Increased expression of angiogenic and inflammatory proteins in the vitreous of patients with ischemic central retinal vein occlusion

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Ehlken, Christoph ^a   Grundel, Bastian ^a   Michels, Daniel ^a   Junker, Bernd ^a,b   Stahl, Andreas ^a   Schlunck, Günther ^a   Hansen, Lutz L ^a   Feltgen, Nicolas ^c   Martin, Gottfried ^a   Agostini, Hansjürgen T ^a   Pielen, Amelie ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ANGIOGENIC PROTEIN; BIOLOGICAL MARKER; GAMMA INTERFERON; GELATINASE B; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPROTEGERIN; PROTEIN ANGPT2; PROTEIN LEP; PROTEIN PPBP; SCATTER FACTOR; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 4; UNCLASSIFIED DRUG; VASCULOTROPIN A; TNFRSF11B PROTEIN, HUMAN;

AGED; ARTICLE; CENTRAL RETINA VEIN OCCLUSION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; PIGMENT EPITHELIUM; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; RADIAL OPTIC NEUROTOMY; RETINA MACULA HOLE; SECONDARY GLAUCOMA; SIGNAL TRANSDUCTION; VERY ELDERLY; VITREOUS BODY; IMMUNOLOGY; METABOLISM; RETINA VEIN OCCLUSION;

AGED; AGED, 80 AND OVER; CHEMOKINE CCL2; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 2; MALE; MATRIX METALLOPROTEINASE 10; OSTEOPROTEGERIN; RETINAL VEIN OCCLUSION; VITREOUS BODY;

EID: 84929319418     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126859     Document Type: Article

References (56)

1. Cugati S, Wang JJ, RochtChina E, Mitchell P. Ten-year incidence of retinal vein occlusion in an older population: the Blue Mountains Eye Study. Arch Ophthalmol. 2006; 124: 726-732. doi: 10.1001/archopht.124.5.726 PMID: 16682596
2. Rogers S, McIntosh RL, Cheung N, Lim L, Wang JJ, Mitchell P, et al. The prevalence of retinal vein occlusion: pooled data from population studies from the United States, Europe, Asia, and Australia. Ophthalmology. 2010; 117: 313-319.e1. doi: 10.1016/j.ophtha.2009.07.017 PMID: 20022117
3. Pielen A, Feltgen N, Isserstedt C, Callizo J, Junker B, Schmucker C. Efficacy and safety of intravitreal therapy in macular edema due to branch and central retinal vein occlusion: a systematic review. PloS One. 2013; 8: e78538. doi: 10.1371/journal.pone.0078538 PMID: 24205253
4. Campochiaro PA, Brown DM, Awh CC, Lee SY, Gray S, Saroj N, et al. Sustained benefits from ranibizumab for macular edema following central retinal vein occlusion: twelve-month outcomes of a phase III study. Ophthalmology. 2011; 118: 2041-2049. doi: 10.1016/j.ophtha.2011.02.038 PMID: 21715011
5. Brown DM, Heier JS, Clark WL, Boyer DS, Vitti R, Berliner AJ, et al. Intravitreal aflibercept injection for macular edema secondary to central retinal vein occlusion: 1-year results from the phase 3 COPERNICUS study. Am J Ophthalmol. 2013; 155: 429-437.e7. doi: 10.1016/j.ajo.2012.09.026 PMID: 23218699
6. Epstein DL, Algvere PV, von Wendt G, Seregard S, Kvanta A. Benefit from bevacizumab for macular edema in central retinal vein occlusion: twelve-month results of a prospective, randomized study. Ophthalmology. 2012; 119: 2587-2591. doi: 10.1016/j.ophtha.2012.06.037 PMID: 22902212
7. Stem MS, Talwar N, Comer GM, Stein JD. A longitudinal analysis of risk factors associated with central retinal vein occlusion. Ophthalmology. 2013; 120: 362-370. doi: 10.1016/j.ophtha.2012.07.080 PMID: 23177364
8. Prisco D, Marcucci R, Bertini L, Gori AM. Cardiovascular and thrombophilic risk factors for central retinal vein occlusion. Eur J Intern Med. 2002; 13: 163-169. PMID: 12020623
9. Mitchell P, Smith W, Chang A. Prevalence and associations of retinal vein occlusion in Australia. The Blue Mountains Eye Study. Arch Ophthalmol. 1996; 114: 1243-1247. PMID: 8859084
10. Zhou JQ, Xu L, Wang S, Wang YX, You QS, Tu Y, et al. The 10-year incidence and risk factors of retinal vein occlusion: the Beijing eye study. Ophthalmology. 2013; 120: 803-808. doi: 10.1016/j.ophtha.2012. 09.033 PMID: 23352194
11. Ehlken C, Rennel ES, Michels D, Grundel B, Pielen A, Junker B, et al. Levels of VEGF but not VEGF (165b) are increased in the vitreous of patients with retinal vein occlusion. Am J Ophthalmol. 2011; 152: 298-303.e1. doi: 10.1016/j.ajo.2011.01.040 PMID: 21621189
12. Yoshimura T, Sonoda K, Sugahara M, Mochizuki Y, Enaida H, Oshima Y, et al. Comprehensive analysis of inflammatory immune mediators in vitreoretinal diseases. PloS One. 2009; 4: e8158. doi: 10. 1371/journal.pone.0008158 PMID: 19997642
13. Suzuki Y, Nakazawa M, Suzuki K, Yamazaki H, Miyagawa Y. Expression profiles of cytokines and chemokines in vitreous fluid in diabetic retinopathy and central retinal vein occlusion. Jpn J Ophthalmol. 2011; 55: 256-263. doi: 10.1007/s10384-011-0004-8 PMID: 21538000
14. Noma H, Mimura T, Masahara H, Shimada K. Pentraxin 3 and other inflammatory factors in central retinal vein occlusion and macular edema. Retina Phila Pa. 2014; 34: 352-359. doi: 10.1097/IAE. 0b013e3182993d74 PMID: 23842103
15. Sodi A, Giambene B, Marcucci R, Sofi F, Fedi S, Abbate R, et al. Atherosclerotic and thrombophilic risk factors in patients with ischemic central retinal vein occlusion. Retina Phila Pa. 2011; 31: 724-729. doi: 10.1097/IAE.0b013e3181eef419 PMID: 21178660
16. Hasselbach HC, Ruefer F, Feltgen N, Schneider U, Bopp S, Hansen LL, et al. Treatment of central retinal vein occlusion by radial optic neurotomy in 107 cases. Graefes Arch Clin Exp Ophthalmol Albrecht Von Graefes Arch Für Klin Exp Ophthalmol. 2007; 245: 1145-1156. doi: 10.1007/s00417-006-0501-5
17. Hayreh SS. Ocular vascular occlusive disorders: natural history of visual outcome. Prog Retin Eye Res. 2014; 41: 1-25. doi: 10.1016/j.preteyeres.2014.04.001 PMID: 24769221
18. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. BioTechniques. 2003; 34: 374-378. PMID: 12613259
19. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72: 248-254. PMID: 942051
20. Koss MJ, Pfister M, Rothweiler F, Michaelis M, Cinatl J, Schubert R, et al. Comparison of cytokine levels from undiluted vitreous of untreated patients with retinal vein occlusion. Acta Ophthalmol (Copenh). 2012; 90: e98-e103. doi: 10.1111/j.1755-3768.2011.02292.x PMID: 22066978
21. Noma H, Funatsu H, Mimura T, Eguchi S. Vitreous inflammatory factors and serous retinal detachment in central retinal vein occlusion: a case control series. J Inflamm Lond Engl. 2011; 8: 38. doi: 10.1186/1476-9255-8-38 PMID: 22152024
22. Koss M, Pfister M, Rothweiler F, Rejdak R, Ribeiro R, Cinatl J, et al. Correlation from undiluted vitreous cytokines of untreated central retinal vein occlusion with spectral domain optical coherence tomography. Open Ophthalmol J. 2013; 7: 11-17. doi: 10.2174/1874364101307010011 PMID: 23560031
23. Noma H, Funatsu H, Mimura T, Harino S, Hori S. Aqueous humor levels of vasoactive molecules correlate with vitreous levels and macular edema in central retinal vein occlusion. Eur J Ophthalmol. 2010; 20: 402-409. PMID: 19967679
24. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE Signal Transduct Knowl Environ. 2005; 2005: re12. doi: 10.1126/stke.3062005re12 PMID: 16234508
25. Mojsilovic-Petrovic J, Callaghan D, Cui H, Dean C, Stanimirovic DB, Zhang W. Hypoxia-inducible factor-1 (HIF-1) is involved in the regulation of hypoxia-stimulated expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) and MCP-5 (Ccl12) in astrocytes. J Neuroinflammation. 2007; 4: 12. doi: 10.1186/1742-2094-4-12 PMID: 17474992
26. Natarajan R, Salloum FN, Fisher BJ, Kukreja RC, Fowler AA 3rd. Hypoxia inducible factor-1 upregulates adiponectin in diabetic mouse hearts and attenuates post-ischemic injury. J Cardiovasc Pharmacol. 2008; 51: 178-187. doi: 10.1097/FJC.0b013e31815f248d PMID: 18287886
27. Simon M-P, Tournaire R, Pouyssegur J. The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol. 2008; 217: 809-818. doi: 10.1002/jcp.21558 PMID: 18720385
28. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003; 3: 721-732. doi: 10.1038/nrc1187 PMID: 13130303
29. Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, Xavier RJ. An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1) -Target genes that form the core response to hypoxia. Nucleic Acids Res. 2009; 37: 4587-4602. doi: 10.1093/nar/gkp425 PMID: 19491311
30. Balasubramani A, Mukasa R, Hatton RD, Weaver CT. Regulation of the Ifng locus in the context of Tlineage specification and plasticity. Immunol Rev. 2010; 238: 216-232. doi: 10.1111/j.1600-065X.2010. 00961.x PMID: 20969595
31. Cummins EP, Taylor CT. Hypoxia-responsive transcription factors. Pflüg Arch Eur J Physiol. 2005; 450: 363-371. doi: 10.1007/s00424-005-1413-7
32. Boring L, Gosling J, Cleary M, Charo IF. Decreased lesion formation in CCR2-/-mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 1998; 394: 894-897. doi: 10.1038/29788 PMID: 9732872
33. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell. 1998; 2: 275-281. PMID: 9734366
34. Ghosh S, Basu M, Roy SS. ETS-1 protein regulates vascular endothelial growth factor-induced matrix metalloproteinase-9 and matrix metalloproteinase-13 expression in human ovarian carcinoma cell line SKOV-3. J Biol Chem. 2012; 287: 15001-15015. doi: 10.1074/jbc.M111.284034 PMID: 22270366
35. Hashiya N, Jo N, Aoki M, Matsumoto K, Nakamura T, Sato Y, et al. In vivo evidence of angiogenesis induced by transcription factor Ets-1: Ets-1 is located upstream of angiogenesis cascade. Circulation. 2004; 109: 3035-3041. doi: 10.1161/01.CIR.0000130643.41587.DB PMID: 15173033
36. Ishida S, Usui T, Yamashiro K, Kaji Y, Amano S, Ogura Y, et al. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J Exp Med. 2003; 198: 483-489. doi: 10.1084/jem.20022027 PMID: 12900522
37. Sato Y, Teruyama K, Nakano T, Oda N, Abe M, Tanaka K, et al. Role of transcription factors in angiogenesis: Ets-1 promotes angiogenesis as well as endothelial apoptosis. Ann N Y Acad Sci. 2001; 947: 117-123. PMID: 11795259
38. Paumelle R, Tulasne D, Kherrouche Z, Plaza S, Leroy C, Reveneau S, et al. Hepatocyte growth factor/scatter factor activates the ETS1 transcription factor by a RAS-RAF-MEK-ERK signaling pathway. Oncogene. 2002; 21: 2309-2319. doi: 10.1038/sj.onc.1205297 PMID: 11948414
39. Oikawa M, Abe M, Kurosawa H, Hida W, Shirato K, Sato Y. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem Biophys Res Commun. 2001; 289: 39-43. doi: 10.1006/bbrc.2001.5927 PMID: 11708773
40. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell. 2006; 126: 321-334. doi: 10.1016/j.cell.2006. 05.040 PMID: 16873063
41. Ha CH, Jhun BS, Kao H-Y, Jin Z-G. VEGF stimulates HDAC7 phosphorylation and cytoplasmic accumulation modulating matrix metalloproteinase expression and angiogenesis. Arterioscler Thromb Vasc Biol. 2008; 28: 1782-1788. doi: 10.1161/ATVBAHA.108.172528 PMID: 18617643
42. Cantón A, Burgos R, Hernández C, Mateo C, Segura RM, Mesa J, et al. Hepatocyte growth factor in vitreous and serum from patients with proliferative diabetic retinopathy. Br J Ophthalmol. 2000; 84: 732-735. PMID: 10873984
43. Cui JZ, Chiu A, Maberley D, Ma P, Samad A, Matsubara JA. Stage specificity of novel growth factor expression during development of proliferative vitreoretinopathy. Eye Lond Engl. 2007; 21: 200-208. doi: 10.1038/sj.eye.6702169
44. Sun W, Funakoshi H, Nakamura T. Differential expression of hepatocyte growth factor and its receptor, c-Met in the rat retina during development. Brain Res. 1999; 851: 46-53. PMID: 10642827
45. Kinnunen K, Puustjärvi T, Teräsvirta M, Nurmenniemi P, Heikura T, Laidinen S, et al. Differences in retinal neovascular tissue and vitreous humour in patients with type 1 and type 2 diabetes. Br J Ophthalmol. 2009; 93: 1109-1115. doi: 10.1136/bjo.2008.148841 PMID: 19304585
46. Seitz R. Die Netzhautgefäße: vergleichende ophthalmoskopische und histologische Studien an gesunden und kranken Augen. Stuttgart: Enke; 1962.
47. Augoulea A, Vrachnis N, Lambrinoudaki I, Dafopoulos K, Iliodromiti Z, Daniilidis A, et al. Osteoprotegerin as a marker of atherosclerosis in diabetic patients. Int J Endocrinol. 2013; 2013: 182060. doi: 10. 1155/2013/182060 PMID: 23401681
48. Van Campenhout A, Golledge J. Osteoprotegerin, vascular calcification and atherosclerosis. Atherosclerosis. 2009; 204: 321-329. doi: 10.1016/j.atherosclerosis.2008.09.033 PMID: 19007931
49. Elias GJ, Ioannis M, Theodora P, Dimitrios PP, Despoina P, Kostantinos V, et al. Circulating tissue inhibitor of matrix metalloproteinase-4 (TIMP-4) in systemic sclerosis patients with elevated pulmonary arterial pressure. Mediators Inflamm. 2008; 2008: 164134. doi: 10.1155/2008/164134 PMID: 19190762
50. Radomski A, Jurasz P, Sanders EJ, Overall CM, Bigg HF, Edwards DR, et al. Identification, regulation and role of tissue inhibitor of metalloproteinases-4 (TIMP-4) in human platelets. Br J Pharmacol. 2002; 137: 1330-1338. doi: 10.1038/sj.bjp.0704936 PMID: 12466243
51. Santos-Martínez MJ, Medina C, Jurasz P, Radomski MW. Role of metalloproteinases in platelet function. Thromb Res. 2008; 121: 535-542. doi: 10.1016/j.thromres.2007.06.002 PMID: 17681591
52. Orbe J, Rodríguez JA, Calvayrac O, Rodríguez-Calvo R, Rodríguez C, Roncal C, et al. Matrix metalloproteinase-10 is upregulated by thrombin in endothelial cells and increased in patients with enhanced thrombin generation. Arterioscler Thromb Vasc Biol. 2009; 29: 2109-2116. doi: 10.1161/ATVBAHA. 109.194589 PMID: 19762781
53. Orbe J, Barrenetxe J, Rodriguez JA, Vivien D, Orset C, Parks WC, et al. Matrix metalloproteinase-10 effectively reduces infarct size in experimental stroke by enhancing fibrinolysis via a thrombin-Activatable fibrinolysis inhibitor-mediated mechanism. Circulation. 2011; 124: 2909-2919. doi: 10.1161/CIRCULATIONAHA.111.047100 PMID: 22104553
54. Brandt E, Petersen F, Ludwig A, Ehlert JE, Bock L, Flad HD. The beta-Thromboglobulins and platelet factor 4: blood platelet-derived CXC chemokines with divergent roles in early neutrophil regulation. J Leukoc Biol. 2000; 67: 471-478. PMID: 10770278
55. Kruidenier L, MacDonald TT, Collins JE, Pender SLF, Sanderson IR. Myofibroblast matrix metalloproteinases activate the neutrophil chemoattractant CXCL7 from intestinal epithelial cells. Gastroenterology. 2006; 130: 127-136. doi: 10.1053/j.gastro.2005.09.032 PMID: 16401476
56. Tan C, Liu Y, Li W, Deng F, Liu X, Wang X, et al. Associations of matrix metalloproteinase-9 and monocyte chemoattractant protein-1 concentrations with carotid atherosclerosis, based on measurements of plaque and intima-media thickness. Atherosclerosis. 2014; 232: 199-203. doi: 10.1016/j. atherosclerosis.2013.11.040 PMID: 24401238