A targeted inhibitor of the alternative complement pathway accelerates recovery from smoke-induced ocular injury

Investigative Ophthalmology and Visual Science

Volumn 57, Issue 4, 2016, Pages 1728-1737

  Woodell, Alex ^a   Jones, Bryan W ^b   Williamson, Tucker ^a   Schnabolk, Gloriane ^c   Tomlinson, Stephen ^a,c   Atkinson, Carl ^a   Rohrer, Bärbel ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Alternative complement pathway; Bruch s membrane deposits; CR2 fH; Dry age related macular degeneration; Knockout mouse; Mitochondria; Smoke exposure

Indexed keywords

BETA ACTIN; CIGARETTE SMOKE; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 2 FACTOR H; UNCLASSIFIED DRUG; CR2-FH PROTEIN; DNA; HYBRID PROTEIN; SMOKE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BRUCH MEMBRANE; COMPLEMENT ALTERNATIVE PATHWAY; CONTRAST SENSITIVITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EYE INJURY; GENE EXPRESSION; MOUSE; NONHUMAN; OPTOKINETIC STIMULATION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING; SPATIAL FREQUENCY DISCRIMINATION; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; SPECTROPHOTOMETRY; ULTRASTRUCTURE; VISUAL ACUITY; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; ELECTRORETINOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; MACULAR DEGENERATION; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; RETINAL PIGMENT EPITHELIUM; SMOKE;

ANIMALS; COMPLEMENT PATHWAY, ALTERNATIVE; DISEASE MODELS, ANIMAL; DNA; ELECTRORETINOGRAPHY; GENE EXPRESSION REGULATION; MACULAR DEGENERATION; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; RECOVERY OF FUNCTION; RETINA; RETINAL PIGMENT EPITHELIUM; SMOKE; VISUAL ACUITY;

EID: 84976864076     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-18471     Document Type: Article

References (46)

1. Wong WL, Su X, Li X, et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Health. 2014;2:e106-e116.
2. Ferris FL III, Wilkinson CP, Bird A, et al. Clinical classification of age-related macular degeneration. Ophthalmology. 2013; 120:844-851.
3. Freund KB, Zweifel SA, Engelbert M. Do we need a new classification for choroidal neovascularization in age-related macular degeneration? Retina. 2010;30:1333-1349.
4. Brown MM, Brown GC, Stein JD, Roth Z, Campanella J, Beauchamp GR. Age-related macular degeneration: economic burden and value-based medicine analysis. Can J Ophthalmol. 2005;40:277-287.
5. Wang JC, Cao S, Wang A, et al. CFH Y402H polymorphism is associated with elevated vitreal GM-CSF and choroidal macrophages in the postmortem human eye. Mol Vis. 2015; 21:264-272.
6. Langford-Smith A, Keenan TD, Clark SJ, Bishop PN, Day AJ. The role of complement in age-related macular degeneration: heparan sulphate, a ZIP code for complement factor H? J Innate Immun. 2014;6:407-416.
7. Clark SJ, Bishop PN. Role of factor H and related proteins in regulating complement activation in the macula, and relevance to age-related macular degeneration. J Clin Med. 2015;4: 18-31.
8. Dikmetas O, Kadayifcilar S, Eldem B. The effect of CFH polymorphisms on the response to the treatment of agerelated macular degeneration (AMD) with intravitreal ranibizumab. Mol Vis. 2013;19:2571-2578.
9. Ni Dhubhghaill SS, Cahill MT, Campbell M, Cassidy L, Humphries MM, Humphries P. The pathophysiology of cigarette smoking and age-related macular degeneration. Adv Exp Med Biol. 2010;664:437-446.
10. Chakravarthy U, Augood C, Bentham GC, et al. Cigarette smoking and age-related macular degeneration in the EUREYE Study. Ophthalmology. 2007;114:1157-1163.
11. Mitchell P, Wang JJ, Smith W, Leeder SR. Smoking and the 5-year incidence of age-related maculopathy: the Blue Mountains Eye Study. Arch Ophthalmol. 2002;120:1357-1363.
12. Khan JC, Thurlby DA, Shahid H, et al. Smoking and age related macular degeneration: the number of pack years of cigarette smoking is a major determinant of risk for both geographic atrophy and choroidal neovascularisation. Br J Ophthalmol. 2006;90:75-80.
13. Bertram KM, Baglole CJ, Phipps RP, Libby RT. Molecular regulation of cigarette smoke induced-oxidative stress in human retinal pigment epithelial cells: implications for agerelated macular degeneration. Am J Physiol Cell Physiol. 2009; 297:C1200-C1210.
14. Pons M, Marin-Castano ME. Cigarette smoke-related hydroquinone dysregulates MCP-1, VEGF and PEDF expression in retinal pigment epithelium in vitro and in vivo. PLoS One. 2011;6:e16722.
15. Kew RR, Ghebrehiwet B, Janoff A. Cigarette smoke can activate the alternative pathway of complement in vitro by modifying the third component of complement. J Clin Invest. 1985;75:1000-1007.
16. Kunchithapautham K, Atkinson C, Rohrer B. Smoke exposure causes endoplasmic reticulum stress and lipid accumulation in retinal pigment epithelium through oxidative stress and complement activation. J Biol Chem. 2014;289:14534-14546.
17. Fujihara M, Nagai N, Sussan TE, Biswal S, Handa JT. Chronic cigarette smoke causes oxidative damage and apoptosis to retinal pigmented epithelial cells in mice. PLoS One. 2008;3: e3119.
18. Wang AL, Lukas TJ, Yuan M, Du N, Handa JT, Neufeld AH. Changes in retinal pigment epithelium related to cigarette smoke: possible relevance to smoking as a risk factor for agerelated macular degeneration. PLoS One. 2009;4:e5304.
19. Jia L, Liu Z, Sun L, et al. Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: protection by (R)-alpha-lipoic acid. Invest Ophthalmol Vis Sci. 2007;48:339-348.
20. Espinosa-Heidmann DG, Suner IJ, Catanuto P, Hernandez EP, Marin-Castano ME, Cousins SW. Cigarette smoke-related oxidants and the development of sub-RPE deposits in an experimental animal model of dry AMD. Invest Ophthalmol Vis Sci. 2006;47:729-737.
21. Woodell A, Coughlin B, Kunchithapautham K, et al. Alternative complement pathway deficiency ameliorates chronic smokeinduced functional and morphological ocular injury. PLoS One. 2013;8:e67894.
22. Jobse BN, McCurry CA, Morissette MC, Rhem RG, Stampfli MR, Labiris NR. Impact of inflammation, emphysema, and smoking cessation on V/Q in mouse models of lung obstruction. Respir Res. 2014;15:42.
23. Koike K, Ishigami A, Sato Y, et al. Vitamin C prevents cigarette smoke-induced pulmonary emphysema in mice and provides pulmonary restoration. Am J Respir Cell Mol Biol. 2014;50: 347-357.
24. Duan MC, Tang HJ, Zhong XN, Huang Y. Persistence of Th17/ Tc17 cell expression upon smoking cessation in mice with cigarette smoke-induced emphysema. Clin Dev Immunol. 2013;2013:350727.
25. 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.
26. Rohrer B, Long Q, Coughlin B, et al. A targeted inhibitor of the alternative complement pathway reduces angiogenesis in a mouse model of age-related macular degeneration. Invest Ophthalmol Vis Sci. 2009;50:3056-3064.
27. 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.
28. Bandyopadhyay M, Rohrer B. Matrix metalloproteinase activity creates pro-angiogenic environment in primary human retinal pigment epithelial cells exposed to complement. Invest Ophthalmol Vis Sci. 2012;53:1953-1961.
29. Joseph K, Kulik L, Coughlin B, et al. Oxidative stress sensitizes RPE cells to complement-mediated injury in a natural antibody-, lectin pathway-and phospholipid epitope-dependent manner. J Biol Chem. 2013;288:12753-12765.
30. Matsumoto M, Fukuda W, Circolo A, et al. Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc Natl Acad Sci U S A. 1997;94:8720-8725.
31. Watson ES, Jones AB, Ashfaq MK, Barrett JT. Spectrophotometric evaluation of carboxyhemoglobin in blood of mice after exposure to marijuana or tobacco smoke in a modified Walton horizontal smoke exposure machine. J Anal Toxicol. 1987;11: 19-23.
32. Yao H, Arunachalam G, Hwang JW, et al. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc Natl Acad Sci U S A. 2010;107:15571-15576.
33. Yao H, Chung S, Hwang JW, et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest. 2012;122:2032-2045.
34. Chen ZH, Kim HP, Sciurba FC, et al. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS One. 2008;3:e3316.
35. Marc RE, Liu W. Fundamental GABAergic amacrine cell circuitries in the retina: nested feedback, concatenated inhibition, and axosomatic synapses. J Comp Neurol. 2000; 425:560-582.
36. Anderson JR, Jones BW, Yang JH, et al. A computational framework for ultrastructural mapping of neural circuitry. PLoS Biol. 2009;7:e1000074.
37. Stoppelkamp S, Riedel G, Platt B. Culturing conditions determine neuronal and glial excitability. J Neurosci Methods. 2010;194:132-138.
38. Mettu PS, Wielgus AR, Ong SS, Cousins SW. Retinal pigment epithelium response to oxidant injury in the pathogenesis of early age-related macular degeneration. Mol Aspects Med. 2012;33:376-398.
39. Owsley C, McGwin G, Jackson GR, et al. Effect of short-term, high-dose retinol on dark adaptation in aging and early agerelated maculopathy. Invest Ophthalmol Vis Sci. 2006;47: 1310-1318.
40. Holers VM, Rohrer B, Tomlinson S. CR2-mediated targeting of complement inhibitors: bench-to-bedside using a novel strategy for site-specific complement modulation. Adv Exp Med Biol. 2013;735:137-154.
41. Neuner B, Komm A, Wellmann J, et al. Smoking history and the incidence of age-related macular degeneration-results from the Muenster Aging and Retina Study (MARS) cohort and systematic review and meta-analysis of observational longitudinal studies. Addict Behav. 2009;34:938-947.
42. Elvington M, Schepp-Berglind J, Tomlinson S. Regulation of the alternative pathway of complement modulates injury and immunity in a chronic model of dextran sulphate sodiuminduced colitis. Clin Exp Immunol. 2015;179:500-508.
43. Hu X, Tomlinson S, Barnum SR. Targeted inhibition of complement using complement receptor 2-conjugated inhibitors attenuates EAE. Neurosci Lett. 2012;531:35-39.
44. Elvington A, Atkinson C, Zhu H, et al. The alternative complement pathway propagates inflammation and injury in murine ischemic stroke. J Immunol. 2012;189:4640-4647.
45. Atkinson C, He S, Morris K, et al. Targeted complement inhibitors protect against posttransplant cardiac ischemia and reperfusion injury and reveal an important role for the alternative pathway of complement activation. J Immunol. 2010;185:7007-7013.
46. Rhoades W, Dickson D, Do DV. Potential role of lampalizumab for treatment of geographic atrophy. Clin Ophthalmol. 2015; 9:1049-1056.