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Original Research

Alterations in Peripheral B Cell Subsets Correlate with the Disease Severity of Human Glaucoma

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Pages 4827-4838 | Published online: 21 Sep 2021

References

  • Xie H, Li L, Zhu G, et al. Correction: infiltrated pre-adipocytes increase prostate cancer metastasis via modulation of the miR-301a/androgen receptor (AR)/TGF-β1/Smad/MMP9 signals. Oncotarget. 2016;7:83829–83830. doi:10.18632/oncotarget.13913
  • Tham YC, Li X, Wong TY, et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121:2081–2090. doi:10.1016/j.ophtha.2014.05.013
  • Kass MA, Heuer DK, Higginbotham EJ, et al. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol. 2002;120:701–713; discussion 829–730. doi:10.1001/archopht.120.6.701
  • Lichter PR, Musch DC, Gillespie BW, et al. Interim clinical outcomes in the Collaborative Initial Glaucoma Treatment Study comparing initial treatment randomized to medications or surgery. Ophthalmology. 2001;108:1943–1953. doi:10.1016/S0161-6420(01)00873-9
  • Heijl A, Leske MC, Bengtsson B, et al. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol. 2002;120:1268–1279. doi:10.1001/archopht.120.10.1268
  • Adornetto A, Russo R, Parisi V. Neuroinflammation as a target for glaucoma therapy. Neural Regen Res. 2019;14:391–394. doi:10.4103/1673-5374.245465
  • Bell K, Und Hohenstein-Blaul NVT, Teister J, Grus F. Modulation of the immune system for the treatment of glaucoma. Curr Neuropharmacol. 2018;16:942–958. doi:10.2174/1570159X15666170720094529
  • Yanagi M, Kawasaki R, Wang JJ, et al. Vascular risk factors in glaucoma: a review. Clin Exp Ophthalmol. 2011;39:252–258. doi:10.1111/j.1442-9071.2010.02455.x
  • Marcus MW, de Vries MM, Junoy Montolio FG, Jansonius NM. Myopia as a risk factor for open-angle glaucoma: a systematic review and meta-analysis. Ophthalmology. 2011;118:1989–1994 e1982. doi:10.1016/j.ophtha.2011.03.012
  • Shen L, Melles RB, Metlapally R, et al. The association of refractive error with glaucoma in a multiethnic population. Ophthalmology. 2016;123:92–101. doi:10.1016/j.ophtha.2015.07.002
  • Tezel G, Yang X, Luo C, et al. Oxidative stress and the regulation of complement activation in human glaucoma. Invest Ophthalmol Vis Sci. 2010;51:5071–5082. doi:10.1167/iovs.10-5289
  • Williams PA, Marsh-Armstrong N, Howell GR, et al. Neuroinflammation in glaucoma: a new opportunity. Exp Eye Res. 2017;157:20–27. doi:10.1016/j.exer.2017.02.014
  • Ramirez AI, de Hoz R, Salobrar-Garcia E, et al. The role of microglia in retinal neurodegeneration: Alzheimer’s disease, Parkinson, and glaucoma. Front Aging Neurosci. 2017;9:214.
  • Jiang S, Kametani M, Chen DF. Adaptive immunity: new aspects of pathogenesis underlying neurodegeneration in glaucoma and optic neuropathy. Front Immunol. 2020;11:65. doi:10.3389/fimmu.2020.00065
  • Gramlich OW, Ding QJ, Zhu W, et al. Adoptive transfer of immune cells from glaucomatous mice provokes retinal ganglion cell loss in recipients. Acta Neuropathol Commun. 2015;3:56. doi:10.1186/s40478-015-0234-y
  • Wax MB, Barrett DA, Pestronk A. Increased incidence of paraproteinemia and autoantibodies in patients with normal-pressure glaucoma. Am J Ophthalmol. 1994;117:561–568. doi:10.1016/S0002-9394(14)70059-5
  • Wax MB, Tezel G, Saito I, et al. Anti-Ro/SS-a positivity and heat shock protein antibodies in patients with normal-pressure glaucoma. Am J Ophthalmol. 1998;125:145–157. doi:10.1016/S0002-9394(99)80084-1
  • Wax MB, Tezel G, Kawase K, Kitazawa Y. Serum autoantibodies to heat shock proteins in glaucoma patients from Japan and the United States. Ophthalmology. 2001;108:296–302. doi:10.1016/S0161-6420(00)00525-X
  • Rizzo MI, Greco A, De Virgilio A, et al. Glaucoma: recent advances in the involvement of autoimmunity. Immunol Res. 2017;65:207–217. doi:10.1007/s12026-016-8837-3
  • Joachim SC, Bruns K, Lackner KJ, Pfeiffer N, Grus FH. Antibodies to alpha B-crystallin, vimentin, and heat shock protein 70 in aqueous humor of patients with normal tension glaucoma and IgG antibody patterns against retinal antigen in aqueous humor. Curr Eye Res. 2007;32:501–509. doi:10.1080/02713680701375183
  • Grus FH, Joachim SC, Bruns K, et al. Serum autoantibodies to alpha-fodrin are present in glaucoma patients from Germany and the United States. Invest Ophthalmol Vis Sci. 2006;47:968–976. doi:10.1167/iovs.05-0685
  • Joachim SC, Reichelt J, Berneiser S, Pfeiffer N, Grus FH. Sera of glaucoma patients show autoantibodies against myelin basic protein and complex autoantibody profiles against human optic nerve antigens. Graefes Arch Clin Exp Ophthalmol. 2008;246:573–580. doi:10.1007/s00417-007-0737-8
  • Tezel G, Seigel GM, Wax MB. Autoantibodies to small heat shock proteins in glaucoma. Invest Ophthalmol Vis Sci. 1998;39:2277–2287.
  • Wax MB, Tezel G, Edward PD. Clinical and ocular histopathological findings in a patient with normal-pressure glaucoma. Arch Ophthalmol. 1998;116:993–1001. doi:10.1001/archopht.116.8.993
  • Gramlich OW, Beck S, von Thun Und Hohenstein-blaul N, et al. Enhanced insight into the autoimmune component of glaucoma: igG autoantibody accumulation and pro-inflammatory conditions in human glaucomatous retina. PLoS One. 2013;8:e57557. doi:10.1371/journal.pone.0057557
  • Wax MB, Tezel G, Yang J, et al. Induced autoimmunity to heat shock proteins elicits glaucomatous loss of retinal ganglion cell neurons via activated T-cell-derived fas-ligand. J Neurosci. 2008;28:12085–12096. doi:10.1523/JNEUROSCI.3200-08.2008
  • Joachim SC, Grus FH, Kraft D, et al. Complex antibody profile changes in an experimental autoimmune glaucoma animal model. Invest Ophthalmol Vis Sci. 2009;50:4734–4742. doi:10.1167/iovs.08-3144
  • Joachim SC, Wax MB, Seidel P, Pfeiffer N, Grus FH. Enhanced characterization of serum autoantibody reactivity following HSP 60 immunization in a rat model of experimental autoimmune glaucoma. Curr Eye Res. 2010;35:900–908. doi:10.3109/02713683.2010.495829
  • Joachim SC, Gramlich OW, Laspas P, et al. Retinal ganglion cell loss is accompanied by antibody depositions and increased levels of microglia after immunization with retinal antigens. PLoS One. 2012;7:e40616. doi:10.1371/journal.pone.0040616
  • Laspas P, Gramlich OW, Müller HD, et al. Autoreactive antibodies and loss of retinal ganglion cells in rats induced by immunization with ocular antigens. Invest Ophthalmol Vis Sci. 2011;52:8835–8848. doi:10.1167/iovs.10-6889
  • Noristani R, Kuehn S, Stute G, et al. Retinal and optic nerve damage is associated with early glial responses in an experimental autoimmune glaucoma model. J Mol Neurosci. 2016;58:470–482. doi:10.1007/s12031-015-0707-2
  • Bell K, Wilding C, Funke S, Pfeiffer N, Grus FH. Protective effect of 14-3-3 antibodies on stressed neuroretinal cells via the mitochondrial apoptosis pathway. BMC Ophthalmol. 2015;15:64. doi:10.1186/s12886-015-0044-9
  • Wilding C, Bell K, Beck S, et al. γ-Synuclein antibodies have neuroprotective potential on neuroretinal cells via proteins of the mitochondrial apoptosis pathway. PLoS One. 2014;9:e90737. doi:10.1371/journal.pone.0090737
  • Chen CL, Bojikian KD, Wen JC, et al. Peripapillary retinal nerve fiber layer vascular microcirculation in eyes with glaucoma and single-hemifield visual field loss. JAMA Ophthalmol. 2017;135:461–468. doi:10.1001/jamaophthalmol.2017.0261
  • He C, Shi Y, Wu R, et al. miR-301a promotes intestinal mucosal inflammation through induction of IL-17A and TNF-alpha in IBD. Gut. 2016;65:1938–1950. doi:10.1136/gutjnl-2015-309389
  • Forestier A, Guerrier T, Jouvray M, et al. Altered B lymphocyte homeostasis and functions in systemic sclerosis. Autoimmun Rev. 2018;17:244–255. doi:10.1016/j.autrev.2017.10.015
  • Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med. 1998;188:1679–1689. doi:10.1084/jem.188.9.1679
  • Li S, Ma F, Hao H, et al. Marked elevation of circulating CD19(+)CD38(hi)CD24(hi) transitional B cells give protection against neonatal sepsis. Pediatr Neonatol. 2018;59:296–304. doi:10.1016/j.pedneo.2017.10.005
  • Piper CJM, Wilkinson MGL, Deakin CT, et al. CD19(+)CD24(hi)CD38(hi) B cells are expanded in juvenile dermatomyositis and exhibit a pro-inflammatory phenotype after activation through toll-like receptor 7 and interferon-alpha. Front Immunol. 2018;9:1372. doi:10.3389/fimmu.2018.01372
  • Sambleben C, Knudsen AD, Hartling HJ, Nielsen CH, Nielsen SD. Increased proportions of B cells with spontaneous production of interleukin-10 in HIV-infected individuals are normalized during combination antiretroviral therapy: a longitudinal study. APMIS. 2018;126:143–151. doi:10.1111/apm.12795
  • Giltiay NV, Giordano D, Clark EA. The plasticity of newly formed B cells. J Immunol. 2019;203:3095–3104. doi:10.4049/jimmunol.1900928
  • Sosa-Hernandez VA, Torres-Ruíz J, Cervantes-Díaz R, et al. B cell subsets as severity-associated signatures in COVID-19 patients. Front Immunol. 2020;11:611004. doi:10.3389/fimmu.2020.611004
  • Oliviero B, Varchetta S, Mele D, et al. Expansion of atypical memory B cells is a prominent feature of COVID-19. Cell Mol Immunol. 2020;17:1101–1103. doi:10.1038/s41423-020-00542-2
  • De Biasi S, Lo Tartaro D, Meschiari M, et al. Expansion of plasmablasts and loss of memory B cells in peripheral blood from COVID-19 patients with pneumonia. Eur J Immunol. 2020;50:1283–1294. doi:10.1002/eji.202048838
  • Anderson MG, Libby RT, Gould DB, Smith RS, John SW. High-dose radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma. Proc Natl Acad Sci U S A. 2005;102:4566–4571. doi:10.1073/pnas.0407357102
  • Chen H, Cho K-S, Vu THK, et al. Commensal microflora-induced T cell responses mediate progressive neurodegeneration in glaucoma. Nat Commun. 2018;9:3209. doi:10.1038/s41467-018-05681-9
  • Yang X, Zeng Q, Göktas E, et al. T-lymphocyte subset distribution and activity in patients with glaucoma. Invest Ophthalmol Vis Sci. 2019;60:877–888. doi:10.1167/iovs.18-26129
  • Yu H, Yuan L, Yang Y, et al. Increased serum IgA concentration and plasmablast frequency in patients with age-related macular degeneration. Immunobiology. 2016;221:650–656. doi:10.1016/j.imbio.2016.01.004
  • Kalinina Ayuso V, van Dijk MR, de Boer JH. Infiltration of plasma cells in the iris of children with ANA-positive anterior uveitis. Invest Ophthalmol Vis Sci. 2015;56:6770–6778. doi:10.1167/iovs.15-17351
  • Wang RX, Yu C-R, Dambuza IM, et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med. 2014;20:633–641. doi:10.1038/nm.3554
  • Abu El-Asrar AM, Dheyab A, Khatib D, Struyf S, Van Damme J, Opdenakker G. Efficacy of B cell depletion therapy with rituximab in refractory chronic recurrent uveitis associated with Vogt-Koyanagi-Harada disease. Ocul Immunol Inflamm. 2020;1–8. doi:10.1080/09273948.2020.1820531
  • Miserocchi E, Modorati G, Berchicci L, et al. Long-term treatment with rituximab in severe juvenile idiopathic arthritis-associated uveitis. Br J Ophthalmol. 2016;100:782–786. doi:10.1136/bjophthalmol-2015-306790
  • Wiendl M, Becker E, Müller TM, et al. Targeting immune cell trafficking - insights from research models and implications for future IBD therapy. Front Immunol. 2021;12:656452. doi:10.3389/fimmu.2021.656452
  • Polman CH, O’Connor PW, Havrdova E, et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med. 2006;354:899–910. doi:10.1056/NEJMoa044397
  • Kappos L, Antel J, Comi G, et al. Oral fingolimod (FTY720) for relapsing multiple sclerosis. N Engl J Med. 2006;355:1124–1140. doi:10.1056/NEJMoa052643
  • Maurer D, Fischer GF, Fae I, et al. IgM and IgG but not cytokine secretion is restricted to the CD27+ B lymphocyte subset. J Immunol. 1992;148:3700–3705.
  • Agematsu K, Hokibara S, Nagumo H, Komiyama A. CD27: a memory B-cell marker. Immunol Today. 2000;21:204–206. doi:10.1016/S0167-5699(00)01605-4
  • Liu YJ, de Bouteiller O, Arpin C, et al. Normal human IgD+IgM- germinal center B cells can express up to 80 mutations in the variable region of their IgD transcripts. Immunity. 1996;4:603–613. doi:10.1016/S1074-7613(00)80486-0
  • Klein U, Kuppers R, Rajewsky K. Human IgM+IgD+ B cells, the major B cell subset in the peripheral blood, express V kappa genes with no or little somatic mutation throughout life. Eur J Immunol. 1993;23:3272–3277. doi:10.1002/eji.1830231232
  • Claes N, Fraussen J, Vanheusden M, et al. Age-associated B cells with proinflammatory characteristics are expanded in a proportion of multiple sclerosis patients. J Immunol. 2016;197:4576–4583. doi:10.4049/jimmunol.1502448
  • Colonna-Romano G, Bulati M, Aquino A, et al. A double-negative (IgD-CD27-) B cell population is increased in the peripheral blood of elderly people. Mech Ageing Dev. 2009;130:681–690. doi:10.1016/j.mad.2009.08.003
  • Fraussen J, Marquez S, Takata K, et al. Phenotypic and Ig repertoire analyses indicate a common origin of IgD− CD27− double negative B cells in healthy individuals and multiple sclerosis patients. J Immunol. 2019;203:1650–1664. doi:10.4049/jimmunol.1801236
  • Wu YC, Kipling D, Dunn-Walters DK. The relationship between CD27 negative and positive B cell populations in human peripheral blood. Front Immunol. 2011;2:81. doi:10.3389/fimmu.2011.00081
  • Bulati M, Buffa S, Candore G, et al. B cells and immunosenescence: a focus on IgG+IgD-CD27- (DN) B cells in aged humans. Ageing Res Rev. 2011;10:274–284. doi:10.1016/j.arr.2010.12.002
  • Wei C, Anolik J, Cappione A, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol. 2007;178:6624–6633. doi:10.4049/jimmunol.178.10.6624
  • Jenks SA, Cashman KS, Zumaquero E, et al. Distinct effector B cells induced by unregulated toll-like receptor 7 contribute to pathogenic responses in systemic lupus erythematosus. Immunity. 2018;49:725–739 e726. doi:10.1016/j.immuni.2018.08.015
  • Richardson C, Chida AS, Adlowitz D, et al. Molecular basis of 9G4 B cell autoreactivity in human systemic lupus erythematosus. J Immunol. 2013;191:4926–4939. doi:10.4049/jimmunol.1202263
  • You X, Zhang R, Shao M, et al. Double negative B cell is associated with renal impairment in systemic lupus erythematosus and acts as a marker for nephritis remission. Front Med (Lausanne). 2020;7:85. doi:10.3389/fmed.2020.00085