P2Y1 receptor signaling contributes to high salt-induced priming of the NLRP3 inflammasome in retinal pigment epithelial cells

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Prager, Philipp ^a   Hollborn, Margrit ^a   Steffen, Anja ^a   Wiedemann, Peter ^a   Kohen, Leon ^a,b   Bringmann, Andreas ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b HELIOS Klinikum Aue   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRYOPYRIN; HYPOXIA INDUCIBLE FACTOR 1; INFLAMMASOME; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOLIPASE C; PROTEIN KINASE C; PURINERGIC P2Y1 RECEPTOR; SMALL INTERFERING RNA; NLRP3 PROTEIN, HUMAN; SODIUM CHLORIDE; TRANSCRIPTION FACTOR;

ARTICLE; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPEROSMOTIC STRESS; IL 18 GENE; IL 1BETA GENE; NLRP3 GENE; OSMOLARITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RETINAL PIGMENT EPITHELIUM; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

CELLS, CULTURED; GENE EXPRESSION; HUMANS; INFLAMMASOMES; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; RECEPTORS, PURINERGIC P2Y1; RETINAL PIGMENT EPITHELIUM; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; TRANSCRIPTION FACTORS;

EID: 84994031419     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165653     Document Type: Article

References (49)

1. Klein R, Klein BE, Knudtson MD, Meuer SM, Swift M, Gangnon RE (2007) Fifteen-year cumulative incidence of age-related macular degeneration: the Beaver Dam Eye Study. Ophthalmology 114: 253-262. doi: 10.1016/j.ophtha.2006.10.040 PMID: 17270675
2. Xu H, Chen M, Forrester JV (2009) Para-inflammation in the aging retina. Prog Retin Eye Res 28: 348-368. doi: 10.1016/j.preteyeres.2009.06.001 PMID: 19560552
3. Cheung CM, Wong TY (2014) Is age-related macular degeneration a manifestation of systemic disease? New prospects for early intervention and treatment. J Intern Med 276: 140-153. doi: 10.1111/ joim.12227 PMID: 24581182
4. Nita M, Grzybowski A, Ascaso FJ, Huerva V (2014) Age-related macular degeneration in the aspect of chronic low-grade inflammation (pathophysiological parainflammation). Mediators Inflamm 2014: 930671. doi: 10.1155/2014/930671 PMID: 25214719
5. Gross O, Thomas CJ, Guarda G, Tschopp J (2011) The inflammasome: an integrated view. Immunological Rev 243: 136-151.
6. Latz E, Xiao TS, Stutz A (2013) Activation and regulation of the inflammasomes. Nat Rev Immunol 13: 397-411. doi: 10.1038/nri3452 PMID: 23702978
7. Tseng WA, Thein T, Kinnunen K, Lashkari K, Gregory MS, D'Amore PA, et al. (2013) NLRP3 inflammasome activation in retinal pigment epithelial cells by lysosomal destabilization: implications for agerelated macular degeneration. Invest Ophthalmol Vis Sci 54: 110-120. doi: 10.1167/iovs.12-10655 PMID: 23221073
8. Kerur N, Hirano Y, Tarallo V, Fowler BJ, Bastos-Carvalho A, Yasuma T, et al. (2013) TLR-independent and P2X7 -dependent signaling mediate Alu RNA-induced NLRP3 inflammasome activation in geographic atrophy. Invest Ophthalmol Vis Sci 54: 7395-7401. doi: 10.1167/iovs.13-12500 PMID: 24114535
9. Fowler BJ, Gelfand BD, Kim Y, Kerur N, Tarallo V, Hirano Y, et al. (2014) Nucleoside reverse transcriptase inhibitors possess intrinsic anti-inflammatory activity. Science 346: 1000-1003. doi: 10.1126/ science.1261754 PMID: 25414314
10. Marneros AG (2013) NLRP3 inflammasome blockade inhibits VEGF-A-induced age-related macular degeneration. Cell Rep 4: 945-958. doi: 10.1016/j.celrep.2013.08.002 PMID: 24012762
11. Doyle SL, Campbell M, Ozaki E, Salomon RG, Mori A, Kenna PF, et al. (2012) NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components. Nat Med 18: 791-798. doi: 10.1038/nm.2717 PMID: 22484808
12. Kauppinen A, Niskanen H, Suuronen T, Kinnunen K, Salminen A, Kaarniranta K (2012) Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells-implications for age-related macular degeneration (AMD). Immunol Lett 147: 29-33. doi: 10.1016/j.imlet.2012.05.005 PMID: 22698681
13. Anderson OA, Finkelstein A, Shima DT (2013) A2E induces IL-1β production in retinal pigment epithelial cells via the NLRP3 inflammasome. PLoS One 8: e67263. doi: 10.1371/journal.pone.0067263 PMID: 23840644
14. Shi G, Chen S, Wandu WS, Ogbeifun O, Nugent LF, Maminishkis A, et al. (2015) Inflammasomes induced by 7-ketocholesterol and other stimuli in RPE and in bone marrow-derived cells differ markedly in their production of IL-1β and IL-18. Invest Ophthalmol Vis Sci 56: 1658-1664. doi: 10.1167/iovs.14-14557 PMID: 25678688
15. Brandstetter C, Mohr LK, Latz E, Holz FG, Krohne TU (2015) Light induces NLRP3 inflammasome activation in retinal pigment epithelial cells via lipofuscin-mediated photooxidative damage. J Mol Med (Berl) 93: 905-916.
16. Sperduto RD, Hiller R (1986) Systemic hypertension and age-related maculopathy in the Framingham Study. Arch Ophthalmol 104: 216-219. PMID: 3947296
17. Klein R, Klein BE, Tomany SC, Cruickshanks KJ (2003) The association of cardiovascular disease with the long-term incidence of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology 110: 1273-1280. doi: 10.1016/S0161-6420(03)00599-2 PMID: 12799274
18. Van Leeuwen R, Ikram MK, Vingerling JR, Witteman JC, Hofman A, de Jong PT (2003) Blood pressure, atherosclerosis, and the incidence of age-related maculopathy: the Rotterdam Study. Invest Ophthalmol Vis Sci 44: 3771-3777. PMID: 12939290
19. Lifton RP, Gharavi AG, Geller DS (2001) Molecular mechanisms of human hypertension. Cell 104: 545-556. PMID: 11239411
20. He FJ, Markandu ND, Sagnella GA, de Wardener HE, MacGregor GA (2005) Plasma sodium: ignored and underestimated. Hypertension 45: 98-102. doi: 10.1161/01.HYP.0000149431.79450.a2 PMID: 15557392
21. Junger WG, Liu FC, Loomis WH, Hoyt DB (1994) Hypertonic saline enhances cellular immune function. Circ Shock 42: 190-196. PMID: 8055665
22. Yi B, Titze J, Rykova M, Feuerecker M, Vassilieva G, Nichiporuk I, et al. (2015) Effects of dietary salt levels on monocytic cells and immune responses in healthy human subjects: a longitudinal study. Transl Res 166: 103-110. doi: 10.1016/j.trsl.2014.11.007 PMID: 25497276
23. Ip WKE, Medzhitov R (2015) Macrophages monitor tissue osmolarity and induce inflammatory response through NLRP3 and NLRC4 inflammasome activation. Nat Commun 6: 6931. doi: 10.1038/ ncomms7931 PMID: 25959047
24. Hollborn M, Vogler S, Reichenbach A, Wiedemann P, Bringmann A, Kohen L (2015) Regulation of the hyperosmotic induction of aquaporin 5 and VEGF in retinal pigment epithelial cells: Involvement of NFAT5. Mol Vis 21: 360-377. PMID: 25878490
25. Veltmann M, Hollborn M, Reichenbach A, Wiedemann P, Kohen L, Bringmann A (2016) Osmotic induction of angiogenic growth factor expression in human retinal pigment epithelial cells. PLoS One 11: e0147312. doi: 10.1371/journal.pone.0147312 PMID: 26800359
26. Chen R, Hollborn M, Grosche A, Reichenbach A, Wiedemann P, Bringmann A, et al. (2014) Effects of the vegetable polyphenols epigallocatechin-3-gallate, luteolin, apigenin, myricetin, quercetin, and cyanidin in retinal pigment epithelial cells. Mol Vis 20: 242-258.
27. Bours MJ, Dagnelie PC, Giuliani AL, Wesselius A, Di Virgilio F (2011) P2 receptors and extracellular ATP: a novel homeostatic pathway in inflammation. Front Biosci (Schol Ed) 3: 1443-1456.
28. Housley GD, Bringmann A, Reichenbach A (2009) Purinergic signaling in special senses. Trends Neurosci 32: 128-141. doi: 10.1016/j.tins.2009.01.001 PMID: 19232752
29. Woehrle T, Yip L, Manohar M, Sumi Y, Yao Y, Chen Y, et al. (2010) Hypertonic stress regulates T cell function via pannexin-1 hemichannels and P2X receptors. J Leukoc Biol 88: 1181-1189. doi: 10.1189/ jlb.0410211 PMID: 20884646
30. Schust J, Sperl B, Hollis A, Mayer TU, Berg T (2006) Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem Biol 13: 1235-1242. doi: 10.1016/j.chembiol.2006.09.018 PMID: 17114005
31. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-êB. Proc Natl Acad Sci U S A 93: 9090-9095. PMID: 8799159
32. Lee K, Lee JH, Boovanahalli SK, Jin Y, Lee M, Jin X, et al. (2007) (Aryloxyacetylamino)benzoic acid analogues: a new class of hypoxia-inducible factor-1 inhibitors. J Med Chem 50: 1675-1684. doi: 10. 1021/jm0610292 PMID: 17328532
33. Cheung CY, Ko BC (2013) NFAT5 in cellular adaptation to hypertonic stress-regulations and functional significance. J Mol Signal 8: 5. doi: 10.1186/1750-2187-8-5 PMID: 23618372
34. Piippo N, Korkmaz A, Hytti M, Kinnunen K, Salminen A, Atalay M, et al. (2014) Decline in cellular clearance systems induces inflammasome signaling in human ARPE-19 cells. Biochim Biophys Acta 1843: 3038-3046. doi: 10.1016/j.bbamcr.2014.09.015 PMID: 25268952
35. Bauernfeind F, Bartok E, Rieger A, Franchi L, Núñez G, Hornung V (2011) Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol 187: 613-617. doi: 10.4049/jimmunol.1100613 PMID: 21677136
36. Taylor SR, Gonzalez-Begne M, Dewhurst S, Chimini G, Higgins CF, Melvin JE, et al. (2008) Sequential shrinkage and swelling underlie P2X7 -stimulated lymphocyte phosphatidylserine exposure and death. J Immunol 180: 300-308. PMID: 18097031
37. Schorn C, Frey B, Lauber K, Janko C, Strysio M, Keppeler H, et al. (2011) Sodium overload and water influx activate the NALP3 inflammasome. J Biol Chem 286: 35-41. doi: 10.1074/jbc.M110.139048 PMID: 21051542
38. Lang F, Böhmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V (2006) (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol Rev 86: 1151-1178. doi: 10.1152/physrev.00050.2005 PMID: 17015487
39. Wu C, Yosef N, Thalhamer T, Zhu C, Xiao S, Kishi Y, et al. (2013) Induction of pathogenic TH 17 cells by inducible salt-sensing kinase SGK1. Nature 496: 513-517. doi: 10.1038/nature11984 PMID: 23467085
40. Chen S, Grigsby CL, Law CS, Ni X, Nekrep N, Olsen K, et al. (2009) Tonicity-dependent induction of Sgk1 expression has a potential role in dehydration-induced natriuresis in rodents. J Clin Invest 119: 1647-1658. doi: 10.1172/JCI35314 PMID: 19436108
41. Nicholas SA, Bubnov VV, Yasinska IM, Sumbayev VV (2011) Involvement of xanthine oxidase and hypoxia-inducible factor 1 in Toll-like receptor 7/8-mediated activation of caspase 1 and interleukin-1β. Cell Mol Life Sci 68: 151-158. doi: 10.1007/s00018-010-0450-3 PMID: 20632067
42. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. (2013) Succinate is an inflammatory signal that induces IL-1β through HIF-1α. Nature 496: 238-242. doi: 10. 1038/nature11986 PMID: 23535595
43. Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z, Olivier AK, et al. (2013) Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 39: 311-323. doi: 10.1016/j.immuni.2013.08. 001 PMID: 23954133
44. Murakami T, Ockinger J, Yu J, Byles V, McColl A, Hofer AM, et al. (2012) Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc Natl Acad Sci U S A 109: 11282-11287. doi: 10.1073/pnas.1117765109 PMID: 22733741
45. Mohr LK, Hoffmann AV, Brandstetter C, Holz FG, Krohne TU (2015) Effects of inflammasome activation on secretion of inflammatory cytokines and vascular endothelial growth factor by retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 56: 6404-6413. doi: 10.1167/iovs.15-16898 PMID: 26444721
46. Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, Muller DN, et al. (2013) Sodium chloride drives autoimmune disease by the induction of pathogenic TH 17 cells. Nature 496: 518-522. doi: 10.1038/nature11868 PMID: 23467095
47. Go WY, Liu X, Roti MA, Liu F, Ho SN (2004) NFAT5/TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc Natl Acad Sci U S A 101: 10673-10678. doi: 10.1073/pnas.0403139101 PMID: 15247420
48. Machnik A, Neuhofer W, Jantsch J, Dahlmann A, Tammela T, Machura K, et al. (2009) Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med 15: 545-552. doi: 10.1038/nm.1960 PMID: 19412173
49. Appel LJ, Frohlich ED, Hall JE, Pearson TA, Sacco RL, Seals DR, et al. (2011) The importance of population-wide sodium reduction as a means to prevent cardiovascular disease and stroke: a call to action from the American Heart Association. Circulation 123: 1138-1143. doi: 10.1161/CIR. 0b013e31820d0793 PMID: 21233236