Spatiotemporal cadence of macrophage polarisation in a model of light-induced retinal degeneration

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Jiao, Haihan ^a   Natoli, Riccardo ^a,b   Valter, Krisztina ^a,b   Provis, Jan M ^a,b   Rutar, Matt ^a  

^a Australian National University   (Australia)

^b The Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; CELL SURFACE RECEPTOR; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARG1 GENE; ARTICLE; CCL3 GENE; CD206 GENE; CELL ACTIVITY; CELL DEATH; CELL POLARITY; CLEC7A GENE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE LOCATION; IGF1 GENE; IL 12 GENE; IL 1BETA GENE; IL 6 GENE; LYVE1 GENE; MACROPHAGE; MACROPHAGE ACTIVATION; MICROGLIA; NONHUMAN; RAT; RETINA DEGENERATION; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; LIGHT; METABOLISM; PATHOLOGY; RADIATION RESPONSE; RETINA;

ANIMALS; CELL POLARITY; INTERLEUKIN-1BETA; LECTINS, C-TYPE; LIGHT; MACROPHAGES; MANNOSE-BINDING LECTINS; MODELS, BIOLOGICAL; RATS; RECEPTORS, CELL SURFACE; RETINA;

EID: 84955461990     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143952     Document Type: Article

References (51)

1. Kaneko H, Nishiguchi KM, Nakamura M, Kachi S, Terasaki H (2008) Characteristics of bone marrowderived microglia in the normal and injured retina. Invest Ophthalmol Vis Sci 49: 4162-4168. doi: 10. 1167/iovs.08-1738 PMID: 18487364
2. Ezzat MK, Hann CR, Vuk-Pavlovic S, Pulido JS (2008) Immune cells in the human choroid. Br J Ophthalmol 92: 976-980. doi: 10.1136/bjo.2007.129742 PMID: 18577650
3. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 76: 463-471. PMID: 12634111
4. Penfold PL, Killingsworth MC, Sarks SH (1986) Senile macular degeneration. The involvement of giant cells in atrophy of the retinal pigment epithelium. Invest Ophthalmol Vis Sci 27: 364-271. PMID: 3949464
5. Wong J, Madigan M, Billson F, Penfold P (2001) Quantification of leukocyte common antigen (CD45) expression in macular degeneration. Invest Ophthalmol Vis Sci 42: S227.
6. Cherepanoff S, McMenamin P, Gillies MC, Kettle E, Sarks SH (2009) Bruch's membrane and choroidal macrophages in early and advanced age-related macular degeneration. Br J Ophthalmol 94: 918-925. doi: 10.1136/bjo.2009.165563 PMID: 19965817
7. Lewis GP, Sethi CS, Carter KM, Charteris DG, Fisher SK (2005) Microglial cell activation following retinal detachment: a comparison between species. Mol Vis 11: 491-500. PMID: 16052164
8. Vrabec F (1975) Activated human retinal microglia under pathological conditions. Albrecht Von Graefes Arch Klin Exp Ophthalmol 196: 49-60. PMID: 1080638
9. Yuan L, Neufeld AH (2001) Activated microglia in the human glaucomatous optic nerve head. J Neurosci Res 64: 523-532. PMID: 11391707
10. Neufeld AH (1999) Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch Ophthalmol 117: 1050-1056. PMID: 10448748
11. Zeng HY, Green WR, Tso MO (2008) Microglial activation in human diabetic retinopathy. Arch Ophthalmol 126: 227-232. doi: 10.1001/archophthalmol.2007.65 PMID: 18268214
12. Kataoka K, Nishiguchi KM, Kaneko H, van Rooijen N, Kachi S, Terasaki H (2010) The roles of vitreal macrophages and circulating leukocytes in retinal neovascularization. Invest Ophthalmol Vis Sci.
13. Hoppeler T, Hendrickson P, Dietrich C, Reme C (1988) Morphology and time-course of defined photochemical lesions in the rabbit retina. Curr Eye Res 7: 849-860. PMID: 3180834
14. Ni YQ, Xu GZ, Hu WZ, Shi L, Qin YW, Da CD (2008) Neuroprotective effects of naloxone against lightinduced photoreceptor degeneration through inhibiting retinal microglial activation. Invest Ophthalmol Vis Sci 49: 2589-2598. doi: 10.1167/iovs.07-1173 PMID: 18515588
15. Chang CJ, Cherng CH, Liou WS, Liao CL (2005) Minocycline partially inhibits caspase-3 activation and photoreceptor degeneration after photic injury. Ophthalmic Res 37: 202-213. PMID: 15990464
16. Yang LP, Zhu XA, Tso MO (2007) A possible mechanism of microglia-photoreceptor crosstalk. Mol Vis 13: 2048-2057. PMID: 18079678
17. Cruz-Guilloty F, Saeed AM, Echegaray JJ, Duffort S, Ballmick A, Tan Y, et al. (2013) Infiltration of proinflammatory m1 macrophages into the outer retina precedes damage in a mouse model of age-related macular degeneration. Int J Inflam 2013: 503725. doi: 10.1155/2013/503725 PMID: 23533946
18. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, et al. (2007) Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci U S A 104: 2425-2430. PMID: 17284607
19. Ibrahim AS, El-Shishtawy MM, Pena A Jr, Liou GI (2010) Genistein attenuates retinal inflammation associated with diabetes by targeting of microglial activation. Mol Vis 16: 2033-2042. PMID: 21042558
20. Krady JK, Basu A, Allen CM, Xu Y, LaNoue KF, Gardner TW, et al. (2005) Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes 54: 1559-1565. PMID: 15855346
21. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, et al. (2008) Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 49: 1437-1446. doi: 10.1167/iovs.07-1337 PMID: 18385061
22. Neufeld AH (2004) Pharmacologic neuroprotection with an inhibitor of nitric oxide synthase for the treatment of glaucoma. Brain Res Bull 62: 455-459. PMID: 15036557
23. Karlstetter M, Scholz R, Rutar M, Wong WT, Provis JM, Langmann T (2014) Retinal microglia: Just bystander or target for therapy? Prog Retin Eye Res doi: 10.1016/j.preteyeres.2014.11.004
24. Cruz-Guilloty F, Saeed AM, Duffort S, Cano M, Ebrahimi KB, Ballmick A, et al. (2014) T cells and macrophages responding to oxidative damage cooperate in pathogenesis of a mouse model of age-related macular degeneration. PLoS One 9: e88201. doi: 10.1371/journal.pone.0088201 PMID: 24586307
25. Hu X, Leak RK, Shi Y, Suenaga J, Gao Y, Zheng P, et al. (2015) Microglial and macrophage polarization-new prospects for brain repair. Nat Rev Neurol 11: 56-64. doi: 10.1038/nrneurol.2014.207 PMID: 25385337
26. Rutar MV, Natoli RC, Provis JM (2012) Small interfering RNA-mediated suppression of Ccl2 in Muller cells attenuates microglial recruitment and photoreceptor death following retinal degeneration. J Neuroinflammation 9: 221. doi: 10.1186/1742-2094-9-221 PMID: 22992301
27. Rutar M, Natoli R, Valter K, Provis JM (2011) Analysis of complement expression in light-induced retinal degeneration: Synthesis and deposition of C3 by microglia/macrophages is associated with focal photoreceptor degeneration. Invest Ophthalmol Vis Sci 52 (8): 5347-5358. doi: 10.1167/iovs.10-7119 PMID: 21571681
28. Rutar M, Provis JM, Valter K (2010) Brief exposure to damaging light causes focal recruitment of macrophages, and long-term destabilization of photoreceptors in the albino rat retina. Curr Eye Res 35: 631-643. doi: 10.3109/02713681003682925 PMID: 20597649
29. Rutar M, Natoli R, Valter K, Provis JM (2011) Early focal expression of the chemokine Ccl2 by Muller cells during exposure to damage-inducing bright continuous light. Invest Ophthalmol Vis Sci 52: 2379-2388. doi: 10.1167/iovs.10-6010 PMID: 21228381
30. Ma W, Cojocaru R, Gotoh N, Gieser L, Villasmil R, Cogliati T, et al. (2013) Gene expression changes in aging retinal microglia: relationship to microglial support functions and regulation of activation. Neurobiol Aging 34: 2310-2321. doi: 10.1016/j.neurobiolaging.2013.03.022 PMID: 23608111
31. Chen L, Wu W, Dentchev T, Zeng Y, Wang J, Tsui I, et al. (2004) Light damage induced changes in mouse retinal gene expression. Exp Eye Res 79: 239-247. PMID: 15325571
32. Rohrer B, Guo Y, Kunchithapautham K, Gilkeson GS (2007) Eliminating complement factor D reduces photoreceptor susceptibility to light-induced damage. Invest Ophthalmol Vis Sci 48: 5282-5289. PMID: 17962484
33. Maslim J, Valter K, Egensperger R (1997) Tissue oxygen during a critical developmental period controls the death and survival of photoreceptors. Invest Ophthalmol Vis Sci 38: 1667-1677. PMID: 9286255
34. Cherry JD, Olschowka JA, O'Banion MK (2014) Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 11: 98. doi: 10.1186/1742-2094-11-98 PMID: 24889886
35. Levy O, Calippe B, Lavalette S, Hu SJ, Raoul W, Dominguez E, et al. (2015) Apolipoprotein E promotes subretinal mononuclear phagocyte survival and chronic inflammation in age-related macular degeneration. EMBO Mol Med 7: 211-226. doi: 10.15252/emmm.201404524 PMID: 25604058
36. Hu SJ, Calippe B, Lavalette S, Roubeix C, Montassar F, Housset M, et al. (2015) Upregulation of P2RX7 in Cx3cr1-Deficient Mononuclear Phagocytes Leads to Increased Interleukin-1beta Secretion and Photoreceptor Neurodegeneration. J Neurosci 35: 6987-6996. doi: 10.1523/JNEUROSCI.3955-14.2015 PMID: 25948251
37. London A, Itskovich E, Benhar I, Kalchenko V, Mack M, Jung S, et al. (2011) Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages. J Exp Med 208: 23-39. doi: 10.1084/jem.20101202 PMID: 21220455
38. Labonte AC, Tosello-Trampont AC, Hahn YS (2014) The role of macrophage polarization in infectious and inflammatory diseases. Mol Cells 37: 275-285. doi: 10.14348/molcells.2014.2374 PMID: 24625576
39. Levy O, Calippe B, Lavalette S, Hu SJ, Raoul W, Dominguez E, et al. (2015) Apolipoprotein E promotes subretinal mononuclear phagocyte survival and chronic inflammation in age-related macular degeneration. EMBO Molecular Medicine: e201404524.
40. Kohno H, Maeda T, Perusek L, Pearlman E, Maeda A (2014) CCL3 production by microglial cells modulates disease severity in murine models of retinal degeneration. J Immunol 192: 3816-3827. doi: 10. 4049/jimmunol.1301738 PMID: 24639355
41. Berger S, Savitz SI, Nijhawan S, Singh M, David J, Rosenbaum PS, et al. (2008) Deleterious role of TNF-alpha in retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci 49: 3605-3610. doi: 10. 1167/iovs.07-0817 PMID: 18660426
42. Patel C, Rojas M, Narayanan SP, Zhang W, Xu Z, Lemtalsi T, et al. (2013) Arginase as a mediator of diabetic retinopathy. Front Immunol 4: 173. doi: 10.3389/fimmu.2013.00173 PMID: 23840196
43. Apte RS, Richter J, Herndon J, Ferguson TA (2006) Macrophages inhibit neovascularization in a murine model of age-related macular degeneration. PLoS Med 3: e310. PMID: 16903779
44. Kelly J, Ali Khan A, Yin J, Ferguson TA, Apte RS (2007) Senescence regulates macrophage activation and angiogenic fate at sites of tissue injury in mice. J Clin Invest 117: 3421-3426. PMID: 17975672
45. Cao X, Shen D, Patel MM, Tuo J, Johnson TM, Olsen TW, et al. (2011) Macrophage polarization in the maculae of age-related macular degeneration: a pilot study. Pathol Int 61: 528-535. doi: 10.1111/j. 1440-1827.2011.02695.x PMID: 21884302
46. Joly S, Francke M, Ulbricht E, Beck S, Seeliger M, Hirrlinger P, et al. (2009) Cooperative phagocytes: resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am J Pathol 174: 2310-2323. doi: 10.2353/ajpath.2009.090023 PMID: 19435787
47. Chen M, Zhao J, Luo C, Pandi SP, Penalva RG, Fitzgerald DC, et al. (2012) Para-inflammation-mediated retinal recruitment of bone marrow-derived myeloid cells following whole-body irradiation is CCL2 dependent. Glia 60: 833-842. doi: 10.1002/glia.22315 PMID: 22362506
48. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, et al. (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117: 902-909. PMID: 17364026
49. Sennlaub F, Auvynet C, Calippe B, Lavalette S, Poupel L, Hu SJ, et al. (2013) CCR2(+) monocytes infiltrate atrophic lesions in age-related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice. EMBO Mol Med 5: 1775-1793. doi: 10.1002/ emmm.201302692 PMID: 24142887
50. Luhmann UF, Robbie S, Munro PM, Barker SE, Duran Y, Luong V, et al. (2009) The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci 50: 5934-5943. doi: 10.1167/iovs.09-3462 PMID: 19578022
51. London A, Benhar I, Mattapallil MJ, Mack M, Caspi RR, Schwartz M (2013) Functional macrophage heterogeneity in a mouse model of autoimmune central nervous system pathology. J Immunol 190: 3570-3578. doi: 10.4049/jimmunol.1202076 PMID: 23447691