The Monocyte Chemokine Receptor Cx3Cr1 Does Not Play a Significant Role in the Pathogenesis of Experimental Autoimmune Uveoretinitis

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 10, 2010, Pages 5121-5127

  Kezic, Jelena ^a   McMenamin, Paul G ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; EYE PROTEIN; INTERPHOTORECEPTOR RETINOID BINDING PROTEIN; INTERSTITIAL RETINOL-BINDING PROTEIN; RETINOL BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; IMMUNOHISTOCHEMISTRY; MICROGLIA; MONOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PHOTORECEPTOR; PRIORITY JOURNAL; UVEORETINITIS; ANIMAL; AUTOIMMUNE DISEASE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; CHIMERA; DISEASE MODEL; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY; RETINITIS; TRANSGENIC MOUSE; UVEITIS;

ANIMALS; AUTOIMMUNE DISEASES; CHIMERA; DISEASE MODELS, ANIMAL; EYE PROTEINS; FEMALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROSCOPY, CONFOCAL; MONOCYTES; RECEPTORS, CHEMOKINE; RETINITIS; RETINOL-BINDING PROTEINS; UVEITIS, POSTERIOR;

EID: 77958134581     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-5325     Document Type: Article

References (61)

1. Agarwal RK, Caspi RR. Rodent models of experimental autoimmune uveitis. In: Perl A, ed. Autoimmunity: Methods and Protocols. Totowa, NJ: Humana Press; 2004:395-415.
2. Caspi RR, Roberge FG, Chan CC, et al. A new model of autoimmune disease: experimental autoimmune uveoretinitis induced in mice with two different retinal antigens. J Immunol. 1988;140: 1490-1495.
3. Shao H, Liao T, Ke Y, Shi H, Kaplan HJ, Sun D. Severe chronic experimental autoimmune uveitis (EAU) of the C57BL/6 mouse induced by adoptive transfer of IRBP1-20-specific T cells. Exp Eye Res. 2006;82:323-331.
4. Mochizuki M, Kuwabara T, McAllister C, Nussenblatt RB, Gery I. Adoptive transfer of experimental autoimmune uveoretinitis in rats: immunopathogenic mechanisms and histologic features. Invest Ophthalmol Vis Sci. 1985;26:1-9.
5. Caspi RR, Roberge FG, McAllister CG, et al. T cell lines mediating experimental autoimmune uveoretinitis (EAU) in the rat. J Immunol. 1986;136:928-933.
6. Forrester JV, Huitinga I, Lumsden L, Dijkstra CD. Marrow-derived activated macrophages are required during the effector phase of experimental autoimmune uveoretinitis in rats. Curr Eye Res. 1998;17:426-437.
7. Robertson MJ, Erwig LP, Liversidge J, et al. Retinal microenvironment controls resident and infiltrating macrophage function during uveoretinitis. Invest Ophthalmol Vis Sci. 2002;43:2250-2257.
8. Chan CC, Caspi RR, Ni M, et al. Pathology of experimental autoimmune uveoretinitis in mice. J Autoimmun. 1990;3:247-255.
9. Butler TL, McMenamin PG. Resident and infiltrating immune cells in the uveal tract in the early and late stages of experimental autoimmune uveoretinitis. Invest Ophthalmol Vis Sci. 1996;37: 2195-2210.
10. Jiang HR, Lumsden L, Forrester JV. Macrophages and dendritic cells in IRBP-induced experimental autoimmune uveoretinitis in B10RIII mice. Invest Ophthalmol Vis Sci. 1999;40:3177-3185.
11. Rao NA, Kimoto T, Zamir E, et al. Pathogenic role of retinal microglia in experimental uveoretinitis. Invest Ophthalmol Vis Sci. 2003;44:22-31.
12. Yeh S, Faia LJ, Nussenblatt RB. Advances in the diagnosis and immunotherapy for ocular inflammatory disease. Semin Immunopathol. 2008;30(2):145-164.
13. Reichle ML. Complications of intravitreal steroid injections. Optometry. 2005;76:450-460.
14. Imrie FR, Dick AD. Biologics in the treatment of uveitis. Curr Opin Ophthalmol. 2007;18:481-486.
15. Lim L, Suhler EB, Smith JR. Biologic therapies for inflammatory eye disease. Clin Exp Ophthalmol. 2006;34:365-374.
16. Ando K, Fujino Y, Mochizuki M. Effects of monoclonal antibodies directed at cell surface molecules on murine experimental autoimmune uveoretinitis. Graefes Arch Clin Exp Ophthalmol. 1999; 237:848-854.
17. Crane IJ, McKillop-Smith S, Wallace CA, Lamont GR, Forrester JV. Expression of the chemokines MIP-1alpha, MCP-1, and RANTES in experimental autoimmune uveitis. Invest Ophthalmol Vis Sci. 2001;42:1547-1552.
18. Crane IJ, Xu H, Wallace C, et al. Involvement of CCR5 in the passage of Th1-type cells across the blood-retina barrier in experimental autoimmune uveitis. J Leukoc Biol. 2006;79:435-443.
19. Yoshimura T, Sonoda KH, Miyazaki Y, et al. Differential roles for IFN-gamma and IL-17 in experimental autoimmune uveoretinitis. Int Immunol. 2008;20:209-214.
20. Su SB, Grajewski RS, Luger D, et al. Altered chemokine profile associated with exacerbated autoimmune pathology under conditions of genetic interferon-gamma deficiency. Invest Ophthalmol Vis Sci. 2007;48:4616-4625.
21. Dagkalis A, Wallace C, Xu H, et al. Development of experimental autoimmune uveitis with efficient recruitment of monocytes is independent of CCR2. Invest Ophthalmol Vis Sci. 2009;50:4288-4294.
22. Bazan JF, Bacon KB, Hardiman G, et al. A new class of membranebound chemokine with a CX3C motif. Nature. 1997;385:640-644.
23. Papadopoulos EJ, Sassetti C, Saeki H, et al. Fractalkine, a CX3C chemokine, is expressed by dendritic cells and is up-regulated upon dendritic cell maturation. Eur J Immunol. 1999;29:2551-2559.
24. Imai T, Hieshima K, Haskell C, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell. 1997;91:521-530.
25. Umehara H, Imai T. Role of fractalkine in leukocyte adhesion and migration and in vascular injury. Drug News Perspect. 2001;14: 460-464.
26. Muehlhoefer A, Saubermann LJ, Gu X, et al. Fractalkine is an epithelial and endothelial cell-derived chemoattractant for intraepithelial lymphocytes in the small intestinal mucosa. J Immunol. 2000;164:3368-3376.
27. Niess JH, Brand S, Gu X, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005;307:254-258.
28. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19:71-82.
29. Kezic J, Xu H, Chinnery HR, Murphy CC, McMenamin PG. Retinal microglia and uveal tract dendritic cells and macrophages are not CX3CR1 dependent in their recruitment and distribution in the young mouse eye. Invest Ophthalmol Vis Sci. 2008;49:1599-1608.
30. Joly S, Francke M, Ulbricht E, et al. Cooperative phagocytes: resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am J Pathol. 2009;174:2310-2323.
31. Fang IM, Lin CP, Yang CM, Chen MS, Yang CH. Expression of CX3C chemokine, fractalkine, and its receptor CX3CR1 in experimental autoimmune anterior uveitis. Mol Vis. 2005;11:443-451.
32. Chan CC, Tuo T, Bojanowski CM, Csaky KG, Green WR. Detection of CX3CR1 single nucleotide polymorphism and expression on archived eyes with age-related macular degeneration. Histol Histopathol. 2005;20:857-863.
33. Tuo J, Smith C, Bojanowski CM, et al. The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration. FASEB J. 2004;18:1297-1299.
34. Wallace GR, Vaughan RW, Kondeatis E, et al. A CX3CR1 genotype associated with retinal vasculitis in patients in the United Kingdom. Invest Ophthalmol Vis Sci. 2006;47:2966-2970.
35. Huang D, Shi FD, Jung S, et al. The neuronal chemokine CX3CL1/ fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J. 2006;20:896-905.
36. Dick AD, Ford AL, Forrester JV, Sedgwick JD. Flow cytometric identification of a minority population of MHC class II positive cells in the normal rat retina distinct from CD45lowCD11b/ c+CD4low parenchymal microglia. Br J Ophthalmol. 1995;79: 834-840.
37. Zhang C, Lam TT, Tso MO. Heterogeneous populations of microglia/ macrophages in the retina and their activation after retinal ischemia and reperfusion injury. Exp Eye Res. 2005;81:700-709.
38. Xu H, Dawson R, Forrester JV, Liversidge J. Identification of novel dendritic cell populations in normal mouse retina. Invest Ophthalmol Vis Sci. 2007;48:1701-1710.
39. Provis JM, Diaz CM, Penfold PL. Microglia in human retina: a heterogeneous population with distinct ontogenies. Perspect Dev Neurobiol. 1996;3:213-222.
40. Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol. 2004;75:388-397.
41. Ulvestad E, Williams K, Bjerkvig R, Tiekotter K, Antel J, Matre R. Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigenpresenting cells. J Leukoc Biol. 1994;56:732-740.
42. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19:312-318.
43. Neumann H, Kotter MR, Franklin RJ. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain. 2009;132(pt 2):288-295.
44. Jung S, Aliberti J, Graemmel P, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol. 2000;20:4106-4114.
45. Kezic J, McMenamin PG. Differential turnover rates of monocytederived cells in varied ocular tissue microenvironments. J Leukoc Biol. 2008;84:721-729.
46. McMenamin PG. Optimal methods for preparation and immunostaining of iris, ciliary body, and choroidal whole mounts. Invest Ophthalmol Vis Sci. 2000;41:3043-3048.
47. Dick AD, Cheng YF, Liversidge J, Forrester JV. Immunomodulation of experimental autoimmune uveoretinitis: a model of tolerance induction with retinal antigens. Eye. 1994;8(pt 1):52-59.
48. Caspi RR, Silver PB, Luger D, et al. Mouse models of experimental autoimmune uveitis. Ophthalmic Res. 2008;40:169-174.
49. Silver PB, Chan CC, Wiggert B, Caspi RR. The requirement for pertussis to induce EAU is strain-dependent: B10.RIII, but not B10.A mice, develop EAU and Th1 responses to IRBP without pertussis treatment. Invest Ophthalmol Vis Sci. 1999;40:2898-2905
50. Crane IJ, Xu H, Manivannan A, et al. Effect of anti-macrophage inflammatory protein-1alpha on leukocyte trafficking and disease progression in experimental autoimmune uveoretinitis. Eur J Immunol. 2003;33:402-410.
51. Combadiere C, Feumi C, Raoul W, et al. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest. 2007; 117:2920-2928.
52. Kitaichi N, Kotake S, Morohashi T, Onoe K, Ohno S, Taylor AW. Diminution of experimental autoimmune uveoretinitis (EAU) in mice depleted of NK cells. J Leukoc Biol. 2002;72:1117-1121.
53. Dagkalis A, Wallace C, Hing B, Liversidge J, Crane IJ. CX3CR1- deficiency is associated with increased severity of disease in experimental autoimmune uveitis. Immunology. 2009;128:25-33.
54. Echigo T, Hasegawa M, Shimada Y, Takehara K, Sato S. Expression of fractalkine and its receptor, CX3CR1, in atopic dermatitis: possible contribution to skin inflammation. J Allergy Clin Immunol. 2004;113:940-948.
55. Nanki T, Urasaki Y, Imai T, et al. Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J Immunol. 2004;173: 7010-7016.
56. Suzuki F, Nanki T, Imai T, et al. Inhibition of CX3CL1 (fractalkine) improves experimental autoimmune myositis in SJL/J mice. J Immunol. 2005;175:6987-6996.
57. Sunnemark D, Eltayeb S, Wallstrom E, et al. Differential expression of the chemokine receptors CX3CR1 and CCR1 by microglia and macrophages in myelin-oligodendrocyte-glycoprotein-induced experimental autoimmune encephalomyelitis. Brain Pathol. 2003; 13:617-629.
58. Zhao L, Ma W, Fariss RN, Wong WT. Retinal vascular repair and neovascularization are not dependent on CX3CR1 signaling in a model of ischemic retinopathy. Exp Eye Res. 2009;88:1004-1013.
59. Liang KJ, Lee JE, Wang YD, et al. Dynamic behavior in retinal microglia is regulated by CX3CR1 signaling. Invest Ophthalmol Vis Sci. 2009;50:4444-4451.
60. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol. 2009;27:119-145.
61. Cardona AE, Sasse ME, Mizutani M, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci. 2006;9: 917-924.