The role of astrocytes in optic nerve head fibrosis in glaucoma

Experimental Eye Research

Volumn 142, Issue , 2015, Pages 49-55

  Schneider, Magdalena ^a   Fuchshofer, Rudolf ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Astrocytes; Fibrosis; Glaucoma; Growth factors; Lamina cribrosa; Optic nerve head

Indexed keywords

BONE MORPHOGENETIC PROTEIN; ENDOTHELIN; TRANSFORMING GROWTH FACTOR BETA;

ASTROCYTE; COLLAGEN FIBER; CONNECTIVE TISSUE; ELASTIC FIBER; EXTRACELLULAR MATRIX; FIBROSIS; GLAUCOMA; HUMAN; OPTIC NERVE; OPTIC NERVE HEAD FIBROSIS; PRIORITY JOURNAL; RETINA GANGLION CELL; REVIEW; RISK FACTOR; METABOLISM; OPTIC DISK; PATHOLOGY; PHYSIOLOGY;

ASTROCYTES; BONE MORPHOGENETIC PROTEINS; ENDOTHELINS; EXTRACELLULAR MATRIX; FIBROSIS; GLAUCOMA; HUMANS; OPTIC DISK; TRANSFORMING GROWTH FACTOR BETA;

EID: 84961655195     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.08.014     Document Type: Review

References (95)

1. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Agapova O.A., Kaufman P.L., Lucarelli M.J., Gabelt B.A.T., Hernandez M.R. Differential expression of matrix metalloproteinases in monkey eyes with experimental glaucoma or optic nerve transection. Brain Res. 2003, 967:132-143.
3. Agapova O.A., Ricard C.S., Salvador-Silva M., Hernandez M.R. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia 2001, 33:205-216.
4. Albon J., Purslow P.P., Karwatowski W.S., Easty D.L. Age related compliance of the lamina cribrosa in human eyes. Br. J. Ophthalmol. 2000, 84:318-323.
5. Anderson D.R. Ultrastructure of human and monkey lamina cribrosa and optic nerve head. Arch. Ophthalmol. 1969, 82:800-814.
6. Anderson D.R., Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest. Ophthalmol. 1974, 13:771-783.
7. Bouzier-Sore A.K., Pellerin L. Unraveling the complex metabolic nature of astrocytes. Front Cell Neurosci. 2013, 7:179.
8. Chauhan B.C. Endothelin and its potential role in glaucoma. Can. J. Ophthalmol. 2008, 43:356-360.
9. Chen D., Zhao M., Mundy G.R. Bone morphogenetic proteins. Growth Factors 2004, 22:233-241.
10. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Collaborative Normal-Tension Glaucoma Study Group. Am. J. Ophthalmol. 1998, 126:487-497. Collaborative-Normal-Tension-Glaucoma-Study-Group.
11. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Collaborative Normal-Tension Glaucoma Study Group. Am. J. Ophthalmol. 1998, 126:498-505. Collaborative-Normal-Tension-Glaucoma-Study-Group.
12. Coudrillier B., Tian J., Alexander S., Myers K.M., Quigley H.A., Nguyen T.D. Biomechanics of the human posterior sclera: age- and glaucoma-related changes measured using inflation testing. Investig. Ophthalmol. Vis. Sci. 2012, 53:1714-1728.
13. Fuchshofer R., Birke M., Welge-Lussen U., Kook D., Lutjen-Drecoll E. Transforming growth factor-beta 2 modulated extracellular matrix component expression in cultured human optic nerve head astrocytes. Investig. Ophthalmol. Vis. Sci. 2005, 46:568-578.
14. Fuchshofer R., Yu A.H., Welge-Lussen U., Tamm E.R. Bone morphogenetic protein-7 is an antagonist of transforming growth factor-beta2 in human trabecular meshwork cells. Investig. Ophthalmol. Vis. Sci. 2007, 48:715-726.
15. Fukuchi T., Ueda J., Hanyu T., Abe H., Sawaguchi S. Distribution and expression of transforming growth factor-beta and platelet-derived growth factor in the normal and glaucomatous monkey optic nerve heads. Jpn. J. Ophthalmol. 2001, 45:592-599.
16. Gao X., Cao Y., Staloch D.A., Gonzales M.A., Aronson J.F., Chao C., Hellmich M.R., Ko T.C. Bone morphogenetic protein signaling protects against cerulein-induced pancreatic fibrosis. PLoS One 2014, 9:e89114.
17. Goldbaum M.H., Jeng S.Y., Logemann R., Weinreb R.N. The extracellular matrix of the human optic nerve. Arch. Ophthalmol. 1989, 107:1225-1231.
18. Gordon M.O., Beiser J.A., Brandt J.D., Heuer D.K., Higginbotham E.J., Johnson C.A., Keltner J.L., Miller J.P., Parrish R.K., Wilson M.R., Kass M.A. The Ocular Hypertension Treatment Study: baseline factors that predict the onset of primary open-angle glaucoma. Arch. Ophthalmol. 2002, 120:714-720. discussion 829-730.
19. Hao C., Xie Y., Peng M., Ma L., Zhou Y., Zhang Y., Kang W., Wang J., Bai X., Wang P., Jia Z. Inhibition of connective tissue growth factor suppresses hepatic stellate cell activation in vitro and prevents liver fibrosis in vivo. Clin. Exp. Med. 2014, 14:141-150.
20. He S., Prasanna G., Yorio T. Endothelin-1-Mediated signaling in the expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in astrocytes. Investig. Ophthalmol. Vis. Sci. 2007, 48:3737-3745.
21. Hernandez M.R. Ultrastructural immunocytochemical analysis of elastin in the human lamina cribrosa. Changes in elastic fibers in primary open-angle glaucoma. Investig. Ophthalmol. Vis. Sci. 1992, 33:2891-2903.
22. Hernandez M.R. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog. Retin. Eye Res. 2000, 19:297-321.
23. Hernandez M.R., Agapova O.A., Yang P., Salvador-Silva M., Ricard C.S., Aoi S. Differential gene expression in astrocytes from human normal and glaucomatous optic nerve head analyzed by cDNA microarray. Glia 2002, 38:45-64.
24. Hernandez M.R., Pena J.D. The optic nerve head in glaucomatous optic neuropathy. Arch. Ophthalmol. 1997, 115:389-395.
25. Hernandez M.R., Wang N., Hanley N.M., Neufeld A.H. Localization of collagen types I and IV mRNAs in human optic nerve head by in situ hybridization. Investig. Ophthalmol. Vis. Sci. 1991, 32:2169-2177.
26. Hernandez M.R., Yang J., Ye H. Activation of elastin mRNA expression in human optic nerve heads with primary open-angle glaucoma. J. Glaucoma 1994, 3:214-225.
27. Hernandez M.R., Ye H., Roy S. Collagen type IV gene expression in human optic nerve heads with primary open angle glaucoma. Exp. Eye Res. 1994, 59:41-51.
28. Hildebrand C., Remahl S., Waxman S.G. Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations. J. Neurocytol. 1985, 14:597-617.
29. 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.M. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007, 179:1523-1537.
30. 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.
31. Hsu D.R., Economides A.N., Wang X., Eimon P.M., Harland R.M. The Xenopus dorsalizing factor gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1998, 1:673-683.
32. Izumi M., Masaki M., Hiramoto Y., Sugiyama S., Kuroda T., Terai K., Hori M., Kawase I., Hirota H. Cross-talk between bone morphogenetic protein 2 and leukemia inhibitory factor through ERK 1/2 and Smad1 in protection against doxorubicin-induced injury of cardiomyocytes. J. Mol. Cell. Cardiol. 2006, 40:224-233.
33. Johansson J.O. The lamina cribrosa in the eyes of rats, hamsters, gerbils and guinea pigs. Acta Anat. (Basel) 1987, 128:55-62.
34. Johnson C.A., Keltner J.L., Cello K.E., Edwards M., Kass M.A., Gordon M.O., Budenz D.L., Gaasterland D.E., Werner E. Baseline visual field characteristics in the ocular hypertension treatment study. Ophthalmology 2002, 109:432-437.
35. Johnson E.C., Deppmeier L.M., Wentzien S.K., Hsu I., Morrison J.C. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Investig. Ophthalmol. Vis. Sci. 2000, 41:431-442.
36. Johnson E.C., Jia L., Cepurna W.O., Doser T.A., Morrison J.C. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Investig. Ophthalmol. Vis. Sci. 2007, 48:3161-3177.
37. Junglas B., Kuespert S., Seleem A.A., Struller T., Ullmann S., Bosl M., BosserhoffA., Kostler J., Wagner R., Tamm E.R., Fuchshofer R. Connective tissue growth factor causes glaucoma by modifying the actin cytoskeleton of the trabecular meshwork. Am. J. Pathol. 2012, 180:2386-2403.
38. Kirsch M., Schneider T., Lee M.Y., Hofmann H.D. Lesion-induced changes in the expression of ciliary neurotrophic factor and its receptor in rat optic nerve. Glia 1998, 23:239-248.
39. Kobayashi S., Vidal I., Pena J.D., Hernandez M.R. Expression of neural cell adhesion molecule (NCAM) characterizes a subpopulation of type 1 astrocytes in human optic nerve head. Glia 1997, 20:262-273.
40. Kompass K.S., Agapova O.A., Li W., Kaufman P.L., Rasmussen C.A., Hernandez M.R. Bioinformatic and statistical analysis of the optic nerve head in a primate model of ocular hypertension. BMC Neurosci. 2008, 9:93.
41. Lam T.T., Kwong J.M., Tso M.O. Early glial responses after acute elevated intraocular pressure in rats. Investig. Ophthalmol. Vis. Sci. 2003, 44:638-645.
42. Leske M.C., Heijl A., Hussein M., Bengtsson B., Hyman L., KomaroffE. Factors for glaucoma progression and the effect of treatment: the early manifest glaucoma trial. Arch. Ophthalmol. 2003, 121:48-56. Early Manifest Glaucoma Trial, G.
43. Lukas T.J., Miao H., Chen L., Riordan S.M., Li W., Crabb A.M., Wise A., Du P., Lin S.M., Hernandez M.R. Susceptibility to glaucoma: differential comparison of the astrocyte transcriptome from glaucomatous African American and Caucasian American donors. Genome Biol. 2008, 9:R111.
44. Lye-Barthel M., Sun D., Jakobs T.C. Morphology of astrocytes in a glaucomatous optic nerve. Investig. Opthalmol. Vis. Sci. 2013, 54:909.
45. MacCumber M.W., Ross C.A., Glaser B.M., Snyder S.H. Endothelin: visualization of mRNAs by in situ hybridization provides evidence for local action. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:7285-7289.
46. May C.A. The optic nerve head region of the aged rat: an immunohistochemical investigation. Curr. Eye Res. 2003, 26:347-354.
47. May C.A., Lutjen-Drecoll E. Morphology of the murine optic nerve. Investig. Ophthalmol. Vis. Sci. 2002, 43:2206-2212.
48. Minton A.Z., Phatak N.R., Stankowska D.L., He S., Ma H.Y., Mueller B.H., Jiang M., Luedtke R., Yang S., Brownlee C., Krishnamoorthy R.R. Endothelin B receptors contribute to retinal ganglion cell loss in a rat model of glaucoma. PLoS One 2012, 7:e43199.
49. Morrison J., Farrell S., Johnson E., Deppmeier L., Moore C.G., Grossmann E. Structure and composition of the rodent lamina cribrosa. Exp. Eye Res. 1995, 60:127-135.
50. Morrison J.C., Jerdan J.A., Dorman M.E., Quigley H.A. Structural proteins of the neonatal and adult lamina cribrosa. Arch. Ophthalmol. 1989, 107:1220-1224.
51. Morrison J.C., L'Hernault N.L., Jerdan J.A., Quigley H.A. Ultrastructural location of extracellular matrix components in the optic nerve head. Arch. Ophthalmol. 1989, 107:123-129.
52. Netland P.A., Ye H., Streeten B.W., Hernandez M.R. Elastosis of the lamina cribrosa in pseudoexfoliation syndrome with glaucoma. Ophthalmology 1995, 102:878-886.
53. Neumann C., Yu A., Welge-Lussen U., Lutjen-Drecoll E., Birke M. The effect of TGF- 2 on elastin, Type VI collagen, and components of the proteolytic degradation system in human optic nerve astrocytes. Investig. Ophthalmol. Vis. Sci. 2008, 49:1464-1472.
54. Nguyen T.Q., Tarnow L., Jorsal A., Oliver N., Roestenberg P., Ito Y., Parving H.H., Rossing P., van Nieuwenhoven F.A., Goldschmeding R. Plasma connective tissue growth factor is an independent predictor of end-stage renal disease and mortality in type 1 diabetic nephropathy. Diabetes Care 2008, 31:1177-1182.
55. Oberheim N.A., Takano T., Han X., He W., Lin J.H., Wang F., Xu Q., Wyatt J.D., Pilcher W., Ojemann J.G., Ransom B.R., Goldman S.A., Nedergaard M. Uniquely hominid features of adult human astrocytes. J. Neurosci. 2009, 29:3276-3287.
56. Pena J.D., Netland P.A., Vidal I., Dorr D.A., Rasky A., Hernandez M.R. Elastosis of the lamina cribrosa in glaucomatous optic neuropathy. Exp. Eye Res. 1998, 67:517-524.
57. Pena J.D., Taylor A.W., Ricard C.S., Vidal I., Hernandez M.R. Transforming growth factor beta isoforms in human optic nerve heads. Br. J. Ophthalmol. 1999, 83:209-218.
58. Pena J.D., Varela H.J., Ricard C.S., Hernandez M.R. Enhanced tenascin expression associated with reactive astrocytes in human optic nerve heads with primary open angle glaucoma. Exp. Eye Res. 1999, 68:29-40.
59. Pohlers D., Brenmoehl J., Loffler I., Muller C.K., Leipner C., Schultze-Mosgau S., Stallmach A., Kinne R.W., Wolf G. TGF-beta and fibrosis in different organs - molecular pathway imprints. Biochim. Biophys. Acta 2009, 1792:746-756.
60. Prasanna G., Hulet C., Desai D., Krishnamoorthy R.R., Narayan S., Brun A.M., Suburo A.M., Yorio T. Effect of elevated intraocular pressure on endothelin-1 in a rat model of glaucoma. Pharmacol. Res. 2005, 51:41-50.
61. Prasanna G., Krishnamoorthy R., Clark A.F., Wordinger R.J., Yorio T. Human optic nerve head astrocytes as a target for endothelin-1. Investig. Ophthalmol. Vis. Sci. 2002, 43:2704-2713.
62. Prasanna G., Krishnamoorthy R., Yorio T. Endothelin, astrocytes and glaucoma. Exp. Eye Res. 2011, 93:170-177.
63. Qu J., Jakobs T.C. The time course of gene expression during reactive gliosis in the optic nerve. PLoS One 2013, 8:e67094.
64. Quigley H.A. Number of people with glaucoma worldwide. Br. J. Ophthalmol. 1996, 80:389-393.
65. Quigley H.A. Recognizing structural damage to the optic nerve head and nerve fiber layer in glaucoma. Am. J. Ophthalmol. 1998, 125:564-565. 563; author reply.
66. Quigley H.A. Glaucoma. Lancet 2011, 377:1367-1377.
67. Quigley H.A., Brown A., Dorman-Pease M.E. Alterations in elastin of the optic nerve head in human and experimental glaucoma. Br. J. Ophthalmol. 1991, 75:552-557.
68. Quigley H.A., Dorman-Pease M.E., Brown A.E. Quantitative study of collagen and elastin of the optic nerve head and sclera in human and experimental monkey glaucoma. Curr. Eye Res. 1991, 10:877-888.
69. Quigley H.A., Hohman R.M., Addicks E.M., Massof R.W., Green W.R. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am. J. Ophthalmol. 1983, 95:673-691.
70. Ransom B., Behar T., Nedergaard M. New roles for astrocytes (stars at last). Trends Neurosci. 2003, 26:520-522.
71. Rao V.R., Krishnamoorthy R.R., Yorio T. Endothelin-1 mediated regulation of extracellular matrix collagens in cells of human lamina cribrosa. Exp. Eye Res. 2008, 86:886-894.
72. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 1997, 20:570-577.
73. Ripodas A., de Juan J.A., Roldan-Pallares M., Bernal R., Moya J., Chao M., Lopez A., Fernandez-Cruz A., Fernandez-Durango R. Localisation of endothelin-1 mRNA expression and immunoreactivity in the retina and optic nerve from human and porcine eye. Evidence for endothelin-1 expression in astrocytes. Brain Res. 2001, 912:137-143.
74. Riser B.L., Denichilo M., Cortes P., Baker C., Grondin J.M., Yee J., Narins R.G. Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis. J. Am. Soc. Nephrol. 2000, 11:25-38.
75. Rogers R.S., Dharsee M., Ackloo S., Sivak J.M., Flanagan J.G. Proteomics analyses of human optic nerve head astrocytes following biomechanical strain. Mol. Cell Proteomics 2012, 11. M111 012302.
76. Schwab J.M., Postler E., Nguyen T.D., Mittelbronn M., Meyermann R., Schluesener H.J. Connective tissue growth factor is expressed by a subset of reactive astrocytes in human cerebral infarction. Neuropathol. Appl. Neurobiol. 2000, 26:434-440.
77. Son J.L., Soto I., Oglesby E., Lopez-Roca T., Pease M.E., Quigley H.A., Marsh-Armstrong N. Glaucomatous optic nerve injury involves early astrocyte reactivity and late oligodendrocyte loss. Glia 2010, 58:780-789.
78. Stockli K.A., Lottspeich F., Sendtner M., Masiakowski P., Carroll P., Gotz R., Lindholm D., Thoenen H. Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 1989, 342:920-923.
79. Sun D., Lye-Barthel M., Masland R.H., Jakobs T.C. The morphology and spatial arrangement of astrocytes in the optic nerve head of the mouse. J. Comp. Neurol. 2009, 516:1-19.
80. Sun D., Lye-Barthel M., Masland R.H., Jakobs T.C. Structural remodeling of fibrous astrocytes after axonal injury. J. Neurosci. 2010, 30:14008-14019.
81. Sun D., Qu J., Jakobs T.C. Reversible reactivity by optic nerve astrocytes. Glia 2013, 61:1218-1235.
82. Tektas O.Y., Lutjen-Drecoll E., Scholz M. Qualitative and quantitative morphologic changes in the vasculature and extracellular matrix of the prelaminar optic nerve head in eyes with POAG. Investig. Ophthalmol. Vis. Sci. 2010, 51:5083-5091.
83. Tonari M., Kurimoto T., Horie T., Sugiyama T., Ikeda T., Oku H. Blocking endothelin-B receptors rescues retinal ganglion cells from optic nerve injury through suppression of neuroinflammation. Investig. Ophthalmol. Vis. Sci. 2012, 53:3490-3500.
84. Varela H.J., Hernandez M.R. Astrocyte responses in human optic nerve head with primary open-angle glaucoma. J. Glaucoma 1997, 6:303-313.
85. Wang L., CioffiG.A., Cull G., Dong J., Fortune B. Immunohistologic evidence for retinal glial cell changes in human glaucoma. Investig. Ophthalmol. Vis. Sci. 2002, 43:1088-1094.
86. Wang L., Fortune B., Cull G., Dong J., CioffiG.A. Endothelin B receptor in human glaucoma and experimentally induced optic nerve damage. Arch. Ophthalmol. 2006, 124:717-724.
87. Wordinger R.J., Agarwal R., Talati M., Fuller J., Lambert W., Clark A.F. Expression of bone morphogenetic proteins (BMP), BMP receptors, and BMP associated proteins in human trabecular meshwork and optic nerve head cells and tissues. Mol. Vis. 2002, 8:241-250.
88. Wordinger R.J., Fleenor D.L., Hellberg P.E., Pang I.H., Tovar T.O., Zode G.S., Fuller J.A., Clark A.F. Effects of TGF- 2, BMP-4, and gremlin in the trabecular Meshwork: Implications for glaucoma. Investig. Ophthalmol. Vis. Sci. 2007, 48:1191-1200.
89. Yan X., Tezel G., Wax M.B., Edward D.P. Matrix metalloproteinases and tumor necrosis factor alpha in glaucomatous optic nerve head. Arch. Ophthalmol. 2000, 118:666-673.
90. Yang Z., Sun Z., Liu H., Ren Y., Shao D., Zhang W., Lin J., Wolfram J., Wang F., Nie S. Connective tissue growth factor stimulates the proliferation, migration and differentiation of lung fibroblasts during paraquat-induced pulmonary fibrosis. Mol. Med. Rep. 2015, 12:1091-1097.
91. Ye H., Hernandez M.R. Heterogeneity of astrocytes in human optic nerve head. J. Comp. Neurol. 1995, 362:441-452.
92. Zeisberg M., Bottiglio C., Kumar N., Maeshima Y., Strutz F., Muller G.A., Kalluri R. Bone morphogenic protein-7 inhibits progression of chronic renal fibrosis associated with two genetic mouse models. Am. J. Physiol. Ren. Physiol. 2003, 285:F1060-F1067.
93. Zode G.S., Clark A.F., Wordinger R.J. Activation of the BMP canonical signaling pathway in human optic nerve head tissue and isolated optic nerve head astrocytes and lamina cribrosa cells. Investig. Ophthalmol. Vis. Sci. 2007, 48:5058-5067.
94. Zode G.S., Clark A.F., Wordinger R.J. Bone morphogenetic protein 4 inhibits TGF-β2 stimulation of extracellular matrix proteins in optic nerve head cells: role of gremlin in ECM modulation. Glia 2009, 57:755-766.
95. Zode G.S., Sethi A., Brun-Zinkernagel A.M., Chang I.F., Clark A.F., Wordinger R.J. Transforming growth factor-beta2 increases extracellular matrix proteins in optic nerve head cells via activation of the Smad signaling pathway. Mol. Vis. 2011, 17:1745-1758.