Early microglia activation in a mouse model of chronic glaucoma

Journal of Comparative Neurology

Volumn 519, Issue 4, 2011, Pages 599-620

  Bosco, Alejandra ^a   Steele, Michael R ^a   Vetter, Monica L ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

DBA 2J; DBA 2J Gpnmb+ SjJ; Iba1; Optic nerve; RGCs

Indexed keywords

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; GLAUCOMA; MICROGLIA; MOUSE; NERVE DEGENERATION; NONHUMAN; NONMYELINATED NERVE; OPTIC NERVE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RETINA;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GLAUCOMA; HUMANS; INTRAOCULAR PRESSURE; MICE; MICE, INBRED DBA; MICE, TRANSGENIC; MICROGLIA; OPTIC NERVE; RECEPTORS, CHEMOKINE; RETINA;

EID: 78751489896     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22516     Document Type: Article

References (110)

1. Anderson DH, Neitz J, Kaska DD, Fenwick J, Jacobs GH, Fisher SK. 1986. Retinoid-binding proteins in cone-dominant retinas. Invest Ophthalmol Vis Sci 27: 1015-1026.
2. Anderson MG, Smith RS, Hawes NL, Zabaleta A, Chang B, Wiggs JL, John SW. 2002. Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice. Nat Genet 30: 81-85.
3. Anderson MG, Nair KS, Amonoo LA, Nehalow A, Trantow CM, Masli S, John SW. 2008. GpnmbR150X allele must be present in bone marrow derived cells to mediate DBA/2J glaucoma. BMC Genet 9: 30.
4. Autieri MV. 1996. cDNA cloning of human allograft inflammatory factor-1: tissue distribution, cytokine induction, and mRNA expression in injured rat carotid arteries. Biochem Biophys Res Commun 228: 29-37.
5. Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8: 57-69.
6. Bodeutsch N, Thanos S. 2000. Migration of phagocytotic cells and development of the murine intraretinal microglial network: an in vivo study using fluorescent dyes. Glia 32: 91-101.
7. + currents fail to change in reactive retinal glial cells in a mouse model of glaucoma. Graefes Arch Clin Exp Ophthalmol 246: 1249-1254.
8. Bosco A, Cusato K, Nicchia GP, Frigeri A, Spray DC. 2005. A developmental switch in the expression of aquaporin-4 and Kir4.1 from horizontal to Müller cells in mouse retina. Invest Ophthalmol Vis Res 46: 3869-3875.
9. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, Hubbard WC, Calkins DJ, Horner PJ, Vetter ML. 2008. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Res 49: 1437-1446.
10. Bosco A, Steele MR, Inman DM, Horner PJ, Vetter ML. 2009. Potential role of retinal microglia in RGC synapse removal in DBA/2J mice. Invest Ophthalmol Vis Res 50: e-abstract 2770.
11. Buckingham BP, Inman DM, Lambert W, Oglesby E, Calkins DJ, Steele MR, Vetter ML, Marsh-Armstrong N, Horner PJ. 2008. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci 28: 2735-2744.
12. Bunt-Milam AH, Saari JC. 1983. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina. J Cell Biol 97: 703-712.
13. Chang B, Smith RS, Hawes NL, Anderson MG, Zabaleta A, Savinova O, Roderick TH, Heckenlively JR, Davisson MT, John SW. 1999. Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice. Nat Genet 21: 405-409.
14. Chauhan BC, Pan J, Archibald ML, LeVatte TL, Kelly ME, Tremblay F. 2002. Effect of intraocular pressure on optic disc topography, electroretinography, and axonal loss in a chronic pressure-induced rat model of optic nerve damage. Invest Ophthalmol Vis Sci 43: 2969-2976.
15. Checchin D, Sennlaub F, Levavasseur E, Leduc M, Chemtob S. 2006. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci 47: 3595-3602.
16. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ. 2010. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci U S A 107: 5196-5201.
17. Cui Q, Yin Y, Benowitz LI. 2009. The role of macrophages in optic nerve regeneration. Neuroscience 158: 1039-1048.
18. Danias J, Lee KC, Zamora MF, Chen B, Shen F, Filippopoulos T, Su Y, Goldblum D, Podos SM, Mittag T. 2003. Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: comparison with RGC loss in aging C57/BL6 mice. Invest Ophthalmol Vis Sci 44: 5151-5162.
19. Davies MH, Eubanks JP, Powers MR. 2006. Microglia and macrophages are increased in response to ischemia-induced retinopathy in the mouse retina. Mol Vis 10: 467-477.
20. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ. 2006. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9: 251-259.
21. Deininger MH, Meyermann R, Schluesener HJ. 2002. The allograft inflammatory factor-1 family of proteins. FEBS Lett 514: 115-121.
22. Douglas RM, Lai JCK, Bian S, Cummins L, Moczydlowski E, Haddad GG. 2006. The calcium-sensitive large-conductance potassium channel (BK/MAXI K) is present in the inner mitochondrial membrane of rat brain. Neuroscience 139: 1249-1261.
23. Du J, Tran F, Fu C, Sretavan DW. 2007. Upregulation of EphB2 and ephrin-B2 at the optic nerve head of DBA/2J glaucomatous mice coincides with axon loss. Invest Ophthalmol Vis Sci 48: 5567-5581.
24. Eisenfeld AJ, Bunt-Milam AH, Saari JC. 1985. Localization of retinoid-binding proteins in developing rat retina. Exp Eye Res 41: 299-304.
25. Elshatory Y, Deng M, Xie X, Gan L. 2007. Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina. J Comp Neurol 503: 182-197.
26. Eter N, Engel DR, Meyer L, Helb HM, Roth F, Maurer J, Holz FG, Kurts C. 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.
27. Fan W, Li X, Wang W, Mo JS, Kaplan H, Cooper NGF. 2010. Early involvement of immune/inflammatory response genes in retinal degeneration in DBA/2J mice. Ophthalmol Eye Dis 11: 23-41.
28. Garcia-Valenzuela E, Sharma SC, Piña AL. 2005. Multilayered retinal microglial response to optic nerve transection in rats. Mol Vis 11: 225-231.
29. Hanisch UK, Kettenmann H. 2007. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
30. Hernandez MR, Miao H, Lukas T. 2008. Astrocytes in glaucomatous optic neuropathy. Prog Brain Res 173: 353-373.
31. Howell GR, Libby RT, Jakobs TC, Smith RS, Phalan FC, Barter JW, Barbay JM, Marchant JK, Mahesh N, Porciatti V, Whitmore AV, Masland RH, John SW. 2007a. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J Cell Biol 179: 1523-1537.
32. Howell GR, Libby RT, Marchant JK, Wilson LA, Cosma IM, Smith RS, Anderson MG, John SW. 2007b. Absence of glaucoma in DBA/2J mice homozygous for wild-type versions of Gpnmb and Tyrp1. BMC Genet 8: 45.
33. Huber G, Matus A. 1984. Differences in the cellular distributions of two microtubule-associated proteins, MAP1 and MAP2, in rat brain. J Neurosci 4: 151-160.
34. Hume DA, Perry VH, Gordon S. 1983. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to for a regular array in the plexiform layers. J Cell Biol 97: 253-257.
35. Imai Y, Kohsaka S. 2002. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40: 164-174.
36. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. 1996. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 224: 855-862.
37. Inman DM, Horner PJ. 2007. Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 55: 942-953.
38. Inman DM, Sappington RM, Horner PJ, Calkins DJ. 2006. Quantitative correlation of optic nerve pathology with ocular pressure and corneal thickness in the DBA/2 mouse model of glaucoma. Invest Ophthalmol Vis Sci 47: 986-996.
39. Ito D, Tanaka K, Suzuki S, Dembo T, Fukuuchi Y. 2001. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32: 1208-1215.
40. Jakobs TC, Libby RT, Ben Y, John SW, Masland RH. 2005. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 171: 313-325.
41. John SW. 2005. Mechanistic insights into glaucoma provided by experimental genetics; the Cogan Lecture. Invest Ophthalmol Vis Sci 46: 2649-2661.
42. John SW, Smith RS, Savinova OV, Hawes L, Chang B, Turnbull D, Davisson M, Roderick TH, Heckenlively JR. 1998. Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Invest Ophthalmol Vis Sci 39: 951-962.
43. Johnson EC, Morrison JC. 2009. Friend or foe? Resolving the impact of glial responses in glaucoma. J Glaucoma 18: 341-353.
44. Johnson TV, Tomarev SI. 2010. Rodent models of glaucoma. Brain Res Bull 15: 349-358.
45. Johnson EC, Jia L, Cepurna WO, Doser TA, Morrison JC. 2007. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Invest Ophthalmol Vis Sci 48: 3161-3177.
46. Joly S, Francke M, Ulbricht E, Beck S, Seeliger M, Hirrlinger P, Hirrlinger J, Lang KS, Zinkernagel M, Odermatt B, Samardzija M, Reichenbach A, Grimm C, Reme CE. 2009. Cooperative phagocytes. Resident microglia and bone marrow immigrants remove dead photoreceptors in retinal lesions. Am J Pathol 174: 2310-2323.
47. Kerr NM, Johnson CS, de Souza CF, Chee K-S, Good WR, Green CR, Danesh-Meyer HV. 2010. Immunolocalization of gap junction protein connexin43 (GJA1) in the human retina and optic nerve. Invest Ophthalmol Vis Sci 51: 4028-4034.
48. Kezic J, Xu H, Chinnery HR, Murphy CC, McMenamin PG. 2008. Retinal microglia and uveal tract dendritic cells and macrophages are not CX3CR1 dependent in their recruitment and distribution in the young mouse eye. Invest Ophthalmol Vis Sci 49: 1599-1608.
49. Kirsch M, Trautmann N, Ernst M, Hofmann H-D. 2010. Involvement of gp130-associated cytokine signaling in Müller cell activation following optic nerve lesion. Glia 58: 768-779.
50. Klück P, van Muijen GN, van der Kamp AW, Tibboel D, van Hoorn WA, Warnaar SO, Molenaar JC. 1984. Hirschsprung's disease studied with monoclonal anti-neurofilament antibodies on tissue sections. Lancet 24: 652-654.
51. Lam TT, Kwong JMK, Tso MOM. 2003. Early glial responses after acute elevated intraocular pressure in rats. Invest Ophthalmol Vis Sci 44: 638-645.
52. Langman T. 2007. Microglia activation in retinal degeneration. J Leukocyte Biol 81: 1345-1351.
53. 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.
54. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT. 2009. Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 50: 4444-4451.
55. Libby RT, Li Y, Savinova OV, Barter J, Smith RS, Nickells RW, John SWM. 2005a. Susceptibility to neurodegeneration in glaucoma is modified by Bax gene dosage. PLos Genet 1: 17-26.
56. Libby RT, Anderson MG, Pang IH, Robinson ZH, Savinova OV, Cosma IM, Snow A, Wilson LA, Smith RS, Clark AF, John SW. 2005b. Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis Neurosci 22: 637-648.
57. Lucin KM, Wyss-Coray T. 2009. Immune activation in brain aging and neurodegeneration: too much or too little? Neuron 64: 110-122.
58. Marnetto F, Hellias B, Granieri L, Frau J, Patanella AK, Nytrova P, Sala A, Capobianco M, Gilli F, Bertolotto A. 2009. Western blot analysis for the detection of serum antibodies recognizing linear aquaporin-4 epitopes in patients with neuromyelitis optica. J Neuroimmunol 217: 74-79.
59. McKinnon SJ, Schlamp CL, Nickells RW. 2009. Mouse models of retinal ganglion cell death and glaucoma. Exp Eye Res 88: 816-824.
60. Mo JS, Anderson MG, Gregory M, Smith RS, Savinova OV, Serreze DV, Ksander R, Streilein JW, John SW. 2003. By altering ocular immune privilege, bone marrow-derived cells pathogenically contribute to DBA/2J pigmentary glaucoma. J Exp Med 197: 1335-1344.
61. Mojumder DK, Sherry DM, Frishman LJ. 2008a. Contribution of voltage-gated sodium channels to the b-wave of the mammalian flash electroretinogram. J Physiol 586: 2551-2580.
62. Mojumder DK, Wensei TG, Frishman LJ. 2008b. Subcellular compartmentalization of two calcium binding proteins, calretinin and calbindin-28kDa, in ganglion and amacrine cells of the rat retina. Mol Vis 14: 1600-1613.
63. Nagelhus EA, Veruki ML, Torp R, Haug F-M, Laake JH, Nielsen S, Agre P, Ottersen OP. 1998. Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Müller cells and fibrous astrocytes. J Neurosci 18: 2506-2519.
64. Naskar R, Wissing M, Thanos S. 2002. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci 43: 2962-2968.
65. Neufeld AH. 1999. Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch Ophthalmol 117: 1050-1056.
66. Neufeld AH, Liu B. 2003. Glaucomatous optic neuropathy: when glia misbehave. Neuroscientist 9: 458-495.
67. Neumann H, Kotter MR, Franklin RJ. 2009. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132: 288-295.
68. Nickells RW. 2007. From ocular hypertension to ganglion cell death: a theoretical sequence of events leading to glaucoma. Can J Ophthalmol 42: 278-287.
69. Nilsson I, Lindfors C, Fetissov SO, Hökfelt T, Johansen JE. 2007. Aberrant agouti-related protein system in the hypothalamus of the anx/anx mouse is associated with activation of microglia. J Comp Neurol 507: 1128-1140.
70. Ohsawa K, Imai Y, Kanazawa H, Sasaki Y, Kohsaka S. 2000. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci 113: 3073-3084.
71. Ohsawa K, Imai Y, Sasaki Y, Kohsaka S. 2004. Microglia/macrophage-specific protein Iba1 binds to fimbrin and enhances its actin-bundling activity. J Neurochem 88: 844-856.
72. Platel J-C, Gordon V, Heintz T, Bordey A. 2009. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 57: 66-79.
73. Poché RA, Furuta Y, Chaboissier MC, Schedl A, Behringer RR. 2008. Sox9 is expressed in mouse multipotent retinal progenitor cells and functions in Müller glial cell development. J Comp Neurol 20: 237-250.
74. Porciatti V, Saleh M, Nagaraju M. 2007. The pattern electroretinogram as a tool to monitor progressive retinal ganglion cell dysfunction in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 48: 745-751.
75. Quigley HA. 1983. Experimental glaucoma damage mechanism. Arch Ophthalmol 101: 1301-1302.
76. Raoul W, Keller N, Rodéro M, Behar-Cohen F, Sennlaub F, Combadière C. 2008. Role of the chemokine receptor CX3CR1 in the mobilization of phagocytic retinal microglial cells. J Neuroimmunol 198: 56-61.
77. Ravichandran KS. 2003. "Recruitment signals" from apoptotic cells: invitation to a quiet meal. Cell 113: 817-820.
78. Reichstein D, Ren L, Filipopoulos T, Mittag T, Danias J. 2007. Apoptotic retinal ganglion cell death in the DBA/2J mouse model of glaucoma. Exp Eye Res 84: 13-21.
79. Ripoll VM, Irvine KM, Ravasi T, Sweet MJ, Hume DA. 2007. Gpnmb is induced in macrophages by IFN-g and lipopolysaccharide an acts as a feedback regulator of proinflammatory responses. J Immunol 178: 6557-6566.
80. Saari JC, Huang J, Possin DE, Fariss RN, Leonard J, Garwin GG, Crabb JW, Milam AH. 1997. Glia. Cellular retinaldehyde-binding protein is expressed by oligodendrocytes in optic nerve and brain. Glia 21: 259-268.
81. Saleh M, Nagaraju M, Porciatti V. 2007. Longitudinal evaluation of retinal ganglion cell function and IOP in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 48: 4564-4572.
82. Santos AM, Calvente R, Tassi M, Carrasco MC, Martín-Oliva D, Martín-Teva JL, Navascués J, Cuadros MA. 2008. Embryonic and postnatal development of microglial cells in the mouse retina. J Comp Neurol 506: 224-239.
83. Saraswathy S, Wu G, Rao NA. 2006. Retinal microglial activation and chemotaxis by docosahexaenoic acid hydroperoxide. Invest Ophthalmol Vis Sci 47: 3656-3663.
84. Sarthy V. 1996. Cellular retinaldehyde-binding protein localization in cornea. Exp Eye Res 63: 759-762.
85. Schlamp CL, Li Y, Dietz JA, Janssen KT, Nickells RW. 2006. Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci 7: 66.
86. Schraermeyer M, Schnichels S, Julien S, Heiduschka P, Bartz-Schmidt K-U, Schraermeyer U. 2009. Ultrastructural analysis of the pigment dispersion syndrome in DBA/2J mice. Graefes Arch Clin Exp Ophthalmol 247: 1493-1504.
87. Schuettauf F, Rejdak R, Walski M, Frontczak-Baniewicz M, Voelker M, Blatsios G, Shinoda K, Zagorski Z, Zrenner E, Grieb P. 2004. Retinal neurodegeneration in the DBA/2J mouse - a model for ocular hypertension. Acta Neuropathol 107: 352-358.
88. Sherry DM, Mitchell R, Standifer KM, du Plessis B. 2006. Distribution of plasma membrane-associated syntaxins 1 through 4 indicates distinct trafficking functions in the synaptic layers of the mouse retina. BMC Neurosci 7: 54-79.
89. Sobrado-Calvo P, Vidal-Sanz M, Villegas-Pérez MP. 2007. Rat retinal microglial cells under normal conditions, after optic nerve section, and optic nerve section and intravitreal injection of trophic factors or macrophage inhibitor factor. J Comp Neurol 501: 866-878.
90. Son JL, Soto I, Oglesby E, Lopez-Roca T, Pease ME, Quigley HA, Marsh-Armstrong N. 2010. Glaucomatous optic nerve injury involves early astrocyte reactivity and late oligodendrocyte loss. Glia 58: 780-789.
91. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson ED, Steele MR, Inman DM, Vetter ML, Horner PJ, Marsh-Armstrong N. 2008. Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci 28: 548-561.
92. Steele MR, Inman DM, Calkins DJ, Horner PJ, Vetter ML. 2006. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest Ophthalmol Vis Sci 47: 977-985.
93. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA. 2007. The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164-1178.
94. Streit WJ. 2005. Microglia and neuroprotection: implications for Alzheimer's disease. Brain Res 48: 234-239.
95. Sun D, Lye-Barthel M, Masland RH, Jakobs TC. 2009. The morphology and spatial arrangement of astrocytes in the optic nerve head of the mouse. J Comp Neurol 516: 1-19.
96. Swanson WH, Felius J, Pan F. 2004. Perimetric defects and ganglion cell damage: interpreting linear relations using a two-stage neural model. Invest Ophthalmol Vis Sci 45: 466-472.
97. Tambuyzer BR, Ponsaerts P, Nouwen ET. 2009. Microglia: gatekeepers of central nervous system immunology. J Leukoc Biol 85: 352-370.
98. Tezel G, Wax MB. 2003. Glial modulation of retinal ganglion cell death in glaucoma. J Glaucoma 12: 63-38.
99. Thanos S. 1991. The relationship of microglial cells to dying neurons during natural neuronal cell death and axotomy-induced degeneration of the rat retina. Eur J Neurosci 3: 1189-1207.
100. Utans U, Arceci RJ, Yamashita Y, Russell ME. 1995. Cloning and characterization of allograft inflammatory fctor-1: a novel macrophage factor identified in rat cardiac allografts with chronic rejection. J Clin Invest 95: 2954-2962.
101. Walter K, Neumann H. 2009. Role of microglia in neuronal degeneration and regeneration. Semin Immunopathol 31: 513-525.
102. Wang X, Tay SS, Ng YK. 2000. An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp Brain Res 132: 476-484.
103. Weber AJ, Kaufman PL, Hubbard WC. 1998. Morphology of single ganglion cells in the glaucomatous primate retina. Invest Ophthalmol Vis Sci 39: 2304-2320.
104. Weishaupt JH, Klöcker N, Bähr M. 2005. Axotomy-induced early down-regulation of POU-IV class transcription factors Brn-3a and Brn-3b in retinal ganglion cells. J Mol Neurosci 26: 17-25.
105. Whitmore AV, Libby RT, SWJohn 2005. Glaucoma: thinking in new ways-a role for autonomous axonal self-destruction and other compartmentalised processes? Prog Retin Eye Res 24: 639-662.
106. Xu H, Chen M, Forrester 2009. Para-inflammation in the ageing retina. Prog Retin Eye Res 28: 348-368.
107. Yuan L, Neufeld AH. 2001. Activated microglia in the human glaucomatous optic nerve head. J Neurosci Res 64: 523-532.
108. Zhang CM, Tso MOM. 2003. Characterization of activated retinal microglia following optic axotomy. J Neurosci Res 73: 840-845.
109. Zhang C, Lam TT, Tso MOM. 2005. Heterogeneous populations of microglia/macrophages in the retina and their activation after retinal ischemia and reperfusion injury. Exp Eye Res 81: 700-709.
110. Zhou X, Li F, Kong L, Tomita H, Li C, Cao W. 2005. Involvement of inflammation, degradation, and apoptosis in a mouse model of glaucoma. J Biol Chem 280: 31240-31248.