Interleukin-18 has antipermeablity and antiangiogenic activities in the eye: Reciprocal suppression with VEGF

Journal of Cellular Physiology

Volumn 229, Issue 8, 2014, Pages 974-983

  Shen, Jikui ^a   Choy, David F ^b   Yoshida, Tsunehiko ^a   Iwase, Takeshi ^a   Hafiz, Gulnar ^c   Xie, Bing ^a   Hackett, Sean F ^a   Arron, Joseph R ^b   Campochiaro, Peter A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GENENTECH INC   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RANIBIZUMAB; THROMBOSPONDIN 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; AQUEOUS HUMOR; ARTICLE; BLOOD VESSEL PERMEABILITY; BONE MARROW CELL; BRANCH RETINAL VEIN OCCLUSION; CENTRAL RETINA VEIN OCCLUSION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DIABETIC RETINOPATHY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIRETINAL MEMBRANE; EYE; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; RETINA MACULA AGE RELATED DEGENERATION; RETINA MACULA EDEMA; RETINA MACULA HOLE; RETINA NEOVASCULARIZATION; RETINA VEIN OCCLUSION; RETINOPATHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBRETINAL NEOVASCULARIZATION; TIGHT JUNCTION; TRANSIENT TRANSFECTION; TREATMENT DURATION; VISUAL ACUITY;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CLAUDIN-5; CYTOKINES; EYE; GENE EXPRESSION REGULATION; INTERLEUKIN-18; MICE; NEOVASCULARIZATION, PATHOLOGIC; PERMEABILITY; RETINAL VESSELS; TIGHT JUNCTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84899095041     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24575     Document Type: Article

References (47)

1. Amin MA, Mansfield PJ, Pakozdi A, Campbell PL, Ahmed S, Martinez RJ, Koch AE. 2007. Interleukin-18 induces angiogenic factors in rheumatoid arthritis synovial tissue fibroblasts via distinct signaling pathways. Arthritis Rheum 56:1787-1797.
2. Argaw AT, Gurfein BT, Zhang Y, Zameer A, Gareth JR. 2008. VEGF-mediated disruption of endothelial CLN-5 promotes bloodbrain barrier breakdown. Proc Natl Acad Sci USA 106:1977-1982.
3. Aslam M, Ahmad N, Srivastava R, Hemmer B. 2011. TNF-alpha induced NFkappaB signaling and p65 (RelA) overexpression repress Cldn5 promoter in mouse brain endothelial cells. Cytokine 57:269-275.
4. Boraschi D, Dinarello CA. 2006. IL-18 in autoimmunity: A review. Eur Cytokine Netw 17:224-252.
5. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, Kim RY, Sy JP, Schneider S, Anchor Study Group. 2006. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355:1432-1444.
6. Brown DM, Campochiaro PA, Singh RP, Gray S, Rundle AC, Li Z, Rubio RG, Murahashi WY, Group CS. 2010. Efficacy and safety of ranibizumab in the treatment of macular edema secondary to central retinal vein occlusion: 6-month results of the phase III CRUISE study. Ophthalmology 117:1124-1133.
7. Brown DM, Campochiaro PA, Bhisitkul RB, Ho AC, Gray S, Saroj N, Adamis AP, Rubio RG, Murahashi WY. 2011. Sustained benefits from ranibizumab for macular edema following branch retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology 118:1594-1602.
8. Campbell M, Nguyen AT, Kiang AS, Tam LC, Goobo OL, Kerskens C, Ni Dhubhghaill S, Humphries MM, Farrar GJ, Kenna PF, Humphries P. 2009. An experimental platform for sytemic drug delivery to the retina. Proc Natl Acad Sci USA 106:17817-17822.
9. Campochiaro PA, Hafiz G, Shah SM, Nguyen QD, Ying H, Do DV, Quinlan E, Zimmer-Galler I, Haller JA, Solomon S, Sung JU, Hadi Y, Janjua KA, Choy DF, Arron JR. 2008. Ranibizumab for macular edema due to retinal vein occlusions; implication of VEGF as a critical stimulator. Mol Ther 16:791-799.
10. Campochiaro PA, Choy DF, Do DV, Hafiz G, Shah SM, Nguyen QD, Rubio R, Arron JR. 2009. Monitoring ocular drug therapy by analysis of aqueous samples. Ophthalmology 116:2158-2164.
11. Campochiaro PA, Hafiz G, Channa R, Shah SM, Nguyen QD, Ying H, Do DV, Zimmer-Galler I, Solomon SD, Sung JU, Syed B. 2010a. Antagonism of vascular endothelial growth factor for macular edema caused by retinal vein occlusion: Two-year outcomes. Ophthalmology 117:2387-2394.
12. Campochiaro PA, Heier JS, Feiner L, Gray S, Saroj N, Rundle AC, Murahashi WY, Rubio RG, Group BS. 2010b. Ranibizumab for macular edema following branch retinal vein occlusion: 6-month primary endpoint results of a phase III study. Ophthalmology 117:1102-1112.
13. Campochiaro PA, Brown DM, Awh CC, Lee Y, Gray S, Saroj N, Murahashi WY, Rubio RG. 2011. Sustained benefits from ranibizumab for macular edema following central retinal vein occlusion: 12-month outcomes of a phase III study. Ophthalmology 118:2041-2049.
14. Cao R, Farnebo J, Kurimoto M, Cao Y. 1999. Interleukin-18 acts as an angiogenesis and tumor suppressor. FASEB J 13:2196-2202.
15. Cho ML, Jung YO, Moon YM, Min SY, Yoon CH, Lee SH, Park SH, Cho CS, Jue DM, Kim HY. 2006. Interleukin-18 induces the production of vascular endothelial growth factor (VEGF) in rheumatoid arthritis synovial fibroblasts via AP-1-dependent pathways. Immunol Lett 103:159-166.
16. Coughlin CM, Salhany KE, Wysocka M, Aruga E, Kurzawa H, Chang AE, Hunter CA, Fox JC, Trinchieri G, Lee WM. 1998. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J Clin Invest 101:1441-1452.
17. Doyle SL, Campbell M, Ozaki E, Salomon RG, More A, Kenna PF, Farrar GJ, Klang A-S, Humphries MM, Lavelle EC, O'Neill LA, Hollyfield JG, Humphries P. 2012. NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components. Nat Med 18:792-799.
18. Dunn KC, Aotaki-Keen AE, Putkey FR, Hjelmeland LM. 1996. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp Eye Res 62:155-169.
19. Ferrara N, Damico L, Shams N, Lowman H, Kim R. 2006. Development of ranibizumab, an anti-vascular endothelial growth factor antigen binding fragment, as therapy for neovascular age-related macular degeneration. Retina 26:859-870.
20. Hothorn T, Hornik K, van de Wiel MA, Zeileis A. 2008. Implementing a class of permutation tests: The coin package. J Stat Softw 28:1-23.
21. Jung HK, Ryu HJ, Kim M-J, Won IK, Choi HK, Choi H-C, Song H-K, Jo S-M, Kang T-C. 2012. Interleukin-18 attenuates disruption of the bloodbrain barrier induced by status epilepticus within the rat piriform cortex in interferon-gamma independent pathway. Brain Res 1447:126-134.
22. Kim B, Lee S, Suvas S, Rouse BT. 2005. Application of plasmid DNA encoding IL-18 diminishes development of herpetic stromal keratitis by antiangiogenic effects. J Immunol 175:509-516.
23. Kim J, Kim C, Kim TS, Sa IB, Yang Y, Park H, Cho D. 2006. IL-18 enhances thrombospondin-1 production in human gastric cancer via JNK pathway. Biochem Biophys Res Commun 344:1284-1289.
24. Kwak N, Okamoto N, Wood JM, Campochiaro PA. 2000. VEGF is an important stimulator in a model of choroidal neovascularization. Invest Ophthalmol Vis Sci 41:3158-3164.
25. Lima e Silva R, Shen J, Hackett SF, Kachi S, Akiyama H, Kiuchi K, Yokoi K, Hatara C, McLauer T, Aslam S, Gong YY, Xiao WH, Khu NH, Thut C, Campochiaro P. 2007. The SDF-1/CXCR4 ligand/receptor pair is an important contributor to several types of ocular neovascularization. FASEB J 21:3219-3230.
26. Mimura K, Kono K, Takahashi A, Kawaguchi Y, Fujii H. 2007. Vascular endothelial growth factor inhibits the function of human mature dendritic cells mediated by VEGF receptor-2. Cancer Immunol Immunother 56:761-770.
27. Mori K, Ando A, Gehlbach P, Nesbitt D, Takahashi K, Goldsteen D, Penn M, Chen CT, Melia M, Phipps S, Moffat D, Brazzell K, Liau G, Dixon KH, Campochiaro PA. 2001a. Inhibition of choroidal neovascularization by intravenous injection of adenoviral vectors expressing secretable endostatin. Am J Pathol 159:313-320.
28. Mori K, Duh E, Gehlbach P, Ando A, Takahashi K, Pearlman J, Mori K, Yang HS, Zack DJ, Ettyreddy D, Brough DE, Wei LL, Campochiaro PA. 2001b. Pigment epithelium-derived factor inhibits retinal and choroidal neovascularization. J Cell Physiol 188:253-263.
29. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S. 2003. Size-selective loosening of the bloodbrain barrier in claudin-5 deficient mice. J Cell Biol 161:653-660.
30. Okamoto N, Tobe T, Hackett SF, Ozaki H, Vinores MA, LaRochelle W, Zack DJ, Campochiaro PA. 1997. Transgenic mice with increased expression of vascular endothelial growth factor in the retina: A new model of intraretinal and subretinal neovascularization. Am J Pathol 151:281-291.
31. Okamoto A, Iwamoto Y, Maru Y. 2006. Oxidative stress-responsive transcription factor ATF3 potentially mediates diabetic angiopathy. Mol Cell Biol 26:108710-108797.
32. Park CC, Morel JC, Amin MA, Connors MA, Harlow LA, Koch AE. 2001. Evidence of IL-18 as a novel angiogenic mediator. J Immunol 167:1644-1653.
33. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LEH. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci USA 92:905-909.
34. Qiao H, Sonoda KH, Sassa Y, Hisatomi T, Yoshikawa H, Ikeda Y, Murata T, Akira S, Ishibashi T. 2004. Abnormal retinal vascular development in IL-18 knockout mice. Lab Invest 84:973-980.
35. Qiao H, Sonoda KH, Ikeda Y, Yoshimura T, Hijioka K, Jo YJ, Sassa Y, Tsutsumi-Miyahara C, Hata Y, Akira S, Ishibashi T. 2007. Interleuikin-18 regulates pathological intraocular neovascularization. J Leukoc Biol 81:1012-1021.
36. Rehak J, Rehak M. 2008. Branch retinal vein occlusion: Pathogenesis, visual prognosis, and treatment modalities. Curr Eye Res 33:111-131.
37. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, Chung CY, Kim RY, Marina Study Group. 2006. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355:1419-1431.
38. Saishin Y, Saishin Y, Takahashi K, Lima Silva R, Hylton D, Rudge J, Wiegand SJ, Campochiaro PA. 2003a. VEGF-TRAPR1R2 suppresses choroidal neovascularization and VEGF-induced breakdown of the blood-retinal barrier. J Cell Physiol 195:241-248.
39. Saishin Y, Saishin Y, Takahashi K, Melia M, Vinores SA, Campochiaro PA. 2003b. Inhibition of protein kinase C decreases prostaglandin-induced breakdown of the blood-retinal barrier. J Cell Physiol 195:210-219.
40. Shen J, Xie B, Dong A, Swaim M, Hackett SF, Campochiaro PA. 2007. In vivo immunostaining demonstrates macrophages associate with growing and regressing vessels. Invest Ophthalmol Vis Sci 48:4335-4341.
41. Takahashi A, Kono K, Ichihara F, Sugai H, Fujii H, Matsumoto Y. 2004. Vascular endothelial growth factor inhibits maturation of dendritic cells induced by lipopolysaccharide, but not proinflammatory cytokines. Canc Immunol Immunother 53:543-550.
42. Tobe T, Okamoto N, Vinores MA, Derevjanik NL, Vinores SA, Zack DJ, Campochiaro PA. 1998a. Evolution of neovascularization in mice with overexpression of vascular endothelial growth factor in photoreceptors. Invest Ophthalmol Vis Sci 39:180-188.
43. Tobe T, Ortega S, Luna JD, Ozaki H, Okamoto N, Derevjanik NL, Vinores SA, Basilico C, Campochiaro PA. 1998b. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am J Pathol 153:1641-1646.
44. Wang J, Wang X, Hussain S, Zheng Y, Sanjabi S, Ouaaz F, Beg AA. 2007. Distinct roles of different NF-kappa B subunits in regulating inflammatory and T cell stimulatory gene expression in dendritic cells. J Immunol 178:6776-6777.
45. Xie B, Shen J, Dong A, Swaim M, Hackett SF, Wyder L, Worpenberg S, Barbieri S, Campochiaro PA. 2008. An Adam15 amplification loop promotes vascular endothelial growth factor-induced ocular neovascularization. FASEB J 22:2775-2783.
46. Yannuzzi LA, Negrao S, Iida T, Carvalho C, Rodriguez-Coleman H, Slakter JS, Freund KB, Sorenson J, Orlock D, Borodoker N. 2001. Retinal angiomatous proliferation in age-related macular degeneration. Retina 21:416-434.
47. Yu L, Wu X, Cheng Z, Lee CV, LeCouter J, Campa C, Fuh G, Lowman H, Ferrara N. 2008. Interaction between bevacizumab and murine VEGF-A: A reassessment. Invest Ophthalmol Vis Sci 49:522-527.