Regeneration of retinal ganglion cell axons in organ culture is increased in rats with hereditary buphthalmos

Experimental Eye Research

Volumn 85, Issue 1, 2007, Pages 90-104

  Lasseck, Julia ^a,b   Schröer, Uwe ^a   Koenig, Simone ^b   Thanos, Solon ^a,b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

buphthalmos; mass spectrometry; organ culture; rat; regeneration

Indexed keywords

ENDOTHELIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 60; NEUROMODULIN; PROTEIN ANTIBODY; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BUPHTHALMOS; CELL LABELING; CONTROLLED STUDY; DISEASE COURSE; DISEASE DURATION; DISEASE SEVERITY; INTRAOCULAR HYPERTENSION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEURITE; NEUROPROTECTION; NONHUMAN; OPTIC NERVE DISEASE; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; RETINA GANGLION CELL;

ANIMALS; AXONS; BLOTTING, WESTERN; CELL COUNT; CHAPERONIN 60; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOTHELIN-1; GAP-43 PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HYDROPHTHALMOS; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; NERVE DEGENERATION; NERVE REGENERATION; ORGAN CULTURE TECHNIQUES; PEPTIDES; RATS; RATS, MUTANT STRAINS; RETINAL GANGLION CELLS; RHODOPSIN;

EID: 34347387766     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2007.03.005     Document Type: Article

References (66)

1. Addison W.H.F., and How H.W. Congenital hypertrophy of the eye of an albino rat. Anat. Rec. (1926) 271-274
2. Bahr M., Vanselow J., and Thanos S. In vitro regeneration of adult rat ganglion cell axons from retinal explants. Exp. Brain Res. 2 (1988) 393-401
3. Benowitz L.I., and Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 2 (1997) 84-91
4. Bodeutsch N., Siebert H., Dermon C., and Thanos S. Unilateral injury to the adult rat optic nerve causes multiple cellular responses in the contralateral site. J. Neurobiol. 1 (1999) 116-128
5. Bunt-Milam A.H., Dennis Jr. M.B., and Bensinger R.E. Optic nerve head axonal transport in rabbits with hereditary glaucoma. Exp. Eye Res. 4 (1987) 537-551
6. Chang B., Smith R.S., Hawes N.L., Anderson M.G., Zabaleta A., Savinova O., Roderick T.H., Heckenlively J.R., Davisson M.T., and John S.W. Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice. Nat. Genet. 4 (1999) 405-409
7. Dreyer E.B. A proposed role for excitotoxicity in glaucoma. J. Glaucoma 1 (1998) 62-67
8. Ekstrom P., Sanyal S., Narfstrom K., Chader G.J., and van Veen T. Accumulation of glial fibrillary acidic protein in Muller radial glia during retinal degeneration. Invest. Ophthalmol. Vis. Sci. 9 (1988) 1363-1371
9. Ellis R.J. The molecular chaperone concept. Semin. Cell Biol. 1 (1990) 1-9
10. Fischer D., Pavlidis M., and Thanos S. Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest. Ophthalmol. Vis. Sci. 12 (2000) 3943-3954
11. Ford-Holevinski T.S., Dahlberg T.A., and Agranoff B.W. A microcomputer-based image analyzer for quantitating neurite outgrowth. Brain Res. 2 (1986) 339-346
12. Fournier A.E., Beer J., Arregui C.O., Essagian C., Aguayo A.J., and McKerracher L. Brain-derived neurotrophic factor modulates GAP-43 but not T alpha1 expression in injured retinal ganglion cells of adult rats. J. Neurosci. Res. 6 (1997) 561-572
13. Garrido C., Gurbuxani S., Ravagnan L., and Kroemer G. Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem. Biophys. Res. Commun. 3 (2001) 433-442
14. Gelatt K.N. Animal models for glaucoma. Invest. Ophthalmol. Vis. Sci. 7 (1977) 592-596
15. Goldblum D., and Mittag T. Prospects for relevant glaucoma models with retinal ganglion cell damage in the rodent eye. Vision Res. 4 (2002) 471-478
16. Grosche J., Hartig W., and Reichenbach A. Expression of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and Bcl-2 protooncogene protein by Muller (glial) cells in retinal light damage of rats. Neurosci. Lett. 2 (1995) 119-122
17. Haefliger I.O., Dettmann E., Liu R., Meyer P., Prunte C., Messerli J., and Flammer J. Potential role of nitric oxide and endothelin in the pathogenesis of glaucoma. Surv. Ophthalmol (1999) S51-S58
18. Hangai M., Yoshimura N., Yoshida M., Yabuuchi K., and Honda Y. Interleukin-1 gene expression in transient retinal ischemia in the rat. Invest. Ophthalmol. Vis. Sci. 3 (1995) 571-578
19. Hebb M.O., Myers T.L., and Clarke D.B. Enhanced expression of heat shock protein 27 is correlated with axonal regeneration in mature retinal ganglion cells. Brain Res (2006) 146-150
20. Herdegen T., Bastmeyer M., Bahr M., Stuermer C., Bravo R., and Zimmermann M. Expression of JUN, KROX, and CREB transcription factors in goldfish and rat retinal ganglion cells following optic nerve lesion is related to axonal sprouting. J. Neurobiol. 4 (1993) 528-543
21. Heywood R. Glaucoma in the rat. Br. Vet. J. 2 (1975) 213-221
22. Hightower L.E. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 2 (1991) 191-197
23. Hiller R., and Kahn H.A. Blindness from glaucoma. Am. J. Ophthalmol. 1 (1975) 62-69
24. John S.W., Smith R.S., Savinova O.V., Hawes N.L., Chang B., Turnbull D., Davisson M., Roderick T.H., and Heckenlively J.R. Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Invest. Ophthalmol. Vis. Sci. 6 (1998) 951-962
25. Johnson E.C., Deppmeier L.M., Wentzien S.K., Hsu I., and Morrison J.C. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Invest. Ophthalmol. Vis. Sci. 2 (2000) 431-442
26. Kallberg M.E., Brooks D.E., Garcia-Sanchez G.A., Komaromy A.M., Szabo N.J., and Tian L. Endothelin 1 levels in the aqueous humor of dogs with glaucoma. J. Glaucoma 2 (2002) 105-109
27. Krupin T., Feitl M., Roshe R., Lee S., and Becker B. Halothane anesthesia and aqueous humor dynamics in laboratory animals. Invest. Ophthalmol. Vis. Sci. 5 (1980) 518-521
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 259 (1970) 680-685
29. Lam T.T., Kwong J.M., and Tso M.O. Early glial responses after acute elevated intraocular pressure in rats. Invest. Ophthalmol. Vis. Sci. 2 (2003) 638-645
30. Leon S., Yin Y., Nguyen J., Irwin N., and Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 12 (2000) 4615-4626
31. Lin K.M., Lin B., Lian I.Y., Mestril R., Scheffler I.E., and Dillmann W.H. Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 13 (2001) 1787-1792
32. Mirakhur R.K., Elliott P., Shepherd W.F., and McGalliard J.N. Comparison of the effects of isoflurane and halothane on intraocular pressure. Acta Anaesthesiol. Scand 4 (1990) 282-285
33. Mittag T.W., Danias J., Pohorenec G., Yuan H.M., Burakgazi E., Chalmers-Redman R., Podos S.M., and Tatton W.G. Retinal damage after 3 to 4 months of elevated intraocular pressure in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 11 (2000) 3451-3459
34. Moore C.G., Milne S.T., and Morrison J.C. Noninvasive measurement of rat intraocular pressure with the Tono-Pen. Invest. Ophthalmol. Vis. Sci. 2 (1993) 363-369
35. Morrison J.C., Moore C.G., Deppmeier L.M., Gold B.G., Meshul C.K., and Johnson E.C. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 1 (1997) 85-96
36. Naskar R., Wissing M., and Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest. Ophthalmol. Vis. Sci. 9 (2002) 2962-2968
37. Neufeld A.H. Nitric oxide: a potential mediator of retinal ganglion cell damage in glaucoma. Surv. Ophthalmol. (1999) S129-S135
38. Noske W., Hensen J., and Wiederholt M. Endothelin-like immunoreactivity in aqueous humor of patients with primary open-angle glaucoma and cataract. Graefes Arch. Clin. Exp. Ophthalmol. 9 (1997) 551-552
39. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 10 (1975) 4007-4021
40. Okada M., Matsumura M., Ogino N., and Honda Y. Muller cells in detached human retina express glial fibrillary acidic protein and vimentin. Graefes Arch. Clin. Exp. Ophthalmol. 5 (1990) 467-474
41. Osborne N.N., Block F., and Sontag K.H. Reduction of ocular blood flow results in glial fibrillary acidic protein (GFAP) expression in rat retinal Muller cells. Vis. Neurosci. 6 (1991) 637-639
42. Pavlidis M., Stupp T., Naskar R., Cengiz C., and Thanos S. Retinal ganglion cells resistant to advanced glaucoma: a postmortem study of human retinas with the carbocyanine dye DiI. Invest. Ophthalmol. Vis. Sci. 12 (2003) 5196-5205
43. Plumier J.C., Hopkins D.A., Robertson H.A., and Currie R.W. Constitutive expression of the 27-kDa heat shock protein (Hsp27) in sensory and motor neurons of the rat nervous system. J. Comp Neurol. 3 (1997) 409-428
44. Plumier J.C., Armstrong J.N., Landry J., Babity J.M., Robertson H.A., and Currie R.W. Expression of the 27,000 mol. wt heat shock protein following kainic acid-induced status epilepticus in the rat. Neuroscience 3 (1996) 849-856
45. Prasanna G., Krishnamoorthy R., Clark A.F., Wordinger R.J., and Yorio T. Human optic nerve head astrocytes as a target for endothelin-1. Invest. Ophthalmol. Vis. Sci. 8 (2002) 2704-2713
46. Prasanna G., Hulet C., Desai D., Krishnamoorthy R.R., Narayan S., Brun A.M., Suburo A.M., and Yorio T. Effect of elevated intraocular pressure on endothelin-1 in a rat model of glaucoma. Pharmacol. Res. 1 (2005) 41-50
47. Samali A., Cai J., Zhivotovsky B., Jones D.P., and Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J. 8 (1999) 2040-2048
48. Satoh J., and Kim S.U. Cytokines and growth factors induce HSP27 phosphorylation in human astrocytes. J. Neuropathol. Exp. Neurol. 4 (1995) 504-512
49. Schwartz M., Belkin M., Yoles E., and Solomon A. Potential treatment modalities for glaucomatous neuropathy: neuroprotection and neuroregeneration. J. Glaucoma 6 (1996) 427-432
50. Shareef S.R., Garcia-Valenzuela E., Salierno A., Walsh J., and Sharma S.C. Chronic ocular hypertension following episcleral venous occlusion in rats. Exp. Eye Res. 3 (1995) 379-382
51. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 5 (1996) 850-858
52. Tanihara H., Inatani M., and Honda Y. Growth factors and their receptors in the retina and pigment epithelium. Prog. Retin. Eye Res (1997) 271-301
53. Tanihara H., Hangai M., Sawaguchi S., Abe H., Kageyama M., Nakazawa F., Shirasawa E., and Honda Y. Up-regulation of glial fibrillary acidic protein in the retina of primate eyes with experimental glaucoma. Arch. Ophthalmol. 6 (1997) 752-756
54. Tezel G., and Wax M.B. Inhibition of caspase activity in retinal cell apoptosis induced by various stimuli in vitro. Invest. Ophthalmol. Vis. Sci. 11 (1999) 2660-2667
55. Tezel G., and Wax M.B. The mechanisms of hsp27 antibody-mediated apoptosis in retinal neuronal cells. J. Neurosci. 10 (2000) 3552-3562
56. Tezel G., Seigel G., and Wax M. Autoantibodies to small heat shock proteins in glaucoma. Invest. Ophthalmol. Vis. Sci. 12 (1998) 2277-2287
57. Tezel G., Hernandez R., and Wax M.B. Immunostaining of heat shock proteins in the retina and optic nerve head of normal and glaucomatous eyes. Arch. Ophthalmol. 4 (2000) 511-518
58. Tezel G., Yang J., and Wax M.B. Heat shock proteins, immunity and glaucoma. Brain Res. Bull. 6 (2004) 473-480
59. Thanos S., and Naskar R. Correlation between retinal ganglion cell death and chronically developing inherited glaucoma in a new rat model. Exp. Eye Res. 1 (2004) 119-129
60. Thanos S., Bahr M., Barde Y.A., and Vanselow J. Survival and Axonal Elongation of Adult Rat Retinal Ganglion Cells. Eur J. Neurosci. 1 (1989) 19-26
61. Ueda J., Sawaguchi S., Hanyu T., Yaoeda K., Fukuchi T., Abe H., and Ozawa H. Experimental glaucoma model in the rat induced by laser trabecular photocoagulation after an intracameral injection of India ink. Jpn. J. Ophthalmol. 5 (1998) 337-344
62. Wang X., Tay S.S., and Ng Y.K. An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp. Brain Res. 4 (2000) 476-484
63. Xanthoudakis S., Roy S., Rasper D., Hennessey T., Aubin Y., Cassady R., Tawa P., Ruel R., Rosen A., and Nicholson D.W. Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis. EMBO J. 8 (1999) 2049-2056
64. Yorio T., Krishnamoorthy R., and Prasanna G. Endothelin: is it a contributor to glaucoma pathophysiology?. J. Glaucoma 3 (2002) 259-270
65. Yoshida A., Ishiguro S., and Tamai M. Expression of glial fibrillary acidic protein in rabbit Muller cells after lensectomy-vitrectomy. Invest. Ophthalmol. Vis. Sci. 11 (1993) 3154-3160
66. Young C., Festing M.F., and Barnett K.C. Buphthalmos (congenital glaucoma) in the rat. Lab Anim 1 (1974) 21-31