The Role of Anti-α-Enolase Autoantibodies in Pathogenicity of Autoimmune-Mediated Retinopathy
Abstract
Autoantibodies against alpha-enolase, a glycolytic enzyme, have been frequently associated with visual loss and retinal degeneration in patients with autoimmune and cancer-associated retinopathy; however their role in the pathogenicity of retinopathy has not been fully explained. Thus, we examined the causative role of anti-enolase antibodies on retinal cells. In the in vitro studies reported here, we found that Enol-1 monoclonal antibody against alpha-enolase significantly inhibited the catalytic function of enolase, which resulted in the depletion of glycolytic ATP. Enol-1 significantly increased intracellular Ca(2+), which led to Bax translocation to the mitochondria, and the release of cytochrome c into the cytoplasm--events that correlated with the initiation of apoptosis. Normal IgG did not induce intracellular calcium or reduce cytosolic ATP. L-type voltage-gated calcium channel blockers (nifedipine, D-cis-diltiazem, and verapamil) were effective in blocking the Ab-induced intracellular Ca(2+) rise and induction of Bax. Based on these findings we propose that chronic access of autoantibodies to the retina results in the inhibition of enolase catalytic function, depletion of ATP, and elevation in intracellular Ca(2+), leading to deregulation of glycolysis in retinal neurons and their destruction.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
All eye tissues except the lens contain antibodies.
“All eye tissues except for the lens contain antibodies, and antibodies have been shown to be capable of mediating ocular pathology in multiple contexts21–25.”
From Investigation of Cas9 Antibodies in the Human Eye (2022) · cites this paper as [22]
Antibodies have been shown to be capable of mediating ocular pathology in multiple contexts.
“All eye tissues except for the lens contain antibodies, and antibodies have been shown to be capable of mediating ocular pathology in multiple contexts21–25.”
From Investigation of Cas9 Antibodies in the Human Eye (2022) · cites this paper as [22]
Cites
The Release of Cytochrome c from Mitochondria: A Primary Site for Bcl-2 Regulation of Apoptosis
Kluck, R. M., Bossy‐Wetzel, E., Green, D. R., & Newmeyer, D. D. (1997) · Science · doi:10.1126/science.275.5303.1132 · Cited by 4,715 · see citing works
Multifunctional α-enolase: its role in diseases
Pancholi, V. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000910 · Cited by 839 · see citing works
Xu, R., Pelicano, H., Zhou, Y. N., Carew, J. S., Feng, L., Bhalla, K. N., Keating, M. J., & Huang, P. (2005) · Cancer Research · doi:10.1158/0008-5472.613.65.2 · Cited by 835 · see citing works
Mechanisms of cytochrome c release by proapoptotic BCL-2 family members
Scorrano, L., & Korsmeyer, S. J. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)00615-6 · Cited by 717 · see citing works
BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis
Danial, N. N., Gramm, C. F., Scorrano, L., Zhang, C.-Y., Krauss, S., Ranger, A. M., Robert Datta, S., Greenberg, M. E., Licklider, L. J., Lowell, B. B., et al. (2003) · Nature · doi:10.1038/nature01825 · Cited by 705 · see citing works
Multifaceted roles of glycolytic enzymes
Kim, J., & Dang, C. V. (2005) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2005.01.005 · Cited by 682 · see citing works
Matrix Metalloproteinase-2 Contributes to Cancer Cell Migration on Collagen
Xu, X., Wang, Y., Chen, Z., Sternlicht, M. D., Hidalgo, M. M., & Steffensen, B. (2005) · Cancer Research · doi:10.1158/0008-5472.130.65.1 · Cited by 414 · see citing works
Rosen, A., & Casciola-Rosen, L. A. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400460 · Cited by 353 · see citing works
Putcha, G. V., Deshmukh, M., & Johnson, E. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07476.1999 · Cited by 310 · see citing works
Functional Coupling Between Glycolysis and Sarcoplasmic Reticulum Ca 2+ Transport
Xu, K. Y., Zweier, J. L., & Becker, L. C. (1995) · Circulation Research · doi:10.1161/01.res.77.1.88 · Cited by 308 · see citing works
Feo, S., Arcuri, D., Piddini, E., Passantino, R., & Giallongo, A. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01494-0 · Cited by 278 · see citing works
Structural Analysis of α-Enolase
Subramanian, A. K., & Miller, D. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.8.5958 · Cited by 265 · see citing works
The Role of an Enolase‐Related Molecule in Plasminogen Binding to Cells
Redlitz, A., Fowler, B. J., Plow, E. F., & Miles, L. A. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20403.x · Cited by 254 · see citing works
Autoantibodies against retinal proteins in paraneoplastic and autoimmune retinopathy
Adamus, G., Ren, G., & Weleber, R. G. (2004) · BMC Ophthalmology · doi:10.1186/1471-2415-4-5 · Cited by 253 · see citing works
Self-citationRetinitis pigmentosa: rod photoreceptor rescue by a calcium-channel blocker in the rd mouse
Frasson, M., Sahel, J., Fabre, M., Simonutti, M., Dreyfus, H., & Picaud, S. A. (1999) · Nature Medicine · doi:10.1038/13508 · Cited by 230 · see citing works
Weleber, R. G., Watzke, R. C., Shults, W. T., Trzupek, K. M., Heckenlively, J. R., Egan, R. A., & Adamus, G. (2005) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2004.12.104 · Cited by 201 · see citing works
Self-citation“Wages of Fear”: transient threefold decrease in intracellular ATP level imposes apoptosis
Izyumov, D. S., Avetisyan, A. V., Pletjushkina, O. Y., Sakharov, D. V., WIRTZ, K. W. A., Chernyak, B. V., & Skulachev, V. P. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.05.007 · Cited by 179 · see citing works
The Occurrence of Serum Autoantibodies against Enolase in Cancer-Associated Retinopathy
Adamus, G., Aptsiauri, N., Guy, J., Heckenlively, J. R., Flannery, J. G., & Hargrave, P. A. (1996) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1996.0021 · Cited by 164 · see citing works
Self-citationMassieu, L., Haces, M. L., Montiel, T., & Hernández‐Fonseca, K. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00266-5 · Cited by 131 · see citing works
Shiraga, S., & Adamus, G. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00314-4 · Cited by 124 · see citing works
Self-citationAutoantibodies specific for alpha-enolase in systemic autoimmune disorders.
Pratesi, F., Moscato, S., Sabbatini, A., CHIMENTI, D., Bombardieri, S., & Migliorini, P. (2000) · PubMed · Cited by 124 · see citing works
Plasminogen Binds Specifically to α‐Enolase on Rat Neuronal Plasma Membrane
Nakajima, K., Hamanoue, M., Takemoto, N., Hattori, T., Kato, K., & Kohsaka, S. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63062048.x · Cited by 122 · see citing works
Adamus, G., Amundson, D., Seigel, G. M., & Machnicki, M. (1998) · Journal of Autoimmunity · doi:10.1006/jaut.1998.0239 · Cited by 119 · see citing works
Self-citationJolodar, A., Fischer, P., Bergmann, S., Büttner, D. W., Hammerschmidt, S., & Brattig, N. W. (2003) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(03)00083-6 · Cited by 115 · see citing works
Maruyama, I., Ohguro, H., & Ikeda, Y. (2000) · PubMed · Cited by 107 · see citing works
Establishment of an e1A-immortalized retinal cell culture
Seigel, G. M. (1996) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/bf02723034 · Cited by 98 · see citing works
Mizukami, Y., Iwamatsu, A., Aki, T., Kimura, M., Nakamura, K., Nao, T., Okusa, T., Matsuzaki, M., Yoshida, K., & Kobayashi, S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402299200 · Cited by 96 · see citing works
Modulation of sarcoplasmic reticulum Ca2+ release by glycolysis in cat atrial myocytes
Kockskämper, J., Zima, A. V., & Blatter, L. A. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.078782 · Cited by 91 · see citing works
Catalase and α-enolase: two novel granulocyte autoantigens in inflammatory bowel disease (IBD)
Roozendaal, C., Zhao, M., Horst, G., Lockwood, C. M., Kleibeuker, J. H., Limburg, P. C., Nelis, G. F., & Kallenberg, C. G. M. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00528.x · Cited by 91 · see citing works
Study of drug effects of calcium channel blockers on retinal degeneration of rd mouse
Takano, Y., Ohguro, H., Dezawa, M., Ishikawa, H., Yamazaki, H., Ohguro, I., Mamiya, K., Metoki, T., Ishikawa, F., & Nakazawa, M. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.12.034 · Cited by 83 · see citing works
Orth, T., Kellner, R., Diekmann, O., Faust, J., BÜSCHENFELDE, K.-H. M. Z., & Mayet, W.-J. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00583.x · Cited by 81 · see citing works
Somatic embryogenesis in plantain banana
Grapin, A., Schwendiman, J., & Teisson, C. (1996) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/bf02823133 · Cited by 80 · see citing works
Alpha-enolase: A novel cytosolic autoantigen in ANCA positive vasculitis
Moodie, F. D. L., Leaker, B. R., Cambridge, G., Totty, N. F., & Segal, A. W. (1993) · Kidney International · doi:10.1038/ki.1993.97 · Cited by 80 · see citing works
Gitlits, V. M., Toh, B., & Sentry, J. W. (2001) · Journal of Investigative Medicine · doi:10.2310/6650.2001.34040 · Cited by 73 · see citing works
High levels of immunoreactive nervous system-specific enolase in sera of patients with neuroblastoma
Ishiguro, Y., Kato, K., Shimizu, A., Ito, T., & Nagaya, M. (1982) · Clinica Chimica Acta · doi:10.1016/0009-8981(82)90056-0 · Cited by 70 · see citing works
Adamus, G., Webb, S., Shiraga, S., & Duvoisin, R. M. (2006) · Journal of Autoimmunity · doi:10.1016/j.jaut.2005.11.007 · Cited by 68 · see citing works
Self-citationLoss of the proapoptotic protein, Bim, breaks B cell anergy
Oliver, P. M., Vass, T., Kappler, J. W., & Marrack, P. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20051407 · Cited by 67 · see citing works
Cellular targets of anti-α-enolase autoantibodies of patients with autoimmune retinopathy
Ren, G., & Adamus, G. (2004) · Journal of Autoimmunity · doi:10.1016/j.jaut.2004.06.003 · Cited by 65 · see citing works
Self-citationNäpänkangas, U., Lindqvist, N., Lindholm, D., & Hallböök, F. (2003) · Molecular Brain Research · doi:10.1016/j.molbrainres.2003.09.016 · Cited by 61 · see citing works
Neuronal gene expression and function in the growth-stimulated R28 retinal precursor cell line
Seigel, G. M., Sun, W., Wang, J., Hershberger, D. H., Campbell, L. M., & Salvi, R. (2004) · Current Eye Research · doi:10.1076/ceyr.28.4.257.27831 · Cited by 60 · see citing works
Anti-α-enolase antibodies in cancer-associated retinopathy with small cell carcinoma of the lung
Dot, C., Guigay, J., & Adamus, G. (2005) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2004.10.044 · Cited by 58 · see citing works
Self-citationSaunders, C., & Limbird, L. E. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.30.19035 · Cited by 57 · see citing works
Fox, D. A., Poblenz, A. T., He, L., Harris, J. B., & Medrano, C. J. (2003) · European Journal of Ophthalmology · doi:10.1177/112067210301303s08 · Cited by 52 · see citing works
Hernández‐Fonseca, K., & Massieu, L. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20631 · Cited by 51 · see citing works
Unique Autoantibody Epitopes in an Immunodominant Region of Thyroid Peroxidase
Arscott, P. L., Koenig, R. J., Kaplan, M. M., Glick, G. D., & Baker, J. R. J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.9.4966 · Cited by 47 · see citing works
Clinical Significance of Serum Antibody Against Neuron-Specific Enolase in Glaucoma Patients
Ikeda, Y. (2002) · Japanese Journal of Ophthalmology · doi:10.1016/s0021-5155(01)00455-5 · Cited by 41 · see citing works
Identification of an autoantibody against alpha-enolase in primary biliary cirrhosis
Akisawa, N., Maeda, T., Iwasaki, S., & Onishi, S. (1997) · Journal of Hepatology · doi:10.1016/s0168-8278(97)80251-6 · Cited by 38 · see citing works
Identification of an Epitope of α-Enolase (a Candidate Plasminogen Receptor) by Phage Display
Arza, B., Félez, J., López‐Alemany, R., Miles, L. A., & Munñoz-Cánoves, P. (1997) · Thrombosis and Haemostasis · doi:10.1055/s-0038-1657693 · Cited by 37 · see citing works
Ohguro, H., Ogawa, K., Maeda, T., Maruyama, I., Maeda, A., Takano, Y., & Nakazawa, M. (2001) · PubMed · Cited by 35 · see citing works
Sato, M., Ohguro, H., Ohguro, I., Mamiya, K., Takano, Y., Yamazaki, H., Metoki, T., Miyagawa, Y., Ishikawa, F., & Nakazawa, M. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01092-1 · Cited by 32 · see citing works
Maruyama, I. (2002) · Japanese Journal of Ophthalmology · doi:10.1016/s0021-5155(01)00453-1 · Cited by 27 · see citing works
Clinical Roles of Serum Autoantibody against Neuron-Specific Enolase in Glaucoma Patients.
Maruyama, I., Ikeda, Y., Nakazawa, M., & Ohguro, H. (2002) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.197.125 · Cited by 26 · see citing works
Hollyfield, J. G., & Rayborn, M. E. (1987) · Experimental Eye Research · doi:10.1016/s0014-4835(87)80119-7 · Cited by 25 · see citing works
Banga, J. P., & McGregor, A. M. (1991) · Autoimmunity · doi:10.3109/08916939109006755 · Cited by 24 · see citing works
Serum Antibodies to Retinal Antigens in Lung Cancer and Sarcoidosis
Jankowska, R., Witkowska, D., Porębska, I., Kuropatwa, M., Kurowska, E., & Gorczyca, W. A. (2004) · Pathobiology · doi:10.1159/000081728 · Cited by 20 · see citing works
Wakabayashi, T., Kosaka, J., & Oshika, T. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03389.x · Cited by 19 · see citing works
Recoverin expression in the R28 retinal precursor cell line
Seigel, G. M., Mutchler, A. L., Adamus, G., & Imperato, E. L. (1997) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-997-0091-5 · Cited by 19 · see citing works
Self-citationEndocytosis in Drosophila: Progress, Possibilities, Prognostications
Narayanan, R., & Ramaswami, M. (2001) · Experimental Cell Research · doi:10.1006/excr.2001.5370 · Cited by 16 · see citing works
Gómez‐Vicente, V., Doonan, F., Donovan, M., & Cotter, T. G. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04990.x · Cited by 11 · see citing works
Tojo, K., Tokuda, T., Yazaki, M., Oide, T., Nakamura, A., Mitsuhashi, S., Kaneko, K., Maruyama, K., Kametani, F., Higuchi, K., et al. (2004) · European Neurology · doi:10.1159/000078547 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bombesin Receptor Antagonists May Be Preferable to Agonists for Tumor Targeting
Cescato, R., Μάινα, Θ., Nock, B. A., Nikolopoulou, A., Charalambidis, D., Piccand, V., & Reubi, J. C. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.107.045054 · Cited by 295 · see citing works
AUTOIMMUNE RETINOPATHY AND ANTIRETINAL ANTIBODIES
Grewal, D. S., Fishman, G. A., & Jampol, L. M. (2014) · Retina · doi:10.1097/iae.0000000000000119 · Cited by 174 · see citing works
Cescato, R., Érchegyi, J., Waser, B., Piccand, V., Maëcke, H. R., Rivier, J., & Reubi, J. C. (2008) · Journal of Medicinal Chemistry · doi:10.1021/jm701618q · Cited by 115 · see citing works
Di Domenico, F., Barone, E., Perluigi, M., & Butterfield, D. A. (2017) · Antioxidants & Redox Signaling · doi:10.1089/ars.2016.6759 · Cited by 114 · see citing works
Bei, R., Masuelli, L., Palumbo, C., Modesti, M., & Modesti, A. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.11.009 · Cited by 105 · see citing works
Alpha-Enolase: Emerging Tumor-Associated Antigen, Cancer Biomarker, and Oncotherapeutic Target
Almaguel, F. A., Sanchez, T. W., Ortiz-Hernández, G. L., & Casiano, C. A. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2020.614726 · Cited by 97 · see citing works
Cauwe, B., Martens, E., Proost, P., & Opdenakker, G. (2009) · Integrative Biology · doi:10.1039/b904701h · Cited by 94 · see citing works
Anekonda, T. S., & Adamus, G. (2008) · BMC Research Notes · doi:10.1186/1756-0500-1-122 · Cited by 88 · see citing works
Self-citationResveratrol and the eye: activity and molecular mechanisms
Bola, C., Bartlett, H. E., & Eperjesi, F. (2014) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-014-2604-8 · Cited by 87 · see citing works
Adamus, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00765 · Cited by 82 · see citing works
Self-citationHuman thymic epithelial primary cells produce exosomes carrying tissue‐restricted antigens
Skogberg, G., Lundberg, V., Berglund, M., Gudmundsdottir, J. A., Telemo, E., Lindgren, S., & Ekwall, O. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.33 · Cited by 80 · see citing works
Optical Coherence Tomography Findings in Autoimmune Retinopathy
Abazari, A., Allam, S. S., Adamus, G., & Ghazi, N. G. (2012) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2011.09.012 · Cited by 79 · see citing works
Self-citationMoonlighting Proteins: The Case of the Hexokinases
Rodríguez-Saavedra, C., Morgado-Martínez, L. E., Burgos-Palacios, A., King-Dı́az, B., López‐Coria, M., & Sánchez‐Nieto, S. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.701975 · Cited by 75 · see citing works
Protective Properties and Surface Localization ofPlasmodium falciparumEnolase
Pal‐Bhowmick, I., Mehta, M., Coppens, I., Sharma, S., & Jarori, G. K. (2007) · Infection and Immunity · doi:10.1128/iai.00551-07 · Cited by 71 · see citing works
The Need for Standardization of Antiretinal Antibody Detection and Measurement
Forooghian, F., MacDonald, I. M., Heckenlively, J. R., Héon, E., Gordon, L. K., Hooks, J. J., Detrick, B., & Nussenblatt, R. B. (2008) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2008.05.046 · Cited by 69 · see citing works
Autoimmunity against carbonic anhydrase II affects retinal cell functions in autoimmune retinopathy
Adamus, G., & Karren, L. J. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.02.001 · Cited by 65 · see citing works
Self-citationAn update on autoimmune retinopathy
Majumder, P. D., Marchese, A., Pichi, F., Garg, I., & Agarwal, A. K. (2020) · Indian Journal of Ophthalmology · doi:10.4103/ijo.ijo_786_20 · Cited by 64 · see citing works
The Role of Enolase in Tissue Invasion and Metastasis of Pathogens and Tumor Cells
Liu, K., & Shih, N. (2007) · doi:10.29685/jcm.200704.0002 · Cited by 63 · see citing works
Iannaccone, A., Giorgianni, F., New, D. D., Hollingsworth, T., Umfress, A. C., Alhatem, A., Neeli, I., Lenchik, N. I., Jennings, B., Calzada, J. I., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0145323 · Cited by 59 · see citing works
Proteomic Modeling for HIV-1 Infected Microglia-Astrocyte Crosstalk
Wang, T., Gong, N., Liu, J., Kadiu, I., Kraft-Terry, S. D., Mosley, R. L., Volsky, D. J., Ciborowski, P. S., & Gendelman, H. E. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002507 · Cited by 51 · see citing works
Adamus, G., Brown, L., Schiffman, J. S., & Iannaccone, A. (2011) · Journal of Ophthalmic Inflammation and Infection · doi:10.1007/s12348-011-0028-8 · Cited by 50 · see citing works
Self-citationZeng, T., Jiang, X., Li, J., Wang, D., Li, G., Lu, L., & Wang, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076917 · Cited by 43 · see citing works
Seliger, B., Dressler, S. P., Wang, E., Kellner, R., Recktenwald, C. V., Lottspeich, F., Marincola, F. M., Baumgärtner, M., Atkins, D., & Lichtenfels, R. (2009) · PROTEOMICS · doi:10.1002/pmic.200700288 · Cited by 43 · see citing works
Komáromy, A. M., Abrams, K. L., Heckenlively, J. R., Lundy, S. K., Maggs, D. J., Leeth, C. M., MohanKumar, P. S., Petersen‐Jones, S. M., SERREZE, D. V., & van der Woerdt, A. (2015) · Veterinary Ophthalmology · doi:10.1111/vop.12291 · Cited by 42 · see citing works
Cossu, D., Mameli, G., Galleri, G., Cocco, E. E., Masala, S., Frau, J., Marrosu, M. G., Manetti, R., & Sechi, L. A. (2014) · Multiple Sclerosis Journal · doi:10.1177/1352458514557304 · Cited by 41 · see citing works
Antibodies to an Intracellular Antigen Penetrate Neuronal Cells and Cause Deleterious Effects
Douglas, J. N. (2013) · Journal of Clinical & Cellular Immunology · doi:10.4172/2155-9899.1000134 · Cited by 41 · see citing works
Antibody-Mediated Retinopathies in Canine Patients: Mechanism, Diagnosis, and Treatment Modalities
Grozdanić, S. D., Harper, M. M., & Kecova, H. (2008) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/j.cvsm.2007.12.003 · Cited by 39 · see citing works
Kimura, Y., Miura, N., Dêbiec, H., Morita, H., Yamada, H., Banno, S., Ronco, P. M., & Imai, H. (2016) · Clinical and Experimental Nephrology · doi:10.1007/s10157-016-1235-2 · Cited by 38 · see citing works
The Enigma of Autoimmune Retinopathy
Forooghian, F., Cao, S., Cui, J. H., & Matsubara, J. A. (2015) · International Ophthalmology Clinics · doi:10.1097/iio.0000000000000063 · Cited by 34 · see citing works
Adamus, G. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00505 · Cited by 33 · see citing works
Self-citationKyger, M., Worley, A. H., & Adamus, G. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.10.007 · Cited by 32 · see citing works
Self-citationOcular Paraneoplastic Syndromes
Przeździecka-Dołyk, J., Brzecka, A., Ejma, M., Misiuk‐Hojło, M., Solis, L. F. T., Herrera, A. S., Somasundaram, S. G., Kirkland, C. E., & Aliev, G. M. (2020) · Biomedicines · doi:10.3390/biomedicines8110490 · Cited by 29 · see citing works
Whittemore, J. C., Hawley, J. R., Jensen, W. A., & Lappin, M. R. (2010) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.2010.0476.x · Cited by 29 · see citing works
Luo, Q., Jiang, L., Chen, G., Feng, Y., Lv, Q., Zhang, C., Qu, S., Zhu, H., Zhou, B., & Xiao, X. (2011) · Free Radical Research · doi:10.3109/10715762.2011.627330 · Cited by 29 · see citing works
Investigation of Cas9 Antibodies in the Human Eye
Toral, M. A., Charlesworth, C. T., Ng, B., Chemudupati, T., Homma, S., Nakauchi, H., Bassuk, A. G., Porteus, M. H., & Mahajan, V. B. (2022) · Nature Communications · doi:10.1038/s41467-022-28674-1 · Cited by 28 · see citing works
Adamus, G. (2017) · Autoimmunity Reviews · doi:10.1016/j.autrev.2017.01.005 · Cited by 28 · see citing works
Self-citationMantel, I., Ramchand, K. V., Holder, G. E., Ohbayashi, M., Morohoshi, K., Patel, N., Toda, M., Fitzke, F. W., Bird, A. C., & Ono, S. J. (2007) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2007.10.006 · Cited by 28 · see citing works
Sen, H. N., Grange, L. K., Akanda, M., & Fox, A. R. (2017) · PubMed Central · Cited by 27 · see citing works
Oxidative modifications of proteins by sodium arsenite in human umbilical vein endothelial cells
Lii, C., Lin, A., Lee, S., Chen, H., & Wang, T. (2010) · Environmental Toxicology · doi:10.1002/tox.20572 · Cited by 26 · see citing works
Paraneoplastic syndromes in neuro-ophthalmology
Alabduljalil, T., & Behbehani, R. S. (2007) · Current Opinion in Ophthalmology · doi:10.1097/icu.0b013e3282f0b497 · Cited by 24 · see citing works
Zeng, H., Liu, Q., Peng, X., Cao, K., Jin, S., & Xu, K. (2019) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-019-04359-2 · Cited by 24 · see citing works
Latest Updates on Antiretinal Autoantibodies Associated With Vision Loss and Breast Cancer
Adamus, G. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-15739 · Cited by 21 · see citing works
Self-citationCarboni, G., Forma, G., Bond, A. D., Adamus, G., & Iannaccone, A. (2012) · Documenta Ophthalmologica · doi:10.1007/s10633-012-9327-0 · Cited by 20 · see citing works
Self-citationWeppelmann, T. A., Khalil, S., Zafrullah, N., Amir, S., & Margo, C. E. (2022) · Cancer Control · doi:10.1177/10732748221144458 · Cited by 19 · see citing works
Autoimmunity against a glycolytic enzyme as a possible cause for persistent symptoms in Lyme disease
Maccallini, P., Bonin, S., & Trevisan, G. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.10.024 · Cited by 19 · see citing works
Neurofilament light as an immune target for pathogenic antibodies
Puentes, F., van der Star, B. J., Boomkamp, S. D., Kipp, M., Boon, L., Boscá, I., Raffel, J., Gnanapavan, S., van der Valk, P., Stephenson, J., et al. (2017) · Immunology · doi:10.1111/imm.12797 · Cited by 17 · see citing works
Yamamoto, Y., Koma, H., & Yagami, T. (2015) · NeuroToxicology · doi:10.1016/j.neuro.2015.05.008 · Cited by 17 · see citing works
The crossroads between cancer immunity and autoimmunity antibodies to self antigens
Bei, R. (2017) · Frontiers in bioscience · doi:10.2741/4545 · Cited by 17 · see citing works
Qu, S., Lin, H., Pfeiffer, N., & Grus, F. H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031624 · Cited by 16 · see citing works
Sculier, C., Bentea, G. P., Ruelle, L., Grigoriu, B. D., Coureau, M., Gorham, J., Sideris, S., Holbrechts, S., Lafitte, J., Meert, A., et al. (2017) · Lung Cancer · doi:10.1016/j.lungcan.2017.07.026 · Cited by 14 · see citing works
AUTOIMMUNE RETINOPATHY AND ANTIRETINAL ANTIBODIES
Grewal, D. S., Fishman, G. A., & Jampol, L. M. (2014) · Retina · doi:10.1097/01.iae.0000450880.26367.4e · Cited by 14 · see citing works
Autoimmune retinopathy associated with carcinoid tumour of the small bowel
Ogra, S., Sharp, D. M., & Danesh-Meyer, H. V. (2013) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2013.07.002 · Cited by 14 · see citing works
Yoshitake, S., Murakami, T., Suzuma, K., Yoshitake, T., Uji, A., Morooka, S., Dodo, Y., Fujimoto, M., Shan, Y., Fort, P. E., et al. (2018) · Diabetologia · doi:10.1007/s00125-018-4773-1 · Cited by 12 · see citing works
Antibody Transfection into Neurons as a Tool to Study Disease Pathogenesis
Douglas, J. N., Gardner, L. A., Lee, S., Shin, Y., Groover, C. J., & Levin, M. C. (2012) · Journal of Visualized Experiments · doi:10.3791/4154 · Cited by 11 · see citing works
Irizarry, F., Kopplin, L. J., Salek, S. S., Adamus, G., Saleh, M. G. A., Biggee, K., Lin, P., & Rosenbaum, J. T. (2017) · American Journal of Ophthalmology Case Reports · doi:10.1016/j.ajoc.2017.08.001 · Cited by 11 · see citing works
Self-citationAnti-retinal autoantibodies in myopic macular degeneration: a pilot study
Sim, S. S., Wong, C. W., Hoang, Q. V., Lee, S. Y., Wong, T. Y., & Cheung, C. M. G. (2020) · Eye · doi:10.1038/s41433-020-01241-y · Cited by 11 · see citing works
Anti–γ-Enolase Autoimmune Retinopathy Manifesting in Early Childhood
Ko, A. C. (2010) · Archives of Ophthalmology · doi:10.1001/archophthalmol.2010.295 · Cited by 11 · see citing works
Impact of taxol on dermal papilla cells — A proteomics and bioinformatics analysis
Chen, P.-H., Wang, C., Hsia, C., Ho, M., Chen, A., Tseng, M., Wu, Y.-F., Chen, H., Huang, T., Liu, H.-T., et al. (2011) · Journal of Proteomics · doi:10.1016/j.jprot.2011.09.019 · Cited by 11 · see citing works
Uslubas, I., Kanlı, A., Kasap, M., Akpınar, G., & Karabas, L. V. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2020.108425 · Cited by 10 · see citing works
Al‐Moujahed, A., Velez, G., Vu, J. T., de Carvalho, J. R. L., Levi, S. R., Bassuk, A. G., Sepah, Y. J., Tsang, S. H., & Mahajan, V. B. (2022) · Ophthalmology Science · doi:10.1016/j.xops.2022.100131 · Cited by 9 · see citing works
Nikoopour, E., Lin, C., Sheskey, S., Heckenlively, J. R., & Lundy, S. K. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800574 · Cited by 9 · see citing works
Ronco, P. M., Dêbiec, H., & Imai, H. (2013) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2013.03.016 · Cited by 8 · see citing works
HIV-1 Envelope Mimicry of Host Enzyme Kynureninase Does Not Disrupt Tryptophan Metabolism
Bradley, T., Yang, G., Ilkayeva, O., Holl, T. M., Zhang, R., Zhang, J., Santra, S., Fox, C. B., Reed, S. G., Parks, R., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601484 · Cited by 8 · see citing works
Diagnosis and treatment of autoimmune retinopathy: review of current approaches
Kalogeropoulos, D., Lotery, A. J., Pavesio, C. E., Kalogeropoulos, C. D., Kanavaros, P., Afshar, F., Shawkat, F. S., & Salvo, G. D. (2025) · International Ophthalmology · doi:10.1007/s10792-025-03696-y · Cited by 7 · see citing works
Andrikopoulou, Α., Koutsoukos, K., Chatziralli, I., THEODOSSIADIS, P. G., Tsivgoulis, G. K., Tzartos, J. S., Anastasakis, A., Zagouri, F., & Dimopoulos, M. A. (2023) · Oncology Letters · doi:10.3892/ol.2023.13894 · Cited by 6 · see citing works
Zhou, Z., Huang, P., Song, G.-H., Zhang, Z., An, K., Lu, H.-W., Ju, X., & Ding, W. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7241 · Cited by 6 · see citing works
Paraneoplastic retinal degeneration
Adamus, G. (2010) · Elsevier eBooks · doi:10.1016/b978-0-7020-2983-7.00076-0 · Cited by 6 · see citing works
Self-citationAutoimmune RNA dysregulation and seizures: therapeutic prospects in neuropsychiatric lupus
Muslimov, I. A., Berardi, V., Stephenson, S. I., Ginzler, E. M., Hanly, J. G., & Tiedge, H. (2022) · Life Science Alliance · doi:10.26508/lsa.202201496 · Cited by 4 · see citing works
Wang, M., Li, H., Wu, Y., Wang, B., Xi, Y., & Hu, K. (2024) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2024.2306129 · Cited by 4 · see citing works
Cancer-associated retinopathy 4 years after surgery for ovarian cancer
Dimitriou, E., Chatzirallis, A., Katopodis, S., THEODOSSIADIS, G. P., THEODOSSIADIS, P. G., & Chatziralli, I. (2021) · Oman Journal of Ophthalmology · doi:10.4103/ojo.ojo_352_20 · Cited by 4 · see citing works
Ocular Paraneoplastic Diseases
Courtney, R. J., Singh, R. P., Aronow, M. E., & Singh, A. D. (2013) · Springer eBooks · doi:10.1007/978-3-642-39489-8_10 · Cited by 4 · see citing works
Application of Ophthalmic Electrophysiology in Inflammatory Disorders of Retina and Optic Nerve
Yu, M., & Kurup, S. K. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13133829 · Cited by 3 · see citing works
Naturally occurring neuroprotectants in glaucoma
Patel, R. P., Shamsher, E., Hill, D., & Cordeiro, M. F. (2020) · Progress in brain research · doi:10.1016/bs.pbr.2020.06.022 · Cited by 3 · see citing works
Fortenbach, C. R., Whitmore, S. S., Thurtell, M. J., Sohn, E. H., Critser, D. B., Stone, E. M., Folk, J. C., Han, I. C., & Boyce, T. M. (2023) · Ocular Immunology and Inflammation · doi:10.1080/09273948.2023.2199334 · Cited by 3 · see citing works
Unusual patterns of recurrence in low grade gliomas
Ellenbogen, J. R., Davies, P., Eldridge, P. R., & Jenkinson, M. D. (2013) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2013.05.013 · Cited by 3 · see citing works
Paraneoplastic Syndromes Involving the Nervous System
Posner, J. B. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-407710-2.00027-8 · Cited by 3 · see citing works
PlasmodiumRiboprotein PfP0 Induces a Deviant Humoral Immune Response in Balb/cMice
Pathak, S., Rajeshwari, K., Garg, S., Rajagopal, S., Patel, K. G., Das, B. K., Pied, S., Ravindran, B., & Sharma, S. (2012) · BioMed Research International · doi:10.1155/2012/695843 · Cited by 2 · see citing works
Xu, H., Tang, N., Wong, W., & Wang, M. (2026) · Ophthalmology Science · doi:10.1016/j.xops.2026.101204 · Cited by 1 · see citing works
Experimental and bioinformatic approach to identifying antigenic epitopes in human α- and β-enolases
Pietkiewicz, J., Danielewicz, R., Bednarz-Misa, I. S., Ceremuga, I., Wiśniewski, J. Ł., Mierzchała-Pasierb, M., Bronowicka-Szydełko, A., Ziomek, E., & Gamian, A. (2018) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2018.05.008 · Cited by 1 · see citing works
Paraneoplastic and Other Autoimmune Disorders
Mohler, A. C., Montalvo, M., & Roth, J. L. (2019) · Current clinical neurology · doi:10.1007/978-3-030-24436-1_13 · Cited by 1 · see citing works
Characteristics of Visual Electrophysiology in Inflammatory Disorders
Iannaccone, A., Senatore, A., Kheir, W. J., Creel, D. J., & Yu, M.-Z. (2019) · Springer eBooks · doi:10.1007/978-3-030-30417-1_8 · Cited by 1 · see citing works
47-kDa (Presumed α-Enolase)–Positive Autoimmune-Related Retinopathy and Optic Neuropathy (ARRON)
Lin, W., Pau, D., Thirkill, C. E., & Lee, A. G. (2012) · Neuro-Ophthalmology · doi:10.3109/01658107.2012.730093
Ronco, P. M., & Dêbiec, H. (2014) · Contributions to nephrology · doi:10.1159/000360051
Kalyuzhin, O. V., Дикинов, З. Х., & Evsegneeva, I. V. (2011)
Antibodies in autoimmune retinopathy
Bhat, P., & Huo, S. (2016) · Expert Opinion on Orphan Drugs · doi:10.1080/21678707.2016.1246247
Cancer-associated retinopathy: an autoimmune retinopathy
Tradjutrisno, N. (2010) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.18051/univmed.2010.v29.56-64
Ocular Paraneoplastic Diseases
Leskov, I. B., & Singh, A. D. (2019) · Springer eBooks · doi:10.1007/978-3-030-04113-7_10
(2007) · Current Opinion in Ophthalmology · doi:10.1097/icu.0b013e3282f292cf
Zhang, L. Q., Zhao, J., Wang, H. Y., Wang, Z. Y., Li, Y. N., Tang, J., Li, S. Y., Qu, J., & Zhao, M. W. (2022) · PubMed Central · doi:10.19723/j.issn.1671-167x.2022.06.007
Review of Autoimmune Retinopathy and Its Association with Melanoma and Other Malignancies
Klepper, E. M., Lee, J., Thapa, S., Helie, M., Theyagaraj, S., & Robinson, H. (2023) · Journal of Dermatology Research · doi:10.46889/jdr.2023.4306
Ocular Paraneoplastic Diseases
Sedaghat, A., & Singh, A. D. (2024) · Springer eBooks · doi:10.1007/978-3-031-72433-6_12
Zeng, Q., Lin, J. M., Syrrou, A., İnam, O., Wesley, S. F., & Tezel, T. H. (2025) · BMC Ophthalmology · doi:10.1186/s12886-025-04302-6
Correlation between anti-retinal antibodies and lupus retinopathy in systemic lupus erythematosus
Zou, Q., Zhang, L., Li, M., Wang, B., Cao, Y., Zhang, X., & Qu, J. (2026) · Scientific Reports · doi:10.1038/s41598-026-44125-z
Blumenthal, K. H., McLellan, J., & de Water, J. V. (2026) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2026.1794161
- Authors
- MAGRYS, A., ANEKONDA, T., REN, G., & ADAMUS, G.
- Affiliations
- Oregon Health & Science University (US)
- Corresponding author
- ADAMUS, GRAZYNA
- ORCID
- ADAMUS, GRAZYNA
- Venue
- Journal of Clinical Immunology
- Published
- 2007-01-19
- Volume
- 27
- Issue
- 2
- Pages
- 181-192
- ISSN
- 0271-9142 (ISSN-L)
- 1573-2592
- OpenAlex
- W1969411640
- Cited by
- 95
- References
- 60
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 5 · 2021: 4 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 9 · 2016: 5 · 2015: 6 · 2014: 6 · 2013: 6 · 2012: 6
- FWCI
- 6.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Clinical Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (EY 13053, R01EY013053)
- Topics
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Health Sciences › Medicine › Neurology › Autoimmune Neurological Disorders and Treatments
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Keywords
- autoimmune retinopathy, intracellular calcium, Bax translocation, cytochrome c release, apoptosis, L-type calcium channels, nifedipine, diltiazem, verapamil, retinal neurons, retinal degeneration, vision loss
- MeSH terms
- Adenosine Triphosphate, Animals, Antibodies, Monoclonal, Autoantibodies, Autoantigens, Calcium, Cell Line, Glycolysis, Neurons, Phosphopyruvate Hydratase, Retinal Diseases, Blotting, Western, Apoptosis, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review