CCL2/CCR2 and CX3CL1/CX3CR1 chemokine axes and their possible involvement in age-related macular degeneration

Journal of Neuroinflammation

Volumn 7, Issue , 2010, Pages

  Raoul, William ^a,b,c   Auvynet, Constance ^a,b,c,d   Camelo, Serge ^a,b,c   Guillonneau, Xavier ^a,b,c   Feumi, Charles ^a,b,c   Combadière, Christophe ^b,d,e   Sennlaub, Florian ^a,b,c,f  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSERM   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^f HÔTEL DIEU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, HUMAN;

GENE SILENCING; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PHOTORECEPTOR; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SUBRETINAL NEOVASCULARIZATION; ANIMAL; CYTOLOGY; DISEASE MODEL; GENETICS; IMMUNOLOGY; MOUSE; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA; RETINA MACULA DEGENERATION;

ANIMALS; CHEMOKINE CCL2; CHEMOKINE CX3CL1; DISEASE MODELS, ANIMAL; HUMANS; MACULAR DEGENERATION; MICE; MICE, KNOCKOUT; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CCR2; RECEPTORS, CHEMOKINE; RETINA; SIGNAL TRANSDUCTION;

EID: 78649539330     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-7-87     Document Type: Review

References (68)

1. Klein R, Peto T, Bird A, Vannewkirk MR. The epidemiology of age-related macular degeneration. Am J Ophthalmol 2004, 137:486-495. 10.1016/j.ajo.2003.11.069, 15013873.
2. Sarks SH. Ageing and degeneration in the macular region: a clinico-pathological study. Br J Ophthalmol 1976, 60:324-341. 10.1136/bjo.60.5.324, 1042725, 952802.
3. Bird AC, Bressler NM, Bressler SB, Chisholm IH, Coscas G, Davis MD, de Jong PT, Klaver CC, Klein BE, Klein R, et al. An international classification and grading system for age-related maculopathy and age-related macular degeneration. The International ARM Epidemiological Study Group. Surv Ophthalmol 1995, 39:367-374. 10.1016/S0039-6257(05)80092-X, 7604360.
4. Farkas TG, Sylvester V, Archer D. The ultrastructure of drusen. Am J Ophthalmol 1971, 71:1196-1205.
5. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, Mullins RF. 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 2001, 20:705-732. 10.1016/S1350-9462(01)00010-6, 11587915.
6. Klein R, Klein BE, Knudtson MD, Meuer SM, Swift M, Gangnon RE. Fifteen-year cumulative incidence of age-related macular degeneration: the Beaver Dam Eye Study. Ophthalmology 2007, 114:253-262. 10.1016/j.ophtha.2006.10.040, 17270675.
7. van Leeuwen R, Klaver CC, Vingerling JR, Hofman A, de Jong PT. The risk and natural course of age-related maculopathy: follow-up at 6 1/2 years in the Rotterdam study. Arch Ophthalmol 2003, 121:519-526. 10.1001/archopht.121.4.519, 12695249.
8. Ramkumar HL, Zhang J, Chan CC. Retinal ultrastructure of murine models of dry age-related macular degeneration (AMD). Prog Retin Eye Res 2010, 29:169-190. 10.1016/j.preteyeres.2010.02.002, 20206286.
9. van der Schaft TL, Mooy CM, de Bruijn WC, de Jong PT. Early stages of age-related macular degeneration: an immunofluorescence and electron microscopy study. Br J Ophthalmol 1993, 77:657-661. 10.1136/bjo.77.10.657, 504611, 8218037.
10. Mullins RF, Russell SR, Anderson DH, Hageman GS. 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 2000, 14:835-846.
11. Luibl V, Isas JM, Kayed R, Glabe CG, Langen R, Chen J. Drusen deposits associated with aging and age-related macular degeneration contain nonfibrillar amyloid oligomers. J Clin Invest 2006, 116:378-385. 10.1172/JCI25843, 1359048, 16453022.
12. Johnson LV, Leitner WP, Staples MK, Anderson DH. Complement activation and inflammatory processes in Drusen formation and age related macular degeneration. Exp Eye Res 2001, 73:887-896. 10.1006/exer.2001.1094, 11846519.
13. Edwards AO, Ritter R, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 2005, 308:421-424. 10.1126/science.1110189, 15761121.
14. Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 2005, 308:419-421. 10.1126/science.1110359, 15761120.
15. Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS, Haynes C, Henning AK, SanGiovanni JP, Mane SM, Mayne ST, et al. Complement factor H polymorphism in age-related macular degeneration. Science 2005, 308:385-389. 10.1126/science.1109557, 1512523, 15761122.
16. Ormsby RJ, Ranganathan S, Tong JC, Griggs KM, Dimasi DP, Hewitt AW, Burdon KP, Craig JE, Hoh J, Gordon DL. Functional and structural implications of the complement factor H Y402H polymorphism associated with age-related macular degeneration. Invest Ophthalmol Vis Sci 2008, 49:1763-1770. 10.1167/iovs.07-1297, 18263814.
17. Hakobyan S, Harris CL, van den Berg CW, Fernandez-Alonso MC, de Jorge EG, de Cordoba SR, Rivas G, Mangione P, Pepys MB, Morgan BP. Complement factor H binds to denatured rather than to native pentameric C-reactive protein. J Biol Chem 2008, 283:30451-30460. 10.1074/jbc.M803648200, 2662140, 18786923.
18. Xu H, Chen M, Forrester JV. Para-inflammation in the aging retina. Prog Retin Eye Res 2009, 28:348-368. 10.1016/j.preteyeres.2009.06.001, 19560552.
19. Combadiere C, Feumi C, Raoul W, Keller N, Rodero M, Pezard A, Lavalette S, Houssier M, Jonet L, Picard E, 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. 10.1172/JCI31692, 1994614, 17909628.
20. Penfold PL, Liew SC, Madigan MC, Provis JM. Modulation of major histocompatibility complex class II expression in retinas with age-related macular degeneration. Invest Ophthalmol Vis Sci 1997, 38:2125-2133.
21. Gupta N, Brown KE, Milam AH. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 2003, 76:463-471. 10.1016/S0014-4835(02)00332-9, 12634111.
22. Nozaki M, Raisler BJ, Sakurai E, Sarma JV, Barnum SR, Lambris JD, Chen Y, Zhang K, Ambati BK, Baffi JZ, Ambati J. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci USA 2006, 103:2328-2333. 10.1073/pnas.0408835103, 1413680, 16452172.
23. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, Matsubara A, Miyahara S, Nakao S, Yin Y, et al. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci USA 2007, 104:2425-2430. 10.1073/pnas.0608167104, 1892947, 17284607.
24. Espinosa-Heidmann DG, Suner IJ, Hernandez EP, Monroy D, Csaky KG, Cousins SW. Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 2003, 44:3586-3592. 10.1167/iovs.03-0038, 12882811.
25. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA, Rollins BJ, Ambati BK. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 2003, 9:1390-1397. 10.1038/nm950, 14566334.
26. Yi X, Ogata N, Komada M, Yamamoto C, Takahashi K, Omori K, Uyama M. Vascular endothelial growth factor expression in choroidal neovascularization in rats. Graefes Arch Clin Exp Ophthalmol 1997, 235:313-319. 10.1007/BF01739641, 9176680.
27. Ishibashi T, Hata Y, Yoshikawa H, Nakagawa K, Sueishi K, Inomata H. Expression of vascular endothelial growth factor in experimental choroidal neovascularization. Graefes Arch Clin Exp Ophthalmol 1997, 235:159-167. 10.1007/BF00941723, 9085111.
28. Luster AD. Chemokines--chemotactic cytokines that mediate inflammation. N Engl J Med 1998, 338:436-445. 10.1056/NEJM199802123380706, 9459648.
29. Combadiere C, Potteaux S, Rodero M, Simon T, Pezard A, Esposito B, Merval R, Proudfoot A, Tedgui A, Mallat Z. Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 2008, 117:1649-1657. 10.1161/CIRCULATIONAHA.107.745091, 18347211.
30. Combadiere C, Potteaux S, Gao JL, Esposito B, Casanova S, Lee EJ, Debre P, Tedgui A, Murphy PM, Mallat Z. Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation 2003, 107:1009-1016. 10.1161/01.CIR.0000057548.68243.42, 12600915.
31. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82. 10.1016/S1074-7613(03)00174-2, 12871640.
32. Bazan JF, Bacon KB, Hardiman G, Wang W, Soo K, Rossi D, Greaves DR, Zlotnik A, Schall TJ. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997, 385:640-644. 10.1038/385640a0, 9024663.
33. Ransohoff RM. Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity 2009, 31:711-721. 10.1016/j.immuni.2009.09.010, 2787682, 19836265.
34. Silverman MD, Zamora DO, Pan Y, Texeira PV, Baek SH, Planck SR, Rosenbaum JT. Constitutive and inflammatory mediator-regulated fractalkine expression in human ocular tissues and cultured cells. Invest Ophthalmol Vis Sci 2003, 44:1608-1615. 10.1167/iovs.02-0233, 12657599.
35. Checchin D, Sennlaub F, Levavasseur E, Leduc M, Chemtob S. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci 2006, 47:3595-3602. 10.1167/iovs.05-1522, 16877434.
36. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. 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. 10.1128/MCB.20.11.4106-4114.2000, 85780, 10805752.
37. Tuo J, Smith BC, Bojanowski CM, Meleth AD, Gery I, Csaky KG, Chew EY, Chan CC. The involvement of sequence variation and expression of CX3CR1 in the pathogenesis of age-related macular degeneration. Faseb J 2004, 18:1297-1299. 1971128, 15208270.
38. Chen H, Liu B, Lukas TJ, Neufeld AH. The aged retinal pigment epithelium/choroid: a potential substratum for the pathogenesis of age-related macular degeneration. PLoS One 2008, 3:e2339. 10.1371/journal.pone.0002339, 2394659, 18523633.
39. de Vos AF, Klaren VN, Kijlstra A. Expression of multiple cytokines and IL-1RA in the uvea and retina during endotoxin-induced uveitis in the rat. Invest Ophthalmol Vis Sci 1994, 35:3873-3883.
40. Yamada K, Sakurai E, Itaya M, Yamasaki S, Ogura Y. Inhibition of laser-induced choroidal neovascularization by atorvastatin by downregulation of monocyte chemotactic protein-1 synthesis in mice. Invest Ophthalmol Vis Sci 2007, 48:1839-1843. 10.1167/iovs.06-1085, 17389519.
41. Higgins GT, Wang JH, Dockery P, Cleary PE, Redmond HP. Induction of angiogenic cytokine expression in cultured RPE by ingestion of oxidized photoreceptor outer segments. Invest Ophthalmol Vis Sci 2003, 44:1775-1782. 10.1167/iovs.02-0742, 12657621.
42. Ma W, Zhao L, Fontainhas AM, Fariss RN, Wong WT. Microglia in the mouse retina alter the structure and function of retinal pigmented epithelial cells: a potential cellular interaction relevant to AMD. PLoS One 2009, 4:e7945. 10.1371/journal.pone.0007945, 2775955, 19936204.
43. Charo IF, Myers SJ, Herman A, Franci C, Connolly AJ, Coughlin SR. Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc Natl Acad Sci USA 1994, 91:2752-2756. 10.1073/pnas.91.7.2752, 43448, 8146186.
44. Tsutsumi C, Sonoda KH, Egashira K, Qiao H, Hisatomi T, Nakao S, Ishibashi M, Charo IF, Sakamoto T, Murata T, Ishibashi T. The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol 2003, 74:25-32. 10.1189/jlb.0902436, 12832439.
45. Luhmann UF, Robbie S, Munro PM, Barker SE, Duran Y, Luong V, Fitzke FW, Bainbridge JW, Ali RR, MacLaren RE. The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci 2009, 50:5934-5943. 10.1167/iovs.09-3462, 2801148, 19578022.
46. Eltayeb S, Berg AL, Lassmann H, Wallstrom E, Nilsson M, Olsson T, Ericsson-Dahlstrand A, Sunnemark D. Temporal expression and cellular origin of CC chemokine receptors CCR1, CCR2 and CCR5 in the central nervous system: insight into mechanisms of MOG-induced EAE. J Neuroinflammation 2007, 4:14. 10.1186/1742-2094-4-14, 1884136, 17484785.
47. Jonas JB, Tao Y, Neumaier M, Findeisen P. Monocyte chemoattractant protein 1, intercellular adhesion molecule 1, and vascular cell adhesion molecule 1 in exudative age-related macular degeneration. Arch Ophthalmol 2010, 128:1281-1286. 10.1001/archophthalmol.2010.227, 20937997.
48. Yang X, Hu J, Zhang J, Guan H. Polymorphisms in CFH, HTRA1 and CX3CR1 confer risk to exudative age-related macular degeneration in Han Chinese. Br J Ophthalmol
49. McDermott DH, Fong AM, Yang Q, Sechler JM, Cupples LA, Merrell MN, Wilson PW, D'Agostino RB, O'Donnell CJ, Patel DD, Murphy PM. Chemokine receptor mutant CX3CR1-M280 has impaired adhesive function and correlates with protection from cardiovascular disease in humans. J Clin Invest 2003, 111:1241-1250. 152935, 12697743.
50. Daoudi M, Lavergne E, Garin A, Tarantino N, Debre P, Pincet F, Combadiere C, Deterre P. Enhanced adhesive capacities of the naturally occurring Ile249-Met280 variant of the chemokine receptor CX3CR1. J Biol Chem 2004, 279:19649-19657. 10.1074/jbc.M313457200, 14990582.
51. Despriet DD, Bergen AA, Merriam JE, Zernant J, Barile GR, Smith RT, Barbazetto IA, van Soest S, Bakker A, de Jong PT, et al. Comprehensive analysis of the candidate genes CCL2, CCR2, and TLR4 in age-related macular degeneration. Invest Ophthalmol Vis Sci 2008, 49:364-371. 10.1167/iovs.07-0656, 2754756, 18172114.
52. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT. Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 2009, 50:4444-4451. 10.1167/iovs.08-3357, 2749316, 19443728.
53. Raoul W, Keller N, Rodero M, Behar-Cohen F, Sennlaub F, Combadiere C. Role of the chemokine receptor CX3CR1 in the mobilization of phagocytic retinal microglial cells. J Neuroimmunol 2008, 198:56-61. 10.1016/j.jneuroim.2008.04.014, 18508131.
54. Xu H, Chen M, Manivannan A, Lois N, Forrester JV. Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 2008, 7:58-68. 10.1111/j.1474-9726.2007.00351.x, 17988243.
55. Ng TF, Streilein JW. Light-induced migration of retinal microglia into the subretinal space. Invest Ophthalmol Vis Sci 2001, 42:3301-3310.
56. Raoul W, Feumi C, Keller N, Lavalette S, Houssier M, Behar-Cohen F, Combadiere C, Sennlaub F. Lipid-bloated subretinal microglial cells are at the origin of drusen appearance in CX3CR1-deficient mice. Ophthalmic Res 2008, 40:115-119. 10.1159/000119860, 2791110, 18421223.
57. Rudolf M, Malek G, Messinger JD, Clark ME, Wang L, Curcio CA. Sub-retinal drusenoid deposits in human retina: organization and composition. Exp Eye Res 2008, 87:402-408. 10.1016/j.exer.2008.07.010, 2613002, 18721807.
58. Zweifel SA, Imamura Y, Spaide TC, Fujiwara T, Spaide RF. Prevalence and Significance of Subretinal Drusenoid Deposits (Reticular Pseudodrusen) in Age-Related Macular Degeneration. Ophthalmology 2010,
59. Cohen SY, Dubois L, Tadayoni R, Delahaye-Mazza C, Debibie C, Quentel G. Prevalence of reticular pseudodrusen in age-related macular degeneration with newly diagnosed choroidal neovascularisation. Br J Ophthalmol 2007, 91:354-359. 10.1136/bjo.2006.101022, 1857688, 16973663.
60. Xu Q, Bernardo A, Walker D, Kanegawa T, Mahley RW, Huang Y. Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. J Neurosci 2006, 26:4985-4994. 10.1523/JNEUROSCI.5476-05.2006, 16687490.
61. Bellander BM, Bendel O, Von Euler G, Ohlsson M, Svensson M. Activation of microglial cells and complement following traumatic injury in rat entorhinal-hippocampal slice cultures. J Neurotrauma 2004, 21:605-615. 10.1089/089771504774129937, 15165368.
62. Matsubara T, Pararajasegaram G, Wu GS, Rao NA. Retinal microglia differentially express phenotypic markers of antigen-presenting cells in vitro. Invest Ophthalmol Vis Sci 1999, 40:3186-3193.
63. Joly S, Francke M, Ulbricht E, Beck S, Seeliger M, Hirrlinger P, Hirrlinger J, Lang KS, Zinkernagel M, Odermatt B, et al. Cooperative phagocytes: resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am J Pathol 2009, 174:2310-2323. 10.2353/ajpath.2009.090023, 2684195, 19435787.
64. Roque RS, Rosales AA, Jingjing L, Agarwal N, Al-Ubaidi MR. Retina-derived microglial cells induce photoreceptor cell death in vitro. Brain Res 1999, 836:110-119. 10.1016/S0006-8993(99)01625-X, 10415410.
65. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, et al. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 2006, 9:917-924. 10.1038/nn1715, 16732273.
66. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 2003, 44:3578-3585. 10.1167/iovs.03-0097, 12882810.
67. Tuo J, Bojanowski CM, Zhou M, Shen D, Ross RJ, Rosenberg KI, Cameron DJ, Yin C, Kowalak JA, Zhuang Z, et al. Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Invest Ophthalmol Vis Sci 2007, 48:3827-3836. 10.1167/iovs.07-0051, 2048751, 17652758.
68. Chan CC, Ross RJ, Shen D, Ding X, Majumdar Z, Bojanowski CM, Zhou M, Salem N, Bonner R, Tuo J. Ccl2/Cx3cr1-deficient mice: an animal model for age-related macular degeneration. Ophthalmic Res 2008, 40:124-128. 10.1159/000119862, 2409067, 18421225.