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Current Medicinal Chemistry

Current Medicinal Chemistry

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ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

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Review Article

Neurodegenerative Process Linking the Eye and the Brain

Author(s): Raffaele Mancino, Massimo Cesareo, Alessio Martucci, Emiliano Di Carlo, Elena Ciuffoletti, Clarissa Giannini, Luigi Antonio Morrone, Carlo Nucci* and Francesco Garaci

Volume 26, Issue 20, 2019

Page: [3754 - 3763] Pages: 10

DOI: 10.2174/0929867325666180307114332

Price: $65

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Abstract

Recent literature agrees that neurodegenerative processes involve both the retina and the central nervous system, which are two strictly related anatomical structures. However, the causal mechanisms of this dual involvement are still uncertain. To date, anterograde transsynaptic neurodegeneration, triggered by retinal ganglion cells’ death, and retrograde transsynaptic neurodegeneration, induced by neurodegenerative processes of the central nervous system, has been considered the major possible causal mechanisms. The development of novel neuroimaging techniques has recently supported both the study of the central stations of the visual pathway as well as the study of the retina which is possibly an open window to the central nervous system.

Keywords: Neurodegeneration, MRI, eye, central nervous system, glaucoma, Alzheimer, Parkinson, multiple sclerosis.

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[1]
Cedrone, C.; Mancino, R.; Cerulli, A.; Cesareo, M.; Nucci, C. Epidemiology of primary glaucoma: prevalence, incidence, and blinding effects. In: Prog. Brain Res; , 2008; 173, pp. 3-14.
[http://dx.doi.org/10.1016/S0079-6123(08)01101-1] [PMID: 18929097]
[2]
Nucci, C.; Martucci, A.; Cesareo, M.; Mancino, R.; Russo, R.; Bagetta, G.; Cerulli, L.; Garaci, F.G. Brain involvement in glaucoma: advanced neuroimaging for understanding and monitoring a new target for therapy. Curr. Opin. Pharmacol., 2013, 13(1), 128-133.
[http://dx.doi.org/10.1016/j.coph.2012.08.004] [PMID: 22981808]
[3]
Sena, D.F.; Lindsley, K. Neuroprotection for treatment of glaucoma in adults. Cochrane Database Syst. Rev., 2017, 1, CD006539.
[http://dx.doi.org/10.1002/14651858.CD006539.pub4] [PMID: 28122126]
[4]
Gupta, N.; Ang, L.C.; Noël de Tilly, L.; Bidaisee, L.; Yücel, Y.H. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br. J. Ophthalmol., 2006, 90(6), 674-678.
[http://dx.doi.org/10.1136/bjo.2005.086769] [PMID: 16464969]
[5]
Mastropasqua, R.; Agnifili, L.; Mattei, P.A.; Caulo, M.; Fasanella, V.; Navarra, R.; Mastropasqua, L.; Marchini, G. Advanced morphological and functional magnetic resonance techniques in glaucoma. BioMed Res. Int., 2015, 2015, 160454.
[http://dx.doi.org/10.1155/2015/160454] [PMID: 26167474]
[6]
Garaci, F.G.; Bolacchi, F.; Cerulli, A.; Melis, M.; Spanò, A.; Cedrone, C.; Floris, R.; Simonetti, G.; Nucci, C. Optic nerve and optic radiation neurodegeneration in patients with glaucoma: in vivo analysis with 3-T diffusion-tensor MR imaging. Radiology, 2009, 252(2), 496-501.
[http://dx.doi.org/10.1148/radiol.2522081240] [PMID: 19435941]
[7]
Nucci, C.; Mancino, R.; Martucci, A.; Bolacchi, F.; Manenti, G.; Cedrone, C.; Culasso, F.; Floris, R.; Cerulli, L.; Garaci, F.G. 3-T Diffusion tensor imaging of the optic nerve in subjects with glaucoma: correlation with GDx-VCC, HRT-III and Stratus optical coherence tomography findings. Br. J. Ophthalmol., 2012, 96(7), 976-980.
[http://dx.doi.org/10.1136/bjophthalmol-2011-301280] [PMID: 22628535]
[8]
Bolacchi, F.; Garaci, F.G.; Martucci, A.; Meschini, A.; Fornari, M.; Marziali, S.; Mancino, R.; Squillaci, E.; Floris, R.; Cerulli, L.; Simonetti, G.; Nucci, C. Differences between proximal versus distal intraorbital optic nerve diffusion tensor magnetic resonance imaging properties in glaucoma patients. Invest. Ophthalmol. Vis. Sci., 2012, 53(7), 4191-4196.
[http://dx.doi.org/10.1167/iovs.11-9345] [PMID: 22570349]
[9]
Nucci, C.; Russo, R.; Martucci, A.; Giannini, C.; Garaci, F.; Floris, R.; Bagetta, G.; Morrone, L.A. New strategies for neuroprotection in glaucoma, a disease that affects the central nervous system. Eur. J. Pharmacol., 2016, 787, 119-126.
[http://dx.doi.org/10.1016/j.ejphar.2016.04.030] [PMID: 27089818]
[10]
Cesareo, M.; Martucci, A.; Ciuffoletti, E.; Mancino, R.; Cerulli, A.; Sorge, R.P.; Martorana, A.; Sancesario, G.; Nucci, C. Association between alzheimer’s disease and glaucoma: Astudy based on heidelberg retinal tomography and frequency doubling technology perimetry. Front. Neurosci., 2015, 9, 479.
[http://dx.doi.org/10.3389/fnins.2015.00479] [PMID: 26733792]
[11]
Nucci, C.; Martucci, A.; Martorana, A.; Sancesario, G.M.; Cerulli, L. Glaucoma progression associated with altered cerebral spinal fluid levels of amyloid beta and tau proteins. Clin. Exp. Ophthalmol., 2011, 39(3), 279-281.
[http://dx.doi.org/10.1111/j.1442-9071.2010.02452.x] [PMID: 20973903]
[12]
Nucci, C.; Martucci, A.; Cesareo, M.; Garaci, F.; Morrone, L.A.; Russo, R.; Corasaniti, M.T.; Bagetta, G.; Mancino, R. Links among glaucoma, neurodegenerative, and vascular diseases of the central nervous system. In: Prog. Brain Res; , 2015; 221, pp. 159-175.
[http://dx.doi.org/10.1016/bs.pbr.2015.06.004] [PMID: 26518077]
[13]
Nucci, C.; Martucci, A.; Mancino, R.; Cerulli, L. Glaucoma progression associated with Leber’s hereditary optic neuropathy. Int. Ophthalmol., 2013, 33(1), 75-77.
[http://dx.doi.org/10.1007/s10792-012-9623-4] [PMID: 22983441]
[14]
Altobelli, S.; Toschi, N.; Mancino, R.; Nucci, C.; Schillaci, O.; Floris, R.; Garaci, F. Brain imaging in glaucoma from clinical studies to clinical practice. Prog. Brain Res.,, 2015, 221, 159-175.
[http://dx.doi.org/10.1016/bs.pbr.2015.06.004] [PMID: 26518077]
[15]
Jones-Odeh, E.; Hammond, C.J. How strong is the relationship between glaucoma, the retinal nerve fibre layer, and neurodegenerative diseases such as Alzheimer’s disease and multiple sclerosis? Eye (Lond.), 2015, 29(10), 1270-1284.
[http://dx.doi.org/10.1038/eye.2015.158] [PMID: 26337943]
[16]
Parisi, V.; Restuccia, R.; Fattapposta, F.; Mina, C.; Bucci, M.G.; Pierelli, F. Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin. Neurophysiol., 2001, 112(10), 1860-1867.
[http://dx.doi.org/10.1016/S1388-2457(01)00620-4] [PMID: 11595144]
[17]
Lu, Y.; Li, Z.; Zhang, X.; Ming, B.; Jia, J.; Wang, R.; Ma, D. Retinal nerve fiber layer structure abnormalities in early Alzheimer’s disease: evidence in optical coherence tomography. Neurosci. Lett., 2010, 480(1), 69-72.
[http://dx.doi.org/10.1016/j.neulet.2010.06.006] [PMID: 20609426]
[18]
Iseri, P.K.; Altinaş, O.; Tokay, T.; Yüksel, N. Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J. Neuroophthalmol., 2006, 26(1), 18-24.
[http://dx.doi.org/10.1097/01.wno.0000204645.56873.26] [PMID: 16518161]
[19]
Paquet, C.; Boissonnot, M.; Roger, F.; Dighiero, P.; Gil, R.; Hugon, J. Abnormal retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease. Neurosci. Lett., 2007, 420(2), 97-99.
[http://dx.doi.org/10.1016/j.neulet.2007.02.090] [PMID: 17543991]
[20]
Kesler, A.; Vakhapova, V.; Korczyn, A.D.; Naftaliev, E.; Neudorfer, M. Retinal thickness in patients with mild cognitive impairment and Alzheimer’s disease. Clin. Neurol. Neurosurg., 2011, 113(7), 523-526.
[http://dx.doi.org/10.1016/j.clineuro.2011.02.014] [PMID: 21454010]
[21]
Fisichella, V.; Giurdanella, G.; Platania, C.B.; Romano, G.L.; Leggio, G.M.; Salomone, S.; Drago, F.; Caraci, F.; Bucolo, C. TGF-β1 prevents rat retinal insult induced by amyloid-β (1-42) oligomers. Eur. J. Pharmacol., 2016, 787(787), 72-77.
[http://dx.doi.org/10.1016/j.ejphar.2016.02.002] [PMID: 26845696]
[22]
Romano, G.L.; Platania, C.B.; Forte, S.; Salomone, S.; Drago, F.; Bucolo, C. MicroRNA target prediction in glaucoma. In: Prog. Brain Res; , 2015; 220, pp. 217-240.
[http://dx.doi.org/10.1016/bs.pbr.2015.04.013] [PMID: 26497793]
[23]
Garcia-Martin, E.; Pablo, L.E.; Bambo, M.P.; Alarcia, R.; Polo, V.; Larrosa, J.M.; Vilades, E.; Cameo, B.; Orduna, E.; Ramirez, T.; Satue, M. Comparison of peripapillary choroidal thickness between healthy subjects and patients with Parkinson’s disease. PLoS One, 2017, 12(5), e0177163.
[http://dx.doi.org/10.1371/journal.pone.0177163] [PMID: 28510576]
[24]
Živković, M.; Dayanir, V.; Stamenović, J.; Ljubisavljević, S.; Pražić, A.; Zlatanović, M.; Zlatanović, G.; Jakšić, V.; Radenković, M.; Jovanović, S. Retinal ganglion cell/inner plexiform layer thickness in patients with Parkinson’s disease. Folia Neuropathol., 2017, 55(2), 168-173.
[http://dx.doi.org/10.5114/fn.2017.68584] [PMID: 28677374]
[25]
Satue, M.; Rodrigo, M.J.; Obis, J.; Vilades, E.; Gracia, H.; Otin, S.; Fuertes, M.I.; Alarcia, R.; Crespo, J.A.; Polo, V.; Larrosa, J.M.; Pablo, L.E.; Garcia-Martin, E. Evaluation of progressive visual dysfunction and retinal degeneration in patients with parkinson’s disease. Invest. Ophthalmol. Vis. Sci., 2017, 58(2), 1151-1157.
[http://dx.doi.org/10.1167/iovs.16-20460] [PMID: 28208185]
[26]
Lee, J.Y.; Ahn, J.; Kim, T.W.; Jeon, B.S. Optical coherence tomography in Parkinson’s disease: is the retina a biomarker? J. Parkinsons Dis., 2014, 4(2), 197-204.
[PMID: 24518436]
[27]
Toussaint, D.; Périer, O.; Verstappen, A.; Bervoets, S. Clinicopathological study of the visual pathways, eyes, and cerebral hemispheres in 32 cases of disseminated sclerosis. J. Clin. Neuroophthalmol., 1983, 3(3), 211-220.
[PMID: 6226722]
[28]
Green, A.J.; McQuaid, S.; Hauser, S.L.; Allen, I.V.; Lyness, R. Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain, 2010, 133(Pt 6), 1591-1601.
[http://dx.doi.org/10.1093/brain/awq080] [PMID: 20410146]
[29]
Parisi, V.; Manni, G.; Spadaro, M.; Colacino, G.; Restuccia, R.; Marchi, S.; Bucci, M.G.; Pierelli, F. Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest. Ophthalmol. Vis. Sci., 1999, 40(11), 2520-2527.
[PMID: 10509645]
[30]
Graham, E.C.; You, Y.; Yiannikas, C.; Garrick, R.; Parratt, J.; Barnett, M.H.; Klistorner, A. Progressive loss of retinal ganglion cells and axons in nonoptic neuritis eyes in multiple sclerosis: a longitudinal optical coherence tomography study. Invest. Ophthalmol. Vis. Sci., 2016, 57(4), 2311-2317.
[http://dx.doi.org/10.1167/iovs.15-19047] [PMID: 27127930]
[31]
Saidha, S.; Sotirchos, E.S.; Oh, J.; Syc, S.B.; Seigo, M.A.; Shiee, N.; Eckstein, C.; Durbin, M.K.; Oakley, J.D.; Meyer, S.A.; Frohman, T.C.; Newsome, S.; Ratchford, J.N.; Balcer, L.J.; Pham, D.L.; Crainiceanu, C.M.; Frohman, E.M.; Reich, D.S.; Calabresi, P.A. Relationships between retinal axonal and neuronal measures and global central nervous system pathology in multiple sclerosis. JAMA Neurol., 2013, 70(1), 34-43.
[http://dx.doi.org/10.1001/jamaneurol.2013.573] [PMID: 23318513]
[32]
Martinez-Lapiscina, E.H.; Arnow, S.; Wilson, J.A.; Saidha, S.; Preiningerova, J.L.; Oberwahrenbrock, T.; Brandt, A.U.; Pablo, L.E.; Guerrieri, S.; Gonzalez, I.; Outteryck, O.; Mueller, A.K.; Albrecht, P.; Chan, W.; Lukas, S.; Balk, L.J.; Fraser, C.; Frederiksen, J.L.; Resto, J.; Frohman, T.; Cordano, C.; Zubizarreta, I.; Andorra, M.; Sanchez-Dalmau, B.; Saiz, A.; Bermel, R.; Klistorner, A.; Petzold, A.; Schippling, S.; Costello, F.; Aktas, O.; Vermersch, P.; Oreja-Guevara, C.; Comi, G.; Leocani, L.; Garcia-Martin, E.; Paul, F.; Havrdova, E.; Frohman, E.; Balcer, L.J.; Green, A.J.; Calabresi, P.A.; Villoslada, P. Retinal thickness measured with optical coherence tomography and risk of disability worsening in multiple sclerosis: a cohort study. Lancet Neurol., 2016, 15(6), 574-584.
[http://dx.doi.org/10.1016/S1474-4422(16)00068-5] [PMID: 27011339]
[33]
Saidha, S.; Al-Louzi, O.; Ratchford, J.N.; Bhargava, P.; Oh, J.; Newsome, S.D.; Prince, J.L.; Pham, D.; Roy, S.; van Zijl, P.; Balcer, L.J.; Frohman, E.M.; Reich, D.S.; Crainiceanu, C.; Calabresi, P.A. Optical coherence tomography reflects brain atrophy in multiple sclerosis: as four-year study. Ann. Neurol., 2015, 78(5), 801-813.
[http://dx.doi.org/10.1002/ana.24487] [PMID: 26190464]
[34]
Garcia-Martin, E.; Polo, V.; Larrosa, J.M.; Marques, M.L.; Herrero, R.; Martin, J.; Ara, J.R.; Fernandez, J.; Pablo, L.E. Retinal layer segmentation in patients with multiple sclerosis using spectral domain optical coherence tomography. Ophthalmology, 2014, 121(2), 573-579.
[http://dx.doi.org/10.1016/j.ophtha.2013.09.035] [PMID: 24268855]
[35]
Britze, J.; Pihl-Jensen, G.; Frederiksen, J.L. Retinal ganglion cell analysis in multiple sclerosis and optic neuritis: a systematic review and meta-analysis. J. Neurol., 2017, 264(9), 1837-1853.
[http://dx.doi.org/10.1007/s00415-017-8531-y] [PMID: 28567539]
[36]
Coric, D.; Balk, L.J.; Verrijp, M.; Eijlers, A.; Schoonheim, M.M.; Killestein, J.; Uitdehaag, B.M.; Petzold, A. Cognitive impairment in patients with multiple sclerosis is associated with atrophy of the inner retinal layers. Mult. Scler., 2017, 24(2), 158-166.
[http://dx.doi.org/10.1177/1352458517694090] [PMID: 28273785]
[37]
Balk, L.J.; Coric, D.; Nij Bijvank, J.A.; Killestein, J.; Uitdehaag, B.M.; Petzold, A. Retinal atrophy in relation to visual functioning and vision-related quality of life in patients with multiple sclerosis. Mult. Scler., 2017, 11352458517708463.
[http://dx.doi.org/journals.sagepub.com/doi10.1177/1352458517708463] [PMID: 28511578]
[38]
Knier, B.; Schmidt, P.; Aly, L.; Buck, D.; Berthele, A.; Mühlau, M.; Zimmer, C.; Hemmer, B.; Korn, T. Retinal inner nuclear layer volume reflects response to immunotherapy in multiple sclerosis. Brain, 2016, 139(11), 2855-2863.
[http://dx.doi.org/10.1093/brain/aww219] [PMID: 27581073]
[39]
Button, J.; Al-Louzi, O.; Lang, A.; Bhargava, P.; Newsome, S.D.; Frohman, T.; Balcer, L.J.; Frohman, E.M.; Prince, J.; Calabresi, P.A.; Saidha, S. Disease-modifying therapies modulate retinal atrophy in multiple sclerosis: A retrospective study. Neurology, 2017, 7, 88(6), 525-532.
[http://dx.doi.org/10.1212/WNL.0000000000003582] [PMID: 28077493]
[40]
Rossi, S.; Mancino, R.; Bergami, A.; Mori, F.; Castelli, M.; De Chiara, V.; Studer, V.; Mataluni, G.; Sancesario, G.; Parisi, V.; Kusayanagi, H.; Bernardi, G.; Nucci, C.; Bernardini, S.; Martino, G.; Furlan, R.; Centonze, D. Potential role of IL-13 in neuroprotection and cortical excitability regulation in multiple sclerosis. Mult. Scler., 2011, 17(11), 1301-1312.
[http://dx.doi.org/10.1177/1352458511410342] [PMID: 21677024]
[41]
Vanburen, J.M. Trans-synaptic retrograde degeneration in the visual system of primates. J. Neurol. Neurosurg. Psychiatry, 1963, 26, 402-409.
[http://dx.doi.org/10.1136/jnnp.26.5.402] [PMID: 14066630]
[42]
Beatty, R.M.; Sadun, A.A.; Smith, L.; Vonsattel, J.P.; Richardson, E.P., Jr Direct demonstration of transsynaptic degeneration in the human visual system: A comparison of retrograde and anterograde changes. J. Neurol. Neurosurg. Psychiatry, 1982, 45(2), 143-146.
[http://dx.doi.org/10.1136/jnnp.45.2.143] [PMID: 7069426]
[43]
Cowey, A.; Alexander, I.; Stoerig, P. Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans. Brain, 2011, 134(Pt 7), 2149-2157.
[http://dx.doi.org/10.1093/brain/awr125] [PMID: 21705429]
[44]
Johnson, H.; Cowey, A. Transneuronal retrograde degeneration of retinal ganglion cells following restricted lesions of striate cortex in the monkey. Exp. Brain Res., 2000, 132(2), 269-275.
[http://dx.doi.org/10.1007/s002210000384] [PMID: 10853951]
[45]
Jindahara, P.; Petrie, A.; Plant, G.T. The time course of retrograde trans-synaptic degeneration following occipital lobe damage in humans. Brain, 2012, 135(Pt2), 534-541.
[http://dx.doi.org/10.1093/brain/awr324] [PMID: 22300877]
[46]
Keller, J.; Sánchez-Dalmau, B.F.; Villoslada, P. Lesions in the posterior visual pathway promote trans-synaptic degeneration of retinal ganglion cells. PLoS One, 2014, 9(5), e97444.
[http://dx.doi.org/10.1371/journal.pone.0097444] [PMID: 24857938]
[47]
Patel, K.R.; Ramsey, L.E.; Metcalf, N.V.; Shulman, G.L.; Corbetta, M. Early diffusion evidence of retrograde transsynaptic degeneration in the human visual system. Neurology, 2016, 87(2), 198-205.
[http://dx.doi.org/10.1212/WNL.0000000000002841] [PMID: 27306632]
[48]
Dinkin, M. Trans-synaptic retrograde degeneration in the human visual system: Slow, silent, and real. Curr. Neurol. Neurosci. Rep., 2017, 17(2), 16.
[http://dx.doi.org/10.1007/s11910-017-0725-2] [PMID: 28229400]
[49]
Vien, L.; DalPorto, C.; Yang, D. Retrograde degeneration of retinal ganglion cells secondary to head Trauma. Optom. Vis. Sci., 2017, 94(1), 125-134.
[http://dx.doi.org/10.1097/OPX.0000000000000899] [PMID: 27273271]
[50]
Jacob, M.; Raverot, G.; Jouanneau, E.; Borson-Chazot, F.; Perrin, G.; Rabilloud, M.; Tilikete, C.; Bernard, M.; Vighetto, A. Predicting visual outcome after treatment of pituitary adenomas with optical coherence tomography. Am.J. Ophthalmol., 2009, 147(1), 64-70 e62..
[http://dx.doi.org/10.1016/j.ajo.2008.07.016] [PMID: 18774545]
[51]
Hood, D.C.; Kardon, R.H. A framework for comparing structural and functional measures of glaucomatous damage. Prog. Retin. Eye Res., 2007, 26(6), 688-710.
[http://dx.doi.org/10.1016/j.preteyeres.2007.08.001] [PMID: 17889587]
[52]
Ohkubo, S.; Higashide, T.; Takeda, H.; Murotani, E.; Hayashi, Y.; Sugiyama, K. Relationship between macular ganglion cell complex parameters and visual field parameters after tumor resection in chiasmal compression. Jpn. J. Ophthalmol., 2012, 56(1), 68-75.
[http://dx.doi.org/10.1007/s10384-011-0093-4] [PMID: 21975828]
[53]
Cesareo, M.; Ciuffoletti, E.; Martucci, A.; Sebastiani, J.; Sorge, R.P.; Lamantea, E.; Garavaglia, B.; Ricci, F.; Cusumano, A.; Nucci, C.; Brancati, F. Assessment of the retinal posterior pole in dominant optic atrophy by spectral-domain optical coherence tomography and microperimetry. PLoS One, 2017, 12(3), e0174560.
[http://dx.doi.org/dx. doi: 10.1371/journal.pone.0174560] [PMID: 28358911]

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