Retinal Microglia and Uveal Tract Dendritic Cells and Macrophages Are Not CX3CR1 Dependent in Their Recruitment and Distribution in the Young Mouse Eye

Investigative Ophthalmology and Visual Science

Volumn 49, Issue 4, 2008, Pages 1599-1608

  Kezic, Jelena ^a   Xu, Heping ^b   Chinnery, Holly R ^a   Murphy, Connor C ^c   McMenamin, Paul G ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c ROYAL PERTH HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; ENHANCED GREEN FLUORESCENT PROTEIN; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL SHAPE; CELLULAR DISTRIBUTION; CILIARY BODY; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; IMMUNOPHENOTYPING; IRIS; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA DEGENERATION; UVEA; UVEITIS; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL COUNT; CELL MOTION; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; CELL COUNT; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; IMMUNOPHENOTYPING; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROSCOPY, CONFOCAL; RECEPTORS, CHEMOKINE; RETINA; UVEA;

EID: 45549085855     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.07-0953     Document Type: Article

References (69)

1. Novak N, Siepmann K, Zierhut M, Bieber T. The good, the bad and the ugly: APCs of the eye. Trends Immunol. 2003;24 (11):570- 574.
2. Forrester JV, McMenamin PG. Immunopathogenic mechanisms in intraocular inflammation. Chem Immunol. 1999;73:159-185.
3. + cells in the murine iris. Invest Ophthalmol Vis Sci. 1991;32 (8):2423-2431.
4. McMenamin PG, Holthouse I, Holt PG. Class II major histocompat- ibility complex (Ia) antigen-bearing dendritic cells within the iris and ciliary body of the rat eye: distribution, phenotype and relation to retinal microglia. Immunology. 1992;77 (3):385-393.
5. McMenamin PG, Crewe J, Morrison S, Holt PG. Immunomorpho-logic studies of macrophages and MHC class II-positive dendritic cells in the iris and ciliary body of the rat, mouse, and human eye. Invest Ophthalmol Vis Sci. 1994;35 (8):3234-3250.
6. Forrester JV, McMenamin PG, Liversidge J, Lumsden L. Dendritic cells and "dendritic" macrophages in the uveal tract. Adv Exp Med Biol. 1993;329:599-604.
7. McMenamin PG. The distribution ofimmune cells in the uveal tract of the normal eye. Eye. 1997;11 (Pt 2):183-193.
8. Hume DA, Perry VH, Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol. 1983;97 (1):253-257.
9. Provis JM, Diaz CM, Penfold PL. Microglia in human retina: a heterogeneous population with distinct ontogenies. Perspect Dev Neurobiol. 1996;3(3):213-222.
10. 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 (11):2195-2210.
11. 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 (4):426-437.
12. 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 (13):3177-3185.
13. Robertson MJ, Erwig LP, Liversidge J, et al. Retinal microenviron- ment controls resident and infiltrating macrophage function during uveoretinitis. Invest Ophthalmol Vis Sci. 2002;43 (7):2250-2257.
14. Caicedo A, Espinosa-Heidmann DG, Pina Y, et al. Blood-derived macrophages infiltrate the retina and activate Muller glial cells under experimental choroidal neovascularization. Exp Eye Res. 2005;81(1):38-47.
15. Sonoda KH, Sasa Y, Qiao H, et al. Immunoregulatory role of ocular macrophages: the macrophages produce RANTES to suppress experimental autoimmune uveitis. J Immunol. 2003;171(5):2652-2659.
16. Chang JH, McCluskey PJ, Wakefield D. Toll-like receptors in ocular immunity and the immunopathogenesis of inflammatory eye disease. Br J Ophthalmol. 2006;90 (1):103-108.
17. Edwards AO, Ritter R 3rd, Abel KJ, et al. Complement factor H polymorphism and age-related macular degeneration. Science. 2005;308 (5720):421-424.
18. Hageman GS, Anderson DH, Johnson LV, et al. A common haplo-type in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci USA. 2005;102(20):7227-7232.
19. Haines JL, Hauser MA, Schmidt S, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308 (5720):419-421.
20. Kijlstra A, La Heij E, Hendrikse F. Immunological factors in the pathogenesis and treatment of age-related macular degeneration. Ocul Immunol Inflamm. 2005;13(1):3-11.
21. Ambati J, Anand A, Fernandez S, et al. An animal model of age- related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med. 2003;9(11):1390-1397.
22. Forrester JV. Macrophages eyed in macular degeneration. Nat Med. 2003;9(11):1350-1351.
23. Tacke F, Alvarez D, Kaplan TJ, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest. 2007;117(1):185-194.
24. Stienstra R, Duval C, Miller M, Kersten S. PPARs, obesity, and inflammation. PPAR Res. 2006;2007:95974.
25. 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 (11):4106-4114.
26. Niess JH, Brand S, Gu X, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005;307 (5707):254-258.
27. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308(5726):1314-1318.
28. Soos TJ, Sims TN, Barisoni L, et al. CX3CR1 + interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int. 2006;70(3):591-596.
29. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19(1):71-82.
30. Bazan JF, Bacon KB, Hardiman G, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature. 1997;385(6617): 640 - 644.
31. 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(4):521-530.
32. 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(8):2551-2559.
33. Muehlhoefer A, Saubermann LJ, Gu X, et al. Fractalkine is an epithelial and endothelial cell- derived chemoattractant for intra- epithelial lymphocytes in the small intestinal mucosa. J Immunol. 2000;164(6):3368-3376.
34. Umehara H, Imai T. Role of fractalkine in leukocyte adhesion and migration and in vascular injury. Drug News Perspect. 2001;14(8):460 - 464.
35. Chinnery HR, Ruitenberg MJ, Plant GW, et al. The chemokine receptor CX3CR1 mediates homing of MHC class II-positive cells to the normal mouse corneal epithelium. Invest Ophthalmol Vis Sci. 2007;48(4):1568-1574.
36. McMenamin PG. Optimal methods for preparation and immuno- staining of iris, ciliary body, and choroidal wholemounts. Invest Ophthalmol Vis Sci. 2000;41(10):3043-3048.
37. McMenamin PG. Dendritic cells and macrophages in the uveal tract of the normal mouse eye. Br JOphthalmol. 1999;83(5):598-604.
38. Auffray C, Fogg D, Garfa M, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science. 2007;317(5838):666 - 670.
39. Diaz-Araya CM, Provis JM, Penfold PL, Billson FA. Development of microglial topography in human retina. J Comp Neurol. 1995;363(1):53-68.
40. Chen L, Yang P, Kijlstra A. Distribution, markers, and functions of retinal microglia. Ocul Immunol Inflamm. 2002;10(1):27-39.
41. 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 JOphthalmol. 1995;79(9):834 - 840.
42. Sedgwick JD, Schwender S, Imrich H, et al. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA. 1991;88(16):7438-7442.
43. Cardona AE, Pioro EP, Sasse ME, et al. Control of microglial neu- rotoxicity by the fractalkine receptor. Nat Neurosci. 2006;9(7):917-924.
44. Checchin D, Sennlaub F, Levavasseur E, et al. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci. 2006;47(8):3595-3602.
45. Ohta K, Yamagami S, Wiggert B, et al. Chemokine gene expression in iris-ciliary body during experimental autoimmune uveoretinitis. Curr Eye Res. 2002;24(6):451- 457.
46. 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(3):435- 443.
47. Lu B, Rutledge BJ, Gu L, et al. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med. 1998;187(4):601-608.
48. Kuziel WA, Morgan SJ, Dawson TC, et al. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc Natl Acad Sci USA. 1997; 94(22):12053-12058.
49. Nakazawa T, Hisatomi T, Nakazawa C, et al. Monocyte chemoat- tractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci USA. 2007;104(7):2425- 2430.
50. Qiao H, Hisatomi T, Sonoda KH, et al. The characterisation of hyalocytes: the origin, phenotype, and turnover. Br JOphthalmol. 2005;89(4):513-517.
51. Lazarus HS, Hageman GS. In situ characterization of the human hyalocyte. Arch Ophthalmol. 1994;112(10):1356-1362.
52. Penfold PL, Killingsworth MC, Sarks SH. Senile macular degeneration: the involvement of immunocompetent cells. Graefes Arch Clin Exp Ophthalmol. 1985;223(2):69 -76.
53. Killingsworth MC, Sarks JP, Sarks SH. Macrophages related to Bruch's membrane in age-related macular degeneration. Eye. 1990; 4(Pt 4):613-621.
54. Forrester JV, McMenamin PG, Holthouse I, et al. Localization and characterization of major histocompatibility complex class II-pos- itive cells in the posterior segment of the eye: implications for induction of autoimmune uveoretinitis. Invest Ophthalmol VisSci. 1994;35(1):64-77.
55. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol. 1995; 154(9):4309-4321.
56. Combadiere C, Feumi C, Raoul W, et al. CX3CR1-dependent sub- retinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest. 2007; 117(10):2920-2928.
57. Xu H, Chen M, Mayer EJ, et al. Turnover of resident retinal microglia in the normal adult mouse. Glia. 2007;55(11):1189-1198.
58. Xu H, Dawson R, Forrester JV, Liversidge J. Identification of novel dendritic cell populations in normal mouse retina. Invest Ophthalmol Vis Sci. 2007;48(4):1701-1710.
59. Echigo T, Hasegawa M, Shimada Y, et al. Expression of fractalkine and its receptor, CX3CR1, in atopic dermatitis: possible contribution to skin inflammation. J Allergy Clin Immunol. 2004;113(5):940 -948.
60. Nanki T, Urasaki Y, Imai T, et al. Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J Immunol. 2004;173(11): 7010-7016.
61. Suzuki F, Nanki T, Imai T, et al. Inhibition of CX3CL1 (fractalkine) improves experimental autoimmune myositis in SJL/J mice. J Immunol. 2005;175(10):6987-6996.
62. 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(4):617- 629.
63. Hulshof S, van Haastert ES, Kuipers HF, et al. CX3CL1 and CX3CR1 expression in human brain tissue: noninflammatory control versus multiple sclerosis. J Neuropathol Exp Neurol. 2003;62(9):899 -907.
64. Silverman MD, Zamora DO, Pan Y, et al. Constitutive and inflammatory mediator-regulated fractalkine expression in human ocular tissues and cultured cells. Invest Ophthalmol Vis Sci. 2003;44(4): 1608-1615.
65. 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(7):896-905.
66. Fang IM, Lin CP, Yang CM, et al. Expression of CX3C chemokine, fractalkine, and its receptor CX3CR1 in experimental autoimmune anterior uveitis. Mol Vis. 2005;11:443-451.
67. Tuo J, Smith BC, 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(11):1297-1299.
68. Chan CC, Tuo J, Bojanowski CM, et al. Detection ofCX3CR1 single nucleotide polymorphism and expression on archived eyes with age-related macular degeneration. Histol Histopathol. 2005;20(3): 857-863.
69. 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(7):2966-2970.