The CD40-ATP-P2X7 Receptor Pathway: Cell to Cell Cross-Talk to Promote Inflammation and Programmed Cell Death of Endothelial Cells

Extracellular adenosine 5′-triphosphate (ATP) functions not only as a neurotransmitter but is also released by non-excitable cells and mediates cell–cell communication involving glia. In pathological conditions, extracellular ATP released by astrocytes may act as a “danger” signal that activates mic...

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Published inFrontiers in immunology Vol. 10
Main Author Subauste, Carlos S.
Format Journal Article
LanguageEnglish
Published Frontiers Media S.A 17.12.2019
Subjects
ATP
CD40
cytokine
endothelial cell
glia
Immunology
retina
Online AccessGet full text
ISSN1664-3224
1664-3224
DOI10.3389/fimmu.2019.02958

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Abstract Extracellular adenosine 5′-triphosphate (ATP) functions not only as a neurotransmitter but is also released by non-excitable cells and mediates cell–cell communication involving glia. In pathological conditions, extracellular ATP released by astrocytes may act as a “danger” signal that activates microglia and promotes neuroinflammation. This review summarizes in vitro and in vivo studies that identified CD40 as a novel trigger of ATP release and purinergic-induced inflammation. The use of transgenic mice with expression of CD40 restricted to retinal Müller glia and a model of diabetic retinopathy (a disease where the CD40 pathway is activated) established that CD40 induces release of ATP in Müller glia and triggers in microglia/macrophages purinergic receptor-dependent inflammatory responses that drive the development of retinopathy. The CD40-ATP-P2X 7 pathway not only amplifies inflammation but also induces death of retinal endothelial cells, an event key to the development of capillary degeneration and retinal ischemia. Taken together, CD40 expressed in non-hematopoietic cells is sufficient to mediate inflammation and tissue pathology as well as cause death of retinal endothelial cells. This process likely contributes to development of degenerate capillaries, a hallmark of diabetic and ischemic retinopathies. Blockade of signaling pathways downstream of CD40 operative in non-hematopoietic cells may offer a novel means of treating diabetic and ischemic retinopathies.
AbstractList Extracellular adenosine 5′-triphosphate (ATP) functions not only as a neurotransmitter but is also released by non-excitable cells and mediates cell–cell communication involving glia. In pathological conditions, extracellular ATP released by astrocytes may act as a “danger” signal that activates microglia and promotes neuroinflammation. This review summarizes in vitro and in vivo studies that identified CD40 as a novel trigger of ATP release and purinergic-induced inflammation. The use of transgenic mice with expression of CD40 restricted to retinal Müller glia and a model of diabetic retinopathy (a disease where the CD40 pathway is activated) established that CD40 induces release of ATP in Müller glia and triggers in microglia/macrophages purinergic receptor-dependent inflammatory responses that drive the development of retinopathy. The CD40-ATP-P2X 7 pathway not only amplifies inflammation but also induces death of retinal endothelial cells, an event key to the development of capillary degeneration and retinal ischemia. Taken together, CD40 expressed in non-hematopoietic cells is sufficient to mediate inflammation and tissue pathology as well as cause death of retinal endothelial cells. This process likely contributes to development of degenerate capillaries, a hallmark of diabetic and ischemic retinopathies. Blockade of signaling pathways downstream of CD40 operative in non-hematopoietic cells may offer a novel means of treating diabetic and ischemic retinopathies.
Extracellular adenosine 5′-triphosphate (ATP) functions not only as a neurotransmitter but is also released by non-excitable cells and mediates cell–cell communication involving glia. In pathological conditions, extracellular ATP released by astrocytes may act as a “danger” signal that activates microglia and promotes neuroinflammation. This review summarizes in vitro and in vivo studies that identified CD40 as a novel trigger of ATP release and purinergic-induced inflammation. The use of transgenic mice with expression of CD40 restricted to retinal Müller glia and a model of diabetic retinopathy (a disease where the CD40 pathway is activated) established that CD40 induces release of ATP in Müller glia and triggers in microglia/macrophages purinergic receptor-dependent inflammatory responses that drive the development of retinopathy. The CD40-ATP-P2X7 pathway not only amplifies inflammation but also induces death of retinal endothelial cells, an event key to the development of capillary degeneration and retinal ischemia. Taken together, CD40 expressed in non-hematopoietic cells is sufficient to mediate inflammation and tissue pathology as well as cause death of retinal endothelial cells. This process likely contributes to development of degenerate capillaries, a hallmark of diabetic and ischemic retinopathies. Blockade of signaling pathways downstream of CD40 operative in non-hematopoietic cells may offer a novel means of treating diabetic and ischemic retinopathies.
Author Subauste, Carlos S.
AuthorAffiliation 2 Department of Pathology, Case Western Reserve University , Cleveland, OH , United States
1 Division of Infectious Diseases and HIV Medicine, Department of Medicine, Case Western Reserve University , Cleveland, OH , United States
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Cites_doi 10.1002/glia.10124
10.1111/imm.12361
10.3390/ijms19040942
10.1038/nrn1928
10.4049/jimmunol.160.9.4271
10.1523/JNEUROSCI.5512-08.2009
10.1016/S0022-3476(97)70123-9
10.2337/db06-0427
10.1126/science.272.5262.735
10.1002/eji.1830241248
10.1128/IAI.01145-12
10.1111/j.1365-2567.2011.03519.x
10.1056/NEJMra1005073
10.1007/s00125-019-4959-1
10.1016/S0002-9394(01)01127-8
10.1055/s-0029-1224151
10.1074/jbc.M707915200
10.1167/iovs.06-0510
10.1016/S1074-7613(03)00230-9
10.1016/S0140-6736(97)01107-0
10.2337/db11-1249
10.1006/exer.2002.2042
10.1167/iovs.14-15340
10.1038/sj.cdd.4400341
10.1002/eji.200323729
10.1038/eye.2013.25
10.2353/ajpath.2008.071070
10.1615/CritRevImmunol.v37.i2-6.100
10.1007/s00125-005-1750-2
10.1096/fj.01-0707fje
10.1002/art.1780400117
10.1073/pnas.96.19.10836
10.1016/j.drudis.2019.01.023
10.4049/jimmunol.155.10.4917
10.1016/j.celrep.2015.02.016
10.1093/emboj/21.4.643
10.1161/CIRCRESAHA.110.223545
10.1016/j.jbior.2013.08.003
10.1016/j.biocel.2010.06.021
10.1096/fj.02-0157fje
10.1016/j.nut.2005.08.011
10.1096/fj.05-4313fje
10.1038/s41598-017-02852-4
10.2337/db16-0051
10.1167/iovs.07-0112
10.1189/jlb.72.1.19
10.1172/JCI27155
10.1055/a-0647-6860
10.1167/iovs.03-1062
10.1111/aos.12812
10.1038/eye.2016.10
10.2337/diabetes.50.6.1432
10.1002/jlb.67.1.2
10.1016/j.preteyeres.2006.05.003
10.2147/ITT.S163614
10.1016/j.preteyeres.2011.05.002
10.1111/j.1600-065X.2009.00782.x
10.1016/j.diabres.2009.01.012
10.1167/iovs.16-20301
10.1080/02713680590923276
10.4049/jimmunol.159.3.1451
10.1111/j.1471-4159.2004.02727.x
10.1002/art.10856
10.2353/ajpath.2010.090461
10.1073/pnas.92.10.4342
10.2337/diabetes.54.5.1559
10.1073/pnas.83.12.4494
10.1006/exer.2001.1072
10.4049/jimmunol.175.9.6014
10.1046/j.0022-3042.2001.00737.x
10.1007/s11302-012-9300-0
10.3390/ijms17081282
10.1016/S2214-109X(13)70113-X
10.1007/s00125-007-0734-9
10.1096/fj.03-1476fje
10.1016/S0014-2999(02)01756-9
10.1167/iovs.17-21973
10.1007/s12079-018-00500-8
10.7554/eLife.30442
10.1016/j.jneuroim.2006.09.015
10.1093/ndt/gfw397
10.1046/j.1471-4159.2000.0750965.x
10.1007/s00125-014-3321-x
10.2337/db09-1420
10.4049/jimmunol.181.12.8719
10.1155/2017/3940241
10.1167/iovs.08-2642
10.4049/jimmunol.161.6.3120
10.1038/28204
10.2337/dc11-1909
10.1167/iovs.04-0860
10.1074/jbc.M300711200
10.1172/JCI118746
10.1016/j.smim.2009.05.012
10.4049/jimmunol.157.8.3569
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Notes Edited by: Antje Kroner, Medical College of Wisconsin, United States
This article was submitted to Multiple Sclerosis and Neuroimmunology, a section of the journal Frontiers in Immunology
Reviewed by: Rishein Gupta, University of Texas at San Antonio, United States; Bruce Hostager, The University of Iowa, United States; Steven F. Abcouwer, Michigan Medicine, United States
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References Ara (B19) 2018; 7
Monif (B76) 2010; 42
Franke (B1) 2012; 8
Yoneda (B50) 2001; 73
Chatzigeorgiou (B60) 2010; 118
Ferrari (B74) 1997; 159
Portillo (B5) 2008; 181
Carriba (B21) 2017; 6
Deregibus (B87) 2003; 278
Zheng (B42) 2007; 50
Antonetti (B3) 2012; 366
Rivera (B48) 2017; 2017
Portillo (B8) 2016; 57
Leal (B41) 2007; 48
Laman (B18) 2017; 37
Tan (B92) 1998; 160
Eid (B27) 2019; 62
Joussen (B85) 2002; 17
Joussen (B79) 2002; 16
Taghavi (B43) 2019
Kobayashi (B97) 2003; 19
Zheng (B49) 2007; 48
Neufeld (B51) 2002; 75
Boumpas (B94) 2003; 48
Li (B66) 2012; 61
Van Kooten (B14) 2000; 67
Tan (B12) 2002; 21
Mach (B22) 1998; 394
Behl (B86) 2008; 172
Vujosevic (B35) 2016; 94
Sugiyama (B91) 2004; 45
Mizutani (B32) 1996; 97
Clark (B9) 1986; 83
Liu (B78) 1996; 157
Wang (B71) 2010; 59
Bourne (B25) 2013; 1
Monif (B77) 2009; 29
Mcleod (B29) 1995; 147
Joussen (B31) 2004; 18
Van Grol (B56) 2013; 81
Yau (B24) 2012; 35
Du (B40) 2002; 80
Portillo (B7) 2017; 66
Tsujikawa (B54) 1999; 40
Mackey (B98) 2003; 33
Zhang (B44) 2006; 20
James (B72) 2002; 447
Karmann (B10) 1995; 92
Mcwilliams (B20) 2015; 10
Okuno (B93) 2004; 91
Andrade (B99) 2005; 175
Yang (B83) 2013; 53
Giacco (B26) 2010; 107
Kern (B84) 2000; 41
Bishop (B95) 2002; 72
Levy (B16) 1997; 131
Kuo (B59) 2018; 33
Hide (B75) 2000; 75
Vinores (B53) 2007; 182
Lee (B62) 2017; 7
Gilbert (B45) 1997; 350
Jun (B90) 2007; 282
Powers (B70) 2005; 30
Klaus (B81) 1994; 24
Joussen (B38) 2009; 15
Elgueta (B17) 2009; 229
Choi (B52) 2006; 22
Portillo (B55) 2009; 15
Peters (B23) 2009; 21
Portillo (B100) 2012; 135
Portillo (B58) 2014; 55
Cipollone (B63) 2005; 48
Tang (B2) 2011; 30
Kiener (B11) 1995; 155
Borcherding (B13) 2010; 176
Vincent (B37) 2007; 56
Gerbardinger (B69) 2005; 46
Rubsam (B4) 2018; 19
Ashraf (B47) 2016; 30
Bringmann (B67) 2006; 25
Lamine (B64) 2018
Devoldere (B68) 2019; 24
Yan (B61) 2016; 17
Yang (B34) 2009; 50
Lazaar (B82) 1998; 161
Portillo (B96) 2015; 144
Varma (B46) 2013; 27
Adamiec-Mroczek (B28) 2009; 84
Boss (B36) 2017; 58
Miyamoto (B30) 1999; 96
Yellin (B57) 1997; 40
Xu (B15) 2006; 116
Abu El-Asrar (B39) 2001; 132
Surprenant (B88) 1996; 272
Portillo (B6) 2014; 57
Fields (B73) 2006; 7
Krady (B33) 2005; 54
Bal-Price (B80) 2002; 40
Di Virgilio (B89) 1998; 5
Boeri (B65) 2001; 50
References_xml – volume: 40
  start-page: 312
  year: 2002
  ident: B80
  article-title: Nitric oxide induces rapid, calcium-dependent release of vesicular glutamate and ATP from cultured rat astrocytes
  publication-title: Glia.
  doi: 10.1002/glia.10124
– volume: 144
  start-page: 21
  year: 2015
  ident: B96
  article-title: Blockade of CD40-TRAF2,3 or CD40-TRAF6 interactions is sufficient to impair pro-inflammatory responses in human aortic endothelial cells and human aortic smooth muscle cells
  publication-title: Immunology.
  doi: 10.1111/imm.12361
– volume: 19
  start-page: E942
  year: 2018
  ident: B4
  article-title: Role of inflammation in diabetic retinopathy
  publication-title: Int J Mol Sci
  doi: 10.3390/ijms19040942
– volume: 7
  start-page: 423
  year: 2006
  ident: B73
  article-title: Purinergic signalling in neuron-glia interactions
  publication-title: Nat Rev Neurosci.
  doi: 10.1038/nrn1928
– volume: 160
  start-page: 4271
  year: 1998
  ident: B92
  article-title: Presentation of proteolipid protein epitopes and B7-1-dependent activation of encephalitogenic T cells by IFN-γ-activated SJL/J astrocytes
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.160.9.4271
– volume: 15
  start-page: 1418
  year: 2009
  ident: B38
  article-title: TNF-α mediated apoptosis plays an important role in the development of early diabetic retinopathy and long-term histopathological alterations
  publication-title: Mol Vision.
– volume: 29
  start-page: 3781
  year: 2009
  ident: B77
  article-title: The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore
  publication-title: J Neurosci.
  doi: 10.1523/JNEUROSCI.5512-08.2009
– volume: 131
  start-page: 47
  year: 1997
  ident: B16
  article-title: Clinical spectrum of X-linked hyper-IgM syndrome
  publication-title: J Pediatr.
  doi: 10.1016/S0022-3476(97)70123-9
– volume: 56
  start-page: 224
  year: 2007
  ident: B37
  article-title: Inhibition of caspase-1/interleukin-1β signaling prevents degeneration of retinal capillaries in diabetes and galactosemia
  publication-title: Diabetes.
  doi: 10.2337/db06-0427
– volume: 272
  start-page: 735
  year: 1996
  ident: B88
  article-title: The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7)
  publication-title: Science.
  doi: 10.1126/science.272.5262.735
– volume: 24
  start-page: 3229
  year: 1994
  ident: B81
  article-title: Properties of mouse CD40. Ligation of CD40 activates B cells via a Ca(++)-dependent, FK506-sensitive pathway
  publication-title: Eur J Immunol
  doi: 10.1002/eji.1830241248
– volume: 81
  start-page: 2002
  year: 2013
  ident: B56
  article-title: CD40 induces anti-Toxoplasma gondii activity in non-hematopoietic cells dependent on autophagy proteins
  publication-title: Infect Immun.
  doi: 10.1128/IAI.01145-12
– volume: 135
  start-page: 140
  year: 2012
  ident: B100
  article-title: CD40 and TNF-α synergize to induce nitric oxide synthase in macrophages
  publication-title: Immunology.
  doi: 10.1111/j.1365-2567.2011.03519.x
– volume: 366
  start-page: 1227
  year: 2012
  ident: B3
  article-title: Diabetic retinopathy
  publication-title: N Engl J Med.
  doi: 10.1056/NEJMra1005073
– volume: 62
  start-page: 1539
  year: 2019
  ident: B27
  article-title: New insights into the mechanisms of diabetic complications: role of lipids and lipid metabolism
  publication-title: Diabetologia.
  doi: 10.1007/s00125-019-4959-1
– volume: 132
  start-page: 551
  year: 2001
  ident: B39
  article-title: Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus
  publication-title: Am J Ophthalmol.
  doi: 10.1016/S0002-9394(01)01127-8
– volume: 118
  start-page: 38
  year: 2010
  ident: B60
  article-title: CD40 expression and its association with low-grade inflammation in a Greek population of type 1 diabetic juveniles: evidence for differences in CD40 mRNA isoforms expressed by peripheral blood mononuclear cells
  publication-title: Exp Clin Endocrinol Diabetes.
  doi: 10.1055/s-0029-1224151
– volume: 282
  start-page: 37350
  year: 2007
  ident: B90
  article-title: Extracellular ATP mediates necrotic cell swelling in SN4741 dopaminergic neurons through P2X7 receptors
  publication-title: J Biol Chem.
  doi: 10.1074/jbc.M707915200
– volume: 48
  start-page: 361
  year: 2007
  ident: B49
  article-title: Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.06-0510
– volume: 19
  start-page: 353
  year: 2003
  ident: B97
  article-title: TRAF6 is a critical factor for dendritic cell maturation and development
  publication-title: Immunity.
  doi: 10.1016/S1074-7613(03)00230-9
– volume: 350
  start-page: 12
  year: 1997
  ident: B45
  article-title: Retinopathy of prematurity in middle-income countries
  publication-title: Lancet
  doi: 10.1016/S0140-6736(97)01107-0
– volume: 61
  start-page: 3294
  year: 2012
  ident: B66
  article-title: Marrow-derived cells regulate the devlopment of early diabetic retinopathy and tactile allodynia in mice
  publication-title: Diabetes.
  doi: 10.2337/db11-1249
– volume: 75
  start-page: 521
  year: 2002
  ident: B51
  article-title: Loss of retinal ganglion cells following retinal ischemia: the role of inducible nitric oxide synthase
  publication-title: Exp Eye Res.
  doi: 10.1006/exer.2002.2042
– volume: 55
  start-page: 8590
  year: 2014
  ident: B58
  article-title: Pro-inflammatory responses induced by CD40 in retinal endothelial and Muller cells are inhibited by blocking CD40-TRAF2,3 or CD40-TRAF6 signaling
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.14-15340
– volume: 5
  start-page: 191
  year: 1998
  ident: B89
  article-title: Cytolytic P2X purinoceptors
  publication-title: Cell Death Differ.
  doi: 10.1038/sj.cdd.4400341
– volume: 33
  start-page: 779
  year: 2003
  ident: B98
  article-title: Distinct contributions of different CD40 TRAF binding sites to CD154-induced dendritic cell maturation and IL-12 secretion
  publication-title: Eur J Immunol.
  doi: 10.1002/eji.200323729
– volume: 27
  start-page: 688
  year: 2013
  ident: B46
  article-title: A review of central retinal artery occlusion: clinical presentation and management
  publication-title: Eye.
  doi: 10.1038/eye.2013.25
– volume: 172
  start-page: 1411
  year: 2008
  ident: B86
  article-title: Diabetes-enhanced tumor necrosis factor-alpha production promotes apoptosis and the loss of retinal microvascular cells in type 1 and type 2 models of diabetic retinopathy
  publication-title: Am J Pathol.
  doi: 10.2353/ajpath.2008.071070
– volume: 37
  start-page: 371
  year: 2017
  ident: B18
  article-title: Functions of CD40 and Its Ligand, gp39 (CD40L)
  publication-title: Crit Rev Immunol.
  doi: 10.1615/CritRevImmunol.v37.i2-6.100
– volume: 48
  start-page: 1216
  year: 2005
  ident: B63
  article-title: Enhanced soluble CD40 ligand contributes to endothelial cell dysfunction in vitro and monocyte activation in patients with diabetes mellitus: effect of improved metabolic control
  publication-title: Diabetologia.
  doi: 10.1007/s00125-005-1750-2
– volume: 15
  start-page: 1383
  year: 2009
  ident: B55
  article-title: Identification of primary retinal cells and ex vivo identification of pro-inflammatory molecules in retinal cells using flow cytometry
  publication-title: Mol Vis.
– volume: 16
  start-page: 438
  year: 2002
  ident: B79
  article-title: Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-α suppression
  publication-title: FASEB J.
  doi: 10.1096/fj.01-0707fje
– volume: 40
  start-page: 124
  year: 1997
  ident: B57
  article-title: Immunohistologic analysis of renal CD40 and CD40L expression in lupus nephritis and other glomerulonephritis
  publication-title: Arthritis Rheum
  doi: 10.1002/art.1780400117
– volume: 96
  start-page: 10836
  year: 1999
  ident: B30
  article-title: Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition
  publication-title: Proc Natl Acad Sci USA.
  doi: 10.1073/pnas.96.19.10836
– volume: 24
  start-page: 1483
  year: 2019
  ident: B68
  article-title: Muller cells as a target for retinal therapy
  publication-title: Drug Discov Today.
  doi: 10.1016/j.drudis.2019.01.023
– volume: 155
  start-page: 4917
  year: 1995
  ident: B11
  article-title: Stimulation of CD40 with purified soluble gp39 induces proinflammatory responses in human monocytes
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.155.10.4917
– volume: 10
  start-page: 1443
  year: 2015
  ident: B20
  article-title: Regulation of autocrine signaling in subsets of sympathetic neurons has regional effects on tissue innervation
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2015.02.016
– volume: 21
  start-page: 643
  year: 2002
  ident: B12
  article-title: CD40 is expressed and functional on neuronal cells
  publication-title: EMBO J.
  doi: 10.1093/emboj/21.4.643
– volume: 107
  start-page: 1058
  year: 2010
  ident: B26
  article-title: Oxidative stress and diabetic complications
  publication-title: Circ Res
  doi: 10.1161/CIRCRESAHA.110.223545
– volume: 53
  start-page: 232
  year: 2013
  ident: B83
  article-title: The physiological roles of primary phospholipase C
  publication-title: Adv Biol Regul.
  doi: 10.1016/j.jbior.2013.08.003
– volume: 42
  start-page: 1753
  year: 2010
  ident: B76
  article-title: Microglia: proliferation and activation driven by the P2X7 receptor
  publication-title: Int J Biochem Cell Biol.
  doi: 10.1016/j.biocel.2010.06.021
– volume: 17
  start-page: 76
  year: 2002
  ident: B85
  article-title: Suppression of Fas-FasL-induced endothelial cell apoptosis prevents diabetic blood-retinal barrier breakdown in a model of streptozotocin-induced diabetes
  publication-title: FASEB J.
  doi: 10.1096/fj.02-0157fje
– volume: 22
  start-page: 668
  year: 2006
  ident: B52
  article-title: Inhibition of nNOS and COX-2 expression by lutein in acute retinal ischemia
  publication-title: Nutrition.
  doi: 10.1016/j.nut.2005.08.011
– volume: 20
  start-page: 323
  year: 2006
  ident: B44
  article-title: Pigmented epithelium-derived factor (PEDF) is na endogenous antiinflammatory factor
  publication-title: FASEB J.
  doi: 10.1096/fj.05-4313fje
– volume: 7
  start-page: 2528
  year: 2017
  ident: B62
  article-title: A PPARγ-dependent miR-424/503-CD40 axis regulates inflammation mediated angiogenesis
  publication-title: Sci Rep.
  doi: 10.1038/s41598-017-02852-4
– volume: 41
  start-page: 3972
  year: 2000
  ident: B84
  article-title: Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia
  publication-title: Invest Ophthalmol Vis Sci.
– volume: 66
  start-page: 483
  year: 2017
  ident: B7
  article-title: CD40 in retinal Muller cells induces P2X7-dependent cytokine expression in macrophages/microglia in diabetic mice and development of early experimental diabetic retinopathy in mice
  publication-title: Diabetes.
  doi: 10.2337/db16-0051
– volume: 48
  start-page: 5257
  year: 2007
  ident: B41
  article-title: Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.07-0112
– volume: 72
  start-page: 19
  year: 2002
  ident: B95
  article-title: Mechanisms of TNF receptor-associated factor (TRAF) regulation in B lymphocytes
  publication-title: J Leuk Biol.
  doi: 10.1189/jlb.72.1.19
– volume: 116
  start-page: 769
  year: 2006
  ident: B15
  article-title: Platelet-derived or soluble CD154 induces vascularized allograft rejection independent of cell-bound CD154
  publication-title: J Clin Invest.
  doi: 10.1172/JCI27155
– year: 2018
  ident: B64
  article-title: Elevation in circulating soluble CD40 ligand concentrations in type 2 diabetic retinopathy and association with its severity
  publication-title: Exp Clin Endocrinol Diabetes
  doi: 10.1055/a-0647-6860
– volume: 45
  start-page: 1026
  year: 2004
  ident: B91
  article-title: Enhancement of of P2X7-induced pore formation and apoptosis: an early effect of diabetes on the retinal microvasculature
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.03-1062
– volume: 94
  start-page: 56
  year: 2016
  ident: B35
  article-title: Proteome analysis of retinal glia cells-related inflammatory cytokines in the aqueous humour of diabetic patients
  publication-title: Acta Ophthalmol.
  doi: 10.1111/aos.12812
– volume: 30
  start-page: 505
  year: 2016
  ident: B47
  article-title: Central retinal vein occlusion: modifying current treatment protocols
  publication-title: Eye.
  doi: 10.1038/eye.2016.10
– volume: 50
  start-page: 1432
  year: 2001
  ident: B65
  article-title: Increased prevalence of microthromboses in retinal capillaries of diabetic individuals
  publication-title: Diabetes.
  doi: 10.2337/diabetes.50.6.1432
– volume: 67
  start-page: 2
  year: 2000
  ident: B14
  article-title: CD40-CD40 ligand
  publication-title: J Leuk Biol.
  doi: 10.1002/jlb.67.1.2
– volume: 147
  start-page: 642
  year: 1995
  ident: B29
  article-title: Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid
  publication-title: Am J Pathol.
– volume: 25
  start-page: 397
  year: 2006
  ident: B67
  article-title: Muller cells in the healthy and diseases retina
  publication-title: Prog Retin Eye Res.
  doi: 10.1016/j.preteyeres.2006.05.003
– volume: 7
  start-page: 55
  year: 2018
  ident: B19
  article-title: Multiple effects of CD40-CD40L axis in immunity against infection and cancer
  publication-title: Immunotargets Ther.
  doi: 10.2147/ITT.S163614
– volume: 30
  start-page: 343
  year: 2011
  ident: B2
  article-title: Inflammation in diabetic retinopathy
  publication-title: Prog Retin Eye Res.
  doi: 10.1016/j.preteyeres.2011.05.002
– volume: 229
  start-page: 152
  year: 2009
  ident: B17
  article-title: Molecular mechanism and function of CD40/CD40L engagement in the immune system
  publication-title: Immunol Rev.
  doi: 10.1111/j.1600-065X.2009.00782.x
– volume: 84
  start-page: 46
  year: 2009
  ident: B28
  article-title: Proliferative diabetic retinopathy - the influence of diabetes control on the activation of the intraocular molecule system
  publication-title: Diabetes Res Clin Pract.
  doi: 10.1016/j.diabres.2009.01.012
– volume: 57
  start-page: 6278
  year: 2016
  ident: B8
  article-title: Ligation of CD40 in human retinal Muller cells induces P2X7 receptor-dependent death of retinal endothelial cells
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.16-20301
– volume: 30
  start-page: 299
  year: 2005
  ident: B70
  article-title: Increased expression of chemokine KC, an interleukin-8 homologue, in a model of oxygen-induced retinopathy
  publication-title: Curr Eye Res.
  doi: 10.1080/02713680590923276
– volume: 159
  start-page: 1451
  year: 1997
  ident: B74
  article-title: Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.159.3.1451
– volume: 91
  start-page: 404
  year: 2004
  ident: B93
  article-title: Induction of cyclooxygenase-2 in reactive glial cells by the CD40 pathway: relevance to amyotrophic lateral sclerosis
  publication-title: J Neurochem.
  doi: 10.1111/j.1471-4159.2004.02727.x
– volume: 48
  start-page: 719
  year: 2003
  ident: B94
  article-title: A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis
  publication-title: Arthritis Rheum.
  doi: 10.1002/art.10856
– volume: 176
  start-page: 1816
  year: 2010
  ident: B13
  article-title: The CD40-CD40L pathway contributes to the proinflammatory function of intestinal epithelial cells in inflammatory bowel disease
  publication-title: Am J Pathol.
  doi: 10.2353/ajpath.2010.090461
– volume: 92
  start-page: 4342
  year: 1995
  ident: B10
  article-title: CD40 on human endothelial cells: inducibility by cytokines and functional regulation of adhesion molecule expression
  publication-title: Proc Natl Acad Sci USA.
  doi: 10.1073/pnas.92.10.4342
– volume: 54
  start-page: 1559
  year: 2005
  ident: B33
  article-title: Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy
  publication-title: Diabetes.
  doi: 10.2337/diabetes.54.5.1559
– volume: 83
  start-page: 4494
  year: 1986
  ident: B9
  article-title: Activation of human B cells mediated through two distinct cell surface differentiation antigens, Bp35 and Bp50
  publication-title: Proc Natl Acad Sci USA.
  doi: 10.1073/pnas.83.12.4494
– volume: 73
  start-page: 661
  year: 2001
  ident: B50
  article-title: Interleukin-1 beta mediates ischemic injury in the rat retina
  publication-title: Exp Eye Res.
  doi: 10.1006/exer.2001.1072
– volume: 175
  start-page: 6014
  year: 2005
  ident: B99
  article-title: TRAF6 signaling downstream of CD40 primes macrophages to acquire anti-microbial activity in response to TNF-α
  publication-title: J. Immunol
  doi: 10.4049/jimmunol.175.9.6014
– volume: 80
  start-page: 771
  year: 2002
  ident: B40
  article-title: Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine
  publication-title: J Neurochem.
  doi: 10.1046/j.0022-3042.2001.00737.x
– volume: 40
  start-page: 1183
  year: 1999
  ident: B54
  article-title: Retinal ischemia-reperfusion injury attenuated by blocking of adhesion molecules of vascular endothelium
  publication-title: Invest Ophthalmol Vis Sci.
– volume: 8
  start-page: 629
  year: 2012
  ident: B1
  article-title: Pathophysiology of astroglial purinergic signalling
  publication-title: Purinergic Signal.
  doi: 10.1007/s11302-012-9300-0
– volume: 17
  start-page: E1282
  year: 2016
  ident: B61
  article-title: MicroRNA-155 mediates augmented CD40 expression in bone marrow derived plasmacytoid dendritic cells in symptomatic lupus-prone NZB/W F1 mice
  publication-title: Int J Mol Sci
  doi: 10.3390/ijms17081282
– volume: 1
  start-page: e339
  year: 2013
  ident: B25
  article-title: Causes of vision loss worldwide, 1990-2010: a systematic analysis
  publication-title: Lancet Glob Health.
  doi: 10.1016/S2214-109X(13)70113-X
– volume: 50
  start-page: 1987
  year: 2007
  ident: B42
  article-title: Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes
  publication-title: Diabetologia.
  doi: 10.1007/s00125-007-0734-9
– volume: 18
  start-page: 1450
  year: 2004
  ident: B31
  article-title: A central role for inflammation in the pathogenesis of diabetic retinopathy
  publication-title: FASEB J.
  doi: 10.1096/fj.03-1476fje
– volume: 447
  start-page: 247
  year: 2002
  ident: B72
  article-title: P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system
  publication-title: Eur J Pharmacol.
  doi: 10.1016/S0014-2999(02)01756-9
– volume: 58
  start-page: 5594
  year: 2017
  ident: B36
  article-title: Assessment of neurotrophins and inflammatory mediators in vitreous of patients with diabetic retinopathy
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.17-21973
– start-page: 1
  year: 2019
  ident: B43
  article-title: Monocyte chemoattractant protein-1 (MCP-1/CCL2) in diabetic retinopathy: latest evidence and clinical considerations
  publication-title: J Cell Commun Signal
  doi: 10.1007/s12079-018-00500-8
– volume: 6
  start-page: e30442
  year: 2017
  ident: B21
  article-title: CD40 is a major regulator of dendrite growth from developing excitatory and inhibitory neurons
  publication-title: Elife
  doi: 10.7554/eLife.30442
– volume: 182
  start-page: 73
  year: 2007
  ident: B53
  article-title: TNF-α is critical for ischemia-induced leukostasis, but not retinal neovascularization nor VEGF-induced leakage
  publication-title: J. Neuroimmunol
  doi: 10.1016/j.jneuroim.2006.09.015
– volume: 33
  start-page: 248
  year: 2018
  ident: B59
  article-title: IL-17 and CD40 ligand synergistically stimulate the chronicity of diabetic nephropathy
  publication-title: Nephrol Dial Transplant.
  doi: 10.1093/ndt/gfw397
– volume: 75
  start-page: 965
  year: 2000
  ident: B75
  article-title: Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia
  publication-title: J Neurochem.
  doi: 10.1046/j.1471-4159.2000.0750965.x
– volume: 57
  start-page: 2222
  year: 2014
  ident: B6
  article-title: CD40 promotes the development of early diabetic retinopathy
  publication-title: Diabetologia.
  doi: 10.1007/s00125-014-3321-x
– volume: 59
  start-page: 2297
  year: 2010
  ident: B71
  article-title: Muller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage
  publication-title: Diabetes.
  doi: 10.2337/db09-1420
– volume: 181
  start-page: 8719
  year: 2008
  ident: B5
  article-title: CD40 mediates retinal inflammation and neuro-vascular degeneration
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.181.12.8719
– volume: 2017
  start-page: 3940241
  year: 2017
  ident: B48
  article-title: Ischemic retinopathies: oxidative stress and inflammation
  publication-title: Oxid Med Cell Longev.
  doi: 10.1155/2017/3940241
– volume: 50
  start-page: 2319
  year: 2009
  ident: B34
  article-title: Baicalein reduces inflammatory process in a rodent model of diabetic retinopathy
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.08-2642
– volume: 161
  start-page: 3120
  year: 1998
  ident: B82
  article-title: CD40-mediated signal transduction in human airway smooth muscle
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.161.6.3120
– volume: 394
  start-page: 200
  year: 1998
  ident: B22
  article-title: Reduction of atherosclerosis in mice by inhibition of CD40 signaling
  publication-title: Nature.
  doi: 10.1038/28204
– volume: 35
  start-page: 556
  year: 2012
  ident: B24
  article-title: Global prevalence and major risk factors of diabetic retinopathy
  publication-title: Diabetes Care.
  doi: 10.2337/dc11-1909
– volume: 46
  start-page: 349
  year: 2005
  ident: B69
  article-title: Expression of acute-phase response proteins in retinal Muller cells in diabetes
  publication-title: Invest Ophthalmol Vis Sci.
  doi: 10.1167/iovs.04-0860
– volume: 278
  start-page: 18008
  year: 2003
  ident: B87
  article-title: CD40-dependent activation of phosphatidylinositol 3-kinase/Akt pathway mediates endothelial cell survival and in vitro angiogenesis
  publication-title: J Biol Chem.
  doi: 10.1074/jbc.M300711200
– volume: 97
  start-page: 2883
  year: 1996
  ident: B32
  article-title: Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy
  publication-title: J Clin Invest.
  doi: 10.1172/JCI118746
– volume: 21
  start-page: 293
  year: 2009
  ident: B23
  article-title: CD40 and autoimmunity: the dark side of a great activator
  publication-title: Semin Immunol.
  doi: 10.1016/j.smim.2009.05.012
– volume: 157
  start-page: 3569
  year: 1996
  ident: B78
  article-title: Expression of type II nitric oxide synthase in primary human astrocytes and microglia: role of IL-1beta and IL-1 receptor antagonist
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.157.8.3569
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Snippet Extracellular adenosine 5′-triphosphate (ATP) functions not only as a neurotransmitter but is also released by non-excitable cells and mediates cell–cell...
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pubmedcentral
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SubjectTerms ATP
CD40
cytokine
endothelial cell
glia
Immunology
retina
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Title The CD40-ATP-P2X7 Receptor Pathway: Cell to Cell Cross-Talk to Promote Inflammation and Programmed Cell Death of Endothelial Cells
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