Proteome Changes Associated with the VEGFR Pathway and Immune System in Diabetic Macular Edema Patients at Different Diabetic Retinopathy Stages

References

• Ford J, Lois N, Royle P, Clar C, Shyangdan D, Waugh N. Current treatments in diabetic macular oedema: systematic review and meta-analysis. BMJ Open. 2013;3(3):e002269. doi:10.1136/bmjopen-2012-002269.
   PubMed Web of Science ®Google Scholar
• Tan G, Cheung N, Simó R, Cheung G, Wong T. Diabetic macular oedema. Lancet Diabetes Endocrinol. 2017;5(2):143–155. doi:10.1016/S2213-8587(16)30052-3.
   PubMed Web of Science ®Google Scholar
• Daruich A, Matet A, Moulin A, Kowalczuk L, Nicolas M, Sellam A, Rothschild P, Omri S, Gélizé E, Jonet L, et al. Mechanisms of macular edema: Beyond the surface. Prog Retin Eye Res. 2018;63:20–68. doi:10.1016/j.preteyeres.2017.10.006.
   PubMed Web of Science ®Google Scholar
• Zur D, Iglicki M, Busch C, Invernizzi A, Mariussi M, Loewenstein A, Busch C, Cebeci Z, Chhablani JK, Chaikitmongkol V, et al. OCT Biomarkers as Functional Outcome Predictors in Diabetic Macular Edema Treated with Dexamethasone Implant. Ophthalmology. 2018;125(2):267–275. doi:10.1016/j.ophtha.2017.08.031.
   PubMed Web of Science ®Google Scholar
• Zur D, Iglicki M, Sala-Puigdollers A, Chhablani J, Lupidi M, Fraser-Bell S, Mendes T, Chaikitmongkol V, Cebeci Z, Dollberg D, the International Retina Group (IRG), et al. Disorganization of retinal inner layers as a biomarker in patients with diabetic macular oedema treated with dexamethasone implant. Acta Ophthalmol. 2020;98(2):e217–e23. doi:10.1111/aos.14230.
   PubMed Web of Science ®Google Scholar
• Iglicki M, Loewenstein A, Barak A, Schwartz S, Zur D. Outer retinal hyperreflective deposits (ORYD): a new OCT feature in naïve diabetic macular oedema after PPV with ILM peeling. Br J Ophthalmol. 2020;104(5):666–671. doi:10.1136/bjophthalmol-2019-314523.
   PubMed Web of Science ®Google Scholar
• Iglicki M, Busch C, Loewenstein A, Fung A, Invernizzi A, Mariussi M, Arias R, Gabrielle P, Cebeci Z, Okada M, et al. UNDERDIAGNOSED OPTIC DISK PIT MACULOPATHY: Spectral Domain Optical Coherence Tomography Features For Accurate Diagnosis. Retina (Philadelphia, Pa). 2019;39(11):2161–2166. doi:10.1097/IAE.0000000000002270.
   PubMed Web of Science ®Google Scholar
• Cehofski LJ, Honore B, Vorum H. A review: proteomics in retinal artery occlusion, retinal vein occlusion, diabetic retinopathy and acquired macular disorders. Int J Mol Sci. 2017;18(5):907.
   PubMed Web of Science ®Google Scholar
• Gao BB, Chen X, Timothy N, Aiello LP, Feener EP. Characterization of the vitreous proteome in diabetes without diabetic retinopathy and diabetes with proliferative diabetic retinopathy. J Proteome Res. 2008;7(6):2516–2525. doi:10.1021/pr800112g.
   PubMed Web of Science ®Google Scholar
• Kim T, Kim SJ, Kim K, Kang UB, Lee C, Park KS, Yu HG, Kim Y. Profiling of vitreous proteomes from proliferative diabetic retinopathy and nondiabetic patients. Proteomics. 2007;7(22):4203–4215. doi:10.1002/pmic.200700745.
   PubMed Web of Science ®Google Scholar
• Li J, Lu Q, Lu P. Quantitative proteomics analysis of vitreous body from type 2 diabetic patients with proliferative diabetic retinopathy. BMC Ophthalmol. 2018;18(1):151. doi:10.1186/s12886-018-0821-3.
   PubMed Web of Science ®Google Scholar
• Loukovaara S, Nurkkala H, Tamene F, Gucciardo E, Liu X, Repo P, Lehti K, Varjosalo M. Quantitative Proteomics Analysis of Vitreous Humor from Diabetic Retinopathy Patients. J Proteome Res. 2015;14(12):5131–5143. doi:10.1021/acs.jproteome.5b00900.
   PubMed Web of Science ®Google Scholar
• Wang H, Feng L, Hu JW, Xie CL, Wang F. Differentiating vitreous proteomes in proliferative diabetic retinopathy using high-performance liquid chromatography coupled to tandem mass spectrometry. Exp Eye Res. 2013;108:110–119. doi:10.1016/j.exer.2012.11.023.
   PubMed Web of Science ®Google Scholar
• Wei Q, Zhang T, Jiang R, Chang Q, Zhang Y, Huang X, Gao X, Jin H, Xu G. Vitreous Fibronectin and Fibrinogen Expression Increased in Eyes With Proliferative Diabetic Retinopathy After Intravitreal Anti-VEGF Therapy. Invest Ophthalmol Vis Sci. 2017;58(13):5783–5791. doi:10.1167/iovs.17-22345.
   PubMed Web of Science ®Google Scholar
• Shitama T, Hayashi H, Noge S, Uchio E, Oshima K, Haniu H, Takemori N, Komori N, Matsumoto H. Proteome Profiling of Vitreoretinal Diseases by Cluster Analysis. Proteomics Clin Appl. 2008;2(9):1265–1280. doi:10.1002/prca.200800017.
   PubMed Web of Science ®Google Scholar
• Chiang S, Tsai M, Wang C, Chen A, Chou Y, Hsia C, Wu Y, Chen H, Huang T, Chen P, et al. Proteomic analysis and identification of aqueous humor proteins with a pathophysiological role in diabetic retinopathy. J Proteomics. 2012;75(10):2950–2959. doi:10.1016/j.jprot.2011.12.006.
   PubMed Web of Science ®Google Scholar
• Wang H, Feng L, Hu J, Xie C, Wang F. Characterisation of the vitreous proteome in proliferative diabetic retinopathy. Proteome Sci. 2012;10(1):15. doi:10.1186/1477-5956-10-15.
   PubMedGoogle Scholar
• Kita T, Clermont A, Murugesan N, Zhou Q, Fujisawa K, Ishibashi T, Aiello L, Feener E. Plasma Kallikrein-Kinin System as a VEGF-Independent Mediator of Diabetic Macular Edema. Diabetes. 2015;64(10):3588–3599. doi:10.2337/db15-0317.
   PubMed Web of Science ®Google Scholar
• Gillet L, Navarro P, Tate S, Röst H, Selevsek N, Reiter L, Bonner R, Aebersold R. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics. 2012;11(6):O111.016717. doi:10.1074/mcp.O111.016717.
   PubMed Web of Science ®Google Scholar
• Röst H, Rosenberger G, Navarro P, Gillet L, Miladinović S, Schubert O, Wolski W, Collins B, Malmström J, Malmström L, et al. OpenSWATH enables automated, targeted analysis of data-independent acquisition MS data. Nat Biotechnol. 2014;32(3):219–223. doi:10.1038/nbt.2841.
   PubMed Web of Science ®Google Scholar
• Egertson J, MacLean B, Johnson R, Xuan Y, MacCoss M. Multiplexed peptide analysis using data-independent acquisition and Skyline. Nat Protoc. 2015;10(6):887–903. doi:10.1038/nprot.2015.055.
   PubMed Web of Science ®Google Scholar
• Guo T, Kouvonen P, Koh C, Gillet L, Wolski W, Röst H, Rosenberger G, Collins B, Blum L, Gillessen S, et al. Rapid mass spectrometric conversion of tissue biopsy samples into permanent quantitative digital proteome maps. Nat Med. 2015;21(4):407–413. doi:10.1038/nm.3807.
   PubMed Web of Science ®Google Scholar
• Panozzo G, Cicinelli MV, Augustin AJ, Battaglia Parodi M, Cunha-Vaz J, Guarnaccia G, Kodjikian L, Jampol LM, Junemann A, Lanzetta P, et al. An optical coherence tomography-based grading of diabetic maculopathy proposed by an international expert panel: The European School for Advanced Studies in Ophthalmology classification. Eur J Ophthalmol. 2020;30(1):8–18. doi:10.1177/1120672119880394.
   PubMed Web of Science ®Google Scholar
• Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98:823–833.
   PubMed Web of Science ®Google Scholar
• Whelton PK, Carey RM, Aronow WS, Casey DE, Jr., Collins KJ, Dennison Himmelfarb C, DePalma SM, Gidding S, Jamerson KA, Jones DW, et al. 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for the Prevention, Detection, Evaluation, and Management of High Blood Pressure in Adults: Executive Summary: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. Hypertension. 2018;71(6):1269–1324. doi:10.1161/HYP.0000000000000066.
   PubMed Web of Science ®Google Scholar
• Kopin L, Lowenstein C. Dyslipidemia. Ann Intern Med. 2017;167(11):ITC81–ITC96. doi:10.7326/AITC201712050.
   PubMed Web of Science ®Google Scholar
• Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–362. doi:10.1038/nmeth.1322.
   PubMed Web of Science ®Google Scholar
• Feng J, Ding C, Qiu N, Ni X, Zhan D, Liu W, Xia X, Li P, Lu B, Zhao Q, et al. Firmiana: towards a one-stop proteomic cloud platform for data processing and analysis. Nat Biotechnol. 2017;35(5):409–412.,. doi:10.1038/nbt.3825.
   PubMed Web of Science ®Google Scholar
• Zhang CC, Chen Y, Mao XF, Huang Y, Jung SY, Jain A, Qin J, Wang Y. A Bioinformatic Algorithm for Analyzing Cell Signaling Using Temporal Proteomic Data. Proteomics. 2017;17(22):1600425. doi:10.1002/pmic.201600425.
   Web of Science ®Google Scholar
• Bayless K, Davis G. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci. 2002;115(Pt 6):1123–1136. doi:10.1242/jcs.115.6.1123.
   PubMed Web of Science ®Google Scholar
• Shen JH, Rossato FA, Cano I, Ng YSE. Novel engineered, membrane-tethered VEGF-A variants promote formation of filopodia, proliferation, survival, and cord or tube formation by endothelial cells via persistent VEGFR2/ERK signaling and activation of CDC42/ROCK pathways. Faseb J. 2021;35(12):e22036.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhuang XJ, Greene KS, Si H, Antonyak MA, Druso JE, Wilson KF, Cerione RA, Feng QY, Wang HY. Cdc42 functions as a regulatory node for tumour-derived microvesicle biogenesis. J Extracell Vesicles. 2021;10(3):e12051.
   PubMed Web of Science ®Google Scholar
• Corry J, Mott H, Owen D. Activation of STAT transcription factors by the Rho-family GTPases. Biochem Soc Trans. 2020;48(5):2213–2227. doi:10.1042/BST20200468.
   PubMed Web of Science ®Google Scholar
• Lopez-Luque J, Bertran E, Crosas-Molist E, Maiques O, Malfettone A, Caja L, Serrano T, Ramos E, Sanz-Moreno V, Fabregat I. Downregulation of Epidermal Growth Factor Receptor in hepatocellular carcinoma facilitates Transforming Growth Factor-β-induced epithelial to amoeboid transition. Cancer Lett. 2019;464:15–24. doi:10.1016/j.canlet.2019.08.011.
   PubMed Web of Science ®Google Scholar
• Samara WA, Shahlaee A, Adam MK, Khan A, Chiang A, Maguire JI, Hsu J, Ho AC. Quantification of Diabetic Macular Ischemia Using Optical Coherence Tomography Angiography and Its Relationship with Visual Acuity. Ophthalmology. 2017;124(2):235–244. doi:10.1016/j.ophtha.2016.10.008.
   PubMed Web of Science ®Google Scholar
• Murakami T, Frey T, Lin CM, Antonetti DA. Protein kinase cβ phosphorylates occludin regulating tight junction trafficking in vascular endothelial growth factor-induced permeability in vivo. Diabetes. 2012;61(6):1573–1583. doi:10.2337/db11-1367.
   PubMed Web of Science ®Google Scholar
• Nguyen QD, Brown DM, Marcus DM, Boyer DS, Patel S, Feiner L, Gibson A, Sy J, Rundle AC, Hopkins JJ, et al. Ranibizumab for diabetic macular edema: results from 2 phase III randomized trials: RISE and RIDE. Ophthalmology. 2012;119(4):789–801. doi:10.1016/j.ophtha.2011.12.039.
   PubMed Web of Science ®Google Scholar
• Elman MJ, Bressler NM, Qin H, Beck RW, Ferris FL, Friedman SM, Glassman AR, Scott IU, Stockdale CR, Sun JK, Diabetic Retinopathy Clinical Research Network Expanded 2-year follow-up of ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology. 2011;118(4):609–614. doi:10.1016/j.ophtha.2010.12.033.
   PubMed Web of Science ®Google Scholar
• Gonzalez VH, Campbell J, Holekamp NM, Kiss S, Loewenstein A, Augustin AJ, Ma J, Ho AC, Patel V, Whitcup SM, et al. Early and Long-Term Responses to Anti-Vascular Endothelial Growth Factor Therapy in Diabetic Macular Edema: Analysis of Protocol I Data. Am J Ophthalmol. 2016;172:72–79. doi:10.1016/j.ajo.2016.09.012.
   PubMed Web of Science ®Google Scholar
• Sun JK, Glassman AR, Beaulieu WT, Stockdale CR, Bressler NM, Flaxel C, Gross JG, Shami M, Jampol LM, Res DRC. Rationale and application of the protocol S anti-vascular endothelial growth factor algorithm for proliferative diabetic retinopathy. Ophthalmology. 2019;126(1):87–95. doi:10.1016/j.ophtha.2018.08.001.
   PubMed Web of Science ®Google Scholar
• Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331(22):1480–1487. doi:10.1056/NEJM199412013312203.
   PubMed Web of Science ®Google Scholar
• Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158(1):147–152. doi:10.1016/S0002-9440(10)63952-1.
   PubMed Web of Science ®Google Scholar
• Zur D, Iglicki M, Loewenstein A. The Role of Steroids in the Management of Diabetic Macular Edema. Ophthalmic Res. 2019;62(4):231–236. doi:10.1159/000499540.
   PubMed Web of Science ®Google Scholar
• Mello P, Andrade G, Maia A, Maia M, Neto LB, Neto AM, Brasil OM, Minelli E, Dalloul C, Iglicki M. Effectiveness and Safety of Intravitreal Dexamethasone Implant (Ozurdex) in Patients with Diabetic Macular Edema: A Real-World Experience. Ophthalmologica. 2019;241(1):9–16. doi:10.1159/000492132.
   PubMed Web of Science ®Google Scholar
• Iglicki M, Busch C, Zur D, Okada M, Mariussi M, Chhablani JK, Cebeci Z, Fraser-Bell S, Chaikitmongkol V, Couturier A, et al. DEXAMETHASONE IMPLANT FOR DIABETIC MACULAR EDEMA IN NAIVE COMPARED WITH REFRACTORY EYES: The International Retina Group Real-Life 24-Month Multicenter Study. The IRGREL-DEX Study. Retina. 2019;39(1):44–51. doi:10.1097/IAE.0000000000002196.
   PubMed Web of Science ®Google Scholar
• Iglicki M, Zur D, Busch C, Okada M, Loewenstein A. Progression of diabetic retinopathy severity after treatment with dexamethasone implant: a 24-month cohort study the 'DR-Pro-DEX Study. Acta Diabetol. 2018;55(6):541–547. doi:10.1007/s00592-018-1117-z.
   PubMed Web of Science ®Google Scholar
• Cehofski L, Kojima K, Terao N, Kitazawa K, Thineshkumar S, Grauslund J, Vorum H, Honoré B. Aqueous Fibronectin Correlates With Severity of Macular Edema and Visual Acuity in Patients With Branch Retinal Vein Occlusion: A Proteome Study. Invest Ophthalmol Vis Sci. 2020;61(14):6. doi:10.1167/iovs.61.14.6.
   PubMed Web of Science ®Google Scholar
• Cunha-Vaz J, Ribeiro L, Lobo C. Phenotypes and biomarkers of diabetic retinopathy. Prog Retin Eye Res. 2014;41:90–111. doi:10.1016/j.preteyeres.2014.03.003.
   PubMed Web of Science ®Google Scholar
• Iglicki M, Lavaque A, Ozimek M, Negri H, Okada M, Chhablani J, Busch C, Loewenstein A, Zur D. Biomarkers and predictors for functional and anatomic outcomes for small gauge pars plana vitrectomy and peeling of the internal limiting membrane in naïve diabetic macular edema: The VITAL Study. PloS One. 2018;13(7):e0200365. doi:10.1371/journal.pone.0200365.
   PubMed Web of Science ®Google Scholar
• Hu Y, Liu F, Shen J, Zeng H, Li L, Zhao J, Zhao J, Lu F, Jia W. Association between serum cystatin C and diabetic peripheral neuropathy: a cross-sectional study of a Chinese type 2 diabetic population. Eur J Endocrinol. 2014;171(5):641–648. doi:10.1530/EJE-14-0381.
   PubMed Web of Science ®Google Scholar
• Kumar Vr S, Darisipudi M, Steiger S, Devarapu S, Tato M, Kukarni O, Mulay S, Thomasova D, Popper B, Demleitner J, et al. Cathepsin S Cleavage of Protease-Activated Receptor-2 on Endothelial Cells Promotes Microvascular Diabetes Complications. J Am Soc Nephrol. 2016;27(6):1635–1649. doi:10.1681/ASN.2015020208.
   PubMed Web of Science ®Google Scholar
• Spaide R, Klancnik J, Cooney M. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1):45–50. doi:10.1001/jamaophthalmol.2014.3616.
   PubMed Web of Science ®Google Scholar