Toll-like receptor 3 activation in retinal pigment epithelium cells - Mitogen-activated protein kinase pathways of cell death and vascular endothelial growth factor secretion

Acta Ophthalmologica

Volumn 91, Issue 3, 2013, Pages

  Klettner, Alexa ^a   Koinzer, Stefan ^a   Meyer, Tim ^b,c   Roider, Johann ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

apoptosis; ERK1 2; geographical atrophy (GA); JNK; retinal pigment epithelium (RPE); TLR3; vascular endothelial growth factor (VEGF)

Indexed keywords

BETA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; POLYCYTIDYLIC ACID; POLYINOSINIC ACID; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 3; VASCULOTROPIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL LYSATE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SWINE; VISUAL ACUITY; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERFERON-BETA; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLY I-C; RETINAL PIGMENT EPITHELIUM; SWINE; TOLL-LIKE RECEPTOR 3; TRYPAN BLUE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84876413038     PISSN: 1755375X     EISSN: 17553768     Source Type: Journal    
DOI: 10.1111/aos.12031     Document Type: Article

References (69)

1. Abcouwer SF, Marjon PI, Loper RK, &, Vander Jagt DL, (2002): Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Invest Ophthalmol Vis Sci 43: 2791-2798.
2. Alexopoulou L, Holt AC, Medzhitov R, &, Flavell RA, (2001): Recognition of double-stranded RNA and activation of NF-kB by Toll-like receptor 3. Nature 413: 732-738.
3. Ashikari M, Tokoro M, Itaya M, Nozaki M, &, Ogura Y, (2010): Non-targeted siRNA suppresses laser-induced choroidal neovascularization. Invest Ophthalmol Vis Sci 51: 3820-3824.
4. Bessero AC, Chiodini F, Rungger-Brändle E, Bonny C, &, Clarke PG, (2010): Role of c-Jun N-terminal kinase pathway in retinal excitotoxicity, and neuroprotection by its inhibition. J Neurochem 3: 1307-1318.
5. Braithwaite SP, Schmid RS, He DN, et al., (2010): Inhibition of c-Jun kinase provides neuroprotection in a model of Alzheimer's disease. Neurobiol Dis 39: 311-317.
6. Brinkmann C, Adrion C, Mansmann U, Schmitz-Valckenberg S, &, Holz F, (2010): Clinical characteristics, progression and risk factors of geographic atrophy. Ophthalmologe 107: 999-1006.
7. Butler J, Sun J, Wertz N, &, Sinkora M, (2006): Antibody repertoire development in swine. Dev Comp Immunol 30: 199-211.
8. Byeon S, Choi S, Lee H, Lee J, Chu Y, &, Kwon O, (2010): Vascular endothelial growth factor as an autocrine survival factor for retinal pigment epithelial cells under oxidative stress via the VEGF-R2/PI3K/Akt. Invest Ophthalmol Vis Sci 51: 1190-1197.
9. Campa C, &, Harding SP, (2011): Anti-VEGF compounds in the treatment of neovascular age related macular degeneration. Curr Drug Targets 12: 173-181.
10. Cho WG, Albuquerque RJ, Kleinman ME, et al., (2009a): Small interfering RNA-induced TLR3 activation inhibits blood and lymphatic vessel growth. Proc Natl Acad Sci USA 106: 7137-7142.
11. Cho Y, Wang J, Chew E, Ferris F, Mitchell P, Chan C, &, Tuo J, (2009b): Toll-like receptor polymorphisms and age-related macular degeneration: replication in three case-control samples. Invest Ophthalmol Vis Sci 50: 5614-5618.
12. Detrick B, &, Hooks JJ, (2010): Immune regulation in the retina. Immunol Res 47: 153-161.
13. Dong X, Li Z, Wang W, Zhang W, Liu S, &, Zhang X, (2011): Protective effect of canolol from oxidative stress induced cell damage in ARPE-19 cells via an ERK mediated antioxidative pathway. Mol Vis 17: 2040-2048.
14. Donovan M, Doonan F, &, Cotter TG, (2011): Differential roles of ERK1/2 and JNK in retinal development and degeneration. J Neurochem 116: 33-42.
15. Doyle SE, O'Connell RO, Vaidya SA, Chow EK, Yee K, &, Cheng G, (2003): Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J Immunol 140: 3565-3571.
16. Dugas B, Charbonnier S, Baarine M, et al., (2010): Effects of oxysterols on cell viability, inflammatory cytokines, VEGF, and reactive oxygen species production on human retinal cells: cytoprotective effects and prevention of VEGF secretion by resveratrol. Eur J Nutr 49: 435-446.
17. Ebihara N, Chen L, Tokura T, Ushio H, Iwatsu M, &, Murakami A, (2007): Distinct function between toll-like receptors 3 and 9 in retinal pigment epithelial cells. Ophthalmic Res 39: 155-163.
18. Eminel S, Roemer L, Waetzig V, &, Herdegen T, (2008): C-Jun N-terminal kinases trigger both degeneration and neurite outgrowth in primary hippocampal and cortical neurons. J Biol Chem 104: 957-969.
19. Fine SL, Berger JW, Maguire MG, &, Ho AC, (2000): Age-related macular degeneration. N Engl J Med 342: 483-492.
20. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, &, Ferrara N, (1998): Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343.
21. Glotin AL, Calipel A, Brossas JY, Faussat AM, Treton J, &, Mascarelli F, (2006): Sustained versus transient ERK1/2 signaling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Invest Ophthalmol Vis Sci 47: 4614-4623.
22. Gu L, Chen H, Tuo J, Gao X, &, Chen L, (2010): Inhibition of experimental choroidal neovascularization in mice by anti-VEGFA/VEGFR2 or non-specific siRNA. Exp Eye Res 91: 433-439.
23. Hollborn M, Wiedemann P, Bringmann A, &, Kohen L, (2010): Chemotactic and cytotoxic effects of minocycline on human retinal pigment epithelial cells. Invest Ophhthalmol Vis Sci 51: 2721-2729.
24. Hooks J, Nagineni C, Hooper L, Hayashi K, &, Detrick B, (2008): IFN-beta provides immuno-protection in the retina by inhibiting ICAM-1 and CXCL9 in retinal pigment epithelial cells. J Immunol 180: 3786-3796.
25. Kalariya NM, Wills NK, Ramana KV, Srivastava S, &, van Kuijk F, (2009): Cadmium-induced apoptotic death of human retinal epithelial cells is mediated by MAPK pathway. Exp Eye Res 89: 494-502.
26. Kaneko H, Dridi S, Tarallo V, et al., (2011): DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471: 325-330.
27. Kinnunen K, &, Yl-Herttuala S, (2012): Vascular endothelial growth factors in retinal and choroidal neovascular disease. Ann Med 44: 1-17. Epub ahead of print.
28. Kleinman ME, Yamada K, Takeda A, et al., (2008): Sequence- and target-independent angiogenesis suppression by siRNA via TLR-3. Nature 452: 591-597.
29. Klettner A, &, Roider J, (2008): Comparison of Bevacizumab, Ranibizumab and Pegaptanib in vitro: efficiency and possible additional pathways. Invest Ophthalmol Vis Sci 49: 4523-4527.
30. Klettner A, &, Roider J, (2009): Constitutive and oxidative-stress-induced expression of VEGF in the RPE are differently regulated by different Mitogen-activated protein kinases. Graefes Arch Clin Exp Ophthalmol 247: 1487-1492.
31. Klettner A, Kruse ML, Meyer T, Wesch D, Kabelitz D, &, Roider J, (2009): Different properties of VEGF-antagonists: Bevacizumab but not Ranibizumab accumulates in RPE cells. Graefes Arch Clin Exp Ophthalmol 247: 1601-1608.
32. Klettner A, Koinzer S, Wätzig V, Herdegen T, &, Roider J, (2010): Deferoxamine mesylate is toxic for RPE cells in vitro, and its toxicity is mediated by p38. Cutan Ocul. Toxicol 29: 122-129.
33. Koff JL, Shao MX, Ueki IF, &, Nadel JA, (2008): Multiple TLRs activated EGFR via a signaling cascade to produce innate immune responses in airway epithelium. Am J Physiol Lung Cell Mol Physiol 294: L1068-L1075.
34. Kumar MV, Nagineni CN, Chin MS, Hooks JJ, &, Detrick B, (2004): Innate immunity in the retina: Toll-like receptor (TLR) signaling in human retina pigment epithelial cells. J Neuroimmunol 153: 7-15.
35. Kunchithapautham K, &, Rohrer B, (2011): Sublytic membrane-attack-complex (MAC) activation alters regulated rather than constitutive VEGF secretion in retinal pigment epithelium monolayers. J Biol Chem 286: 23717-23724.
36. Lassota N, (2008): Clinical and histological aspects of CNV formation: studies in an animal model. Acta Ophthalmol 86: Thesis 2:1: 1-24.
37. Lu M, Kuroki M, Amano S, Tolentino M, Keough K, Kim I, Bucala R, &, Adamis AP, (1998): Advanced glycation end products increases retinal vascular endothelial growth factor expression. J Clin Invest 101: 1219-1224.
38. Maloney SC, Antecka E, Orellana ME, Fernandes BR, Odashiro AN, Eghtedari M, &, Burnier MN, (2010): Choroidal neovascular membranes express Toll-Like Receptor 3. Ophthalmic Res 44: 237-241.
39. Matsumoto M, Kikkawa S, Kohase M, Miyake K, &, Seya T, (2002): Establishment of a monoclonal antibody against human Toll-like receptor 3 that blocks double-stranded RNA-mediated signaling. Biochem Biophys Res Commun 293: 1364-1369.
40. McLeod D, Grebe R, Bhutto I, Merges C, Baba T, &, Lutty G, (2009): Relationship between RPE and choriocapillaris in age-related macular degeneration. Invest Ophthalmol Vis Sci 50: 4982-4991.
41. Middleton S, (2010): Porcine Ophthalmology. Vet Clin Food Anim 26: 557-572.
42. Mitchell D, &, Olive C, (2010): Regulation of Toll-like receptor-induced chemokine production in murine dendritic cells by mitogen-activated protein kinases. Mol Immunol 47: 2065-2073.
43. Moon SJ, Park MK, Oh HJ, et al., (2010): Engagement of toll-like receptor 3 induces vascular endothelial growth factor and interleukin-8 in human rheumatoid synovial fibroblasts. Korean J Intern Med 25: 429-435.
44. Nishijima K, Ng YS, Zhong L, et al., (2007): Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 171: 53-67.
45. Numata T, Araya J, Fujii S, et al., (2011): Insulin-dependent phosphatidylinositol 3-kinase/Akt and ERK signaling pathways inhibit TLR3-mediated human bronchial epithelial cell apoptosis. J Immunol 187: 510-519.
46. Ohkuni T, Kojima T, Ogasawara N, et al., (2011): Poly(I:C) reduces expression of JAM-A and induces secretion of IL-8 and TNF-α via distinct NF-kB pathways in human nasal epithelial cells. Toxicol Appl Pharmacol 250: 29-38.
47. Pacheco-Dominguez RL, Palma-Nicolas JP, Lopez E, &, Lopez-Colorne AM, (2008): The activation of MEK-ERK1/2 by glutamate receptor-stimulation is involved in the regulation of RPE proliferation and morphologic transformation. Exp Eye Res 86: 207-219.
48. Paone A, Galli R, Gabellini C, et al., (2010): Toll-like receptor 3 regulates angiogenesis and apoptosis in prostate cancer cell lines through hypoxia-inducible factor 1 alpha. Neoplasia 12: 539-549.
49. Pisegna S, Pirozzi G, Piccoli M, Frati L, Santoni A, &, Palmieri G, (2004): p38 MAPK activation controls the TLR3-mediated up-regulation of cytotoxicity and cytokine production in human NK cells. Blood 104: 4157-4164.
50. Richard DE, Berra E, Gothie E, Roux D, &, Pouyssegur J, (1999): p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem 274: 32631-32637.
51. Roduit R, &, Schorderet DF, (2008): MAP kinase pathways in UV-induced apoptosis of retinal pigment epithelium ARPE19 cells. Apoptosis 13: 343-353.
52. Saint-Geniez M, Kurihara T, Sekiyama E, Maldonado AE, &, D'Amore PA, (2009): An essential role for RPE-derived soluble VEGF in the maintenance of the choriocapillaris. Proc Natl Acad Sci USA 106: 18751-18756.
53. Sanchez I, Martin R, Ussa F, &, Fernandez-Bueno I, (2011): The parameters of the porcine eyeball. Graefes Arch Clin Exp Ophthalmol 249: 475-482.
54. Strauss O, (2005): The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881.
55. Sunness JS, Bressler NM, &, Maguire MG, (1995): Scanning laser ophthalmoscopic analysis of the pattern of visual loss in age-related geographic atrophy of the macula. Am J Ophthalmol 199: 143-151.
56. Sunness JS, Gonzales-Baron J, Bressler NM, Hawkins B, &, Applegate C, (1999): The development of choroidal neovascularization in eyes with the geographic atrophy form of age-related macular degeneration. Ophthalmology 106: 910-919.
57. Suzuma I, Suzuma K, Ueki K, Hata Y, Feener EP, King GL, &, Aiello LP, (2002): Strech-induced retinal vascular endothelial growth factor expression is mediated by phosphatidylinositol 3-kinase and protein kinase C (PKC)-zeta but not by strech-induced ERK1/2, Akt, Ras or classical/novel PKC pathways. J Biol Chem 277: 1047-1057.
58. Takeda K, &, Akira S, (2004): TLR signaling pathways. Sem Immunol 16: 3-9.
59. Tsao YP, Ho TC, Chen SL, &, Cheng HC, (2006): Pigment epithelium-derived factor inhibits oxidative stress-induced cell death by activation of extracellular signal-regulated kinases in cultured retinal pigment epithelial cells. Life Sci 76: 545-550.
60. Vercammen E, Staal J, &, Beyaert R, (2008): Sensing of viral infection and activation of innate immunity by Toll-like receptor 3. Clin Microbiol Rev 21: 13-25.
61. Wiencke AK, Kiilgaard JF, Nicolini J, Bundgaard M, Röpke C, &, la Cour M, (2003): Growth of cultured porcine retinal pigment epithelial cells. Acta Ophthalmol 81: 170-176.
62. Wong CK, Cheung PF, Ip WK, &, Lam CW, (2007): Intracellular signaling mechanisms regulating toll-like receptor-mediated activation of eosinophils. Am J Respir Cell Mol Biol 37: 85-96.
63. Wörnle M, Merkle M, Wolf A, Ribeiro A, Himmelein S, Kernt M, Kampik A, &, Eibl-Lindner KH, (2011): Inhibition of TLR3-mediated proinflammatory effects by alkylphosphocholines in human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 52: 6536-6544.
64. Yang P, Chen L, Zwart R, &, Kijlstra A, (2002): Immune cells in the porcine retina: Distribution, characterization and morphological features. Invest Ophthalmol Vis Sci 43: 1488-1492.
65. Yang Z, Stratton C, Francis PJ, et al., (2008): Toll-like receptor 3 and geographic atrophy in age-related macular degeneration. N Engl J Med 359: 1456-1463.
66. Ye X, Xu G, Chang Q, Fan J, Sun Z, Qin Y, &, Jiang AC, (2010): Erk1/2 signaling pathways involved in VEGF release in diabetic rat retina. Invest Ophthalmol Vis Sci 51: 5226-5233.
67. Yehoshua Z, Rosenfeld PJ, &, Albini TA, (2011): Current Clinical Trials in Dry AMD and the Definition of Appropriate Clinical Outcome Measures. Semin Ophthalmol 26: 167-180.
68. Yin L, Wu X, Gong Y, Shi Y, Qui Y, Zhang H, Liu X, &, Gu Q, (2011): OX-LDL up-regulates the vascular endothelial growth factor-to-pigment epithelium derived factor ratio in human retinal pigment epithelial cells. Curr Eye Res 36: 379-385.
69. Zhou P, Fan L, Yu K, Zhao M, &, Li X, (2011): oll-like receptor 3 C1234T may protect against geographic atrophy through decreased dsRNA binding capacity. FASEB J 25: 3489-3495.