A targeted inhibitor of the alternative complement pathway reduces angiogenesis in a mouse model of age-related macular degeneration

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 7, 2009, Pages 3056-3064

  Rohrer, Bärbel ^a   Long, Qin ^a   Coughlin, Beth ^a   Brooks Wilson, R ^a   Huang, Yuxiang ^a   Qiao, Fei ^a   Tang, Peter H ^a   Kunchithapautham, Kannan ^a   Gilkeson, Gary S ^a   Tomlinson, Stephen ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT FACTOR H; COMPLEMENT INHIBITOR; HISTIDINE; MESSENGER RNA; PHOSPHATE BUFFERED SALINE; TYROSINE; VASCULOTROPIN; COMPLEMENT COMPONENT C3; CR2 CRRY FUSION PROTEIN, MOUSE; CR2-CRRY FUSION PROTEIN, MOUSE; HYBRID PROTEIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL SURFACE; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT DEFICIENCY; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFICACY; DRUG TARGETING; FEMALE; GENETIC VARIABILITY; HISTOPATHOLOGY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION; SENSORY SYSTEM ELECTROPHYSIOLOGY; SUBRETINAL NEOVASCULARIZATION; TREATMENT OUTCOME; ANIMAL; C57BL MOUSE; CHOROID; COMPLEMENT ACTIVATION; DRUG ANTAGONISM; DRUG EFFECT; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; INTRAVENOUS DRUG ADMINISTRATION; MALE; METABOLISM; MOUSE MUTANT; PATHOPHYSIOLOGY; PIGMENT EPITHELIUM; RETINA; RETINA MACULA DEGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; CHOROID; CHOROIDAL NEOVASCULARIZATION; COMPLEMENT ACTIVATION; COMPLEMENT C3; COMPLEMENT FACTOR H; COMPLEMENT PATHWAY, ALTERNATIVE; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; INFUSIONS, INTRAVENOUS; MACULAR DEGENERATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT FUSION PROTEINS; RETINA; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 67649989567     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-2222     Document Type: Article

References (39)

1. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005;308: 385-389.
2. Edwards AO, Ritter R 3rd, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science. 2005;308:421-424.
3. 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.
4. 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.
5. Li M, Atmaca-Sonmez P, Othman M, et al. CFH haplotypes without the Y402H coding variant show strong association with susceptibility to age-related macular degeneration. Nat Genet. 2006;38: 1049-1054.
6. Gold B, Merriam JE, Zernant J, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with agerelated macular degeneration. Nat Genet. 2006;38:458-462.
7. Yates JR, Sepp T, Matharu BK, et al. Complement C3 variant and the risk of age-related macular degeneration. N Engl J Med. 2007; 357:553-561.
8. Despriet DD, Klaver CC, Witteman JC, et al. Complement factor H polymorphism, complement activators, and risk of age-related macular degeneration. JAMA. 2006;296:301-309.
9. de Cordoba SR, de Jorge EG. Translational mini-review series on complement factor H: genetics and disease associations of human complement factor H. Clin Exp Immunol. 2008;151:1-13.
10. Prosser BE, Johnson S, Roversi P, et al. Structural basis for complement factor H linked age-related macular degeneration. J Exp Med. 2007;204:2277-2283.
11. Clark SJ, Higman VA, Mulloy B, et al. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the non-disease-associated form. J Biol Chem. 2006;281:24713-24720.
12. Ormsby RJ, Ranganathan S, Tong JC, et al. Functional and structural implications of the complement factor H Y402H polymorphism associated with age-related macular degeneration. Invest Ophthalmol Vis Sci. 2008;49:1763-1770.
13. Hakobyan S, Harris CL, van den Berg CW, et al. Complement factor H binds to denatured rather than to native pentameric C-reactive protein. J Biol Chem. 2008;283:30451-30460.
14. Atkinson C, Qiao F, Song H, Gilkeson GS, Tomlinson S. Low-dose targeted complement inhibition protects against renal disease and other manifestations of autoimmune disease in MRL/lpr mice. J Immunol. 2008;180:1231-1238.
15. Atkinson C, Song H, Lu B, et al. Targeted complement inhibition by C3d recognition ameliorates tissue injury without apparent increase in susceptibility to infection. J Clin Invest. 2005;115:2444-2453.
16. Huang Y, Qiao F, Atkinson C, Holers VM, Tomlinson S. A novel targeted inhibitor of the alternative pathway of complement and its therapeutic application in ischemia/reperfusion injury. J Immunol. 2008;181:8068-8076.
17. 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.
18. Song H, He C, Knaak C, Guthridge JM, Holers VM, Tomlinson S. Complement receptor 2-mediated targeting of complement inhibitors to sites of complement activation. J Clin Invest. 2003;111: 1875-1885.
19. Rohrer B, Korenbrot JI, LaVail MM, Reichardt LF, Xu B. Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J Neurosci. 1999;19:8919-8930.
20. Molina H, Kinoshita T, Inoue K, Carel JC, Holers VM. A molecular and immunochemical characterization of mouse CR2: evidence for a single gene model of mouse complement receptors 1 and 2. J Immunol. 1990;145:2974-2983.
21. Gresh J, Goletz PW, Crouch RK, Rohrer B. Structure-function analysis of rods and cones in juvenile, adult, and aged C57bl/6 and Balb/c mice. Vis Neurosci. 2003;20:211-220.
22. Richards A, Emondi AA, Rohrer B. Long-term ERG analysis in the partially light-damaged mouse retina reveals regressive and compensatory changes. Vis Neurosci. 2006;23:91-97.
23. Lohr HR, Kuntchithapautham K, Sharma AK, Rohrer B. Multiple, parallel cellular suicide mechanisms participate in photoreceptor cell death. Exp Eye Res. 2006;83:380-389.
24. Espinosa-Heidmann DG, Suner I, Hernandez EP, Frazier WD, Csaky KG, Cousins SW. Age as an independent risk factor for severity of experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2002;43:1567-1573.
25. Bora PS, Hu Z, Tezel TH, et al. Immunotherapy for choroidal neovascularization in a laser-induced mouse model simulating exudative (wet) macular degeneration. Proc Natl Acad Sci U S A. 2003;100:2679-2684.
26. Caicedo A, Espinosa-Heidmann DG, Hamasaki D, Pina Y, Cousins SW. Photoreceptor synapses degenerate early in experimental choroidal neovascularization. J Comp Neurol. 2005;483:263-277.
27. Johnson MA, Marcus S, Elman MJ, McPhee TJ. Neovascularization in central retinal vein occlusion: electroretinographic findings. Arch Ophthalmol. 1988;106:348-352.
28. Sabates R, Hirose T, McMeel JW. Electroretinography in the prognosis and classification of central retinal vein occlusion. Arch Ophthalmol. 1983;101:232-235.
29. Pugh EN Jr, Falsini B, Lyubarsky AL. The Origin of the Major Rodand Cone-Driven Components of the Rodent Electroretinogram and the Effect of Age and Light-Rearing History on the Magnitude of These Components. New York: Plenum Press;1998:93-128.
30. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, Mullins RF. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res. 2001;20:705-732.
31. Bora NS, Kaliappan S, Jha P, et al. Complement activation via alternative pathway is critical in the development of laser-induced choroidal neovascularization: role of factor B and factor H. J Immunol. 2006;177:1872-1878.
32. Bora NS, Kaliappan S, Jha P, et al. CD59, a complement regulatory protein, controls choroidal neovascularization in a mouse model of wet-type age-related macular degeneration. J Immunol. 2007;178: 1783-1790.
33. Hu W, Criswell MH, Fong SL, et al. Differences in the temporal expression of regulatory growth factors during choroidal neovascular development. Exp Eye Res. 2009;88:79-91.
34. Bora PS, Sohn JH, Cruz JM, et al. Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization. J Immunol. 2005;174:491-497.
35. Kleinman ME, Yamada K, Takeda A, et al. Sequence-and targetindependent angiogenesis suppression by siRNA via TLR3. Nature. 2008;452:591-597.
36. Coffey PJ, Gias C, McDermott CJ, et al. Complement factor H deficiency in aged mice causes retinal abnormalities and visual dysfunction. Proc Natl Acad Sci U S A. 2007;104:16651-16656.
37. Rose KL, Paixao-Cavalcante D, Fish J, et al. Factor I is required for the development of membranoproliferative glomerulonephritis in factor H-deficient mice. J Clin Invest. 2008;118:608-618.
38. Rohrer B, Guo Y, Kunchithapautham K, Gilkeson GS. Eliminating complement factor D reduces photoreceptor susceptibility to light-induced damage. Invest Ophthalmol Vis Sci. 2007;48:5282-5289.
39. Oshima Y, Oshima S, Nambu H, et al. Increased expression of VEGF in retinal pigmented epithelial cells is not sufficient to cause choroidal neovascularization. J Cell Physiol. 2004;201: 393-400.