Viewing ageing eyes: Diverse sites of amyloid beta accumulation in the ageing mouse retina and the up-regulation of macrophages

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Kam, Jaimie Hoh ^a   Lenassi, Eva ^a,b   Jeffery, Glen ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRUCH MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MORPHOLOGY; MOUSE; NONHUMAN; PHOTORECEPTOR OUTER SEGMENT; QUANTITATIVE ANALYSIS; RETINA; UPREGULATION;

AGING; AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; HUMANS; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MACROPHAGES; MACULAR DEGENERATION; MICE; RETINA; UP-REGULATION;

EID: 78049299159     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013127     Document Type: Article

References (59)

1. Leibowitz HM, Krueger DE, Maunder LR, Milton RC, Kini MM, et al. (1980) The Framingham Eye Study monograph: An ophthalmological and epidemiological study of cataract, glaucoma, diabetic retinopathy, macular degeneration, and visual acuity in a general population of 2631 adults, 1973-1975. Surv Ophthalmol 24: 335-610.
2. Klein R, Peto T, Bird A, Vannewkirk MR (2004) The epidemiology of agerelated macular degeneration. Am J Ophthalmol 137: 486-495.
3. Klein R, Klein BE, Jensen SC, Meuer SM (1997) The five-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology 104: 7-21.
4. Green WR (1999) Histopathology of age-related macular degeneration. Mol Vis 5: 27.
5. Feeney-Burns L, Hilderbrand ES, Eldridge S (1984) Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells. Invest Ophthalmol Vis Sci 25: 195-200.
6. Sarks SH (1976) Ageing and degeneration in the macular region: a clinicopathological study. Br J Ophthalmol 60: 324-341.
7. Anderson DH, Mullins RF, Hageman GS, Johnson LV (2002) A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol 134: 411-431.
8. Isas JM, Luibl V, Johnson LV, Kayed R, Wetzel R, et al. (2010) Soluble and mature amyloid fibrils in drusen deposits. Invest Ophthalmol Vis Sci 51: 1304-1310.
9. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, et al. (2001) An integrated hypothesis that considers drusen as biomarkers of immunemediated processes at the RPE-Bruch's membrane interface in aging and agerelated macular degeneration. Prog Retin Eye Res 20: 705-732.
10. Dentchev T, Milam AH, Lee VM, Trojanowski JQ, Dunaief JL (2003) Amyloidbeta is found in drusen from some age-related macular degeneration retinas, but not in drusen from normal retinas. Mol Vis 9: 184-190.
11. Anderson DH, Talaga KC, Rivest AJ, Barron E, Hageman GS, et al. (2004) Characterization of beta amyloid assemblies in drusen: the deposits associated with aging and age-related macular degeneration. Exp Eye Res 78: 243-256.
12. Bruban J, Glotin AL, Dinet V, Chalour N, Sennlaub F, et al. (2009) Amyloidbeta(1-42) alters structure and function of retinal pigmented epithelial cells. Aging Cell 8: 162-177.
13. Davis JB, McMurray HF, Schubert D (1992) The amyloid beta-protein of Alzheimer's disease is chemotactic for mononuclear phagocytes. Biochem Biophys Res Commun 189: 1096-1100.
14. Meda L, Bonaiuto C, Szendrei GI, Ceska M, Rossi F, et al. (1995) beta- Amyloid(25-35) induces the production of interleukin-8 from human monocytes. J Neuroimmunol 59: 29-33.
15. Meda L, Cassatella MA, Szendrei GI, Otvos L, Jr., Baron P, et al. (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374: 647-650.
16. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, et al. (1992) Complement activation by beta-amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 89: 10016-10020.
17. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, et al. (2009) Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29: 4252-4262.
18. D'Andrea MR, Cole GM, Ard MD (2004) The microglial phagocytic role with specific plaque types in the Alzheimer disease brain. Neurobiol Aging 25: 675-683.
19. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23: 2665-2674.
20. Shirahama T, Miura K, Ju ST, Kisilevsky R, Gruys E, et al. (1990) Amyloid enhancing factor-loaded macrophages in amyloid fibril formation. Lab Invest 62: 61-68.
21. Raoul W, Feumi C, Keller N, Lavalette S, Houssier M, et al. (2008) Lipidbloated subretinal microglial cells are at the origin of drusen appearance in CX3CR1-deficient mice. Ophthalmic Res 40: 115-119.
22. Combadiere C, Feumi C, Raoul W, Keller N, Rodero M, et al. (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest 117: 2920-2928.
23. Ma W, Zhao L, Fontainhas AM, Fariss RN, Wong WT (2009) Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD. PLoS One 4: e7945.
24. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
25. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, et al. (2001) TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 7: 612-618.
26. Takechi R, Galloway S, Pallebage-Gamarallage M, Wellington C, Johnsen R, et al. (2009) Three-dimensional colocalization analysis of plasma-derived apolipoprotein B with amyloid plaques in APP/PS1 transgenic mice. Histochem Cell Biol 131: 661-666.
27. Muresan V, Varvel NH, Lamb BT, Muresan Z (2009) The cleavage products of amyloid-beta precursor protein are sorted to distinct carrier vesicles that are independently transported within neurites. J Neurosci 29: 3565-3578.
28. Hickman SE, Allison EK, El Khoury J (2008) Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28: 8354-8360.
29. Ning A, Cui J, To E, Ashe KH, Matsubara J (2008) Amyloid-beta deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Invest Ophthalmol Vis Sci 49: 5136-5143.
30. Perez SE, Lumayag S, Kovacs B, Mufson EJ, Xu S (2009) Beta-amyloid deposition and functional impairment in the retina of the APPswe/PS1DeltaE9 transgenic mouse model of Alzheimer's disease. Invest Ophthalmol Vis Sci 50: 793-800.
31. Dutescu RM, Li QX, Crowston J, Masters CL, Baird PN, et al. (2009) Amyloid precursor protein processing and retinal pathology in mouse models of Alzheimer's disease. Graefes Arch Clin Exp Ophthalmol 247: 1213-1221.
32. Xu H, Chen M, Manivannan A, Lois N, Forrester JV (2008) Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 7: 58-68.
33. Cunea A, Jeffery G (2007) The ageing photoreceptor. Vis Neurosci 24: 151-155.
34. Young RW (1971) The Renewal of Rod and Cone Outer Segments in the Rhesus Monkey. J Cell Biol 49: 303-318.
35. Kevany BM, Palczewski K (2010) Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 25: 8-15.
36. Johnson LV, Leitner WP, Rivest AJ, Staples MK, Radeke MJ, et al. (2002) The Alzheimer's A beta -peptide is deposited at sites of complement activation in pathologic deposits associated with aging and age-related macular degeneration. Proc Natl Acad Sci U S A 99: 11830-11835.
37. Bressler SB, Maguire MG, Bressler NM, Fine SL (1990) Relationship of drusen and abnormalities of the retinal pigment epithelium to the prognosis of neovascular macular degeneration. The Macular Photocoagulation Study Group. Arch Ophthalmol 108: 1442-1447.
38. Sarks SH (1980) Council Lecture. Drusen and their relationship to senile macular degeneration. Aust J Ophthalmol 8: 117-130.
39. Pauleikhoff D, Barondes MJ, Minassian D, Chisholm IH, Bird AC (1990) Drusen as risk factors in age-related macular disease. Am J Ophthalmol 109: 38-43.
40. Baker DR, Mendez MF, Townsend JC, Ilsen PF, Bright DC (1997) Optometric management of patients with Alzheimer's disease. J Am Optom Assoc 68: 483-494.
41. Katz B, Rimmer S (1989) Ophthalmologic manifestations of Alzheimer's disease. Surv Ophthalmol 34: 31-43.
42. Sadun AA, Borchert M, DeVita E, Hinton DR, Bassi CJ (1987) Assessment of visual impairment in patients with Alzheimer's disease. Am J Ophthalmol 104: 113-120.
43. Iseri PK, Altinas O, Tokay T, Yuksel N (2006) Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J Neuroophthalmol 26: 18-24.
44. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL (2007) Retinal abnormalities in early Alzheimer's disease. Invest Ophthalmol Vis Sci 48: 2285-2289.
45. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, et al. (2003) Adult mouse astrocytes degrade amyloid-[beta] in vitro and in situ. Nat Med 9: 453-457.
46. Terman A, Brunk UT (1998) Lipofuscin: mechanisms of formation and increase with age. APMIS 106: 265-276.
47. Gray DA, Woulfe J (2005) Lipofuscin and aging: a matter of toxic waste. Sci Aging Knowledge Environ 2005: re1.
48. Luhmann UF, Robbie S, Munro PM, Barker SE, Duran Y, et al. (2009) The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci 50: 5934-5943.
49. Boissonneault V, Filali M, Lessard M, Relton J, Wong G, et al. (2009) Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 132: 1078-1092.
50. Coimbra A, Andrade C (1971) Familial amyloid polyneuropathy: an electron microscope study of the peripheral nerve in five cases. II. Nerve fibre changes. Brain 94: 207-212.
51. Coimbra A, Andrade C (1971) Familial amyloid polyneuropathy: an electron microscope study of the peripheral nerve in five cases. I. Interstitial changes. Brain 94: 199-206.
52. Curcio CA, Millican CL, Allen KA, Kalina RE (1993) Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci 34: 3278-3296.
53. Gresh J, Goletz PW, Crouch RK, Rohrer B (2003) Structure-function analysis of rods and cones in juvenile, adult, and aged C57bl/6 and Balb/c mice. Vis Neurosci 20: 211-220.
54. Jackson GR, McGwin G, Jr., Phillips JM, Klein R, Owsley C (2004) Impact of aging and age-related maculopathy on activation of the a-wave of the rodmediated electroretinogram. Invest Ophthalmol Vis Sci 45: 3271-3278.
55. Jackson GR, McGwin G, Jr., Phillips JM, Klein R, Owsley C (2006) Impact of aging and age-related maculopathy on inactivation of the a-wave of the rodmediated electroretinogram. Vision Res 46: 1422-1431.
56. Wright CE, Drasdo N (1985) The influence of age on the spatial and temporal contrast sensitivity function. Doc Ophthalmol 59: 385-395.
57. Medrano CJ, Fox DA (1995) Oxygen consumption in the rat outer and inner retina: light- and pharmacologically-induced inhibition. Exp Eye Res 61: 273-284.
58. Graymore CN (1969) General aspects of the metabolism of the retina. In: Davson H, ed. In the Eye. 2nd ed. New York: Academic Press. pp 601-645.
59. Lewis H, Straatsma BR, Foos RY (1986) Chorioretinal juncture. Multiple extramacular drusen. Ophthalmology 93: 1098-1112.