IOP induces upregulation of GFAP and MHC-II and microglia reactivity in mice retina contralateral to experimental glaucoma

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Gallego, Beatriz I ^a   Salazar, Juan J ^a   de Hoz, Rosa ^a   Rojas, Blanca ^a   Ramírez, Ana I ^a   Salinas Navarro, Manuel ^b   Ortín Martínez, Arturo ^b   Valiente Soriano, Francisco J ^b   Avilés Trigueros, Marcelino ^b   Villegas Perez, Maria P ^b   Vidal Sanz, Manuel ^b   Triviño, Alberto ^a   Ramírez, Jose M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

Astrocytes; Experimental glaucoma; GFAP; MHC II; Mice; Microglia; M ller cell; Retina

Indexed keywords

ADAPTOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IONIZED CALCIUM BINDING ADAPTOR MOLECULE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NEUROFILAMENT 200 PROTEIN; NEUROFILAMENT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL POPULATION; CONTROLLED STUDY; EXPERIMENTAL MOUSE; GLAUCOMA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTRAOCULAR HYPERTENSION; INTRAOCULAR PRESSURE; MALE; MICROGLIA; MOUSE; MUELLER CELL; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; QUANTITATIVE STUDY; RETINA DEGENERATION; RETINA GANGLION CELL; UPREGULATION;

EID: 84860815301     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-92     Document Type: Article

References (85)

1. Quigley HA, Green WR. The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. Ophthalmology 1979, 86:1803-1830.
2. Quigley HA, Addicks EM, Green WR, Maumenee AE. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol 1981, 99:635-649. 10.1001/archopht.1981.03930010635009, 6164357.
3. Quigley HA, Dunkelberger GR, Green WR. Chronic human glaucoma causing selectively greater loss of large optic nerve fibers. Ophthalmology 1988, 95:357-363.
4. Quigley HA, Dunkelberger GR, Green WR. Retinal ganglion cell atrophy correlated with automated perimetry in human eyes with glaucoma. Am J Ophthalmol 1989, 107:453-464. 10.1001/archopht.1989.01070010463046, 2712129.
5. Quigley HA. Selective citation of evidence regarding photoreceptor loss in glaucoma. Arch Ophthalmol 2001, 119:1390-1391. 10.1001/archopht.119.9.1390, 11545654.
6. Kerrigan-Baumrind LA, Quigley HA, Pease ME, Kerrigan DF, Mitchell RS. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest Ophthalmol Vis Sci 2000, 41:741-748.
7. Nork TM, Ver Hoeve JN, Poulsen GL, Nickells RW, Davis MD, Weber AJ, Vaegan, Sarks SH, Lemley HL, Millecchia LL. Swelling and loss of photoreceptors in chronic human and experimental glaucomas. Arch Ophthalmol 2000, 118:235-245. 10.1001/archopht.118.2.235, 10676789.
8. Johnson EC, Morrison JC. Friend or foe? Resolving the impact of glial responses in glaucoma. J Glaucoma 2009, 18:341-353. 10.1097/IJG.0b013e31818c6ef6, 2697444, 19525723.
9. Hernandez MR, Miao H, Lukas T. Astrocytes in glaucomatous optic neuropathy. Prog Brain Res 2008, 173:353-373.
10. Tezel G, . the Fourth ARVO/Pfizer Ophthalmics Research Institute Conference Working Group The role of glia, mitochondria, and the immune system in glaucoma. Invest Ophthalmol Vis Sci 2009, 50:1001-1012. the Fourth ARVO/Pfizer Ophthalmics Research Institute Conference Working Group.
11. Prasanna G, Krishnamoorthy R, Yorio T. Endothelin, astrocytes and glaucoma. Exp Eye Res 2011, 93:170-177. 10.1016/j.exer.2010.09.006, 3046320, 20849847.
12. Newman EA. A dialogue between glia and neurons in the retina: modulation of neuronal excitability. Neuron Glia Biol 2004, 1:245-252. 2367255, 18458754.
13. Ramírez JM, Triviño A, Ramírez AI, Salazar JJ, Garcia-Sanchez J. Structural specializations of human retinal glial cells. Vision Res 1996, 36:2029-2036. 10.1016/0042-6989(95)00322-3, 8776469.
14. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A. Muller cells in the healthy and diseased retina. Prog Retin Eye Res 2006, 25:397-424. 10.1016/j.preteyeres.2006.05.003, 16839797.
15. Kumpulainen T, Dahl D, Korhonen LK, Nystrom SH. Immunolabeling of carbonic anhydrase isoenzyme C and glial fibrillary acidic protein in paraffin-embedded tissue sections of human brain and retina. J Histochem Cytochem 1983, 31:879-886. 10.1177/31.7.6406590, 6406590.
16. Sofroniew M, Vinters H. Astrocytes: biology and pathology. Acta Neuropathol 2010, 119:7-35. 10.1007/s00401-009-0619-8, 2799634, 20012068.
17. Kimelberg HK, Nedergaard M. Functions of astrocytes and their potential as therapeutic targets. Neurotherapeutics 2010, 7:338-353. 10.1016/j.nurt.2010.07.006, 2982258, 20880499.
18. Nag S. Morphology and properties of astrocytes. Methods Mol Biol 2011, 686:69-100. 10.1007/978-1-60761-938-3_3, 21082367.
19. Tout S, Chan-Ling T, Hollander H, Stone J. The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 1993, 55:291-301. 10.1016/0306-4522(93)90473-S, 8350991.
20. Bosco A, Steele MR, Vetter ML. Early microglia activation in a mouse model of chronic glaucoma. J Comp Neurol 2011, 519:599-620. 10.1002/cne.22516, 21246546.
21. Varela HJ, Hernandez MR. Astrocyte responses in human optic nerve head with primary open-angle glaucoma. J Glaucoma 1997, 6:303-313.
22. Asahara H, Taniwaki T, Ohyagi Y, Yamada T, Kira J. Glutamate enhances phosphorylation of neurofilaments in cerebellar granule cell culture. J Neurol Sci 1999, 171:84-87. 10.1016/S0022-510X(99)00256-7, 10581372.
23. Ackerley S, Grierson AJ, Brownlees J, Thornhill P, Anderton BH, Leigh PN, Shaw CE, Miller CC. Glutamate slows axonal transport of neurofilaments in transfected neurons. J Cell Biol 2000, 150:165-176. 10.1083/jcb.150.1.165, 2185569, 10893265.
24. Julien JP, Mushynski WE. Neurofilaments in health and disease. Prog Nucleic Acid Res Mol Biol 1998, 61:1-23.
25. Di Polo A, Aigner LJ, Dunn RJ, Bray GM, Aguayo AJ. Prolonged delivery of brain-derived neurotrophic factor by adenovirus-infected Muller cells temporarily rescues injured retinal ganglion cells. Proc Natl Acad Sci U S A 1998, 95:3978-3983. 10.1073/pnas.95.7.3978, 19948, 9520478.
26. Dreyer EB, Zurakowski D, Schumer RA, Podos SM, Lipton SA. Elevated glutamate levels in the vitreous body of humans and monkeys with glaucoma. Arch Ophthalmol 1996, 114:299-305. 10.1001/archopht.1996.01100130295012, 8600890.
27. Kawasaki A, Otori Y, Barnstable CJ. Muller cell protection of rat retinal ganglion cells from glutamate and nitric oxide neurotoxicity. Invest Ophthalmol Vis Sci 2000, 41:3444-3450.
28. Wang L, Cioffi GA, Cull G, Dong J, Fortune B. Immunohistologic evidence for retinal glial cell changes in human glaucoma. Invest Ophthalmol Vis Sci 2002, 43:1088-1094.
29. Johnson EC, Jia L, Cepurna WO, Doser TA, Morrison JC. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Invest Ophthalmol Vis Sci 2007, 48:3161-3177. 10.1167/iovs.06-1282, 1950563, 17591886.
30. Wang X, Ng YK, Tay SS. Factors contributing to neuronal degeneration in retinas of experimental glaucomatous rats. J Neurosci Res 2005, 82:674-689. 10.1002/jnr.20679, 16273539.
31. Tezel G, Wax MB. Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci 2000, 20:8693-8700.
32. Dahl D, Björklund H, Bignami A. Immunological markers in astrocytes. Astrocytes: Cell Biology and Pathology of Astrocytes. Volume III 1986, 1-25. Academic, London, Federoff S, Vernadakis A.
33. Drager UC, Hofbauer A. Antibodies to heavy neurofilament subunit detect a subpopulation of damaged ganglion cells in retina. Nature 1984, 309:624-626. 10.1038/309624a0, 6203041.
34. Inman DM, Horner PJ. Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 2007, 55:942-953. 10.1002/glia.20516, 17457855.
35. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S. 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 1996, 224:855-862. 10.1006/bbrc.1996.1112, 8713135.
36. Kaneko H, Nishiguchi KM, Nakamura M, Kachi S, Terasaki H. Characteristics of bone marrow-derived microglia in the normal and injured retina. Invest Ophthalmol Vis Sci 2008, 49:4162-4168. 10.1167/iovs.08-1738, 18487364.
37. Danias J, Kontiola AI, Filippopoulos T, Mittag T. Method for the noninvasive measurement of intraocular pressure in mice. Invest Ophthalmol Vis Sci 2003, 44:1138-1141. 10.1167/iovs.02-0553, 12601041.
38. Aihara M, Lindsey JD, Weinreb RN. Twenty-four-hour pattern of mouse intraocular pressure. Exp Eye Res 2003, 77:681-686. 10.1016/j.exer.2003.08.011, 14609556.
39. Drouyer E, Dkhissi-Benyahya O, Chiquet C, WoldeMussie E, Ruiz G, Wheeler LA, Denis P, Cooper HM. Glaucoma alters the circadian timing system. PLoS One 2008, 3:e3931. 10.1371/journal.pone.0003931, 2592693, 19079596.
40. Salinas-Navarro M, Alarcon-Martinez L, Valiente-Soriano FJ, Ortin-Martinez A, Jimenez-Lopez M, Aviles-Trigueros M, Villegas-Perez MP, de la Villa P, Vidal-Sanz M. Functional and morphological effects of laser-induced ocular hypertension in retinas of adult albino Swiss mice. Mol Vis 2009, 15:2578-2598. 2790482, 20011633.
41. Ramírez JM, Triviño A, Ramírez AI, Salazar JJ, Garcia-Sanchez J. Immunohistochemical study of human retinal astroglia. Vision Res 1994, 34:1935-1946. 10.1016/0042-6989(94)90024-8, 7941395.
42. Triviño A, de Hoz R, Salazar JJ, Ramirez AI, Rojas B, Ramirez JM. Distribution and organization of the nerve fiber and ganglion cells of the human choroid. Anat Embryol (Berl) 2002, 205:417-430.
43. Ramirez AI, Salazar JJ, de Hoz R, Rojas B, Gallego BI, Salinas-Navarro M, Alarcon-Martinez L, Ortin-Martinez A, Aviles-Trigueros M, Vidal-Sanz M, Trivino A, Ramirez JM. Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma. Invest Ophthalmol Vis Sci 2010, 51:5690-5696. 10.1167/iovs.10-5248, 20538983.
44. McKinnon SJ, Schlamp CL, Nickells RW. Mouse models of retinal ganglion cell death and glaucoma. Exp Eye Res 2009, 88:816-824. 10.1016/j.exer.2008.12.002, 3056071, 19105954.
45. Kanamori A, Nakamura M, Nakanishi Y, Yamada Y, Negi A. Long-term glial reactivity in rat retinas ipsilateral and contralateral to experimental glaucoma. Exp Eye Res 2005, 81:48-56. 10.1016/j.exer.2005.01.012, 15978254.
46. Rungger-Brandle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci 2000, 41:1971-1980.
47. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. Invest Ophthalmol Vis Sci 2000, 41:3561-3568.
48. Xue LP, Lu J, Cao Q, Hu S, Ding P, Ling EA. Müller glial cells express nestin coupled with glial fibrillary acidic protein in experimentally induced glaucoma in the rat retina. Neuroscience 2006, 139:723-732. 10.1016/j.neuroscience.2005.12.032, 16458441.
49. Hernandez MR. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retin Eye Res 2000, 19:297-321. 10.1016/S1350-9462(99)00017-8, 10749379.
50. Ramírez JM, Ramírez AI, Salazar JJ, de Hoz R, Triviño A. Changes of astrocytes in retinal ageing and age-related macular degeneration. Exp Eye Res 2001, 73:601-615. 10.1006/exer.2001.1061, 11747361.
51. Reichenbach A, Bringmann A. Müller cells in the diseased retina. Müller Cells in the Healthy and Diseased Retina 2010, 215. Springer, New York, Reichenbach A, Bringmann A.
52. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol 2011, 93:421-443. 10.1016/j.pneurobio.2011.01.005, 21219963.
53. Perez-Alvarez MJ, Isiegas C, Santano C, Salazar JJ, Ramírez AI, Triviño A, Ramírez JM, Albar JP, de la Rosa EJ, Prada C. Vimentin isoform expression in the human retina characterized with the monoclonal antibody 3CB2. J Neurosci Res 2008, 86:1871-1883. 10.1002/jnr.21623, 18241054.
54. Lorber B, Guidi A, Fawcett JW, Martin KR. Activated retinal glia mediated axon regeneration in experimental glaucoma. Neurobiol Dis 2012, 45:243-252. 10.1016/j.nbd.2011.08.008, 21867754.
55. Bolz S, Schuettauf F, Fries JE, Thaler S, Reichenbach A, Pannicke T. K(+) currents fail to change in reactive retinal glial cells in a mouse model of glaucoma. Graefes Arch Clin Exp Ophthalmol 2008, 246:1249-1254. 10.1007/s00417-008-0872-x, 18546005.
56. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson ED, Steele MR, Inman DM, Vetter ML, Horner PJ, 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. 10.1523/JNEUROSCI.3714-07.2008, 18184797.
57. Bizzi A, Schaetzle B, Patton A, Gambetti P, Autilio-Gambetti L. Axonal transport of two major components of the ubiquitin system: free ubiquitin and ubiquitin carboxyl-terminal hydrolase PGP 9.5. Brain Res 1991, 548:292-299. 10.1016/0006-8993(91)91135-N, 1714333.
58. Mabuchi F, Aihara M, Mackey MR, Lindsey JD, Weinreb RN. Regional optic nerve damage in experimental mouse glaucoma. Invest Ophthalmol Vis Sci 2004, 45:4352-4358. 10.1167/iovs.04-0355, 15557443.
59. Pease ME, McKinnon SJ, Quigley HA, Kerrigan-Baumrind LA, Zack DJ. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest Ophthalmol Vis Sci 2000, 41:764-774.
60. Quigley HA, Anderson DR. Distribution of axonal transport blockade by acute intraocular pressure elevation in the primate optic nerve head. Invest Ophthalmol Vis Sci 1977, 16:640-644.
61. Minckler DS, Tso MO, Zimmerman LE. A light microscopic, autoradiographic study of axoplasmic transport in the optic nerve head during ocular hypotony, increased intraocular pressure, and papilledema. Am J Ophthalmol 1976, 82:741-757.
62. Anderson DR, Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest Ophthalmol Vis Sci 1974, 13:771-783.
63. Lee MK, Cleveland DW. Neuronal intermediate filaments. Annu Rev Neurosci 1996, 19:187-217. 10.1146/annurev.ne.19.030196.001155, 8833441.
64. Nixon RA, Sihag RK. Neurofilament phosphorylation: a new look at regulation and function. Trends Neurosci 1991, 14:501-506. 10.1016/0166-2236(91)90062-Y, 1726767.
65. Pant HC, Veeranna. Neurofilament phosphorylation. Biochem Cell Biol 1995, 73:575-592. 10.1139/o95-063, 8714676.
66. Kashiwagi K, Ou B, Nakamura S, Tanaka Y, Suzuki M, Tsukahara S. Increase in dephosphorylation of the heavy neurofilament subunit in the monkey chronic glaucoma model. Invest Ophthalmol Vis Sci 2003, 44:154-159. 10.1167/iovs.02-0398, 12506068.
67. Morrison JC, Cepurna Ying Guo WO, Johnson EC. Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma. Exp Eye Res 2011, 93:156-164. 10.1016/j.exer.2010.08.005, 3010442, 20708000.
68. Dibas A, Yang MH, He S, Bobich J, Yorio T. Changes in ocular aquaporin-4 (AQP4) expression following retinal injury. Mol Vis 2008, 14:1770-1783. 2559817, 18836575.
69. Dahlmann B. Role of proteasomes in disease. BMC Biochem 2007, 8(Suppl 1):S3. 10.1186/1471-2091-8-S1-S3, 2106367, 18047740.
70. Conforti L, Adalbert R, Coleman MP. Neuronal death: where does the end begin?. Trends Neurosci 2007, 30:159-166. 10.1016/j.tins.2007.02.004, 17339056.
71. Schlamp CL, Li Y, Dietz JA, Janssen KT, Nickells RW. Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci 2006, 7:66. 10.1186/1471-2202-7-66, 1621073, 17018142.
72. Buckingham BP, Inman DM, Lambert W, Oglesby E, Calkins DJ, Steele MR, Vetter ML, Marsh-Armstrong N, Horner PJ. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci 2008, 28:2735-2744. 10.1523/JNEUROSCI.4443-07.2008, 18337403.
73. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci U S A 2010, 107:5196-5201. 10.1073/pnas.0913141107, 2841892, 20194762.
74. 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. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J Cell Biol 2007, 179:1523-1537. 10.1083/jcb.200706181, 2373494, 18158332.
75. Whitmore AV, Libby RT, John SW. Glaucoma: thinking in new ways-a role for autonomous axonal self-destruction and other compartmentalised processes?. Prog Retin Eye Res 2005, 24:639-662. 10.1016/j.preteyeres.2005.04.004, 15953750.
76. Fu CT, Sretavan D. Laser-induced ocular hypertension in Albino CD-1 Mice. Invest Ophthalmol Vis Sci 2010, 51:980-990. 10.1167/iovs.09-4324, 2868470, 19815738.
77. Soto I, Pease ME, Son JL, Shi X, Quigley HA, Marsh-Armstrong N. Retinal ganglion cell loss in a rat ocular hypertension model is sectorial and involves early optic nerve axon loss. Invest Ophthalmol Vis Sci 2011, 52:434-441. 10.1167/iovs.10-5856, 3053289, 20811062.
78. Steele MR, Inman DM, Calkins DJ, Horner PJ, Vetter ML. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest Ophthalmol Vis Sci 2006, 47:977-985. 10.1167/iovs.05-0865, 16505032.
79. Yang J, Yang P, Tezel G, Patil RV, Hernandez MR, Wax MB. Induction of HLA-DR expression in human lamina cribrosa astrocytes by cytokines and simulated ischemia. Invest Ophthalmol Vis Sci 2001, 42:365-371.
80. Tezel G, Chauhan BC, LeBlanc RP, Wax MB. Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest Ophthalmol Vis Sci 2003, 44:3025-3033.
81. Neufeld AH. Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch Ophthalmol 1999, 117:1050-1056. 10.1001/archopht.117.8.1050, 10448748.
82. Wang X, Tay SS, Ng YK. An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp Brain Res 2000, 132:476-484. 10.1007/s002210000360, 10912828.
83. Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci 2002, 43:2962-2968.
84. Fan W, Li X, Wang W, Mo JS, Kaplan H, Cooper NG. Early involvement of immune/inflammatory response genes in retinal degeneration in DBA/2J Mice. Ophthalmol Eye Dis 2010, 1:23-41. 2845995, 20352036.
85. Shao H, Kaplan HJ, Sun D. Major histocompatibility complex molecules on parenchymal cells of the target organ protect against autoimmune disease. Chem Immunol Allergy 2007, 92:94-104. 2951609, 17264486.