Upregulation of P2RX7 in Cx3cr1-deficient mononuclear phagocytes leads to increased interleukin-1β secretion and photoreceptor neurodegeneration

Journal of Neuroscience

Volumn 35, Issue 18, 2015, Pages 6987-6996

  Hu, Shulong J ^a,b,c   Calippe, Bertrand ^a,b,c   Lavalette, Sophie ^a,b,c   Roubeix, Christophe ^a,b,c   Montassar, Fadoua ^a,b,c   Housset, Michael ^a,b,c   Levy, Olivier ^a,b,c   Delarasse, Cecile ^c   Paques, Michel ^a,b,c,d   Sahel, José Alain ^a,b,c,d   Sennlaub, Florian ^a,b,c   Guillonneau, Xavier ^a,b,c  

^a INSTITUT DE LA VISION   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d CENTRE HOSPITALIER NATIONAL D OPHTALMOLOGIE DES QUINZE VINGTS   (France)

Author keywords

IL 1; Inflammasome; Monocytes; P2RX7; Retina

Indexed keywords

INTERLEUKIN 1BETA; PURINERGIC P2X RECEPTOR; TOLL LIKE RECEPTOR; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; P2RX7 PROTEIN, MOUSE; PURINERGIC P2X7 RECEPTOR;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL SELECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENETIC ANALYSIS; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MONOCYTE; MONONUCLEAR PHAGOCYTE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUNEL ASSAY; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; COCULTURE; DEFICIENCY; KNOCKOUT MOUSE; MACULAR DEGENERATION; METABOLISM; MOUSE; PATHOLOGY; PHAGOCYTE; PHOTORECEPTOR CELL; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; COCULTURE TECHNIQUES; FEMALE; INTERLEUKIN-1BETA; MACULAR DEGENERATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONONUCLEAR PHAGOCYTE SYSTEM; PHAGOCYTES; PHOTORECEPTOR CELLS; RECEPTORS, CHEMOKINE; RECEPTORS, PURINERGIC P2X7; UP-REGULATION;

EID: 84929378436     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3955-14.2015     Document Type: Article

References (59)

1. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629-640. CrossRef Medline
2. ArbeloaJ, Pérez-Samartín A, Gottlieb M, Matute C (2012) P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol Dis 45:954-961. CrossRef Medline
3. Bartlett R, Yerbury JJ, Sluyter R (2013) P2X7 receptor activation induces reactive oxygen species formation and cell death in murine EOC13 microglia. Mediators Inflamm 2013:271813. CrossRef Medline
4. Bond SR, Naus CC (2014) The pannexins: past and present. Front Physiol 5:58. CrossRef Medline
5. Brändle U, Kohler K, Wheeler-Schilling TH (1998) Expression of the P2X7-receptor subunit in neurons of the rat retina. Brain Res Mol Brain Res 62:106-109. CrossRef Medline
6. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924. CrossRef Medline
7. Chow A, Brown BD, Merad M (2011) Studying the mononuclear phagocyte system in the molecular age. Nat Rev Immunol 11:788-798. CrossRef Medline
8. Chu K, Yin B, Wang J, Peng G, Liang H, Xu Z, Du Y, Fang M, Xia Q, Luo B (2012) Inhibition of P2X7 receptor ameliorates transient global cerebral ischemia/reperfusion injury via modulating inflammatory responses in the rat hippocampus. J Neuroinflammation 9:69. CrossRef Medline
9. Combadière C, Feumi C, Raoul W, Keller N, Rodéro M, Pézard A, Lavalette S, Houssier M, Jonet L, Picard E, Debré P, Sirinyan M, Deterre P, Ferroukhi T, Cohen SY, Chauvaud D, Jeanny JC, Chemtob S, Behar-Cohen F, Senn-laub F (2007) CX3CR1-dependent subretinal microglia cell accumula-tion is associated with cardinal features of age-related macular degeneration. J Clin Invest 117:2920-2928. CrossRef Medline
10. Conductier G, Blondeau N, Guyon A, Nahon JL, Rovère C (2010) The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflamma-tory diseases. J Neuroimmunol 224:93-100. CrossRef Medline
11. Cruz-Guilloty F, Saeed AM, Echegaray JJ, Duffort S, Ballmick A, Tan Y, Betancourt M, Viteri E, Ramkhellawan GC, Ewald E, Feuer W, Huang D, Wen R, Hong L, Wang H, Laird JM, Sene A, Apte RS, Salomon RG, Hollyfìeld JG, et al. (2013) Infiltration of proinflammatory ml macrophages into the outer retina precedes damage in a mouse model of age-related macular degeneration. Int J Inflam 2013:503725. CrossRef Medline
12. Diaz-Hernandez M, Díez-Zaera M, Sánchez-Nogueiro J, Gómez-Villafuertes R, Canals JM, Alberch J, Miras-Portugal MT, Lucas JJ (2009) Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEB J 23: 1893-1906. CrossRef Medline
13. Dinarello CA (1996) Biologic basis for interleukin-1 in disease. Blood 87: 2095-2147. Medline
14. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101:890-898. CrossRef Medline
15. Galea I, Bechmann I, Perry VH (2007) What is immune privilege (not)? Trends Immunol 28:12-18. CrossRef Medline
16. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82. CrossRef Medline
17. Guo C, Otani A, Oishi A, Kojima H, Makiyama Y, Nakagawa S, YoshimuraN (2012) Knockout of ccr2 alleviates photoreceptor cell death in a model of retinitis pigmentosa. Exp Eye Res 104:39-47. CrossRef Medline
18. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 76:463-471. CrossRef Medline
19. Hangai M, Yoshimura N, Yoshida M, Yabuuchi K, Honda Y (1995) Interleukin-1 gene expression in transient retinal ischemia in the rat. Invest Ophthalmol Vis Sci 36:571-578. Medline
20. Huynh ML, Fadok VA, Henson PM (2002) Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-betal secretion and the resolution of inflammation. J Clin Invest 109:41-50. CrossRef Medline
21. Kerur N, Hirano Y, Tarallo V, Fowler BJ, Bastos-Carvalho A, Yasuma T, Yasuma R, Kim Y, Hinton DR, Kirschning CJ, Gelfand BD, Ambati J (2013) TLR-independent and P2X7-dependent signaling mediate Alu RNA-induced NLRP3 inflammasome activation in geographic atrophy. Invest Ophthalmol Vis Sci 54:7395-7401. CrossRef Medline
22. Kido N, Inatani M, Honjo M, Yoneda S, Hara H, Miyawaki N, Honda Y, Tanihara H (2001) Dual effects of interleukin-lbeta on N-methyl-D-aspartate-induced retinal neuronal death in rat eyes. Brain Res 910:153-162. CrossRef Medline
23. Klein R, Peto T, Bird A, Vannewkirk MR (2004) The epidemiology of age-related macular degeneration. Am J Ophthalmol 137:486-495. CrossRef Medline
24. Kohno H, Chen Y, Kevany BM, Pearlman E, Miyagi M, Maeda T, Palczewski K, Maeda A (2013) Photoreceptor proteins initiate microglial activation via toll-like receptor 4 in retinal degeneration mediated by all-trans-retinal. J Biol Chem 288:15326-15341. CrossRef Medline
25. Kraft AD, Harry GJ (2011) Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health 8:2980-3018. CrossRef Medline
26. Lavalette S, Raoul W, Houssier M, Camelo S, Levy O, Calippe B, Jonet L, Behar-Cohen F, Chemtob S, Guillonneau X, Combadière C, Sennlaub F (2011) Interleukin-lbeta inhibition prevents choroidal neovascularization and does not exacerbate photoreceptor degeneration. Am J Pathol 178:2416-2423. CrossRef Medline
27. Lee SJ, Evers S, Roeder D, Parlow AF, Risteli J, Risteli L, Lee YC, Feizi T, Langen H, Nussenzweig MC (2002) Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295:1898-1901. CrossRef Medline
28. Levy O, Calippe B, Lavalette S, Hu SJ, Raoul W, Dominguez E, Housset M, Paques M, Sahel JA, Bemelmans AP, Combadiere C, Guillonneau X, Sennlaub F (2015) Apolipoprotein E promotes subretinal mononuclear phagocyte survival and chronic inflammation in age-related macular degeneration. EMBO Mol Med 7:211-226. CrossRef Medline
29. Liu Y, Biarnés Costa M, Gerhardinger C (2012) IL-lbeta is upregulated in the diabetic retina and retinal vessels: cell-specific effect of high glucose and IL-lbeta autostimulation. PLoS One 7:e36949. CrossRef Medline
30. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677-686. CrossRef Medline
31. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232. CrossRef Medline
32. Miljanich GP, Nemes PP, White DL, Dratz EA (1981) The asymmetric transmembrane distribution of phosphatidylethanolamine, phosphati-dylserine, and fatty acids of the bovine retinal rod outer segment disk membrane. J Membr Biol 60:249-255. CrossRef Medline
33. Molday LL, Molday RS (1987) Glycoproteins specific for the retinal rod outer segment plasma membrane. Biochim Biophys Acta 897:335-340. Medline
34. Murakami Y, Notomi S, Hisatomi T, Nakazawa T, Ishibashi T, Miller JW, Vawas DG (2013) Photoreceptor cell death and rescue in retinal detachment and degenerations. Prog Retin Eye Res 37:114-140. CrossRef Medline
35. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, Mat-subara A, Miyahara S, Nakao S, Yin Y, Benowitz L, Hafezi-Moghadam A, Miller JW (2007) Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci U S A 104:2425-2430. CrossRef Medline
36. Nakazawa T, Kayama M, Ryu M, Kunikata H, Watanabe R, Yasuda M, Kinu-gawa J, Vawas D, Miller JW (2011) Tumor necrosis factor-alpha mediates photoreceptor death in a rodent model of retinal detachment. Invest Ophthalmol Vis Sci 52:1384-1391. CrossRef Medline
37. Niyadurupola N, Sidaway P, Ma N, Rhodes JD, Broadway DC, Sanderson J (2013) P2X7 receptor activation mediates retinal ganglion cell death in a human retina model of ischemic neurodegeneration. Invest Ophthalmol Vis Sci 54:2163-2170. CrossRef Medline
38. Notomi S, Hisatomi T, Murakami Y, Terasaki H, Sonoda S, Asato R, Takeda A, Ikeda Y, Enaida H, Sakamoto T, Ishibashi T (2013) Dynamic increase in extracellular ATP accelerates photoreceptor cell apoptosis via ligation of P2RX7 in subretinal hemorrhage. PLoS One 8:e53338. CrossRef Medline
39. Pelegrin P, Surprenant A (2006) Pannexin-1 mediates large pore formation and interleukin-lbeta release by the ATP-gated P2X7 receptor. EMBO J 25:5071-5082. CrossRef Medline
40. Praetorius HA, Leipziger J (2009) ATP release from non-excitable cells. Pu-rinergic Signal 5:433-446. CrossRef Medline
41. Puthussery T, Fletcher E (2009) Extracellular ATP induces retinal photoreceptor apoptosis through activation of purinoceptors in rodents. J Comp Neurol 513:430-440. CrossRef Medline
42. Puthussery T, Fletcher EL (2004) Synaptic localization of P2X7 receptors in the rat retina. J Comp Neurol 472:13-23. CrossRef Medline
43. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE, Dubyak GR, Hackos D, Dixit VM (2011) Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186:6553-6561. CrossRef Medline
44. Ransohoff RM (2009) Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity 31:711-721. CrossRef Medline
45. Rutar M, Natoli R, Provis JM (2012) Small interfering RNA-mediated suppression of Ccl2 in Muller cells attenuates microglial recruitment and photoreceptor death following retinal degeneration. J Neuroinflammation 9:221. CrossRef Medline
46. Sarks SH (1976) Ageing and degeneration in the macular region: a clinico-pathological study. Br J Ophthalmol 60:324-341. CrossRef Medline
47. Schroder K, Tschopp J (2010) The inflammasomes. Cell 140:821-832. CrossRef Medline
48. Sennlaub F, Auvynet C, Calippe B, Lavalette S, Poupel L, Hu SJ, Dominguez E, Camelo S, Levy O, Guyon E, Saederup N, Charo IF, Rooijen NV, Nandrot E, Bourges JL, Behar-Cohen F, Sahel JA, Guillonneau X, Raoul W, Combadiere C (2013) CCR2(+) monocytes infiltrate atrophic lesions in age-related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3crl deficient mice. EMBO Mol Med 5:1775-1793. CrossRef Medline
49. Shaftel SS, Griffin WS, O'Banion MK (2008) The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J Neuroinflammation 5:7. CrossRef Medline
50. Simi A, Lerouet D, Pinteaux E, Brough D (2007) Mechanisms of regulation for interleukin-lbeta in neurodegenerative disease. Neuropharmacology 52:1563-1569. CrossRef Medline
51. Skaper SD, Facci L, Culbert AA, Evans NA, Chessell I, Davis JB, Richardson JC (2006) P2X(7) receptors on microglial cells mediate injury to cortical neurons in vitro. Glia 54:234-242. CrossRef Medline
52. Srinivasan B, Roque CH, Hempstead BL, Al-Ubaidi MR, Roque RS (2004) Microglia-derived pronerve growth factor promotes photoreceptor cell death via p75 neurotrophin receptor. J Biol Chem 279:41839-41845. CrossRef Medline
53. Streilein JW (2003) Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat Rev Immunol 3:879-889. CrossRef Medline
54. Sugiyama T, Oku H, Shibata M, Fukuhara M, Yoshida H, Ikeda T (2010) Involvement of P2X7 receptors in the hypoxia-induced death of rat retinal neurons. Invest Ophthalmol Vis Sci 51:3236-3243. CrossRef Medline
55. Wolf Y, Yona S, Kim KW, Jung S (2013) Microglia, seen from the CXCR1 angle. Front Cell Neurosci 7:26. CrossRef Medline
56. Wu GS, Jiang M, Liu YH, Nagaoka Y, Rao NA (2012) Phenotype of transgenic mice overexpressed with inducible nitric oxide synthase in the retina. PLoS One 7:e43089. CrossRef Medline
57. Yoneda S, Tanihara H, Kido N, Honda Y, Goto W, Hara H, Miyawaki N (2001) Interleukin-lbeta mediates ischemic injury in the rat retina. Exp Eye Res 73:661-667. CrossRef Medline
58. Yu Q, Guo Z, Liu X, Ouyang Q, He C, Burnstock G, Yuan H, Xiang Z (2013) Block of P2X7 receptors could partly reverse the delayed neuronal death in area CA1 of the hippocampus after transient global cerebral ischemia. Purinergic Signal 9:663-675. CrossRef Medline
59. Zieger M, Ahnelt PK, Uhrin P (2014) CX3CL1 (fractalkine) protein expression in normal and degenerating mouse retina: in vivo studies. PLoS One 9:el06562. CrossRef Medline