Ranibizumab Alters Levels of Intraocular Soluble Cytokine Receptors in Patients with Diabetic Macular Edema

References

• Holekamp NM. Overview of diabetic macular edema. Am J Manag Care. 2016;22:s284–s291.
   PubMedGoogle Scholar
• Aiello LP; DCCT/EDIC Research Group. Diabetic retinopathy and other ocular findings in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study. Diabetes Care. 2014;37(1):17–23. doi:10.2337/dc13-2251.
   PubMed Web of Science ®Google Scholar
• Cunha-Vaz J, Faria de Abreu JR, Campos AJ. Early breakdown of the blood-retinal barrier in diabetes. Br J Ophthalmol. 1975;59(11):649–56. doi:10.1136/bjo.59.11.649.
   PubMed Web of Science ®Google Scholar
• Klaassen I, Van Noorden CJF, Schlingemann RO. Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions. Prog Retin Eye Res. 2013;34:19–48. doi:10.1016/j.preteyeres.2013.02.001.
   PubMed Web of Science ®Google Scholar
• Busik JV, Mohr S, Grant MB. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes. 2008;57(7):1952–65. doi:10.2337/db07-1520.
   PubMed Web of Science ®Google Scholar
• Muto T, Tien T, Kim D, Sarthy VP, Roy S. High glucose alters Cx43 expression and gap junction intercellular communication in retinal Müller cells: promotes Müller cell and pericyte apoptosis. Invest Ophthalmol Vis Sci. 2014;55(7):4327–37. doi:10.1167/iovs.14-14606.
   PubMed Web of Science ®Google Scholar
• Coughlin BA, Feenstra DJ, Mohr S. Müller cells and diabetic retinopathy. Vision Res. 2017;139:93–100. doi:10.1016/j.visres.2017.03.013.
   PubMed Web of Science ®Google Scholar
• Feenstra DJ, Yego EC, Mohr S. Modes of Retinal Cell Death in Diabetic Retinopathy. J Clin Exp Ophthalmol. 2013;4(5):298. doi:10.4172/2155-9570.1000298.
   PubMedGoogle Scholar
• Daruich A, Matet A, Moulin A, Kowalczuk L, Nicolas M, Sellam A, Rothschild P-R, 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
• Miller K, Fortun JA. Diabetic macular edema: current understanding, pharmacologic treatment options, and developing therapies. Asia Pac J Ophthalmol. 2018;7(1):28–35. doi:10.22608/APO.2017529.
   PubMed Web of Science ®Google Scholar
• Holmes DI, Zachary I. The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease. Genome Biol. 2005;6(2):209. doi:10.1186/gb-2005-6-2-209.
   PubMed Web of Science ®Google Scholar
• Gupta N. Diabetic retinopathy and VEGF. Open Ophthalmol J. 2013;7(1):4–10. doi:10.2174/1874364101307010004.
   PubMedGoogle Scholar
• Le Y-Z. VEGF production and signaling in Müller glia are critical to modulating vascular function and neuronal integrity in diabetic retinopathy and hypoxic retinal vascular diseases. Vision Res. 2017;139:108–14. doi:10.1016/j.visres.2017.05.005.
   PubMed Web of Science ®Google Scholar
• Antonetti DA, Barber AJ, Hollinger LA, Wolpert EB, Gardner TW. Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors. J Biol Chem. 1999;274(33):23463–67. doi:10.1074/jbc.274.33.23463.
   PubMed Web of Science ®Google Scholar
• Selim KM, Sahan D, Muhittin T, Osman C, Mustafa O. Increased levels of vascular endothelial growth factor in the aqueous humor of patients with diabetic retinopathy. I Indian J Ophthalmol. 2010;58(5):375–79. doi:10.4103/0301-4738.67042.
   PubMed Web of Science ®Google Scholar
• Shin ES, Sorenson CM, Sheibani N. Diabetes and Retinal Vascular Dysfunction. J Ophthalmic Vis Res. 2014;9(3):362–73. doi:10.4103/2008-322X.143378.
   PubMedGoogle Scholar
• Poulaki V, Qin W, Joussen AM, Hurlbut P, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP. Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor-1alpha and VEGF. J Clin Invest. 2002;109(6):805–15. doi:10.1172/JCI13776.
   PubMed Web of Science ®Google Scholar
• Wu H, Hwang D-K, Song X, Tao Y. Association between aqueous cytokines and diabetic retinopathy stage. J Ophthalmol. 2017. doi:10.1155/2017/9402198.
   Web of Science ®Google Scholar
• Demircan N, Safran BG, Soylu M, Ozcan AA, Sizmaz S. Determination of vitreous interleukin-1 (IL-1) and tumour necrosis factor (TNF) levels in proliferative diabetic retinopathy. Eye. 2006;20(12):1366–69. doi:10.1038/sj.eye.6702138.
   PubMed Web of Science ®Google Scholar
• Shi X, Semkova I, Müther PS, Dell S, Kociok N, Joussen AM. Inhibition of TNF-alpha reduces laser-induced choroidal neovascularization. Exp Eye Res. 2006;83(6):1325–34. doi:10.1016/j.exer.2006.07.007.
   PubMed Web of Science ®Google Scholar
• Yego ECK, Vincent JA, Sarthy V, Busik JV, Mohr S. Differential regulation of high glucose–induced glyceraldehyde-3-phosphate dehydrogenase nuclear accumulation in müller cells by IL-1β and IL-6. Invest Ophthalmol Vis Sci. 2009;50(4):1920–28. doi:10.1167/iovs.08-2082.
   PubMed Web of Science ®Google Scholar
• Vincent JA, Mohr S. Inhibition of caspase-1/interleukin-1beta signaling prevents degeneration of retinal capillaries in diabetes and galactosemia. Diabetes. 2007;56(1):224–30. doi:10.2337/db06-0427.
   PubMed Web of Science ®Google Scholar
• Aveleira CA, Lin C-M, Abcouwer SF, Ambrósio AF, Antonetti DA. TNF-α signals through PKCζ/NF-κB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes. 2010;59(11):2872–82. doi:10.2337/db09-1606.
   PubMed Web of Science ®Google Scholar
• Clark PR, Kim RK, Pober JS, Kluger MS. Tumor necrosis factor disrupts claudin-5 endothelial tight junction barriers in two distinct NF-κB-dependent phases. PLoS One. 2015;10(3):e0120075. doi:10.1371/journal.pone.0120075.
   PubMed Web of Science ®Google Scholar
• Valle ML, Dworshak J, Sharma A, Ibrahim AS, Al-Shabrawey M, Sharma S. Inhibition of interleukin-6 trans-signaling prevents inflammation and endothelial barrier disruption in retinal endothelial cells. Exp Eye Res. 2019;178:27–36. doi:10.1016/j.exer.2018.09.009.
   PubMed Web of Science ®Google Scholar
• Chen H, Zhang X, Liao N, Wen F. Increased levels of IL-6, sIL-6R, and sgp130 in the aqueous humor and serum of patients with diabetic retinopathy. Mol Vis. 2016;22:1005–14.
   PubMed Web of Science ®Google Scholar
• Mocan MC, Kadayifcilar S, Eldem B. Elevated intravitreal interleukin-6 levels in patients with proliferative diabetic retinopathy. Can J Ophthalmol. 2006;41(6):747–52. doi:10.3129/i06-070.
   PubMed Web of Science ®Google Scholar
• Shimura M, Yasuda K, Motohashi R, Kotake O, Noma H. Aqueous cytokine and growth factor levels indicate response to ranibizumab for diabetic macular oedema. Br J Ophthalmol. 2017;101(11):1518–23. doi:10.1136/bjophthalmol-2016-309953.
   PubMed Web of Science ®Google Scholar
• Shiraya T, Kato S, Araki F, Ueta T, Miyaji T, Yamaguchi T. Aqueous cytokine levels are associated with reduced macular thickness after intravitreal ranibizumab for diabetic macular edema. PLoS One. 2017;12(3):e0174340. doi:10.1371/journal.pone.0174340.
   PubMed Web of Science ®Google Scholar
• Forooghian F, Kertes PJ, Eng KT, Albiani DA, Kirker AW, Merkur AB, Fallah N, Cao S, Cui J, Or C, et al. Alterations in intraocular cytokine levels following intravitreal ranibizumab. Can J Ophthalmol. 2016;51(2):87–90. doi:10.1016/j.jcjo.2015.11.001.
   PubMed Web of Science ®Google Scholar
• Hillier RJ, Ojaimi E, Wong DT, Mak MYK, Berger AR, Kohly RP, Kertes PJ, Forooghian F, Boyd SR, Eng K, et al. Aqueous humor cytokine levels and anatomic response to intravitreal ranibizumab in diabetic macular edema. JAMA Ophthalmol. 2018;136(4):382–88. doi:10.1001/jamaophthalmol.2018.0179.
   PubMed Web of Science ®Google Scholar
• Wang X, Sawada T, Kakinoki M, Miyake T, Kawamura H, Saishin Y, Liu P, Ohji M. Aqueous vascular endothelial growth factor and ranibizumab concentrations after monthly and bimonthly intravitreal injections of ranibizumab for age-related macular degeneration. Graefe’s Arch Clin Exp Ophthalmol. 2014;252(7):1033–39. doi:10.1007/s00417-013-2505-2.
   PubMed Web of Science ®Google Scholar
• Sakamoto S, Takahashi H, Tan X, Inoue Y, Nomura Y, Arai Y, Fujino Y, Kawashima H, Yanagi Y. Changes in multiple cytokine concentrations in the aqueous humour of neovascular age-related macular degeneration after 2 months of ranibizumab therapy. Br J Ophthalmol. 2018;102(4):448–54. doi:10.1136/bjophthalmol-2017-310284.
   PubMed Web of Science ®Google Scholar
• Motohashi R, Noma H, Yasuda K, Kotake O, Goto H, Shimura M. Dynamics of soluble vascular endothelial growth factor receptors and their ligands in aqueous humour during ranibizumab for age-related macular degeneration. J Inflamm. 2018;15:26. doi:10.1186/s12950-018-0203-x.
   Google Scholar
• Shiraya T, Kato S, Araki F, Ueta T. Effect of intravitreal ranibizumab injection on aqueous humour cytokine levels in patients with diabetic macular oedema. Acta Ophthalmol. 2017;95(4):e340–e341. doi:10.1111/aos.13232.
   PubMed Web of Science ®Google Scholar
• Lim SW, Bandala-Sanchez E, Kolic M, Rogers SL, McAuley AK, Lim LL, Wickremasinghe SS. The influence of intravitreal ranibizumab on inflammation-associated cytokine concentrations in eyes with diabetic macular edema. Invest Opthalmol Vis Sci. 2018;59(13):5382. doi:10.1167/iovs.17-23325.
   PubMed Web of Science ®Google Scholar
• Mukaka M. A guide to appropriate use of Correlation coefficient in medical research. Malawi Med J. 2012;24:69–71.
   PubMed Web of Science ®Google Scholar
• Amrhein V, Greenland S, McShane B. Scientists rise up against statistical significance. Nature. 2019;567(7748):305. doi:10.1038/d41586-019-00857-9.
   PubMed Web of Science ®Google Scholar
• Chang-Lin J-E, Attar M, Acheampong AA, Robinson MR, Whitcup SM, Kuppermann BD, Welty D. Pharmacokinetics and pharmacodynamics of a sustained-release dexamethasone intravitreal implant. Invest Ophthalmol Vis Sci. 2011;52(1):80. doi:10.1167/iovs.10-5285.
   PubMed Web of Science ®Google Scholar
• Ogura Y, Kondo M, Kadonosono K, Shimura M, Kamei M, Tsujikawa A. Current practice in the management of branch retinal vein occlusion in Japan: survey results of retina specialists in Japan. Jpn J Ophthalmol. Aug 2019;19. doi:10.1007/s10384-019-00685-4.
   Web of Science ®Google Scholar
• Mohr S, Vincent J. Minocycline prevents caspase–1 activation, interleukin–1ß production, and the formation of acellular capillaries in the retina of diabetic mice. Invest Ophthalmol Vis Sci. 2005;46:4706–4706.
   Web of Science ®Google Scholar
• Mohr S. Potential new strategies to prevent the development of diabetic retinopathy. Expert Opin Investig Drugs. 2004;13(3):189–98. doi:10.1517/13543784.13.3.189.
   PubMed Web of Science ®Google Scholar
• Mohr S, Xi X, Tang J, Kern TS. Caspase activation in retinas of diabetic and galactosemic mice and diabetic patients. Diabetes. 2002;51(4):1172–79. doi:10.2337/diabetes.51.4.1172.
   PubMed Web of Science ®Google Scholar
• Rojas MA, Zhang W, Xu Z, Nguyen DT, Caldwell RW, Caldwell RB. Interleukin 6 has a critical role in diabetes-induced retinal vascular inflammation and permeability. Invest Ophthalmol Vis Sci. 2011;52:1003–1003.
   PubMedGoogle Scholar
• Funatsu H, Yamashita H, Noma H, Mimura T, Nakamura S, Sakata K, Hori S. Aqueous humor levels of cytokines are related to vitreous levels and progression of diabetic retinopathy in diabetic patients. Graefe’s Arch Clin Exp Ophthalmol. 2005;243:3–8. doi:10.1007/s00417-004-0950-7.
   PubMed Web of Science ®Google Scholar
• 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(3):256–63. doi:10.1007/s10384-011-0004-8.
   PubMed Web of Science ®Google Scholar
• Tsai T, Kuehn S, Tsiampalis N, Vu M-K, Kakkassery V, Stute G, Dick HB, Joachim SC. Anti-inflammatory cytokine and angiogenic factors levels in vitreous samples of diabetic retinopathy patients. PLoS One. 2018. doi:10.1371/journal.pone.0194603.
   Web of Science ®Google Scholar
• Chen H, Zhang X, Liao N, Wen F. Assessment of biomarkers using multiplex assays in aqueous humor of patients with diabetic retinopathy. BMC Ophthalmol. 2017;17(1). doi:10.1186/s12886-017-0572-6.
   Google Scholar
• Takeuchi M, Sato T, Sakurai Y, Taguchi M, Harimoto K, Karasawa Y, Ito M. Association between aqueous humor and vitreous fluid levels of Th17 cell-related cytokines in patients with proliferative diabetic retinopathy. PLoS One. 2017;12(5):e0178230. doi:10.1371/journal.pone.0178230.
   PubMed Web of Science ®Google Scholar
• Cheung CMG, Vania M, Ang M, Chee SP, Li J. Comparison of aqueous humor cytokine and chemokine levels in diabetic patients with and without retinopathy. Mol Vis. 2012;18:830.
   PubMed Web of Science ®Google Scholar
• Nagata K, Maruyama K, Yoneda K, Yoshimura T, Sonoda K, Kinoshita S. Cytokine levels in the vitreous fluid of patients with ocular sarcoidosis and patients with diabetic retinopathy. Invest Ophthalmol Vis Sci. 2012;53:6287–6287.
   Google Scholar
• Asrar AMAE, Maimone D, Morse PH, Gregory S, Reder AT. Cytokines in the vitreous of patients with proliferative diabetic retinopathy. Am J Ophthalmol. 1992;114(6):731–36. doi:10.1016/S0002-9394(14)74052-8.
   PubMed Web of Science ®Google Scholar
• Balaiya S, Grant MB, Priluck J, Chalam KV. Growth factors/chemokines in diabetic vitreous and aqueous alter the function of bone marrow-derived progenitor (CD34+) cells in humans. Am J Physiol - Endocrinol Metab. 2014;307(8):E695–E702. doi:10.1152/ajpendo.00253.2014.
   PubMed Web of Science ®Google Scholar
• Bromberg-White JL, Glazer L, Downer R, Furge K, Boguslawski E, Duesbery NS. Identification of VEGF-independent cytokines in proliferative diabetic retinopathy vitreous. Invest Ophthalmol Vis Sci. 2013;54(10):6472–80. doi:10.1167/iovs.13-12518.
   PubMed Web of Science ®Google Scholar
• Chernykh VV, Varvarinsky EV, Smirnov EV, Chernykh DV, Trunov AN. Proliferative and inflammatory factors in the vitreous of patients with proliferative diabetic retinopathy. Indian J Ophthalmol. 2015;63(1):33. doi:10.4103/0301-4738.151464.
   PubMed Web of Science ®Google Scholar
• Adachi Y, Aoki C, Yoshio-Hoshino N, Takayama K, Curiel DT, Nishimoto N. Interleukin-6 induces both cell growth and VEGF production in malignant mesotheliomas. Int J Cancer. 2006;119(6):1303–11. doi:10.1002/ijc.22006.
   PubMed Web of Science ®Google Scholar
• Catar R, Witowski J, Zhu N, Lücht C, Derrac Soria A, Uceda Fernandez J, Chen L, Jones SA, Fielding CA, Rudolf A, et al. IL-6 trans-signaling links inflammation with angiogenesis in the peritoneal membrane. J Am Soc Nephrol. 2017;28(4):1188–99. doi:10.1681/ASN.2015101169.
   PubMed Web of Science ®Google Scholar
• Weiss TW, Simak R, Kaun C, Rega G, Pflüger H, Maurer G, Huber K, Wojta J. Oncostatin M and IL-6 induce u-PA and VEGF in prostate cancer cells and correlate in vivo. Anticancer Res. 2011;31:3273–78.
   PubMed Web of Science ®Google Scholar
• Ebrahem Q, Minamoto A, Hoppe G, Anand-Apte B, Sears JE. Triamcinolone acetonide inhibits IL-6– and VEGF-Induced angiogenesis downstream of the IL-6 and VEGF receptors. Invest Opthalmol Vis Sci. 2006;47(11):4935. doi:10.1167/iovs.05-1651.
   PubMed Web of Science ®Google Scholar
• Tang J, Mohr S, Du Y-D, Kern TS. Non-uniform distribution of lesions and biochemical abnormalities within the retina of diabetic humans. Curr Eye Res. 2003;27(1):7–13. doi:10.1076/ceyr.27.2.7.15455.
   PubMed Web of Science ®Google Scholar
• Krady JK, Basu A, Allen CM, Xu Y, LaNoue KF, Gardner TW, Levison SW. Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes. 2005;54(5):1559–65. doi:10.2337/diabetes.54.5.1559.
   PubMed Web of Science ®Google Scholar
• Cukras CA, Petrou P, Chew EY, Meyerle CB, Wong WT. Oral minocycline for the treatment of diabetic macular edema (DME): results of a Phase I/II Clinical Study. Invest Ophthalmol Vis Sci. 2012;53(7):3865–74. doi:10.1167/iovs.11-9413.
   PubMed Web of Science ®Google Scholar
• Wang X, Zhao J, Qin L. VEGF-C mediated enhancement of lymphatic drainage reduces intestinal inflammation by regulating IL-9/IL-17 balance and improving gut microbiota in experimental chronic colitis. Am J Transl Res. 2017;9:4772–84.
   PubMed Web of Science ®Google Scholar
• Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H, Swartz M, Fukumura D, Jain RK, Alitalo K. Hyperplasia of Lymphatic Vessels in VEGF-C Transgenic Mice. Science. 1997;276(5317):1423–25. doi:10.1126/science.276.5317.1423.
   PubMed Web of Science ®Google Scholar
• Stacker SA, Achen MG. Emerging roles for VEGF-D in human disease. Biomolecules. 2018;8(1). doi:10.3390/biom8010001.
   PubMed Web of Science ®Google Scholar
• Koina ME, Baxter L, Adamson SJ, Arfuso F, Hu P, Madigan MC, Chan-Ling T. Evidence for lymphatics in the developing and adult human choroid. Investig Ophthalmol Vis Sci. 2015;56(2):1310–27. doi:10.1167/iovs.14-15705.
   PubMed Web of Science ®Google Scholar
• Zhao B, Smith G, Cai J, Ma A, Boulton M. Vascular endothelial growth factor C promotes survival of retinal vascular endothelial cells via vascular endothelial growth factor receptor-2. Br J Ophthalmol. 2007;91(4):538–45. doi:10.1136/bjo.2006.101543.
   PubMed Web of Science ®Google Scholar
• Kaidonis G, Burdon KP, Gillies MC, Abhary S, Essex RW, Chang JH, Pal B, Pefkianaki M, Daniell M, Lake S, et al. Common sequence variation in the VEGFC gene is associated with diabetic retinopathy and diabetic macular edema. Ophthalmology. 2015;122(9):1828–36. doi:10.1016/j.ophtha.2015.05.004.
   PubMed Web of Science ®Google Scholar
• Zhao B, Ma A, Cai J, Boulton M. VEGF-A regulates the expression of VEGF-C in human retinal pigment epithelial cells. Br J Ophthalmol. 2006;90(8):1052–59. doi:10.1136/bjo.2006.091215.
   PubMed Web of Science ®Google Scholar
• Kumar B, Chile SA, Ray KB, Vidyadhar Reddy GEC, Addepalli MK, Manoj Kumar AS, Ramana V, Rajagopal V. VEGF-C differentially regulates VEGF-A expression in ocular and cancer cells; promotes angiogenesis via RhoA mediated pathway. Angiogenesis. 2011;14:371–80. doi:10.1007/s10456-011-9221-5.
   PubMed Web of Science ®Google Scholar