Complement component C3 plays a critical role in protecting the aging retina in a murine model of age-related macular degeneration

American Journal of Pathology

Volumn 183, Issue 2, 2013, Pages 480-492

  Hoh Kam, Jaimie ^a   Lenassi, Eva ^a,b   Malik, Talat H ^c   Pickering, Matthew C ^c   Jeffery, Glen ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; GENOTYPE; HISTOPATHOLOGY; INFLAMMATION; MACROPHAGE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA MACULA AGE RELATED DEGENERATION; WESTERN BLOTTING;

AMYLOID BETA-PEPTIDES; ANIMALS; BRUCH MEMBRANE; COMPLEMENT C3; COMPLEMENT FACTOR H; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; MACULAR DEGENERATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; RETINAL PIGMENT EPITHELIUM;

EID: 84880576637     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.04.008     Document Type: Article

References (60)

1. M.J. Walport Complement: second of two parts N Engl J Med 344 2001 1140 1144
2. M.J. Walport Complement: first of two parts N Engl J Med 344 2001 1058 1066
3. D.T. Fearon Cellular receptors for fragments of the third component of complement Immunol Today 5 1984 105 110
4. E.A. Nordahl, V. Rydengard, P. Nyberg, D.P. Nitsche, M. Morgelin, M. Malmsten, L. Bjorck, and A. Schmidtchen Activation of the complement system generates antibacterial peptides Proc Natl Acad Sci U S A 101 2004 16879 16884
5. T.C. Farries, and J.P. Atkinson Evolution of the complement system Immunol Today 12 1991 295 300
6. A. Erdei, G. Fust, and J. Gergely The role of C3 in the immune response Immunol Today 12 1991 332 337
7. M. Kida, H. Fujioka, Y. Kosaka, K. Hayashi, Y. Sakiyama, and T. Ariga The first confirmed case with C3 deficiency caused by compound heterozygous mutations in the C3 gene: a new aspect of pathogenesis for C3 deficiency Blood Cells Mol Dis 40 2008 410 413
8. H.M. Leibowitz, D.E. Krueger, L.R. Maunder, R.C. Milton, M.M. Kini, H.A. Kahn, R.J. Nickerson, J. Pool, T.L. Colton, J.P. Ganley, J.I. Loewenstein, and T.R. Dawber 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 Suppl 1980 335 610
9. R. Klein, T. Peto, A. Bird, and M.R. Vannewkirk The epidemiology of age-related macular degeneration Am J Ophthalmol 137 2004 486 495
10. R. Klein, B.E. Klein, S.C. Jensen, and S.M. Meuer The five-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study Ophthalmology 104 1997 7 21
11. L.V. Johnson, W.P. Leitner, M.K. Staples, and D.H. Anderson Complement activation and inflammatory processes in Drusen formation and age related macular degeneration Exp Eye Res 73 2001 887 896
12. G.S. Hageman, P.J. Luthert, N.H. Victor Chong, L.V. Johnson, D.H. Anderson, and R.F. Mullins An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration Prog Retin Eye Res 20 2001 705 732
13. D.H. Anderson, R.F. Mullins, G.S. Hageman, and L.V. Johnson A role for local inflammation in the formation of drusen in the aging eye Am J Ophthalmol 134 2002 411 431
14. P.L. Penfold, M.C. Madigan, M.C. Gillies, and J.M. Provis Immunological and aetiological aspects of macular degeneration Prog Retin Eye Res 20 2001 385 414
15. R.F. Mullins, S.R. Russell, D.H. Anderson, and G.S. Hageman Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease FASEB J 14 2000 835 846
16. D.H. Anderson, M.J. Radeke, N.B. Gallo, E.A. Chapin, P.T. Johnson, C.R. Curletti, L.S. Hancox, J. Hu, J.N. Ebright, G. Malek, M.A. Hauser, C.B. Rickman, D. Bok, G.S. Hageman, and L.V. Johnson The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis re-visited Prog Retin Eye Res 29 2010 95 112
17. R.J. Klein, C. Zeiss, E.Y. Chew, J.Y. Tsai, R.S. Sackler, C. Haynes, A.K. Henning, J.P. SanGiovanni, S.M. Mane, S.T. Mayne, M.B. Bracken, F.L. Ferris, J. Ott, C. Barnstable, and J. Hoh Complement factor H polymorphism in age-related macular degeneration Science 308 2005 385 389
18. A.O. Edwards, R. Ritter 3rd, K.J. Abel, A. Manning, C. Panhuysen, and L.A. Farrer Complement factor H polymorphism and age-related macular degeneration Science 308 2005 421 424
19. J.L. Haines, M.A. Hauser, S. Schmidt, W.K. Scott, L.M. Olson, P. Gallins, K.L. Spencer, S.Y. Kwan, M. Noureddine, J.R. Gilbert, N. Schnetz-Boutaud, A. Agarwal, E.A. Postel, and M.A. Pericak-Vance Complement factor H variant increases the risk of age-related macular degeneration Science 308 2005 419 421
20. G.S. Hageman, D.H. Anderson, L.V. Johnson, L.S. Hancox, A.J. Taiber, L.I. Hardisty, J.L. Hageman, H.A. Stockman, J.D. Borchardt, K.M. Gehrs, R.J. Smith, G. Silvestri, S.R. Russell, C.C. Klaver, I. Barbazetto, S. Chang, L.A. Yannuzzi, G.R. Barile, J.C. Merriam, R.T. Smith, A.K. Olsh, J. Bergeron, J. Zernant, J.E. Merriam, B. Gold, M. Dean, and R. Allikmets A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration Proc Natl Acad Sci U S A 102 2005 7227 7232
21. B. Gold, J.E. Merriam, J. Zernant, L.S. Hancox, A.J. Taiber, K. Gehrs, K. Cramer, J. Neel, J. Bergeron, G.R. Barile, R.T. Smith, G.S. Hageman, M. Dean, and R. Allikmets Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration Nat Genet 38 2006 458 462
22. J.R. Yates, T. Sepp, B.K. Matharu, J.C. Khan, D.A. Thurlby, H. Shahid, D.G. Clayton, C. Hayward, J. Morgan, A.F. Wright, A.M. Armbrecht, B. Dhillon, I.J. Deary, E. Redmond, A.C. Bird, and A.T. Moore Complement C3 variant and the risk of age-related macular degeneration N Engl J Med 357 2007 553 561
23. J.B. Maller, J.A. Fagerness, R.C. Reynolds, B.M. Neale, M.J. Daly, and J.M. Seddon Variation in complement factor 3 is associated with risk of age-related macular degeneration Nat Genet 39 2007 1200 1201
24. K.M. Gehrs, J.R. Jackson, E.N. Brown, R. Allikmets, and G.S. Hageman Complement, age-related macular degeneration and a vision of the future Arch Ophthalmol 128 2010 349 358
25. M.J. Mattapallil, E.F. Wawrousek, C.C. Chan, H. Zhao, J. Roychoudhury, T.A. Ferguson, and R.R. Caspi The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes Invest Ophthalmol Vis Sci 53 2012 2921 2927
26. P. Lundh von Leithner, J.H. Kam, J. Bainbridge, I. Catchpole, G. Gough, and P. Coffey Jeffery G: Complement factor h is critical in the maintenance of retinal perfusion Am J Pathol 175 2009 412 421
27. H. Al-Hussaini, J.H. Kam, A. Vugler, M. Semo, and G. Jeffery Mature retinal pigment epithelium cells are retained in the cell cycle and proliferate in vivo Mol Vis 14 2008 1784 1791
28. L.V. Del Priore, Y.H. Kuo, and T.H. Tezel Age-related changes in human RPE cell density and apoptosis proportion in situ Invest Ophthalmol Vis Sci 43 2002 3312 3318
29. J. Hoh Kam, E. Lenassi, and G. Jeffery Viewing ageing eyes: diverse sites of amyloid Beta accumulation in the ageing mouse retina and the up-regulation of macrophages PLoS One 5 2010 pii: e13127
30. S. Lesne, M.T. Koh, L. Kotilinek, R. Kayed, C.G. Glabe, A. Yang, M. Gallagher, and K.H. Ashe A specific amyloid-beta protein assembly in the brain impairs memory Nature 440 2006 352 357
31. P. Brouckaert, C. Libert, B. Everaerdt, N. Takahashi, A. Cauwels, and W. Fiers Tumor necrosis factor, its receptors and the connection with interleukin 1 and interleukin 6 Immunobiology 187 1993 317 329
32. Z.M. Bian, S.G. Elner, R.M. Strieter, S.L. Kunkel, N.W. Lukacs, and V.M. Elner IL-4 potentiates IL-1beta- and TNF-alpha-stimulated IL-8 and MCP-1 protein production in human retinal pigment epithelial cells Curr Eye Res 18 1999 349 357
33. S.G. Elner, R.M. Strieter, V.M. Elner, B.J. Rollins, M.A. Del Monte, and S.L. Kunkel Monocyte chemotactic protein gene expression by cytokine-treated human retinal pigment epithelial cells Lab Invest 64 1991 819 825
34. M. Chen, E. Muckersie, J.V. Forrester, and H. Xu Immune activation in retinal aging: a gene expression study Invest Ophthalmol Vis Sci 51 2010 5888 5896
35. N. Rougier, M.D. Kazatchkine, J.P. Rougier, V. Fremeaux-Bacchi, J. Blouin, G. Deschenes, B. Soto, V. Baudouin, B. Pautard, W. Proesmans, E. Weiss, and L. Weiss Human complement factor H deficiency associated with hemolytic uremic syndrome J Am Soc Nephrol 9 1998 2318 2326
36. M. Levy, L. Halbwachs-Mecarelli, M.C. Gubler, G. Kohout, A. Bensenouci, P. Niaudet, G. Hauptmann, and P. Lesavre H deficiency in two brothers with atypical dense intramembranous deposit disease Kidney Int 30 1986 949 956
37. K. Hogasen, J.H. Jansen, T.E. Mollnes, J. Hovdenes, and M. Harboe Hereditary porcine membranoproliferative glomerulonephritis type II is caused by factor H deficiency J Clin Invest 95 1995 1054 1061
38. M.C. Pickering, H.T. Cook, J. Warren, A.E. Bygrave, J. Moss, M.J. Walport, and M. Botto Uncontrolled C3 activation causes membranoproliferative glomerulonephritis in mice deficient in complement factor H Nat Genet 31 2002 424 428
39. P.J. Coffey, C. Gias, C.J. McDermott, P. Lundh, M.C. Pickering, C. Sethi, A. Bird, F.W. Fitzke, A. Maass, L.L. Chen, G.E. Holder, P.J. Luthert, T.E. Salt, S.E. Moss, and J. Greenwood Complement factor H deficiency in aged mice causes retinal abnormalities and visual dysfunction Proc Natl Acad Sci U S A 104 2007 16651 16656
40. J.C. Booij, D.C. Baas, J. Beisekeeva, T.G. Gorgels, and A.A. Bergen The dynamic nature of Bruch's membrane Prog Retin Eye Res 29 2010 1 18
41. C.N. Graymore, and R.D. Kissun Use of phenazine methosulphate (PMS) in the histochemical localization of lactic acid dehydrogenase (LDH) in the retina Exp Eye Res 8 1969 375 378
42. C.J. Medrano, and D.A. Fox Oxygen consumption in the rat outer and inner retina: light- and pharmacologically-induced inhibition Exp Eye Res 61 1995 273 284
43. G.B. Arden, A.M. Hamilton, J. Wilson-Holt, S. Ryan, J.S. Yudkin, and A. Kurtz Pattern electroretinograms become abnormal when background diabetic retinopathy deteriorates to a preproliferative stage: possible use as a screening test Br J Ophthalmol 70 1986 330 335
44. E. Usami [Studies on the method of measurement of the oscillatory potential in ERG]. Japanese Nihon Ganka Gakkai Zasshi 70 1966 84 87
45. E. Usami Studies on ERG of occlusion of the retinal artery and vein especially on that prognostic value [in Japanese] Nihon Ganka Gakkai Zasshi 71 1967 39 45
46. I. Lengyel, A. Tufail, H.A. Hosaini, P. Luthert, A.C. Bird, and G. Jeffery Association of drusen deposition with choroidal intercapillary pillars in the aging human eye Invest Ophthalmol Vis Sci 45 2004 2886 2892
47. T. Wyss-Coray, F. Yan, A.H. Lin, J.D. Lambris, J.J. Alexander, R.J. Quigg, and E. Masliah Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice Proc Natl Acad Sci U S A 99 2002 10837 10842
48. A.L. Wang, T.J. Lukas, M. Yuan, N. Du, M.O. Tso, and A.H. Neufeld Autophagy and exosomes in the aged retinal pigment epithelium: possible relevance to drusen formation and age-related macular degeneration PLoS One 4 2009 e4160
49. A. Tamaoka, N. Sawamura, T. Fukushima, S. Shoji, E. Matsubara, M. Shoji, S. Hirai, Y. Furiya, R. Endoh, and H. Mori Amyloid beta protein 42(43) in cerebrospinal fluid of patients with Alzheimer's disease J Neurol Sci 148 1997 41 45
50. C. Haass, M.G. Schlossmacher, A.Y. Hung, C. Vigo-Pelfrey, A. Mellon, B.L. Ostaszewski, I. Lieberburg, E.H. Koo, D. Schenk, D.B. Teplow, and D.J. Selkow Amyloid β-peptide is produced by cultured cells during normal metabolism Nature 359 1992 322 325
51. D. Puzzo, L. Privitera, and A. Palmeri Hormetic effect of amyloid-beta peptide in synaptic plasticity and memory Neurobiol Aging 33 2012 1484.e15 1484.e24
52. A.T. Dailey, A.M. Avellino, L. Benthem, J. Silver, and M. Kliot Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration J Neurosci 18 1998 6713 6722
53. D.T. Fearon, and W.W. Wong Complement ligand-receptor interactions that mediate biological responses Annu Rev Immunol 1 1983 243 271
54. L.M. Stuart, and R.A. Ezekowitz Phagocytosis: elegant complexity Immunity 22 2005 539 550
55. H.P. Hartung, U. Hadding, D. Bitter-Suermann, and D. Gemsa Release of prostaglandin E and thromboxane from macrophages by stimulation with factor H Clin Exp Immunol 56 1984 453 458
56. M.P. Dierich, A. Erdei, H. Huemer, A. Petzer, R. Stauder, T.F. Schulz, and J. Gergely Involvement of complement in B-cell, T-cell and monocyte/macrophage activation Immunol Lett 14 1987 235 242
57. R. Brambilla, V. Bracchi-Ricard, W.H. Hu, B. Frydel, A. Bramwell, S. Karmally, E.J. Green, and J.R. Bethea Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury J Exp Med 202 2005 145 156
58. J. Koenigsknecht-Talboo, and G.E. Landreth Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines J Neurosci 25 2005 8240 8249
59. K.P. Townsend, T. Town, T. Mori, L.F. Lue, D. Shytle, P.R. Sanberg, D. Morgan, F. Fernandez, R.A. Flavell, and J. Tan CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide Eur J Immunol 35 2005 901 910
60. M. Yu, W. Zou, N.S. Peachey, T.M. McIntyre, and J. Liu A novel role of complement in retinal degeneration Invest Ophthalmol Vis Sci 53 2012 7684 7692