Intravitreal inhibition of complement C5a reduces choroidal neovascularization in mice

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 253, Issue 10, 2015, Pages 1695-1704

  Brockmann, Claudia ^a   Brockmann, Tobias ^a   Dege, Sabrina ^a   Busch, Catharina ^a   Kociok, Norbert ^a   Vater, Axel ^b   Klussmann, Sven ^b   Strauß, Olaf ^a   Joussen, Antonia M ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b NOXXON PHARMA AG   (Germany)

Author keywords

C5a inhibition; Complement component C5a; Complement system; Intravitreal injection; l aptamer; Laser induced neovascularization; Spiegelmer

Indexed keywords

APTAMER; COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A; FLUORESCEIN; GLUCOSE; NOX D 20; UNCLASSIFIED DRUG; COMPLEMENT C5A-INHIBITORS; NOX-D20; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOCOMPATIBILITY; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; FLUORESCENCE ANGIOGRAPHY; GLIA CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MOUSE; NONHUMAN; OPHTHALMOSCOPY; PRIORITY JOURNAL; SUBRETINAL NEOVASCULARIZATION; TUNEL ASSAY; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CAPILLARY PERMEABILITY; CHOROIDAL NEOVASCULARIZATION; DISEASE MODEL; DRUG EFFECTS; GIANT CELL; INTRAVITREAL DRUG ADMINISTRATION; LEUKOCYTE; METABOLISM; PATHOLOGY; VITREOUS BODY;

ANIMALS; APOPTOSIS; APTAMERS, NUCLEOTIDE; CAPILLARY PERMEABILITY; CHOROIDAL NEOVASCULARIZATION; COMPLEMENT C5A; DISEASE MODELS, ANIMAL; FLUORESCEIN ANGIOGRAPHY; GIANT CELLS; IMMUNOHISTOCHEMISTRY; INTRAVITREAL INJECTIONS; LEUKOCYTES; MICE; MICE, INBRED C57BL; SERINE ENDOPEPTIDASES; VITREOUS BODY;

EID: 84941993540     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-015-3041-z     Document Type: Article

References (55)

1. Pascolini D, Mariotti SP, Pokharel GP, Pararajasegaram R, Etya’ale D, Négrel AD, Resnikoff S (2004) 2002 global update of available data on visual impairment: a compilation of population-based prevalence studies. Ophthalmic Epidemiol 11:67–115
2. Smith W, Assink J, Klein R, Mitchell P, Klaver CC, Klein BE, Hofman A, Jensen S, Wang JJ, de Jong PT (2001) Risk factors for age-related macular degeneration: pooled findings from three continents. Ophthalmology 108:697–704
3. Rosenfeld P, Brown D, Heier J, Boyer D, Kaiser P, Chung C, Kim R (2006) Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355:1419–1431
4. Martin DF, Maguire MG, Ying GS, Grunwald JE, Fine SL, Jaffe GJ, Group CR (2011) Ranibizumab and bevacizumab for neovascular age-related macular degeneration. N Engl J Med 364:1897–1908. doi:10.1056/NEJMoa1102673
5. Browning DJ, Kaiser PK, Rosenfeld PJ, Stewart MW (2012) Aflibercept for age-related macular degeneration: a game-changer or quiet addition? Am J Ophthalmol 154:222–226. doi:10.1016/j.ajo.2012.04.020
6. Heier JS, Brown DM, Chong V, Korobelnik JF, Kaiser PK, Nguyen QD, Kirchhof B, Ho A, Ogura Y, Yancopoulos GD, Stahl N, Vitti R, Berliner AJ, Soo Y, Anderesi M, Groetzbach G, Sommerauer B, Sandbrink R, Simader C, Schmidt-Erfurth U, Groups VVS (2012) Intravitreal aflibercept (VEGF trap-eye) in wet age-related macular degeneration. Ophthalmology 119:2537–2548. doi:10.1016/j.ophtha.2012.09.006
7. Sivaprasad S, Chong NV (2006) The complement system and age-related macular degeneration. Eye (Lond) 20:867–872. doi:10.1038/sj.eye.6702176
8. Ricklin D, Hajishengallis G, Yang K, Lambris JD (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11:785–797. doi:10.1038/ni.1923
9. Reynolds R, Hartnett ME, Atkinson JP, Giclas PC, Rosner B, Seddon JM (2009) Plasma complement components and activation fragments: associations with age-related macular degeneration genotypes and phenotypes. Invest Ophthalmol Vis Sci 50:5818–5827. doi:10.1167/iovs.09-3928
10. Penfold PL, Liew SC, Madigan MC, Provis JM (1997) Modulation of major histocompatibility complex class II expression in retinas with age-related macular degeneration. Invest Ophthalmol Vis Sci 38:2125–2133
11. Umeda S, Suzuki MT, Okamoto H, Ono F, Mizota A, Terao K, Yoshikawa Y, Tanaka Y, Iwata T (2005) Molecular composition of drusen and possible involvement of anti-retinal autoimmunity in two different forms of macular degeneration in cynomolgus monkey (macaca fascicularis). FASEB J 19:1683–1685. doi:10.1096/fj.04-3525fje
12. Köhl J (2001) Anaphylatoxins and infectious and non-infectious inflammatory diseases. Mol Immunol 38:175–187
13. Björk J, Hugli TE, Smedegård G (1985) Microvascular effects of anaphylatoxins C3a and C5a. J Immunol 134:1115–1119
14. Joussen AM, Poulaki V, Qin W, Kirchhof B, Mitsiades N, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP (2002) Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol 160:501–509. doi:10.1016/S0002-9440(10)64869-9
15. Cortright DN, Meade R, Waters SM, Chenard BL, Krause JE (2009) C5a, but not C3a, increases VEGF secretion in ARPE-19 human retinal pigment epithelial cells. Curr Eye Res 34:57–61. doi:10.1080/02713680802546658
16. Nozaki M, Raisler BJ, Sakurai E, Sarma JV, Barnum SR, Lambris JD, Chen Y, Zhang K, Ambati BK, Baffi JZ, Ambati J (2006) Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A 103:2328–2333. doi:10.1073/pnas.0408835103
17. Hoehlig K, Maasch C, Shushakova N, Buchner K, Huber-Lang M, Purschke WG, Vater A, Klussmann S (2013) A novel C5a-neutralizing mirror-image (l-)aptamer prevents organ failure and improves survival in experimental sepsis. Mol Ther 21(12):2236–2246. doi:10.1038/mt.2013.178
18. Klussmann S, Nolte A, Bald R, Erdmann VA, Fürste JP (1996) Mirror-image RNA that binds D-adenosine. Nat Biotechnol 14:1112–1115. doi:10.1038/nbt0996-1112
19. Vater A, Sahlmann J, Kröger N, Zöllner S, Lioznov M, Maasch C, Buchner K, Vossmeyer D, Schwoebel F, Purschke WG, Vonhoff S, Kruschinski A, Hübel K, Humphrey M, Klussmann S, Fliegert F (2013) Hematopoietic stem and progenitor cell mobilization in mice and humans by a first-in-class mirror-image oligonucleotide inhibitor of CXCL12. Clin Pharmacol Ther 94(1):150–157. doi:10.1038/clpt.2013.58
20. Semkova I, Peters S, Welsandt G, Janicki H, Jordan J, Schraermeyer U (2003) Investigation of laser-induced choroidal neovascularization in the rat. Invest Ophthalmol Vis Sci 44:5349–5354
21. Xia X, Wen R, Chou TH, Li Y, Wang Z, Porciatti V (2014) Protection of pattern electroretinogram and retinal ganglion cells by oncostatin m after optic nerve injury. PLoS One 9, e108524. doi:10.1371/journal.pone.0108524
22. Greenberg KP, Geller SF, Schaffer DV, Flannery JG (2007) Targeted transgene expression in muller glia of normal and diseased retinas using lentiviral vectors. Invest Ophthalmol Vis Sci 48:1844–1852. doi:10.1167/iovs.05-1570
23. Jasielska M, Semkova I, Shi X, Schmidt K, Karagiannis D, Kokkinou D, Mackiewicz J, Kociok N, Joussen AM (2010) Differential role of tumor necrosis factor (TNF)-alpha receptors in the development of choroidal neovascularization. Invest Ophthalmol Vis Sci 51:3874–3883. doi:10.1167/iovs.09-5003
24. Sheets KG, Zhou Y, Ertel MK, Knott EJ, Regan CE, Elison JR, Gordon WC, Gjorstrup P, Bazan NG (2010) Neuroprotectin D1 attenuates laser-induced choroidal neovascularization in mouse. Mol Vis 16:320–329
25. Müther PS, Semkova I, Schmidt K, Abari E, Kuebbeler M, Beyer M, Abken H, Meyer KL, Kociok N, Joussen AM (2010) Conditions of retinal glial and inflammatory cell activation after irradiation in a GFP-chimeric mouse model. Invest Ophthalmol Vis Sci 51:4831–4839. doi:10.1167/iovs.09-4923
26. Shi X, Semkova I, Müther PS, Dell S, Kociok N, Joussen AM (2006) Inhibition of TNF-alpha reduces laser-induced choroidal neovascularization. Exp Eye Res 83:1325–1334. doi:10.1016/j.exer.2006.07.007
27. Kociok N, Krohne TU, Poulaki V, Joussen AM (2007) Geldanamycin treatment reduces neovascularization in a mouse model of retinopathy of prematurity. Graefes Arch Clin Exp Ophthalmol 245:258–266. doi:10.1007/s00417-006-0355-x
28. Kociok N, Radetzky S, Krohne TU, Gavranic C, Liang Y, Semkova I, Joussen AM (2009) ICAM-1 depletion does not alter retinal vascular development in a model of oxygen-mediated neovascularization. Exp Eye Res 89:503–510. doi:10.1016/j.exer.2009.05.005
29. Michalewski J, Nawrocki J, Izdebski B, Michalewska Z (2014) Morphological changes in spectral domain optical coherence tomography guided bevacizumab injections in wet age-related macular degeneration, 12 months results. Indian J Ophthalmol 62:554–560. doi:10.4103/0301-4738.133485
30. Falkenstein IA, Cheng L, Wong-Staal F, Tammewar AM, Barron EC, Silva GA, Li QX, Yu D, Hysell M, Liu G, Ke N, Macdonald JE, Freeman WR (2008) Toxicity and intraocular properties of a novel long-acting anti-proliferative and anti-angiogenic compound IMS2186. Curr Eye Res 33:599–609. doi:10.1080/02713680802226582
31. Zhuang P, Shen Y, Lin BQ, Zhang WY, Chiou GC (2011) Effect of quercetin on formation of choroidal neovascularization (CNV) in age-related macular degeneration(AMD). Yan Ke Xue Bao 26:23–29. doi:10.3969/j.issn.1000-4432.2011.01.006
32. Semkova I, Fauser S, Lappas A, Smyth N, Kociok N, Kirchhof B, Paulsson M, Poulaki V, Joussen AM (2006) Overexpression of FasL in retinal pigment epithelial cells reduces choroidal neovascularization. FASEB J 20:1689–1691. doi:10.1096/fj.05-5653fje
33. Kemper C, Atkinson JP (2007) T-cell regulation: with complements from innate immunity. Nat Rev Immunol 7:9–18. doi:10.1038/nri1994
34. Rohrer B, Long Q, Coughlin B, Wilson RB, Huang Y, Qiao F, Tang PH, Kunchithapautham K, Gilkeson GS, Tomlinson S (2009) A targeted inhibitor of the alternative complement pathway reduces angiogenesis in a mouse model of age-related macular degeneration. Invest Ophthalmol Vis Sci 50:3056–3064. doi:10.1167/iovs.08-2222
35. Rohrer B, Coughlin B, Bandyopadhyay M, Holers VM (2012) Systemic human CR2-targeted complement alternative pathway inhibitor ameliorates mouse laser-induced choroidal neovascularization. J Ocul Pharmacol Ther 28:402–409. doi:10.1089/jop.2011.0212
36. Fukuoka Y, Strainic M, Medof ME (2003) Differential cytokine expression of human retinal pigment epithelial cells in response to stimulation by C5a. Clin Exp Immunol 131:248–253
37. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA, Rollins BJ, Ambati BK (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9:1390–1397. doi:10.1038/nm950
38. Anderson DH, Radeke MJ, Gallo NB, Chapin EA, Johnson PT, Curletti CR, Hancox LS, Hu J, Ebright JN, Malek G, Hauser MA, Rickman CB, Bok D, Hageman GS, Johnson LV (2010) The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis re-visited. Prog Retin Eye Res 29:95–112. doi:10.1016/j.preteyeres.2009.11.003
39. Bora PS, Sohn JH, Cruz JM, Jha P, Nishihori H, Wang Y, Kaliappan S, Kaplan HJ, Bora NS (2005) Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization. J Immunol 174:491–497
40. Yu M, Zou W, Peachey NS, McIntyre TM, Liu J (2012) A novel role of complement in retinal degeneration. Invest Ophthalmol Vis Sci 53:7684–7692. doi:10.1167/iovs.12-10069
41. Zarbin MA, Rosenfeld PJ (2010) Pathway-based therapies for age-related macular degeneration: an integrated survey of emerging treatment alternatives. Retina 30:1350–1367. doi:10.1097/IAE.0b013e3181f57e30
42. Khan MA, Maasch C, Vater A, Klussmann S, Morser J, Leung LL, Atkinson C, Tomlinson S, Heeger PS, Nicolls MR (2013) Targeting complement component 5a promotes vascular integrity and limits airway remodeling. Proc Natl Acad Sci U S A 110:6061–6066. doi:10.1073/pnas.1217991110
43. Remtulla S, Hallett PE (1985) A schematic eye for the mouse, and comparisons with the rat. Vis Res 25:21–31
44. Yu DY, Cringle SJ (2006) Oxygen distribution in the mouse retina. Invest Ophthalmol Vis Sci 47:1109–1112. doi:10.1167/iovs.05-1118
45. Tobe T, Ortega S, Luna JD, Ozaki H, Okamoto N, Derevjanik NL, Vinores SA, Basilico C, Campochiaro PA (1998) Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am J Pathol 153:1641–1646. doi:10.1016/S0002-9440(10)65753-7
46. Solovjov DA, Pluskota E, Plow EF (2005) Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem 280:1336–1345. doi:10.1074/jbc.M406968200
47. Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO (2004) Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci 45:2753–2759. doi:10.1167/iovs.03-1344
48. Morimura T, Neuchrist C, Kitz K, Budka H, Scheiner O, Kraft D, Lassmann H (1990) Monocyte subpopulations in human gliomas: expression of Fc and complement receptors and correlation with tumor proliferation. Acta Neuropathol 80:287–294
49. Graeber MB, Streit WJ, Kreutzberg GW (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J Neurosci Res 21:18–24. doi:10.1002/jnr.490210104
50. Arnaout MA (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75:1037–1050
51. Larson RS, Springer TA (1990) Structure and function of leukocyte integrins. Immunol Rev 114:181–217
52. Todd RF (1996) The continuing saga of complement receptor type 3 (CR3). J Clin Invest 98:1–2. doi:10.1172/JCI118752
53. Thurman JM, Kulik L, Orth H, Wong M, Renner B, Sargsyan SA, Mitchell LM, Hourcade DE, Hannan JP, Kovacs JM, Coughlin B, Woodell AS, Pickering MC, Rohrer B, Holers VM (2013) Detection of complement activation using monoclonal antibodies against C3d. J Clin Invest 123:2218–2230. doi:10.1172/JCI65861
54. Thurman JM, Rohrer B (2013) Noninvasive detection of complement activation through radiologic imaging. Adv Exp Med Biol 735:271–282
55. Framme C, Wolf S, Wolf-Schnurrbusch U (2010) Small dense particles in the retina observable by spectral-domain optical coherence tomography in age-related macular degeneration. Invest Ophthalmol Vis Sci 51:5965–5969. doi:10.1167/iovs.10-5779