Complement factor C3a alters proteasome function in human RPE cells and in an animal model of age-related RPE degeneration

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 10, 2013, Pages 6489-6501

  Ramos de Carvalhol, J Emanuel ^a   Klaassen, Ingeborg ^a   Vogels, Ilse M C ^a   Schipper Krom, Sabine ^a   van Noorden, Cornelis J F ^a   Reits, Eric ^a   Gorgels, Theo G M F ^b   Bergen, Arthur A B ^b   Schlingemann, Reinier O ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

interferon; Age related macular degeneration; C3a; CCL2 ; Complement; Ophthalmology; Proteasome; Retina

Indexed keywords

COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A; GAMMA INTERFERON; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEASOME; UBIQUITIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DNA POLYMORPHISM; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; NUCLEOTIDE SEQUENCE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA MACULA AGE RELATED DEGENERATION; UPREGULATION; WESTERN BLOTTING;

Γ-INTERFERON; AGE-RELATED MACULAR DEGENERATION; C3A; CCL2-/-; COMPLEMENT; OPHTHALMOLOGY; PROTEASOME; RETINA;

ADOLESCENT; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHILD; COMPLEMENT ACTIVATION; COMPLEMENT C3A; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER; UP-REGULATION;

EID: 84885084906     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12374     Document Type: Article

References (72)

1. Augood CA, Vingerling JR, De Jong PTVM, et al. Prevalence of age-related maculopathy in older Europeans: the European Eye Study (EUREYE). Arch Ophthalmol. 2006;124:529-535.
2. Javitt JC, Zhou ZY, Maguire MG, Fine SL, Willke RJ. Incidence of exudative age-related macular degeneration among elderly Americans. Ophthalmology. 2003;110:1534-1539.
3. Bora NS, Jha P, Bora PS. The role of complement in ocular pathology. Semin Immunopathol. 2008;30:85-95.
4. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv Ophthalmol. 2006;51:137-152.
5. Kijlstra A, La Heij EC, Hendrikse F. Immunological factors in the pathogenesis and treatment of age-related macular degeneration. Ocul Immunol Inflamm. 2005;13:3-11.
6. Anderson DH, Mullins RF, Hageman GS, Johnson LV. A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol. 2002;134:411-431.
7. Hageman GS, Luthert PJ, Chong NHV, Johnson LV, Anderson DH, Mullins RF. 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. Progr Retin Eye Res. 2001;20:705-732.
8. Jakobsdottir J, Conley YP, Weeks DE, Ferrell RE, Gorin MB. C2 and CFB genes in age-related maculopathy and joint action with CFH and LOC387715 genes. PLoS One. 2008;3: e2199.
9. Maller JB, Fagerness JA, Reynolds RC, Neale BM, Daly MJ, Seddon JM. Variation in complement factor 3 is associated with risk of age-related macular degeneration. Nat Genet. 2007;39:1200-1201.
10. Spencer KL, Hauser MA, Olson LM, et al. Protective effect of complement factor B and complement component 2 variants in age-related macular degeneration. Hum Mol Genet. 2007;16:1986-1992.
11. Spencer KL, Olson LM, Anderson BM, et al. C3 R102G polymorphism increases risk of age-related macular degeneration. Hum Mol Genet. 2008;17:1821-1824.
12. Edwards AO, Ritter R, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and agerelated macular degeneration. Science. 2005;308:421-424.
13. Hageman GS, Anderson DH, Johnson LV, et al. 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. 2005;102:7227-7232.
14. Haines JL, Hauser MA, Schmidt S, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308:419-421.
15. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005;308:385-389.
16. Zareparsi S, Branham KEH, Li MY, et al. Strong association of the Y402H variant in complement factor H at 1q32 with susceptibility to age-related macular degeneration. Am J Hum Genet. 2005;77:149-153.
17. Crabb JW, Miyagi M, Gu XR, et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci U S A. 2002;99:14682-14687.
18. Hageman GS, Mullins RF. Molecular composition of drusen as related to substructural phenotype. Mol Vis. 1999;5:28.
19. Johnson LV, Leitner WP, Staples MK, Anderson DH. Complement activation and inflammatory processes in drusen formation and age related macular degeneration. Exp Eye Res. 2001;73:887-896.
20. Johnson LV, Ozaki S, Staples MK, Erickson PA, Anderson DH. A potential role for immune complex pathogenesis in drusen formation. Exp Eye Res. 2000;70:441-449.
21. Mullins RF, Aptsiauri N, Hageman GS. Structure and composition of drusen associated with glomerulonephritis: implications for the role of complement activation in drusen biogenesis. Eye. 2001;15:390-395.
22. Nozaki M, Raisler BJ, Sakurai E, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A. 2006;103:2328-2333.
23. Hollyfield JG. Age-related macular degeneration: the molecular link between oxidative damage, tissue-specific inflammation and outer retinal disease: the Proctor Lecture. Invest Ophthalmol Vis Sci. 2010;51:1276-1281.
24. Murata S, Yashiroda H, Tanaka K. Molecular mechanisms of proteasome assembly. Nature Rev Mol Cell Biol. 2009;10:104-115.
25. Dahlmann B, Ruppert T, Kuehn L, Merforth S, Kloetzel PM. Different proteasome subtypes in a single tissue exhibit different enzymatic properties. J Mol Biol. 2000;303:643-653.
26. Klare N, Seeger M, Janek K, Jungblut PR, Dahlmann B. Intermediate-type 20 S proteasomes in HeLa cells: "asymmetric" subunit composition, diversity and adaptation. J Mol Biol. 2007;373:1-10.
27. Goldberg AL, Cascio P, Saric T, Rock KL. The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol. 2002;39:147-164.
28. Rock KL, Gramm C, Rothstein L, et al. Inhibitors of the proteasome block the degradation of most cell-proteins and the generation of peptides presented on Mhc Class-I molecules. Cell. 1994;78:761-771.
29. Ding QX, Martin S, Dimayuga E, Bruce-Keller AJ, Keller JN. LMP2 knock-out mice have reduced proteasome activities and increased levels of oxidatively damaged proteins. Antioxid Redox Signal. 2006;8:130-135.
30. Hayashi T, Faustman D. NOD mice are defective in proteasome production and activation of NF-kappa B. Mol Cell Biol. 1999;19:8646-8659.
31. Hayashi T, Faustman DL. Genome and hormones: gender differences in physiology selected contribution: association of gender-related LMP2 inactivation with autoimmune pathogenesis. J Appl Physiol. 2001;91:2804-2815.
32. Ferrington DA, Hussong SA, Roehrich H, et al. Immunoproteasome responds to injury in the retina and brain. J Neurochem. 2008;106:158-169.
33. Zhang XY, Zhou JL, Fernandes AF, et al. The proteasome: a target of oxidative damage in cultured human retina pigment epithelial cells. Invest Ophthalmol Vis Sci. 2008;49:3622-3630.
34. Hope AD, de Silva R, Fischer DF, Hol EM, van Leeuwen FW, Lees AJ. Alzheimer's associated variant ubiquitin causes inhibition of the 26S proteasome and chaperone expression. J Neurochem. 2003;86:394-404.
35. Dawson TM, Dawson VL. Molecular pathways of neurodegeneration in Parkinson's disease. Science. 2003;302:819-822.
36. Jahngenhodge J, Cyr D, Laxman E, Taylor A. Ubiquitin and ubiquitin conjugates in human lens. Exp Eye Res. 1992;55:897-902.
37. Dudek EJ, Shang F, Liu Q, Valverde P, Hobbs M, Taylor A. Selectivity of the ubiquitin pathway for oxidatively modified proteins: relevance to protein precipitation diseases. FASEB J. 2005;19:1707-1709.
38. Shang F, Gong X, Palmer HJ, Nowell TR, Taylor A. Age-related decline in ubiquitin conjugation in response to oxidative stress in the lens. Exp Eye Res. 1997;64:21-30.
39. Coux O, Tanaka K, Goldberg AL. Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem. 1996;65:801-847.
40. Louie JL, Kapphahn RJ, Ferrington DA. Proteasome function and protein oxidation in the aged retina. Exp Eye Res. 2002;75:271-284.
41. Kapphahn RJ, Bigelow EJ, Ferrington DA. Age-dependent inhibition of proteasome chymotrypsin-like activity in the retina. Exp Eye Res. 2007;84:646-654.
42. Mattapallil MJ, Wawrousek EF, Chan CC, et al. 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. 2012;53:2921-2927.
43. Despriet DDG, Klaver CCW, Witteman JCM, et al. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA. 2006;296:301-309.
44. Molday RS, Hicks D, Molday L. Peripherin. A rim-specific membrane-protein of rod outer segment disks. Invest Ophthalmol Vis Sci. 1987;28:50-61.
45. Papermaster DS. Preparation of retinal rod outer segments. Methods Enzymol. 1982;81:48-52.
46. Verdoes M, Florea BI, Menendez-Benito V, et al. A fluorescent broad-spectrum proteasome inhibitor for labeling proteasomes in vitro and in vivo. Chem Biol. 2006;13:1217-1226.
47. Berkers CR, van Leeuwen FWB, Groothuis TA, et al. Profiling proteasome activity in tissue with fluorescent probes. Mol Pharma. 2007;4:739-748.
48. Sambrook J, Gething MJ. Protein-structure. Chaperones, paperones. Nature. 1989;342:224-225.
49. Florea BI, Verdoes M, Li N, et al. Activity-based profiling reveals reactivity of the murine thymoproteasome-specific subunit beta 5t. Chem Biol. 2010;17:795-801.
50. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.
51. Bose S, Brooks P, Mason GGF, Rivett AJ. gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation. Biochem J. 2001;353:291-297.
52. Rivett AJ, Bose S, Brooks P, Broadfoot KI. Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie. 2001;83:363-366.
53. Tanaka K, Tanahashi N, Tsurumi C, Yokota KY, Shimbara N. Proteasomes and antigen processing. Adv Immunol. 1997;64:1-38.
54. Li ZM, Arnaud L, Rockwell P, Figueiredo-Pereira ME. A single amino acid substitution in a proteasome subunit triggers aggregation of ubiquitinated proteins in stressed neuronal cells. J Neurochem. 2004;90:19-28.
55. Boulton M, Rozanowska M, Rozanowski B. Retinal photodamage. J Photochem Photobiol B. 2001;64:144-161.
56. Fernandes AF, Guo WM, Zhang XY et al. Proteasomedependent regulation of signal transduction in retinal pigment epithelial cells. Exp Eye Res. 2006;83:1472-1481.
57. Witmer AN, Vrensen GFJM, Van Noorden CJF, Schlingemann RO. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res. 2003;22:1-29.
58. Grimm C, Wenzel A, Behrens A, Hafezi F, Wagner EF, Reme CE. AP-1 mediated retinal photoreceptor apoptosis is independent of N-terminal phosphorylation of c-Jun. Cell Death Differ. 2001;8:859-867.
59. Wenzel A, Grimm C, Seeliger MW et al. Prevention of photoreceptor apoptosis by activation of the glucocorticoid receptor. Invest Ophthalmol Vis Sci. 2001;42:1653-1659.
60. Iuvone PM, Brown AD, Haque R et al. Retinal melatonin production: role of proteasomal proteolysis in circadian and photic control of arylalkylamine N-acetyltransferase. Invest Ophthalmol Vis Sci. 2002;43:564-572.
61. Hohn A, Jung T, Grimm S, Catalgol B, Weber D, Grune T. Lipofuscin inhibits the proteasome by binding to surface motifs. Free Rad Biol Med. 2011;50:585-591.
62. Burke JM, Skumatz CMB. Autofluorescent inclusions in longterm postconfluent cultures of retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1998;39:1478-1486.
63. Wassell J, Ellis S, Burke J, Boulton M. Fluorescence properties of autofluorescent granules generated by cultured human RPE cells. Invest Ophthalmol Vis Sci. 1998;39:1487-1492.
64. Katz ML. Factors influencing lipofuscin accumulation in the retinal-pigment epithelium of the eye. Arch Biol. 1985;96:360.
65. Katz ML, Shanker MJ. Development of lipofuscin-Like fluorescence in the retinal-pigment epithelium in response to protease inhibitor treatment. Mech Ageing Dev. 1989;49:23-40.
66. Katz ML, Drea CM, Eldred GE, Hess HH, Robison WG. Influence of early photoreceptor degeneration on lipofuscin in the retinal-pigment epithelium. Exp Eye Res. 1986;43:561-573.
67. Katz ML, Eldred GE. Retinal light damage reduces autofluorescent pigment deposition in the retinal-pigment epithelium. Invest Ophthalmol Vis Sci. 1989;30:37-43.
68. Katz ML, Norberg M, Stientjes HJ. Reduced phagosomal content of the retinal-pigment epithelium in response to retinoid deprivation. Invest Ophthalmol Vis Sci. 1992;33:2612-2618.
69. Ambati J, Anand A, Fernandez S, et al. An animal model of agerelated macular degeneration in senescent Ccl-2-or Ccr-2-deficient mice. Nat Med. 2003;9:1390-1397.
70. Chen M, Forrester JV, Xu HP. Dysregulation in retinal parainflammation and age-related retinal degeneration in CCL2 or CCR2 deficient mice. PLoS One. 2011;6:e22818.
71. Luhmann UFO, Robbie S, Munro PMG, et al. The drusen-like phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci. 2009;50:5934-5943.
72. Vessey K, Greferath U, Jobling A, et al. Ccl2/Cx3Cr1 knock-out mice have inner retinal dysfunction but are not an accelerated model of age-related macular degeneration. Clin Exp Ophthalmol. 2012;40:131.