The microglia in healthy and diseased retina

Experimental Eye Research

Volumn 136, Issue , 2015, Pages 116-130

  Li, Lu ^a   Eter, Nicole ^a   Heiduschka, Peter ^a  

^a INST OF REPRO MED OF THE UNIV   (Germany)

Author keywords

Microglia; Neuroprotection; Photoreceptors; Retinal degeneration; Retinal ganglion cells

Indexed keywords

CELL SURFACE MARKER; CELL SURFACE RECEPTOR; MINOCYCLINE; NALOXONE; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID;

AGING; CELL FUNCTION; GENETIC DISORDER; GLAUCOMA; HUMAN; INFLAMMATION; MESODERMAL CELL; MICROGLIA; MONOCYTE; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; OPTIC NERVE INJURY; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DISEASE; RETINA GANGLION CELL; REVIEW; YOLK SAC; HUMANS; PHYSIOLOGY; PHYSIOPATHOLOGY; RETINA; RETINAL DISEASES;

HUMANS; MICROGLIA; RETINA; RETINAL DISEASES;

EID: 84940101240     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.04.020     Document Type: Review

References (221)

1. Agudo M., Pérez-Marín M.C., Sobrado-Calvo P., Lönngren U., Salinas-Navarro M., Cánovas I., Nadal-Nicolás F.M., Miralles-Imperial J., Hallböök F., Vidal-Sanz M. Immediate upregulation of proteins belonging to different branches of the apoptotic cascade in the retina after optic nerve transection and optic nerve crush. Investig. Ophthalmol. Vis. Sci. 2009, 50:424-431.
2. Akiyama H., Kawamata T., Dedhar S., McGeer P.L. Immunohistochemical localization of vitronectin, its receptor and beta-3 integrin in Alzheimer brain tissue. J. Neuroimmunol. 1991, 32:19-28.
3. Alavi M.V., Bette S., Schimpf S., Schuettauf F., Schraermeyer U., Wehrl H.F., Ruttiger L., Beck S.C., Tonagel F., Pichler B.J., Knipper M., Peters T., Laufs J., Wissinger B. A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 2007, 130:1029-1042.
4. Alirezaei M., Kemball C.C., Whitton J.L. Autophagy, inflammation and neurodegenerative disease. Eur. J. Neurosci. 2011, 33:197-204.
5. Alliot F., Lecain E., Grima B., Pessac B. Microglial progenitors with a high proliferative potential in the embryonic and adult mouse brain. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:1541-1545.
6. Alliot F., Godin I., Pessac B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res. Dev. Brain Res. 1999, 117:145-152.
7. Ambati J., Anand A., Fernandez S., Sakurai E., Lynn B.C., Kuziel W.A., Rollins B.J., Ambati B.K. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat. Med. 2003, 9:1390-1397.
8. Arroba A.I., Alvarez-Lindo N., van Rooijen N., de la Rosa E.J. Microglia-mediated IGF-I neuroprotection in the rd10 mouse model of retinitis pigmentosa. Investig. Ophthalmol. Vis. Sci. 2011, 52:9124-9130.
9. Asheuer M., Pflumio F., Benhamida S., Dubart-Kupperschmitt A., Fouquet F., Imai Y., Aubourg P., Cartier N. Human CD34+ cells differentiate into microglia and express recombinant therapeutic protein. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3557-3562.
10. Ashwell K. The distribution of microglia and cell death in the fetal rat forebrain. Brain Res. Dev. Brain Res. 1991, 58:1-12.
11. Aslanidis A., Karlstetter M., Scholz R., Fauser S., Neumann H., Fried C., Pietsch M., Langmann T. Activated microglia/macrophage whey acidic protein (AMWAP) inhibits NFκB signaling and induces a neuroprotective phenotype in microglia. J. Neuroinflammation 2015, 12:77.
12. Auriault C., Joseph M., Tartar A., Capron A. Characterization and synthesis of a macrophage inhibitory peptide from the second constant domain of human immunoglobulin G. FEBS Lett. 1983, 153:11-15.
13. Banati R.B., Middleton R.J., Chan R., Hatty C.R., Kam W.W., Quin C., Graeber M.B., Parmar A., Zahre D., Callaghan P., Fok S., Howell N.R., Gregoire M., Szabo A., Pham T., Davis E., Liu G.J. Positron emission tomography and functional characterization of a complete PBR/TSPO knockout. Nat. Commun. 2014, 5:5452.
14. Baptiste D.C., Powell K.J., Jollimore C.A., Hamilton C., LeVatte T.L., Archibald M.L., Chauhan B.C., Robertson G.S., Kelly M.E. Effects of minocycline and tetracycline on retinal ganglion cell survival after axotomy. Neuroscience 2005, 134:575-582.
15. Bejarano-Escobar R., Blasco M., Martin-Partido G., Francisco-Morcillo J. Light-induced degeneration and microglial response in the retina of an epibenthonic pigmented teleost: age-dependent photoreceptor susceptibility to cell death. J. Exp. Biol. 2012, 215:3799-3812.
16. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 1994, 14:4368-4374.
17. Boscia F., Esposito C.L., Casamassa A., de Franciscis V., Annunziato L., Cerchia L. The isolectin IB4 binds RET receptor tyrosine kinase in microglia. J. Neurochem. 2013, 126:428-436.
18. Bosco A., Inman D.M., Steele M.R., Wu G., Soto I., Marsh-Armstrong N., Hubbard W.C., Calkins D.J., Horner P.J., Vetter M.L. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Investig. Ophthalmol. Vis. Sci. 2008, 49:1437-1446.
19. Bosco A., Steele M.R., Vetter M.L. Early microglia activation in a mouse model of chronic glaucoma. J. Comp. Neurol. 2011, 519:599-620.
20. Bourne M.C., Campbell D.A., Tansley K. Hereditary degeneration of the rat retina. Br. J. Ophthalmol. 1938, 22:613-623.
21. Boya J., Calvo J., Prado A. The origin of microglial cells. J. Anat. 1979, 129:177-186.
22. Boya J., Calvo J.L., Carbonell A.L., Borregon A. A lectin histochemistry study on the development of rat microglial cells. J. Anat. 1991, 175:229-236.
23. Brundula V., Rewcastle N.B., Metz L.M., Bernard C.C., Yong V.W. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 2002, 125:1297-1308.
24. Buschini E., Piras A., Nuzzi R., Vercelli A. Age related macular degeneration and drusen: neuroinflammation in the retina. Prog. Neurobiol. 2011, 95:14-25.
25. Cammermeyer J. The life history of the microglial cell: a light microscopic study. Neurosci. Res. (N Y) 1970, 3:43-129.
26. Cantoni C., Bollman B., Licastro D., Xie M., Mikesell R., Schmidt R., Yuede C.M., Galimberti D., Olivecrona G., Klein R.S., Cross A.H., Otero K., Piccio L. TREM2 regulates microglial cell activation in response to demyelination in vivo. Acta Neuropathol. 2015, 129:429-447.
27. Cebulla C.M., Zelinka C.P., Scott M.A., Lubow M., Bingham A., Rasiah S., Mahmoud A.M., Fischer A.J. A chick model of retinal detachment : cone rich and novel. PloS One 2012, 7:e44257.
28. Chan W.Y., Kohsaka S., Rezaie P. The origin and cell lineage of microglia: new concepts. Brain Res. Rev. 2007, 53:344-354.
29. Checchin D., Sennlaub F., Levavasseur E., Leduc M., Chemtob S. Potential role of microglia in retinal blood vessel formation. Investig. Ophthalmol. Vis. Sci. 2006, 47:3595-3602.
30. Chen M., Ona V.O., Li M., Ferrante R.J., Fink K.B., Zhu S., Bian J., Guo L., Farrell L.A., Hersch S.M., Hobbs W., Vonsattel J.P., Cha J.H., Friedlander R.M. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med. 2000, 6:797-801.
31. Chen L., Yang P., Kijlstra A. Distribution, markers, and functions of retinal microglia. Ocul. Immunol. Inflamm. 2002, 10:27-39.
32. Columba-Cabezas S., Serafini B., Ambrosini E., Sanchez M., Penna G., Adorini L., Aloisi F. Induction of macrophage-derived chemokine/CCL22 expression in experimental autoimmune encephalomyelitis and cultured microglia: implications for disease regulation. J. Neuroimmunol. 2002, 130:10-21.
33. Columba-Cabezas S., Serafini B., Ambrosini E., Aloisi F. Lymphoid chemokines CCL19 and CCL21 are expressed in the central nervous system during experimental autoimmune encephalomyelitis: implications for the maintenance of chronic neuroinflammation. Brain Pathol. 2003, 13:38-51.
34. Combadière C., Feumi C., Raoul W., Keller N., Rodéro M., Pézard A., Lavalette S., Houssier M., Jonet L., Picard E., Debré P., Sirinyan M., Deterre P., Ferroukhi T., Cohen S.Y., Chauvaud D., Jeanny J.C., Chemtob S., Behar-Cohen F., Sennlaub F. CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J. Clin. Investig. 2007, 117:2920-2928.
35. Cuadros M.A., Navascués J. The origin and differentiation of microglial cells during development. Prog. Neurobiol. 1998, 56:173-189.
36. Cukras C.A., Petrou P., Chew E.Y., Meyerle C.B., Wong W.T. Oral minocycline for the treatment of diabetic macular edema: results of a phase I/II clinical study. Investig. Ophthalmol. Vis. Sci. 2012, 53:3865-3874.
37. Dalmau I., Vela J.M., González B., Castellano B. Expression of LFA-1alpha and ICAM-1 in the developing rat brain: a potential mechanism for the recruitment of microglial cell precursors. Brain Res. Dev. Brain Res. 1997, 103:163-170.
38. Damani M.R., Zhao L., Fontainhas A.M., Amaral J., Fariss R.N., Wong W.T. Age-related alterations in the dynamic behavior of microglia. Aging Cell 2011, 10:263-276.
39. Davies M.H., Stempel A.J., Powers M.R. MCP-1 deficiency delays regression of pathologic retinal neovascularization in a model of ischemic retinopathy. Investig. Ophthalmol. Vis. Sci. 2008, 49:4195-4202.
40. de Groot C.J., Huppes W., Sminia T., Kraal G., Dijkstra C.D. Determination of the origin and nature of brain macrophages and microglial cells in mouse central nervous system, using non-radioactive in situ hybridization and immunoperoxidase techniques. Glia 1992, 6:301-309.
41. del Río-Hortega P. Art and artifice in the science of histology. Histopathology 1933, 22:515-525. Reprinted in, 1993.
42. Deliyanti D., Miller A.G., Tan G., Binger K.J., Samson A.L., Wilkinson-Berka J.L. Neovascularization is attenuated with aldosterone synthase inhibition in rats with retinopathy. Hypertension 2012, 59:607-613.
43. Diaz-Araya C.M., Provis J.M., Penfold P.L., Billson F.A. Development of microglial topography in human retina. J. Comp. Neurol. 1995, 363:53-68.
44. Domaradzka-Pytel B., Ludkiewicz B., Moryś J., Wisniewski H.M. Expression and distribution of various antigens of developing microglial cells in the rat telencephalon. J. Hirnforsch. 1999, 39:283-291.
45. Dowling J.E., Sidman R.L. Inherited retinal dystrophy in the rat. J. Cell Biol. 1962, 14:73-109.
46. Drew P.D., Chavis J.A. Inhibition of microglial cell activation by cortisol. Brain Res. Bull. 2000, 52:391-396.
47. Eglitis M.A., Mezey É. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4080-4085.
48. Emmetsberger J., Tsirka S.E. Microglial inhibitory factor (MIF/TKP) mitigates secondary damage following spinal cord injury. Neurobiol. Dis. 2012, 47:295-309.
49. Eter N., Engel D.R., Meyer L., Helb H.M., Roth F., Maurer J., Holz F.G., Kurts C. In vivo visualization of dendritic cells, macrophages, and microglial cells responding to laser-induced damage in the fundus of the eye. Investig. Ophthalmol. Vis. Sci. 2008, 49:3649-3658.
50. Eyo U.B., Wu L.J. Bidirectional microglia-neuron communication in the healthy brain. Neural Plast. 2013, 2013:456857.
51. Fan W., Li X., Wang W., Mo J.S., Kaplan H., Cooper N.G. Early involvement of Immune/Inflammatory response genes in retinal degeneration in DBA/2J mice. Ophthalmol. Eye Dis. 2010, 11:23-41.
52. Fedoroff S., Zhai R., Novak J.P. Microglia and astroglia have a common progenitor cell. J. Neurosci. Res. 1997, 50:477-486.
53. Fernandez-Bueno I., Garcia-Gutierrez M.T., Srivastava G.K., Gayoso M.J., Gonzalo-Orden J.M., Pastor J.C. Adalimumab (tumor necrosis factor-blocker) reduces the expression of glial fibrillary acidic protein immunoreactivity increased by exogenous tumor necrosis factor alpha in an organotypic culture of porcine neuroretina. Mol. Vis. 2013, 19:894-903.
54. Ferrari D., Wesselborg S., Bauer M.K., Schulze-Osthoff K. Extracellular ATP activates transcription factor NF-kappaB through the P2Z purinoreceptor by selectively targeting NF-kappaB p65. J. Cell Biol. 1997, 139:1635-1643.
55. Fischer F., Martin G., Agostini H.T. Activation of retinal microglia rather than microglial cell density correlates with retinal neovascularization in the mouse model of oxygen-induced retinopathy. J. Neuroinflammation 2011, 8:120.
56. Fischer A.J., Zelinka C., Milani-Nejad N. Reactive retinal microglia, neuronal survival, and the formation of retinal folds and detachments. Glia 2015, 63:313-327.
57. Flynn G., Maru S., Loughlin J., Romero I.A., Male D. Regulation of chemokine receptor expression in human microglia and astrocytes. J. Neuroimmunol. 2003, 136:84-93.
58. Frei K., Siepl C., Groscurth P., Bodmer S., Schwerdel C., Fontana A. Antigen presentation and tumor cytotoxicity by interferon-gamma-treated microglial cells. Eur. J. Immunol. 1987, 17:1271-1278.
59. Galasso J.M., Miller M.J., Cowell R.M., Harrison J.K., Warren J.S., Silverstein F.S. Acute excitotoxic injury induces expression of monocyte chemoattractant protein-1 and its receptor, CCR2, in neonatal rat brain. Exp. Neurol. 2000, 165:295-305.
60. Garcia-Valenzuela E., Gorczyca W., Darzynkiewicz Z., Sharma S.C. Apoptosis in adult retinal ganglion cells after axotomy. J. Neurobiol. 1994, 25:431-438.
61. Garden G.A., Möller T. Microglia biology in health and disease. J. Neuroimmune Pharmacol. 2006, 1:127-137.
62. Ginhoux F., Greter M., Leboeuf M., Nandi S., See P., Gokhan S., Mehler M.F., Conway S.J., Ng L.G., Stanley E.R., Samokhvalov I.M., Merad M. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010, 330:841-845.
63. Ginhoux F., Lim S., Hoeffel G., Low D., Huber T. Origin and differentiation of microglia. Front. Cell. Neurosci. 2013, 7:45.
64. Glybina I.V., Kennedy A., Ashton P., Abrams G.W., Lezzi R. Photoreceptor neuroprotection in RCS rats via low-dose intravitreal sustained-delivery of fluocinolone acetonide. Investig. Ophthalmol. Vis. Sci. 2009, 50:4847-4857.
65. Glybina I.V., Kennedy A., Ashton P., Abrams G.W., Lezzi R. Intravitreous delivery of the corticosteroid fluocinolone acetonide attenuates retinal degeneration in S334ter-4 rats. Investig. Ophthalmol. Vis. Sci. 2010, 51:4243-4252.
66. Golub R., Cumano A. Embryonic hematopoiesis. Blood Cells Mol. Dis. 2013, 51:226-231.
67. Goodbrand I.A., Gaze R.M. Microglia in tadpoles of Xenopus laevis: normal distribution and the response to optic nerve injury. Anat. Embryol. (Berl) 1991, 184:71-82.
68. Gosh A. Brain APCs including microglia are only differential and positional polymorphs. Ann. Neurosci. 2010, 17:191-199.
69. Graeber M.B. Changing face of microglia. Science 2010, 330:783-788.
70. Grossniklaus H.E., Kang S.J., Berglin L. Animal models of choroidal and retinal neovascularization. Prog. Retin. Eye Res. 2010, 29:500-519.
71. Gullapalli V.K., Zhang J., Pararajasegaram G., Rao N.A. Hematopoietically derived retinal perivascular microglia initiate uveoretinitis in experimental autoimmune uveitis. Graefes Arch. Clin. Exp. Ophthalmol. 2000, 238:319-325.
72. Gupta N., Brown K.E., Milam A.H. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp. Eye Res. 2003, 76:463-471.
73. Handa J.T., Keithahn M.A., Jaffe G.J. Transferrin-ricin A chain toxin limits the development of experimental proliferative vitreoretinopathy. Exp. Eye Res. 1996, 62:689-696.
74. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40:140-155.
75. Hanisch U.K. Proteins in microglial activation-inputs and outputs by subsets. Curr. Protein Pept. Sci. 2013, 14:3-15.
76. Hao C., Richardson A., Fedoroff S. Macrophage-like cells originate from neuroepithelium in culture: characterization and properties of the macrophage-like cells. Int. J. Dev. Neurosci. 1991, 9:1-14.
77. Harada T., Harada C., Kohsaka S., Wada E., Yoshida K., Ohno S., Mamada H., Tanaka K., Parada L.F., Wada K. Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J. Neurosci. 2002, 22:9228-9236.
78. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., Thompson D.A., Botti P., Bacon K.B., Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10896-10901.
79. Hashioka S., Han Y.H., Fujii S., Kato T., Monji A., Utsumi H., Sawada M., Nakanishi H., Kanba S. Phosphatidylserine and phosphatidylcholine-containing liposomes inhibit amyloid beta and interferon-gamma-induced microglial activation. Free Radic. Biol. Med. 2007, 42:945-954.
80. Heiduschka P., Fischer D., Thanos S. Neuroprotection and regeneration after traumatic lesion of the optic nerve. Klin. Monbl. Augenheilkd. 2004, 221:684-701.
81. Heiduschka P., Thanos S. Cortisol promotes survival and regeneration of axotomised retinal ganglion cells and enhances effects of aurintricarboxylic acid. Graefes Arch. Clin. Exp. Ophthalmol. 2006, 244:1512-1521.
82. Heiduschka P., Schnichels S., Fuhrmann N., Hofmeister S., Schraermeyer U., Wissinger B., Alavi M.V. Electrophysiological and histologic assessment of retinal ganglion cell fate in a mouse model for OPA1-associated autosomal dominant optic atrophy. Investig. Ophthalmol. Vis. Sci. 2010, 51:1424-1431.
83. Hess D.C., Abe T., Hill W.D., Studdard A.M., Carothers J., Masuya M., Fleming P.A., Drake C.J., Ogawa M. Hematopoietic origin of microglial and perivascular cells in brain. Exp. Neurol. 2004, 186:134-144.
84. Hetier E., Ayala J., Denèfle P., Bousseau A., Rouget P., Mallat M., Prochiantz A. Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J. Neurosci. Res. 1988, 21:391-397.
85. Hickey W.F., Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988, 239:290-292.
86. Hide I., Tanaka M., Inoue A., Nakajima K., Kohsaka S., Inoue K., Nakata Y. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J. Neurochem. 2000, 75:965-972.
87. Howell G.R., Libby R.T., Jakobs T.C., Smith R.S., Phalan F.C., Barter J.W., Barbay J.M., Marchant J.K., Mahesh N., Porciatti V., Whitmore A.V., Masland R.H., John S.W. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007, 179:1523-1537.
88. Howell G.R., Macalinao D.G., Sousa G.L., Walden M., Soto I., Kneeland S.C., Barbay J.M., King B.L., Marchant J.K., Hibbs M., Stevens B., Barres B.A., Clark A.F., Libby R.T., John S.W. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J. Clin. Investig. 2011, 121:1429-1444.
89. Htain W.W., Leong S.K., Ling E.A. A comparative Mac-1 immunocytochemical and lectin histochemical study of microglial cells in the normal and athymic mice. Glia 1994, 12:44-51.
90. Hua J.Y., Smith S.J. Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 2004, 7:327-332.
91. Huang T.L., Chang C.H., Lin K.H., Sheu M.M., Tsai R.K. Lack of protective effect of local administration of triamcinolone or systemic treatment with methylprednisolone against damages caused by optic nerve crush in rats. Exp. Eye Res. 2011, 92:112-119.
92. Huang H., Parlier R., Shen J.K., Lutty G.A., Vinores S.A. VEGF receptor blockade markedly reduces retinal microglia/macrophage infiltration into laser-induced CNV. PLoS One 2013, 8:e71808.
93. Hughes E.H., Schlichtenbrede F.C., Murphy C.C., Sarra G.M., Luthert P.J., Ali R.R., Dick A.D. Generation of activated sialoadhesin-positive microglia during retinal degeneration. Investig. Ophthalmol. Vis. Sci. 2003, 44:2229-2234.
94. Hughes V. Microglia: the constant gardeners. Nature 2012, 485:570-572.
95. Hutchins K.D., Dickson D.W., Rashbaum W.K., Lyman W.D. Localization of morphologically distinct microglial populations in the developing human fetal brain: implications for ontogeny. Brain Res. Dev. Brain Res. 1990, 55:95-102.
96. Iandiev I., Uckermann O., Pannicke T., Wurm A., Tenckhoff S., Pietsch U.C., Reichenbach A., Wiedemann P., Bringmann A., Uhlmann S. Glial cell reactivity in a porcine model of retinal detachment. Investig. Ophthalmol. Vis. Sci. 2006, 47:2161-2171.
97. Ibrahim A.S., El-Shishtawy M.M., Peña A., Liou G.I. Genistein attenuates retinal inflammation associated with diabetes by targeting of microglial activation. Mol. Vis. 2010, 16:2033-2042.
98. Iezzi R., Guru B.R., Glybina I.V., Mishra M.K., Kennedy A., Kannan R.M. Dendrimer-based targeted intravitreal therapy for sustained attenuation of neuroinflammation in retinal degeneration. Biomaterials 2012, 33:979-988.
99. Inoue K., Nakajima K., Morimoto T., Kikuchi Y., Koizumi S., Illes P., Kohsaka S. ATP stimulation of Ca2+ -dependent plasminogen release from cultured microglia. Br. J. Pharmacol. 1998, 123:1304-1310.
100. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002, 40:156-163.
101. Inoue K. ATP receptors of microglia involved in pain. Novartis Found. Symp. 2006, 276:263-272.
102. Inoue K. The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol. Ther. 2006, 109:210-226.
103. Ishibashi T., Miller H., Orr G., Sorgente N., Ryan S.J. Morphologic observations on experimental subretinal neovascularization in the monkey. Investig. Ophthalmol. Vis. Sci. 1987, 28:1116-1130.
104. Janabi N., Hau I., Tardieu M. Negative feedback between prostaglandin and alpha- and beta-chemokine synthesis in human microglial cells and astrocytes. J. Immunol. 1999, 162:1701-1706.
105. Johnson E.C., Morrison J.C. Friend or foe? Resolving the impact of glial responses in glaucoma. J. Glaucoma 2009, 18:341-353.
106. Joly S., Francke M., Ulbricht E., Beck S., Seeliger M., Hirrlinger P., Hirrlinger J., Lang K.S., Zinkernagel M., Odermatt B., Samardzija M., Reichenbach A., Grimm C., Remé C.E. Cooperative phagocytes: resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am. J. Pathol. 2009, 174:2310-2323.
107. Jun C.D., Hoon-Ryu, Um J.Y., Kim J.M., Kang S.S., Kim H.M., Chung H.T. Involvement of protein kinase C in the inhibition of nitric oxide production from murine microglial cells by glucocorticoid. Biochem. Biophys. Res. Commun. 1994, 199:633-638.
108. Karlstetter M., Ebert S., Langmann T. Microglia in the healthy and degenerating retina: insights from novel mouse models. Immunobiology 2010, 215:685-691.
109. Karlstetter M., Nothdurfter C., Aslanidis A., Moeller K., Horn F., Scholz R., Neumann H., Weber B.H.F., Rupprecht R., Langmann T. Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J. Neuroinflammation 2014, 11:3.
110. Katsumoto A., Lu H., Miranda A.S., Ransohoff R.M. Ontogeny and functions of central nervous system macrophages. J. Immunol. 2014, 193:2615-2621.
111. Kaur C., Wu C.H., Wen C.Y., Ling E.A. The effects of subcutaneous injections of glucocorticoids on amoeboid microglia in postnatal rats. Arch. Histol. Cytol. 1994, 57:449-459.
112. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
113. Kierdorf K., Erny D., Goldmann T., Sander V., Schulz C., Perdiguero E.G., Wieghofer P., Heinrich A., Riemke P., Hölscher C., Müller D.N., Luchow B., Brocker T., Debowski K., Fritz G., Opdenakker G., Diefenbach A., Biber K., Heikenwalder M., Geissmann F., Rosenbauer F., Prinz M. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 2013, 16:273-280.
114. Kim J.E., Kwak S.E., Jo S.M., Kang T.C. Blockade of P2X receptor prevents astroglial death in the dentate gyrus following pilocarpine-induced status epilepticus. Neurol. Res. 2009, 31:982-988.
115. Kitamura T., Miyake T., Fujita S. Genesis of resting microglia in the gray matter of mouse hippocampus. J. Comp. Neurol. 1984, 226:421-433.
116. Kovács G.G., Höftberger R., Majtényi K., Horváth R., Barsi P., Komoly S., Lassmann H., Budka H., Jakab G. Neuropathology of white matter disease in Leber's hereditary optic neuropathy. Brain 2005, 128:35-41.
117. Krause T.A., Alex A.F., Engel D.R., Kurts C., Eter N. VEGF-production by CCR2-dependent macrophages contributes to laser-induced choroidal neovascularization. PLoS One 2014, 9:e94313.
118. Langmann T. Microglia activation in retinal degeneration. J. Leukoc. Biol. 2007, 81:1345-1351.
119. Lee J.E., Liang K.J., Fariss R.N., Wong W.T. Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Investig. Ophthalmol. Vis. Sci. 2008, 49:4169-4176.
120. Levkovitch-Verbin H., Waserzoog Y., Vander S., Makarovsky D., Piven I. Minocycline upregulates pro-survival genes and downregulates pro-apoptotic genes in experimental glaucoma. Graefes Arch. Clin. Exp. Ophthalmol. 2014, 252:761-772.
121. Lewis G.P., Sethi C.S., Carter K.M., Charteris D.G., Fisher S.K. Microglial cell activation following retinal detachment: a comparison between species. Mol. Vis. 2005, 11:491-500.
122. Lewis G.P., Chapin E.A., Luna G., Linberg K.A., Fisher S.K. The fate of Müller's glia following experimental retinal detachment: nuclear migration, celll division, and subretinal glial scar formation. Mol. Vis. 2010, 16:1361-1372.
123. Li L., Niekämper, D., Heiduschka, P., Eter, N. (2015a) Purinergic receptors and their inhibition in the model of laser-induced choroidal neovascularisation, in preparation.
124. Li L., Heiduschka, P., Alex, A.F., Niekämper, D., Eter, N. (2015b) Behaviour of microglial cells in an animal model of laser-induced choroidal neovascularisation, in preparation.
125. Ling E.A., Penney D., Leblond C.P. Use of carbon labelling to demonstrate the role of blood monocytes as precursors of the "ameboid cells" present in the corpus callosum of postnatal rats. J. Comp. Neurol. 1980, 193:631-657.
126. Ling E.A. A light microscopic demonstration of amoeboid microglia and microglial cells in the retina of rats of various ages. Arch. Histol. Jpn. 1982, 45:37-44.
127. Ling E.A. Influence of cortisone on amoeboid microglia and microglial cells in the corpus callosum in postnatal rats. J. Anat. 1982, 134:705-717.
128. Luhmann U.F., Robbie S., Munro P.M., Barker S.E., Duran Y., Luong V., Fitzke F.W., Bainbridge J.W., Ali R.R., MacLaren R.E. The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Investig. Ophthalmol. Vis. Sci. 2009, 50:5934-5943.
129. Luhmann U.F., Carvalho L.S., Robbie S.J., Cowing J.A., Duran Y., Munro P.M., Bainbridge J.W., Ali R.R. Ccl2, Cx3cr1 and Ccl2/Cx3cr1 chemokine deficiencies are not sufficient to cause age-related retinal degeneration. Exp. Eye Res. 2013, 107:80-87.
130. Marchesani O. Die Morphologie der Glia im Nervus opticus und in der Retina, dargestellt nach den neuesten Untersuchungsmethoden und Untersuchungsergebnissen. Graefes Arch. Ophthalmol. 1926, 117:575-605.
131. Marin-Teva J.L., Cuadro M.A., Martin-Oliva D., Navascués J. Microglia and neuronal cell death. Neuron Glia Biol. 2011, 7:25-40.
132. Matsubara T., Pararajasegaram G., Wu G.S., Rao N.A. Retinal microglia differentially express phenotypic markers of antigen-presenting cells in vitro. Investig. Ophthalmol. Vis. Sci. 1999, 40:3186-3193.
133. McCarthy C.A., Widdop R.E., Deliyanti D., Wilkinson-Berka J.L. Brain and retinal microglia in health and disease: an unrecognized target of the renin-angiotensin system. Clin. Exp. Pharmacol. Physiol. 2013, 40:571-579.
134. McKanna J.A. Primitive glial compartments in the floor plate of mammalian embryos: distinct progenitors of adult astrocytes and microglia support the notoplate hypothesis. Perspect. Dev. Neurobiol. 1993, 1:245-255.
135. McKanna J.A. Lipocortin 1 immunoreactivity identifies microglia in adult rat brain. J. Neurosci. Res. 1993, 36:491-500.
136. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008, 454:428-435.
137. Mercanti G., Ragazzi E., Toffano G., Giusti P., Zusso M. Phosphatidylserine and curcumin act synergistically to down-regulate release of interleukin-1β from lipopolysaccharide-stimulated cortical primary microglial cells. CNS Neurol. Disord. Drug Targets 2014, 13:792-800.
138. Mizutani M., Pino P.A., Saederup N., Charo I.F., Ransohoff R.M., Cardona A.E. The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J. Immunol. 2012, 188:29-36.
139. Möller T. Calcium signaling in microglial cells. Glia 2002, 40:184-194.
140. Naskar R., Wissing M., Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Investig. Ophthalmol. Vis. Sci. 2002, 43:2962-2968.
141. Navascués J., Moujahid A., Quesada A., Cuadros M.A. Microglia in the avian retina: immunocytochemical demonstration in the adult quail. J. Comp. Neurol. 1994, 350:171-186.
142. Neufeld A.H. Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch. Ophthalmol. 1999, 117:1050-1056.
143. Neumann J., Sauerzweig S., Rönicke R., Gunzer F., Dinkel K., Ullrich O., Gunzer M., Reymann K.G. Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J. Neurosci. 2008, 28:5965-5975.
144. Neumann H., Kotter M.R., Franklin R.J. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 2009, 132:288-295.
145. Niekämper, D., Li, L., Alex, A.F., Heiduschka, P. Eter, N. (2015) Effects of microglial inhibition in the experimental model of laser-induced choroidal neovascularisation, in preparation.
146. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
147. Paolicelli R.C., Bolasco G., Pagani F., Maggi L., Scianni M., Panzanelli P., Giustetto M., Ferreira T.A., Guiducci E., Dumas L., Ragozzino D., Gross C.T. Synaptic pruning by microglia is necessary for normal brain development. Science 2011, 333:1456-1458.
148. Pearson H.E., Payne B.R., Cunningham T.J. Microglial invasion and activation in response to naturally occurring neuronal degeneration in the ganglion cell layer of the postnatal cat retina. Brain Res. Dev. Brain Res. 1993, 76:249-255.
149. Perdiguero E.G., Klapproth K., Schulz C., Busch K., Azzoni E., Crozet L., Garner H., Trouillet C., de Bruijn M.F., Geissmann F., Rodewald H.R. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature Dec 3 2014, 10.1038/nature13989.
150. Perry V.H., Hume D.A., Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985, 15:313-326.
151. Power C.A., Proudfoot A.E. The chemokine system: novel broad-spectrum therapeutic targets. Curr. Opin. Pharmacol. 2001, 1:417-424.
152. Provis J.M., Penfold P.L. Cell death and the elimination of retinal axons during development. Prog. Neurobiol. 1988, 31:331-347.
153. Provis J.M., Diaz C.M., Penfold P.L. Microglia in human retina: a heterogeneous population with distinct ontogenies. Perspect. Dev. Neurobiol. 1996, 3:213-222.
154. Quigley H.A., Nickells R.W., Kerrigan L.A., Pease M.E., Thibault D.J., Zack D.J. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Investig. Ophthalmol. Vis. Sci. 1995, 36:774-786.
155. Rao N.A., Kimoto T., Zamir E., Giri R., Wang R., Ito S., Pararajasegaram G., Read R.W., Wu G.S. Pathogenic role of retinal microglia in experimental uveoretinitis. Investig. Ophthalmol. Vis. Sci. 2003, 44:22-31.
156. Rezaie P., Male D. Mesoglia and microglia - a historical review of the concept of mononuclear phagocytes within the central nervous system. J. Hist. Neurosci. 2002, 11:325-374.
157. Richardson A., Hao C., Fedoroff S. Microglia progenitor cells: a subpopulation in cultures of mouse neopallial astroglia. Glia 1993, 7:25-33.
158. Rivest S. Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 2009, 9:429-439.
159. Ross R.J., Zhou M., Shen D., Fariss R.N., Ding X., Bojanowski C.M., Tuo J., Chan C.C. Immunological protein expression profile in Ccl2/Cx3cr1 deficient mice with lesions similar to age-related macular degeneration. Exp. Eye Res. 2008, 86:675-683.
160. Rosque R.S., Imperial C.J., Caldwell R.B. Microglial cells invade the outer retina as photoreceptors degenerate in Royal College of Surgeons rats. Investig. Ophthalmol. Vis. Sci. 1996, 37:196-203.
161. Rungger-Brändle E., Dosso S.S., Leuenberger P.M. Glial reactivity, an early feature of diabetic retinopathy. Investig. Ophthalmol. Vis. Sci. 2000, 41:1971-1980.
162. Rymo S.F., Gerhardt H., Wolfhagen Sand F., Lang R., Uv A., Betsholtz C. A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS One 2011, 6:e15846.
163. Saijo K., Glass C.K. Microglial cell origin and phenotypes in health and disease. Nat. Rev. Immunol. 2011, 11:775-787.
164. Sanes J.R., Lichtman J.W. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 1999, 22:389-442.
165. Santos A.M., Martin-Oliva D., Ferrer-Martin R.M., Tassi M., Calvente R., Sierra A., Carrasco M.C., Marín-Teva J.L., Navascués J., Cuadros M.A. Microglial response to light-induced photoreceptor degeneration in the mouse retina. J. Comp. Neurol. 2010, 518:477-492.
166. Schafer D.P., Lehrman E.K., Kautzman A.G., Koyama R., Mardinly A.R., Yamasaki R., Ransohoff R.M., Greenberg M.E., Barres B.A., Stevens B. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012, 74:691-705.
167. Schafer D.P., Lehrman E.K., Stevens B. The "quad-partite" synapse: microglia-synapse interactions in the developing and mature CNS. Glia 2013, 61:24-36.
168. Schulz C., Gomez P.E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., Prinz M., Wu B., Jacobsen S.E., Pollard J.W., Frampton J., Liu K.J., Geissmann F. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012, 336:86-90.
169. Seo M.S., Kwak N., Ozaki H., Yamada H., Okamoto N., Yamada E., Fabbro D., Hofmann F., Wood J.M., Campochiaro P.A. Dramatic inhibition of retinal and choroidal neovascularization by oral administration of a kinase inhibitor. Am. J. Pathol. 1999, 154:1743-1753.
170. Shen D., Cao X., Zhao L., Tuo J., Wong W.T., Chan C.C. Naloxone ameliorates retinal lesions in Ccl2/Cx3cr1 double-deficient mice via modulation of microglia. Investig. Ophthalmol. Vis. Sci. 2011, 52:2897-2904.
171. Shen W., Lee S.R., Araujo J., Chung S.H., Zhu L., Gillies M.C. Effect of glucocorticoids on neuronal and vascular pathology in a transgenic model of selective Müller cell ablation. Glia 2014, 62:1110-1124.
172. Sheu J.N., Liao W.C., Wu U.I., Shyu L.Y., Mai F.D., Chen L.Y., Chen M.J., Youn S.C., Chang H.M. Resveratrol suppresses calcium-mediated microglial activation and rescues hippocampal neurons of adult rats following acute bacterial meningitis. Comp. Immunol. Microbiol. Infect. Dis. 2013, 36:137-148.
173. Shigemoto-Mogami Y., Koizumi S., Tsuda M., Ohsawa K., Kohsaka S., Inoue K. Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. J. Neurochem. 2001, 78:1339-1349.
174. Simpson J., Rezaie P., Newcombe J., Cuzner M.L., Male D., Woodroofe M.N. Expression of the beta-chemokine receptors CCR2, CCR3 and CCR5 in multiple sclerosis central nervous system tissue. J. Neuroimmunol. 2000, 108:192-200.
175. Soto I., Oglesby E., Buckingham B.P., Son J.L., Roberson E.D., Steele M.R., Inman D.M., Vetter M.L., Horner P.J., Marsh-Armstrong N. Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J. Neurosci. 2008, 28:548-561.
176. Steele M.R., Inman D.M., Calkins D.J., Horner P.J., Vetter M.L. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Investig. Ophthalmol. Vis. Sci. 2006, 47:977-985.
177. Stirling D.P., Khodarahmi K., Liu J., McPhail L.T., McBride C.B., Steeves J.D., Ramer M.S., Tetzlaff W. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. 2004, 24:2182-2190.
178. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40:133-139.
179. Sun C., Li X.X., He X.J., Zhang Q., Tao Y. Neuroprotective effect of minocycline in a rat model of branch retinal vein occlusion. Exp. Eye Res. 2013, 113:105-116.
180. Suzuki H., Franz H., Yamamoto T., Iwasaki Y., Konno H. Identification of the normal microglial population in human and rodent nervous tissue using lectin-histochemistry. Neuropathol. Appl. Neurobiol. 1988, 14:221-227.
181. Suzuki T., Hide I., Ido K., Kohsaka S., Inoue K., Nakata Y. Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J. Neurosci. 2004, 24:1-7.
182. Suzuki H., Sugimura Y., Iwama S., Suzuki H., Nobuaki O., Nagasaki H., Arima H., Sawada M., Oiso Y. Minocycline prevents osmotic demyelination syndrome by inhibiting the activation of microglia. J. Am. Soc. Nephrol. 2010, 21:2090-2098.
183. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu. Rev. Immunol. 2003, 21:335-376.
184. Thanos S. The relationship of microglial cells to dying neurons during natural neuronal cell death and axotomy-induced degeneration of the rat retina. Eur. J. Neurosci. 1991, 3:1189-1207.
185. Thanos S. Specific transcellular carbocyanine-labelling of rat retinal microglia during injury-induced neuronal degeneration. Neurosci. Lett. 1991, 127:108-112.
186. Thanos S., Pavlidis C., Mey J., Thiel H.J. Specific transcellular staining of microglia in the adult rat after traumatic degeneration of carbocyanine-filled retinal ganglion cells. Exp. Eye Res. 1992, 55:101-117.
187. Thanos S. Sick photoreceptors attract activated microglia from the ganglion cell layer: a model to study the inflammatory cascades in rats with inherited retinal dystrophy. Brain Res. 1992, 588:21-28.
188. Thanos S., Mey J., Wild M. Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degradation and enhances axonal regeneration in vivo and in vitro. J. Neurosci. 1993, 13:455-466.
189. Thanos S., Richter W. The migratory potential of vitally labelled microglial cells within the retina of rats with hereditary photoreceptor dystrophy. Int. J. Dev. Neurosci. 1993, 11:671-680.
190. Thanos S., Moore S., Hong Y.M. Retinal microglia. Prog. Ret Eye Res. 1996, 15:331-361.
191. Tikka T.M., Koistinaho J.E. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 2001, 166:7527-7533.
192. Tobe T., Ortega S., Luna J.D., Ozaki H., Okamoto N., Derevjanik N.L., Vinores S.A., Basilico C., Campochiaro P.A. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am. J. Pathol. 1998, 153:1641-1646.
193. Tremblay M.E., Lowery R.L., Majewska A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 2010, 8:e100527.
194. Tuo J., Bojanowski C.M., Zhou M., Shen D., Ross R.J., Rosenberg K.I., Cameron D.J., Yin C., Kowalak J.A., Zhuang Z., Zhang K., Chan C.C. Murine ccl2/cx3cr1 deficiency results in retinal lesions mimicking human age-related macular degeneration. Investig. Ophthalmol. Vis. Sci. 2007, 48:3827-3836.
195. Unoki N., Murakami T., Nishijima K., Ogino K., van Rooijen N., Yoshimura N. SDF-1/CXCR4 contributes to the activation of tip cells and microglia in retinal angiogenesis. Investig. Ophthalmol. Vis. Sci. 2010, 51:3362-3371.
196. Vallières L., Sawchenko P.E. Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity. J. Neurosci. 2003, 23:5197-5207.
197. van Rossum D., Hanisch U.K. Microglia. Metab. Brain Dis. 2004, 19:393-411.
198. Vincent J.A., Mohr S. Inhibition of caspase-1/interleukin-1 beta signalling prevents degeneration of retinal capillaries in diabetes and galactosemia. Diabetes 2007, 56:224-230.
199. Vitry S., Bertrand J.Y., Cumano A., Dubois-Dalcq M. Primordial hematopoietic stem cells generate microglia but not myelin-forming cells in a neural environment. J. Neurosci. 2003, 23:10724-10731.
200. Vrabec F. Microglia in the monkey and rabbit retina. J. Neuropathol. Exp. Neurol. 1970, 29:217-224.
201. Vrabec F., Vrabec J. Retinal microglia in cases of choroidal melanoblastoma. Ophthalmologica 1973, 166:342-348.
202. Wake H., Moorhouse A.J., Jinno S., Kohsaka S., Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 2009, 29:3974-3980.
203. Wang J., Tsirka S. Tuftsin fragment 1-3 is beneficial when delivered after the induction of intracerebral hemorrhage. Stroke 2005, 36:613-618.
204. Weller M., Heimann K., Wiedemann P. Mononuclear phagocytes and their growth factors: pacemakers of proliferative vitreoretinopathy?. Klin. Monbl. Augenheilkd. 1990, 196:121-127.
205. Weller M., Heimann K., Wiedemann P. The pathogenesis of vitreoretinal proliferation and traction: a working hypothesis. Med. Hypotheses 1990, 31:157-159.
206. Weller M., Clausen R., Heimann K., Wiedemann P. Iron-binding proteins in the human vitreous: lactoferrin and transferrin in health and in proliferative intraocular disorders. Ophthalmic Res. 1990, 22:194-200.
207. Wenzel A., Grimm C., Samardzija M., Remé C.E. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog. Retin. Eye Res. 2005, 24:275-306.
208. Witting A., Müller P., Herrmann A., Kettenmann H., Nolte C. Phagocytic clearance of apoptotic neurons by Microglia/Brain macrophages in vitro: involvement of lectin-, integrin-, and phosphatidylserine-mediated recognition. J. Neurochem. 2000, 75:1060-1070.
209. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 2002, 22:1763-1771.
210. Xu H., Chen M., Mayer E.J., Forrester J.V., Dick A.D. Turnover of resident retinal microglia in the normal adult mouse. Glia 2007, 55:1189-1198.
211. Xu H., Chen M., Forrester J.V. Para-inflammation in the aging retina. Prog. Retin. Eye Res. 2009, 28:348-368.
212. Yang L., Kim J.H., Kovacs K.D., Arroyo J.G., Chen D.F. Minocycline inhibition of photoreceptor degeneration. Arch. Ophthalmol. 2009, 127:1475-1480.
213. Yong V.W., Wells J., Giuliani F., Casha S., Power C., Metz L.M. The promise of minocycline in neurology. Lancet Neurol. 2004, 3:744-751.
214. Yrjänheikki J., Keinänen R., Pellikka M., Hökfelt T., Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15769-15774.
215. Zeng H.Y., Zhu X.A., Zhang C., Yang L.P., Wu L.M., Tso M.O. Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Investig. Ophthalmol. Vis. Sci. 2005, 46:2992-2999.
216. Zeng H.Y., Green W.R., Tso M.O. Microglial activation in human diabetic retinopathy. Arch. Ophthalmol. 2008, 126:227-232.
217. Zhang J., Wu G.S., Ishimoto S., Pararajasegaram G., Rao N.A. Expression of major histocompatibility complex molecules in rodent retina. Immunohistochemical study. Investig. Ophthalmol. Vis. Sci. 1997, 38:1848-1857.
218. Zhang C., Lei B., Lam T.T., Yang F., Sinha D., Tso M.O. Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Investig. Ophthalmol. Vis. Sci. 2004, 45:2753-2759.
219. Zhao L., Ma W., Fariss R.N., Wong W.T. Minocycline attenuates photoreceptor degeneration in a mouse model of subretinal hemorrhage microglial: inhibition as a potential therapeutic strategy. Am. J. Pathol. 2011, 179:1265-1277.
220. Zhu S., Stavrovskaya I.G., Drozda M., Kim B.Y., Ona V., Li M., Sarang S., Liu A.S., Hartley D.M., Wu D.C., Gullans S., Ferrante R.J., Przedborski S., Kristal B.S., Friedlander R.M. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002, 417:74-78.
221. Ziganshin A.U., Hoyle C.H., Bo X., Lambrecht G., Mutschler E., Bäumert H.G., Burnstock G. PPADS selectively antagonizes P2X-purinoceptor-mediated responses in the rabbit urinary bladder. Br. J. Pharmacol. 1993, 110:1491-1495.