Visual Dysfunction in Multiple Sclerosis and its Animal Model, Experimental Autoimmune Encephalomyelitis: a Review

Molecular Neurobiology - Tập 58 - Trang 3484-3493 - 2021
Taekyun Shin1, Meejung Ahn2, Jeongtae Kim3, Kyungsook Jung4, Changjong Moon5, Moon-Doo Kim6
1College of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University, Jeju, Republic of Korea
2Department of Animal Science, College of Life Science, Sangji University, Wonju, Republic of Korea
3Department of Anatomy, Kosin University College of Medicine, Busan, Republic of Korea
4Functional Biomaterials Research Center, Korea Research Institute of Bioscience and Biotechnology, Jeongeup-si, Republic of Korea
5Department of Veterinary Anatomy, College of Veterinary Medicine and BK21 Plus Project Team, Chonnam National University, Gwangju, Republic of Korea
6Department of Psychiatry, School of Medicine, Jeju National University, Jeju, Republic of Korea

Tóm tắt

Visual disabilities in central nervous system autoimmune diseases such as multiple sclerosis (MS) and its animal model, experimental autoimmune encephalomyelitis (EAE), are important symptoms. Past studies have focused on neuro-inflammatory changes and demyelination in the white matter of the brain and spinal cord. In MS, neuro-inflammatory lesions have been diagnosed in the visual pathway; the lesions may perturb visual function. Similarly, neuropathological changes in the retina and optic nerves have been found in animals with chronic EAE. Although the retina and optic nerves are immunologically privileged sites via the blood–retina barrier and blood–brain barrier, respectively, inflammation can occur via other routes, such as the uvea (e.g., iris and choroid) and cerebrospinal fluid in the meninges. This review primarily addresses the direct involvement of the blood–retina barrier and the blood–brain barrier in the development of retinitis and optic neuritis in EAE models. Additional routes, including pro-inflammatory mediator-filled choroidal and subarachnoid spaces, are also discussed with respect to their roles in EAE-induced visual disability and as analogues of MS in humans.

Tài liệu tham khảo

Bo L, Vedeler CA, Nyland HI, Trapp BD, Mork SJ (2003) Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol 62(7):723–732. https://doi.org/10.1093/jnen/62.7.723

Gray E, Thomas TL, Betmouni S, Scolding N, Love S (2008) Elevated activity and microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosis. Brain Pathol 18(1):86–95. https://doi.org/10.1111/j.1750-3639.2007.00110.x

Garcia-Martin E, Rodriguez-Mena D, Herrero R, Almarcegui C, Dolz I, Martin J, Ara JR, Larrosa JM et al (2013) Neuro-ophthalmologic evaluation, quality of life, and functional disability in patients with MS. Neurology 81(1):76–83. https://doi.org/10.1212/WNL.0b013e318299ccd9

Shin T, Kojima T, Tanuma N, Ishihara Y, Matsumoto Y (1995) The subarachnoid space as a site for precursor T cell proliferation and effector T cell selection in experimental autoimmune encephalomyelitis. J Neuroimmunol 56(2):171–178. https://doi.org/10.1016/0165-5728(94)00144-d

Soler B, Ramari C, Valet M, Dalgas U, Feys P (2020) Clinical assessment, management, and rehabilitation of walking impairment in MS: an expert review. Expert Rev Neurother 20(8):875–886. https://doi.org/10.1080/14737175.2020.1801425

Testa V, De Santis N, Scotto R, Pastorino CE, Cellerino M, Olivari S, Morlacchi AJ, Inglese M et al (2020) Neuroaxonal degeneration in patients with multiple sclerosis: an optical coherence tomography and in vivo corneal confocal microscopy study. Cornea 39(10):1221–1226. https://doi.org/10.1097/ICO.0000000000002396

Sailer M, Fischl B, Salat D, Tempelmann C, Schonfeld MA, Busa E, Bodammer N, Heinze HJ et al (2003) Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126(Pt 8):1734–1744. https://doi.org/10.1093/brain/awg175

Donadieu M, Kelly H, Szczupak D, Lin JP, Song Y, Yen CCC, Ye FQ, Kolb H et al (2020) Ultrahigh-resolution MRI reveals extensive cortical demyelination in a nonhuman primate model of multiple sclerosis. Cereb Cortex 31:439–447. https://doi.org/10.1093/cercor/bhaa235

Goektas O, Schmidt F, Bohner G, Erb K, Ludemann L, Dahlslett B, Harms L, Fleiner F (2011) Olfactory bulb volume and olfactory function in patients with multiple sclerosis. Rhinology 49(2):221–226. https://doi.org/10.4193/Rhino10.136

Satue M, Rodrigo MJ, Otin S, Bambo MP, Fuertes MI, Ara JR, Martin J, Polo V et al (2016) Relationship between visual dysfunction and retinal changes in patients with multiple sclerosis. PLoS One 11(6):e0157293. https://doi.org/10.1371/journal.pone.0157293

Britze J, Pihl-Jensen G, Frederiksen JL (2017) Retinal ganglion cell analysis in multiple sclerosis and optic neuritis: a systematic review and meta-analysis. J Neurol 264(9):1837–1853. https://doi.org/10.1007/s00415-017-8531-y

Carcelen-Gadea M, Quintanilla-Bordas C, Gracia-Garcia A, Garcia-Villanueva C, Jannone-Pedro N, Alvarez-Sanchez L, Vilaplana-Dominguez L, Blanco-Hernandez T et al (2019) Functional and structural changes in the visual pathway in multiple sclerosis. Brain Behav 9(12):e01467. https://doi.org/10.1002/brb3.1467

Doty RL, MacGillivray MR, Talab H, Tourbier I, Reish M, Davis S, Cuzzocreo JL, Shepard NT et al (2018) Balance in multiple sclerosis: relationship to central brain regions. Exp Brain Res 236(10):2739–2750. https://doi.org/10.1007/s00221-018-5332-1

Centonze D, Rossi S, Boffa L, Versace V, Palmieri MG, Caramia MD, Bernardi G (2005) CSF from MS patients can induce acute conduction block in the isolated optic nerve. Eur J Neurol 12(1):45–48. https://doi.org/10.1111/j.1468-1331.2004.00946.x

Huang J, Khademi M, Fugger L, Lindhe O, Novakova L, Axelsson M, Malmestrom C, Constantinescu C et al (2020) Inflammation-related plasma and CSF biomarkers for multiple sclerosis. Proc Natl Acad Sci U S A 117(23):12952–12960. https://doi.org/10.1073/pnas.1912839117

Swanborg RH (2001) Experimental autoimmune encephalomyelitis in the rat: lessons in T-cell immunology and autoreactivity. Immunol Rev 184:129–135. https://doi.org/10.1034/j.1600-065x.2001.1840112.x

Lassmann H (2019) The changing concepts in the neuropathology of acquired demyelinating central nervous system disorders. Curr Opin Neurol 32(3):313–319. https://doi.org/10.1097/wco.0000000000000685

Wekerle H (2008) Lessons from multiple sclerosis: models, concepts, observations. Ann Rheum Dis 67(Suppl 3):iii56–iii60. https://doi.org/10.1136/ard.2008.098020

Schmitz K, Tegeder I (2017) Bioluminescence and near-infrared imaging of optic neuritis and brain inflammation in the EAE model of multiple sclerosis in mice. J Vis Exp 121. https://doi.org/10.3791/55321

Shindler KS, Ventura E, Dutt M, Rostami A (2008) Inflammatory demyelination induces axonal injury and retinal ganglion cell apoptosis in experimental optic neuritis. Exp Eye Res 87(3):208–213. https://doi.org/10.1016/j.exer.2008.05.017

Dutt M, Tabuena P, Ventura E, Rostami A, Shindler KS (2010) Timing of corticosteroid therapy is critical to prevent retinal ganglion cell loss in experimental optic neuritis. Invest Ophthalmol Vis Sci 51(3):1439–1445. https://doi.org/10.1167/iovs.09-4009

Meeson AP, Piddlesden S, Morgan BP, Reynolds R (1994) The distribution of inflammatory demyelinated lesions in the central nervous system of rats with antibody-augmented demyelinating experimental allergic encephalomyelitis. Exp Neurol 129(2):299–310. https://doi.org/10.1006/exnr.1994.1172

Hasan M, Min H, Rahaman KA, Muresan AR, Kim H, Han D, Kwon OS (2019) Quantitative proteome analysis of brain subregions and spinal cord from experimental autoimmune encephalomyelitis mice by TMT-based mass spectrometry. Proteomics 19(5):e1800355. https://doi.org/10.1002/pmic.201800355

Shields DC, Tyor WR, Deibler GE, Banik NL (1998) Increased calpain expression in experimental demyelinating optic neuritis: an immunocytochemical study. Brain Res 784(1-2):299–304. https://doi.org/10.1016/s0006-8993(97)01381-4

Das A, Guyton MK, Smith A, Wallace G, McDowell ML, Matzelle DD, Ray SK, Banik NL (2013) Calpain inhibitor attenuated optic nerve damage in acute optic neuritis in rats. J Neurochem 124(1):133–146. https://doi.org/10.1111/jnc.12064

Manogaran P, Samardzija M, Schad AN, Wicki CA, Walker-Egger C, Rudin M, Grimm C, Schippling S (2019) Correction to: Retinal pathology in experimental optic neuritis is characterized by retrograde degeneration and gliosis. Acta Neuropathol Commun 7(1):157. https://doi.org/10.1186/s40478-019-0825-0

Villarroya H, Klein C, Thillaye-Goldenberg B, Eclancher F (2001) Distribution in ocular structures and optic pathways of immunocompetent and glial cells in an experimental allergic encephalomyelitis (EAE) relapsing model. J Neurosci Res 63(6):525–535. https://doi.org/10.1002/jnr.1047

Castoldi V, Marenna S, d’Isa R, Huang SC, De Battista D, Chirizzi C, Chaabane L, Kumar D et al (2020) Non-invasive visual evoked potentials to assess optic nerve involvement in the dark agouti rat model of experimental autoimmune encephalomyelitis induced by myelin oligodendrocyte glycoprotein. Brain Pathol 30(1):137–150. https://doi.org/10.1111/bpa.12762

Hsu M, Rayasam A, Kijak JA, Choi YH, Harding JS, Marcus SA, Karpus WJ, Sandor M et al (2019) Neuroinflammation-induced lymphangiogenesis near the cribriform plate contributes to drainage of CNS-derived antigens and immune cells. Nat Commun 10(1):229. https://doi.org/10.1038/s41467-018-08163-0

Weller RO (1998) Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol 57(10):885–894. https://doi.org/10.1097/00005072-199810000-00001

Shin T, Matsumoto Y (2001) A quantitative analysis of CD45Rlow CD4+ T cells in the subarachnoid space of Lewis rats with autoimmune encephalomyelitis. Immunol Investig 30(1):57–64. https://doi.org/10.1081/imm-100103691

Jouve L, Benrabah R, Héron E, Bodaghi B, Le Hoang P, Touitou V (2017) Multiple sclerosis-related uveitis: does MS treatment affect uveitis course? Ocul Immunol Inflamm 25(3):302–307. https://doi.org/10.3109/09273948.2015.1125508

Fairless R, Williams SK, Hoffmann DB, Stojic A, Hochmeister S, Schmitz F, Storch MK, Diem R (2012) Preclinical retinal neurodegeneration in a model of multiple sclerosis. J Neurosci 32(16):5585–5597. https://doi.org/10.1523/JNEUROSCI.5705-11.2012

Adamus G, Machnicki M, Amundson D, Adlard K, Offner H (1997) Similar pattern of MCP-1 expression in spinal cords and eyes of Lewis rats with experimental autoimmune encephalomyelitis associated anterior uveitis. J Neurosci Res 50(4):531–538. https://doi.org/10.1002/(sici)1097-4547(19971115)50:4<531::aid-jnr4>3.0.co;2-f

Adamus G, Sugden B, Arendt A, Hargrave PA (2001) Importance of cryptic myelin basic protein epitopes in the pathogenicity of acute and recurrent anterior uveitis associated with EAE. J Neuroimmunol 113(2):212–219. https://doi.org/10.1016/s0165-5728(00)00439-2

Mastorakos P, McGavern D (2019) The anatomy and immunology of vasculature in the central nervous system. Sci Immunol 4(37). https://doi.org/10.1126/sciimmunol.aav0492

Horstmann L, Kuehn S, Pedreiturria X, Haak K, Pfarrer C, Dick HB, Kleiter I, Joachim SC (2016) Microglia response in retina and optic nerve in chronic experimental autoimmune encephalomyelitis. J Neuroimmunol 298:32–41. https://doi.org/10.1016/j.jneuroim.2016.06.008

Jin J, Smith MD, Kersbergen CJ, Kam TI, Viswanathan M, Martin K, Dawson TM, Dawson VL et al (2019) Glial pathology and retinal neurotoxicity in the anterior visual pathway in experimental autoimmune encephalomyelitis. Acta Neuropathol Commun 7(1):125. https://doi.org/10.1186/s40478-019-0767-6

Vecino E, Rodriguez FD, Ruzafa N, Pereiro X, Sharma SC (2016) Glia-neuron interactions in the mammalian retina. Prog Retin Eye Res 51:1–40. https://doi.org/10.1016/j.preteyeres.2015.06.003

Lefevere E, Salinas-Navarro M, Andries L, Noterdaeme L, Etienne I, Van Wonterghem E, Vinckier S, Davis BM et al (2020) Tightening the retinal glia limitans attenuates neuroinflammation after optic nerve injury. Glia 68(12):2643–2660. https://doi.org/10.1002/glia.23875

Sonia D’Souza C, Li Z, Luke Maxwell D, Trusler O, Murphy M, Crewther S, Peter K, Orian JM (2018) Platelets drive inflammation and target gray matter and the retina in autoimmune-mediated encephalomyelitis. J Neuropathol Exp Neurol 77(7):567–576. https://doi.org/10.1093/jnen/nly032

Sonn I, Nakamura M, Renault-Mihara F, Okano H (2020) Polarization of reactive astrocytes in response to spinal cord injury is enhanced by M2 macrophage-mediated activation of Wnt/beta-Catenin pathway. Mol Neurobiol 57(4):1847–1862. https://doi.org/10.1007/s12035-019-01851-y

Lloyd AF, Miron VE (2019) The pro-remyelination properties of microglia in the central nervous system. Nat Rev Neurol 15(8):447–458. https://doi.org/10.1038/s41582-019-0184-2

Eastlake K, Luis J, Limb GA (2020) Potential of Muller glia for retina neuroprotection. Curr Eye Res 45(3):339–348. https://doi.org/10.1080/02713683.2019.1648831

Shin T, Kang B, Tanuma N, Matsumoto Y, Wie M, Ahn M, Kang J (2001) Intrathecal administration of endothelin-1 receptor antagonist ameliorates autoimmune encephalomyelitis in Lewis rats. Neuroreport 12(7):1465–1468. https://doi.org/10.1097/00001756-200105250-00034

Pradeep T, Mehra D, Le PH (2020) Histology, Eye. In: StatPearls. © 2020, StatPearls Publishing LLC., Treasure Island FL,