Inflammatory Cytokines Protect Retinal Pigment Epithelial Cells from Oxidative Stress-Induced Death

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Juel, Helene B ^a   Faber, Carsten ^a   Svendsen, Signe G ^a   Vallejo, Abbe N ^b   Nissen, Mogens H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN P62; TUMOR NECROSIS FACTOR ALPHA;

ANTIOXIDANT ACTIVITY; ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ADULT; AUTOPHAGY; CELL DEATH; CELL LINE; CELL SURVIVAL; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; CYTOKINES; CYTOPROTECTION; EPITHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; IODATES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDANTS; OXIDATIVE STRESS; RETINAL PIGMENT EPITHELIUM; SUPEROXIDE DISMUTASE; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84877996041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064619     Document Type: Article

References (72)

1. Bonilha VL, (2008) Age and disease-related structural changes in the retinal pigment epithelium. Clin Ophthalmol 2: 413-424.
2. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, et al. (2004) Global data on visual impairment in the year 2002. Bull World Health Organ 82: 844-851.
3. Khandhadia S, Cherry J, Lotery AJ, (2012) Age-related macular degeneration. Adv Exp Med Biol 724: 15-36.
4. Crabb JW, Miyagi M, Gu X, Shadrach K, West KA, et al. (2002) Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci U S A 99: 14682-14687.
5. Russell SR, Mullins RF, Schneider BL, Hageman GS, (2000) Location, substructure, and composition of basal laminar drusen compared with drusen associated with aging and age-related macular degeneration. Am J Ophthalmol 129: 205-214.
6. Johnson LV, Leitner WP, Staples MK, Anderson DH, (2001) Complement activation and inflammatory processes in Drusen formation and age related macular degeneration. Exp Eye Res 73: 887-896.
7. Mullins RF, Russell SR, Anderson DH, Hageman GS, (2000) Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J 14: 835-846.
8. Umeda S, Suzuki MT, Okamoto H, Ono F, Mizota A, et al. (2005) Molecular composition of drusen and possible involvement of anti-retinal autoimmunity in two different forms of macular degeneration in cynomolgus monkey (Macaca fascicularis). FASEB J 19: 1683-1685.
9. Rodrigues EB, (2007) Inflammation in dry age-related macular degeneration. Ophthalmologica 221: 143-152.
10. Laine M, Jarva H, Seitsonen S, Haapasalo K, Lehtinen MJ, et al. (2007) Y402H polymorphism of complement factor H affects binding affinity to C-reactive protein. J Immunol 178: 3831-3836.
11. Johnson LV, Ozaki S, Staples MK, Erickson PA, Anderson DH, (2000) A potential role for immune complex pathogenesis in drusen formation. Exp Eye Res 70: 441-449.
12. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, et al. (2001) An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res 20: 705-732.
13. Shankar A, Mitchell P, Rochtchina E, Tan J, Wang JJ, (2007) Association between circulating white blood cell count and long-term incidence of age-related macular degeneration: the Blue Mountains Eye Study. Am J Epidemiol 165: 375-382.
14. Boekhoorn SS, Vingerling JR, Witteman JC, Hofman A, de Jong PT, (2007) C-reactive protein level and risk of aging macula disorder: The Rotterdam Study. Arch Ophthalmol 125: 1396-1401.
15. Schaumberg DA, Christen WG, Buring JE, Glynn RJ, Rifai N, et al. (2007) High-sensitivity C-reactive protein, other markers of inflammation, and the incidence of macular degeneration in women. Arch Ophthalmol 125: 300-305.
16. Seddon JM, George S, Rosner B, Rifai N, (2005) Progression of age-related macular degeneration: prospective assessment of C-reactive protein, interleukin 6, and other cardiovascular biomarkers. Arch Ophthalmol 123: 774-782.
17. Klein R, Knudtson MD, Klein BE, Wong TY, Cotch MF, et al. (2008) Inflammation, complement factor h, and age-related macular degeneration: the Multi-ethnic Study of Atherosclerosis. Ophthalmology 115: 1742-1749.
18. Gehrs KM, Jackson JR, Brown EN, Allikmets R, Hageman GS, (2010) Complement, age-related macular degeneration and a vision of the future. Arch Ophthalmol 128: 349-358.
19. Markomichelakis NN, Theodossiadis PG, Sfikakis PP, (2005) Regression of neovascular age-related macular degeneration following infliximab therapy. American Journal of Ophthalmology 139: 537-540.
20. Wang Y, Wang VM, Chan CC, (2011) The role of anti-inflammatory agents in age-related macular degeneration (AMD) treatment. Eye (Lond) 25: 127-139.
21. Theodossiadis PG, Liarakos VS, Sfikakis PP, Vergados IA, Theodossiadis GP, (2009) Intravitreal Administration of the Anti-Tumor Necrosis Factor Agent Infliximab for Neovascular Age-related Macular Degeneration. American Journal of Ophthalmology 147: 825-830.
22. Kang KH, Lemke G, Kim JW, (2009) The PI3K-PTEN tug-of-war, oxidative stress and retinal degeneration. Trends Mol Med 15: 191-198.
23. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB, (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49: 1603-1616.
24. Cano M, Thimmalappula R, Fujihara M, Nagai N, Sporn M, et al. (2010) Cigarette smoking, oxidative stress, the anti-oxidant response through Nrf2 signaling, and Age-related Macular Degeneration. Vision Research 50: 652-664.
25. Liang FQ, Godley BF, (2003) Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Experimental Eye Research 76: 397-403.
26. Age-related Eye Disease Study Research Group (2001) A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene, and zinc for age-related macular degeneration and vision loss: AREDS report no. 8. Arch Ophthalmol 119: 1417-1436.
27. SanGiovanni JP, Chew EY, Clemons TE, Ferris FL III, Gensler G, et al. (2007) The relationship of dietary carotenoid and vitamin A, E, and C intake with age-related macular degeneration in a case-control study: AREDS Report No. 22. Arch Ophthalmol 125: 1225-1232.
28. Kansagara D, Gleitsmann K, Gillingham M, Freeman M, Quinones A, (2012) Nutritional Supplements for Age-Related Macular Degeneration: A Systematic Review. VA Evidence-based Synthesis Program Reports.
29. Kinnunen K, Petrovski G, Moe MC, Berta A, Kaarniranta K, (2012) Molecular mechanisms of retinal pigment epithelium damage and development of age-related macular degeneration. Acta Ophthalmologica 90: 299-309.
30. Glick D, Barth S, Macleod KF, (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221: 3-12.
31. Hyttinen JM, Petrovski G, Salminen A, Kaarniranta K, (2011) 5′-Adenosine monophosphate-activated protein kinase-mammalian target of rapamycin axis as therapeutic target for age-related macular degeneration. Rejuvenation Res 14: 651-660.
32. Kaarniranta K, Hyttinen J, Ryhanen T, Viiri J, Paimela T, et al. (2010) Mechanisms of protein aggregation in the retinal pigment epithelial cells. Front Biosci (Elite Ed) 2: 1374-1384.
33. Rosello A, Warnes G, Meier UC, (2012) Cell death pathways and autophagy in the central nervous system and its involvement in neurodegeneration, immunity and central nervous system infection: to die or not to die- that is the question. Clinical & Experimental Immunology 168: 52-57.
34. Fong WG, Tsilfidis C, (2012) Retinal degeneration and cellular suicide. Adv Exp Med Biol 723: 207-214.
35. Kaarniranta K, (2010) Autophagy-hot topic in AMD. Acta Ophthalmol 88: 387-388.
36. Wang AL, Lukas TJ, Yuan M, Du N, Tso MO, et al. (2009) Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration. PLoS ONE 4: e4160.
37. Ehrlich R, Harris A, Kheradiya NS, Winston DM, Ciulla TA, et al. (2008) Age-related macular degeneration and the aging eye. Clin Interv Aging 3: 473-482.
38. Sparrow JR, Gregory-Roberts E, Yamamoto K, Blonska A, Ghosh SK, et al. (2012) The bisretinoids of retinal pigment epithelium. Progress in Retinal and Eye Research 31: 121-135.
39. Mitter SK, Rao HV, Qi X, Cai J, Sugrue A, et al. (2012) Autophagy in the retina: a potential role in age-related macular degeneration. Adv Exp Med Biol 723: 83-90.
40. Juel HB, Faber C, Udsen MS, Folkersen L, Nissen MH, (2012) Chemokine Expression in Retinal Pigment Epithelial Cells in Response to Co-culture with Activated T Cells. Invest Ophthalmol Vis Sci E-pub ahead of print.
41. Juel HB, Kaestel C, Folkersen L, Faber C, Heegaard NH, et al. (2011) Retinal pigment epithelial cells upregulate expression of complement factors after co-culture with activated T cells. Exp Eye Res 92: 180-188.
42. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9: 671-675.
43. Cossarizza A, Baccaranicontri M, Kalashnikova G, Franceschi C, (1993) A New Method for the Cytofluorometric Analysis of Mitochondrial Membrane Potential Using the J-Aggregate Forming Lipophilic Cation 5,5-,6,6-Tetrachloro-1,1-,3,3-tetraethylbenzimidazolcarbocyanine Iodide (JC-1). Biochemical and Biophysical Research Communications 197: 40-45.
44. Barth S, Glick D, Macleod KF, (2010) Autophagy: assays and artifacts. J Pathol 221: 117-124.
45. Rusten TE, Stenmark H, (2010) p62, an autophagy hero or culprit? Nat Cell Biol 12: 207-209.
46. Zhao C, Yasumura D, Li X, Matthes M, Lloyd M, et al. (2011) mTOR-mediated dedifferentiation of the retinal pigment epithelium initiates photoreceptor degeneration in mice. J Clin Invest 121 (1) (): 369-383.
47. Kim JH, Kim JH, Jun HO, Yu YS, Min BH, et al. (2010) Protective effect of clusterin from oxidative stress-induced apoptosis in human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 51: 561-566.
48. Liu JH, Chen MM, Huang JW, Wann H, Ho LK, et al. (2010) Therapeutic effects and mechanisms of action of mannitol during H2O2-induced oxidative stress in human retinal pigment epithelium cells. J Ocul Pharmacol Ther 26: 249-257.
49. Choi SH, Park SJ, Cha GH, Quan JH, Chang NS, et al. (2011) Toxoplasma gondii protects against H2O2-induced apoptosis in ARPE-19 cells through the transcriptional regulation of apoptotic elements and downregulation of the p38 MAPK pathway. Acta Ophthalmologica 89: e350-e356.
50. Kasahara E, Lin LR, Ho YS, Reddy VN, (2005) SOD2 protects against oxidation-induced apoptosis in mouse retinal pigment epithelium: implications for age-related macular degeneration. Invest Ophthalmol Vis Sci 46: 3426-3434.
51. Lin H, Qian J, Castillo AC, Long B, Keyes KT, et al. (2011) Effect of miR-23 on Oxidant-Induced Injury in Human Retinal Pigment Epithelial Cells. Investigative Ophthalmology & Visual Science 52: 6308-6314.
52. Byeon SH, Lee SC, Choi SH, Lee HK, Lee JH, et al. (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.
53. Cao GF, Liu Y, Yang W, Wan J, Yao J, et al. (2011) Rapamycin sensitive mTOR activation mediates nerve growth factor (NGF) induced cell migration and pro-survival effects against hydrogen peroxide in retinal pigment epithelial cells. Biochemical and Biophysical Research Communications 414: 499-505.
54. Yin J, Thomas F, Lang JC, Chaum E, (2011) Modulation of oxidative stress responses in the human retinal pigment epithelium following treatment with vitamin C. J Cell Physiol 226: 2025-2032.
55. Cao X, Liu M, Tuo J, Shen D, Chan CC, (2010) The effects of quercetin in cultured human RPE cells under oxidative stress and in Ccl2/Cx3cr1 double deficient mice. Exp Eye Res 91: 15-25.
56. Barot M, Gokulgandhi MR, Mitra AK, (2011) Mitochondrial Dysfunction in Retinal Diseases. Curr Eye Res 36: 1069-1077.
57. Feher J, Kovacs I, Artico M, Cavallotti C, Papale A, et al. (2006) Mitochondrial alterations of retinal pigment epithelium in age-related macular degeneration. Neurobiology of Aging 27: 983-993.
58. Ding X, Patel M, Chan CC, (2009) Molecular pathology of age-related macular degeneration. Prog Retin Eye Res 28: 1-18.
59. Malek G, Dwyer M, McDonnell D, (2012) Exploring the potential role of the oxidant-activated transcription factor aryl hydrocarbon receptor in the pathogenesis of AMD. Adv Exp Med Biol 723: 51-59.
60. Lin H, Xu H, Liang FQ, Liang H, Gupta P, et al. (2011) Mitochondrial DNA Damage and Repair in RPE Associated with Aging and Age-Related Macular Degeneration. Investigative Ophthalmology & Visual Science 52: 3521-3529.
61. Burke JM, (1989) Stimulation of DNA synthesis in human and bovine RPE by peptide growth factors: the response to TNF-alpha and EGF is dependent upon culture density. Curr Eye Res 8: 1279-1286.
62. Harris MS, Sakamoto T, Kimura H, He S, Spee C, et al. (1996) Hypericin inhibits cell growth and induces apoptosis in retinal pigment epithelial cells: possible involvement of protein kinase C. Curr Eye Res 15: 255-262.
63. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
64. Viiri J, Hyttinen JM, Ryhanen T, Rilla K, Paimela T, et al. (2010) p62/sequestosome 1 as a regulator of proteasome inhibitor-induced autophagy in human retinal pigment epithelial cells. Mol Vis 16: 1399-1414.
65. Yoon YH, Cho KS, Hwang JJ, Lee SJ, Choi JA, et al. (2010) Induction of Lysosomal Dilatation, Arrested Autophagy, and Cell Death by Chloroquine in Cultured ARPE-19 Cells. Investigative Ophthalmology & Visual Science 51: 6030-6037.
66. Arjamaa O, Nikinmaa M, Salminen A, Kaarniranta K, (2009) Regulatory role of HIF-1alpha in the pathogenesis of age-related macular degeneration (AMD). Ageing Res Rev 8: 349-358.
67. Kurz T, Karlsson M, Brunk UT, Nilsson SE, (2009) ARPE-19 retinal pigment epithelial cells are highly resistant to oxidative stress and exercise strict control over their lysosomal redox-active iron. Autophagy 5: 494-501.
68. Usui S, Oveson BC, Iwase T, Lu L, Lee SY, et al. (2011) Overexpression of SOD in retina: Need for increase in H2O2-detoxifying enzyme in same cellular compartment. Free Radical Biology and Medicine 51: 1347-1354.
69. Thampi P, Rao HV, Mitter SK, Cai J, Mao H, et al. (2012) The 5HT-1a Receptor Agonist 8-Oh DPAT Induces Protection from Lipofuscin Accumulation and Oxidative Stress in the Retinal Pigment Epithelium. PLoS ONE 7: e34468.
70. Yang D, Elner SG, Lin LR, Reddy VN, Petty H, et al. (2009) Association of Superoxide Anions with Retinal Pigment Epithelial Cell Apoptosis Induced by Mononuclear Phagocytes. Invest Ophthalmol Vis Sci 50: 4998-5005.
71. Zhao Z, Chen Y, Wang J, Sternberg P, Freeman ML, et al. (2011) Age-Related Retinopathy in NRF2-Deficient Mice. PLoS ONE 6: e19456.
72. Khandhadia S, Cipriani V, Yates JRW, Lotery AJ, (2012) Age-related macular degeneration and the complement system. Immunobiology 217: 127-146.