; Stühmer, W. Characterization of recombinant human P2X4 receptor reveals pharmacological differences to the rat homologue. Mol. Pharmacol., 1997, 51(1), 109-118.
7. Lê, K.T.; Parquet, M.; Nouel, D.; Babinski, K.; Séguéla P. Primary structure and expression of a naturally truncated human P2X ATP receptor subunit from brain and immune system. FEBS Lett., 1997, 418(1-2), 195-199.
8. Urano, T.; Nishimori, H.; Han, H.; Furuhata, T.; Kimura, Y.; Nakamura, Y.; Tokino T. Cloning of a novel human P2X receptor gene regulated by p53 P2XM. Cancer Res., 1997, 57(15), 3281-3287.
9. Rassendren, F.; Buell, G.N.; Virginio, C.; Collo, G.; North, R.A. Surprenant, A. The permeabilizing ATP receptor, P2X7. Cloning and expression of a human cDNA. J. Biol. Chem., 1997, 28(9), 5482-5486.
10. Ayyanathan, K.; Webbs, T.E.; Sandhu, A.K.; Athwal, R.S.; Barnard, E.A.; Kunapuli, S.P. Cloning and chromosomal localization of the human P2Y1 purinoceptor. Biochem. Biophys. Res. Commun., 1996, 218(3), 783-788.
11. Parr, C.E.; Sullivan, D.M.; Paradiso, A.M.; Lazarowsky, E.R.; Burch, L.H.; Olsen, J.C.; Erb, L.; Weisman, G.A.; Boucher, R.C.; Turner, J.T. Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy. Proc. Nat. Acad. Sci. USA, 1994, 91(8), 3275-3279.
12. Communi, D.; Pirotton, S.; Parmentier, M.; Boeynaems, J. Cloning and functional expression of a human uridine nucleotide receptor. J. Biol. Chem., 1995, 270(52), 30849-30852.
13. Communi, D.; Parmentier, M.; Boeynaems J. Cloning, functional expression and tissue distribution of the human P2Y6 receptor. Biochem. Biophys. Res. Commun., 1996, 222(2), 303-308.
14. Communi, D.; Govaerts, C.; Parmentier, M.; Boeynaems J. Cloning of a human purinergic P2Y receptor coupled to phospholipase C and adenylyl cyclase. J. Biol. Chem., 1997, 272(51), 31969-31973.
15. Hollopeter, G.; Jantzen, H.M.; Vincent, D.; Li, G.; England, L.; Ramakrishnan, V.; Yang, R.B.; Nurden, P.; Nurden, A.; Julius D.; Conley, P.B. Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature, 2001, 409, 202-207.
16. Communi, D.; Gonzalez, N.S.; Detheux, M.; Brézillon, S.; Lannoy, V.; Parmentier, M.; Boeynaems, J.M. Identification of a novel human ADP receptor coupled to Gi. J. Biol. Chem., 2001, 276(44), 41479-41485.
17. Chambers, J.K.; Macdonald, L.E.; Sarau, H.M.; Ames, R.S.; Freeman, K.; Foley, J.J.; Zhu, Y.; McLaughlin, M.M.; Murdock, P.; McMillan, L.; Trill, J.; Swift, A.; Aiyar, N.; Taylor, P.; Vawter, L.; Naheed, S.; Szekeres, P.; Hervieu, G.; Scott, C.; Watson, J.M.; Murphy, A.J.; Duzic, E.; Klein, C.; Bergsma, D.J.; Wilson, S.; Livi, G.P. A G Protein-coupled Receptor for UDP-glucose. J. Biol. Chem., 2000, 275(15), 10767-10771.
18. Liberti, F.; Van Sande, J.; Lefort, A.; Czernilofsky, A.; Dumont, J.E.; Vassart, G.; Ensinger, H.A.; Mendla, K.D. Cloning and functional characterization of a human A1 adenosine receptor. Biochem. Biophys. Res. Commun., 1992, 187, 919-926.
19. Furlong, T.J.; Pierce, K.D.; Selbie, L.A.; Shine, J. Molecular characterization of a human brain adenosine A2 receptor. Mol. Brain Res., 1992, 15(1-2), 62-66.
20. Pierce, K.D.; Furlong, T.J.; Selbie, L.A.; Shine, J. Molecular cloning and expression of an adenosine A2b receptor from human brain. Biochem. Biophys. Res. Commun., 1992, 187(1), 86-93.
21. Salvatore, C.A.; Jacobson, M.A.; Taylor, H.E.; Linden, J.; Johnson, R.G. Molecular cloning and characterization of the human A3 adenosine receptor. Proc. Natl. Acad. Sci. USA, 1993, 90(21), 10365-10369.
22. Maliszewski, C.R.; Delespesse, G.J.; Schoenborn, M.A.; Armitage, R.J.; Fanslow, W.C.; Nakajima, T.; Baker, E.; Sutherland, G.R.; Poindexter, K.; Birks, C.; Alpert, A.; Friend, D.; Gimpel, S.D.; Gayle, R.B. The CD39 Lymphoid Cell Activation Antigen Molecular Cloning and Structural Characterization. J. Immunol., 1994, 153(8), 3574-3583.
23. Hansen, K.R.; Resta, R.; Webb, C.F.; Thompson, L.F. Ecto-5'-nucleotidase (CD73): genomic cloning and characterization of regions upstream of the translation start site. Adv. Exp. Med. Biol., 1994, 370, 689-692.
24. Ralevic, V.; Burnstock, G. Receptors for purines and pyrimidines. Pharmacol. Rev., 1998, 50(3), 413-492.
25. Burnstock, G. Purine and pyrimidine receptors. Cell. Mol. Life Sci., 2007 64(12), 1471-1483.
26. Volonté, C.; D'Ambrosi, N. Membrane compartments and purinergic signalling: the purinome, a complex interplay among ligands, degrading enzymes, receptors and transporters. FEBS J., 2009, 276(2), 318-329.
27. Volonté, C.; Amadio, S.; D'Ambrosi, N. Receptor webs: can the chunking theory tell us more about it? Brain Res. Rev., 2008, 59(1), 1-8.
28. Guo, W.; Xu, X.; Gao, X.; Burnstock, G.; He, C.; Xiang Z. Expression of P2X5 receptors in the mouse CNS. Neuroscience, 2008, 156(3), 673-692.
29. Cheung, K.K.; Chan, W.Y.; 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(4), 937-945.
30. Birdsong, W.T.; Fierro, L.; Williams, F.G.; Spelta, V.; Naves, L.A.; Knowles, M.; Marsh-Haffner, J.; Adelman, J.P.; Almers, W.; Elde, R.P.; McCleskey, E.W. Sensing muscle ischemia: coincident detection of acid and ATP via interplay of two ion channels. Neuron, 2010, 68(4), 739-749.
31. Light, A.R.; White, A.T.; Hughen, R.W.; Light, K.C. Moderate exercise increases expression for sensory, adrenergic, and immune genes in chronic fatigue syndrome patients but not in normal subjects. J. Pain, 2009, 10(10), 1099-1112.
32. Greig, A.V.H.; Linge, C.; Terenghi, G.; McGrouther, D.A.; Burnstock, G. Purinergic receptors are part of a functional signalling system for proliferation and differentiation of human epidermal keratinocytes. J. Invest. Dermatol., 2003, 120(6), 1007-1015.
33. White, N.; Burnstock, G. P2 receptors and cancer. Trends Pharmacol. Sci., 2006, 27(4), 211-217.
34. Burnstock, G.; Verkhratsky, A. Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis., 2010, 1, e9.
35. Chu, Y.; Mouat, M.F.; Coffield, J.A.; Orlando, R.; Grider, A. Expression of P2X6, a purinergic receptor subunit, is affected by dietary zinc deficiency in rat hippocampus. Biol. Trace Elem. Res., 2003, 91(1), 77-87.
36. Loesch, A.; Burnstock, G. Immunoreactivity to P2X(6) receptors in the rat hypothalamo-neurohypophysial system: an ultrastructural study with extravidin and colloidal gold-silver labelling. Neuroscience, 2001, 106(3), 621-631.
37. Da Silva, R.L.; Resende, R.R.; Ulrich H. Alternative splicing of P2X6 receptors in developing mouse brain and during in vitro neuronal differentiation. Exp. Physiol., 2007, 92(1), 139-145.
38. Guénet, J.L. The mouse genome. Genome Res., 2005, 15(12), 1729-1740.
39. Wei, C.J.; Li, W.; Chen, J.F. Normal and abnormal functions of adenosine receptors in the central nervous system revealed by genetic knockout studies. Biochim. Biophys. Acta, 2011, 1808(5), 1358-1379.
40. Johansson, B.; Halldner, L.; Dunwiddie, T.V.; Masino, S.A.; Poelchen, W.; Gimenez-Llort, L.; Escorihuela, R.M.; Fernandez-Teruel, A.; Wiesenfeld-Hallin, Z.; Xu, X.J.; Hardemark, A.; Betsholtz, C.; Herlenius, E.; Fredholm, B.B. Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc. Natl. Acad. Sci. USA, 2001, 98(16), 9407-9412.
41. Sun, D.; Samuelson, L.C.; Yang, T.; Huang, Y.; Paliege, A.; Saunders T.; Briggs, J.; Schnermann, J. Mediation of tubuloglomerular feedback by adenosine: evidence from mice lacking adenosine 1 receptors. Proc. Natl. Acad. Sci. USA, 2001, 98(17), 9983-9988.
42. Bjorness, T.E.; Kelly, C.L.; Gao, T.; Poffenberger, V.; Greene, R.W. Control and function of the homeostatic sleep response by adenosine A1 receptors. J. Neurosci., 2009, 29(5), 1267-1276.
43. Halassa, M.M.; Florian, C.; Fellin, T.; Munoz, J.R.; Lee, S.Y.; Abel, T.; Haydon, P.G.; Frank, M.G. Astrocytic modulation of sleep hom eostasis and cognitive consequences of sleep loss. Neuron, 2009, 61(2), 213-219.
44. Masino, S.A.; Diao, L.; Illes, P.;. Zahniser, N.R.; Larson, G.A.; Johansson, B.; Fredholm, B.B.; Dunwiddie, T.V. Modulation of hippocampal glutamatergic transmission by ATP is dependent on adenosine a(1) receptors. J. Pharmacol. Exp. Ther., 2002, 303(1), 356-363.
45. Tsutsui, S.; Schnermann, J.; Noorbakhsh, F.; Henry, S.; Yong, V.W.; Winston, B.W.; Warren, K.; Power, C. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J. Neurosci., 2004, 24(6), 1521-1529.
46. Ledent, C.; Vaugeois, J.M.; Schiffmann S.N.; Pedrazzini, T.; El Yacoubi M.; Vanderhaeghen J.J.; Costentin, J.; Heath, J.K.; Vassart G.; Parmentier, M. Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor. Nature, 1997, 388(6643), 674-678.
47. Chen, J.F.; Huang, Z.; Ma, J.; Zhu, J.; Moratalla, R.; Standaert, D.; Moskowitz, M.A.; Fink, J.S.; Schwarzschild, M.A. A(2A) adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J. Neurosci., 1999, 19(21), 9192-9200.
48. Day, Y.J.; Huang, L.; McDuffie, M.J.; Rosin, D.L.; Ye, H.; Chen, J.F.; Schwarzschild, M.A.; Fink, J.S.; Linden, J.; Okusa, M.D. Renal protection from ischemia mediated by A2A adenosine receptors on bone marrow-derived cells. J. Clin. Invest., 2003, 112(6), 883-891.
49. Huang, Q.Y.; Wei, C.; Yu, L.; Coelho, J.E.; Shen, H.Y.; Kalda, A.; Linden, J.; Chen, J.F. Adenosine A2A receptors in bone marrowderived cells but not in forebrain neurons are important contributors to 3-nitropropionic acid-induced striatal damage as revealed by cell-type-selective inactivation. J. Neurosci., 2006, 26(44), 11371-11378.
50. Huang, Z.L.; Qu, W.M.; Eguchi, N.; Chen, J.F.; Schwarzschild, M.A.; Fredholm, B.B.; Urade, Y.; Hayaishi, O. Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nat. Neurosci., 2005, 8(7), 858-859.
51. Tebano, M.T.; Martire, A.; Potenza, R.L.; Gro, C.; Pepponi, R.; Armida, M.; Domenici, M.R.; Schwarzschild, M.A.; Chen, J.F.; Popoli P. Adenosine A(2A) receptors are required for normal BDNF levels and BDNF-induced potentiation of synaptic transmission in the mouse hippocampus. J. Neurochem., 2008, 104(1), 279-286.
52. Zhou, S.J.; Zhu, M.E.; Shu, D.; Du, X.P.; Song, X.H.; Wang, X.T.; Zheng, R.Y.; Cai, X.H.; Chen, J.F.; He, J.C. Preferential enhancement of working memory in mice lacking adenosine A(2A) receptors. Brain Res., 2009, 1303, 74-83.
53. Dai, S.S.; Zhou, Y.G.; Li, W.; An, J.H.; Li, P.; Yang, N.; Chen, X.Y.; Xiong, R.P.; Liu, P.; Zhao, Y.; Shen, H.Y.; Zhu, P.F.; Chen, J.F. Local glutamate level dictates adenosine A2A receptor regulation of neuroinflammation and traumatic brain injury. J. Neurosci., 2010, 30(16), 5802-5810.
54. Yang, D.; Zhang, Y.; Nguyen, H.G.; Koupenova, M.; Chauhan, A.K.; Makitalo, M.; Jones, M.R.; St Hilaire, C.; Seldin, D.C.; Toselli, P.; Lamperti, E.; Schreiber, B.M.; Gavras, H.; Wagner, D.D.; Ravid, K. The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J. Clin. Invest., 2006, 116(7), 1913-1923.
55. Hu, X.; Kovarova, M.; Chason, K.D.; Nguyen, M.; Koller, B.H.; Tilley, S.L. Enhanced mast cell activation in mice deficient in the A2b adenosine receptor. J. Exp. Med., 2007, 204(1), 117-128.
56. Salvatore, C.A.; Tilley, S.L.; Latour, A.M.; Fletcher, D.S.; Koller, B.H.; Jacobson, M.A. Disruption of the A(3) adenosine receptor gene in mice and its effect on stimulated inflammatory cells. J. Biol. Chem., 2000, 275(6), 4429-4434.
57. Avila, M.Y.; Stone, R.A.; Civan, M.M. Knockout of A3 adenosine receptors reduces mouse intraocular pressure. Investig. Ophthalmol. Vis. Sci., 2002, 43(9), 3021-3026.
58. Mulryan, K.; Gitterman, D.P.; Lewis, C.J.; Vial, C.; Leckie, B.J.; Cobb, A.L.; Brown, J.E.; Conley, E.C., Buell, G.; Pritchard, C.A.; Evans, R.J. Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature, 2000, 403(6765), 86-89.
59. Shour, F.; Atterbury-Thomas, M.; Deuchars, J.; Evans, R.J. An evaluation of antibody detection of the P2X1 receptor subunit in the CNS of wild type and P2X1-knockout mice. Neurosci. Lett., 2006, 397(1-2), 120-125.
60. Cockayne, D.A.; Dunn, P.M.; Zhong, Y.; Rong, W.; Hamilton, S.G.; Knight, G.E.; Ruan, H.Z.; Ma, B.; Yip, P.; Nunn.; McMahon, S.B.; Burnstock, G.; 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., 2005, 567(Pt 2), 621-639.
61. Custer, E.E.; Knott, T.K.; Quadra, A.E.; Ortiz-Miranda, S.; Lemos, J.R. P2X purinergic receptor knockout mice reveal endogenous ATP modulation of both vasopressin and oxytocin release from the intact neurohypophysis. J. Neuroendocrinol., 2012, 24(4), 674-680.
62. 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 pain-related behaviour in P2X3-deficient mice. Nature, 2000, 407(6807), 1011-1015.
63. Wang, Y.; Mackes, J.; Chan, S.; Haughey, N.J.; Guo, Z.; Ouyang, X.; Furukawa, K.; Ingram, D.K.; Mattson, M.P. Impaired long-term depression in P2X3 deficient mice is not associated with a spatial learning deficit. J. Neurochem., 2006, 99(5), 1425-1434.
64. Sim, J.A.; Chaumont, S.; Jo, J.; Ulmann, L.; Young, M.T.; Cho, K.; Buell, G.; North, R.A.; Rassendren, F. Altered hippocampal synaptic potentiation in P2X4 knock-out mice. J. Neurosci., 2006, 26(35), 9006-9009.
65. Baxter, A.W.; Choi, S.J.; Sim, J.A.; North, R.A. Role of P2X4 receptors in synaptic strengthening in mouse CA1 hippocampal neurons. Eur. J. Neurosci., 2011, 34(2), 213-220.
66. Ulmann, L.; Hatcher, J.P.; Hughes, J.P.; Chaumont, S.; Green, P.J.; Conquet, F.; Buell, G.N.; Reeve, A.J.; Chessell, I.P.; Rassendren, F. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci., 2008, 28(44), 11263-11268.
67. Solle, M.; Labasi, J.; Perregaux, D.G.; Stam, E.; Petrushova, N.; Koller, B.H.; Griffiths, R.J.; Gabel, C.A. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem., 2001, 276(1), 125-132.
68. Chessell, I.P.; Hatcher, J.P.; Bountra, C.; Michel, A.D.; Hughes, J.P.; Green, P.; Egerton, J.; Murfin, M.; Richardson, J.; Peck, W.L.; Grahames, C.B.; Casula, M.A.; Yiangou, Y.; Birch, R.; Anand, P.; Buell, G.N. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain, 2005, 114(3), 386-396.
69. Nicke, A.; Kuan, Y.H.; Masin, M.; Rettinger, J.; Marquez-Klaka, B.; Bender, O.; Górecki, D.C.; Murrell-Lagnado, R.D.; Soto, F. A functional P2X7 splice variant with an alternative transmembrane domain 1 escapes gene inactivation in P2X7 knock-out mice. J. Biol. Chem., 2009, 284(38), 25813-25822.
70. Masin, M.; Young, C.; Lim, K.; Barnes, S.J.; Xu, X.J.; Marschall, V.; Brutkowski, W.; Mooney, E.R.; Gorecki, D.C.; Murrell-Lagnado, R. Expression, assembly and function of novel Cterminal truncated variants of the mouse P2X7 receptor: reevaluation of P2X7 knockouts. Br. J. Pharmacol., 2012, 165(4), 978-993.
71. Fabre, J.E.; Nguyen, M.; Latour, A.; Keifer, J.A.; Audoly, L.P.; Coffman, T.M.; Koller, B.H. Decreased platelet aggregation, increased bleeding time and resistance to thromboembolism in P2Y1-deficient mice. Nat. Med., 1999, 5(10), 1199-2102.
72. Léon, C.; Hechler, B.; Freund, M.; Eckly, A.; Vial, C.; Ohlmann, P.; Dierich, A.; LeMeur, M.; Cazenave, J.P.; Gachet, C. Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y(1) receptor-null mice. J. Clin. Invest., 1999, 104(12), 1731-1737.
73. Guzman, S.J.; Schmidt, H.; Franke, H.; Krügel, U.; Eilers, J.; Illes, P.; Gerevich Z. P2Y1 receptors inhibit long-term depression in the prefrontal cortex. Neuropharmacology, 2010, 59(6), 406-415.
74. Homolya, L.; Watt, W.C.; Lazarowski, E.R.; Koller, B.H.; Boucher, R.C. Nucleotide-regulated calcium signaling in lung fibroblasts and epithelial cells from normal and P2Y(2) receptor (-/-) mice. J. Biol. Chem., 1999, 274(37), 26454-26460.
75. Chen, Y.; Corriden, R.; Inoue, Y.; Yip, L.; Hashiguchi, N.; Zinkernagel, A.; Nizet, V.; Insel, P.A.; Junger, W.G. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science, 2006, 314(5806), 1792-1795.
76. Elliott, M.R.; Chekeni, F.B.; Trampont, P.C.; Lazarowski, E.R.; Kadl, A.; Walk, S.F.; Park, D.; Woodson, R.I.; Ostankovich, M.; Sharma, P.; Lysiak, J.J.; Harden, T.K.; Leitinger, N.; Ravichandran, K.S. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature, 2009, 461(7261), 282-286.
77. Malin, S.A.; Davis, B.M.; Koerber, H.R.; Reynolds, I.J.; Albers, K.M.; Molliver, D.C. Thermal nociception and TRPV1 function are attenuated in mice lacking the nucleotide receptor P2Y2. Pain, 2008, 138(3), 484-496.
78. Robaye, B.; Ghanem, E.; Wilkin, F.; Fokan, D.; Van Driessche, W.; Schurmans, S.; Boeynaems, J.M.; Beauwens, R. Loss of nucleotide regulation of epithelial chloride transport in the Jejunum of P2Y4-null mice. Pharmacology, 2003 63(4), 777-778.
79. Horckmans, M.; Robaye, B.; Léon-Gmez, E.; Lantz, N.; Unger, P.; Dol-Gleizes, F.; Clouet, S.; Cammarata, D.; Schaeffer, P.; Savi, P.; Gachet, C.; Balligand, J.L.; Dessy, C.; Boeynaems, J.M.; Communi, D. P2Y(4) nucleotide receptor: a novel actor in postnatal cardiac development. Angiogenesis, 2012.
80. Matos, J.E.; Robaye, B.; Boeynaems, J.M.; Beauwens, R.; Leipziger, J. K+ secretion activated by luminal P2Y2 and P2Y4 receptors in mouse colon. J. Physiol., 2005, 564(Pt 1), 269-279.
81. Bar, I.; Guns, P.J.; Metallo, J.; Cammarata, D.; Wilkin, F.; Boeynams, J.M.; Bult, H.; Robaye, B. Knockout mice reveal a role for P2Y6 receptor in macrophages, endothelial cells, and vascular smooth muscle cells. Mol. Pharmacol., 2008, 7(3), 777-784.
82. Andre, P.; Delaney, S.M.; LaRocca T.; Vincent, D.; DeGuzman, F.; Jurek, M.; Koller, B.; Phillips, D.R.; Conley, P.B. P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J. Clin. Invest., 2003, 11(3), 398-406.
83. Tozaki-Saitoh, H.; Tsuda, M.; Miyata, H.; Ueda, K.; Kohsaka, S.; Inoue, K. P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury. J. Neurosci., 2008, 28(19), 4949-4956.
84. Haynes, S.E.; Hollopeter, G.; Yang, G.; Kurpius, D.; Dailey, M.E.; Gan, W.B.; Julius, D. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci., 2006, 9(12), 1512-1519.
85. Amadio, S.; Montilli, C.; Magliozzi, R.; Bernardi, G.; Reynolds, R.; Volonté C. P2Y12 receptor protein in cortical gray matter lesions in multiple sclerosis. Cereb. Cortex, 2010, 20(6), 1263-1273.
86. Blom, D.; Yamin, T.T.; Champy, M.F.; Selloum, M.; Bedu, E.; Carballo-Jane, E.; Gerckens, L; Luell, S.; Meurer, R.; Chin, J.; Mudgett, J.; Puig, O. Altered lipoprotein metabolism in P2Y(13) knockout mice. Biochim. Biophys. Acta, 2010, 1801(12), 1349-1360.
87. Bassil, A.K.; Bourdu, S.; Townson, K.A.; Wheeldon, A.; Jarvie, E.M.; Zebda, N.; Abuin, A.; Grau, E.; Livi, G.P.; Punter, L.; Latcham, J.; Grimes, A.M.; Hurp, D.P.; Downham, K.M.; Sanger, G.J.; Winchester, W.J.; Morrison, A.D.; Moore, G.B. UDP-glucose modulates gastric function through P2Y14 receptor-dependent and-independent mechanisms. Am. J. Physiol. Gastrointest., Liver Physiol., 2009, 296(4), G923-G930.
88. Malin, S.A.; Molliver, D.C. Gi-and Gq-coupled ADP (P2Y) receptors act in opposition to modulate nociceptive signaling and inflammatory pain behavior. Mol. Pain, 2010, 6, 21.
89. Enjyoji, K.; Sévigny, J.; Lin, Y.; Frenette, P.S.; Christie, P.D.; Esch, J.S., 2nd; Imai, M.; Edelberg, J.M.; Rayburn, H.; Lech, M.; Beeler, D.L.; Csizmadia, E.; Wagner, D.D.; Robson, S.C.; Rosenberg, R.D. Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat. Med., 1999, 5(9), 1010-1017.
90. Färber, K.; Markworth, S.; Pannasch, U.; Nolte, C.; Prinz, V.; Kronenberg, G.; Gertz, K.; Endres, M.; Bechmann, I.; Enjyoji, K.; Robson, S.C.; Kettenmann, H. The ectonucleotidase cd39/ENTPDASE1 modulates purunergic-mediated microglial migration. Glia, 2008, 56(3), 331-341.
91. Thompson, L.F.; Eltzschig, H.K.; Ibla, J.C.; Van De Wiele, C.J.; Resta, R.; Morote-Garcia, J.C.; Colgan, S.P. Crucial role for ecto-5'-nucleotidase (CD73) in vascular leakage during hypoxia. J. Exp. Med., 2004, 200(11), 1395-1405.
92. Sowa, N.A.; Taylor-Blake, B.; Zylka, M.J. Ecto-5'-nucleotidase (CD73) inhibits nociception by hydrolyzing AMP to adenosine in nociceptive circuits. J. Neurosci., 2010, 30(6), 2235-2244.
93. Kawate, T.; Michel, J.C.; Birdsong, W.T.; Gouaux, E. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature, 2009, 460(7255), 592-598.
94. Jiang, R.; Lemoine, D.; Martz, A.; Taly, A.; Gonin, S.; Prado de Carvalho, L.; Specht, A.; Grutter, T. Agonist trapped in ATP binding sites of the P2X2 receptor. Proc. Natl. Acad. Sci. USA, 2011, 108(22), 9066-9071.
95. Kracun, S.; Chaptal, V.; Abramson, J.; Khakh, B.S. Gated access to the pore of a P2X receptor: structural implications for closed-open transitions. J. Biol. Chem., 2010, 285(13), 10110-10121.
96. Hattori, M.; Gouaux, E. Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature, 2012, 485(7397), 207-212.
97. Okada, T.; Le Trong, I.; Fox, B.A.; Behnke, C.A.; Stenkamp, R.E.; Palczewski, K. X-Ray diffraction analysis of three-dimensional crystals of bovine rhodopsin obtained from mixed micelles. J. Struct. Biol., 2000, 130(1), 73-80.
98. Jaakola, V.P.; Griffith, M.T.; Hanson, M.A.; Cherezov, V.; Chien, E.Y.; Lane, J.R.; Ijzerman, P.; Stevens, R.C. The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science, 2008, 322(5905), 1211-1217.
99. Dal Ben, D.; Lambertucci, C.; Marucci, G.; Volpini, R.; Cristalli G. Adenosine receptor modeling: what does the A2A crystal structure tell us? Curr. Top. Med. Chem., 2010, 10(10), 993-1018.
100. Doré, A.S.; Robertson, N.; Errey, J.C.; Ng, I.; Hollenstein, K.; Tehan, B.; Hurrell, E.; Ennett, K.; Congreve, M.; Magnani, F.; Tate, C.G.; Weir, M.; Marshall, F.H. Structure of the denosine A(2A) receptor in complex with ZM241385 and the xanthines XAC and caffeine. Structure, 2011, 19(9), 1283-1293.
101. Lebon, G.; Warne, T.; Edwards, P.C.; Bennett, K.; Langmead, C.J.; Leslie, A.G.; Tate, C.G. Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature, 2011, 474(7352), 521-525.
102. Piirainen, H.; Ashok, Y.; Nanekar, R.T.; Jaakola, V.P. Structural features of adenosine receptors: from crystal to function. Biochim. Biophys. Acta, 2011, 1808(5), 1233-1244.
103. Rodríguez, D.; Piñeiro, Á.; Gutiérrez-de-Terán, H. Molecular dynamics simulations reveal insights into key structural elements of adenosine receptors. Biochemistry, 2011, 50(19), 4194-4208.
104. Vivian, J.P.; Riedmaier, P.; Ge, H.; Le Nours, J.; Sansom, F.M.; Wilce, M.C.; Byres, E.; Dias, M.; Schmidberger, J.W.; Cowan, P.J.; d'Apice, A.J.; Hartland, E.L.; Rossjohn, J.; Beddoe, T. Crystal structure of a Legionella pneumophila ecto-triphosphate diphosphohydrolase, a structural and functional homolog of the eukaryotic NTPDases. Structure, 2010, 18(2), 228-238.
105. Zebisch, M.; Krauss, M.; Schäfer, P.; Sträter, N.J. Crystallographic evidence for a domain motion in rat nucleoside triphosphate diphosphohydrolase (NTPDase) 1. Mol. Biol., 2012, 415(2), 288-306.
106. Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2), 281-297.
107. Selbach, M.; Schwanhausser, B.; Thierfelder, N.; Fang, Z.; Khanin, R.; Rajewsky, N. Widespread changes in protein synthesis induced by micro-RNAs. Nature, 2008, 455(7209), 58-63.
108. Baek, D.; Villen, J.; Shin, C.; Camargo, F.D.; Gygi, S.P.; Bartel, D.P. The impact of microRNAs on protein output. Nature, 2008, 455(7209), 64-71.
109. 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.
110. von Schack, D.; Agostino, M.J.; Murray, B.S.; Li, Y.; Reddy, P.S.; Chen, J.; Choe, S.E.; Strassle, B.W.; Li, C.; Bates, B.; Zhang, L.; Hu, H.; Kotnis, S.; Bingham, B.; Liu, W.; Whiteside, G.T.; Samad, T.A.; Kennedy, J.D.; Ajit, S.K. Dynamic changes in the microRNA expression profile reveal multiple regulatory mechanisms in the spinal nerve ligation model of neuropathic pain. PLoS One, 2011, 6(3), e17670.
111. Wang, Q.; Wang, L.; Feng, Y.H.; Li, X.; Zeng, R.; Gorodeski, G.I. P2X7 receptor-mediated apoptosis of human cervical epithelial cells. Am. J. Physiol., 2004, 287(5), C1349-C134958.
112. Zhou, L.; Qi, X.; Potashkin, J.A.; Abdul-Karim, F.W.; Gorodeski, G.I. MicroRNAs miR-186 and miR-150 down-regulate expression of the pro-apoptotic purinergic P2X7 receptor by activation of instability sites at the 3'-untranslated region of the gene that decrease steady-state levels of the transcript. J. Biol. Chem., 2008, 283(42), 28274-28286.
113. Borel, C.; Antonarakis, S.E. Functional genetic variation of human miRNAs and phenotypic consequences. Mamm. Genome, 2008, 19(7-8), 503-509.
114. Mishra, P.J.; Banerjee, D.; Bertino, J.R. MiRSNPs or MiRpolymorphisms, new players in microRNA mediated regulation of the cell: Introducing microRNA pharmacogenomics Cell Cycle, 2008, 7(7), 853-858.
115. Sethupathy, P.; Collins, F.S. MicroRNA target site polymorphisms and human disease. Trends Genet., 2008, 24(10), 489-497.
116. Wang, L.; Ostberg, O.; Wihlborg, A.K.; Brogren, H.; Jern, S.; Erlinge, D. Quantification of ADP and ATP receptor expression in human platelets. J. Thromb. Haemost., 2003, 1(2), 330-336.
117. Landry, P.; Plante, I.; Ouellet, D.L.; Perron, M.P.; Rousseau, G.; Provost, P. Existence of a microRNA pathway in anucleate platelets. Nat. Struct. Mol. Biol., 2009, 16(9), 961-966.
118. Heyn, J.; Ledderose, C.; Hinske, L.C.; Limbeck, E., Möhnle, P.; Lindner, H.A.; Kreth, S. Adenosine A2A receptor upregulation in human PMNs is controlled by miRNA-214, miRNA-15, and miRNA-16. Shock, 2012, 37(2), 156-163.
119. Kolachala, V.L.; Wang, L.; Obertone, T.S.; Prasad, M.; Yan, Y.; Dalmasso, G.; Gewirtz, A.T.; Merlin, D.; Sitaraman, S.V. Adenosine 2B receptor expression is post-transcriptionally regulated by microRNA. J. Biol. Chem., 2010, 285(24), 18184-18190.