Differential modulation of retinal degeneration by Ccl2 and Cx3cr1 chemokine signalling

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Luhmann, Ulrich F O ^a   Lange, Clemens A ^a   Robbie, Scott ^a,b   Munro, Peter M G ^a   Cowing, Jill A ^a   Armer, Hannah E J ^a   Luong, Vy ^a   Carvalho, Livia S ^a   MacLaren, Robert E ^a,b,c   Fitzke, Frederick W ^a   Bainbridge, James W B ^a,b   Ali, Robin R ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CX3CR1; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; CHEMOKINE RECEPTOR; CRB1 PROTEIN, MOUSE; CX3CR1 PROTEIN, MOUSE; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; BACKCROSSING; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE LOCUS; GENE MUTATION; GENE SEGREGATION; GENOTYPE; HISTOPATHOLOGY; HOMOZYGOSITY; KNOCKOUT MOUSE; MALE; MICROGLIA; MOUSE; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PHENOTYPE; PHOTORECEPTOR; RETINA DEGENERATION; RETINA FLUORESCEIN ANGIOGRAPHY; RETINAL TELANGIECTASIA; SCANNING ELECTRON MICROSCOPY; SCANNING LASER OPHTHALMOSCOPY; SIGNAL TRANSDUCTION; SUBRETINAL NEOVASCULARIZATION; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MUTATION; PATHOLOGY; RETINA;

ANIMALS; CHEMOKINE CCL2; FEMALE; GENOTYPE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NERVE TISSUE PROTEINS; RECEPTORS, CHEMOKINE; RETINA; RETINAL DEGENERATION;

EID: 84860179093     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035551     Document Type: Article

References (63)

1. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, et al. (2000) Analysis of Fractalkine Receptor CX3CR1 Function by Targeted Deletion and Green Fluorescent Protein Reporter Gene Insertion. Mol Cell Biol 20: 4106-4114.
2. Auffray C, Sieweke MH, Geissmann F, (2009) Blood Monocytes: Development, Heterogeneity, and Relationship with Dendritic Cells. Annual Review of Immunology 27: 669-692.
3. Geissmann F, Jung S, Littman DR, (2003) Blood Monocytes Consist of Two Principal Subsets with Distinct Migratory Properties. Immunity 19: 71-82.
4. McMenamin PG, (1999) Dendritic cells and macrophages in the uveal tract of the normal mouse eye. Br J Ophthalmol 83: 598-604.
5. Gordon S, Taylor PR, (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964.
6. Kreutzberg GW, (1996) Microglia: a sensor for pathological events in the CNS. Trends in Neurosciences 19: 312-318.
7. Guillemin GJ, Brew BJ, (2004) Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 75: 388-397.
8. Hanisch UK, Kettenmann H, (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
9. Langmann T, (2007) Microglia activation in retinal degeneration. J Leukoc Biol 81: 1345-1351.
10. Nimmerjahn A, Kirchhoff F, Helmchen F, (2005) Resting Microglial Cells Are Highly Dynamic Surveillants of Brain Parenchyma in Vivo. Science 308: 1314-1318.
11. Lee JE, Liang KJ, Fariss RN, Wong WT, (2008) Ex Vivo Dynamic Imaging of Retinal Microglia Using Time-Lapse Confocal Microscopy. Invest Ophthalmol Vis Sci 49: 4169-4176.
12. Joly S, Francke M, Ulbricht E, Beck S, Seeliger M, et al. (2009) Cooperative Phagocytes: Resident Microglia and Bone Marrow Immigrants Remove Dead Photoreceptors in Retinal Lesions. Am J Pathol 174: 2310-2323.
13. Eter N, Engel DR, Meyer L, Helb HM, Roth F, et al. (2008) In Vivo Visualization of Dendritic Cells, Macrophages, and Microglial Cells Responding to Laser-Induced Damage in the Fundus of the Eye. Invest Ophthalmol Vis Sci 49: 3649-3658.
14. Hughes EH, Schlichtenbrede FC, Murphy CC, Sarra GM, Luthert PJ, et al. (2003) Generation of Activated Sialoadhesin-Positive Microglia during Retinal Degeneration. Invest Ophthalmol Vis Sci 44: 2229-2234.
15. Ng TF, Streilein JW, (2001) Light-Induced Migration of Retinal Microglia into the Subretinal Space. Invest Ophthalmol Vis Sci 42: 3301-3310.
16. Xu H, Chen M, Forrester JV, (2009) Para-inflammation in the ageing retina. Progress in Retinal and Eye Research 28: 348-368.
17. Xu H, Chen M, Manivannan A, Lois N, Forrester JV, (2007) Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 7: 58-68.
18. Robertson MJ, Erwig LP, Liversidge J, Forrester JV, Rees AJ, et al. (2002) Retinal Microenvironment Controls Resident and Infiltrating Macrophage Function during Uveoretinitis. Invest Ophthalmol Vis Sci 43: 2250-2257.
19. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology 25: 677-686.
20. Colton C, (2009) Heterogeneity of Microglial Activation in the Innate Immune Response in the Brain. Journal of Neuroimmune Pharmacology 4: 399-418.
21. Friedman D, O'Colmain B, Muñoz B, Tomany S, McCarty C, et al. (2004) Prevalence of Age-Related Macular Degeneration in the United States. Arch Ophthalmol 122: 564-572.
22. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, et al. (2004) Global data on visual impairment in the year 2002. Bull.World Health Organ 82: 844-851.
23. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr, et al. (1997) Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest 100: 2552-2561.
24. Randolph GJ, Furie MB, (1995) A soluble gradient of endogenous monocyte chemoattractant protein-1 promotes the transendothelial migration of monocytes in vitro. J Immunol 155: 3610-3618.
25. Dzenko KA, Song L, Ge S, Kuziel WA, Pachter JS, (2005) CCR2 expression by brain microvascular endothelial cells is critical for macrophage transendothelial migration in response to CCL2. Microvascular Research 70: 53-64.
26. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, et al. (2007) Monitoring of Blood Vessels and Tissues by a Population of Monocytes with Patrolling Behavior. Science 317: 666-670.
27. Marchesi F, Locatelli M, Solinas G, Erreni M, Allavena P, et al. (2010) Role of CX3CR1/CX3CL1 axis in primary and secondary involvement of the nervous system by cancer. Journal of Neuroimmunology 224: 39-44.
28. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, et al. (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924.
29. Combadiere C, Feumi C, Raoul W, Keller N, Rodero M, et al. (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest 117: 2920-2928.
30. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, et al. (2009) Regulation of Dynamic Behavior of Retinal Microglia by CX3CR1 Signaling. Invest Ophthalmol Vis Sci 50: 4444-4451.
31. Tuo J, Smith BC, Bojanowski CM, Meleth AD, Gery I, et al. (2004) The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration. FASEB J 18: 1297-1299.
32. Neale BM, Fagerness J, Reynolds R, Sobrin L, Parker M, et al. (2010) Genome-wide association study of advanced age-related macular degeneration identifies a role of the hepatic lipase gene (LIPC). PNAS 107: 7395-7400.
33. McKay GJ, Patterson CC, Chakravarthy U, Dasari S, Klaver CC, et al. (2011) Evidence of association of APOE with age-related macular degeneration- a pooled analysis of 15 studies. Hum Mutat 32: 1407-1416.
34. Zerbib J, Puche N, Richard F, Leveziel N, Cohen SY, et al. (2011) No association between the T280M polymorphism of the CX3CR1 gene and exudative AMD. Experimental Eye Research 93: 382-386.
35. Seidler S, Zimmermann H, Bartneck M, Trautwein C, Tacke F, (2010) Age-dependent alterations of monocyte subsets and monocyte-related chemokine pathways in healthy adults. BMC Immunology 11: 30.
36. Jonas JB, Tao Y, Neumaier M, Findeisen P, (2010) Monocyte Chemoattractant Protein 1, Intercellular Adhesion Molecule 1, and Vascular Cell Adhesion Molecule 1 in Exudative Age-Related Macular Degeneration. Arch Ophthalmol 128: 1281-1286.
37. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, et al. (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9: 1390-1397.
38. Chen M, Forrester JV, Xu H, (2011) Dysregulation in Retinal Para-Inflammation and Age-Related Retinal Degeneration in CCL2 or CCR2 Deficient Mice. PLoS ONE 6: e22818.
39. Raoul W, Feumi C, Keller N, Lavalette S, Houssier M, et al. (2008) Lipid-bloated subretinal microglial cells are at the origin of drusen appearance in CX3CR1-deficient mice. Ophthalmic Res 40: 115-119.
40. Luhmann UFO, Robbie S, Munro PM, Barker SE, Duran Y, et al. (2009) The drusen-like phenotype in aging Ccl2 knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci 50: 5934-5943.
41. Tuo J, Bojanowski CM, Zhou M, Shen D, Ross RJ, et al. (2007) Murine Ccl2/Cx3cr1 Deficiency Results in Retinal Lesions Mimicking Human Age-Related Macular Degeneration. Invest Ophthalmol Vis Sci 48: 3827-3836.
42. Tuo J, Ross RJ, Herzlich AA, Shen D, Ding X, et al. (2009) A High Omega-3 Fatty Acid Diet Reduces Retinal Lesions in a Murine Model of Macular Degeneration. Am J Pathol 175: 799-807.
43. Tuo J, Pang Jj, Cao X, Shen D, Zhang J, et al. (2012) AAV5-mediated sFLT01 gene therapy arrests retinal lesions in Ccl2-/-/Cx3cr1-/- mice. Neurobiology of Aging 33: 433.e1-433.e10.
44. Combadiere C, Potteaux S, Gao JL, Esposito B, Casanova S, et al. (2003) Decreased Atherosclerotic Lesion Formation in CX3CR1/Apolipoprotein E Double Knockout Mice. Circulation 107: 1009-1016.
45. Hollyfield JG, Bonilha VL, Rayborn ME, Yang X, Shadrach KG, et al. (2008) Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 14: 194-198.
46. West JB, Fu Z, Deerinck TJ, Mackey MR, Obayashi JT, et al. (2010) Structure-function studies of blood and air capillaries in chicken lung using 3D electron microscopy. Respiratory Physiology & Neurobiology 170: 202-209.
47. Chan CC, Ross RJ, Shen D, Ding X, Majumdar Z, et al. (2008) Ccl2/Cx3cr1-deficient mice: an animal model for age-related macular degeneration. Ophthalmic Res 40: 124-128.
48. Shu X, Luhmann UF, Aleman TS, Barker SE, Lennon A, et al. (2011) Characterisation of a C1qtnf5 Ser163Arg Knock-In Mouse Model of Late-Onset Retinal Macular Degeneration. PLoS ONE 6: e27433.
49. Tsutsumi C, Sonoda KH, Egashira K, Qiao H, Hisatomi T, et al. (2003) The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol 74: 25-32.
50. Zhou Y, Sheets KG, Knott EJ, Regan J, Tuo J, et al. (2011) Cellular and 3D optical coherence tomography assessment during the initiation and progression of retinal degeneration in the Ccl2/Cx3cr1-deficient mouse. Experimental Eye Research 93: 636-648.
51. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM, et al. (2003) CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet 12: 2179-2189.
52. van de Pavert SA, Kantardzhieva A, Malysheva A, Meuleman J, Versteeg I, et al. (2004) Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. Journal of Cell Science 117: 4169-4177.
53. van de Pavert SA, Sanz AS, Aartsen WM, Vos RM, Versteeg I, et al. (2007) Crb1 is a determinant of retinal apical Müller glia cell features. Glia 55: 1486-1497.
54. Henderson RH, Mackay DS, Li Z, Moradi P, Sergouniotis P, et al. (2011) Phenotypic variability in patients with retinal dystrophies due to mutations in CRB1. Br J Ophthalmol 95: 811-817.
55. Jaissle G, May C, van de Pavert S, Wenzel A, Claes-May E, et al. (2010) Bone spicule pigment formation in retinitis pigmentosa: insights from a mouse model. Graefe's Archive for Clinical and Experimental Ophthalmology 248: 1063-1070.
56. Silverman MD, Zamora DO, Pan Y, Texeira PV, Baek SH, et al. (2003) Constitutive and Inflammatory Mediator-Regulated Fractalkine Expression in Human Ocular Tissues and Cultured Cells. Investigative Ophthalmology & Visual Science 44: 1608-1615.
57. Rutar M, Natoli R, Valter K, Provis JM, (2011) Early Focal Expression of the Chemokine Ccl2 by Müller Cells during Exposure to Damage-Inducing Bright Continuous Light. Investigative Ophthalmology & Visual Science 52: 2379-2388.
58. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, et al. (2007) From the Cover: Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. PNAS 104: 2425-2430.
59. Cook DN, Chen SC, Sullivan LM, Manfra DJ, Wiekowski MT, et al. (2001) Generation and Analysis of Mice Lacking the Chemokine Fractalkine. Mol Cell Biol 21: 3159-3165.
60. Blomster LV, Vukovic J, Hendrickx DAE, Jung S, Harvey AR, et al. (2011) CX3CR1 deficiency exacerbates neuronal loss and impairs early regenerative responses in the target-ablated olfactory epithelium. Molecular and Cellular Neuroscience 48: 236-245.
61. Ross RJ, Zhou M, Shen D, Fariss RN, Ding X, et al. (2008) Immunological protein expression profile in Ccl2/Cx3cr1 deficient mice with lesions similar to age-related macular degeneration. Experimental Eye Research 86: 675-683.
62. Boring L, Gosling J, Cleary M, Charo IF, (1998) Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394: 894-897.
63. Lange CAK, Stavrakas P, Luhmann UFO, de Silva DJ, Ali RR, et al. (2011) Intraocular Oxygen Distribution in Advanced Proliferative Diabetic Retinopathy. American Journal of Ophthalmology 152: 406-412.