Autoimmunity in retinal degeneration: Autoimmune retinopathy and age-related macular degeneration

Journal of Autoimmunity

Volumn 33, Issue 3-4, 2009, Pages 247-254

  Morohoshi, Kei ^a   Goodwin, Anne M ^b   Ohbayashi, Masaharu ^a   Ono, Santa Jeremy ^a  

^a EMORY EYE CENTER   (United States)

^b MASSACHUSETTS COLLEGE OF LIBERAL ARTS   (United States)

Author keywords

Age related macular degeneration; Antigen microarray; Autoantibody profile; Autoimmune retinopathy; Mouse models; Retinal degeneration

Indexed keywords

OCULAR ANTIINFLAMMATORY AGENT;

ANTERIOR EYE CHAMBER; ANTIBODY PRODUCTION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BLOOD RETINA BARRIER; EYE INFLAMMATION; HUMAN; IMMUNOLOGICAL TOLERANCE; MICROARRAY ANALYSIS; NONHUMAN; PATHOGENESIS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA DEGENERATION; RETINA MACULA AGE RELATED DEGENERATION; RETINOPATHY;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; BLOOD-RETINAL BARRIER; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE TOLERANCE; MACULAR DEGENERATION; PROTEIN ARRAY ANALYSIS; RETINA; RETINAL DISEASES;

EID: 71649108317     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2009.09.003     Document Type: Article

References (94)

1. Cunha-Vaz J.G. The blood-retinal barriers system: basic concepts and clinical evaluation. Exp Eye Res 78 (2004) 715-721
2. Caspi R.R. Ocular autoimmunity: the price of privilege?. Immunol Rev 213 (2006) 23-35
3. Niederkorn J.Y. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat Immunol 7 (2006) 354-359
4. Niederkorn J.Y. The induction of anterior chamber-associated immune deviation. Chem Immunol Allergy 92 (2007) 27-35
5. Zamiri P., Sugita S., and Streilein J.W. Immunosuppressive properties of the pigmented epithelial cells and the subretinal space. Chem Immunol Allergy 92 (2007) 86-93
6. Egwuagu C.E., Charukamnoetkanok P., and Gery I. Thymic expression of autoantigens correlates with resistance to autoimmune disease. J Immunol 159 (1997) 3109-3112
7. Rose N.R. Infection, mimics, and autoimmune disease. J Clin Invest 107 (2001) 943-944
8. Rose N.R. The adjuvant effect in infection and autoimmunity. Clin Rev Allergy Immunol 34 (2008) 279-282
9. Adamus G. Autoantibody targets and their cancer relationship in the pathogenicity of paraneoplastic retinopathy. Autoimmun Rev 8 (2009) 410-414
10. Adamus G., Machnicki M., and Seigel G.M. Apoptotic retinal cell death induced by antirecoverin autoantibodies of cancer-associated retinopathy. Invest Ophthalmol Vis Sci 38 (1997) 283-291
11. Shiraga S., and Adamus G. Mechanism of CAR syndrome: anti-recoverin antibodies are the inducers of retinal cell apoptotic death via the caspase 9- and caspase 3-dependent pathway. J Neuroimmunol 132 (2002) 72-82
12. Heckenlively J.R., and Ferreyra H.A. Autoimmune retinopathy: a review and summary. Semin Immunopathol 30 (2008) 127-134
13. Weleber R.G., Watzke R.C., Shults W.T., Trzupek K.M., Heckenlively J.R., Egan R.A., et al. Clinical and electrophysiologic characterization of paraneoplastic and autoimmune retinopathies associated with antienolase antibodies. Am J Ophthalmol 139 (2005) 780-794
14. Guy J., and Aptsiauri N. Treatment of paraneoplastic visual loss with intravenous immunoglobulin: report of 3 cases. Arch Ophthalmol 117 (1999) 471-477
15. Goldstein S.M., Syed N.A., Milam A.H., Maguire A.M., Lawton T.J., and Nichols C.W. Cancer-associated retinopathy. Arch Ophthalmol 117 (1999) 1641-1645
16. Caspi R.R., Sun B., Agarwal R.K., Silver P.B., Rizzo L.V., Chan C.C., et al. T cell mechanisms in experimental autoimmune uveoretinitis: susceptibility is a function of the cytokine response profile. Eye 11 Pt 2 (1997) 209-212
17. Becker M.D., Adamus G., Davey M.P., and Rosenbaum J.T. The role of T cells in autoimmune uveitis. Ocul Immunol Inflamm 8 (2000) 93-100
18. Sawyer R.A., Selhorst J.B., Zimmerman L.E., and Hoyt W.F. Blindness caused by photoreceptor degeneration as a remote effect of cancer. Am J Ophthalmol 81 (1976) 606-613
19. Berson E.L., and Lessell S. Paraneoplastic night blindness with malignant melanoma. Am J Ophthalmol 106 (1988) 307-311
20. Alexander K.R., Fishman G.A., Peachey N.S., Marchese A.L., and Tso M.O. 'On' response defect in paraneoplastic night blindness with cutaneous malignant melanoma. Invest Ophthalmol Vis Sci 33 (1992) 477-483
21. Adamus G., Ren G., and Weleber R.G. Autoantibodies against retinal proteins in paraneoplastic and autoimmune retinopathy. BMC Ophthalmol 4 (2004) 5
22. Heckenlively J.R., Fawzi A.A., Oversier J., Jordan B.L., and Aptsiauri N. Autoimmune retinopathy: patients with antirecoverin immunoreactivity and panretinal degeneration. Arch Ophthalmol 118 (2000) 1525-1533
23. Mantel I., Ramchand K.V., Holder G.E., Ohbayashi M., Morohoshi K., Patel N., et al. Macular and retinal dysfunction of unknown origin in adults with normal fundi: evidence for an autoimmune pathophysiology. Exp Mol Pathol 84 (2008) 90-101
24. Adamus G., Amundson D., Seigel G.M., and Machnicki M. Anti-enolase-α autoantibodies in cancer-associated retinopathy: epitope mapping and cytotoxicity on retinal cells. J Autoimmun 11 (1998) 671-677
25. Adamus G., and Chan C.C. Experimental autoimmune uveitides: multiple antigens, diverse diseases. Int Rev Immunol 21 (2002) 209-229
26. Adamus G., Aptsiauri N., Guy J., Heckenlively J., Flannery J., and Hargrave P.A. The occurrence of serum autoantibodies against enolase in cancer-associated retinopathy. Clin Immunol Immunopathol 78 (1996) 120-129
27. Resnikoff S., Pascolini D., Etya'ale D., Kocur I., Pararajasegaram R., Pokharel G.P., et al. Global data on visual impairment in the year 2002. Bull World Health Organ 82 (2004) 844-851
28. de Jong P.T. Age-related macular degeneration. N Engl J Med 355 (2006) 1474-1485
29. Hageman G.S., Luthert P.J., Chong N.H.V., Johnson L.V., Anderson D.H., and Mullins R.F. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and age-related macular degeneration. Prog Retin Eye Res 20 (2001) 705-732
30. Mullins R.F., Russell S.R., Anderson D.H., and Hageman G.S. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J 14 (2000) 835-846
31. Russell S.R., Mullins R.F., Schneider B.L., and Hageman G.S. Location, substructure, and composition of basal laminar drusen compared with drusen associated with aging and age-related macular degeneration. Am J Ophthalmol 129 (2000) 205-214
32. Hageman G.S., and Mullins R.F. Molecular composition of drusen as related to substructural phenotype. Mol Vis 5 (1999) 28
33. Johnson L.V., Ozaki S., Staples M.K., Erickson P.A., and Anderson D.H. A potential role for immune complex pathogenesis in drusen formation. Exp Eye Res 70 (2000) 441-449
34. Crabb J.W., Miyagi M., Gu X., Shadrach K., West K.A., Sakaguchi H., et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci U S A 99 (2002) 14682-14687
35. Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., 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 102 (2005) 7227-7232
36. Haines J.L., Hauser M.A., Schmidt S., Scott W.K., Olson L.M., Gallins P., et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 308 (2005) 419-421
37. Xing C., Sivakumaran T.A., Wang J.J., Rochtchina E., Joshi T., Smith W., et al. Complement factor H polymorphisms, renal phenotypes and age-related macular degeneration: the Blue Mountains Eye Study. Genes Immun 9 (2008) 231-239
38. Tuo J., Bojanowski C.M., and Chan C.C. Genetic factors of age-related macular degeneration. Prog Retin Eye Res 23 (2004) 229-249
39. Kalayoglu M.V., Galvan C., Mahdi O.S., Byrne G.I., and Mansour S. Serological association between Chlamydia pneumoniae infection and age-related macular degeneration. Arch Ophthalmol 121 (2003) 478-482
40. Miller D.M., Espinosa-Heidmann D.G., Legra J., Dubovy S.R., Suñer I.J., Sedmak D.D., et al. The association of prior cytomegalovirus infection with neovascular age-related macular degeneration. Am J Ophthalmol 138 (2004) 323-328
41. Kalayoglu M.V., Bula D., Arroyo J., Gragoudas E.S., D'Amico D., and Miller J.W. Identification of Chlamydia pneumoniae within human choroidal neovascular membranes secondary to age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 243 (2005) 1080-1090
42. Patel N., Ohbayashi M., Nugent A.K., Ramchand K., Toda M., Chau K.Y., et al. Circulating anti-retinal antibodies as immune markers in age-related macular degeneration. Immunology 115 (2005) 422-430
43. Penfold P.L., Provis J.M., Furby J.H., Gatenby P.A., and Billson F.A. Autoantibodies to retinal astrocytes associated with age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 228 (1990) 270-274
44. Gu X., Meer S.G., Miyagi M., Rayborn M.E., Hollyfield J.G., Crabb J.W., et al. Carboxyethylpyrrole protein adducts and autoantibodies, biomarkers for age-related macular degeneration. J Biol Chem 278 (2003) 42027-42035
45. Joachim S.C., Bruns K., Lackner K.J., Pfeiffer N., and Grus F.H. Analysis of IgG antibody patterns against retinal antigens and antibodies to α-crystallin, GFAP, and α-enolase in sera of patients with "wet" age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 245 (2007) 619-626
46. Umeda S., Suzuki M.T., Okamoto H., Ono F., Mizota A., Terao K., et al. 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 (2005) 1683-1685
47. Ebrahem Q., Renganathan K., Sears J., Vasanji A., Gu X., Lu L., et al. Carboxyethylpyrrole oxidative protein modifications stimulate neovascularization: implications for age-related macular degeneration. Proc Natl Acad Sci U S A 103 (2006) 13480-13484
48. Gu J., Pauer G.J., Yue X., Narendra U., Sturgill G.M., Bena J., et al. Assessing susceptibility to age-related macular degeneration with proteomic and genomic biomarkers. Mol Cell Proteomics 8 (2009) 1338-1349
49. Hollyfield J.G., Bonilha V.L., Rayborn M.E., Yang X., Shadrach K.G., Lu L., et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 14 (2008) 194-198
50. Haas P., Steindl K., Schmid-Kubista K.E., Aggermann T., Krugluger W., Hageman G.S., et al. Complement factor H gene polymorphisms and Chlamydia pneumoniae infection in age-related macular degeneration. Eye (2009)
51. Shen D., Tuo J., Patel M., Herzlich A.A., Ding X., Chew E.Y., et al. Chlamydia pneumoniae infection, complement factor H variants and age-related macular degeneration. Br J Ophthalmol 93 (2009) 405-408
52. Robman L., Mahdi O.S., Wang J.J., Burlutsky G., Mitchell P., Byrne G., et al. Exposure to Chlamydia pneumoniae infection and age-related macular degeneration: the Blue Mountains Eye Study. Invest Ophthalmol Vis Sci 48 (2007) 4007-4011
53. Guymer R., and Robman L. Chlamydia pneumoniae and age-related macular degeneration: a role in pathogenesis or merely a chance association?. Clin Exp Ophthalmol 35 (2007) 89-93
54. Rose N.R. Predictors of autoimmune disease: autoantibodies and beyond. Autoimmunity 41 (2008) 419-428
55. Wallimann T., Wegmann G., Moser H., Huber R., and Eppenberger H.M. High content of creatine kinase in chicken retina: compartmentalized localization of creatine kinase isoenzymes in photoreceptor cells. Proc Natl Acad Sci U S A 83 (1986) 3816-3819
56. Wegmann G., Huber R., Zanolla E., Eppenberger H.M., and Wallimann T. Differential expression and localization of brain-type and mitochondrial creatine kinase isoenzymes during development of the chicken retina: Mi-CK as a marker for differentiation of photoreceptor cells. Differentiation 46 (1991) 77-87
57. Okunuki Y., Usui Y., Kezuka T., Hattori T., Masuko K., Nakamura H., et al. Proteomic surveillance of retinal autoantigens in endogenous uveitis: implication of esterase D and brain-type creatine kinase as novel autoantigens. Mol Vis 14 (2008) 1094-1104
58. Ahn B.Y., Song E.S., Cho Y.J., Kwon O.W., Kim J.K., and Lee N.G. Identification of an anti-aldolase autoantibody as a diagnostic marker for diabetic retinopathy by immunoproteomic analysis. Proteomics 6 (2006) 1200-1209
59. Arawaka S., Daimon M., Sasaki H., Suzuki J.I., and Kato T. A novel autoantibody in paraneoplastic sensory-dominant neuropathy reacts with brain-type creatine kinase. Int J Mol Med 1 (1998) 597-600
60. Whitcup S.M., DeBarge L.R., Caspi R.R., Harning R., Nussenblatt R.B., and Chan C.C. Monoclonal antibodies against ICAM-1 (CD54) and LFA-1 (CD11a/CD18) inhibit experimental autoimmune uveitis. Clin Immunol Immunopathol 67 (1993) 143-150
61. Rao N.A., Atalla L., Linker-Israeli M., Chen F.Y., George F., Martin W.J., et al. Suppression of experimental uveitis in rats by anti-I-A antibodies. Invest Ophthalmol Vis Sci 30 (1989) 2348-2355
62. de Kozak Y., Mirshahi M., Boucheix C., and Faure J.P. Inhibition of S-antigen-induced experimental autoimmune uveoretinitis by active immunization against anti-idiotypic antibody to an S-antigen epitope. Reg Immunol 4 (1992) 168-174
63. Wittstock M., Benecke R., and Zettl U.K. Therapy with intravenous immunoglobulins: complications and side-effects. Eur Neurol 50 (2003) 172-175
64. Caspi R.R. Experimental autoimmune uveoretinitis in the rat and mouse. Curr Protoc Immunol (2003) [Chapter 15:Unit 15.6]
65. Ryan S.J. The development of an experimental model of subretinal neovascularization in disciform macular degeneration. Trans Am Ophthalmol Soc 77 (1979) 707-745
66. Miller H., Miller B., and Ryan S.J. The role of retinal pigment epithelium in the involution of subretinal neovascularization. Invest Ophthalmol Vis Sci 27 (1986) 1644-1652
67. Dobi E.T., Puliafito C.A., and Destro M. A new model of experimental choroidal neovascularization in the rat. Arch Ophthalmol 107 (1989) 264-269
68. Tobe T., Ortega S., Luna J.D., Ozaki H., Okamoto N., Derevjanik N.L., et al. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am J Pathol 153 (1998) 1641-1646
69. Bora P.S., Sohn J.H., Cruz J.M., Jha P., Nishihori H., Wang Y., et al. Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization. J Immunol 174 (2005) 491-497
70. Bora N.S., Kaliappan S., Jha P., Xu Q., Sohn J.H., Dhaulakhandi D.B., 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 177 (2006) 1872-1878
71. Ambati J., Anand A., Fernandez S., Sakurai E., Lynn B.C., Kuziel W.A., et al. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9 (2003) 1390-1397
72. Skeie J.M., and Mullins R.F. Macrophages in neovascular age-related macular degeneration: friends or foes?. Eye 23 (2009) 747-755
73. Jager M.J., and Klaver C.C. Macrophages feel their age in macular degeneration. J Clin Invest 117 (2007) 3182-3184
74. Imamura Y., Noda S., Hashizume K., Shinoda K., Yamaguchi M., Uchiyama S., et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc Natl Acad Sci U S A 103 (2006) 11282-11287
75. Tuo J., Bojanowski C.M., Zhou M., Shen D., Ross R.J., Rosenberg K.I., et al. Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Invest Ophthalmol Vis Sci 48 (2007) 3827-3836
76. Chan C.C., Ross R.J., Shen D., Ding X., Majumdar Z., Bojanowski C.M., et al. Ccl2/Cx3cr1-deficient mice: an animal model for age-related macular degeneration. Ophthalmic Res 40 (2008) 124-128
77. Whitcup S.M., Vistica B.P., Milam A.H., Nussenblatt R.B., and Gery I. Recoverin-associated retinopathy: a clinically and immunologically distinctive disease. Am J Ophthalmol 126 (1998) 230-237
78. Polans A.S., Burton M.D., Haley T.L., Crabb J.W., and Palczewski K. Recoverin, but not visinin, is an autoantigen in the human retina identified with a cancer-associated retinopathy. Invest Ophthalmol Vis Sci 34 (1993) 81-90
79. Thirkill C.E., Tait R.C., Tyler N.K., Roth A.M., and Keltner J.L. Intraperitoneal cultivation of small-cell carcinoma induces expression of the retinal cancer-associated retinopathy antigen. Arch Ophthalmol 111 (1993) 974-978
80. Heckenlively J.R., Jordan B.L., and Aptsiauri N. Association of antiretinal antibodies and cystoid macular edema in patients with retinitis pigmentosa. Am J Ophthalmol 127 (1999) 565-573
81. Kikuchi T., Arai J., Shibuki H., Kawashima H., and Yoshimura N. Tubby-like protein 1 as an autoantigen in cancer-associated retinopathy. J Neuroimmunol 103 (2000) 26-33
82. Ohguro H., Ogawa K., and Nakagawa T. Recoverin and Hsc 70 are found as autoantigens in patients with cancer-associated retinopathy. Invest Ophthalmol Vis Sci 40 (1999) 82-89
83. Bazhin A.V., Dalke C., Willner N., Abschutz O., Wildberger H.G., Philippov P.P., et al. Cancer-retina antigens as potential paraneoplastic antigens in melanoma-associated retinopathy. Int J Cancer 124 (2009) 140-149
84. Potter M.J., Adamus G., Szabo S.M., Lee R., Mohaseb K., and Behn D. Autoantibodies to transducin in a patient with melanoma-associated retinopathy. Am J Ophthalmol 134 (2002) 128-130
85. Njoku D.B., Li Z., Mellerson J.L., Sharma R., Talor M.V., Barat N., et al. IP-10 protects while MIP-2 promotes experimental anesthetic hapten - induced hepatitis. J Autoimmun 32 (2009) 52-59
86. Li H.S., Ligons D.L., and Rose N.R. Genetic complexity of autoimmune myocarditis. Autoimmun Rev 7 (2008) 168-173
87. Frisancho-Kiss S., Nyland J.F., Davis S.E., Barrett M.A., Gatewood S.J., Njoku D.B., et al. Cutting edge: T cell Ig mucin-3 reduces inflammatory heart disease by increasing CTLA-4 during innate immunity. J Immunol 176 (2006) 6411-6415
88. Silverstein A.M., and Rose N.R. On the implications of polyclonal B cell activation. Nat Immunol 4 (2003) 931-932 author reply 932
89. Neumann D.A., Lane J.R., LaFond-Walker A., Allen G.S., Wulff S.M., Herskowitz A., et al. Heart-specific autoantibodies can be eluted from the hearts of Coxsackievirus B3-infected mice. Clin Exp Immunol 86 (1991) 405-412
90. Mackay I.R., Leskovsek N.V., and Rose N.R. Cell damage and autoimmunity: a critical appraisal. J Autoimmun 30 (2008) 5-11
91. Shoenfeld Y., Selmi C., Zimlichman E., and Gershwin M.E. The autoimmunologist: geoepidemiology, a new center of gravity, and prime time for autoimmunity. J Autoimmun 31 (2008) 325-330
92. Whittingham S., Rowley M.J., and Gershwin M.E. A tribute to an outstanding immunologist - Ian Reay Mackay. J Autoimmun 31 (2008) 197-200
93. Gershwin M.E. Bone marrow transplantation, refractory autoimmunity and the contributions of Susumu Ikehara. J Autoimmun 30 (2008) 105-107
94. Blank M., and Gershwin M.E. Autoimmunity: from the mosaic to the kaleidoscope. J Autoimmun 30 (2008) 1-4