Complement factor H binds malondialdehyde epitopes and protects from oxidative stress

Nature

Volumn 478, Issue 7367, 2011, Pages 76-81

  Weismann, David ^a,b   Hartvigsen, Karsten ^a,b,c   Lauer, Nadine ^d   Bennett, Keiryn L ^a   Scholl, Hendrik P N ^e   Issa, Peter Charbel ^f   Cano, Marisol ^e   Brandstätter, Hubert ^b,g   Tsimikas, Sotirios ^c   Skerka, Christine ^d   Superti Furga, Giulio ^a   Handa, James T ^e   Zipfel, Peter F ^d   Witztum, Joseph L ^c   Binder, Christoph J ^a,b,c  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d HANS KNÖLL INSTITUTE   (Germany)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g Octapharma PPGmbH Research and Development   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT FACTOR H; MALONALDEHYDE;

BLINDNESS; ETIOLOGY; IMMUNE RESPONSE; LIPID; POLYMORPHISM; PROTEIN; RODENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; GENE DELETION; HUMAN; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; RETINA MACULA AGE RELATED DEGENERATION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; APOPTOSIS; BINDING SITES; COMPLEMENT FACTOR H; COMPLEMENT INACTIVATOR PROTEINS; COMPLEMENT SYSTEM PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; FEMALE; HUMANS; INFLAMMATION; LIPID PEROXIDATION; MACROPHAGES, PERITONEAL; MACULAR DEGENERATION; MALE; MALONDIALDEHYDE; MICE; MICE, INBRED C57BL; MUTATION; NECROSIS; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RETINA;

MUS;

EID: 80053904386     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10449     Document Type: Article

References (42)

1. Chou, M. Y. et al. Oxidation-specific epitopes are important targets of innate immunity. J. Intern. Med. 263, 479-488 (2008).
2. Esterbauer, H., Schaur, R. J. & Zollner, H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11, 81-128 (1991). (Pubitemid 121003917)
3. Chang, M. K. 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 96, 6353-6358 (1999).
4. Miller, Y. I. et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized bypattern recognition receptors of innate immunity. Circ. Res. 108, 235-248 (2011).
5. Hollyfield, J. G. et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nature Med. 14, 194-198 (2008). (Pubitemid 351214555)
6. Suzuki, M. et al. Oxidized phospholipids in the macula increase with age and in eyes with age-related macular degeneration. Mol. Vis. 13, 772-778 (2007). (Pubitemid 46850583)
7. Jager, R. D., Mieler, W. F.&Miller, J. W. Age-relatedmacular degeneration. N. Engl. J. Med. 358, 2606-2617 (2008).
8. Schutt, F., Bergmann, M., Holz, F. G. & Kopitz, J. Proteins modified by malondialdehyde, 4-hydroxynonenal, or advanced glycation end products in lipofuscin of human retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 44, 3663-3668 (2003). (Pubitemid 36909809)
9. Thiele, G. M. et al.Malondialdehyde-acetaldehyde (MAA)modified proteins induce pro-inflammatory and pro-fibrotic responses by liver endothelial cells. Comp. Hepatol. 3 (suppl. 1), S25 (2004).
10. Shanmugam, N. et al. Proinflammatory effects of advanced lipoxidation end products in monocytes. Diabetes 57, 879-888 (2008).
11. Shechter, I. et al. The metabolism of native and malondialdehyde-altered low density lipoproteins by human monocyte-macrophages. J. Lipid Res. 22, 63-71 (1981). (Pubitemid 11144708)
12. Chou, M. Y. et al. Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 119, 1335-1349 (2009).
13. Xu, D. et al. Epitope characterization of malondialdehyde-acetaldehyde adducts using an enzyme-linked immunosorbent assay. Chem. Res. Toxicol. 10, 978-986 (1997). (Pubitemid 27418013)
14. Zipfel, P. F. & Skerka, C. Complement regulators and inhibitory proteins. Nature Rev. Immunol. 9, 729-740 (2009).
15. Józsi, M. & Zipfel, P. F. Factor H family proteins and human diseases. Trends Immunol. 29, 380-387 (2008).
16. Haines, J. L. et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 308, 419-421 (2005). (Pubitemid 40530081)
17. Klein, R. J. et al. Complement factor H polymorphism in age-related macular degeneration. Science 308, 385-389 (2005). (Pubitemid 40530070)
18. Edwards, A. O. et al. Complement factorHpolymorphismand age-related macular degeneration. Science 308, 421-424 (2005). (Pubitemid 40530082)
19. Hageman, G. S. 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 102, 7227-7232 (2005). (Pubitemid 40696361)
20. Hughes, A. E. et al.AcommonCFHhaplotype, with deletion of CFHR1 andCFHR3, is associated with lower risk of age-related macular degeneration. Nature Genet. 38, 1173-1177 (2006). (Pubitemid 44470363)
21. Takizawa, F., Tsuji, S. & Nagasawa, S. Enhancement of macrophage phagocytosis upon iC3b deposition on apoptotic cells. FEBS Lett. 397, 269-272 (1996). (Pubitemid 26414031)
22. Amarilyo, G. et al. iC3b-opsonized apoptotic cells mediate a distinct antiinflammatory response and transcriptional NF-kB-dependent blockade. Eur. J. Immunol. 40, 699-709 (2010).
23. Higgins, G. T., Wang, J. H., Dockery, P., Cleary, P. E. & Redmond, H. P. Induction of angiogenic cytokine expression in cultured RPE by ingestion of oxidized photoreceptorouter segments. Invest.Ophthalmol. Vis. Sci.44,1775-1782(2003). (Pubitemid 36378609)
24. de Jong, P. T. Age-related macular degeneration. N. Engl. J. Med. 355, 1474-1485 (2006). (Pubitemid 44511562)
25. Binder, C. J. et al. Innate and acquired immunity in atherogenesis. Nature Med. 8, 1218-1226 (2002). (Pubitemid 35373552)
26. Flierman, R. & Daha, M. R. The clearance of apoptotic cells by complement. Immunobiology 212, 363-370 (2007). (Pubitemid 46825236)
27. Trouw, L. A. et al. C4b-binding protein and factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. J. Biol. Chem. 282, 28540-28548 (2007). (Pubitemid 47606049)
28. Meri, S. & Pangburn, M. K. Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl Acad. Sci. USA 87, 3982-3986 (1990).
29. Leffler, J. et al. Annexin-II, DNA, and histones serve as factor H ligands on the surface of apoptotic cells. J. Biol. Chem. 285, 3766-3776 (2010).
30. Savill, J., Dransfield, I., Gregory, C. & Haslett, C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nature Rev. Immunol. 2, 965-975 (2002). (Pubitemid 37323217)
31. Chang, M. K. et al. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J. Exp. Med. 200, 1359-1370 (2004).
32. Mihlan, M., Stippa, S., Jozsi, M. & Zipfel, P. F. Monomeric CRP contributes to complement control in fluid phase and on cellular surfaces and increases phagocytosis by recruiting factor H. Cell Death Differ. 16, 1630-1640 (2009).
33. Thakkinstian, A. et al. Systematic review and meta-analysis of the association between complement factor H Y402H polymorphisms and age-related macular degeneration. Hum. Mol. Genet. 15, 2784-2790 (2006). (Pubitemid 44400405)
34. Donoso, L. A., Vrabec, T. & Kuivaniemi, H. The role of complement factor H in agerelated macular degeneration: a review. Surv. Ophthalmol. 55, 227-246 (2010).
35. Clark, S. J. et al. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the nondisease-associated form. J. Biol. Chem. 281, 24713-24720 (2006). (Pubitemid 44274245)
36. Green, W. R. & Enger, C. Age-related macular degeneration histopathologic studies. The 1992 Lorenz E. Zimmerman Lecture. Ophthalmology 100, 1519-1535 (1993). (Pubitemid 23292863)
37. Sun, M. et al. Light-induced oxidation of photoreceptor outer segment phospholipids generates ligands for CD36-mediated phagocytosis by retinal pigment epithelium: a potential mechanism for modulating outer segment phagocytosis under oxidant stress conditions. J. Biol. Chem. 281, 4222-4230 (2006). (Pubitemid 43847851)
38. Kaemmerer, E., Schutt, F., Krohne, T. U., Holz, F. G. & Kopitz, J. Effects of lipid peroxidation-related protein modifications on RPE lysosomal functions and POS phagocytosis. Invest. Ophthalmol. Vis. Sci. 48, 1342-1347 (2007). (Pubitemid 351261433)
39. Goverdhan, S. V. et al. Interleukin-8 promoter polymorphism 2251A/T is a risk factor for age-related macular degeneration. Br. J. Ophthalmol. 92, 537-540 (2008). (Pubitemid 351497986)
40. Sofat, R. et al. Genetic variation in complement factor H and risk of coronary heart disease: eight new studies and a meta-analysis of around 48,000 individuals. Atherosclerosis 213, 184-190 (2010).
41. Scholl, H. P. et al. Systemic complement activation in age-related macular degeneration. PLoS ONE 3, e2593 (2008).
42. Binder, C. J. et al. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nature Med. 9, 736-743 (2003). (Pubitemid 36749223)