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      The Exposure of Phosphatidylserine Influences Procoagulant Activity in Retinal Vein Occlusion by Microparticles, Blood Cells, and Endothelium

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          Abstract

          The pathogenesis of hypercoagulability in retinal vein occlusion (RVO) is largely unknown. Whether the exposure of phosphatidylserine (PS) and microparticle (MPs) release will affect procoagulant activity (PCA) in RVO needs to be investigated. Objectives. To evaluate PS expression, circulating MPs, and the corresponding PCA in RVO patients. Twenty-five RVO patients were compared with 25 controls. PS-positive cells were detected by flow cytometry. Cell-specific MPs were measured by lactadherin for PS and relevant CD antibody. We explored PCA with coagulation time, purified coagulation complex assays, and fibrin production assays. In RVO, MPs from platelets, erythrocytes, leukocyte, and endothelial cells were increased and the exposure of PS was elevated significantly when compared with controls. In addition, we showed that circulating MPs in RVO patients were mostly derived from platelets, representing about 60–70% of all MPs, followed by erythrocytes and leukocytes. Moreover, PS exposure, ECs, and MPs in RVO lead to shortened clotting time with upregulation of FXa and thrombin formation obviously. Importantly, ECs treated with RVO serum which bounded FVa and FXa explicitly suggested the damage of retinal vein endothelial cells. Furthermore, lactadherin can inhibit the combination between PS and coagulation factors by approximately 70% and then exert an anticoagulant effect. In summary, circulating MPs and exposed PS from different cells may contribute to the increased PCA in patients with RVO. Lactadherin can be used for PS detection and an anticoagulant agent.

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          Most cited references31

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          Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation.

          We determined the numbers, cellular origin and thrombin-generating properties of microparticles in healthy individuals (n = 15). Microparticles, isolated from fresh blood samples and identified by flow cytometry, originated from platelets [237 x 10(6)/L (median; range 116-565)], erythrocytes (28 x 10(6)/L; 13-46), granulocytes (46 x 10(6)/L; 16-94) and endothelial cells (64 x 10(6)/L; 16-136). They bound annexin V, indicating surface exposure of phosphatidylserine, and supported coagulation in vitro. Interestingly, coagulation occurred via tissue factor (TF)-independent pathways, because antibodies against TF or factor (F)VII were ineffective. In contrast, in our in vitro experiments coagulation was partially inhibited by antibodies against FXII (12%, p = 0.006), FXI (36%, p <0.001), FIX (28%, p <0.001) or FVIII (32%, p <0.001). Both the number of annexin V-positive microparticles present in plasma and the thrombin-generating capacity inversely correlated to the plasma concentrations of thrombin-antithrombin complex (r = -0.49, p = 0.072 and r = -0.77, p = 0.001, respectively), but did not correlate to prothrombin fragment F1+2 (r = -0.002, p = 0.99). The inverse correlations between the number of microparticles and their thrombin-forming capacity and the levels of thrombin-antithrombin complex in plasma may indicate that microparticles present in the circulation of healthy individuals have an anticoagulant function by promoting the generation of low amounts of thrombin that activate protein C. We conclude that microparticles in blood from healthy individuals support thrombin generation via TF- and FVII-independent pathways, and which may have an anticoagulant function.
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            Baseline and early natural history report. The Central Vein Occlusion Study.

            (1993)
            To evaluate panretinal photocoagulation for ischemic central vein occlusion and macular grid-pattern photocoagulation for macular edema with reduced visual acuity due to central vein occlusion and to further define the natural history of central vein occlusion. A multicenter randomized controlled clinical trial supported by the National Eye Institute, Bethesda, Md. A total of 728 eyes from 725 patients were entered into one or more of four study groups: perfused, nonperfused, indeterminate perfusion, and macular edema. Follow-up of study patients is still in progress and no results are available for the randomized groups (nonperfused and macular edema). Thirty-eight (83%) of 46 evaluable eyes in the indeterminate group eventually demonstrated at least 10 disc areas of nonperfusion (28 eyes) or developed iris and/or angle neovascularization before retinal status could be determined (10 eyes). Four-month follow-up information is available for 522 of the 547 eyes in the perfused group. Thirty of these 522 eyes demonstrated iris and/or angle neovascularization at or before the 4-month follow-up visit. An additional 51 eyes had developed evidence of at least 10 disc areas of nonperfusion by the time of the 4-month visit. These findings confirm the importance of frequent follow-up examinations, including undilated slit-lamp examination of the iris, and gonioscopy in the management of all patients with recent onset of central vein occlusion.
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              Association of inflammatory factors with macular edema in branch retinal vein occlusion.

              To evaluate the association between vitreous fluid levels of inflammatory factors and macular edema in patients with branch retinal vein occlusion (BRVO). In 39 patients with BRVO and macular edema and 21 individuals with idiopathic macular hole (MH) serving as controls, vitreous fluid samples were obtained during vitreoretinal surgery, and the levels of vascular endothelial growth factor (VEGF), soluble VEGF receptor 2 (sVEGFR-2), soluble intercellular adhesion molecule 1 (sICAM-1), interleukin 6 (IL-6), monocyte chemotactic protein 1 (MCP-1), pentraxin 3 (PTX3), and pigment epithelium-derived factor (PEDF) were measured by enzyme-linked immunosorbent assay. Macular edema was examined by optical coherence tomography. Vitreous fluid levels of sVEGFR-2, VEGF, sICAM-1, IL-6, MCP-1, and PTX3 were significantly higher in the patients with BRVO than in those with MH; however, the PEDF level was significantly lower in the BRVO group. Vitreous fluid levels of all 7 factors were significantly correlated with the retinal thickness at the central fovea. There were also significant correlations of sVEGFR-2 with sICAM-1, IL-6, MCP-1, and PTX3 but no correlation with VEGF. However, there were significant correlations of VEGF with sICAM-1, IL-6, MCP-1, and PEDF in the BRVO group. Vitreous fluid levels of sVEGFR-2, VEGF, sICAM-1, IL-6, MCP-1, PTX3, and PEDF are strongly correlated with retinal vascular permeability and the severity of macular edema in patients with BRVO. These findings may be useful for understanding macular edema and developing new treatments for BRVO.
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                Author and article information

                Contributors
                Journal
                Oxid Med Cell Longev
                Oxid Med Cell Longev
                OMCL
                Oxidative Medicine and Cellular Longevity
                Hindawi
                1942-0900
                1942-0994
                2018
                3 July 2018
                : 2018
                : 3658476
                Affiliations
                1Department of Ophthalmology, The First Affiliated Hospital, Harbin Medical University, Harbin, China
                2Health Ministry Key Laboratory of Cell Transplantation, Heilongjiang Institute of Hematology and Oncology, Department of Hematology, The First Affiliated Hospital, Harbin Medical University, Harbin, China
                3Department of Cardiology, The First Affiliated Hospital, Harbin Medical University, Harbin, China
                4Veterans Affairs Boston Healthcare System, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA
                Author notes

                Academic Editor: Vladimir Jakovljevic

                Author information
                http://orcid.org/0000-0003-3952-7216
                http://orcid.org/0000-0002-3466-9058
                http://orcid.org/0000-0003-2015-5053
                http://orcid.org/0000-0002-1755-6115
                Article
                10.1155/2018/3658476
                6051034
                00494ea7-5b7c-4aaa-8735-916edce1b522
                Copyright © 2018 Ying Su et al.

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 14 March 2018
                : 21 May 2018
                Funding
                Funded by: National Natural Science Foundation of China
                Award ID: 81100659
                Award ID: 81470633
                Funded by: Ministry of Education of the People's Republic of China
                Award ID: LC2013C33/H1204
                Award ID: 20092307120003
                Funded by: China Postdoctoral Science Foundation
                Award ID: 20080430137
                Award ID: 200902418
                Funded by: Harbin Medical University
                Award ID: 2018L002
                Categories
                Research Article

                Molecular medicine
                Molecular medicine

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