Retinal pigment epithelial cells upregulate expression of complement factors after co-culture with activated T cells

Experimental Eye Research

Volumn 92, Issue 3, 2011, Pages 180-188

  Juel, Helene B ^a   Kaestel, Charlotte ^a   Folkersen, Lasse ^b   Faber, Carsten ^a   Heegaard, Niels H H ^c   Borup, Rehannah ^d   Nissen, Mogens H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b KAROLINSKA INSTITUTE   (Sweden)

^c STATENS SERUM INSTITUT   (Denmark)

^d Mental Health Services CPH   (Denmark)

Author keywords

Age related macular degeneration; Complement; Retinal pigment epithelium; T cells; Uveitis

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CD28 ANTIGEN; CD3 ANTIGEN; CD59 ANTIGEN; CLUSTERIN; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H; DECAY ACCELERATING FACTOR; MEMBRANE COFACTOR PROTEIN;

ARTICLE; CELL CULTURE; GENE EXPRESSION; HUMAN; HUMAN CELL; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION;

ANTIGENS, CD28; ANTIGENS, CD3; ANTIGENS, CD46; ANTIGENS, CD59; CELL LINE; CLUSTERIN; COCULTURE TECHNIQUES; COMPLEMENT C3B INACTIVATOR PROTEINS; COMPLEMENT FACTOR H; COMPLEMENT SYSTEM PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOBLOTTING; LYMPHOCYTE ACTIVATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES; UP-REGULATION;

EID: 79952106968     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2011.01.003     Document Type: Article

References (50)

1. Alm A., Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp. Eye Res. 1973, 15:15-29.
2. An E., Gordish-Dressman H., Hathout Y. Effect of TNF-alpha on human ARPE-19-secreted proteins. Mol. Vis. 2008, 14:2292-2303.
3. An E., Lu X., Flippin J., Devaney J.M., Halligan B., Hoffman E., Csaky K., Hathout Y. Secreted proteome profiling in human rpe cell cultures derived from donors with age related macular degeneration and age matched healthy donors. J. Proteome. Res. 2007, 6:1615.
4. An F., Li Q., Tu Z., Bu H., Chan C.C., Caspi R.R., Lin F. Role of DAF in protecting against T-cell autoreactivity that leads to experimental autoimmune uveitis. Invest. Ophthalmol. Vis. Sci. 2009, 50:3778-3782.
5. Anderson D.H., Radeke M.J., Gallo N.B., Chapin E.A., Johnson P.T., Curletti C.R., Hancox L.S., Hu J., Ebright J.N., Malek G., Hauser M.A., Bowes R.C., Bok D., Hageman G.S., Johnson L.V. The pivotal role of the complement system in aging and age-related macular degeneration: hypothesis re-visited. Prog. Retin. Eye Res 2009.
6. Boekhoorn S.S., Vingerling J.R., Witteman J.C., Hofman A., de Jong P.T. C-reactive protein level and risk of aging macula disorder: the Rotterdam Study. Arch. Ophthalmol. 2007, 125:1396-1401.
7. Bora N.S., Jha P., Bora P.S. The role of complement in ocular pathology. Semin. Immunopathol. 2008, 30:85-95.
8. Chen H., Liu B., Lukas T.J., Neufeld A.H. The aged retinal pigment epithelium/choroid: a potential substratum for the pathogenesis of age-related macular degeneration. PLoS ONE 2008, 3:e2339.
9. Chen M., Forrester J.V., Xu H. Synthesis of complement factor H by retinal pigment epithelial cells is down-regulated by oxidized photoreceptor outer segments. Exp. Eye Res. 2007, 84:635-645.
10. Chen M., Muckersie E., Roberston M., Forrester J.V., Xu H. Up-regulation of complement factor B in retinal pigment epithelial cells is accompanied by complement activation in the aged retina. Exp. Eye Res. 2008, 87:543-550.
11. Coffey P.J., Gias C., McDermott C.J., Lundh P., Pickering M.C., Sethi C., Bird A., Fitzke F.W., Maass A., Chen L.L., Holder G.E., Luthert P.J., Salt T.E., Moss S.E., Greenwood J. Complement factor H deficiency in aged mice causes retinal abnormalities and visual dysfunction. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16651-16656.
12. Dasch B., Fuhs A., Behrens T., Meister A., Wellmann J., Fobker M., Pauleikhoff D., Hense H.W. Inflammatory markers in age-related maculopathy: cross-sectional analysis from the Muenster Aging and Retina Study. Arch. Ophthalmol. 2005, 123:1501-1506.
13. Ferrara D.C., Merriam J.E., Freund K.B., Spaide R.F., Takahashi B.S., Zhitomirsky I., Fine H.F., Yannuzzi L.A., Allikmets R. Analysis of major alleles associated with age-related macular degeneration in patients with multifocal choroiditis: strong association with complement factor H. Arch. Ophthalmol. 2008, 126:1562-1566.
14. Folkersen L., Diez D., Wheelock C.E., Haeggstrom J.Z., Goto S., Eriksson P., Gabrielsen A. GeneRegionScan: a Bioconductor package for probe level analysis of specific, small regions of the genome. Bioinformatics 2009, 25:1978-1979.
15. Futagami Y., Sugita S., Vega J., Ishida K., Takase H., Maruyama K., Aburatani H., Mochizuki M. Role of thrombospondin-1 in T cell response to ocular pigment epithelial cells. J. Immunol. 2007, 178:6994-7005.
16. Hecker L.A., Edwards A.O., Ryu E., Tosakulwong N., Baratz K.H., Brown W.L., Charbel I.P., Scholl H.P., Pollok-Kopp B., Schmid-Kubista K.E., Bailey K.R., Oppermann M. Genetic control of the alternative pathway of complement in humans and age-related macular degeneration. Hum. Mol. Genet. 2010, 19:209-215.
17. Holtkamp G.M., Kijlstra A., Peek R., de Vos A.F. Retinal pigment epithelium-immune system interactions: cytokine production and cytokine-induced changes. Prog. Retin. Eye Res. 2001, 20:29-48.
18. Ishida K., Panjwani N., Cao Z., Streilein J.W. Participation of pigment epithelium in ocular immune privilege. 3. Epithelia cultured from iris, ciliary body, and retina suppress T-cell activation by partially non-overlapping mechanisms. Ocul. Immunol. Inflamm. 2003, 11:91-105.
19. Jha P., Bora P.S., Bora N.S. The role of complement system in ocular diseases including uveitis and macular degeneration. Mol. Immunol. 2007, 44:3901-3908.
20. Kikuchi M., Nakamura M., Ishikawa K., Suzuki T., Nishihara H., Yamakoshi T., Nishio K., Taki K., Niwa T., Hamajima N., Terasaki H. Elevated C-reactive protein levels in patients with polypoidal choroidal vasculopathy and patients with neovascular age-related macular degeneration. Ophthalmology 2007, 114:1722-1727.
21. Klein R., Klein B.E., Knudtson M.D., Wong T.Y., Shankar A., Tsai M.Y. Systemic markers of inflammation, endothelial dysfunction, and age-related maculopathy. Am. J. Ophthalmol. 2005, 140:35-44.
22. Laine M., Jarva H., Seitsonen S., Haapasalo K., Lehtinen M.J., Lindeman N., Anderson D.H., Johnson P.T., Jarvela I., Jokiranta T.S., Hageman G.S., Immonen I., Meri S. Y402H polymorphism of complement factor H affects binding affinity to C-reactive protein. J. Immunol. 2007, 178:3831-3836.
23. Liversidge J., McKay D., Mullen G., Forrester J.V. Retinal pigment epithelial cells modulate lymphocyte function at the blood-retina barrier by autocrine PGE2 and membrane-bound mechanisms. Cell Immunol. 1993, 149:315-330.
24. Machalinska A., Dziedziejko V., Mozolewska-Piotrowska K., Karczewicz D., Wiszniewska B., Machalinski B. Elevated plasma levels of C3a complement compound in the exudative form of age-related macular degeneration. Ophthal. Res. 2009, 42:54-59.
25. Mahesh S.P., Li Z., Liu B., Fariss R.N., Nussenblatt R.B. Expression of GITR ligand abrogates immunosuppressive function of ocular tissue and differentially modulates inflammatory cytokines and chemokines. Eur. J. Immunol. 2006, 36:2128-2138.
26. McGwin G., Hall T.A., Xie A., Owsley C. The relation between C reactive protein and age related macular degeneration in the Cardiovascular Health Study. Br. J. Ophthalmol. 2005, 89:1166-1170.
27. Mitchell R., Chiang C.Y., Berry C., Bushman F. Global analysis of cellular transcription following infection with an HIV-based vector. Mol. Ther. 2003, 8:674-687.
28. Montalvo V., Campos M.M., Chan C.C., Wawrousek E.F., Bush R.A., Lambris J.D., Gery I. Complement deposits on ocular tissues adjacent to sites of inflammation. Curr. Eye Res. 2007, 32:917-922.
29. R Development Core Team R: A Language and Environment for Statistical Computing 2008, R Foundation for Statistical Computing.
30. Read R.W., Szalai A.J., Vogt S.D., McGwin G., Barnum S.R. Genetic deficiency of C3 as well as CNS-targeted expression of the complement inhibitor sCrry ameliorates experimental autoimmune uveoretinitis. Exp. Eye Res. 2006, 82:389-394.
31. Reynolds R., Hartnett M.E., Atkinson J.P., Giclas P.C., Rosner B., Seddon J.M. Plasma complement components and activation fragments are associated with age-related macular degeneration genotypes and phenotypes. Invest. Ophthalmol. Vis. Sci 2009.
32. Schaumberg D.A., Christen W.G., Buring J.E., Glynn R.J., Rifai N., Ridker P.M. High-sensitivity C-reactive protein, other markers of inflammation, and the incidence of macular degeneration in women. Arch. Ophthalmol. 2007, 125:300-305.
33. Scholl H.P., Charbel I.P., Walier M., Janzer S., Pollok-Kopp B., Borncke F., Fritsche L.G., Chong N.V., Fimmers R., Wienker T., Holz F.G., Weber B.H., Oppermann M. Systemic complement activation in age-related macular degeneration. PLoS ONE 2008, 3:e2593.
34. Seddon J.M., Gensler G., Milton R.C., Klein M.L., Rifai N. Association between C-reactive protein and age-related macular degeneration. JAMA 2004, 291:704-710.
35. Seddon J.M., George S., Rosner B., Rifai N. Progression of age-related macular degeneration: prospective assessment of C-reactive protein, interleukin 6, and other cardiovascular biomarkers. Arch. Ophthalmol. 2005, 123:774-782.
36. Serinsoz E., Bock O., Gwinner W., Schwarz A., Haller H., Kreipe H., Mengel M. Local complement C3 expression is upregulated in humoral and cellular rejection of renal allografts. Am. J. Transplant 2005, 5:1490-1494.
37. Seth A., Cui J., To E., Kwee M., Matsubara J. Complement-associated deposits in the human retina. Invest. Ophthalmol. Vis. Sci. 2008, 49:743-750.
38. Strainic M.G., Liu J., Huang D., An F., Lalli P.N., Muqim N., Shapiro V.S., Dubyak G.R., Heeger P.S., Medof M.E. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4 + T cells. Immunity 2008, 28:425-435.
39. Sugita S., Futagami Y., Smith S.B., Naggar H., Mochizuki M. Retinal and ciliary body pigment epithelium suppress activation of T lymphocytes via transforming growth factor beta. Exp. Eye Res. 2006, 83:1459-1471.
40. Sugita S., Usui Y., Horie S., Futagami Y., Aburatani H., Okazaki T., Honjo T., Takeuchi M., Mochizuki M. T cell suppression by programmed cell death 1 ligand 1 on retinal pigment epithelium during inflammatory conditions. Invest Ophthalmol. Vis. Sci 2009.
41. Tian J., Ishibashi K., Handa J.T. The expression of native and cultured RPE grown on different matrices. Physiol. Genom. 2004, 17:170-182.
42. Tian J., Ishibashi K., Honda S., Boylan S.A., Hjelmeland L.M., Handa J.T. The expression of native and cultured human retinal pigment epithelial cells grown in different culture conditions. Br. J. Ophthalmol. 2005, 89:1510-1517.
43. Usui Y., Okunuki Y., Hattori T., Kezuka T., Keino H., Ebihara N., Sugita S., Usui M., Goto H., Takeuchi M. Functional expression of B7H1 on retinal pigment epithelial cells. Exp. Eye Res. 2008, 86:52-59.
44. Vine A.K., Stader J., Branham K., Musch D.C., Swaroop A. Biomarkers of cardiovascular disease as risk factors for age-related macular degeneration. Ophthalmology 2005, 112:2076-2080.
45. Walport M.J. Complement. Second of two parts. N. Engl. J. Med. 2001, 344:1140-1144.
46. Wang J., Ohno-Matsui K., Yoshida T., Shimada N., Ichinose S., Sato T., Mochizuki M., Morita I. Amyloid-beta up-regulates complement factor B in retinal pigment epithelial cells through cytokines released from recruited macrophages/microglia: another mechanism of complement activation in age-related macular degeneration. J. Cell Physiol. 2009, 220:119-128.
47. Wu Z., Lauer T.W., Sick A., Hackett S.F., Campochiaro P.A. Oxidative stress modulates complement factor H expression in retinal pigmented epithelial cells by acetylation of FOXO3. J. Biol. Chem. 2007, 282:22414-22425.
48. Xu H., Chen M., Forrester J.V. Para-inflammation in the ageing retina. Prog. Retin. Eye Res. 2009, 28:348-368.
49. Yang P., Tyrrell J., Han I., Jaffe G.J. Expression and modulation of RPE cell membrane complement regulatory proteins (mCRPs). Invest. Ophthalmol. Vis. Sci. 2009, 50:3473-3481.
50. Zamiri P., Masli S., Kitaichi N., Taylor A.W., Streilein J.W. Thrombospondin plays a vital role in the immune privilege of the eye. Invest. Ophthalmol. Vis. Sci. 2005, 46:908-919.