Review: Tauopathy in the retina and optic nerve: Does it shadow pathological changes in the brain?

Molecular Vision

Volumn 18, Issue , 2012, Pages 2700-2710

  Ho, Wing Lau ^a   Leung, Yen ^a   Tsang, Andrea Wing Ting ^a   So, Kwok Fai ^a   Chiu, Kin ^a   Chang, Raymond Chuen Chung ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIN DEPENDENT KINASE 5; EPHRIN A TYROSINE KINASE RECEPTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN KINASE FYN; PROTEIN P25; PROTEIN P35; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN ASSOCIATED KINASE; TAU PROTEIN; TYROSINE KINASE RECEPTOR; UBIQUINONE; UBIQUINONE OXIDOREDUCTASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; DIABETIC RETINOPATHY; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GLIA CELL; HISTOPATHOLOGY; HUMAN; IMMUNOREACTIVITY; INTRAOCULAR HYPERTENSION; NERVE CELL; NONHUMAN; OPEN ANGLE GLAUCOMA; OPTIC NERVE DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RETINA; RETINA DISEASE; RETINA GANGLION CELL; RETINA MACULA AGE RELATED DEGENERATION; RETINITIS PIGMENTOSA; REVIEW; TAU GENE; TAUOPATHY; TRANSGENIC MOUSE; VISUAL SYSTEM PARAMETERS;

ALZHEIMER DISEASE; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; EXONS; FRONTOTEMPORAL DEMENTIA; GLAUCOMA; HUMANS; OPTIC NERVE; RETINA; TAU PROTEINS; TAUOPATHIES;

EID: 84870047040     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Review

References (69)

1. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathol 2009; 118:167-79. [PMID: 19390859].
2. Spires-Jones TL, Stoothoff WH, de Calignon A, Jones PB, Hyman BT. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci 2009; 32:150-9. [PMID: 19162340].
3. Katz B, Rimmer S, Iragui V, Katzman R. Abnormal pattern electroretinogram in Alzheimer's disease: evidence for retinal ganglion cell degeneration? Ann Neurol 1989; 26:221-5. [PMID: 2774509].
4. Jackson GR, Owsley C. Visual dysfunction, neurodegenerative diseases, and aging. Neurol Clin 2003; 21:709-28. [PMID: 13677819].
5. Lee AG, Martin CO. Neuro-ophthalmic findings in the visual variant of Alzheimer's disease. Ophthalmology 2004; 111:376-80. [PMID: 15019393].
6. Cronin-Golomb A, Corkin S, Rizzo JF, Cohen J, Growdon JH, Banks KS. Visual dysfunction in Alzheimer's disease: relation to normal aging. Ann Neurol 1991; 29:41-52. [PMID: 1996878].
7. Mendez MF, Cherrier MM, Meadows RS. Depth perception in Alzheimer's disease. Percept Mot Skills 1996; 83:987-95. [PMID: 8961335].
8. Cronin-Golomb A. Vision in Alzheimer's disease. Gerontologist 1995; 35:370-6. [PMID: 7622089].
9. Gilmore GC, Whitehouse PJ. Contrast sensitivity in Alzheimer's disease: a 1-year longitudinal analysis. Optom Vis Sci 1995; 72:83-91. [PMID: 7753532].
10. 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; 420:97-9. [PMID: 17543991].
11. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL. Retinal abnormalities in early Alzheimer's disease. Invest Ophthalmol Vis Sci 2007; 48:2285-9. [PMID: 17460292].
12. Iseri PK, Altinas O, Tokay T, Yuksel N. Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J Neuroophthalmol 2006; 26:18-24. [PMID: 16518161].
13. Parisi V. Correlation between morphological and functional retinal impairment in patients affected by ocular hypertension, glaucoma, demyelinating optic neuritis and Alzheimer's disease. Semin Ophthalmol 2003; 18:50-7. [PMID: 14566623].
14. Valenti DA. Neuroimaging of retinal nerve fiber layer in AD using optical coherence tomography. Neurology 2007; 69:1060-[PMID: 17785676].
15. Danesh-Meyer HV, Birch H, Ku JY, Carroll S, Gamble G. Reduction of optic nerve fibers in patients with Alzheimer disease identified by laser imaging. Neurology 2006; 67:1852-4. [PMID: 17130422].
16. Hinton DR, Sadun AA, Blanks JC, Miller CA. Optic-nerve degeneration in Alzheimer's disease. N Engl J Med 1986; 315:485-7. [PMID: 3736630].
17. Sadun AA, Bassi CJ. Optic nerve damage in Alzheimer's disease. Ophthalmology 1990; 97:9-17. [PMID: 2314849].
18. Blanks JC, Hinton DR, Sadun AA, Miller CA. Retinal ganglion cell degeneration in Alzheimer's disease. Brain Res 1989; 501:364-72. [PMID: 2819446].
19. Guo L, Duggan J, Cordeiro MF. Alzheimer's disease and retinal neurodegeneration. Curr Alzheimer Res 2010; 7:3-14. [PMID: 20205667].
20. Ning A, Cui J, To E, Ashe KH, Matsubara J. Amyloid-beta deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Invest Ophthalmol Vis Sci 2008; 49:5136-43. [PMID: 18566467].
21. Shimazawa M, Inokuchi Y, Okuno T, Nakajima Y, Sakaguchi G, Kato A, Oku H, Sugiyama T, Kudo T, Ikeda T, Takeda M, Hara H. Reduced retinal function in amyloid precursor protein-over-expressing transgenic mice via attenuating glutamate-N-methyl-d-aspartate receptor signaling. J Neurochem 2008; 107:279-90. [PMID: 18691390].
22. Morris M, Maeda S, Vossel K, Mucke L. The many faces of tau. Neuron 2011; 70:410-26. [PMID: 21555069].
23. Liu F, Gong CX. Tau exon 10 alternative splicing and tauopathies. Mol Neurodegener 2008; 3:8-[PMID: 18616804].
24. Shahani N, Brandt R. Functions and malfunctions of the tau proteins. Cell Mol Life Sci 2002; 59:1668-80. [PMID: 12475178].
25. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA, Eckert A, Staufenbiel M, Hardeman E, Gotz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010; 142:387-97. [PMID: 20655099].
26. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 2001; 114:1179-87. [PMID: 11228161].
27. Hwang SC, Jhon DY, Bae YS, Kim JH, Rhee SG. Activation of phospholipase C-gamma by the concerted action of tau proteins and arachidonic acid. J Biol Chem 1996; 271:18342-9. [PMID: 8702475].
28. Perez M, Santa-Maria I, Gomez de Barreda E, Zhu X, Cuadros R, Cabrero JR, Sanchez-Madrid F, Dawson HN, Vitek MP, Perry G, Smith MA, Avila J. Tau-an inhibitor of deacetylase HDAC6 function. J Neurochem 2009; 109:1756-66. [PMID: 19457097].
29. Miao Y, Chen J, Zhang Q, Sun A. Deletion of tau attenuates heat shock-induced injury in cultured cortical neurons. J Neurosci Res 2010; 88:102-10. [PMID: 19642195].
30. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 1998; 282:1914-7. [PMID: 9836646].
31. Denk F, Wade-Martins R. Knock-out and transgenic mouse models of tauopathies. Neurobiol Aging 2009; 30:1-13. [PMID: 17590238].
32. Goedert M, Ghetti B, Spillantini MG. Tau Gene Mutations in Frontotemporal Dementia and Parkinsonism Linked to Chromosome 17 (FTDP-17). Ann N Y Acad Sci 2000; 920:74-83. [PMID: 11193179].
33. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000; 25:402-5. [PMID: 10932182].
34. Lin WL, Zehr C, Lewis J, Hutton M, Yen SH, Dickson DW. Progressive white matter pathology in the spinal cord of transgenic mice expressing mutant (P301L) human tau. J Neurocytol 2005; 34:397-410. [PMID: 16902761].
35. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW. Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J Neurocytol 2003; 32:1091-105. [PMID: 15044841].
36. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW. Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation. Am J Pathol 2003; 162:213-8. [PMID: 12507904].
37. Zehr C, Lewis J, McGowan E, Crook J, Lin WL, Godwin K, Knight J, Dickson DW, Hutton M. Apoptosis in oligodendrocytes is associated with axonal degeneration in P301L tau mice. Neurobiol Dis 2004; 15:553-62. [PMID: 15056463].
38. Sahara N, Lewis J, DeTure M, McGowan E, Dickson DW, Hutton M, Yen SH. Assembly of tau in transgenic animals expressing P301L tau: alteration of phosphorylation and solubility. J Neurochem 2002; 83:1498-508. [PMID: 12472903].
39. David DC, Ittner LM, Gehrig P, Nergenau D, Shepherd C, Halliday G, Gotz J. Beta-amyloid treatment of two complementary P301L tau-expressing Alzheimer's disease models reveals similar deregulated cellular processes. Proteomics 2006; 6:6566-77. [PMID: 17111439].
40. Murakami T, Paitel E, Kawarabayashi T, Ikeda M, Chishti MA, Janus C, Matsubara E, Sasaki A, Kawarai T, Phinney AL, Harigaya Y, Horne P, Egashira N, Mishima K, Hanna A, Yang J, Iwasaki K, Takahashi M, Fujiwara M, Ishiguro K, Bergeron C, Carlson GA, Abe K, Westaway D, St George-Hyslop P, Shoji M. Cortical neuronal and glial pathology in TgTauP301L transgenic mice: neuronal degeneration, memory disturbance, and phenotypic variation. Am J Pathol 2006; 169:1365-75. [PMID: 17003492].
41. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G, Hutton M, Ashe KH. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 2005; 25:10637-47. [PMID: 16291936].
42. David DC, Hauptmann S, Scherping I, Schuessel K, Keil U, Rizzu P, Ravid R, Drose S, Brandt U, Muller WE, Eckert A, Gotz J. Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J Biol Chem 2005; 280:23802-14. [PMID: 15831501].
43. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC, Atzori C, Migheli A, Crowther RA, Ghetti B, Spillantini MG, Goedert M. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 2002; 22:9340-51. [PMID: 12417659].
44. Bellucci A, Westwood AJ, Ingram E, Casamenti F, Goedert M, Spillantini MG. Induction of inflammatory mediators and microglial activation in mice transgenic for mutant human P301S tau protein. Am J Pathol 2004; 165:1643-52. [PMID: 15509534].
45. Schindowski K, Bretteville A, Leroy K, Begard S, Brion JP, Hamdane M, Buee L. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am J Pathol 2006; 169:599-616. [PMID: 16877359].
46. Lieven CJ, Millet LE, Hoegger MJ, Levin LA. Induction of axon and dendrite formation during early RGC-5 cell differentiation. Exp Eye Res 2007; 85:678-83. [PMID: 17904550].
47. Nakayama T, Goshima Y, Misu Y, Kato T. Role of cdk5 and tau phosphorylation in heterotrimeric G protein-mediated retinal growth cone collapse. J Neurobiol 1999; 41:326-39. [PMID: 10526312].
48. Liu B, Rasool S, Yang Z, Glabe CG, Schreiber SS, Ge J, Tan Z. Amyloid-peptide vaccinations reduce β-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer's transgenic mice. Am J Pathol 2009; 175:2099-110. [PMID: 19834067].
49. Nikolic M, Dudek H, Kwon YT, Ramos YF, Tsai LH. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev 1996; 10:816-25. [PMID: 8846918].
50. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K, Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 1999; 285:895-8. [PMID: 10436159].
51. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, Amano M, Iwamatsu A, Goshima Y, Kaibuchi K. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 2000; 275:23973-80. [PMID: 10818093].
52. Cheng Q, Sasaki Y, Shoji M, Sugiyama Y, Tanaka H, Nakayama T, Mizuki N, Nakamura F, Takei K, Goshima Y. Cdk5/p35 and Rho-kinase mediate ephrin-A5-induced signaling in retinal ganglion cells. Mol Cell Neurosci 2003; 24:632-45. [PMID: 14664814].
53. Liu N, Cooper NG. The Ca2+/calmodulin-dependent protein kinase II-associated protein complex isolated from chicken retina. J Mol Neurosci 1996; 7:1-12. [PMID: 8835778].
54. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 2002; 156:1051-63. [PMID: 11901170].
55. Magnani E, Fan J, Gasparini L, Golding M, Williams M, Schiavo G, Goedert M, Amos LA, Spillantini MG. Interaction of tau protein with the dynactin complex. EMBO J 2007; 26:4546-54. [PMID: 17932487].
56. Léveillard T, Sahel JA. Rod-derived cone viability factor for treating blinding diseases: from clinic to redox signaling. Sci Transl Med 2010; 2:26ps16-[PMID: 20375363].
57. Leger F, Fernagut PO, Canron MH, Leoni S, Vital C, Tison F, Bezard E, Vital A. Protein aggregation in the aging retina. J Neuropathol Exp Neurol 2011; 70:63-8. [PMID: 21157377].
58. Löffler KU, Edward DP, Tso MO. Immunoreactivity against tau, amyloid precursor protein, and beta-amyloid in the human retina. Invest Ophthalmol Vis Sci 1995; 36:24-31. [PMID: 7822152].
59. Yoneda S, Hara H, Hirata A, Fukushima M, Inomata Y, Tanihara H. Vitreous fluid levels of beta-amyloid((1-42)) and tau in patients with retinal diseases. Jpn J Ophthalmol 2005; 49:106-8. [PMID: 15838725].
60. Gupta N, Fong J, Ang LC, Yucel YH. Retinal tau pathology in human glaucomas. Can J Ophthalmol 2008; 43:53-60. [PMID: 18219347].
61. Yang Y, Yu M, Zhu J, Chen X, Liu X. Role of cerebrospinal fluid in glaucoma: Pressure and beyond. Med Hypotheses 2010; 74:31-4. [PMID: 19819083].
62. Oka T, Tamada Y, Nakajima E, Shearer TR, Azuma M. Presence of calpain-induced proteolysis in retinal degeneration and dysfunction in a rat model of acute ocular hypertension. J Neurosci Res 2006; 83:1342-51. [PMID: 16528750].
63. Tamada Y, Nakajima E, Nakajima T, Shearer TR, Azuma M. Proteolysis of neuronal cytoskeletal proteins by calpain contributes to rat retinal cell death induced by hypoxia. Brain Res 2005; 1050:148-55. [PMID: 15979593].
64. Fett AL, Hermann MM, Muether PS, Kirchhof B, Fauser S. Immunohistochemical localization of complement regulatory proteins in the human retina. Histol Histopathol 2012; 27:357-64. [PMID: 22237713].
65. Gasparini L, Crowther RA, Martin KR, Berg N, Coleman M, Goedert M, Spillantini MG. Tau inclusions in retinal ganglion cells of human P301S tau transgenic mice: effects on axonal viability. Neurobiol Aging 2011; 32:419-33. [PMID: 19356824].
66. Chiu K, Chan TF, Wu A, Leung IY, So KF, Chang RC. Neurodegeneration of the retina in mouse models of Alzheimer's disease: what can we learn from the retina? Age (Dordr) 2012; 34:633-49. [PMID: 21559868].
67. Tatton W, Chen D, Chalmers-Redman R, Wheeler L, Nixon R, Tatton N. Hypothesis for a common basis for neuroprotection in glaucoma and Alzheimer's disease: anti-apoptosis by alpha-2-adrenergic receptor activation. Surv Ophthalmol 2003; 48:S25-37. [PMID: 12852432].
68. Buckingham BP, Inman DM, Lambert W, Oglesby E, Calkins DJ, Steele MR, Vetter ML, Marsh-Armstrong N, Horner PJ. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci 2008; 28:2735-44. [PMID: 18337403].
69. Howell GR, Soto I, Libby RT, John SW. Intrinsic axonal degeneration pathways are critical for glaucomatous damage. Exp Neurol 2012. [PMID: 22285251].