Suppression of Oxidative Stress as Potential Therapeutic Approach for Normal Tension Glaucoma
Abstract
:1. Introduction
2. Identification of Sequence Variants in EAAT1/GLAST in Glaucoma Patients
3. Animal Models of Normal Tension Glaucoma
3.1. Glutamate Transporter Deficient Mice
3.2. Aged Marmosets Present with Naturally Occurring NTG
3.2.1. Glaucomatous Characteristics in Marmosets are Similar to Human Glaucoma
3.2.2. Oxidative Stress is Increased in Glaucomatous Marmosets
4. Effects of Suppression of Oxidative Stress in Rodent Models of NTG
4.1. Apoptosis Signal-Regulating Kinase 1
4.2. Valproic Acid
4.3. N-acetylcysteine
4.4. Spermidine
4.5. Coenzyme Q10
5. Effects of Dietary Intake of Antioxidants in Glaucoma Patients
6. Conclusions
Funding
Conflicts of Interest
References
- Rheaume, B.A.; Jereen, A.; Bolisetty, M.; Sajid, M.S.; Yang, Y.; Renna, K.; Sun, L.; Robson, P.; Trakhtenberg, E.F. Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes. Nat. Commun. 2018, 9, 2759. [Google Scholar] [CrossRef] [PubMed]
- Tran, N.M.; Shekhar, K.; Whitney, I.E.; Jacobi, A.; Benhar, I.; Hong, G.; Yan, W.; Adiconis, X.; Arnold, M.E.; Lee, J.M.; et al. Single-cell profiles of retinal ganglion cells differing in resilience to injury reveal neuroprotective genes. Neuron 2019. [Google Scholar] [CrossRef] [PubMed]
- Honda, S.; Namekata, K.; Kimura, A.; Guo, X.; Harada, C.; Murakami, A.; Matsuda, A.; Harada, T. Survival of alpha and intrinsically photosensitive retinal ganglion cells in NMDA-induced neurotoxicity and a mouse model of normal tension glaucoma. Investig. Ophthalmol. Vis. Sci. 2019, 60, 3696–3707. [Google Scholar] [CrossRef] [Green Version]
- Daniel, S.; Clark, A.F.; McDowell, C.M. Subtype-specific response of retinal ganglion cells to optic nerve crush. Cell Death Discov. 2018, 4, 7. [Google Scholar] [CrossRef] [PubMed]
- Osborne, N.N. Recent clinical findings with memantine should not mean that the idea of neuroprotection in glaucoma is abandoned. Acta Ophthalmol. 2009, 87, 450–454. [Google Scholar] [CrossRef]
- Ready, T. Stiff penalty for vision researcher guilty of scientific misconduct. Nat. Med. 2001, 7, 8. [Google Scholar] [CrossRef] [PubMed]
- Reichelt, W.; Stabel-Burow, J.; Pannicke, T.; Weichert, H.; Heinemann, U. The glutathione level of retinal Muller glial cells is dependent on the high-affinity sodium-dependent uptake of glutamate. Neuroscience 1997, 77, 1213–1224. [Google Scholar] [CrossRef]
- Gherghel, D.; Griffiths, H.R.; Hilton, E.J.; Cunliffe, I.A.; Hosking, S.L. Systemic reduction in glutathione levels occurs in patients with primary open-angle glaucoma. Investig. Ophthalmol. Vis. Sci. 2005, 46, 877–883. [Google Scholar] [CrossRef] [Green Version]
- Gherghel, D.; Mroczkowska, S.; Qin, L. Reduction in blood glutathione levels occurs similarly in patients with primary-open angle or normal tension glaucoma. Investig. Ophthalmol. Vis. Sci. 2013, 54, 3333–3339. [Google Scholar] [CrossRef]
- Noro, T.; Namekata, K.; Kimura, A.; Azuchi, Y.; Hashimoto, N.; Moriya-Ito, K.; Komaki, Y.; Lee, C.Y.; Okahara, N.; Guo, X.; et al. Normal tension glaucoma-like degeneration of the visual system in aged marmosets. Sci. Rep. 2019, 9, 14852. [Google Scholar] [CrossRef]
- Inman, D.M.; Lambert, W.S.; Calkins, D.J.; Horner, P.J. Alpha-lipoic acid antioxidant treatment limits glaucoma-related retinal ganglion cell death and dysfunction. PLoS ONE 2013, 8, e65389. [Google Scholar] [CrossRef] [Green Version]
- Namekata, K.; Kimura, A.; Kawamura, K.; Guo, X.; Harada, C.; Tanaka, K.; Harada, T. Dock3 attenuates neural cell death due to NMDA neurotoxicity and oxidative stress in a mouse model of normal tension glaucoma. Cell Death Differ. 2013, 20, 1250–1256. [Google Scholar] [CrossRef]
- Akaiwa, K.; Namekata, K.; Azuchi, Y.; Guo, X.; Kimura, A.; Harada, C.; Mitamura, Y.; Harada, T. Edaravone suppresses retinal ganglion cell death in a mouse model of normal tension glaucoma. Cell Death Dis. 2017, 8, e2934. [Google Scholar] [CrossRef] [PubMed]
- Akiyama, G.; Azuchi, Y.; Guo, X.; Noro, T.; Kimura, A.; Harada, C.; Namekata, K.; Harada, T. Edaravone prevents retinal degeneration in adult mice following optic nerve injury. Investig. Ophthalmol. Vis. Sci. 2017, 58, 4908–4914. [Google Scholar] [CrossRef]
- Yang, X.; Hondur, G.; Tezel, G. Antioxidant treatment limits neuroinflammation in experimental glaucoma. Investig. Ophthalmol. Vis. Sci. 2016, 57, 2344–2354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harada, T.; Harada, C.; Nakamura, K.; Quah, H.M.; Okumura, A.; Namekata, K.; Saeki, T.; Aihara, M.; Yoshida, H.; Mitani, A.; et al. The potential role of glutamate transporters in the pathogenesis of normal tension glaucoma. J. Clin. Investig. 2007, 117, 1763–1770. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harada, T.; Harada, C.; Watanabe, M.; Inoue, Y.; Sakagawa, T.; Nakayama, N.; Sasaki, S.; Okuyama, S.; Watase, K.; Wada, K.; et al. Functions of the two glutamate transporters GLAST and GLT-1 in the retina. Proc. Natl. Acad. Sci. USA 1998, 95, 4663–4666. [Google Scholar] [CrossRef] [Green Version]
- Naskar, R.; Vorwerk, C.K.; Dreyer, E.B. Concurrent downregulation of a glutamate transporter and receptor in glaucoma. Investig. Ophthalmol. Vis. Sci. 2000, 41, 1940–1944. [Google Scholar]
- Ishikawa, M. Abnormalities in glutamate metabolism and excitotoxicity in the retinal diseases. Scientifica 2013, 2013, 528940. [Google Scholar] [CrossRef] [Green Version]
- Yanagisawa, M.; Namekata, K.; Aida, T.; Katou, S.; Takeda, T.; Harada, T.; Fuse, N.; Tanaka, K. EAAT1 variants associated with glaucoma. Biochem. Biophys. Res. Commun. 2020, 529, 943–949. [Google Scholar] [CrossRef]
- Yasumura, R.; Meguro, A.; Ota, M.; Nomura, E.; Uemoto, R.; Kashiwagi, K.; Mabuchi, F.; Iijima, H.; Kawase, K.; Yamamoto, T.; et al. Investigation of the association between SLC1A3 gene polymorphisms and normal tension glaucoma. Mol. Vis. 2011, 17, 792–796. [Google Scholar] [PubMed]
- Tsuji, S. Genetics of neurodegenerative diseases: Insights from high-throughput resequencing. Hum. Mol. Genet. 2010, 19, R65–R70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harada, C.; Namekata, K.; Guo, X.; Yoshida, H.; Mitamura, Y.; Matsumoto, Y.; Tanaka, K.; Ichijo, H.; Harada, T. ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell Death Differ. 2010, 17, 1751–1759. [Google Scholar] [CrossRef] [Green Version]
- Kimura, A.; Guo, X.; Noro, T.; Harada, C.; Tanaka, K.; Namekata, K.; Harada, T. Valproic acid prevents retinal degeneration in a murine model of normal tension glaucoma. Neurosci. Lett. 2015, 588, 108–113. [Google Scholar] [CrossRef] [PubMed]
- Dong, Z.; Shinmei, Y.; Dong, Y.; Inafuku, S.; Fukuhara, J.; Ando, R.; Kitaichi, N.; Kanda, A.; Tanaka, K.; Noda, K.; et al. Effect of geranylgeranylacetone on the protection of retinal ganglion cells in a mouse model of normal tension glaucoma. Heliyon 2016, 2, e00191. [Google Scholar] [CrossRef] [Green Version]
- Sano, H.; Namekata, K.; Kimura, A.; Shitara, H.; Guo, X.; Harada, C.; Mitamura, Y.; Harada, T. Differential effects of N-acetylcysteine on retinal degeneration in two mouse models of normal tension glaucoma. Cell Death Dis. 2019, 10, 75. [Google Scholar] [CrossRef]
- Tanaka-Gonome, T.; Xie, Y.; Yamauchi, K.; Maeda-Monai, N.; Tanabu, R.; Kudo, T.; Nakazawa, M. The protective effect of astaxanthin on the ganglion cell complex in glutamate/aspartate transporter deficient mice, a model of normal tension glaucoma, analyzed by spectral domain-optical coherence tomography. Biochem Biophys Rep. 2020, 23, 100777. [Google Scholar] [CrossRef]
- Noro, T.; Namekata, K.; Azuchi, Y.; Kimura, A.; Guo, X.; Harada, C.; Nakano, T.; Tsuneoka, H.; Harada, T. Spermidine ameliorates neurodegeneration in a mouse model of normal tension glaucoma. Investig. Ophthalmol. Vis. Sci. 2015, 56, 5012–5019. [Google Scholar] [CrossRef] [Green Version]
- Akaiwa, K.; Namekata, K.; Azuchi, Y.; Sano, H.; Guo, X.; Kimura, A.; Harada, C.; Mitamura, Y.; Harada, T. Topical ripasudil suppresses retinal ganglion cell death in a mouse model of normal tension glaucoma. Investig. Ophthalmol. Vis. Sci. 2018, 59, 2080–2089. [Google Scholar] [CrossRef]
- Perez de Lara, M.J.; Santano, C.; Guzman-Aranguez, A.; Valiente-Soriano, F.J.; Aviles-Trigueros, M.; Vidal-Sanz, M.; de la Villa, P.; Pintor, J. Assessment of inner retina dysfunction and progressive ganglion cell loss in a mouse model of glaucoma. Exp. Eye Res. 2014, 122, 40–49. [Google Scholar] [CrossRef]
- Schaub, J.A.; Kimball, E.C.; Steinhart, M.R.; Nguyen, C.; Pease, M.E.; Oglesby, E.N.; Jefferys, J.L.; Quigley, H.A. Regional retinal ganglion cell axon loss in a murine glaucoma model. Investig. Ophthalmol. Vis. Sci. 2017, 58, 2765–2773. [Google Scholar] [CrossRef] [PubMed]
- Nakano, N.; Ikeda, H.O.; Hasegawa, T.; Muraoka, Y.; Iwai, S.; Tsuruyama, T.; Nakano, M.; Fuchigami, T.; Shudo, T.; Kakizuka, A.; et al. Neuroprotective effects of VCP modulators in mouse models of glaucoma. Heliyon 2016, 2, e00096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, S.; Wang, B.; Xie, Y.; Zhu, S.; Thomas, R.; Qing, G.; Zhang, C.; Wang, N. Retinotopic changes in the gray matter volume and cerebral blood flow in the primary visual cortex of patients with primary open-angle glaucoma. Investig. Ophthalmol. Vis. Sci. 2015, 56, 6171–6178. [Google Scholar] [CrossRef] [PubMed]
- Himori, N.; Kunikata, H.; Shiga, Y.; Omodaka, K.; Maruyama, K.; Takahashi, H.; Nakazawa, T. The association between systemic oxidative stress and ocular blood flow in patients with normal-tension glaucoma. Graefes Arch. Clin. Exp. Ophthalmol. 2016, 254, 333–341. [Google Scholar] [CrossRef] [PubMed]
- Kimura, A.; Namekata, K.; Guo, X.; Noro, T.; Harada, C.; Harada, T. Targeting oxidative stress for treatment of glaucoma and optic neuritis. Oxid. Med. Cell. Longev. 2017, 2017, 2817252. [Google Scholar] [CrossRef]
- Harada, C.; Kimura, A.; Guo, X.; Namekata, K.; Harada, T. Recent advances in genetically modified animal models of glaucoma and their roles in drug repositioning. Br. J. Ophthalmol. 2019, 103, 161–166. [Google Scholar] [CrossRef] [Green Version]
- Sasaki, E.; Suemizu, H.; Shimada, A.; Hanazawa, K.; Oiwa, R.; Kamioka, M.; Tomioka, I.; Sotomaru, Y.; Hirakawa, R.; Eto, T.; et al. Generation of transgenic non-human primates with germline transmission. Nature 2009, 459, 523–527. [Google Scholar] [CrossRef]
- Sato, K.; Oiwa, R.; Kumita, W.; Henry, R.; Sakuma, T.; Ito, R.; Nozu, R.; Inoue, T.; Katano, I.; Sato, K.; et al. Generation of a nonhuman primate model of severe combined immunodeficiency using highly efficient genome editing. Cell Stem Cell 2016, 19, 127–138. [Google Scholar] [CrossRef] [Green Version]
- Ruan, Y.; Jiang, S.; Musayeva, A.; Gericke, A. Oxidative stress and vascular dysfunction in the retina: Therapeutic strategies. Antioxidants 2020, 9, 761. [Google Scholar] [CrossRef]
- Nishitoh, H.; Kadowaki, H.; Nagai, A.; Maruyama, T.; Yokota, T.; Fukutomi, H.; Noguchi, T.; Matsuzawa, A.; Takeda, K.; Ichijo, H. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 2008, 22, 1451–1464. [Google Scholar] [CrossRef] [Green Version]
- Hattori, K.; Naguro, I.; Runchel, C.; Ichijo, H. The roles of ASK family proteins in stress responses and diseases. Cell Commun. Signal. 2009, 7, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ichijo, H.; Nishida, E.; Irie, K.; ten Dijke, P.; Saitoh, M.; Moriguchi, T.; Takagi, M.; Matsumoto, K.; Miyazono, K.; Gotoh, Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997, 275, 90–94. [Google Scholar] [CrossRef]
- Matsuzawa, A.; Nishitoh, H.; Tobiume, K.; Takeda, K.; Ichijo, H. Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: Advanced findings from ASK1 knockout mice. Antioxid. Redox Signal. 2002, 4, 415–425. [Google Scholar] [CrossRef] [PubMed]
- Harada, C.; Nakamura, K.; Namekata, K.; Okumura, A.; Mitamura, Y.; Iizuka, Y.; Kashiwagi, K.; Yoshida, K.; Ohno, S.; Matsuzawa, A.; et al. Role of apoptosis signal-regulating kinase 1 in stress-induced neural cell apoptosis in vivo. Am. J. Pathol. 2006, 168, 261–269. [Google Scholar] [CrossRef] [Green Version]
- Katome, T.; Namekata, K.; Guo, X.; Semba, K.; Kittaka, D.; Kawamura, K.; Kimura, A.; Harada, C.; Ichijo, H.; Mitamura, Y.; et al. Inhibition of ASK1-p38 pathway prevents neural cell death following optic nerve injury. Cell Death Differ. 2013, 20, 270–280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osaka, N.; Takahashi, T.; Murakami, S.; Matsuzawa, A.; Noguchi, T.; Fujiwara, T.; Aburatani, H.; Moriyama, K.; Takeda, K.; Ichijo, H. ASK1-dependent recruitment and activation of macrophages induce hair growth in skin wounds. J. Cell Biol. 2007, 176, 903–909. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, X.; Harada, C.; Namekata, K.; Matsuzawa, A.; Camps, M.; Ji, H.; Swinnen, D.; Jorand-Lebrun, C.; Muzerelle, M.; Vitte, P.A.; et al. Regulation of the severity of neuroinflammation and demyelination by TLR-ASK1-p38 pathway. EMBO Mol. Med. 2010, 2, 504–515. [Google Scholar] [CrossRef]
- Tezel, G. TNF-alpha signaling in glaucomatous neurodegeneration. Prog. Brain Res. 2008, 173, 409–421. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.X.; Ji, Y.X.; Zhang, X.J.; Zhao, L.P.; Yan, Z.Z.; Zhang, P.; Shen, L.J.; Yang, X.; Fang, J.; Tian, S.; et al. Targeting CASP8 and FADD-like apoptosis regulator ameliorates nonalcoholic steatohepatitis in mice and nonhuman primates. Nat. Med. 2017, 23, 439–449. [Google Scholar] [CrossRef]
- Loomba, R.; Lawitz, E.; Mantry, P.S.; Jayakumar, S.; Caldwell, S.H.; Arnold, H.; Diehl, A.M.; Djedjos, C.S.; Han, L.; Myers, R.P.; et al. The ASK1 inhibitor selonsertib in patients with nonalcoholic steatohepatitis: A randomized, phase 2 trial. Hepatology 2018, 67, 549–559. [Google Scholar] [CrossRef]
- Gottlicher, M.; Minucci, S.; Zhu, P.; Kramer, O.H.; Schimpf, A.; Giavara, S.; Sleeman, J.P.; Lo Coco, F.; Nervi, C.; Pelicci, P.G.; et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 2001, 20, 6969–6978. [Google Scholar] [CrossRef] [Green Version]
- Phiel, C.J.; Zhang, F.; Huang, E.Y.; Guenther, M.G.; Lazar, M.A.; Klein, P.S. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 2001, 276, 36734–36741. [Google Scholar] [CrossRef] [Green Version]
- Romoli, M.; Mazzocchetti, P.; D’Alonzo, R.; Siliquini, S.; Rinaldi, V.E.; Verrotti, A.; Calabresi, P.; Costa, C. Valproic acid and epilepsy: From molecular mechanisms to clinical evidences. Curr. Neuropharmacol. 2019, 17, 926–946. [Google Scholar] [CrossRef]
- Kimura, A.; Namekata, K.; Guo, X.; Noro, T.; Harada, C.; Harada, T. Valproic acid prevents NMDA-induced retinal ganglion cell death via stimulation of neuronal TrkB receptor signaling. Am. J. Pathol. 2015, 185, 756–764. [Google Scholar] [CrossRef]
- Suda, S.; Katsura, K.; Kanamaru, T.; Saito, M.; Katayama, Y. Valproic acid attenuates ischemia-reperfusion injury in the rat brain through inhibition of oxidative stress and inflammation. Eur. J. Pharmacol. 2013, 707, 26–31. [Google Scholar] [CrossRef]
- Lee, J.Y.; Maeng, S.; Kang, S.R.; Choi, H.Y.; Oh, T.H.; Ju, B.G.; Yune, T.Y. Valproic acid protects motor neuron death by inhibiting oxidative stress and endoplasmic reticulum stress-mediated cytochrome C release after spinal cord injury. J. Neurotrauma 2014, 31, 582–594. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Qin, X.; Zhao, X.; Tong, N.; Gong, Y.; Zhang, W.; Wu, X. Valproic acid regulates antioxidant enzymes and prevents ischemia/reperfusion injury in the rat retina. Curr. Eye Res. 2012, 37, 429–437. [Google Scholar] [CrossRef]
- Clemson, C.M.; Tzekov, R.; Krebs, M.; Checchi, J.M.; Bigelow, C.; Kaushal, S. Therapeutic potential of valproic acid for retinitis pigmentosa. Br. J. Ophthalmol. 2011, 95, 89–93. [Google Scholar] [CrossRef]
- Kumar, A.; Midha, N.; Gogia, V.; Gupta, S.; Sehra, S.; Chohan, A. Efficacy of oral valproic acid in patients with retinitis pigmentosa. J. Ocul. Pharmacol. Ther. 2014, 30, 580–586. [Google Scholar] [CrossRef]
- Iraha, S.; Hirami, Y.; Ota, S.; Sunagawa, G.A.; Mandai, M.; Tanihara, H.; Takahashi, M.; Kurimoto, Y. Efficacy of valproic acid for retinitis pigmentosa patients: A pilot study. Clin. Ophthalmol. 2016, 10, 1375–1384. [Google Scholar] [CrossRef] [Green Version]
- Eisenberg, T.; Knauer, H.; Schauer, A.; Buttner, S.; Ruckenstuhl, C.; Carmona-Gutierrez, D.; Ring, J.; Schroeder, S.; Magnes, C.; Antonacci, L.; et al. Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol. 2009, 11, 1305–1314. [Google Scholar] [CrossRef]
- Rider, J.E.; Hacker, A.; Mackintosh, C.A.; Pegg, A.E.; Woster, P.M.; Casero, R.A., Jr. Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 2007, 33, 231–240. [Google Scholar] [CrossRef]
- Noro, T.; Namekata, K.; Kimura, A.; Guo, X.; Azuchi, Y.; Harada, C.; Nakano, T.; Tsuneoka, H.; Harada, T. Spermidine promotes retinal ganglion cell survival and optic nerve regeneration in adult mice following optic nerve injury. Cell Death Dis. 2015, 6, e1720. [Google Scholar] [CrossRef] [Green Version]
- Soda, K.; Kano, Y.; Sakuragi, M.; Takao, K.; Lefor, A.; Konishi, F. Long-term oral polyamine intake increases blood polyamine concentrations. J. Nutr. Sci. Vitaminol. 2009, 55, 361–366. [Google Scholar]
- Spindler, M.; Beal, M.F.; Henchcliffe, C. Coenzyme Q10 effects in neurodegenerative disease. Neuropsychiatr. Dis. Treat. 2009, 5, 597–610. [Google Scholar] [CrossRef] [Green Version]
- Qu, J.; Kaufman, Y.; Washington, I. Coenzyme Q10 in the human retina. Investig. Ophthalmol. Vis. Sci. 2009, 50, 1814–1818. [Google Scholar] [CrossRef] [Green Version]
- Lee, D.; Shim, M.S.; Kim, K.Y.; Noh, Y.H.; Kim, H.; Kim, S.Y.; Weinreb, R.N.; Ju, W.K. Coenzyme Q10 inhibits glutamate excitotoxicity and oxidative stress-mediated mitochondrial alteration in a mouse model of glaucoma. Investig. Ophthalmol. Vis. Sci. 2014, 55, 993–1005. [Google Scholar] [CrossRef] [Green Version]
- Davis, B.M.; Tian, K.; Pahlitzsch, M.; Brenton, J.; Ravindran, N.; Butt, G.; Malaguarnera, G.; Normando, E.M.; Guo, L.; Cordeiro, M.F. Topical Coenzyme Q10 demonstrates mitochondrial-mediated neuroprotection in a rodent model of ocular hypertension. Mitochondrion 2017, 36, 114–123. [Google Scholar] [CrossRef]
- Lulli, M.; Witort, E.; Papucci, L.; Torre, E.; Schipani, C.; Bergamini, C.; Dal Monte, M.; Capaccioli, S. Coenzyme Q10 instilled as eye drops on the cornea reaches the retina and protects retinal layers from apoptosis in a mouse model of kainate-induced retinal damage. Investig. Ophthalmol. Vis. Sci. 2012, 53, 8295–8302. [Google Scholar] [CrossRef]
- Parisi, V.; Centofanti, M.; Gandolfi, S.; Marangoni, D.; Rossetti, L.; Tanga, L.; Tardini, M.; Traina, S.; Ungaro, N.; Vetrugno, M.; et al. Effects of coenzyme Q10 in conjunction with vitamin E on retinal-evoked and cortical-evoked responses in patients with open-angle glaucoma. J. Glaucoma 2014, 23, 391–404. [Google Scholar] [CrossRef]
- Quaranta, L.; Riva, I.; Biagioli, E.; Rulli, E.; Rulli, E.; Poli, D.; Legramandi, L.; CoQun Study, G. Evaluating the effects of an ophthalmic solution of coenzyme Q10 and vitamin E in open-angle glaucoma patients: A study protocol. Adv. Ther. 2019, 36, 2506–2514. [Google Scholar] [CrossRef]
- Mozaffarieh, M.; Grieshaber, M.C.; Orgul, S.; Flammer, J. The potential value of natural antioxidative treatment in glaucoma. Surv. Ophthalmol. 2008, 53, 479–505. [Google Scholar] [CrossRef]
- Zanon-Moreno, V.; Ortega-Azorin, C.; Asensio-Marquez, E.M.; Garcia-Medina, J.J.; Pinazo-Duran, M.D.; Coltell, O.; Ordovas, J.M.; Corella, D. A multi-locus genetic risk score for primary open-angle glaucoma (POAG) variants is associated with POAG risk in a mediterranean population: Inverse correlations with plasma vitamin C and E concentrations. Int. J. Mol. Sci. 2017, 18, 2302. [Google Scholar] [CrossRef] [Green Version]
- Lopez-Riquelme, N.; Villalba, C.; Tormo, C.; Belmonte, A.; Fernandez, C.; Torralba, G.; Hernandez, F. Endothelin-1 levels and biomarkers of oxidative stress in glaucoma patients. Int. Ophthalmol. 2015, 35, 527–532. [Google Scholar] [CrossRef]
- Giaconi, J.A.; Yu, F.; Stone, K.L.; Pedula, K.L.; Ensrud, K.E.; Cauley, J.A.; Hochberg, M.C.; Coleman, A.L.; Study of Osteoporotic Fractures Research Group. The association of consumption of fruits/vegetables with decreased risk of glaucoma among older African-American women in the study of osteoporotic fractures. Am. J. Ophthalmol. 2012, 154, 635–644. [Google Scholar] [CrossRef] [Green Version]
- Verdina, T.; Passarelli, N.; Carlini, A.; Chemello, F.; Mastropasqua, R.; Cavallini, G.M. Association of ultrapure citicoline, homotaurine and vitamin E in the management of normotensive glaucoma: A case report. Case Rep. Ophthalmol. 2020, 11, 222–228. [Google Scholar] [CrossRef]
- Kang, J.H.; Pasquale, L.R.; Willett, W.; Rosner, B.; Egan, K.M.; Faberowski, N.; Hankinson, S.E. Antioxidant intake and primary open-angle glaucoma: A prospective study. Am. J. Epidemiol. 2003, 158, 337–346. [Google Scholar] [CrossRef] [Green Version]
- Ramdas, W.D.; Wolfs, R.C.; Kiefte-de Jong, J.C.; Hofman, A.; de Jong, P.T.; Vingerling, J.R.; Jansonius, N.M. Nutrient intake and risk of open-angle glaucoma: The Rotterdam Study. Eur. J. Epidemiol. 2012, 27, 385–393. [Google Scholar] [CrossRef] [Green Version]
- Williams, P.A.; Harder, J.M.; Foxworth, N.E.; Cochran, K.E.; Philip, V.M.; Porciatti, V.; Smithies, O.; John, S.W. Vitamin B3 modulates mitochondrial vulnerability and prevents glaucoma in aged mice. Science 2017, 355, 756–760. [Google Scholar] [CrossRef] [Green Version]
- Jung, K.I.; Kim, Y.C.; Park, C.K. Dietary niacin and open-angle glaucoma: The Korean National Health and Nutrition Examination Survey. Nutrients 2018, 10, 387. [Google Scholar] [CrossRef] [Green Version]
- Hui, F.; Tang, J.; Williams, P.A.; McGuinness, M.B.; Hadoux, X.; Casson, R.J.; Coote, M.; Trounce, I.A.; Martin, K.R.; van Wijngaarden, P.; et al. Improvement in inner retinal function in glaucoma with nicotinamide (vitamin B3) supplementation: A crossover randomized clinical trial. Clin. Exp. Ophthalmol. 2020. [Google Scholar] [CrossRef]
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Harada, C.; Noro, T.; Kimura, A.; Guo, X.; Namekata, K.; Nakano, T.; Harada, T. Suppression of Oxidative Stress as Potential Therapeutic Approach for Normal Tension Glaucoma. Antioxidants 2020, 9, 874. https://doi.org/10.3390/antiox9090874
Harada C, Noro T, Kimura A, Guo X, Namekata K, Nakano T, Harada T. Suppression of Oxidative Stress as Potential Therapeutic Approach for Normal Tension Glaucoma. Antioxidants. 2020; 9(9):874. https://doi.org/10.3390/antiox9090874
Chicago/Turabian StyleHarada, Chikako, Takahiko Noro, Atsuko Kimura, Xiaoli Guo, Kazuhiko Namekata, Tadashi Nakano, and Takayuki Harada. 2020. "Suppression of Oxidative Stress as Potential Therapeutic Approach for Normal Tension Glaucoma" Antioxidants 9, no. 9: 874. https://doi.org/10.3390/antiox9090874