Decreased membrane complement regulators in the retinal pigmented epithelium contributes to age-related macular degeneration

Journal of Pathology

Volumn 229, Issue 5, 2013, Pages 729-742

  Ebrahimi, Katayoon B ^a   Fijalkowski, Natalia ^a   Cano, Marisol ^a   Handa, James T ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

age related macular degeneration; ageing; apoptosis; complement; exosome; oxidative stress

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CD59 ANTIGEN; CD63 ANTIGEN; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5B; LOW DENSITY LIPOPROTEIN; MEMBRANE COFACTOR PROTEIN; MESSENGER RNA; PROTEIN IRE1;

ADULT; AGED; APOPTOSIS; ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; EXOSOME; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION;

AGE FACTORS; AGED; AGED, 80 AND OVER; ANTIGENS, CD46; ANTIGENS, CD59; APOPTOSIS; CELL LINE; CELL MEMBRANE; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; DISEASE PROGRESSION; DOWN-REGULATION; ENDORIBONUCLEASES; EPITHELIAL CELLS; EXOSOMES; FEMALE; HUMANS; LIPOPROTEINS, LDL; MACULAR DEGENERATION; MALE; MEMBRANE PROTEINS; MIDDLE AGED; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN-SERINE-THREONINE KINASES; RETINAL DRUSEN; RETINAL PIGMENT EPITHELIUM; RNA INTERFERENCE; RNA, MESSENGER; TRANSFECTION; YOUNG ADULT;

EID: 84875053341     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4128     Document Type: Article

References (52)

1. Abdelsalam A, Del Priore L, Zarbin MA,. Drusen in age-related macular degeneration: pathogenesis, natural course, and laser photocoagulation-induced regression. Surv Ophthalmol 1999; 44: 1-29.
2. Dunaief JL, Dentchev T, Ying GS, et al,. The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 2002; 120: 1435-1442.
3. Del Priore LV, Kuo YH, Tezel TH,. Age-related changes in human RPE cell density and apoptosis proportion in situ. Invest Ophthalmol Vis Sci 2002; 43: 3312-3318.
4. Spaide RF, Ho-Spaide WC, Browne RW, et al,. Characterization of peroxidized lipids in Bruch's membrane. Retina 1999; 19: 141-147.
5. Green WR, McDonnell PJ, Yeo JH,. Pathologic features of senile macular degeneration. Ophthalmology 1985; 92: 615-627.
6. Malek G, Li CM, Guidry C, et al,. Apolipoprotein B in cholesterol-containing drusen and basal deposits of human eyes with age-related maculopathy. Am J Pathol 2003; 162: 413-425.
7. Li CM, Chung BH, Presley JB, et al,. Lipoprotein-like particles and cholesteryl esters in human Bruch's membrane: initial characterization. Invest Ophthalmol Vis Sci 2005; 46: 2576-2586.
8. Curcio CA, Presley JB, Malek G, et al,. Esterified and unesterified cholesterol in drusen and basal deposits of eyes with age-related maculopathy. Exp Eye Res 2005; 81: 731-741.
9. Yamada Y, Tian J, Yang Y, et al,. Oxidized low density lipoproteins induce a pathologic response by retinal pigmented epithelial cells. J Neurochem 2008; 105: 1187-1197.
10. Sarks JP, Sarks SH, Killingsworth MC,. Evolution of geographic atrophy of the retinal pigment epithelium. Eye 1988; 2 (5): 552-577.
11. Edwards AO, Ritter Iii R, Abel KJ, et al,. Complement factor H polymorphism and age-related macular degeneration. Science 2005; 308: 421-424.
12. 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 USA 2005; 102: 7227-7232.
13. 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.
14. Klein RJ, Zeiss C, Chew EY, et al,. Complement factor H polymorphism in age-related macular degeneration. Science 2005; 308: 385-389.
15. Atkinson JP, Goodship TH,. Complement factor H and the hemolytic uremic syndrome. J Exp Med 2007; 204: 1245-1248.
16. Elward K, Griffiths M, Mizuno M, et al,. CD46 plays a key role in tailoring innate immune recognition of apoptotic and necrotic cells. J Biol Chem 2005; 280: 36342-36354.
17. Anderson DH, Radeke MJ, Gallo NB, et al,. The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis revisited. Prog Retin Eye Res 2010; 29: 95-112.
18. Johnson LV, Leitner WP, Staples MK, et al,. Complement activation and inflammatory processes in Drusen formation and age related macular degeneration. Exp Eye Res 2001; 73: 887-896.
19. Vogt SD, Barnum SR, Curcio CA, et al,. Distribution of complement anaphylatoxin receptors and membrane-bound regulators in normal human retina. Exp Eye Res 2006; 83: 834-840.
20. Cole DS, Hughes TR, Gasque P, et al,. Complement regulator loss on apoptotic neuronal cells causes increased complement activation and promotes both phagocytosis and cell lysis. Mol Immunol 2006; 43: 1953-1964.
21. Vogt SD, Curcio CA, Wang L, et al,. Retinal pigment epithelial expression of complement regulator CD46 is altered early in the course of geographic atrophy. Exp Eye Res 2011; 93: 413-423.
22. Seibold S, Schurle D, Heinloth A, et al,. Oxidized LDL induces proliferation and hypertrophy in human umbilical vein endothelial cells via regulation of p27Kip1 expression: role of RhoA. J Am Soc Nephrol 2004; 15: 3026-3034.
23. Satirapoj B, Bruhn KW, Nast CC, et al,. Oxidized low-density lipoprotein antigen transport induces autoimmunity in the renal tubulointerstitium. Am J Nephrol 2012; 35: 520-530.
24. Hirose K, Iwabuchi K, Shimada K, et al,. Different responses to oxidized low-density lipoproteins in human polarized macrophages. Lipids Health Dis 2011; 10: 1.
25. Holvoet P, Mertens A, Verhamme P, et al,. Circulating oxidized LDL is a useful marker for identifying patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2001; 21: 844-848.
26. Nishi K, Itabe H, Uno M, et al,. Oxidized LDL in carotid plaques and plasma associates with plaque instability. Arterioscler Thromb Vasc Biol 2002; 22: 1649-1654.
27. Seimon TA, Nadolski MJ, Liao X, et al,. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab 12: 467-482.
28. Cox JS, Shamu CE, Walter P,. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 1993; 73: 1197-1206.
29. van Niel G, Porto-Carreiro I, Simoes S, et al,. Exosomes: a common pathway for a specialized function. J Biochem 2006; 140: 13-21.
30. Chang MK, Bergmark C, Laurila A, et al,. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA 1999; 96: 6353-6358.
31. Nicholson DW, Ali A, Thornberry NA, et al,. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376: 37-43.
32. Tewari M, Quan LT, O'Rourke K, et al,. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995; 81: 801-809.
33. Oliver FJ, de la Rubia G, Rolli V, et al,. Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem 1998; 273: 33533-33539.
34. Bhutto IA, Baba T, Merges C, et al,. C-reactive protein and complement factor H in aged human eyes and eyes with age-related macular degeneration. Br J Ophthalmol 2011; 95: 1323-1330.
35. Esparza-Gordillo J, Soria JM, Buil A, et al,. Genetic and environmental factors influencing the human factor H plasma levels. Immunogenetics 2004; 56: 77-82.
36. Call TW, Hollyfield JG,. Sulfated proteoglycans in Bruch's membrane of the human eye: localization and characterization using cupromeronic blue. Exp Eye Res 1990; 51: 451-462.
37. Kelly U, Yu L, Kumar P, et al,. Heparan sulfate, including that in Bruch's membrane, inhibits the complement alternative pathway: implications for age-related macular degeneration. J Immunol 2010; 185: 5486-5494.
38. Nadanaka S, Kitagawa H,. Heparan sulphate biosynthesis and disease. J Biochem 2008; 144: 7-14.
39. Hussain AA, Starita C, Hodgetts A, et al,. Macromolecular diffusion characteristics of ageing human Bruch's membrane: implications for age-related macular degeneration (AMD). Exp Eye Res 90: 703-710.
40. Wu Z, Lauer TW, Sick A, et al,. Oxidative stress modulates complement factor H expression in retinal pigmented epithelial cells by acetylation of FOXO3. J Biol Chem 2007; 282: 22414-22425.
41. Thurman JM, Renner B, Kunchithapautham K, et al,. Oxidative stress renders retinal pigment epithelial cells susceptible to complement-mediated injury. J Biol Chem 2009; 284: 16939-16947.
42. Hakulinen J, Junnikkala S, Sorsa T, et al,. Complement inhibitor membrane cofactor protein (MCP; CD46) is constitutively shed from cancer cell membranes in vesicles and converted by a metalloproteinase to a functionally active soluble form. Eur J Immunol 2004; 34: 2620-2629.
43. Van Den Berg CW, De Andrade RM, Magnoli FC, et al,. Loxosceles spider venom induces metalloproteinase mediated cleavage of MCP/CD46 and MHCI and induces protection against C-mediated lysis. Immunology 2002; 107: 102-110.
44. Lehto MT, Sharom FJ,. PI-specific phospholipase C cleavage of a reconstituted GPI-anchored protein: modulation by the lipid bilayer. Biochemistry 2002; 41: 1398-1408.
45. Oikawa D, Tokuda M, Hosoda A, et al,. Identification of a consensus element recognized and cleaved by IRE1α. Nucleic Acids Res 2010; 38: 6265-6273.
46. Hollien J, Lin JH, Li H, et al,. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009; 186: 323-331.
47. Huang Y, Qiao F, Abagyan R, et al,. Defining the CD59-C9 binding interaction. J Biol Chem 2006; 281: 27398-27404.
48. Scholl HP, Charbel Issa P, Walier M, et al,. Systemic complement activation in age-related macular degeneration. PLoS One 2008; 3: e2593.
49. Papadimitriou JC, Ramm LE, Drachenberg CB, et al,. Quantitative analysis of adenine nucleotides during the prelytic phase of cell death mediated by C5b-9. J Immunol 1991; 147: 212-217.
50. Papadimitriou JC, Drachenberg CB, Shin ML, et al,. Ultrastructural studies of complement mediated cell death: a biological reaction model to plasma membrane injury. Virchows Archiv 1994; 424: 677-685.
51. Cragg MS, Howatt WJ, Bloodworth L, et al,. Complement mediated cell death is associated with DNA fragmentation. Cell Death Differ 2000; 7: 48-58.
52. Tegla CA, Cudrici C, Patel S, et al,. Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res 2011; 51: 45-60.