Reactive oxygen species activated NLRP3 inflammasomes initiate inflammation in hyperosmolarity stressed human corneal epithelial cells and environment-induced dry eye patients

Experimental Eye Research

Volumn 134, Issue , 2015, Pages 133-140

  Zheng, Qinxiang ^a   Ren, Yueping ^a   Reinach, Peter S ^a   Xiao, Bing ^a   Lu, Huihui ^a   Zhu, Yirui ^a   Qu, Jia ^a   Chen, Wei ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Caspase 1; Dry eye; IL 1 ; Inflammasomes; Inflammation; NLRP3; Reactive oxygen species; Tear film hyperosmolarity

Indexed keywords

ACETYLCYSTEINE; CARRIER PROTEIN; IL1B PROTEIN, HUMAN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MESSENGER RNA; NLRP3 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ADULT; CELL LINE; CORNEA EPITHELIUM; DRUG EFFECTS; DRY EYE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HUMAN; INFLAMMATION; KERATITIS; MALE; METABOLISM; MIDDLE AGED; OSMOTIC PRESSURE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; YOUNG ADULT;

ACETYLCYSTEINE; ADULT; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 1; CELL LINE; DRY EYE SYNDROMES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIUM, CORNEAL; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; KERATITIS; MALE; MIDDLE AGED; OSMOTIC PRESSURE; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; YOUNG ADULT;

EID: 84937546116     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.02.013     Document Type: Article

References (53)

1. 2007. The definition and classification of dry eye disease: report of the Definition and Classification Subcommittee of the International Dry Eye WorkShop (2007). Ocul Surf 5, 75-92.
2. Abelson M.B., Ousler G.W., Nally L.A., Welch D., Krenzer K. Alternative reference values for tear film break up time in normal and dry eye populations. Adv. Exp. Med. Biol. 2002, 506:1121-1125.
3. Augustin A.J., Spitznas M., Kaviani N., Meller D., Koch F.H., Grus F., Gobbels M.J. Oxidative reactions in the tear fluid of patients suffering from dry eyes. Graefes Arch. Clin. Exp. Ophthalmol. 1995, 233:694-698.
4. Backman H., Haghighat F. Indoor-air quality and ocular discomfort. J.Am. Optom. Assoc. 1999, 70:309-316.
5. Bankers-Fulbright J.L., Kalli K.R., McKean D.J. Interleukin-1 signal transduction. Life Sci. 1996, 59:61-83.
6. Bauernfeind F., Bartok E., Rieger A., Franchi L., Nunez G., Hornung V. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J.Immunol. 2011, 187:613-617.
7. Boehm N., Riechardt A.I., Wiegand M., Pfeiffer N., Grus F.H. Proinflammatory cytokine profiling of tears from dry eye patients by means of antibody microarrays. Invest Ophthalmol. Vis. Sci. 2011, 52:7725-7730.
8. Cejkova J., Ardan T., Jirsova K., Jechova G., Malec J., Simonova Z., Cejka C., Filipec M., Dotrelova D., Brunova B. The role of conjunctival epithelial cell xanthine oxidoreductase/xanthine oxidase in oxidative reactions on the ocular surface of dry eye patients with Sjogren's syndrome. Histol. Histopathol. 2007, 22:997-1003.
9. Chen Y., Li M., Li B., Wang W., Lin A., Sheng M. Effect of reactive oxygen species generation in rabbit corneal epithelial cells on inflammatory and apoptotic signaling pathways in the presence of high osmotic pressure. PLoS One 2013, 8:e72900.
10. Chi W., Li F., Chen H., Wang Y., Zhu Y., Yang X., Zhu J., Wu F., Ouyang H., Ge J., Weinreb R.N., Zhang K., Zhuo Y. Caspase-8 promotes NLRP1/NLRP3 inflammasome activation and IL-1beta production in acute glaucoma. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:11181-11186.
11. De Paiva C.S., Chotikavanich S., Pangelinan S.B., Pitcher J.D., Fang B., Zheng X., Ma P., Farley W.J., Siemasko K.F., Niederkorn J.Y., Stern M.E., Li D.Q., Pflugfelder S.C. IL-17 disrupts corneal barrier following desiccating stress. Mucosal Immunol. 2009, 2:243-253.
12. El Annan J., Chauhan S.K., Ecoiffier T., Zhang Q., Saban D.R., Dana R. Characterization of effector T cells in dry eye disease. Invest Ophthalmol. Vis. Sci. 2009, 50:3802-3807.
13. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., Perfettini J.L., Schlemmer F., Tasdemir E., Uhl M., Genin P., Civas A., Ryffel B., Kanellopoulos J., Tschopp J., Andre F., Lidereau R., McLaughlin N.M., Haynes N.M., Smyth M.J., Kroemer G., Zitvogel L. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 2009, 15:1170-1178.
14. Gross O., Thomas C.J., Guarda G., Tschopp J. The inflammasome: an integrated view. Immunol. Rev. 2011, 243:136-151.
15. Hoffman H.M., Mueller J.L., Broide D.H., Wanderer A.A., Kolodner R.D. Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nat. Genet. 2001, 29:301-305.
16. Ikari A., Atomi K., Yamazaki Y., Sakai H., Hayashi H., Yamaguchi M., Sugatani J. Hyperosmolarity-induced up-regulation of claudin-4 mediated by NADPH oxidase-dependent H2O2 production and Sp1/c-Jun cooperation. Biochim. Biophys. Acta 2013, 1833:2617-2627.
17. Jacobi C., Jacobi A., Kruse F.E., Cursiefen C. Tear film osmolarity measurements in dry eye disease using electrical impedance technology. Cornea 2011, 30:1289-1292.
18. Kaido M., Uchino M., Yokoi N., Uchino Y., Dogru M., Kawashima M., Komuro A., Sonomura Y., Kato H., Kinoshita S., Tsubota K. Dry-eye screening by using a functional visual acuity measurement system: the Osaka Study. Invest Ophthalmol. Vis. Sci. 2014, 55:3275-3281.
19. Karthikeyan R.S., Priya J.L., Leal S.M., Toska J., Rietsch A., Prajna V., Pearlman E., Lalitha P. Host response and bacterial virulence factor expression in Pseudomonas aeruginosa and Streptococcus pneumoniae corneal ulcers. PLoS One 2013, 8:e64867.
20. Kryczek I., Wei S., Vatan L., Escara-Wilke J., Szeliga W., Keller E.T., Zou W. Cutting edge: opposite effects of IL-1 and IL-2 on the regulation of IL-17+ T cell pool IL-1 subverts IL-2-mediated suppression. J.Immunol. 2007, 179:1423-1426.
21. Kummer J.A., Broekhuizen R., Everett H., Agostini L., Kuijk L., Martinon F., van Bruggen R., Tschopp J. Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J.Histochem Cytochem 2007, 55:443-452.
22. Latz E., Xiao T.S., Stutz A. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 2013, 13:397-411.
23. Lee H.S., Hattori T., Park E.Y., Stevenson W., Chauhan S.K., Dana R. Expression of toll-like receptor 4 contributes to corneal inflammation in experimental dry eye disease. Invest Ophthalmol. Vis. Sci. 2012, 53:5632-5640.
24. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J.Biol. Chem. 2003, 278:8516-8525.
25. Li D.Q., Chen Z., Song X.J., Luo L., Pflugfelder S.C. Stimulation of matrix metalloproteinases by hyperosmolarity via a JNK pathway in human corneal epithelial cells. Invest Ophthalmol. Vis. Sci. 2004, 45:4302-4311.
26. Li H., Willingham S.B., Ting J.P., Re F. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J.Immunol. 2008, 181:17-21.
27. Liang L., Tan X., Zhou Q., Zhu Y., Tian Y., Yu H., Kijlstra A., Yang P. IL-1beta triggered by peptidoglycan and lipopolysaccharide through TLR2/4 and ROS-NLRP3 inflammasome-dependent pathways is involved in ocular Behcet's disease. Invest Ophthalmol. Vis. Sci. 2013, 54:402-414.
28. Liu H., Begley C., Chen M., Bradley A., Bonanno J., McNamara N.A., Nelson J.D., Simpson T. Alink between tear instability and hyperosmolarity in dry eye. Invest Ophthalmol. Vis. Sci. 2009, 50:3671-3679.
29. Luo L., Li D.Q., Doshi A., Farley W., Corrales R.M., Pflugfelder S.C. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest Ophthalmol. Vis. Sci. 2004, 45:4293-4301.
30. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell. 2002, 10:417-426.
31. Meng G., Zhang F., Fuss I., Kitani A., Strober W. Amutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses. Immunity 2009, 30:860-874.
32. Na K.S., Mok J.W., Kim J.Y., Rho C.R., Joo C.K. Correlations between tear cytokines, chemokines, and soluble receptors and clinical severity of dry eye disease. Invest Ophthalmol. Vis. Sci. 2012, 53:5443-5450.
33. Nakahira K., Haspel J.A., Rathinam V.A., Lee S.J., Dolinay T., Lam H.C., Englert J.A., Rabinovitch M., Cernadas M., Kim H.P., Fitzgerald K.A., Ryter S.W., Choi A.M. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 2011, 12:222-230.
34. Nakamura S., Shibuya M., Nakashima H., Hisamura R., Masuda N., Imagawa T., Uehara M., Tsubota K. Involvement of oxidative stress on corneal epithelial alterations in a blink-suppressed dry eye. Invest Ophthalmol. Vis. Sci. 2007, 48:1552-1558.
35. Ousler G.W., Abelson M.B., Nally L.A., Welch D., Casavant J.S. Evaluation of the time to "natural compensation" in normal and dry eye subject populations during exposure to a controlled adverse environment. Adv. Exp. Med. Biol. 2002, 506:1057-1063.
36. Ozcura F., Aydin S., Helvaci M.R. Ocular surface disease index for the diagnosis of dry eye syndrome. Ocul. Immunol. Inflamm. 2007, 15:389-393.
37. Posa A., Brauer L., Schicht M., Garreis F., Beileke S., Paulsen F. Schirmer strip vs. capillary tube method: non-invasive methods of obtaining proteins from tear fluid. Ann. Anat. 2013, 195:137-142.
38. Qiao Y., Wang P., Qi J., Zhang L., Gao C. TLR-induced NF-kappaB activation regulates NLRP3 expression in murine macrophages. FEBS Lett. 2012, 586:1022-1026.
39. Redfern R.L., Patel N., Hanlon S., Farley W., Gondo M., Pflugfelder S.C., McDermott A.M. Toll-like receptor expression and activation in mice with experimental dry eye. Invest Ophthalmol. Vis. Sci. 2013, 54:1554-1563.
40. Reinehr R., Haussinger D. Hyperosmotic activation of the CD95 death receptor system. Acta Physiol. (Oxf) 2006, 187:199-203.
41. Reinehr R., Haussinger D. Hyperosmotic activation of the CD95 system. Methods Enzymol. 2007, 428:145-160.
42. Rubartelli A., Gattorno M., Netea M.G., Dinarello C.A. Interplay between redox status and inflammasome activation. Trends Immunol. 2011, 32:559-566.
43. Salminen A., Ojala J., Kaarniranta K., Kauppinen A. Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell. Mol. Life Sci. 2012, 69:2999-3013.
44. Schiffman R.M., Christianson M.D., Jacobsen G., Hirsch J.D., Reis B.L. Reliability and validity of the ocular surface disease Index. Arch. Ophthalmol. 2000, 118:615-621.
45. Schlote T., Kadner G., Freudenthaler N. Marked reduction and distinct patterns of eye blinking in patients with moderately dry eyes during video display terminal use. Graefes Arch. Clin. Exp. Ophthalmol. 2004, 242:306-312.
46. Solomon A., Dursun D., Liu Z., Xie Y., Macri A., Pflugfelder S.C. Pro- and anti-inflammatory forms of interleukin-1 in the tear fluid and conjunctiva of patients with dry-eye disease. Invest Ophthalmol. Vis. Sci. 2001, 42:2283-2292.
47. Stevenson W., Chauhan S.K., Dana R. Dry eye disease: an immune-mediated ocular surface disorder. Arch. Ophthalmol. 2012, 130:90-100.
48. Szalai E., Berta A., Szekanecz Z., Szucs G., Modis L. Evaluation of tear osmolarity in non-Sjogren and Sjogren syndrome dry eye patients with the TearLab system. Cornea 2012, 31:867-871.
49. Tarallo V., Hirano Y., Gelfand B.D., Dridi S., Kerur N., Kim Y., Cho W.G., Kaneko H., Fowler B.J., Bogdanovich S., Albuquerque R.J., Hauswirth W.W., Chiodo V.A., Kugel J.F., Goodrich J.A., Ponicsan S.L., Chaudhuri G., Murphy M.P., Dunaief J.L., Ambati B.K., Ogura Y., Yoo J.W., Lee D.K., Provost P., Hinton D.R., Nunez G., Baffi J.Z., Kleinman M.E., Ambati J. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 2012, 149:847-859.
50. Uchino Y., Kawakita T., Miyazawa M., Ishii T., Onouchi H., Yasuda K., Ogawa Y., Shimmura S., Ishii N., Tsubota K. Oxidative stress induced inflammation initiates functional decline of tear production. PLoS One 2012, 7:e45805.
51. Wakamatsu T.H., Dogru M., Matsumoto Y., Kojima T., Kaido M., Ibrahim O.M., Sato E.A., Igarashi A., Ichihashi Y., Satake Y., Shimazaki J., Tsubota K. Evaluation of lipid oxidative stress status in Sjogren syndrome patients. Invest Ophthalmol. Vis. Sci. 2013, 54:201-210.
52. Zheng Q., Ren Y., Reinach P.S., She Y., Xiao B., Hua S., Qu J., Chen W. Reactive oxygen species activated NLRP3 inflammasomes prime environment-induced murine dry eye. Exp. Eye Res. 2014, 125:1-8.
53. Zhou R., Yazdi A.S., Menu P., Tschopp J. Arole for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.