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Published in: BMC Ophthalmology 1/2017

Open Access 01-12-2017 | Research article

Link between neurodegeneration and trabecular meshwork injury in glaucomatous patients

Authors: Yong Zhang, Qinmei Yang, Feng Guo, Xia Chen, Lin Xie

Published in: BMC Ophthalmology | Issue 1/2017

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Abstract

Background

Glaucoma is classified as a neurodegenerative disease. However, the biomarkers of neurodegeneration in the aqueous humour of primary open angle glaucoma (POAG) eyes have not been quantitatively examined yet. In this study, levels of neurodegeneration-related cytokines in the aqueous humour of POAG eyes were measured and compared with those of non-glaucoma (senile cataract) control eyes.

Methods

This cross-sectional study included 24 patients (24 eyes) with POAG and 22 patients (22 eyes) with cataract. Aqueous humour samples were collected before the commencement of phacoemulsification surgery. The concentrations of brain-derived neurotrophic factor (BDNF), cathepsin D, myeloperoxidase (MPO), soluble intercellular adhesion molecule-1 (sICAM-1), soluble neural cell adhesion molecule (sNCAM), soluble vascular cell adhesion molecule-1 (sVCAM-1), and plasminogen activator inhibitor-1 (PAI-1) were measured using the Luminex suspension array technique. The clinical characteristics of the patients were also obtained for correlation analysis.

Results

Compared with the cataract group, the levels of cathepsin D (P < 0.001), sNCAM (P < 0.001) and sVCAM-1 (P = 0.007) were significantly higher in the aqueous humour samples from POAG. The levels of BDNF, sICAM-1, MPO and PAI-1 did not differ among the groups. Mean deviation (MD) values measured by the Humphrey Visual Field Analyzer were significantly associated with levels of cathepsin D (P < 0.001; ρ= − 0.668), sICAM-1 (P = 0.003; ρ= − 0.579), sVCAM-1(P < 0.001; ρ= − 0.695), and PAI-1 (P = 0.007; ρ= − 0.533). The cytokines showed a positive correlation among each other (P < 0.0083).

Conclusion

These data suggest that POAG patients had elevated levels of multiple biomarkers of neurodegeneration in the aqueous humour, and these elevated biomarkers may be related to trabecular meshwork injury.

Trial registration

This study was registered in the Chinese Clinical Trial Registry (ChiCTR-OOC-16008516) on May 22, 2016.
Literature
1.
go back to reference Mac NC, Nickells RW. Neuroinflammation in glaucoma and optic nerve damage. Prog Mol Biol Transl Sci. 2015;134:343–63.CrossRef Mac NC, Nickells RW. Neuroinflammation in glaucoma and optic nerve damage. Prog Mol Biol Transl Sci. 2015;134:343–63.CrossRef
2.
go back to reference Tham YC, Li X, Wong TY, Quigley HA, Aung T, Cheng CY. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121(11):2081–90.CrossRefPubMed Tham YC, Li X, Wong TY, Quigley HA, Aung T, Cheng CY. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121(11):2081–90.CrossRefPubMed
3.
go back to reference Gupta N, Ang LC, Noel DTL, Bidaisee L, Yucel YH. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br J Ophthalmol. 2006;90(6):674–8.CrossRefPubMedPubMedCentral Gupta N, Ang LC, Noel DTL, Bidaisee L, Yucel YH. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br J Ophthalmol. 2006;90(6):674–8.CrossRefPubMedPubMedCentral
4.
go back to reference Yucel YH, Zhang Q, Weinreb RN, Kaufman PL, Gupta N. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res. 2003;22(4):465–81.CrossRefPubMed Yucel YH, Zhang Q, Weinreb RN, Kaufman PL, Gupta N. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res. 2003;22(4):465–81.CrossRefPubMed
6.
go back to reference Nowak A, Majsterek I, Przybylowska-Sygut K, Pytel D, Szymanek K, Szaflik J, Szaflik JP. Analysis of the expression and polymorphism of APOE, HSP, BDNF, and GRIN2B genes associated with the neurodegeneration process in the pathogenesis of primary open angle glaucoma. Biomed Res Int. 2015;2015:258281.PubMedPubMedCentral Nowak A, Majsterek I, Przybylowska-Sygut K, Pytel D, Szymanek K, Szaflik J, Szaflik JP. Analysis of the expression and polymorphism of APOE, HSP, BDNF, and GRIN2B genes associated with the neurodegeneration process in the pathogenesis of primary open angle glaucoma. Biomed Res Int. 2015;2015:258281.PubMedPubMedCentral
7.
go back to reference Bayer AU, Keller ON, Ferrari F, Maag KP. Association of glaucoma with neurodegenerative diseases with apoptotic cell death: Alzheimer's disease and Parkinson's disease. Am J Ophthalmol. 2002;133(1):135–7.CrossRefPubMed Bayer AU, Keller ON, Ferrari F, Maag KP. Association of glaucoma with neurodegenerative diseases with apoptotic cell death: Alzheimer's disease and Parkinson's disease. Am J Ophthalmol. 2002;133(1):135–7.CrossRefPubMed
8.
9.
go back to reference Schwagerl AL, Mohan PS, Cataldo AM, Vonsattel JP, Kowall NW, Nixon RA. Elevated levels of the endosomal-lysosomal proteinase cathepsin D in cerebrospinal fluid in Alzheimer disease. J Neurochem. 1995;64(1):443–6.CrossRefPubMed Schwagerl AL, Mohan PS, Cataldo AM, Vonsattel JP, Kowall NW, Nixon RA. Elevated levels of the endosomal-lysosomal proteinase cathepsin D in cerebrospinal fluid in Alzheimer disease. J Neurochem. 1995;64(1):443–6.CrossRefPubMed
10.
go back to reference Matsuda M, Tsukada N, Miyagi K, Yanagisawa N. Increased levels of soluble vascular cell adhesion molecule-1 (VCAM-1) in the cerebrospinal fluid and sera of patients with multiple sclerosis and human T lymphotropic virus type-1-associated myelopathy. J Neuroimmunol. 1995;59(1–2):35–40.CrossRefPubMed Matsuda M, Tsukada N, Miyagi K, Yanagisawa N. Increased levels of soluble vascular cell adhesion molecule-1 (VCAM-1) in the cerebrospinal fluid and sera of patients with multiple sclerosis and human T lymphotropic virus type-1-associated myelopathy. J Neuroimmunol. 1995;59(1–2):35–40.CrossRefPubMed
11.
go back to reference Hartung HP, Michels M, Reiners K, Seeldrayers P, Archelos JJ, Toyka KV. Soluble ICAM-1 serum levels in multiple sclerosis and viral encephalitis. Neurology. 1993;43(11):2331–5.CrossRefPubMed Hartung HP, Michels M, Reiners K, Seeldrayers P, Archelos JJ, Toyka KV. Soluble ICAM-1 serum levels in multiple sclerosis and viral encephalitis. Neurology. 1993;43(11):2331–5.CrossRefPubMed
12.
go back to reference Welge-Lussen U, May CA, Neubauer AS, Priglinger S. Role of tissue growth factors in aqueous humor homeostasis. Curr Opin Ophthalmol. 2001;12(2):94–9.CrossRefPubMed Welge-Lussen U, May CA, Neubauer AS, Priglinger S. Role of tissue growth factors in aqueous humor homeostasis. Curr Opin Ophthalmol. 2001;12(2):94–9.CrossRefPubMed
13.
go back to reference Streilein JW. Anterior chamber associated immune deviation: the privilege of immunity in the eye. Surv Ophthalmol. 1990;35(1):67–73.CrossRefPubMed Streilein JW. Anterior chamber associated immune deviation: the privilege of immunity in the eye. Surv Ophthalmol. 1990;35(1):67–73.CrossRefPubMed
14.
go back to reference Ohira S, Inoue T, Iwao K, Takahashi E, Tanihara H. Factors influencing aqueous Proinflammatory cytokines and growth factors in Uveitic glaucoma. PLoS One. 2016;11(1):e147080.CrossRef Ohira S, Inoue T, Iwao K, Takahashi E, Tanihara H. Factors influencing aqueous Proinflammatory cytokines and growth factors in Uveitic glaucoma. PLoS One. 2016;11(1):e147080.CrossRef
15.
go back to reference Jonas JB, Tao Y, Neumaier M, Findeisen P. Cytokine concentration in aqueous humour of eyes with exudative age-related macular degeneration. Acta Ophthalmol. 2012;90(5):e381–8.CrossRefPubMed Jonas JB, Tao Y, Neumaier M, Findeisen P. Cytokine concentration in aqueous humour of eyes with exudative age-related macular degeneration. Acta Ophthalmol. 2012;90(5):e381–8.CrossRefPubMed
16.
go back to reference Zhu X, Zhang K, He W, Yang J, Sun X, Jiang C, Dai J, Lu Y. Proinflammatory status in the aqueous humor of high myopic cataract eyes. Exp Eye Res. 2016;142:13–8.CrossRefPubMed Zhu X, Zhang K, He W, Yang J, Sun X, Jiang C, Dai J, Lu Y. Proinflammatory status in the aqueous humor of high myopic cataract eyes. Exp Eye Res. 2016;142:13–8.CrossRefPubMed
17.
go back to reference Izzotti A, Longobardi M, Cartiglia C, Sacca SC. Proteome alterations in primary open angle glaucoma aqueous humor. J Proteome Res. 2010;9(9):4831–8.CrossRefPubMed Izzotti A, Longobardi M, Cartiglia C, Sacca SC. Proteome alterations in primary open angle glaucoma aqueous humor. J Proteome Res. 2010;9(9):4831–8.CrossRefPubMed
18.
go back to reference Alvarado JA, Yeh RF, Franse-Carman L, Marcellino G, Brownstein MJ. Interactions between endothelia of the trabecular meshwork and of Schlemm's canal: a new insight into the regulation of aqueous outflow in the eye. Trans Am Ophthalmol Soc. 2005;103:148–62. 162-163PubMedPubMedCentral Alvarado JA, Yeh RF, Franse-Carman L, Marcellino G, Brownstein MJ. Interactions between endothelia of the trabecular meshwork and of Schlemm's canal: a new insight into the regulation of aqueous outflow in the eye. Trans Am Ophthalmol Soc. 2005;103:148–62. 162-163PubMedPubMedCentral
19.
go back to reference Fuchshofer R, Tamm ER. Modulation of extracellular matrix turnover in the trabecular meshwork. Exp Eye Res. 2009;88(4):683–8.CrossRefPubMed Fuchshofer R, Tamm ER. Modulation of extracellular matrix turnover in the trabecular meshwork. Exp Eye Res. 2009;88(4):683–8.CrossRefPubMed
20.
go back to reference Foster PJ, Buhrmann R, Quigley HA, Johnson GJ. The definition and classification of glaucoma in prevalence surveys. Br J Ophthalmol. 2002;86(2):238–42.CrossRefPubMedPubMedCentral Foster PJ, Buhrmann R, Quigley HA, Johnson GJ. The definition and classification of glaucoma in prevalence surveys. Br J Ophthalmol. 2002;86(2):238–42.CrossRefPubMedPubMedCentral
21.
go back to reference Sharma RK, Rogojina AT, Chalam KV. Multiplex immunoassay analysis of biomarkers in clinically accessible quantities of human aqueous humor. Mol Vis. 2009;15:60–9.PubMedPubMedCentral Sharma RK, Rogojina AT, Chalam KV. Multiplex immunoassay analysis of biomarkers in clinically accessible quantities of human aqueous humor. Mol Vis. 2009;15:60–9.PubMedPubMedCentral
22.
23.
go back to reference Rusnak S, Vrzalova J, Sobotova M, Hecova L, Ricarova R, Topolcan O. The measurement of intraocular biomarkers in various stages of proliferative diabetic retinopathy using multiplex xMAP technology. J Ophthalmol. 2015;2015:424783.CrossRefPubMedPubMedCentral Rusnak S, Vrzalova J, Sobotova M, Hecova L, Ricarova R, Topolcan O. The measurement of intraocular biomarkers in various stages of proliferative diabetic retinopathy using multiplex xMAP technology. J Ophthalmol. 2015;2015:424783.CrossRefPubMedPubMedCentral
24.
go back to reference Sacca SC, Bolognesi C, Battistella A, Bagnis A, Izzotti A. Gene-environment interactions in ocular diseases. Mutat Res. 2009;667(1–2):98–117.CrossRefPubMed Sacca SC, Bolognesi C, Battistella A, Bagnis A, Izzotti A. Gene-environment interactions in ocular diseases. Mutat Res. 2009;667(1–2):98–117.CrossRefPubMed
25.
go back to reference Sacca SC, Izzotti A, Rossi P, Traverso C. Glaucomatous outflow pathway and oxidative stress. Exp Eye Res. 2007;84(3):389–99.CrossRefPubMed Sacca SC, Izzotti A, Rossi P, Traverso C. Glaucomatous outflow pathway and oxidative stress. Exp Eye Res. 2007;84(3):389–99.CrossRefPubMed
26.
go back to reference DP L, Tian L, O'Neill C, King NJ. Regulation of cellular adhesion molecule expression in murine oocytes, peri-implantation and post-implantation embryos. Cell Res. 2002;12(5–6):373–83. DP L, Tian L, O'Neill C, King NJ. Regulation of cellular adhesion molecule expression in murine oocytes, peri-implantation and post-implantation embryos. Cell Res. 2002;12(5–6):373–83.
27.
go back to reference Sacca SC, Gandolfi S, Bagnis A, Manni G, Damonte G, Traverso CE, Izzotti A. From DNA damage to functional changes of the trabecular meshwork in aging and glaucoma. Ageing Res Rev. 2016;29:26–41.CrossRefPubMed Sacca SC, Gandolfi S, Bagnis A, Manni G, Damonte G, Traverso CE, Izzotti A. From DNA damage to functional changes of the trabecular meshwork in aging and glaucoma. Ageing Res Rev. 2016;29:26–41.CrossRefPubMed
28.
go back to reference Anastassiou G, Esser M, Bader E, Steuhl KP, Bornfeld N. Expression of cell adhesion molecules and tumour infiltrating leucocytes in conjunctival melanoma. Melanoma Res. 2004;14(5):381–5.CrossRefPubMed Anastassiou G, Esser M, Bader E, Steuhl KP, Bornfeld N. Expression of cell adhesion molecules and tumour infiltrating leucocytes in conjunctival melanoma. Melanoma Res. 2004;14(5):381–5.CrossRefPubMed
29.
go back to reference Armentero M, Levandis G, Bazzini E, Cerri S, Ghezzi C, Blandini F. Adhesion molecules as potential targets for neuroprotection in a rodent model of Parkinson's disease. Neurobiol Dis. 2011;43(3):663–8.CrossRefPubMed Armentero M, Levandis G, Bazzini E, Cerri S, Ghezzi C, Blandini F. Adhesion molecules as potential targets for neuroprotection in a rodent model of Parkinson's disease. Neurobiol Dis. 2011;43(3):663–8.CrossRefPubMed
30.
go back to reference Ewers M, Mielke MM, Hampel H. Blood-based biomarkers of microvascular pathology in Alzheimer's disease. Exp Gerontol. 2010;45(1):75–9.CrossRefPubMed Ewers M, Mielke MM, Hampel H. Blood-based biomarkers of microvascular pathology in Alzheimer's disease. Exp Gerontol. 2010;45(1):75–9.CrossRefPubMed
31.
go back to reference Barks JL, McQuillan JJ, Iademarco MF. TNF-alpha and IL-4 synergistically increase vascular cell adhesion molecule-1 expression in cultured vascular smooth muscle cells. J Immunol. 1997;159(9):4532–8.PubMed Barks JL, McQuillan JJ, Iademarco MF. TNF-alpha and IL-4 synergistically increase vascular cell adhesion molecule-1 expression in cultured vascular smooth muscle cells. J Immunol. 1997;159(9):4532–8.PubMed
32.
go back to reference Balaiya S, Edwards J, Tillis T, Khetpal V, Chalam KV. Tumor necrosis factor-alpha (TNF-alpha) levels in aqueous humor of primary open angle glaucoma. Clin Ophthalmol. 2011;5:553–6.CrossRefPubMedPubMedCentral Balaiya S, Edwards J, Tillis T, Khetpal V, Chalam KV. Tumor necrosis factor-alpha (TNF-alpha) levels in aqueous humor of primary open angle glaucoma. Clin Ophthalmol. 2011;5:553–6.CrossRefPubMedPubMedCentral
33.
go back to reference Perkumas KM, Stamer WD. Protein markers and differentiation in culture for Schlemm's canal endothelial cells. Exp Eye Res. 2012;96(1):82–7.CrossRefPubMed Perkumas KM, Stamer WD. Protein markers and differentiation in culture for Schlemm's canal endothelial cells. Exp Eye Res. 2012;96(1):82–7.CrossRefPubMed
34.
go back to reference Kalin R, Righi A, Del RA, Bagchi D, Generini S, Cerinic MM, Das DK. Activin, a grape seed-derived proanthocyanidin extract, reduces plasma levels of oxidative stress and adhesion molecules (ICAM-1, VCAM-1 and E-selectin) in systemic sclerosis. Free Radic Res. 2002;36(8):819–25.CrossRefPubMed Kalin R, Righi A, Del RA, Bagchi D, Generini S, Cerinic MM, Das DK. Activin, a grape seed-derived proanthocyanidin extract, reduces plasma levels of oxidative stress and adhesion molecules (ICAM-1, VCAM-1 and E-selectin) in systemic sclerosis. Free Radic Res. 2002;36(8):819–25.CrossRefPubMed
35.
go back to reference Kobayashi N, Mita S, Yoshida K, Honda T, Kobayashi T, Hara K, Nakano S, Tsubokou Y, Matsuoka H. Celiprolol activates eNOS through the PI3K-Akt pathway and inhibits VCAM-1 via NF-kappaB induced by oxidative stress. Hypertension. 2003;42(5):1004–13.CrossRefPubMed Kobayashi N, Mita S, Yoshida K, Honda T, Kobayashi T, Hara K, Nakano S, Tsubokou Y, Matsuoka H. Celiprolol activates eNOS through the PI3K-Akt pathway and inhibits VCAM-1 via NF-kappaB induced by oxidative stress. Hypertension. 2003;42(5):1004–13.CrossRefPubMed
36.
go back to reference Gnanapavan S, Ho P, Heywood W, Jackson S, Grant D, Rantell K, Keir G, Mills K, Steinman L, Giovannoni G. Progression in multiple sclerosis is associated with low endogenous NCAM. J Neurochem. 2013;125(5):766–73.CrossRefPubMedPubMedCentral Gnanapavan S, Ho P, Heywood W, Jackson S, Grant D, Rantell K, Keir G, Mills K, Steinman L, Giovannoni G. Progression in multiple sclerosis is associated with low endogenous NCAM. J Neurochem. 2013;125(5):766–73.CrossRefPubMedPubMedCentral
37.
go back to reference Gnanapavan S, Grant D, Illes-Toth E, Lakdawala N, Keir G, Giovannoni G. Neural cell adhesion molecule--description of a CSF ELISA method and evidence of reduced levels in selected neurological disorders. J Neuroimmunol. 2010;225(1–2):118–22.CrossRefPubMed Gnanapavan S, Grant D, Illes-Toth E, Lakdawala N, Keir G, Giovannoni G. Neural cell adhesion molecule--description of a CSF ELISA method and evidence of reduced levels in selected neurological disorders. J Neuroimmunol. 2010;225(1–2):118–22.CrossRefPubMed
38.
go back to reference Ottervald J, Franzen B, Nilsson K, Andersson LI, Khademi M, Eriksson B, Kjellstrom S, Marko-Varga G, Vegvari A, Harris RA, et al. Multiple sclerosis: identification and clinical evaluation of novel CSF biomarkers. J Proteome. 2010;73(6):1117–32.CrossRef Ottervald J, Franzen B, Nilsson K, Andersson LI, Khademi M, Eriksson B, Kjellstrom S, Marko-Varga G, Vegvari A, Harris RA, et al. Multiple sclerosis: identification and clinical evaluation of novel CSF biomarkers. J Proteome. 2010;73(6):1117–32.CrossRef
39.
go back to reference van Kammen DP, Poltorak M, Kelley ME, Yao JK, Gurklis JA, Peters JL, Hemperly JJ, Wright RD, Freed WJ. Further studies of elevated cerebrospinal fluid neuronal cell adhesion molecule in schizophrenia. Biol Psychiatry. 1998;43(9):680–6.CrossRefPubMed van Kammen DP, Poltorak M, Kelley ME, Yao JK, Gurklis JA, Peters JL, Hemperly JJ, Wright RD, Freed WJ. Further studies of elevated cerebrospinal fluid neuronal cell adhesion molecule in schizophrenia. Biol Psychiatry. 1998;43(9):680–6.CrossRefPubMed
40.
go back to reference Pantovic-Stefanovic M, Petronijevic N, Dunjic-Kostic B, Velimirovic M, Nikolic T, Jurisic V, Lackovic M, Damjanovic A, Totic-Poznanovic S, Jovanovic AA, et al. sVCAM-1, sICAM-1, TNF-alpha, and IL-6 levels in bipolar disorder type I: acute, longitudinal, and therapeutic implications. World J Biol Psychiatry. 2016:1–34. Pantovic-Stefanovic M, Petronijevic N, Dunjic-Kostic B, Velimirovic M, Nikolic T, Jurisic V, Lackovic M, Damjanovic A, Totic-Poznanovic S, Jovanovic AA, et al. sVCAM-1, sICAM-1, TNF-alpha, and IL-6 levels in bipolar disorder type I: acute, longitudinal, and therapeutic implications. World J Biol Psychiatry. 2016:1–34.
41.
go back to reference Wakabayashi Y, Uchida S, Funato H, Matsubara T, Watanuki T, Otsuki K, Fujimoto M, Nishida A, Watanabe Y. State-dependent changes in the expression levels of NCAM-140 and L1 in the peripheral blood cells of bipolar disorders, but not in the major depressive disorders. Prog Neuro-Psychopharmacol Biol Psychiatry. 2008;32(5):1199–205.CrossRef Wakabayashi Y, Uchida S, Funato H, Matsubara T, Watanuki T, Otsuki K, Fujimoto M, Nishida A, Watanabe Y. State-dependent changes in the expression levels of NCAM-140 and L1 in the peripheral blood cells of bipolar disorders, but not in the major depressive disorders. Prog Neuro-Psychopharmacol Biol Psychiatry. 2008;32(5):1199–205.CrossRef
42.
go back to reference Liu G, Jiang Y, Wang P, Feng R, Jiang N, Chen X, Song H, Chen Z. Cell adhesion molecules contribute to Alzheimer's disease: multiple pathway analyses of two genome-wide association studies. J Neurochem. 2012;120(1):190–8.CrossRefPubMed Liu G, Jiang Y, Wang P, Feng R, Jiang N, Chen X, Song H, Chen Z. Cell adhesion molecules contribute to Alzheimer's disease: multiple pathway analyses of two genome-wide association studies. J Neurochem. 2012;120(1):190–8.CrossRefPubMed
43.
go back to reference Todaro L, Puricelli L, Gioseffi H, Guadalupe PM, Lastiri J, Bal DKJE, Varela M, Sacerdote DLE. Neural cell adhesion molecule in human serum. Increased levels in dementia of the Alzheimer type. Neurobiol Dis. 2004;15(2):387–93.CrossRefPubMed Todaro L, Puricelli L, Gioseffi H, Guadalupe PM, Lastiri J, Bal DKJE, Varela M, Sacerdote DLE. Neural cell adhesion molecule in human serum. Increased levels in dementia of the Alzheimer type. Neurobiol Dis. 2004;15(2):387–93.CrossRefPubMed
44.
go back to reference Ricard CS, Kobayashi S, Pena JD, Salvador-Silva M, Agapova O, Hernandez MR. Selective expression of neural cell adhesion molecule (NCAM)-180 in optic nerve head astrocytes exposed to elevated hydrostatic pressure in vitro. Brain Res Mol Brain Res. 2000;81(1–2):62–79.CrossRefPubMed Ricard CS, Kobayashi S, Pena JD, Salvador-Silva M, Agapova O, Hernandez MR. Selective expression of neural cell adhesion molecule (NCAM)-180 in optic nerve head astrocytes exposed to elevated hydrostatic pressure in vitro. Brain Res Mol Brain Res. 2000;81(1–2):62–79.CrossRefPubMed
45.
go back to reference Foets B, van den Oord J, Engelmann K, Missotten L. A comparative immunohistochemical study of human corneotrabecular tissue. Graefes Arch Clin Exp Ophthalmol. 1992;230(3):269–74.CrossRefPubMed Foets B, van den Oord J, Engelmann K, Missotten L. A comparative immunohistochemical study of human corneotrabecular tissue. Graefes Arch Clin Exp Ophthalmol. 1992;230(3):269–74.CrossRefPubMed
46.
go back to reference Vidoni C, Follo C, Savino M, Melone MA, Isidoro C. The role of Cathepsin D in the pathogenesis of human neurodegenerative disorders. Med Res Rev. 2016;36(5):845–70.CrossRefPubMed Vidoni C, Follo C, Savino M, Melone MA, Isidoro C. The role of Cathepsin D in the pathogenesis of human neurodegenerative disorders. Med Res Rev. 2016;36(5):845–70.CrossRefPubMed
47.
go back to reference Cesen MH, Pegan K, Spes A, Turk B. Lysosomal pathways to cell death and their therapeutic applications. Exp Cell Res. 2012;318(11):1245–51.CrossRefPubMed Cesen MH, Pegan K, Spes A, Turk B. Lysosomal pathways to cell death and their therapeutic applications. Exp Cell Res. 2012;318(11):1245–51.CrossRefPubMed
48.
go back to reference Lin Y, Epstein DL, Liton PB. Intralysosomal iron induces lysosomal membrane permeabilization and cathepsin D-mediated cell death in trabecular meshwork cells exposed to oxidative stress. Invest Ophthalmol Vis Sci. 2010;51(12):6483–95.CrossRefPubMedPubMedCentral Lin Y, Epstein DL, Liton PB. Intralysosomal iron induces lysosomal membrane permeabilization and cathepsin D-mediated cell death in trabecular meshwork cells exposed to oxidative stress. Invest Ophthalmol Vis Sci. 2010;51(12):6483–95.CrossRefPubMedPubMedCentral
Metadata
Title
Link between neurodegeneration and trabecular meshwork injury in glaucomatous patients
Authors
Yong Zhang
Qinmei Yang
Feng Guo
Xia Chen
Lin Xie
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Ophthalmology / Issue 1/2017
Electronic ISSN: 1471-2415
DOI
https://doi.org/10.1186/s12886-017-0623-z

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