Topographical and Morphological Differences of Corneal Dendritic Cells during Steady State and Inflammation

REFERENCES

• Labbe A, Liang Q, Wang Z, et al. Corneal nerve structure and function in patients with non-sjogren dry eye: clinical correlations. Invest Ophthalmol Vis Sci. 2013;54:5144–5150. doi:10.1167/iovs.13-12370.
   PubMed Web of Science ®Google Scholar
• Chinnery HR, Naranjo Golborne C, Downie LE. Omega-3 supplementation is neuroprotective to corneal nerves in dry eye disease: a pilot study. Ophthalmic Physiol Opt. 2017. doi:10.1111/opo.12365.
   PubMed Web of Science ®Google Scholar
• Steger B, Speicher L, Philipp W, Bechrakis NE. In vivo confocal microscopic characterisation of the cornea in chronic graft-versus-host disease related severe dry eye disease. Br J Ophthalmol. 2015;99:160–165. doi:10.1136/bjophthalmol-2014-305072.
   PubMed Web of Science ®Google Scholar
• Malik RA, Kallinikos P, Abbott CA, et al. Corneal confocal microscopy: a non-invasive surrogate of nerve fibre damage and repair in diabetic patients. Diabetologia. 2003;46:683–688. doi:10.1007/s00125-003-1086-8.
   PubMed Web of Science ®Google Scholar
• Tavakoli M, Quattrini C, Abbott C, et al. Corneal confocal microscopy: a novel noninvasive test to diagnose and stratify the severity of human diabetic neuropathy. Diabetes Care. 2010;33:1792–1797. doi:10.2337/dc10-0253.
   PubMed Web of Science ®Google Scholar
• Dehghani C, Pritchard N, Edwards K, Russell AW, Malik RA, Efron N. Fully automated, semiautomated, and manual morphometric analysis of corneal subbasal nerve plexus in individuals with and without diabetes. Cornea. 2014;33:696–702. doi:10.1097/ICO.0000000000000152.
   PubMed Web of Science ®Google Scholar
• Hamrah P, Sahin A, Dastjerdi MH, et al. Cellular changes of the corneal epithelium and stroma in herpes simplex keratitis: an in vivo confocal microscopy study. Ophthalmology. 2012;119:1791–1797. doi:10.1016/j.ophtha.2012.03.005.
   PubMed Web of Science ®Google Scholar
• Hillenaar T, van Cleynenbreugel H, Verjans GM, Wubbels RJ, Remeijer L. Monitoring the inflammatory process in herpetic stromal keratitis: the role of in vivo confocal microscopy. Ophthalmology. 2012;119:1102–1110. doi:10.1016/j.ophtha.2011.12.002.
   PubMed Web of Science ®Google Scholar
• Rosenberg ME, Tervo TM, Muller LJ, Moilanen JA, Vesaluoma MH. In vivo confocal microscopy after herpes keratitis. Cornea. 2002;21:265–269.
   PubMed Web of Science ®Google Scholar
• Mastropasqua L, Nubile M, Lanzini M, et al. Epithelial dendritic cell distribution in normal and inflamed human cornea: in vivo confocal microscopy study. Am J Ophthalmol. 2006;142:736–744. doi:10.1016/j.ajo.2006.06.057.
   PubMed Web of Science ®Google Scholar
• Zhivov A, Stave J, Vollmar B, Guthoff R. In vivo confocal microscopic evaluation of Langerhans cell density and distribution in the normal human corneal epithelium. Graefes Arch Clin Exp Ophthalmol. 2005;243:1056–1061. doi:10.1007/s00417-004-1075-8.
   PubMed Web of Science ®Google Scholar
• Yamagami S, Yokoo S, Usui T, Yamagami H, Amano S, Ebihara N. Distinct populations of dendritic cells in the normal human donor corneal epithelium. Invest Ophthalmol Vis Sci. 2005;46:4489–4494. doi:10.1167/iovs.05-0054.
   PubMed Web of Science ®Google Scholar
• Mayer WJ, Irschick UM, Moser P, et al. Characterization of antigen-presenting cells in fresh and cultured human corneas using novel dendritic cell markers. Invest Ophthalmol Vis Sci. 2007;48:4459–4467. doi:10.1167/iovs.06-1184.
   PubMed Web of Science ®Google Scholar
• Knickelbein JE, Watkins SC, McMenamin PG, Hendricks RL. Stratification of antigen-presenting cells within the normal cornea. Ophthalmol Eye Dis. 2009;1:45–54.
   PubMedGoogle Scholar
• Leppin K, Behrendt AK, Reichard M, et al. Diabetes mellitus leads to accumulation of dendritic cells and nerve fiber damage of the subbasal nerve plexus in the cornea. Invest Ophthalmol Vis Sci. 2014;55:3603–3615. doi:10.1167/iovs.14-14307.
   PubMed Web of Science ®Google Scholar
• Gao N, Yan C, Lee P, Sun H, Yu FS. Dendritic cell dysfunction and diabetic sensory neuropathy in the cornea. J Clin Invest. 2016;126:1998–2011. doi:10.1172/JCI85097.
   PubMed Web of Science ®Google Scholar
• Hamrah P, Zhang Q, Liu Y, Dana MR. Novel characterization of MHC class II-negative population of resident corneal Langerhans cell-type dendritic cells. Invest Ophthalmol Vis Sci. 2002;43:639–646.
   PubMed Web of Science ®Google Scholar
• Villani E, Magnani F, Viola F, et al. In vivo confocal evaluation of the ocular surface morpho-functional unit in dry eye. Optom Vis Sci. 2013;90:576–586. doi:10.1097/OPX.0b013e318294c184.
   PubMed Web of Science ®Google Scholar
• Kheirkhah A, Rahimi Darabad R, Cruzat A, et al. Corneal epithelial immune dendritic cell alterations in subtypes of dry eye disease: a pilot In Vivo confocal microscopic study. Invest Ophthalmol Vis Sci. 2015;56:7179–7185. doi:10.1167/iovs.15-17433.
   PubMed Web of Science ®Google Scholar
• Cruzat A, Witkin D, Baniasadi N, et al. Inflammation and the nervous system: the connection in the cornea in patients with infectious keratitis. Invest Ophthalmol Vis Sci. 2011;52:5136–5143. doi:10.1167/iovs.10-7048.
   PubMed Web of Science ®Google Scholar
• Cavalcanti BM, Cruzat A, Sahin A, Pavan-Langston D, Samayoa E, Hamrah P. In vivo confocal microscopy detects bilateral changes of corneal immune cells and nerves in unilateral herpes zoster ophthalmicus. Ocul Surf. 2018;16:101–111. doi:10.1016/j.jtos.2017.09.004.
   PubMed Web of Science ®Google Scholar
• Tavakoli M, Boulton AJ, Efron N, Malik RA. Increased Langerhan cell density and corneal nerve damage in diabetic patients: role of immune mechanisms in human diabetic neuropathy. Contact Lens Anterior Eye. 2011;34:7–11. doi:10.1016/j.clae.2010.08.007.
   PubMed Web of Science ®Google Scholar
• Lagali NS, Badian RA, Liu X, et al. Dendritic cell maturation in the corneal epithelium with onset of type 2 diabetes is associated with tumor necrosis factor receptor superfamily member 9. Sci Rep. 2018;8:14248. doi:10.1038/s41598-018-32410-5.
   PubMed Web of Science ®Google Scholar
• Chinnery HR, Leong CM, Chen W, Forrester JV, McMenamin PG. TLR9 and TLR7/8 activation induces formation of keratic precipitates and giant macrophages in the mouse cornea. J Leukoc Biol. 2015;97:103–110. doi:10.1189/jlb.3AB0414-216R.
   PubMed Web of Science ®Google Scholar
• Downie LE, Choi J, Lim JK, Chinnery HR. Longitudinal changes to tight junction expression and endothelial cell integrity in a mouse model of sterile corneal inflammation. Invest Ophthalmol Vis Sci. 2016;57:3477–3484. doi:10.1167/iovs.15-19005.
   PubMedGoogle Scholar
• Dando SJ, Naranjo Golborne C, Chinnery HR, Ruitenberg MJ, McMenamin PG. A case of mistaken identity: CD11c-eYFP cells in the normal mouse brain parenchyma and neural retina display the phenotype of microglia, not dendritic cells. Glia. 2016;64:1331–1349. doi:10.1002/glia.23005.
   PubMed Web of Science ®Google Scholar
• Downie LE, Stainer MJ, Chinnery HR. Monitoring of strain-dependent responsiveness to TLR activation in the mouse anterior segment using SD-OCT. Invest Ophthalmol Vis Sci. 2014;55:8189–8199. doi:10.1167/iovs.14-15595.
   PubMed Web of Science ®Google Scholar
• Lee EJ, Rosenbaum JT, Planck SR. Epifluorescence intravital microscopy of murine corneal dendritic cells. Invest Ophthalmol Vis Sci. 2010;51:2101–2108. doi:10.1167/iovs.08-2213.
   PubMed Web of Science ®Google Scholar
• Shetty R, Sethu S, Deshmukh R, et al. Corneal dendritic cell density Is associated with subbasal nerve plexus features, ocular surface disease index, and serum Vitamin D in evaporative dry eye disease. Biomed Res Int. 2016;2016:4369750. doi:10.1155/2016/4369750.
   PubMed Web of Science ®Google Scholar
• Mastropasqua R, Agnifili L, Fasanella V, et al. In Vivo distribution of corneal epithelial dendritic cells in patients with glaucoma. Invest Ophthalmol Vis Sci. 2016;57:5996–6002. doi:10.1167/iovs.16-20333.
   PubMed Web of Science ®Google Scholar
• Liu M, Gao H, Wang T, Wang S, Li S, Shi W. An essential role for dendritic cells in vernal keratoconjunctivitis: analysis by laser scanning confocal microscopy. Clin Exp Allergy. 2014;44:362–370. doi:10.1111/cea.12264.
   PubMed Web of Science ®Google Scholar
• Marsovszky L, Nemeth J, Resch MD, et al. Corneal Langerhans cell and dry eye examinations in ankylosing spondylitis. Innate Immun. 2014;20:471–477. doi:10.1177/1753425913498912.
   PubMed Web of Science ®Google Scholar
• Bitirgen G, Turkmen K, Malik RA, Ozkagnici A, Zengin N. Corneal confocal microscopy detects corneal nerve damage and increased dendritic cells in Fabry disease. Sci Rep. 2018;8:12244. doi:10.1038/s41598-018-30688-z.
   PubMed Web of Science ®Google Scholar
• Wu LQ, Cheng JW, Cai JP, et al. Observation of corneal Langerhans cells by In Vivo confocal microscopy in thyroid-associated ophthalmopathy. Curr Eye Res. 2016;41:927–932. doi:10.3109/02713683.2015.1133833.
   PubMed Web of Science ®Google Scholar
• Marsovszky L, Resch MD, Nemeth J, et al. In vivo confocal microscopic evaluation of corneal Langerhans cell density, and distribution and evaluation of dry eye in rheumatoid arthritis. Innate Immun. 2013;19:348–354. doi:10.1177/1753425912461677.
   PubMed Web of Science ®Google Scholar
• Bitirgen G, Akpinar Z, Malik RA, Ozkagnici A. Use of corneal confocal microscopy to detect corneal nerve loss and increased dendritic cells in patients with multiple sclerosis. JAMA Ophthalmol. 2017;135:777–782. doi:10.1001/jamaophthalmol.2017.1590.
   PubMed Web of Science ®Google Scholar
• Zhivov A, Stave J, Vollmar B, Guthoff R. In vivo confocal microscopic evaluation of langerhans cell density and distribution in the corneal epithelium of healthy volunteers and contact lens wearers. Cornea. 2007;26:47–54. doi:10.1097/ICO.0b013e31802e3b55.
   PubMed Web of Science ®Google Scholar
• Catry L, Van Den Oord J, Foets B, Missotten L. Morphologic and immunophenotypic heterogeneity of corneal dendritic cells. Graefes Arch Clin Exp Ophthalmol. 1991;229:182–185.
   PubMed Web of Science ®Google Scholar
• Meng Q, Yang P, Jin H, et al. Phenotypes, distribution, and morphological features of antigen-presenting cells in the murine cornea following intravitreal injection. Mol Vis. 2007;13:475–486.
   PubMed Web of Science ®Google Scholar
• Williams KA, Ash JK, Coster DJ. Histocompatibility antigen and passenger cell content of normal and diseased human cornea. Transplantation. 1985;39:265–269. doi:10.1097/00007890-198503000-00011.
   PubMed Web of Science ®Google Scholar
• Hamrah P, Huq SO, Liu Y, Zhang Q, Dana MR. Corneal immunity is mediated by heterogeneous population of antigen-presenting cells. J Leukoc Biol. 2003;74:172–178. doi:10.1189/jlb.1102544.
   PubMed Web of Science ®Google Scholar
• Chinnery HR, Ruitenberg MJ, Plant GW, Pearlman E, Jung S, McMenamin PG. The chemokine receptor CX3CR1 mediates homing of MHC class II-positive cells to the normal mouse corneal epithelium. Invest Ophthalmol Vis Sci. 2007;48:1568–1574. doi:10.1167/iovs.06-0746.
   PubMed Web of Science ®Google Scholar
• Lin H, Li W, Dong N, et al. Changes in corneal epithelial layer inflammatory cells in aqueous tear-deficient dry eye. Invest Ophthalmol Vis Sci. 2010;51:122–128. doi:10.1167/iovs.09-3629.
   PubMed Web of Science ®Google Scholar
• Cruzat A, Schrems WA, Schrems-Hoesl LM, et al. Contralateral clinically unaffected eyes of patients with unilateral infectious keratitis demonstrate a sympathetic immune response. Invest Ophthalmol Vis Sci. 2015;56:6612–6620. doi:10.1167/iovs.15-16560.
   PubMed Web of Science ®Google Scholar
• Lee HK, Kim KW, Ryu JS, Jeong HJ, Lee SM, Kim MK. Bilateral effect of the unilateral corneal nerve cut on both ocular surface and lacrimal gland. Invest Ophthalmol Vis Sci. 2019;60:430–441. doi:10.1167/iovs.18-26051.
   PubMed Web of Science ®Google Scholar
• Paunicka KJ, Mellon J, Robertson D, Petroll M, Brown JR, Niederkorn JY. Severing corneal nerves in one eye induces sympathetic loss of immune privilege and promotes rejection of future corneal allografts placed in either eye. Am J Transplant. 2015;15:1490–1501. doi:10.1111/ajt.13240.
   PubMed Web of Science ®Google Scholar
• Guzman M, Miglio MS, Zgajnar NR, et al. The mucosal surfaces of both eyes are immunologically linked by a neurogenic inflammatory reflex involving TRPV1 and substance P. Mucosal Immunol. 2018;11:1441–1453. doi:10.1038/s41385-018-0040-5.
   PubMed Web of Science ®Google Scholar
• Schain AJ, Melo-Carrillo A, Borsook D, Grutzendler J, Strassman AM, Burstein R. Activation of pial and dural macrophages and dendritic cells by cortical spreading depression. Ann Neurol. 2018;83:508–521. doi:10.1002/ana.25169.
   PubMed Web of Science ®Google Scholar
• Dando SJ, Kazanis R, Chinnery HR, McMenamin PG. Regional and functional heterogeneity of antigen presenting cells in the mouse brain and meninges. Glia. 2018;67:935–949. doi:10.1002/glia.23581.
   PubMed Web of Science ®Google Scholar
• Kozlowski C, Weimer RM. An automated method to quantify microglia morphology and application to monitor activation state longitudinally in vivo. PLoS One. 2012;7:e31814. doi:10.1371/journal.pone.0031814.
   PubMed Web of Science ®Google Scholar
• Chu CJ, Gardner PJ, Copland DA, et al. Multimodal analysis of ocular inflammation using the endotoxin-induced uveitis mouse model. Dis Model Mech. 2016;9:473–481. doi:10.1242/dmm.022475.
   PubMed Web of Science ®Google Scholar
• Seyed-Razavi Y, Lopez MJ, Mantopoulos D, et al. Kinetics of corneal leukocytes by intravital multiphoton microscopy. Faseb J. 2018;33:2199–2211. doi:10.1096/fj.201800684RR.
   PubMed Web of Science ®Google Scholar
• Pal-Ghosh S, Pajoohesh-Ganji A, Menko AS, et al. Cytokine deposition alters leukocyte morphology and initial recruitment of monocytes and gamma deltaT cells after corneal injury. Invest Ophthalmol Vis Sci. 2014;55:2757–2765. doi:10.1167/iovs.13-13557.
   PubMed Web of Science ®Google Scholar