Adenosine A2AR blockade prevents neuroinflammation-induced death of retinal ganglion cells caused by elevated pressure

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Madeira, Maria H ^a,b   Elvas, Filipe ^a   Boia, Raquel ^a,b   Gonçalves, Francisco Q ^b,d   Cunha, Rodrigo A ^b,d,e   Ambrósio, Francisco A ^a,b,c   Santiago, Raquel A ^a,b,c,e  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c ASSOCIATION FOR INNOVATION AND BIOMEDICAL RESEARCH ON LIGHT AND IMAGE AIBILI   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Adenosine; Glaucoma; Microglia; Neuroprotection

Indexed keywords

5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; ADENOSINE A2A RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR POU4F1; TUMOR NECROSIS FACTOR ALPHA; 5-AMINO-7-(2-PHENYLETHYL)-2-(2-FURYL)PYRAZOLO(4,3-E)-1,2,4-TRIAZOLO(1,5-C)PYRIMIDINE; ADENOSINE A2 RECEPTOR ANTAGONIST; LIPOPOLYSACCHARIDE; NEUROPROTECTIVE AGENT; NITRIC OXIDE; PYRIMIDINE DERIVATIVE; TRIAZOLE DERIVATIVE;

ADULT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL LOSS; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LOCALIZATION; GENE EXPRESSION; GLAUCOMA; IMMUNOREACTIVITY; IN VITRO STUDY; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; RETINA GANGLION CELL; UPREGULATION; ADVERSE EFFECTS; ANIMAL; ANIMAL MODEL; APOPTOSIS; COMPLICATION; DRUG EFFECTS; HYDROSTATIC PRESSURE; INFLAMMATION; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; APOPTOSIS; GLAUCOMA; HYDROSTATIC PRESSURE; INFLAMMATION; LIPOPOLYSACCHARIDES; MODELS, ANIMAL; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; ORGAN CULTURE TECHNIQUES; PYRIMIDINES; RATS; RATS, WISTAR; RETINAL GANGLION CELLS; TRIAZOLES;

EID: 84931263960     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0333-5     Document Type: Article

References (81)

1. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, Pokharel GP, et al. Global data on visual impairment in the year 2002. Bull World Health Org. 2004;82:844-51.
2. Caprioli J. Glaucoma: a disease of early cellular senescence. Invest Ophthalmol Vis Sci. 2013;54(14):ORSF60-7. doi:10.1167/iovs.13-12716.
3. Cordeiro MF, Levin LA. Clinical evidence for neuroprotection in glaucoma. Am J Ophthalmol. 2011;152(5):715-6. doi: 10.1016/j.ajo.2011.06.015 .
4. Howell GR, Macalinao DG, Sousa GL, Walden M, Soto I, Kneeland SC, et al. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J Clin Invest. 2011;121(4):1429-44. doi: 10.1172/JCI44646 .
5. Krizaj D, Ryskamp DA, Tian N, Tezel G, Mitchell CH, Slepak VZ, et al. From mechanosensitivity to inflammatory responses: new players in the pathology of glaucoma. Curr Eye Res. 2013;39(2):105-19. doi: 10.3109/02713683.2013.836541 .
6. Joachim SC, Gramlich OW, Laspas P, Schmid H, Beck S, von Pein HD, et al. Retinal ganglion cell loss is accompanied by antibody depositions and increased levels of microglia after immunization with retinal antigens. PLoS One. 2012;7(7):e40616. doi: 10.1371/journal.pone.0040616 .
7. Neufeld AH. Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch Ophthalmol. 1999;117:1050-6.
8. Wang L, Cioffi GA, Cull G, Dong J, Fortune B. Immunohistologic evidence for retinal glial cell changes in human glaucoma. I Invest Ophthalmol Vis Sci. 2002;43(4):1088-94.
9. Bosco A, Steele MR, Vetter ML. Early microglia activation in a mouse model of chronic glaucoma. J Comp Neurol. 2011;519(4):599-620. doi: 10.1002/cne.22516 .
10. Taylor S, Calder CJ, Albon J, Erichsen JT, Boulton ME, Morgan JE. Involvement of the CD200 receptor complex in microglia activation in experimental glaucoma. Exp Eye Res. 2011;92(5):338-43. doi: 10.1016/j.exer.2011.01.012 .
11. Tezel G, Wax MB. Increased production of tumor necrosis factor-α by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000;20(23):8693-700.
12. Yuan L, Neufeld AH. Tumor necrosis factor-α: a potentially neurodestructive cytokine produced by glia in the human glaucomatous optic nerve head. Glia. 2000;32:42-50.
13. Cho KJ, Kim JH, Park HY, Park CK. Glial cell response and iNOS expression in the optic nerve head and retina of the rat following acute high IOP ischemia-reperfusion. Brain Res. 2011;1403:67-77. doi: 10.1016/j.brainres.2011.06.005 .
14. Gramlich OW, Beck S, von Thun Und Hohenstein-Blaul N, Boehm N, Ziegler A, Vetter JM, et al. Enhanced insight into the autoimmune component of glaucoma: IgG autoantibody accumulation and pro-inflammatory conditions in human glaucomatous retina. PLoS One. 2013;8(2):e57557. doi: 10.1371/journal.pone.0057557 .
15. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, et al. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci. 2008;49(4):1437-46. doi: 10.1167/iovs.07-1337 .
16. Yang X, Chou TH, Ruggeri M, Porciatti V. A new mouse model of inducible, chronic retinal ganglion cell dysfunction not associated with cell death. Invest Ophthalmol Vis Sci. 2013;54(3):1898-904. doi: 10.1167/iovs.12-11375 .
17. Wang K, Peng B, Lin B. Fractalkine receptor regulates microglial neurotoxicity in an experimental mouse glaucoma model. Glia. 2014;62(12):1943-54. doi: 10.1002/glia.22715 .
18. Roh M, Zhang Y, Murakami Y, Thanos A, Lee SC, Vavvas DG, et al. Etanercept, a widely used inhibitor of tumor necrosis factor-α (TNF-α), prevents retinal ganglion cell loss in a rat model of glaucoma. PLoS One. 2012;7(7):e40065. doi: 10.1371/journal.pone.0040065.g001 .
19. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev. 2011;91(2):461-553. doi: 10.1152/physrev.00011.2010 .
20. 2A receptors. Annu Rev Immunol. 2004;22:657-82. doi: 10.1146/annurev.immunol.22.012703.104731 .
21. Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nature Rev Drug Discovery. 2008;7(9):759-70. doi: 10.1038/nrd2638 .
22. 2A receptor stimulation potentiates nitric oxide release by activated microglia. J Neurochem. 2005;95(4):919-29. doi: 10.1111/j.1471-4159.2005.03395.x .
23. 2A receptor antagonist SCH 58621 on cyclooxygenase-2 expression, glial activation, and brain-derived neurotrophic factor availability in a rat model of striatal neurodegeneration. J Neuropathol Exp Neurol. 2007;66(5):363-71. doi: 10.1097/nen.0b013e3180517477 .
24. 2A receptors control neuroinflammation and consequent hippocampal neuronal dysfunction. J Neurochem. 2011;117(1):100-11. doi: 10.1111/j.1471-4159.2011.07178.x .
25. Gomes CV, Kaster MP, Tomé AR, Agostinho PM, Cunha RA. Adenosine receptors and brain diseases: neuroprotection and neurodegeneration. Bioch Biophys Acta. 2011;1808(5):1380-99. doi: 10.1016/j.bbamem.2010.12.001 .
26. Kretz A, Hermening SH, Isenmann S. A novel primary culture technique for adult retina allows for evaluation of CNS axon regeneration in rodents. J Neurosci Methods. 2004;136(2):207-19. doi: 10.1016/j.jneumeth.2004.01.012 .
27. Sappington RM, Chan M, Calkins DJ. Interleukin-6 protects retinal ganglion cells from pressure-induced death. Invest Ophthalmol Vis Sci. 2006;47(7):2932-42. doi: 10.1167/iovs.05-1407 .
28. Sappington R, Calkins DJ. Pressure-induced regulation of IL-6 in retinal glial cells: involvement of the ubiquitin/proteasome pathway and NF-kB. Invest Ophthalmol Vis Sci. 2006;47:3860-9. doi: 10.1167/.
29. Gavet O, Pines J. Progressive activation of cyclin B1-Cdk1 coordinates entry to mitosis. Dev Cell. 2010;18(4):533-43. doi: 10.1016/j.devcel.2010.02.013 .
30. Kurpius D, Wilson N, Fuller L, Hoffman A, Dailey ME. Early activation, motility, and homing of neonatal microglia to injured neurons does not require protein synthesis. Glia. 2006;54(1):58-70. doi: 10.1002/glia.20355 .
31. Morrison HW, Filosa JA. A quantitative spatiotemporal analysis of microglia morphology during ischemic stroke and reperfusion. J Neuroinflamm. 2013;10(1):4. doi: 10.1186/1742-2094-10-4 .
32. Cunha RA, Almeida T, Ribeiro JA. Modification by arachidonic acid of extracellular adenosine metabolism and neuromodulatory action in the rat hippocampus. J Biol Chem. 2000;275(48):37572-81. doi: 10.1074/jbc.M003011200 .
33. Santiago AR, Gaspar JM, Baptista FI, Cristóvão AJ, Santos PF, Kamphuis W, et al. Diabetes changes the levels of ionotropic glutamate receptors in the rat retina. Mol Vis. 2009;15:1620-30.
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25(4):402-8. doi:10.1006/meth.2001.1262. S1046-2023(01)91262-9.
35. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64(15):5245-50. doi: 10.1158/0008-5472.CAN-04-0496 .
36. 2A receptor functions. J Neurosci. 2013;33(28):11390-9. doi: 10.1523/JNEUROSCI.5817-12.2013 .
37. Kraft AD, Harry GJ. Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health. 2011;8(7):2980-3018. doi: 10.3390/ijerph8072980 .
38. Brown GC. Mechanisms of inflammatory neurodegeneration: iNOS and NADPH oxidase. Biochem Soc Trans. 2007;35(Pt 5):1119-21. doi: 10.1042/BST0351119 .
39. Nadal-Nicolas FM, Jimenez-Lopez M, Sobrado-Calvo P, Nieto-Lopez L, Canovas-Martinez I, Salinas-Navarro M, et al. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci. 2009;50(8):3860-8. doi: 10.1167/iovs.08-3267 .
40. Sanchez-Migallon MC, Nadal-Nicolas FM, Jimenez-Lopez M, Sobrado-Calvo P, Vidal-Sanz M, Agudo-Barriuso M. Brain derived neurotrophic factor maintains Brn3a expression in axotomized rat retinal ganglion cells. Exp Eye Res. 2011;92(4):260-7. doi: 10.1016/j.exer.2011.02.001 .
41. Bull ND, Johnson TV, Welsapar G, DeKorver NW, Tomarev SI, Martin KR. Use of an adult rat retinal explant model for screening of potential retinal ganglion cell neuroprotective therapies. Invest Ophthalmol Vis Sci. 2011;52(6):3309-20. doi: 10.1167/iovs.10-6873 .
42. Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci. 2002;43:2962-9.
43. Tezel G, Li LY, Patil RV, Wax MB. TNF-α and TNF-α receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis Sci. 2001;42:1787-94.
44. Yoneda S, Tanihara H, Kido N, Honda Y, Goto W, Hara H, et al. Interleukin-1beta mediates ischemic injury in the rat retina. Exp Eye Res. 2001;73(5):661-7. doi: 10.1006/exer.2001.1072 .
45. Manni G, Centofanti M, Oddone F, Parravano M, Bucci MG. Interleukin-1beta tear concentration in glaucomatous and ocular hypertensive patients treated with preservative-free nonselective beta-blockers. Am J Ophthalmol. 2005;139(1):72-7. doi: 10.1016/j.ajo.2004.08.028 .
46. Sivakumar V, Foulds WS, Luu CD, Ling E-A, Kaur C. Retinal ganglion cell death is induced by microglia derived pro-inflammatory cytokines in the hypoxic neonatal retina. J Pathol. 2011;224(2):245-60. doi: 10.1002/path.2858 .
47. Gyoneva S, Davalos D, Biswas D, Swanger SA, Garnier-Amblard E, Loth F, et al. Systemic inflammation regulates microglial responses to tissue damage in vivo. Glia. 2014;62(8):1345-60. doi: 10.1002/glia.22686 .
48. Ahmad S, Fatteh N, El-Sherbiny NM, Naime M, Ibrahim AS, El-Sherbini AM, et al. Potential role of A2A adenosine receptor in traumatic optic neuropathy. J Neuroimmunol. 2013;264(1-2):54-4. doi: 10.1016/j.jneuroim.2013.09.015 .
49. 2A adenosine receptor (A2AR) as a therapeutic target in diabetic retinopathy. Am J Pathol. 2011;178(5):2136-45. doi: 10.1016/j.ajpath.2011.01.018 .
50. Ibrahim AS, El-Remessy AB, Matragoon S, Zhang W, Patel Y, Khan S, et al. Retinal microglial activation and inflammation induced by amadori-glycated albumin in a rat model of diabetes. Diabetes. 2011;60:1122-33. doi: 10.2337/db10-1160/-/DC1 .
51. Johnson TV, Martin KR. Development and characterization of an adult retinal explant organotypic tissue culture system as an in vitro intraocular stem cell transplantation model. Invest Ophthalmol Vis Sci. 2008;49(8):3503-12. doi: 10.1167/iovs.07-1601 .
52. Ferrer-Martin RM, Martin-Oliva D, Sierra A, Carrasco MC, Martin-Estebane M, Calvente R. Microglial cells in organotypic cultures of developing and adult mouse retina and their relationship with cell death. Exp Eye Res. 2014;121:42-57. doi: 10.1016/j.exer.2014.02.015 .
53. 2A receptor regulation of neuroinflammation and traumatic brain injury. J Neurosci. 2010;30(16):5802-10. doi: 10.1523/jneurosci.0268-10.2010 .
54. 1 receptors in hippocampus. Naunyn-Schmiedeberg's Arch Pharmacol. 2004;370(4):270-8. doi: 10.1007/s00210-004-0970-1 .
55. 2A receptor heteromers in human brain caudate nucleus. J Neurochem. 2010;114(4):972-80. doi: 10.1111/j.1471-4159.2010.06810.x .
56. Fredholm BB, Ijzerman AP, Jacobson KA, Linden J, Muller CE. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol Rev. 2011;63(1):1-34. doi: 10.1124/pr.110.003285 .
57. 2A antagonists. J Neurosci. 2003;23(12):5361-9.
58. Li W, Dai S, An J, Li P, Chen X, Xiong R, et al. Chronic but not acute treatment with caffeine attenuates traumatic brain injury in the mouse cortical impact model. Neuroscience. 2008;151(4):1198-07. doi: 10.1016/j.neuroscience.2007.11.020 .
59. Silva CG, Porciuncula LO, Canas PM, Oliveira CR, Cunha RA. Blockade of adenosine A(2A) receptors prevents staurosporine-induced apoptosis of rat hippocampal neurons. Neurobiol Dis. 2007;27(2):182-9. doi: 10.1016/j.nbd.2007.04.018 .
60. 2A receptor blockade prevents synaptotoxicity and memory dysfunction caused by β-Amyloid peptides via p38 mitogen-activated protein kinase pathway. J Neurosci. 2009;29(47):14741-51. doi: 10.1523/jneurosci.3728-09.2009 .
61. 2A receptors prevents interleukin-1β-induced exacerbation of neuronal toxicity through a p38 mitogen-activated protein kinase pathway. J Neuroinflamm. 2012;9(1):204. doi: 10.1186/1742-2094-9-204 .
62. 2A receptors blocks glutamate excitotoxicity in cultures of avian retinal neurons. Brain Res. 2001;900:169-76.
63. 3 receptors in controlling kainate-induced toxicity in cortical cultured neurons. Neurochem Int. 2005;47(5):317-25. doi: 10.1016/j.neuint.2005.05.009 .
64. Silva CG, Metin C, Fazeli W, Machado NJ, Darmopil S, Launay PS, et al. Adenosine receptor antagonists including caffeine alter fetal brain development in mice. Science Transl Med. 2013;5(197):12. doi: 10.1126/scitranslmed.3006258. 197ra04 .
65. Xia J, Lim JC, Lu W, Beckel JM, Macarak EJ, Laties AM, et al. Neurons respond directly to mechanical deformation with pannexin-mediated ATP release and autostimulation of P2X7 receptors. J Physiol. 2012;590(Pt 10):2285-304. doi: 10.1113/jphysiol.2012.227983 .
66. Imura Y, Morizawa Y, Komatsu R, Shibata K, Shinozaki Y, Kasai H, et al. Microglia release ATP by exocytosis. Glia. 2013;61(8):1320-30. doi: 10.1002/glia.22517 .
67. Newman EA. Glial cell inhibition of neurons by release of ATP. J Neurosci. 2003;23(5):1659-66.
68. Beckel JM, Argall AJ, Lim JC, Xia J, Lu W, Coffey EE, et al. 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. 2014;62(9):1486-501. doi: 10.1002/glia.22695 .
69. Reigada D, Lu W, Zhang M, Mitchell CH. Elevated pressure triggers a physiological release of ATP from the retina: possible role for pannexin hemichannels. Neuroscience. 2008;157(2):396-404. doi: 10.1016/j.neuroscience.2008.08.036 .
70. Resta V, Novelli E, Vozzi G, Scarpa C, Caleo M, Ahluwalia A, et al. Acute retinal ganglion cell injury caused by intraocular pressure spikes is mediated by endogenous extracellular ATP. Eur J Neurosci. 2007;25(9):2741-54. doi: 10.1111/j.1460-9568.2007.05528.x .
71. Zhang X, Li A, Ge J, Reigada D, Laties AM, Mitchell CH. Acute increase of intraocular pressure releases ATP into the anterior chamber. Exp Eye Res. 2007;85(5):637-43. doi: 10.1016/j.exer.2007.07.016 .
72. Li A, Zhang X, Zheng D, Ge J, Laties AM, Mitchell CH. Sustained elevation of extracellular ATP in aqueous humor from humans with primary chronic angle-closure glaucoma. Exp Eye Res. 2011;93(4):528-33. doi: 10.1016/j.exer.2011.06.020 .
73. Rodrigues R, Tomé A, Cunha R. ATP as a multi-target danger signal in the brain. Front Neurosci. 2015;9:148. doi: 10.3389/fnins.2015.00148 .
74. Hu H, Lu W, Zhang M, Zhang X, Argall AJ, Patel S, et al. Stimulation of the P2X7 receptor kills rat retinal ganglion cells in vivo. Exp Eye Res. 2010;91(3):425-32. doi: 10.1016/j.exer.2010.06.017 .
75. Niyadurupola N, Sidaway P, Ma N, Rhodes JD, Broadway DC, Sanderson J. P2X7 receptor activation mediates retinal ganglion cell death in a human retina model of ischemic neurodegeneration. Invest Ophthalmol Vis Sci. 2013;54(3):2163-70. doi: 10.1167/iovs.12-10968 .
76. Sugiyama T, Lee SY, Horie T, Oku H, Takai S, Tanioka H, et al. P2X(7) receptor activation may be involved in neuronal loss in the retinal ganglion cell layer after acute elevation of intraocular pressure in rats. Mol Vis. 2013;19:2080-91.
77. 2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron. 2008;57(1):121-34. doi: 10.1016/j.neuron.2007.11.023 .
78. 2A receptor blockade. Purinergic Signalling. 2005;1:111-34.
79. 2A receptor blockade prevents BDNF release and proliferation of microglia. J Neuroinflammation. 2013;10(1):16. doi: 10.1186/1742-2094-10-16 .
80. 2A receptors in retinal and brain neurodegenerative diseases. Mediat Inflamm. 2014;2014:465694. doi: 10.1155/2014/465694 .
81. Avila MY, Stone RA, Civan MM. A(1)-, A(2A)- and A(3)-subtype adenosine receptors modulate intraocular pressure in the mouse. Br J Pharmacol. 2001;134(2):241-5. doi: 10.1038/sj.bjp.0704267 .