Neuroinflammation in glaucoma: A new opportunity

Williams, Pete A.; Marsh-Armstrong, Nick; Howell, Gareth R.; Bosco, Alejandra; Danias, John; Simon, John; Di Polo, Adriana; Kuehn, Markus H.; Przedborski, Serge; Raff, Martin; Trounce, Ian

doi:10.1016/j.exer.2017.02.014

Cited by 253Glaucoma and retinal disordersNeuroinflammation and Neurodegeneration MechanismsOcular Diseases and Behçet’s Syndrome

Neuroinflammation in glaucoma: A new opportunity

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Williams, Pete A., Marsh-Armstrong, Nick, Howell, Gareth R., Bosco, Alejandra, Danias, John, Simon, John, Di Polo, Adriana, Kuehn, Markus H. +3 more·2017·Experimental Eye Research

DOI 10.1016/j.exer.2017.02.014PMC PMC5497582

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Abstract

Mounting evidence suggests neuroinflammation is a key process in glaucoma, yet the precise roles are not known. Understanding these complex processes, which may also be a key in other common neurodegenerations such as Alzheimer's disease, will lead to targeted therapeutics for a disease that affects as many as 80 million people worldwide. Here, we define neuroinflammation as any immune-relevant response by a variety of cell types including astrocytes, microglia, and peripherally derived cells occurring in the optic nerve head and/or retina. In this review article, we first discuss clinical evidence for neuroinflammation in glaucoma and define neuroinflammation in glaucoma. We then review the inflammatory pathways that have been associated with glaucoma. Finally, we set out key research directions that we believe will greatly advance our understanding of the role of neuroinflammation in glaucoma. This review arose from a discussion of neuroinflammation in glaucoma at the 2015 meeting of The Lasker/IRRF Initiative for Innovation in Vision Science. This manuscript sets out to summarize one of these sessions; "Inflammation and Glaucomatous Neurodegeneration", as well as to review the current state of the literature surrounding neuroinflammation in glaucoma.

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“However, discussions focused on regions felt by the group to be most relevant to glaucoma: retinal ganglion cell (RGC) dysfunction/loss; the ONH, where many studies have shown critical events occur in glaucoma; the retina, where RGC soma, dendrites and synapses maybe affected by neuroinflammation, and the peripheral i…”
BackgroundInfluential
Deficiency of complement component 5 ameliorates glaucoma in DBA/2J mice
Howell, G. R., Soto, I., Ryan, M. M., Graham, L. C., Smith, R. S., & John, S. W. M. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-76 · Cited by 97 · cited 4× · see citing works
“…in both human glaucoma (Stasi et al., 2006; Nikolskaya et al., 2009; Tezel et al., 2010; Doudevski et al., 2014) and animal models of glaucoma (Howell et al., 2008; 2011; 2013; Ren and Danias, 2010; Howell et al., 2011; Howell et al., 2013; Astafurov et al., 2014; Howell et al., 2014), as…”
BackgroundInfluentialSelf-citation
VEGF Receptor Blockade Markedly Reduces Retinal Microglia/Macrophage Infiltration into Laser-Induced CNV
Hu, H., Parlier, R., Shen, J.-K., Lutty, G. A., & Vinores, S. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071808 · Cited by 97 · cited 1× · see citing works
“There is some evidence that retinal and ONH microglia deactivation by minocycline at early stages of disease may result in reduced neurodegeneration (Shimazawa et al., 2005; ; Bosco et al., 2008; Levkovitch-Verbin et al., 2011; 2006; 2014a; 2014b; Huang et al., 2013).”
Background
Minocycline Delays Death of Retinal Ganglion Cells in Experimental Glaucoma and After Optic Nerve Transection
Levkovitch-Verbin, H. (2006) · Archives of Ophthalmology · doi:10.1001/archopht.124.4.520 · Cited by 95 · cited 1× · see citing works
“There is some evidence that retinal and ONH microglia deactivation by minocycline at early stages of disease may result in reduced neurodegeneration (Shimazawa et al., 2005; ; Bosco et al., 2008; Levkovitch-Verbin et al., 2011; 2006; 2014a; 2014b; Huang et al., 2013).”
Background
The role of astrocytes in optic nerve head fibrosis in glaucoma
Schneider, M., & Fuchshofer, R. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.08.014 · Cited by 90 · see citing works
Enhanced Tenascin Expression Associated with Reactive Astrocytes in Human Optic Nerve Heads with Primary Open Angle Glaucoma
Pena, J. D. O., Varela, H. J., Ricard, C. S., & Hernandez, M. R. (1999) · Experimental Eye Research · doi:10.1006/exer.1998.0577 · Cited by 90 · cited 2× · see citing works
“Interestingly, one of the endogenous ligands for TLR4 is Tenascin-C, which is highly upregulated in glaucomatous ONH (Pena et al., 1999; Wallace et al., 2014; 2015) and animal models of glaucoma (Johnson et al., 2007).”
Background
The role of Müller glia and microglia in glaucoma
Seitz, R., Ohlmann, A., & Tamm, E. R. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1666-y · Cited by 90 · cited 1× · see citing works
“Both in the retina and, most importantly in the ONH, the principal microglial cells show signs of increased reactivity in glaucoma (Bosco et al., 2011; Howell et al., 2011; Qu and Jakobs, 2013; Seitz et al., 2013; Howell et al., 2014).”
Background
Inflammatory glaucoma
Bodh, S. A., Kumar, V., Raina, U. K., Ghosh, B., & Thakar, M. (2011) · Oman Journal of Ophthalmology · doi:10.4103/0974-620x.77655 · Cited by 90 · cited 1× · see citing works
“In the case of uveitis, a form of glaucoma called inflammatory, or uveitic, glaucoma can result from obstruction of drainage structures in the anterior segment as a secondary consequence of the ocular inflammation (Bodh et al., 2011; Siddique et al., 2013; Baneke et al., 2015).”
Background
Astrocyte loss and astrogliosis in neuroinflammatory disorders
Hostenbach, S., Cambron, M., D’haeseleer, M., Kooijman, R., & Keyser, J. D. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.10.012 · Cited by 87 · cited 1× · see citing works
“Interestingly, the TNFa is produced by astrocytes and especially microglia (Sawada et al., 1989; Hostenbach et al., 2014).”
Background
Rapamycin Is Neuroprotective in a Rat Chronic Hypertensive Glaucoma Model
Su, W., Li, Z., Jia, Y., & Zhuo, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099719 · Cited by 86 · cited 1× · see citing works
“Pharmacological inhibition of TNFa or FasL activity has been shown to be neuroprotective in animal models of glaucoma (Roh et al., 2012; Su et al., 2014), although these inhibitors have not provided protection in other neurodegenerative disorders.”
Background
Human CNS immune senescence and neurodegeneration
Streit, W. J., & Xue, Q.-S. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.05.005 · Cited by 86 · cited 1× · see citing works
“It is also worth noting the neuroinflammation occurs in the aging brain and involves multiple cell types, including astrocytes, microglia and macrophages ((Streit and Xue, 2014; Ward et al., 2015), Fig.”
Background
Association of tumour necrosis factor alpha −308 gene polymorphism with primary open-angle glaucoma in Chinese
Lin, H.-J., Tsai, F.-J., Chen, W. C., Shi, Y.-R., Hsu, Y.-C., & Tsai, S.-W. (2003) · Eye · doi:10.1038/sj.eye.6700227 · Cited by 85 · cited 2× · see citing works
“Certain polymorphisms in TNFa confer an increased risk of glaucoma (Lin et al., 2003; Mossb€ ock et al., 2006; Bozkurt et al., 2012; Wang et al., 2012; Xin et al., 2013; Dubey et al., 2015).”
Background
Glaucoma Genes and Mechanisms
Wiggs, J. L. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.04.008 · Cited by 80 · cited 1× · see citing works
“Moreover, there is extensive data showing increased TNFa in vitreous, retina and optic nerve in glaucoma (Wakefield and Lloyd, 1992; Yuan and Neufeld, 2000; Tezel, 2008; Yang et al., 2011; Wiggs, 2015).”
Background
Neuroprotective effects of minocycline against in vitro and in vivo retinal ganglion cell damage
Shimazawa, M., Yamashima, T., Agarwal, N. A., & Hara, H. (2005) · Brain Research · doi:10.1016/j.brainres.2005.06.053 · Cited by 75 · cited 1× · see citing works
“There is some evidence that retinal and ONH microglia deactivation by minocycline at early stages of disease may result in reduced neurodegeneration (Shimazawa et al., 2005; ; Bosco et al., 2008; Levkovitch-Verbin et al., 2011; 2006; 2014a; 2014b; Huang et al., 2013).”
Background
VISUAL FIELD AND RETINAL NERVE FIBRE LAYER IN EARLY GLAUCOMA AFTER OPTIC DISC HAEMORRHAGE
Airaksinen, P. J., & Heijl, A. (1983) · Acta Ophthalmologica · doi:10.1111/j.1755-3768.1983.tb01412.x · Cited by 74 · see citing works
Potential regulatory molecules in the human trabecular meshwork of patients with glaucoma: Immunohistochemical profile of a number of inflammatory cytokines
Taurone, S., Ripandelli, G., Pacella, E., Bianchi, E., Plateroti, A. M., VITO, S. D., Plateroti, P., Grippaudo, F. R., Cavallotti, C. A. P., & Artico, M. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2772 · Cited by 70 · cited 2× · see citing works
“directly to affect the drainage structures, among other things, by increasing extracellular matrix deposition by trabecular meshwork cells, which increases outflow resistance and consequently increased intraocular pressure (Clark et al., 1995; Tektas et al., 2011; Overby et al., 2014; Raghunathan et al., 2015; Taurone…”
Background
The Pathogenesis of Raised Intraocular Pressure in Uveitis
Baneke, A. J., Lim, K. S., & Stanford, M. R. (2015) · Current Eye Research · doi:10.3109/02713683.2015.1017650 · Cited by 63 · cited 1× · see citing works
“In the case of uveitis, a form of glaucoma called inflammatory, or uveitic, glaucoma can result from obstruction of drainage structures in the anterior segment as a secondary consequence of the ocular inflammation (Bodh et al., 2011; Siddique et al., 2013; Baneke et al., 2015).”
Background
Ageing neuroinflammation and neurodegeneration
Ward, R. J. (2015) · Frontiers in Bioscience-Scholar · doi:10.2741/s433 · Cited by 63 · cited 1× · see citing works
“It is also worth noting the neuroinflammation occurs in the aging brain and involves multiple cell types, including astrocytes, microglia and macrophages ((Streit and Xue, 2014; Ward et al., 2015), Fig.”
Background
Network analysis of human glaucomatous optic nerve head astrocytes
Nikolskaya, T., Nikolsky, Y., Serebryiskaya, T., Zvereva, S. D., Sviridov, E., Dezső, Z., Rahkmatulin, E., Brennan, R., Yankovsky, N. K., Bhattacharya, S. K., et al. (2009) · BMC Medical Genomics · doi:10.1186/1755-8794-2-24 · Cited by 62 · cited 2× · see citing works
“Various components of the complement system are increased in both human glaucoma (Stasi et al., 2006; Nikolskaya et al., 2009; Tezel et al., 2010; Doudevski et al., 2014) and animal models of glaucoma (Howell et al.”
Background
Association of Toll-like Receptor 4 Gene Polymorphisms in Japanese Subjects With Primary Open-Angle, Normal-Tension, and Exfoliation Glaucoma
Takano, Y., Shi, D., Shimizu, A., Funayama, T., Mashima, Y., Yasuda, N., Fukuchi, T., Abe, H., Ideta, H., Zheng, X., et al. (2012) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2012.03.050 · Cited by 61 · cited 2× · see citing works
“…in the pathogenesis of glaucoma in two ways: certain alleles of the TLR4 gene are associated with an increased risk of glaucoma, at least in some populations (Shibuya et al., 2008; Takano et al., 2012), and TLR4 and other TLRs are reported to be increased in glaucoma retinas (Luo et al., 2010).”
Background
Clusterin and Complement Activation in Exfoliation Glaucoma
Doudevski, I., Rostagno, A. A., Cowman, M. K., Liebmann, J. M., Ritch, R. H., & Ghiso, J. A. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.13-12941 · Cited by 60 · cited 2× · see citing works
“Various components of the complement system are increased in both human glaucoma (Stasi et al., 2006; Nikolskaya et al., 2009; Tezel et al., 2010; Doudevski et al., 2014) and animal models of glaucoma (Howell et al.”
Background
Astrocytes phagocytose focal dystrophies from shortening myelin segments in the optic nerve of Xenopus laevis at metamorphosis
Mills, E. A., Davis, C.-H. O., Bushong, E. A., Boassa, D., Kim, K.-Y., Ellisman, M. H., & Marsh‐Armstrong, N. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506486112 · Cited by 60 · cited 1× · see citing works
“Recent data also show that ONH astrocytes are phagocytic (Nguyen et al., 2011; Mills et al., 2015).”
BackgroundSelf-citation
Adoptive transfer of immune cells from glaucomatous mice provokes retinal ganglion cell loss in recipients
Gramlich, O. W., Ding, Q. J., Zhu, W., Cook, A. C., Anderson, M. G., & Kuehn, M. H. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0234-y · Cited by 60 · cited 2× · see citing works
“, 2014), and pathways involved in antigen presentation to T cells (Yang et al., 2001; Gramlich et al., 2015; Wong et al., 2015), such as b2-microglobulin and CD3, are likely involved in glaucoma, or at least in RGC damage in animal models of glaucoma.”
BackgroundSelf-citation
Tumor necrosis factor alpha has an early protective effect on retinal ganglion cells after optic nerve crush
Nair, C. E. M., Fernandes, K. A., Schlamp, C. L., Libby, R. T., & Nickells, R. W. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0194-3 · Cited by 58 · cited 1× · see citing works
“Generally, secretion of TNFa and a related protein FasL are thought to promote RGC cell death, through a variety of mechanisms (Wajant et al., 2003; Mac Nair et al., 2014; Cueva Vargas et al., 2015), whichmost likely involve direct killing of RGCs.”
Background
T-Helper1/T-Helper2 Cytokine Imbalance in the Iris of Patients with Glaucoma
Wong, M., Huang, P. H., Li, W., Li, Y., Zhang, S. S.-M., & Zhang, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122184 · Cited by 52 · cited 2× · see citing works
“, 2014), and pathways involved in antigen presentation to T cells (Yang et al., 2001; Gramlich et al., 2015; Wong et al., 2015), such as b2-microglobulin and CD3, are likely involved in glaucoma, or at least in RGC damage in animal models of glaucoma.”
Background
Neuroprotection in glaucoma: present and future
Shi-da, C. H. E. N., Wang, L., & Zhang, X. (2013) · Chinese Medical Journal · doi:10.3760/cma.j.issn.0366-6999.20123565 · Cited by 51 · cited 2× · see citing works
“An increasing body of literature, especially from various animal models, suggests neuroinflammation (generally considered to be immune responses relevant to the central nervous system (CNS)) is a key process in glaucoma (Xu et al., 2009; Baltmr et al., 2010; Chen et al., 2013; Soto and Howell, 2014).”
Background
Relationship Between Retinal Glial Cell Activation in Glaucoma and Vascular Dysregulation
Grieshaber, M. C., Orgül, S., Schoetzau, A., & Flammer, J. (2007) · Journal of Glaucoma · doi:10.1097/ijg.0b013e31802d045a · Cited by 50 · cited 2× · see citing works
“In healthy tissues, astrocytes occupy discrete domains and help preserve a homeostatic environment for neurons to function, in part, through themaintenance of the neurovascular unit (Grieshaber et al., 2007; del Zoppo, 2010, 2012; Kur et al., 2012; da Fonseca et al., 2014).”
Background
The two sides of cytokine signaling and glaucomatous optic neuropathy
Huang, P. C., Zhang, S. S.-M., & Zhang, C. (2009) · Journal of ocular biology, diseases, and informatics · doi:10.1007/s12177-009-9026-6 · Cited by 50 · cited 2× · see citing works
“In addition to these, interferons, interleukins, and various other pro- and anti-inflammatory cytokines (Wakefield and Lloyd, 1992; Tezel, 2008; Huang et al., 2009; Agarwal and Agarwal, 2012; Al-Gayyar and Elsherbiny, 2013; Krizaj et al., 2014), and pathways involved in antigen presentation to T…”
Background
Mouse genetic models: an ideal system for understanding glaucomatous neurodegeneration and neuroprotection
Howell, G. R., Libby, R. T., & John, S. W. M. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)01122-9 · Cited by 49 · cited 2× · see citing works
“…in both human glaucoma (Stasi et al., 2006; Nikolskaya et al., 2009; Tezel et al., 2010; Doudevski et al., 2014) and animal models of glaucoma (Howell et al., 2008; 2011; 2013; Ren and Danias, 2010; Howell et al., 2011; Howell et al., 2013; Astafurov et al., 2014; Howell et al., 2014), as…”
BackgroundSelf-citation
Glaucomatous neurodegeneration: An eye on tumor necrosis factor-alpha
Agarwal, R., & Agarwal, P. (2012) · Indian Journal of Ophthalmology · doi:10.4103/0301-4738.98700 · Cited by 48 · cited 1× · see citing works
“…of glaucoma patients have small optic disk hemorrhages visible upon ophthalmic examinations, which are generally associated with disease progression (Airaksinen and Heijl, 1983; Drance, 1989; Gordon and PiltzSeymour, 1997; Wang et al., 2006; Uhler and Piltz-Seymour, 2008; De Moraes et al., 2012).”
Background
Contribution of TNF-α to the development of retinal neurodegenerative disorders
Al-Gayyar, M. M. H., & Elsherbiny, N. M. (2013) · European Cytokine Network · doi:10.1684/ecn.2013.0334 · Cited by 48 · cited 2× · see citing works
“…and various other pro- and anti-inflammatory cytokines (Wakefield and Lloyd, 1992; Tezel, 2008; Huang et al., 2009; Agarwal and Agarwal, 2012; Al-Gayyar and Elsherbiny, 2013; Krizaj et al., 2014), and pathways involved in antigen presentation to T cells (Yang et al., 2001; Gramlich et al.,…”
Background
Minocycline upregulates pro-survival genes and downregulates pro-apoptotic genes in experimental glaucoma
Levkovitch-Verbin, H., Waserzoog, Y., Vander, S., Makarovsky, D., & Piven, I. (2014) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-014-2588-4 · Cited by 44 · cited 1× · see citing works
“There is some evidence that retinal and ONH microglia deactivation by minocycline at early stages of disease may result in reduced neurodegeneration (Shimazawa et al., 2005; ; Bosco et al., 2008; Levkovitch-Verbin et al., 2011; 2006; 2014a; 2014b; Huang et al., 2013).”
Background
Optic Disc Hemorrhage May Be Associated with Retinal Nerve Fiber Loss in Otherwise Normal Eyes
Jeoung, J. W., Park, K. H., Kim, J. M., Kang, S. H., Kang, J. H., Kim, T., & Kim, D. M. (2008) · Ophthalmology · doi:10.1016/j.ophtha.2008.08.024 · Cited by 43 · cited 2× · see citing works
“Since hemorrhages necessarily mean that there is a breach of the blood-retina barrier, circulating immune cells certainly enter the retina, including in the nerve fiber layer where these hemorrhages are most common (Drance, 1989; Choi et al., 2007; Jeoung et al., 2008; Kurvinen et al., 2010; Hwang et al., 2014), which…”
Background
Optic disc hemorrhages in glaucoma and ocular hypertension: implications and recommendations
Uhler, T. A., & Piltz‐Seymour, J. R. (2008) · Current Opinion in Ophthalmology · doi:10.1097/icu.0b013e3282f3e6bc · Cited by 42 · cited 1× · see citing works
“…of glaucoma patients have small optic disk hemorrhages visible upon ophthalmic examinations, which are generally associated with disease progression (Airaksinen and Heijl, 1983; Drance, 1989; Gordon and PiltzSeymour, 1997; Wang et al., 2006; Uhler and Piltz-Seymour, 2008; De Moraes et al., 2012).”
Background
Optic disk characteristics before the occurrence of disk hemorrhage in glaucoma patients
Law, S. K., Choe, R., & Caprioli, J. (2001) · American Journal of Ophthalmology · doi:10.1016/s0002-9394(01)01009-1 · Cited by 42 · cited 2× · see citing works
“Given that only those bleeds that are seen during the very brief time that patients are undergoing ophthalmic examinations are considered (and only those in front rather than behind the lamina cribrosa would be visible), it is quite possible that small focal bleeds may occur in most and maybe all glaucoma patients (La…”
Background
Aging and the neurovascular unit
del Zoppo, G. J. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06686.x · Cited by 35 · cited 1× · see citing works
“In healthy tissues, astrocytes occupy discrete domains and help preserve a homeostatic environment for neurons to function, in part, through themaintenance of the neurovascular unit (Grieshaber et al., 2007; del Zoppo, 2010, 2012; Kur et al., 2012; da Fonseca et al., 2014).”
Background
A Role for Complement in Glaucoma?
Ren, L., & Danias, J. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-5635-4_7 · Cited by 32 · cited 3× · see citing works
“…et al., 2006; Nikolskaya et al., 2009; Tezel et al., 2010; Doudevski et al., 2014) and animal models of glaucoma (Howell et al., 2008; 2011; 2013; Ren and Danias, 2010; Howell et al., 2011; Howell et al., 2013; Astafurov et al., 2014; Howell et al., 2014), as well as in the aging retina (Xu et…”
BackgroundSelf-citation
Association of tumour necrosis factor‐alpha ‐308 G/A polymorphism with primary open‐angle glaucoma
Bozkurt, B., Mesci, L., Irkec, M. T., Ozdag, B. B., Sanal, Ö., Arslan, U., Ersoy, F., & Tezcan, İ. (2011) · Clinical and Experimental Ophthalmology · doi:10.1111/j.1442-9071.2011.02595.x · Cited by 32 · cited 2× · see citing works
“Certain polymorphisms in TNFa confer an increased risk of glaucoma (Lin et al., 2003; Mossb€ ock et al., 2006; Bozkurt et al., 2012; Wang et al., 2012; Xin et al., 2013; Dubey et al., 2015).”
Background
Early Involvement of Immune/Inflammatory Response Genes in Retinal Degeneration in DBA/2J Mice
Cooper, N. G. F., Fan, Li, Wang, Mo, M., & Kaplan (2010) · Ophthalmology and Eye Diseases · doi:10.4137/oed.s2854 · Cited by 32 · see citing works
TNF-α promoter polymorphisms and primary open-angle glaucoma
Mossböck, G., Weger, M., Moray, M., Renner, W., Haller-Schober, E.-M., Mattes, D., Schmut, O., Wegscheider, B. J., & El‐Shabrawi, Y. (2005) · Eye · doi:10.1038/sj.eye.6702078 · Cited by 32 · cited 1× · see citing works
“Certain polymorphisms in TNFa confer an increased risk of glaucoma (Lin et al., 2003; Mossb€ock et al., 2006; Bozkurt et al., 2012; Wang et al., 2012; Xin et al., 2013; Dubey et al., 2015).”
Background
Roles of tumor necrosis factor alpha gene polymorphisms, tumor necrosis factor alpha level in aqueous humor, and the risks of open angle glaucoma: a meta-analysis.
Xin, X., Gao, L., Wu, T., & Sun, F.-Y. (2013) · Europe PMC (PubMed Central) · Cited by 31 · see citing works
Morphological Changes of Trabeculectomy Specimens in Different Kinds of Uveitic Glaucoma
Tektas, O.-Y., Heinz, C., Heiligenhaus, A., Hammer, C. M., & Luetjen-Drecoll, E. (2011) · Current Eye Research · doi:10.3109/02713683.2011.566409 · Cited by 31 · cited 2× · see citing works
“directly to affect the drainage structures, among other things, by increasing extracellular matrix deposition by trabecular meshwork cells, which increases outflow resistance and consequently increased intraocular pressure (Clark et al., 1995; Tektas et al., 2011; Overby et al., 2014; Raghunathan et al., 2015; Taurone…”
Background
Altered temporal peripapillary retinal flow in patients with disc hemorrhages
Kurvinen, L., Harju, M. P., Saari, J. M., & Vesti, E. T. (2010) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-010-1441-7 · Cited by 29 · cited 2× · see citing works
“…cells certainly enter the retina, including in the nerve fiber layer where these hemorrhages are most common (Drance, 1989; Choi et al., 2007; Jeoung et al., 2008; Kurvinen et al., 2010; Hwang et al., 2014), which is the layer in the retina carrying the delicate axons which are damaged in glaucoma.”
Background
Changes in Retinal Nerve Fiber Layer Thickness After Optic Disc Hemorrhage in Glaucomatous Eyes
Hwang, Y. H., Kim, Y. Y., Kim, H. K., & Sohn, Y. H. (2014) · Journal of Glaucoma · doi:10.1097/ijg.0000000000000083 · Cited by 29 · cited 2× · see citing works
“…cells certainly enter the retina, including in the nerve fiber layer where these hemorrhages are most common (Drance, 1989; Choi et al., 2007; Jeoung et al., 2008; Kurvinen et al., 2010; Hwang et al., 2014), which is the layer in the retina carrying the delicate axons which are damaged in glaucoma.”
Background
In Vivo Dynamics of Retinal Microglial Activation During Neurodegeneration: Confocal Ophthalmoscopic Imaging and Cell Morphometry in Mouse Glaucoma
Bosco, A., Romero, C. O., Ambati, B. K., & Vetter, M. L. (2015) · Journal of Visualized Experiments · doi:10.3791/52731 · Cited by 28 · cited 1× · see citing works
“And yet, many studies have reported microglial responses in glaucoma, which are considered neuroinflammation in other neurodegenerative disorders (Tezel and Wax, 2004; Johnson et al., 2007; Bosco et al., 2011; Howell et al., 2011; Johnson et al., 2011; Astafurov et al., 2014; Bosco et al., 2015).”
BackgroundSelf-citation
Polymorphism in the TNF-α(-863) locus associated with reduced risk of primary open angle glaucoma.
Wang, C.-Y., Shen, Y.-C., Wei, L.-C., Lin, K., Feng, S.-C., Yang, Y.-Y., Chiu, C., & Tsai, H.-Y. (2012) · PubMed Central · Cited by 26 · see citing works
The Function of Matricellular Proteins in the Lamina Cribrosa and Trabecular Meshwork in Glaucoma
Wallace, D., Pokrovskaya, O., & O'Brien, C. J. (2015) · Journal of Ocular Pharmacology and Therapeutics · doi:10.1089/jop.2014.0163 · Cited by 25 · cited 1× · see citing works
“Interestingly, one of the endogenous ligands for TLR4 is Tenascin-C, which is highly upregulated in glaucomatous ONH (Pena et al., 1999; Wallace et al., 2014; 2015) and animal models of glaucoma (Johnson et al., 2007).”
Background
Similarities and differences between primary and secondary degeneration of the optic nerve and the effect of minocycline
Levkovitch-Verbin, H., Spierer, O., Vander, S., & Dardik, R. (2011) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-010-1608-2 · Cited by 24 · cited 1× · see citing works
“There is some evidence that retinal and ONH microglia deactivation by minocycline at early stages of disease may result in reduced neurodegeneration (Shimazawa et al., 2005; ; Bosco et al., 2008; Levkovitch-Verbin et al., 2011; 2006; 2014a; 2014b; Huang et al., 2013).”
Background
Minocycline mechanism of neuroprotection involves the Bcl-2 gene family in optic nerve transection
Levkovitch-Verbin, H., Waserzoog, Y., Vander, S., Makarovsky, D., & Piven, I. (2014) · International Journal of Neuroscience · doi:10.3109/00207454.2013.878340 · Cited by 18 · see citing works
The significance of optic disc hemorrhages in glaucoma.
Gordon, J. A., & Piltz‐Seymour, J. R. (1997) · PubMed · Cited by 16 · see citing works
Retinal Nerve Fiber Layer Thickness Evaluation Using Optical Coherence Tomography in Eyes With Optic Disc Hemorrhage
Choi, J. H., Park, K. H., Kim, D. M., & Kim, T. (2007) · Ophthalmic surgery, lasers & imaging retina · doi:10.3928/15428877-20070301-06 · Cited by 13 · cited 2× · see citing works
“…circulating immune cells certainly enter the retina, including in the nerve fiber layer where these hemorrhages are most common (Drance, 1989; Choi et al., 2007; Jeoung et al., 2008; Kurvinen et al., 2010; Hwang et al., 2014), which is the layer in the retina carrying the delicate axons…”
Background
Immune Phenomena in Glaucoma and Conformational Disorders
Kuehn, M. H. (2014) · Journal of Glaucoma · doi:10.1097/ijg.0000000000000115 · Cited by 12 · cited 1× · see citing works
“For those interested in a more comprehensive review of the literature, we recommended a number of relevant review articles (e.g., References (Wax and Tezel, 2009; Ren and Danias, 2010; Nickells et al., 2012; Vohra et al., 2013; Kuehn, 2014; Soto and Howell, 2014) and see Fig.”
BackgroundSelf-citation
Evaluation of Genetic Polymorphisms in Clusterin and Tumor Necrosis Factor-Alpha Genes in South Indian Individuals with Pseudoexfoliation Syndrome
Dubey, S. K., Hejtmancik, J. F., Krishnadas, S. R., Sharmila, R., Haripriya, A., & Sundaresan, P. (2015) · Current Eye Research · doi:10.3109/02713683.2014.997884 · Cited by 11 · cited 2× · see citing works
“Certain polymorphisms in TNFa confer an increased risk of glaucoma (Lin et al., 2003; Mossb€ ock et al., 2006; Bozkurt et al., 2012; Wang et al., 2012; Xin et al., 2013; Dubey et al., 2015).”
Background
Astrocytes and glaucomatous neurodegeneration
Tamm, E. R., & Dowling, J. E. (2017) · Experimental Eye Research · doi:10.1016/j.exer.2017.02.013 · Cited by 9 · see citing works
Predictive Factors Within the Optic Nerve Complex for Glaucoma Progression
Moraes, C. G. D., Liebmann, J. M., & Ritch, R. H. (2012) · Asia-Pacific Journal of Ophthalmology · doi:10.1097/apo.0b013e31824a65f8 · Cited by 8 · see citing works
[The prevalence of disc hemorrhage and papillary atrophy in Beijing Eye Study].
Wang, Y., Xu, L., & Yang, H. (2006) · PubMed · Cited by 1 · see citing works

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The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma.
Ramirez, A. I., de Hoz, R., Salobrar-Garcia, E., Salazar, J. J., Rojas, B., Ajoy, D., López-Cuenca, I., Rojas, P., Triviño, A., & Ramírez, J. M. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00214 · Cited by 466 · see citing works
Inflammation in Glaucoma: From the back to the front of the eye, and beyond
Baudouin, C., Kolko, M., Parsadaniantz, S. M., & Messmer, E. S. B. M. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100916 · Cited by 470 · see citing works
Microglia in the Retina: Roles in Development, Maturity, and Disease
Silverman, S. M., & Wong, W. T. (2018) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091517-034425 · Cited by 351 · see citing works
Solving neurodegeneration: common mechanisms and strategies for new treatments
Wareham, L. K., Liddelow, S. A., Temple, S., Benowitz, L. I., Di Polo, A., Wellington, C., Goldberg, J. L., He, Z., Duan, X., Bu, G., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00524-0 · Cited by 324 · see citing works
Immune responses to injury and their links to eye disease
Stepp, M. A., & Menko, A. S. (2021) · Translational research · doi:10.1016/j.trsl.2021.05.005 · Cited by 199 · see citing works
“Neuroinflammation, defined as inflammation of nervous tissue, is considered a major factor in the death of RGCs and their axons in the optic nerve [126, 127].”
Background
Molecular regulation of neuroinflammation in glaucoma: Current knowledge and the ongoing search for new treatment targets
Tezel, G. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.100998 · Cited by 172 · see citing works
GLP-1 Receptor Agonist NLY01 Reduces Retinal Inflammation and Neuron Death Secondary to Ocular Hypertension
Sterling, J. K., Adetunji, M. O., Guttha, S., Bargoud, A. R., Uyhazi, K. E., Ross, A. G., Dunaief, J. L., & Cui, Q. N. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108271 · Cited by 148 · see citing works
SARM1 acts downstream of neuroinflammatory and necroptotic signaling to induce axon degeneration
Ko, K. W., Milbrandt, J., & DiAntonio, A. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.201912047 · Cited by 133 · see citing works
Disturbed glucose and pyruvate metabolism in glaucoma with neuroprotection by pyruvate or rapamycin
Harder, J. M., Guymer, C., Wood, J. P. M., Daskalaki, E., Chidlow, G., Zhang, C., Balasubramanian, R., Cardozo, B. H., Foxworth, N. E., Deering, K. E., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2014213117 · Cited by 127 · see citing works
Self-citation
Targets of Neuroprotection in Glaucoma
He, S., Stankowska, D. L., Ellis, D. Z., Krishnamoorthy, R. R., & Yorio, T. (2017) · Journal of Ocular Pharmacology and Therapeutics · doi:10.1089/jop.2017.0041 · Cited by 132 · see citing works
“Increasingly, it has been proposed that a neuroinflammation component may play an important role in the progression of glaucoma.(77) In animal models, intravitreal injection of TNF-a mimics glaucomatous damage in control mice(73) and an inhibitor of TNF-a prevents RGC loss in a rat model of glaucoma.”
Background
Apolipoprotein E4 impairs the response of neurodegenerative retinal microglia and prevents neuronal loss in glaucoma
Margeta, M. A., Yin, Z., Madore, C., Pitts, K. M., Letcher, S. M., Tang, J., Jiang, S., Gauthier, C. D., Silveira, S. R., Schroeder, C. M., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.07.014 · Cited by 130 · see citing works
Activation of retinal glial cells contributes to the degeneration of ganglion cells in experimental glaucoma
Miao, Y., Zhao, G., Cheng, S., Wang, Z., & Yang, X.-L. (2023) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2023.101169 · Cited by 124 · see citing works
Glial Cells in Glaucoma: Friends, Foes, and Potential Therapeutic Targets
García-Bermúdez, M. Y., Freude, K., Mouhammad, Z. A., van Wijngaarden, P., Martin, K., & Kolko, M. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.624983 · Cited by 108 · see citing works
Complement C3-Targeted Gene Therapy Restricts Onset and Progression of Neurodegeneration in Chronic Mouse Glaucoma
Bosco, A., Anderson, S., Breen, K., Romero, C. O., Steele, M. R., Chiodo, V. A., Boye, S. L., Hauswirth, W. W., Tomlinson, S., & Vetter, M. L. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.08.017 · Cited by 110 · see citing works
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Complement Targets Newborn Retinal Ganglion Cells for Phagocytic Elimination by Microglia
Anderson, S., Zhang, J., Steele, M. R., Romero, C. O., Kautzman, A. G., Schafer, D. P., & Vetter, M. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1854-18.2018 · Cited by 106 · see citing works
“Complement is upregulated early and implicated in driving pathology in various contexts of injury and neurodegeneration (Bonifati and Kishore, 2007; Zabel and Kirsch, 2013), including glaucoma, which is the progressive decline and loss of RGCs (Soto and Howell, 2014; Williams et al., 2017).”
Background
Neuroinflammation in Primary Open-Angle Glaucoma
Vernazza, S., Tirendi, S., Bassi, A. M., Traverso, C. E., & Saccà, S. C. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9103172 · Cited by 104 · see citing works
“In the CNS, the term “neuroinflammation” refers mainly to microglial activation but also to astrocytes response, without there being necessarily leukocyte influx from the blood [341].”
Background
Investigations into Hypoxia and Oxidative Stress at the Optic Nerve Head in a Rat Model of Glaucoma
Chidlow, G., Wood, J. P. M., & Casson, R. J. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00478 · Cited by 99 · see citing works
“…the tissue volume—a much greater percentage than in the myelinated optic nerve (Skoff et al., 1986)—and they likely have a significant influence upon the progression of glaucoma, whether supporting axonal survival or contributing to neuroinflammation (Soto andHowell, 2014; Williams et al., 2017).”
Background
Mechanisms of Drug Resistance in the Pathogenesis of Epilepsy: Role of Neuroinflammation. A Literature Review
Бажанова, Е. Д., Kozlov, А. А., & Litovchenko, A. V. (2021) · Brain Sciences · doi:10.3390/brainsci11050663 · Cited by 92 · see citing works
Absence of TGFβ signaling in retinal microglia induces retinal degeneration and exacerbates choroidal neovascularization
Ma, W., Silverman, S. M., Zhao, L., Villasmil, R., Campos, M. M., Amaral, J., & Wong, W. T. (2019) · eLife · doi:10.7554/elife.42049 · Cited by 85 · see citing works
Taurine and oxidative stress in retinal health and disease
Castelli, V., Paladini, A., d’Angelo, M., Allegretti, M., Mantelli, F., Brandolini, L., Cocchiaro, P., Cimini, A., & Varrassi, G. (2021) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13610 · Cited by 81 · see citing works
Inhibition of monocyte-like cell extravasation protects from neurodegeneration in DBA/2J glaucoma
Williams, P. A., Braine, C., Kizhatil, K., Foxworth, N. E., Tolman, N. G., Harder, J. M., Scott, R. A., Sousa, G. L., Panitch, A., Howell, G. R., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0303-3 · Cited by 79 · see citing works
“Neuroinflammation may be a critical, and treatable, pathogenic event in glaucoma [3].”
BackgroundSelf-citation
Glaucoma Clinical Research: Trends in Treatment Strategies and Drug Development
Storgaard, L. H., Tran, T. L., Freiberg, J. C., Hauser, A. S., & Kolko, M. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.733080 · Cited by 80 · see citing works
Glucagon-like peptide 1 receptor agonist use is associated with reduced risk for glaucoma
Sterling, J., Hua, P., Dunaief, J. L., Cui, Q. N., & VanderBeek, B. L. (2023) · British Journal of Ophthalmology · doi:10.1136/bjophthalmol-2021-319232 · Cited by 75 · see citing works
The Role of Endogenous Neuroprotective Mechanisms in the Prevention of Retinal Ganglion Cells Degeneration
Pietrucha‐Dutczak, M., Amadio, M., Govoni, S. M., Lewin‐Kowalik, J., & Smędowski, A. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00834 · Cited by 74 · see citing works
AMPK hyperactivation promotes dendrite retraction, synaptic loss, and neuronal dysfunction in glaucoma
Belforte, N., Agostinone, J., Alarcon-Martinez, L., Villafranca-Baughman, D., Dotigny, F., Cueva Vargas, J. L., & Di Polo, A. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00466-z · Cited by 67 · see citing works
“Early changes at the optic nerve head (ONH), including infiltrating cells and reactive astrocytes, have been propose to contribute to RGC damage in glaucoma [51].”
Background
Therapeutic Drugs and Devices for Tackling Ocular Hypertension and Glaucoma, and Need for Neuroprotection and Cytoprotective Therapies
Sharif, N. A. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.729249 · Cited by 74 · see citing works
Recent advances of smart materials for ocular drug delivery
Wang, X., Luan, F., Yue, H., Song, C., Wang, S., Feng, J., Zhang, X., Yang, W. H., Li, Y., Wei, W., et al. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.115006 · Cited by 69 · see citing works
Targeting the NLRP3 Inflammasome in Glaucoma
Coyle, S., Khan, M. N., Chemaly, M., Callaghan, B., Doyle, C., Willoughby, C. E., Atkinson, S. D., Gregory-Ksander, M. S., & McGilligan, V. (2021) · Biomolecules · doi:10.3390/biom11081239 · Cited by 68 · see citing works
“Inflammation in glaucoma primarily occurs in the retina and ONH [21].”
Background
Retinal Ganglion Cell Survival and Axon Regeneration after Optic Nerve Injury: Role of Inflammation and Other Factors
Wong, K. A., & Benowitz, L. I. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231710179 · Cited by 66 · see citing works
Time course of bilateral microglial activation in a mouse model of laser-induced glaucoma
Ramirez, A. I., de Hoz, R., Fernández‐Albarral, J. A., Salobrar‐García, E., Rojas, B., Valiente‐Soriano, F. J., Avilés‐Trigueros, M., Villegas‐Pérez, M. P., Vidal‐Sanz, M., Triviño, A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-61848-9 · Cited by 69 · see citing works
The role of pyroptosis in inflammatory diseases
Chai, R., Li, Y., Shui, L., Ni, L., & Zhang, A. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1173235 · Cited by 67 · see citing works
“Inflammation occurs primarily in the optic nerve head tissue and retina tissue, which show an accumulation of activated astrocytes and microglia, along with high levels of IL-1β (Bordone et al., 2017; Williams et al., 2017).”
Background
Multifactorial Pathogenic Processes of Retinal Ganglion Cell Degeneration in Glaucoma towards Multi-Target Strategies for Broader Treatment Effects
Tezel, G. (2021) · Cells · doi:10.3390/cells10061372 · Cited by 68 · see citing works
Smart nano-micro platforms for ophthalmological applications: The state-of-the-art and future perspectives
Lyu, Q., Peng, L., Hong, X., Fan, T., Li, J., Cui, Y., Zhang, H., & Zhao, J. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120682 · Cited by 65 · see citing works
Short chain fatty acids inhibit endotoxin-induced uveitis and inflammatory responses of retinal astrocytes
Chen, N., Wu, J., Wang, J., Piri, N., Chen, F., Xiao, T., Zhao, Y., Sun, D., Kaplan, H. J., & Shao, H. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2021.108520 · Cited by 66 · see citing works
Transgenic inhibition of astroglial NF-κB restrains the neuroinflammatory and neurodegenerative outcomes of experimental mouse glaucoma
Yang, X., Zeng, Q., Barış, M. E., & Tezel, G. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01930-1 · Cited by 64 · see citing works
A lncRNA-encoded mitochondrial micropeptide exacerbates microglia-mediated neuroinflammation in retinal ischemia/reperfusion injury
Zheng, X., Wang, M., Liu, S., Chen, H., Li, Y., Yuan, F., Yang, L., Qiu, S., Wang, H., Xie, Z., et al. (2023) · Cell Death and Disease · doi:10.1038/s41419-023-05617-2 · Cited by 65 · see citing works
“Retinal IR causes inflammation by activating resident microglia [83, 84] and 181-Rik clearly regulates this activation process because: (1) in IR-treated 181-Rik KO mice, we observed obviously fewer activated microglia in both the retina and optic nerve.”
Background
The Role of Neuroinflammation in Glaucoma: An Update on Molecular Mechanisms and New Therapeutic Options
Rolle, T., Ponzetto, A., & Malinverni, L. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2020.612422 · Cited by 65 · see citing works
Risk Factors for Retinal Ganglion Cell Distress in Glaucoma and Neuroprotective Potential Intervention
Vernazza, S., Oddone, F., Tirendi, S., & Bassi, A. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157994 · Cited by 65 · see citing works
“Furthermore, it would seem that some proteins belonging to the Complement system, including C1q, C3 and C4, are mainly up-regulated at both the optic nerve head (ONH) and the inner plexiform layer in the early stages of glaucoma degeneration [5,125].”
Background
T-Lymphocyte Subset Distribution and Activity in Patients With Glaucoma
Yang, X., Zeng, Q., Göktaş, E., Gopal, K., Al‐Aswad, L. A., Blumberg, D. M., Cioffi, G. A., Liebmann, J. M., & Tezel, G. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-26129 · Cited by 58 · see citing works
The Interaction Between Microglia and Macroglia in Glaucoma
Zhao, X., Sun, R., Luo, X., Wang, F., & Sun, X. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.610788 · Cited by 56 · see citing works
Visions of Eye Commensals: The Known and the Unknown About How the Microbiome Affects Eye Disease
Leger, A. J. S., & Caspi, R. R. (2018) · BioEssays · doi:10.1002/bies.201800046 · Cited by 56 · see citing works
The role of microglia in the progression of glaucomatous neurodegeneration- a review
Zeng, H.-L., & Shi, J. (2018) · International Journal of Ophthalmology · doi:10.18240/ijo.2018.01.22 · Cited by 55 · see citing works
Ocular hypertension suppresses homeostatic gene expression in optic nerve head microglia of DBA/2 J mice
Tribble, J. R., Harder, J. M., Williams, P. A., & John, S. W. M. (2020) · Molecular Brain · doi:10.1186/s13041-020-00603-7 · Cited by 55 · see citing works
“microglia in regulating neuroinflammation (such as in Alzheimer’s disease [8–11]), identifying any dysregulation of microglia is of paramount importance for the development of neuroprotective treatments [12].”
BackgroundSelf-citation
When Is a Control Not a Control? Reactive Microglia Occur Throughout the Control Contralateral Pathway of Retinal Ganglion Cell Projections in Experimental Glaucoma
Tribble, J. R., Kokkali, E., Otmani, A., Plastino, F., Lardner, E., Vohra, R., Kolko, M., André, H., Morgan, J. E., & Williams, P. A. (2021) · Translational Vision Science & Technology · doi:10.1167/tvst.10.1.22 · Cited by 53 · see citing works
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Targeting Diet and Exercise for Neuroprotection and Neurorecovery in Glaucoma
Tribble, J. R., Hui, F., Jöe, M., Bell, K. C., Chrysostomou, V., Crowston, J. G., & Williams, P. A. (2021) · Cells · doi:10.3390/cells10020295 · Cited by 55 · see citing works
“These include the regulation of vasculature tone [15], oxygen demand [16], and inflammation [17], which will not be reviewed here, but are likely to be important in the context of glaucoma and glaucoma management.”
BackgroundSelf-citation
A neuroglia-based interpretation of glaucomatous neuroretinal rim thinning in the optic nerve head
Lee, E. J., Han, J. C., Park, D. Y., & Kee, C. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100840 · Cited by 54 · see citing works
CCL2-mediated inflammatory pathogenesis underlies high myopia-related anxiety
Zhu, X., Meng, J., Han, C., Wu, Q., Du, Y., Qi, J., Wei, L., Li, H., He, W., Zhang, K., et al. (2023) · Cell Discovery · doi:10.1038/s41421-023-00588-2 · Cited by 52 · see citing works
Novel Therapeutics in Glaucoma Management
Bucolo, C., Platania, C. B. M., Drago, F., Bonfiglio, V. M. E., Reibaldi, M., Avitabile, T., & Uva, M. G. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666170915142727 · Cited by 52 · see citing works
“It is noteworthy that δopioid receptor activation can counteract neuroinflammation [68], which is detrimental to RGCs function and progression of glaucoma [69, 70].”
Background
P2X7 receptor antagonism preserves retinal ganglion cells in glaucomatous mice
Romano, G. L., Amato, R., Lazzara, F., Porciatti, V., Chou, T.-H., Drago, F., & Bucolo, C. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114199 · Cited by 51 · see citing works
CD163+ macrophages infiltrate axon bundles of postmortem optic nerves with glaucoma
Margeta, M. A., Lad, E. M., & Proia, A. D. (2018) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-018-4081-y · Cited by 49 · see citing works
Developmental roles of microglia: A window into mechanisms of disease
Anderson, S., & Vetter, M. L. (2018) · Developmental Dynamics · doi:10.1002/dvdy.1 · Cited by 50 · see citing works
AIBP protects retinal ganglion cells against neuroinflammation and mitochondrial dysfunction in glaucomatous neurodegeneration
Choi, S., Keun-young Kim, A., Perkins, G. A., Phan, S., Edwards, G., Xia, Y., Kim, J., Skowronska‐Krawczyk, D., Weinreb, R. N., Ellisman, M. H., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101703 · Cited by 50 · see citing works
Soluble tumor necrosis factor-alpha-induced hyperexcitability contributes to retinal ganglion cell apoptosis by enhancing Nav1.6 in experimental glaucoma
Cheng, S., Wang, H., Xu, L., Li, F., Miao, Y., Lei, B., Sun, X., & Wang, Z. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02236-6 · Cited by 50 · see citing works
Pyroptosis: A New Insight Into Eye Disease Therapy
Zhang, Y., Jiao, Y., Li, X., Gao, S., Zhou, N., Duan, J., & Zhang, M. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.797110 · Cited by 50 · see citing works
“Inflammation activation primarily occurs in the optic nerve head (ONH) and retina, in which activated astrocytes, activated microglia, and proinflammatory cytokines (IL-1β) are detected (Sun et al., 2013; Bordone et al., 2017; Williams et al., 2017).”
Background
Measurable Aspects of the Retinal Neurovascular Unit in Diabetes, Glaucoma, and Controls
Spaide, R. F. (2019) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2019.04.035 · Cited by 45 · see citing works
Glial Cell Activation and Immune Responses in Glaucoma: A Systematic Review of Human Postmortem Studies of the Retina and Optic Nerve
Salkar, A., Wall, R. V., Basavarajappa, D. K., Chitranshi, N., Parrilla, G. E., Mirzaei, M., Yan, P., Graham, S. L., & You, Y. (2024) · Aging and Disease · doi:10.14336/ad.2024.0103 · Cited by 43 · see citing works
“Moreover, neuro-inflammation may affect synaptic disruptions within the retina [3].”
Lactate: More Than Merely a Metabolic Waste Product in the Inner Retina
Vohra, R., & Kolko, M. (2020) · Molecular Neurobiology · doi:10.1007/s12035-019-01863-8 · Cited by 40 · see citing works
Transplantation of iPSC-TM stimulates division of trabecular meshwork cells in human eyes
Zhu, W., Godwin, C. R., Cheng, L. Z., Scheetz, T. E., & Kuehn, M. H. (2020) · Scientific Reports · doi:10.1038/s41598-020-59941-0 · Cited by 42 · see citing works
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MicroRNA-93/STAT3 signalling pathway mediates retinal microglial activation and protects retinal ganglion cells in an acute ocular hypertension model
Wang, Y., Chen, S., Wang, J., Liu, Y., Chen, Y., Wen, T., Fang, X., Vidal‐Sanz, M., Jonas, J. B., & Zhang, X. (2021) · Cell Death and Disease · doi:10.1038/s41419-020-03337-5 · Cited by 43 · see citing works
Interleukin-4 promotes microglial polarization toward a neuroprotective phenotype after retinal ischemia/reperfusion injury
Xu, L., Guo, W., Chen, D., Peng, C., Ding, X.-M., Wu, Y., & Zeng, C. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.339500 · Cited by 41 · see citing works
“Subsequently, these complexes initiate tyrosine phosphorylation of STAT6 and activate the classical STAT6 signaling cascades to support M2 activation (Murray et al., 2014; Han et al., 2015; Xiong et al., 2015).”
Background
Protective effect of the natural flavonoid naringenin in mouse models of retinal injury
Zeng, L., Qian, Y., Lou, H., Wang, F., Pang, Y., Hu, H., Zhang, Z., Song, Y., Liu, P., & Zhang, X. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.176231 · Cited by 40 · see citing works
Eye Drops of Metformin Prevents Fibrosis After Glaucoma Filtration Surgery in Rats via Activating AMPK/Nrf2 Signaling Pathway
Li, X., Leng, Y., Jiang, Q., Wang, Z., Luo, P., Zhang, C., Chen, L., Wang, Y., Wang, H., Yue, X., et al. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.01038 · Cited by 39 · see citing works
“Glaucoma is the leading cause of irreversible blindness and reduces the vision-related quality of life worldwide (Crish and Calkins, 2015; Williams et al., 2017).”
Background
Microbiome Dysbiosis: A Pathological Mechanism at the Intersection of Obesity and Glaucoma
Pezzino, S., Sofia, M., Greco, L. P., Litrico, G., Filippello, G., Sarvà, I., Greca, G. L., & Latteri, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021166 · Cited by 39 · see citing works
“Increased IOP is only one factor in the development of glaucoma; other factors include neuroinflammation [30,31], decreased ocular blood flow [36,37], ocular vascular dysregulation [36,38], and changes in systemic blood pressure [39,40].”
Background
Metabolic Syndrome Is Associated With Ocular Hypertension and Glaucoma
Roddy, G. W. (2020) · Journal of Glaucoma · doi:10.1097/ijg.0000000000001593 · Cited by 39 · see citing works
Cannabidiol and the Canonical WNT/β-Catenin Pathway in Glaucoma
Vallée, A., Lecarpentier, Y., & Vallée, J.-N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073798 · Cited by 40 · see citing works
“Pathogenic processes of the neurodegenerative mechanism lead to mechanical and vascular stress enhancing mitochondrial dysregulation, chronic oxidative stress (OS) and metabolic stress [10,11], excitotoxicity [12], and neuroinflammation [13,14].”
Background
Association of systemic inflammation indices with visual field loss progression in patients with primary angle-closure glaucoma: potential biomarkers for 3P medical approaches
Li, S.-J., Qiu, Y., Yu, J., Shao, M., Li, Y.-Z., Cao, W.-J., & Sun, X.-H. (2021) · The EPMA Journal · doi:10.1007/s13167-021-00260-3 · Cited by 33 · see citing works
Remodeling of the Lamina Cribrosa: Mechanisms and Potential Therapeutic Approaches for Glaucoma
Strickland, R. G., Garner, M. A., Gross, A. K., & Girkin, C. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158068 · Cited by 40 · see citing works
Sub-region-Specific Optic Nerve Head Glial Activation in Glaucoma
Oikawa, K., Hoeve, J. N. V., Teixeira, L. B. C., Snyder, K. C., Kiland, J. A., Ellinwood, N. M., & McLellan, G. J. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01910-9 · Cited by 37 · see citing works
GlyCAM1 negatively regulates monocyte entry into the optic nerve head and contributes to radiation-based protection in glaucoma
Williams, P. A., Braine, C., Foxworth, N. E., Cochran, K. E., & John, S. W. M. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0868-8 · Cited by 36 · see citing works
“Thus, and although there is evidence for infiltrating immune cells and immune cell activation in multiple models of glaucoma [3, 5, 58–62], additional work is required to definitively establish their function and to extend these studies to other models of glaucoma and human glaucoma [54].”
Self-citation
Is primary open-angle glaucoma an ocular manifestation of systemic disease?
Wey, S., Amanullah, S., Spaeth, G. L., Ustaoğlu, M., Rahmatnejad, K., & Katz, L. J. (2019) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-019-04239-9 · Cited by 36 · see citing works
Astrocyte polarization in glaucoma: a new opportunity
Sun, H., Guo, W., & Liu, Y. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.339470 · Cited by 37 · see citing works
“Glial cells (microglia and astrocytes) are resident immune monitoring cells in neuroinflammation (Soto and Howell, 2014; Williams et al., 2017).”
Background
Loss of the Extracellular Matrix Molecule Tenascin-C Leads to Absence of Reactive Gliosis and Promotes Anti-inflammatory Cytokine Expression in an Autoimmune Glaucoma Mouse Model
Wiemann, S., Reinhard, J., Reinehr, S., Cibir, Z., Joachim, S. C., & Faissner, A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.566279 · Cited by 33 · see citing works
“Neuroinflammatory changes in the retina occur during glaucomatous damage (Williams et al., 2017).”
Background
Restoring the oxidative balance in age-related diseases – An approach in glaucoma
Cáceres‐Vélez, P. R., Hui, F., Hercus, J., Bui, B. V., & Jusuf, P. R. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101572 · Cited by 34 · see citing works
Valproic Acid Reduces Neuroinflammation to Provide Retinal Ganglion Cell Neuroprotection in the Retina Axotomy Model
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Authors: Williams, P. A., Marsh-Armstrong, N., Howell, G. R., Bosco, A., Danias, J., Simon, J., Di Polo, A., Kuehn, M. H., Przedborski, S., Raff, M., & Trounce, I.
Affiliations: Jackson Laboratory (US)
Kennedy Krieger Institute (US)
Tufts University (US)
University of Utah (US)
SUNY Downstate Health Sciences University (US)
University of Iowa (US)
Columbia University Irving Medical Center (US)
MRC Laboratory for Molecular Cell Biology (GB)
The University of Melbourne (AU)
Corresponding author: Howell, Gareth R.
ORCID: Williams, Pete A.
Howell, Gareth R.
Bosco, Alejandra
Kuehn, Markus H.
Przedborski, Serge
Trounce, Ian
Venue: Experimental Eye Research
Publisher: Elsevier BV
Published: 2017-04
Volume: 157
Pages: 20-27
ISSN: 0014-4835 (ISSN-L)
DOI: 10.1016/j.exer.2017.02.014
PMC: PMC5497582
OpenAlex: W2590373630
Cited by: 253
References: 106
Citations by year: 2026: 20 · 2025: 16 · 2024: 25 · 2023: 33 · 2022: 31 · 2021: 48 · 2020: 37 · 2019: 18 · 2018: 14 · 2017: 10
FWCI: 3.96
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Experimental Eye Research (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: National Eye Institute (R01EY021525)
Topics: Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
Keywords: neuroinflammation, glaucoma, glaucomatous neurodegeneration, optic nerve head, retina, astrocytes, microglia, peripheral immune cells, inflammatory signaling, Alzheimer's disease, neurodegeneration
MeSH terms: Animals, Astrocytes, Glaucoma, Humans, Inflammation, Optic Nerve, Optic Neuritis, Retinal Ganglion Cells

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