P2X7 receptor antagonism: Implications in diabetic retinopathy

Biochemical Pharmacology

Volumn 138, Issue , 2017, Pages 130-139

  Platania, Chiara Bianca Maria ^a   Giurdanella, Giovanni ^a   Di Paola, Luisa ^b   Leggio, Gian Marco ^a   Drago, Filippo ^a   Salomone, Salvatore ^a   Bucolo, Claudio ^a  

^a UNIVERSITY OF CATANIA   (Italy)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

Diabetic retinopathy; IL 1 ; Inflammation; Molecular modeling; P2X7 receptor; Pericytes

Indexed keywords

GLUCOSE; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X7 RECEPTOR; BIOLOGICAL MARKER; JNJ-47965567; LIGAND; NICOTINAMIDE; NONSTEROID ANTIINFLAMMATORY AGENT; P2XR RECEPTOR, HUMAN; PIPERAZINE DERIVATIVE;

ALLOSTERIC SITE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DIABETIC RETINOPATHY; DRUG ABSORPTION; DRUG DISTRIBUTION; DRUG EXCRETION; DRUG METABOLISM; ENZYME RELEASE; HUMAN; HUMAN CELL; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR DOCKING; MOLECULAR MODEL; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN INTERACTION; RETINA CELL; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; BIOLOGY; CELL CULTURE; CHEMICAL DATABASE; CHEMISTRY; CONFORMATION; DRUG EFFECTS; EXPERT SYSTEM; IMMUNOLOGY; METABOLISM; PATHOLOGY; PROTEIN DATABASE; RECEIVER OPERATING CHARACTERISTIC; STRUCTURAL HOMOLOGY;

ALLOSTERIC SITE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; BIOMARKERS; CELLS, CULTURED; COMPUTATIONAL BIOLOGY; DATABASES, CHEMICAL; DATABASES, PROTEIN; DIABETIC RETINOPATHY; EXPERT SYSTEMS; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DOCKING SIMULATION; NIACINAMIDE; PERICYTES; PIPERAZINES; PURINERGIC P2X RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2X7; ROC CURVE; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 85018914127     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2017.05.001     Document Type: Article

References (58)

1. Klein, R., Klein, B.E., Body fat distribution and diabetic retinopathy in people with Type 2 diabetes. JAMA 315:16 (2016), 1778–1779.
2. Forga, L., Goni, M.J., Ibanez, B., Cambra, K., Garcia-Mouriz, M., Iriarte, A., Influence of age at diagnosis and time-dependent risk factors on the development of diabetic retinopathy in patients with Type 1 diabetes. J. Diab. Res., 2016, 2016, 9898309.
3. Mizutani, M., Kern, T.S., Lorenzi, M., Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J. Clin. Investig. 97:12 (1996), 2883–2890.
4. Hammes, H.P., Feng, Y., Pfister, F., Brownlee, M., Diabetic retinopathy: targeting vasoregression. Diabetes 60:1 (2011), 9–16.
5. Ejaz, S., Chekarova, I., Ejaz, A., Sohail, A., Lim, C.W., Importance of pericytes and mechanisms of pericyte loss during diabetes retinopathy. Diabetes Obes. Metab. 10:1 (2008), 53–63.
6. Diabetic Retinopathy Clinical Research, N., Randomized clinical trial evaluating intravitreal ranibizumab or saline for vitreous hemorrhage from proliferative diabetic retinopathy. JAMA Ophthalmol. 131:3 (2013), 283–293.
7. Feenstra, D.J., Yego, E.C., Mohr, S., Modes of retinal cell death in diabetic retinopathy. J. Clin. Exp. Ophthalmol., 4(5), 2013, 298.
8. Sanderson, J., Dartt, D.A., Trinkaus-Randall, V., Pintor, J., Civan, M.M., Delamere, N.A., Fletcher, E.L., Salt, T.E., Grosche, A., Mitchell, C.H., Purines in the eye: recent evidence for the physiological and pathological role of purines in the RPE, retinal neurons, astrocytes. Muller cells, lens, trabecular meshwork, cornea and lacrimal gland. Exp. Eye Res. 127 (2014), 270–279.
9. Kerur, N., Hirano, Y., Tarallo, V., Fowler, B.J., Bastos-Carvalho, A., Yasuma, T., Yasuma, R., Kim, Y., Hinton, D.R., Kirschning, C.J., Gelfand, B.D., Ambati, J., TLR-independent and P2X7-dependent signaling mediate Alu RNA-induced NLRP3 inflammasome activation in geographic atrophy. Invest. Ophthalmol. Vis. Sci. 54:12 (2013), 7395–7401.
10. Beckel, J.M., Argall, A.J., Lim, J.C., Xia, J., Lu, W., Coffey, E.E., Macarak, E.J., Shahidullah, M., Delamere, N.A., Zode, G.S., Sheffield, V.C., Shestopalov, V.I., Laties, A.M., Mitchell, C.H., Mechanosensitive release of adenosine 5’-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: a mechanism for purinergic involvement in chronic strain. Glia 62:9 (2014), 1486–1501.
11. Portillo, J.C., Corcino, Y.L., Miao, Y., Tang, J., Sheibani, N., Kern, T.S., Dubyak, G.R., Subauste, C.S., CD40 in Retinal Muller Cells Induces P2X7-dependent cytokine expression in macrophages/microglia in diabetic mice and development of early experimental diabetic retinopathy. Diabetes, 2016.
12. Kawamura, H., Sugiyama, T., Wu, D.M., Kobayashi, M., Yamanishi, S., Katsumura, K., Puro, D.G., ATP: a vasoactive signal in the pericyte-containing microvasculature of the rat retina. J. Physiol. 551:Pt 3 (2003), 787–799.
13. Sugiyama, T., Kawamura, H., Yamanishi, S., Kobayashi, M., Katsumura, K., Puro, D.G., Regulation of P2X7-induced pore formation and cell death in pericyte-containing retinal microvessels. Am. J. Physiol. Cell Physiol. 288:3 (2005), C568–C576.
14. Sugiyama, T., Kobayashi, M., Kawamura, H., Li, Q., Puro, D.G., Enhancement of P2X(7)-induced pore formation and apoptosis: an early effect of diabetes on the retinal microvasculature. Invest. Ophthalmol. Vis. Sci. 45:3 (2004), 1026–1032.
15. Newman, E.A., Propagation of intercellular calcium waves in retinal astrocytes and Muller cells. J. Neurosci. 21:7 (2001), 2215–2223.
16. Corriden, R., Insel, P.A., Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci. Signal., 3(104), 2010 re1.
17. Karmakar, M., Katsnelson, M.A., Dubyak, G.R., Pearlman, E., Neutrophil P2X7 receptors mediate NLRP3 inflammasome-dependent IL-1beta secretion in response to ATP. Nat. Commun., 7, 2016, 10555.
18. Caseley, E.A., Muench, S.P., Fishwick, C.W., Jiang, L.H., Structure-based identification and characterisation of structurally novel human P2X7 receptor antagonists. Biochem. Pharmacol. 116 (2016), 130–139.
19. Capitao, M., Soares, R., Angiogenesis and inflammation crosstalk in diabetic retinopathy. J. Cell. Biochem. 117:11 (2016), 2443–2453.
20. Lister, M.F., Sharkey, J., Sawatzky, D.A., Hodgkiss, J.P., Davidson, D.J., Rossi, A.G., Finlayson, K., The role of the purinergic P2X7 receptor in inflammation. J. Inflamm., 4, 2007, 5.
21. Gombault, A., Baron, L., Couillin, I., ATP release and purinergic signaling in NLRP3 inflammasome activation. Front. Immunol., 3, 2012, 414.
22. Giuliani, A.L., Sarti, A.C., Falzoni, S., Di Virgilio, F., The P2X7 Receptor-Interleukin-1 Liaison. Front. Pharmacol., 8, 2017, 123.
23. Kowluru, R.A., Zhong, Q., Kanwar, M., Metabolic memory and diabetic retinopathy: role of inflammatory mediators in retinal pericytes. Exp. Eye Res. 90:5 (2010), 617–623.
24. Nehme, A., Edelman, J., Dexamethasone inhibits high glucose-, TNF-alpha-, and IL-1beta-induced secretion of inflammatory and angiogenic mediators from retinal microvascular pericytes. Invest. Ophthalmol. Vis. Sci. 49:5 (2008), 2030–2038.
25. Bhattacharya, A., Wang, Q., Ao, H., Shoblock, J.R., Lord, B., Aluisio, L., Fraser, I., Nepomuceno, D., Neff, R.A., Welty, N., Lovenberg, T.W., Bonaventure, P., Wickenden, A.D., Letavic, M.A., Pharmacological characterization of a novel centrally permeable P2X7 receptor antagonist: JNJ-47965567. Br. J. Pharmacol. 170:3 (2013), 624–640.
26. Arnold, K., Bordoli, L., Kopp, J., Schwede, T., The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:2 (2006), 195–201.
27. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Gallo Cassarino, T., Bertoni, M., Bordoli, L., Schwede, T., SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42:1 (2014), W252–W258 (Web Server issue).
28. Karasawa, A., Kawate, T., Structural basis for subtype-specific inhibition of the P2X7 receptor. eLife, 5, 2016.
29. Phillips, J.C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R.D., Kale, L., Schulten, K., Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:16 (2005), 1781–1802.
30. Tse, A., Verkhivker, G.M., Molecular dynamics simulations and structural network analysis of c-Abl and c-Src kinase core proteins: capturing allosteric mechanisms and communication pathways from residue centrality. J. Chem. Inf. Model. 55:8 (2015), 1645–1662.
31. Tse, A., Verkhivker, G.M., Exploring molecular mechanisms of paradoxical activation in the BRAF kinase dimers: atomistic simulations of conformational dynamics and modeling of allosteric communication networks and signaling pathways. PLoS ONE, 11(11), 2016, e0166583.
32. Platania, C.B., Di Paola, L., Leggio, G.M., Romano, G.L., Drago, F., Salomone, S., Bucolo, C., Molecular features of interaction between VEGFA and anti-angiogenic drugs used in retinal diseases: a computational approach. Frontiers in pharmacology, 6, 2015, 248.
33. Blacklock, K., Verkhivker, G.M., Computational modeling of allosteric regulation in the hsp90 chaperones: a statistical ensemble analysis of protein structure networks and allosteric communications. PLoS Comput. Biol., 10(6), 2014, e1003679.
34. Ullman, J.D., Yannakakis, M., High-probability parallel transitive-closure algorithms. SIAM J. Comput. 20:1 (1991), 100–125.
35. Amitai, G., Shemesh, A., Sitbon, E., Shklar, M., Netanely, D., Venger, I., Pietrokovski, S., Network analysis of protein structures identifies functional residues. J. Mol. Biol. 344:4 (2004), 1135–1146.
36. Chakrabarty, B., Parekh, N., Identifying tandem Ankyrin repeats in protein structures. BMC Bioinformatics, 15, 2014, 6599.
37. Das, A., Gur, M., Cheng, M.H., Jo, S., Bahar, I., Exploring the conformational transitions of biomolecular systems using a simple two-state Anisotropic Network Model (vol 10, e1003521, 2014). PLoS Comput. Biol., 10(8), 2014.
38. Cimini, S., Di Paola, L., Giuliani, A., Ridolfi, A., De Gara, L., GH32 family activity: a topological approach through protein contact networks. Plant Mol. Biol., 2016.
39. Hattori, M., Gouaux, E., Molecular mechanism of ATP binding and ion channel activation in P2X receptors. Nature 485:7397 (2012), 207–212.
40. Bartlett, R., Stokes, L., Sluyter, R., The P2X7 receptor channel: recent developments and the Use of P2X7 antagonists in models of disease. Pharmacol. Rev. 66:3 (2014), 638–675.
41. Donnelly-Roberts, D.L., Namovic, M.T., Surber, B., Vaidyanathan, S.X., Perez-Medrano, A., Wang, Y., Carroll, W.A., Jarvis, M.F., [3H]A-804598 ([3H]2-cyano-1-[(1S)-1-phenylethyl]-3-quinolin-5-ylguanidine) is a novel, potent, and selective antagonist radioligand for P2X7 receptors. Neuropharmacology 56:1 (2009), 223–229.
42. Michel, A.D., Chambers, L.J., Walter, D.S., Negative and positive allosteric modulators of the P2X(7) receptor. Br. J. Pharmacol. 153:4 (2008), 737–750.
43. Di Paola, L., Giuliani, A., Protein contact network topology: a natural language for allostery. Curr. Opin. Struct. Biol. 31 (2015), 43–48.
44. James, K.A., Verkhivker, G.M., Structure-based network analysis of activation mechanisms in the ErbB family of receptor tyrosine kinases: the regulatory spine residues are global mediators of structural stability and allosteric interactions. PLoS ONE, 9(11), 2014, e113488.
45. Halgren, T.A., Identifying and characterizing binding sites and assessing druggability. J. Chem. Inf. Model. 49:2 (2009), 377–389.
46. Caseley, E.A., Muench, S.P., Baldwin, S.A., Simmons, K., Fishwick, C.W., Jiang, L.H., Docking of competitive inhibitors to the P2X7 receptor family reveals key differences responsible for changes in response between rat and human. Bioorg. Med. Chem. Lett. 25:16 (2015), 3164–3167.
47. Giurdanella, G., Anfuso, C.D., Olivieri, M., Lupo, G., Caporarello, N., Eandi, C.M., Drago, F., Bucolo, C., Salomone, S., Aflibercept, bevacizumab and ranibizumab prevent glucose-induced damage in human retinal pericytes in vitro, through a PLA2/COX-2/VEGF-A pathway. Biochem. Pharmacol. 96:3 (2015), 278–287.
48. Lupo, G., Motta, C., Giurdanella, G., Anfuso, C.D., Alberghina, M., Drago, F., Salomone, S., Bucolo, C., Role of phospholipases A2 in diabetic retinopathy: in vitro and in vivo studies. Biochem. Pharmacol. 86:11 (2013), 1603–1613.
49. Franceschini, A., Capece, M., Chiozzi, P., Falzoni, S., Sanz, J.M., Sarti, A.C., Bonora, M., Pinton, P., Di Virgilio, F., The P2X7 receptor directly interacts with the NLRP3 inflammasome scaffold protein. FASEB J. 29:6 (2015), 2450–2461.
50. del Sol, A., Fujihashi, H., Amoros, D., Nussinov, R., Residue centrality, functionally important residues, and active site shape: analysis of enzyme and non-enzyme families. Protein Sci.: A Publ. Protein Soc. 15:9 (2006), 2120–2128.
51. Kowalski, M., Hausmann, R., Dopychai, A., Grohmann, M., Franke, H., Nieber, K., Schmalzing, G., Illes, P., Riedel, T., Conformational flexibility of the agonist binding jaw of the human P2X3 receptor is a prerequisite for channel opening. Br. J. Pharmacol. 171:22 (2014), 5093–5112.
52. Jiang, R., Taly, A., Lemoine, D., Martz, A., Cunrath, O., Grutter, T., Tightening of the ATP-binding sites induces the opening of P2X receptor channels. EMBO J. 31:9 (2012), 2134–2143.
53. Michel, A.D., Ng, S.W., Roman, S., Clay, W.C., Dean, D.K., Walter, D.S., Mechanism of action of species-selective P2X(7) receptor antagonists. Br. J. Pharmacol. 156:8 (2009), 1312–1325.
54. Michel, A.D., Thompson, K.M., Simon, J., Boyfield, I., Fonfria, E., Humphrey, P.P., Species and response dependent differences in the effects of MAPK inhibitors on P2X(7) receptor function. Br. J. Pharmacol. 149:7 (2006), 948–957.
55. Chessell, I.P., Michel, A.D., Humphrey, P.P., Effects of antagonists at the human recombinant P2X7 receptor. Br. J. Pharmacol. 124:6 (1998), 1314–1320.
56. Fischer, W., Franke, H., Krugel, U., Muller, H., Dinkel, K., Lord, B., Letavic, M.A., Henshall, D.C., Engel, T., Critical evaluation of P2X7 receptor antagonists in selected seizure models. PLoS ONE, 11(6), 2016, e0156468.
57. Jimenez-Pacheco, A., Diaz-Hernandez, M., Arribas-Blazquez, M., Sanz-Rodriguez, A., Olivos-Ore, L.A., Artalejo, A.R., Alves, M., Letavic, M., Miras-Portugal, M.T., Conroy, R.M., Delanty, N., Farrell, M.A., O'Brien, D.F., Bhattacharya, A., Engel, T., Henshall, D.C., Transient P2X7 receptor antagonism produces lasting reductions in spontaneous seizures and gliosis in experimental temporal lobe epilepsy. J. Neurosci. 36:22 (2016), 5920–5932.
58. Rajamani, U., Jialal, I., Hyperglycemia induces Toll-like receptor-2 and -4 expression and activity in human microvascular retinal endothelial cells: implications for diabetic retinopathy. J. Diabetes Res., 2014, 2014, 790902.