Retinal ganglion cell dendritic degeneration in a mouse model of Alzheimer's disease

Neurobiology of Aging

Volumn 34, Issue 7, 2013, Pages 1799-1806

  Williams, Pete A ^a,d   Thirgood, Rebecca A ^a   Oliphant, Huw ^b   Frizzati, Aura ^a   Littlewood, Elinor ^b   Votruba, Marcela ^a   Good, Mark A ^c   Williams, Julie ^b   Morgan, James E ^a,b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d JACKSON LABORATORY   (United States)

Author keywords

Alzheimer's disease; Dendrite; Hippocampus; Mitochondrion; Retinal ganglion cell; Synapse

Indexed keywords

AMYLOID BETA PROTEIN; MITOCHONDRIAL PROTEIN; MITOFUSIN 2; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOPHYSIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEGENERATION; CELL DENSITY; CELL LOSS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC SPINE; FEMALE; HIPPOCAMPAL CA1 REGION; MALE; MITOCHONDRION; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; SYNAPTIC POTENTIAL;

ALZHEIMER DISEASE; ANIMALS; DENDRITES; DISEASE MODELS, ANIMAL; FEMALE; MICE; MICE, TRANSGENIC; RETINAL DEGENERATION; RETINAL GANGLION CELLS;

EID: 84875854947     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.01.006     Document Type: Article

References (65)

1. Anderton B.H., Callahan L., Coleman P., Davies P., Flood D., Jicha G.A., Ohm T., Weaver C. Dendritic changes in Alzheimer's disease and factors that may underlie these changes. Prog. Neurobiol. 1998, 55:595-609.
2. Blanks J.C., Hinton D.R., Sadun A.A., Miller C.A. Retinal ganglion cell degeneration in Alzheimer's disease. Brain Res. 1989, 501:364-372.
3. Blanks J.C., Schmidt S.Y., Torigoe Y., Porrello K.V., Hinton D.R., Blanks R.H. Retinal pathology in Alzheimer's disease. II. Regional neuron loss and glial changes in GCL. Neurobiol. Aging 1996, 17:385-395.
4. Blanks J.C., Torigoe Y., Hinton D.R., Blanks R.H. Retinal pathology in Alzheimer's disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiol. Aging 1996, 17:377-384.
5. Calkins M.J., Manczak M., Mao P., Shirendeb U., Reddy P.H. Impaired mitochondrial biogenesis, defective axonal transport of mitochondria. Hum. Mol. Genet. 2011, 20:4515-4529.
6. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 1999, 2:271-276.
7. Chetkovich D.M., Bunn R.C., Kuo S.-H., Kawasaki Y., Kohwi M., Bredt D.S. Postsynaptic targeting of alternative postsynaptic density-95 isoforms by distinct mechanisms. J. Neurosci. 2002, 22:6415-6425.
8. Coombs J., van der List D., Wang G.Y., Chalupa L.M. Morphological properties of mouse retinal ganglion cells. Neuroscience 2006, 140:123-136.
9. Cordeiro M.F., Guo L., Coxon K.M., Duggan J., Nizari S., Normando E.M., Sensi S.L., Sillito A.M., Fitzke F.W., Salt T.E., Moss S.E. Imaging multiple phases of neurodegeneration: a novel approach to assessing cell. Cell Death Dis. 2010, 1:e3.
10. Curcio C.A., Drucker D.N. Retinal ganglion cells in Alzheimer's disease and aging. Ann. Neurol. 1993, 33:248-257.
11. Damiani D., Novelli E., Mazzoni F., Strettoi E. Undersized dendritic arborizations in retinal ganglion cells of the rd1 mutant. J. Comp. Neurol. 2012, 520:1406-1423.
12. Doi M., Uji Y., Yamamura H. Morphological classification of retinal ganglion-cells in mice. J. Comp. Neurol. 1995, 356:368-386.
13. Drexler W., Fujimoto J.G. State-of-the-art retinal optical coherence tomography. Prog. Retin. Eye Res. 2008, 27:45-88.
14. Dutescu R.M., Li Q.X., Crowston J., Masters C.L., Baird P.N., Culvenor J.G. Amyloid precursor protein processing and retinal pathology in mouse models of Alzheimer's disease. Graefes. Arch. Clin. Exp. Ophthalmol. 2009, 247:1213-1221.
15. Furst A.J., Kerchner G.A. From Alois to Amyvid: seeing Alzheimer disease. Neurology 2012, 79:1628-1629.
16. Gan W.B., Grutzendler J., Wong W.T., Wong R.O., Lichtman J.W. Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 2000, 27:219-225.
17. Garcia M.F., Gordon M.N., Hutton M., Lewis J., McGowan E., Dickey C.A., Morgan D., Arendash G.W. The retinal degeneration (rd) gene seriously impairs spatial cognitive. Neuroreport 2004, 15:73-77.
18. Gossage K.W., Tkaczyk T.S., Rodriguez J.J., Barton J.K. Texture analysis of optical coherence tomography images: feasibility for tissue classification. J. Biomed. Opt. 2003, 8:570-575.
19. Guo L., Salt T.E., Luong V., Wood N., Cheung W., Maass A., Ferrari G., Russo-Marie F., Sillito A.M., Cheetham M.E., Moss S.E., Fitzke F.W., Cordeiro M.F. Targeting amyloid-beta in glaucoma treatment. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13444-13449.
20. Gutierrez H., Davies A.M. A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology. J. Neurosci. Methods 2007, 163:24-30.
21. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
22. Jakobs T.C., Libby R.T., Ben Y., John S.W., Masland R.H. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 2005, 171:313-325.
23. Jimenez A.J., Garcia-Fernandez J.M., Gonzalez B., Foster R.G. The spatio-temporal pattern of photoreceptor degeneration in the aged rd/rd mouse. Cell Tissue Res. 1996, 284:193-202.
24. Jindahra P., Hedges T.R., Mendoza-Santiesteban C.E., Plant G.T. Optical coherence tomography of the retina: applications in neurology. Curr. Opin. Neurol. 2010, 23:16-23.
25. Kajic V., Povazay B., Hermann B., Hofer B., Marshall D., Rosin P.L., Drexler W. Robust segmentation of intraretinal layers in the normal human fovea using a novel statistical model based on texture and shape analysis. Opt. Express 2010, 18:14730-14744.
26. Klunk W.E., Engler H., Nordberg A., Wang Y., Blomqvist G., Holt D.P., Bergstrom M., Savitcheva I., Huang G.F., Estrada S., Ausen B., Debnath M.L., Barletta J., Price J.C., Sandell J., Lopresti B.J., Wall A., Koivisto P., Antoni G., Mathis C.A., Langstrom B. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol. 2004, 55:306-319.
27. Kong J.-H., Fish D.R., Rockhill R.L., Masland R.H. Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J. Comp. Neurol. 2005, 489:293-310.
28. Koronyo Y., Salumbides B.C., Black K.L., Koronyo-Hamaoui M. Alzheimer's disease in the retina: imaging retinal aß plaques for early diagnosis and therapy assessment. Neurodegener. Dis. 2012, 10:285-293.
29. Koronyo-Hamaoui M., Koronyo Y., Ljubimov A.V., Miller C.A., Ko M.K., Black K.L., Schwartz M., Farkas D.L. Identification of amyloid plaques in retinas from Alzheimer's patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage 2011, 54:S204-S217.
30. Lee V., Rekhi E., Hoh Kam J., Jeffery G. Vitamin D rejuvenates aging eyes by reducing inflammation, clearing amyloid beta. Neurobiol. Aging 2012, 33:2382-2389.
31. Liu B., Rasool S., Yang Z., Glabe C.G., Schreiber S.S., Ge J., Tan Z. Amyloid-peptide vaccinations reduce {beta}-amyloid plaques but exacerbate. Am. J. Pathol. 2009, 175:2099-2110.
32. Liu S., Li Z.W., Weinreb R.N., Xu G., Lindsey J.D., Ye C., Yung W.H., Pang C.P., Lam D.S., Leung C.K. Tracking retinal microgliosis in models of retinal ganglion cell damage. Invest. Ophthalmol. Vis. Sci. 2012, 53:6254-6262.
33. 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, 480:69-72.
34. Manczak M., Calkins M.J., Reddy P.H. Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with. Hum. Mol. Genet. 2011, 20:2495-2509.
35. McEvoy L.K., Brewer J.B. Quantitative structural MRI for early detection of Alzheimer's disease. Expert Rev. Neurother. 2010, 10:1675-1688.
36. McKinnon S.J., Lehman D.M., Kerrigan-Baumrind L.A., Merges C.A., Pease M.E., Kerrigan D.F., Ransom N.L., Tahzib N.G., Reitsamer H.A., Levkovitch-Verbin H., Quigley H.A., Zack D.J. Caspase activation and amyloid precursor protein cleavage in rat ocular hypertension. Invest. Ophthalmol. Vis. Sci. 2002, 43:1077-1087.
37. Miller N., Drachman D.A. The optic nerve: a window into diseases of the brain?. Neurology 2006, 67:1742-1743.
38. Morgan J.E., Datta A.V., Erichsen J.T., Albon J., Boulton M.E. Retinal ganglion cell remodelling in experimental glaucoma. Adv. Exp. Med. Biol. 2006, 572:397-402.
39. Morin P.J., Abraham C.R., Amaratunga A., Johnson R.J., Huber G., Sandell J.H., Fine R.E. Amyloid precursor protein is synthesized by retinal ganglion cells, rapidly transported to the optic nerve plasma membrane and nerve terminals, and metabolized. J. Neurochem. 1993, 61:464-473.
40. Naskar R., Wissing M., Thanos S. Detection of early neuron degeneration and accompanying microglial responses in. Invest. Ophthalmol. Vis. Sci. 2002, 43:2962-2968.
41. Ning A., Cui J., To E., Ashe K.H., Matsubara J. Amyloid-beta deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Invest. Ophthalmol. Vis. Sci. 2008, 49:5136-5143.
42. O'Brien J., Lummis S.C.R. Biolistic and diolistic transfection: using the gene gun to deliver DNA and lipophilic dyes into mammalian cells. Methods 2004, 33:121-125.
43. O'Brien J.A., Lummis S.C.R. Diolistic labeling of neuronal cultures and intact tissue using a hand-held gene gun. Nat. Protoc. 2006, 1:1517-1521.
44. Ohno-Matsui K. Parallel findings in age-related macular degeneration and Alzheimer's disease. Prog. Retin. Eye Res. 2011, 30:217-238.
45. Osborne N.N. Pathogenesis of ganglion "cell death" in glaucoma and neuroprotection: focus on ganglion cell axonal mitochondria. Prog. Brain Res. 2008, 173:339-352.
46. Osborne N.N., Lascaratos G., Bron A.J., Chidlow G., Wood J.P.M. A hypothesis to suggest that light is a risk factor in glaucoma and the mitochondrial optic neuropathies. Br. J. Ophthalmol. 2006, 90:237-241.
47. 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, 420:97-99.
48. Perez S.E., Lumayag S., Kovacs B., Mufson E.J., Xu S. Beta-amyloid deposition and functional impairment in the retina of the. Invest. Ophthalmol. Vis. Sci. 2009, 50:793-800.
49. Povazay B., Hofer B., Torti C., Hermann B., Tumlinson A.R., Esmaeelpour M., Egan C.A., Bird A.C., Drexler W. Impact of enhanced resolution, speed and penetration on three-dimensional retinal optical coherence tomography. Opt. Express 2009, 17:4134-4150.
50. Reynolds E.S. Use of lead citrate at high ph as an electron-opaque stain in electron microscopy. J. Cell Biol. 1963, 17:208-212.
51. Rowe C.C., Ackermann U., Browne W., Mulligan R., Pike K.L., O'Keefe G., Tochon-Danguy H., Chan G., Berlangieri S.U., Jones G., Dickinson-Rowe K.L., Kung H.P., Zhang W., Kung M.P., Skovronsky D., Dyrks T., Holl G., Krause S., Friebe M., Lehman L., Lindemann S., Dinkelborg L.M., Masters C.L., Villemagne V.L. Imaging of amyloid beta in Alzheimer's disease with 18F-BAY94-9172, a novel PET tracer: proof of mechanism. Lancet Neurol. 2008, 7:129-135.
52. Rowe C.C., Ng S., Ackermann U., Gong S.J., Pike K., Savage G., Cowie T.F., Dickinson K.L., Maruff P., Darby D., Smith C., Woodward M., Merory J., Tochon-Danguy H., O'Keefe G., Klunk W.E., Mathis C.A., Price J.C., Masters C.L., Villemagne V.L. Imaging beta-amyloid burden in aging and dementia. Neurol. 2007, 68:1718-1725.
53. Scheff S.W., Price D.A. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol. Aging 2003, 24:1029-1046.
54. Scheff S.W., Price D.A., Schmitt F.A., Mufson E.J. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2006, 27:1372-1384.
55. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
56. Smith D.L., Pozueta J., Gong B., Arancio O., Shelanski M. Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16877-16882.
57. Sun W., Li N., He S. Large-scale morphological survey of mouse retinal ganglion cells. J. Comp. Neurol. 2002, 451:115-126.
58. Torti C., Povazay B., Hofer B., Unterhuber A., Carroll J., Ahnelt P.K., Drexler W. Adaptive optics optical coherence tomography at 120,000 depth scans for non-invasive cellular phenotyping of the living human retina. Opt. Express 2009, 17:19382-19400.
59. Wang L., Dong J., Cull G., Fortune B., Cioffi G.A. Varicosities of intraretinal ganglion cell axons in human and nonhuman primates. Invest. Ophthalmol. Vis. Sci. 2003, 44:2-9.
60. Wang X., Su B., Lee H.G., Li X., Perry G., Smith M.A., Zhu X. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 2009, 29:9090-9103.
61. Wang X., Su B., Siedlak S.L., Moreira P.I., Fujioka H., Wang Y., Casadesus G., Zhu X. Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19318-19323.
62. Weber A.J., Kaufman P.L., Hubbard W.C. Morphology of single ganglion cells in the glaucomatous primate retina. Invest. Ophthalmol. Vis. Sci. 1998, 39:2304-2320.
63. Williams P.A., Morgan J.E., Votruba M. Opa1 deficiency in a mouse model of dominant optic atrophy leads to retinal ganglion cell dendropathy. Brain 2010, 133:2942-2951.
64. Williams P.A., Piechota M., von Ruhland C., Taylor E., Morgan J.E., Votruba M. Opa1 is essential for retinal ganglion cell synaptic architecture and connectivity. Brain 2012, 135:493-505.
65. Yu D., Corbett B., Yan Y., Zhang G.X., Reinhart P., Cho S.J., Chin J. Early cerebrovascular inflammation in a transgenic mouse model of Alzheimer's. Neurobiol. Aging 2012, 33:2942-2947.