Gene therapy with brain-derived neurotrophic factor as a protection: Retinal ganglion cells in a rat glaucoma model

Investigative Ophthalmology and Visual Science

Volumn 44, Issue 10, 2003, Pages 4357-4365

  Martin, Keith R G ^a   Quigley, Harry A ^a   Zack, Donald J ^a   Levkovitch Verbin, Hana ^a   Kielczewski, Jennifer ^a   Valenta, Danielle ^a   Baumrind, Lisa ^a   Pease, Mary Ellen ^b   Klein, Ronald L ^b   Hauswirth, William W ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; SODIUM CHLORIDE; VIRUS VECTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; GENE THERAPY; GENETIC TRANSFECTION; GLAUCOMA; IMMUNOHISTOCHEMISTRY; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; TRABECULAR MESHWORK; TRANSCRIPTION REGULATION; TRANSGENE; WESTERN BLOTTING;

ANIMALS; AXONS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL COUNT; CELL SURVIVAL; CYTOPROTECTION; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GLAUCOMA; GREEN FLUORESCENT PROTEINS; INTRAOCULAR PRESSURE; LUMINESCENT PROTEINS; OPTIC NERVE DISEASES; RATS; RATS, WISTAR; RETINAL GANGLION CELLS;

EID: 0141430092     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.02-1332     Document Type: Article

References (70)

1. Quigley HA. Number of people with glaucoma worldwide. Br J Ophthalmol. 1996;80:389-393.
2. Nickells RW. Apoptosis of retinal ganglion cells in glaucoma: an update of the molecular pathways involved in cell death. Surv Ophthalmol. 1999;43(suppl 1):S151-S161.
3. Quigley H, Nickells R, Kerrigan L, et al. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774-786.
4. Kerrigan L, Zack D, Quigley H, et al. TUNEL-positive ganglion cells in human primary open angle glaucoma. Arch Ophthalmol. 1997;115:1031-1035.
5. Garcia-Valenzuela E, Shareef S, Walsh J, Sharma SC. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp Eye Res. 1995;61:33-44.
6. Anderson DR. Glaucoma: the damage caused by pressure: XLVI Edward Jackson memorial lecture. Am J Ophthalmol. 1989;108:485-495.
7. Sommer A, Tielsch JM, Katz J, et al. Relationship between intraocular pressure and primary open angle glaucoma among white and black Americans. The Baltimore Eye Survey. Arch Ophthalmol. 1991;109:1090-1095.
8. Gramer E, Tausch M. The risk profile of the glaucomatous patient. Curr Opin Ophthalmol. 1995;6:78-88.
9. The Collaborative Normal-Tension Glaucoma Study Group. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Collaborative Normal-Tension Glaucoma Study Group (see comments) (published correction appears in Am J Ophthalmol. 1999;127:120). Am J Ophthalmol 1998;126:487-497.
10. Kass MA, Heuer DK, Higginbotham EJ, et al. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol 2002;120:701-713; discussion 829-830.
11. Heijl A, Leske MC, Bengtsson B, et al. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol. 2002;120:1268-1279.
12. Georgopoulos G, Andreanos D, Liokis N, et al. Risk factors in ocular hypertension. Eur J Ophthalmol. 1997;7:357-363.
13. Caprioli J. Neuroprotection of the optic nerve in glaucoma. Acta Ophthalmol Scand. 1997;75:364-367.
14. Chew SJ, Ritch R. Neuroprotection: the next breakthrough in glaucoma? Proceedings of the Third Annual Optic Nerve Rescue and Restoration Think Tank. J Glaucoma. 1997;6:263-266.
15. Osborne NN, Ugarte M, Chao M, et al. Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol 1999;43 Suppl 1:S102-S128.
16. Schwartz M, Belkin M, Yoles E, Solomon A. Potential treatment modalities for glaucomatous neuropathy: neuroprotection and neuroregeneration. J Glaucoma. 1996;5:427-432.
17. Yoles E, Schwartz M. Potential neuroprotective therapy for glaucomatous optic neuropathy. Surv Ophthalmol. 1998;42:367-372.
18. Ma YT, Hsieh T, Forbes ME, et al. BDNF injected into the superior colliculus reduces developmental retinal ganglion cell death. J Neurosci. 1998;18:2097-2107.
19. Weibel D, Kreutzberg GW, Schwab ME. Brain-derived neurotrophic factor (BDNF) prevents lesion-induced axonal die-back in young rat optic nerve. Brain Res. 1995;679:249-254.
20. Mansour-Robaey S, Clarke DB, Wang YC, et al. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc Natl Acad Sci USA. 1994;91:1632-1636.
21. Takano M, Horie H, Iijima Y, et al. Brain-derived neurotrophic factor enhances neurite regeneration from retinal ganglion cells in aged human retina in vitro. Exp Eye Res. 2002;74:319-323.
22. Watanabe M, Sawai H, Fukuda Y. Survival of axotomized retinal ganglion cells in adult mammals. Clin Neurosci. 1997;4:233-239.
23. DiStefano PS, Friedman B, Radziejewski C, et al. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 1992;8:983-993.
24. von Bartheld CS, Williams R, Lefcort F, et al. Retrograde transport of neurotrophins from the eye to the brain in chick embryos: roles of the p75NTR and trkB receptors. J Neurosci. 1996;16:2995-3008.
25. Pease ME, McKinnon SJ, Quigley HA, et al. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest Ophthalmol Vis Sci. 2000;41:764-774.
26. Ko ML, Hu DN, Ritch R, et al. Patterns of retinal ganglion cell survival after brain-derived neurotrophic factor administration in hypertensive eyes of rats. Neurosci Lett. 2001;305:139-142.
27. Acland GM, Aguirre GD, Ray J, et al. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet. 2001;28:92-95.
28. Ali RR, Sarra GM, Stephens C, et al. Restoration of photoreceptor ultrastructure and function in retinal degeneration slow mice by gene therapy. Nat Genet. 2000;25:306-310.
29. Jomary C, Vincent KA, Grist J, et al. Rescue of photoreceptor function by AAV-mediated gene transfer in a mouse model of inherited retinal degeneration. Gene Ther. 1997;4:683-690.
30. Lau D, McGee LH, Zhou S, et al. Retinal degeneration is slowed in transgenic rats by AAV-mediated delivery of FGF-2. Invest Ophthalmol Vis Sci. 2000;41:3622-3633.
31. Liang FQ, Dejneka NS, Cohen DR, et al. AAV-mediated delivery of ciliary neurotrophic factor prolongs photoreceptor survival in the rhodopsin knockout mouse. Mol Ther. 2001;3:241-248.
32. Liang FQ, Aleman TS, Dejneka NS, et al. Long-term protection of retinal structure but not function using RAAV: CNTF in animal models of retinitis pigmentosa. Mol Ther. 2001;4:461-472.
33. Di Polo A, Aigner LJ, Dunn RJ, et al. Prolonged delivery of brain-derived neurotrophic factor by adenovirus-infected Muller cells temporarily rescues injured retinal ganglion cells. Proc Natl Acad Sci USA. 1998;95:3978-983.
34. Hauswirth WW, Lewin AS, Zolotukhin S, Muzyczka N. Production and purification of recombinant adeno-associated virus. Methods Enzymol. 2000;316:743-761.
35. Peel AL, Klein RL. Adeno-associated virus vectors: activity and applications in the CNS. J Neurosci Methods. 2000;98:95-104.
36. Hauswirth WW, McInnes RR. Retinal gene therapy 1998: summary of a workshop. Mol Vis. 1998;4:11.
37. Dudus L, Anand V, Acland GM, et al. Persistent transgene product in retina, optic nerve and brain after intraocular injection of rAAV. Vision Res. 1999;39:2545-2553.
38. Guy J, Qi X, Muzyczka N, Hauswirth WW. Reporter expression persists 1 year after adeno-associated virus-mediated gene transfer to the optic nerve. Arch Ophthalmol. 1999;117:929-937.
39. Levkovitch-Verbin H, Quigley HA, Martin KR, et al. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol Vis Sci. 2002;43:402-410.
40. Martin KR, Klein RL, Quigley HA. Gene delivery to the eye using adeno-associated viral vectors. Methods 2002:28;267-275.
41. Klein RL, Hamby ME, Gong Y, et al. Dose and promoter effects of adeno-associated viral vector for green fluorescent protein expression in the rat brain. Exp Neurol. 2002;176:66-74.
42. Paterna JC, Moccetti T, Mura A, et al. Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther. 2000;7:1304-1311.
43. Klein RL, Lewis MH, Muzyczka N, Meyer EM. Prevention of 6-hydroxydopamine-induced rotational behavior by BDNF somatic gene transfer. Brain Res. 1999;847:314-320.
44. Klein RL, Muir D, King MA, et al. Long-term actions of vector-derived nerve growth factor or brain-derived neurotrophic factor on choline acetyltransferase and Trk receptor levels in the adult rat basal forebrain. Neuroscience. 1999;90:815-821.
45. Zolotukhin S, Byrne BJ, Mason E, et al. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther. 1999;6:973-985.
46. Grimm D, Kern A, Rittner K, Kleinschmidt JA. Novel tools for production and purification of recombinant adenoassociated virus vectors. Hum Gene Ther. 1998;9:2745-2760.
47. Levkovitch-Verbin H, Harris-Cerruti C, Groner Y, et al. RGC death in mice after optic nerve crush injury: oxidative stress and neuroprotection. Invest Ophthalmol Vis Sci. 2000;41:4169-4174.
48. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
49. Klocker N, Kermer P, Weishaupt JH, et al. Brain-derived neurotrophic factor-mediated neuroprotection of adult rat retinal ganglion cells in vivo does not exclusively depend on phosphatidyl-inositol-3′-kinase/protein kinase B signaling. J Neurosci. 2000;20:6962-6967.
50. Mo X, Yokoyama A, Oshitari T, et al. Rescue of axotomized retinal ganglion cells by BDNF gene electroporation in adult rats. Invest Ophthalmol Vis Sci. 2002;43:2401-2405.
51. Quigley HA, McKinnon SJ, Zack DJ, et al. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci. 2000;41:3460-3466.
52. Shen S, Wiemelt AP, McMorris FA, Barres BA. Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron. 1999;23:285-295.
53. Cheng L, Sapieha P, Kittlerova P, et al. TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. J Neurosci. 2002;22:3977-3986.
54. McKinnon SJ, Lehman DM, Tahzib NG, et al. Baculoviral IAP repeat-containing-4 protects optic nerve axons in a rat glaucoma model. Mol Ther. 2002;5:780-787.
55. Dudus L, Anand V, Acland GM, et al. Persistent transgene product in retina, optic nerve and brain after intraocular injection of rAAV. Vision Res. 1999;39:2545-2553.
56. Guy J, Qi X, Muzyczka N, Hauswirth WW. Reporter expression persists 1 year after adeno-associated virus-mediated gene transfer to the optic nerve. Arch Ophthalmol. 1999;117:929-937.
57. Grant CA, Ponnazhagan S, Wang XS, Srivastava A, Li T. Evaluation of recombinant adeno-associated virus as a gene transfer vector for the retina. Curr Eye Res. 1997;16:949-956.
58. Loeb JE, Cordier WS, Harris ME, et al. Enhanced expression of transgenes from adeno-associated virus vectors with the wood-chuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum Gene Ther. 1999;10:2295-2305.
59. Choi T, Huang M, Gorman C, Jaenisch R. A generic intron increases gene expression in transgenic mice. Mol Cell Biol. 1991;11:3070-3074.
60. Donello JE, Loeb JE, Hope TJ. Woodchuck hepatitis virus contains a tripartite posttranscriptional regulatory element. J Virol. 1998;72:5085-5092.
61. Ricard CS, Agapova OA, Salvador-Silva M, Kaufman PL, Hernandez MR. Expression of myocilin/TIGR in normal and glaucomatous primate optic nerves. Exp Eye Res. 2001;73:433-447.
62. Yucel YH, Kalichman MW, Mizisin AP, Powell HC, Weinreb RN. Histomorphometric analysis of optic nerve changes in experimental glaucoma. J Glaucoma. 1999;8:38-45.
63. Yucel YH, Zhang Q, Weinreb RN, Kaufman PL, Gupta N. Atrophy of relay neurons in magno- and parvocellular layers in the lateral geniculate nucleus in experimental glaucoma. Invest Ophthalmol Vis Sci. 2001;42:3216-3222;
64. Morrison JC, Moore CG, Deppmeier LM, Gold BG, Meshul CK, Johnson EC. A rat model of chronic pressure-induced optic nerve damage. Exp Eye Res. 1997;64:85-96.
65. Morrison JC, Nylander KB, Lauer AK, Cepuma WO, Johnson E. Glaucoma drops control intraocular pressure and protect optic nerves in a rat model of glaucoma. Invest Ophthalmol Vis Sci. 1998;39:526-531.
66. Chauhan BC, Pan J, Archibald ML, LeVatte TL, Kelly MEM, Tremblay F. 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. 2002;43:2969-2976.
67. Quigley HA, Davis EB, Anderson DR. Descending optic nerve degeneration in primates. Invest Ophthalmol. 1977;16:841-849.
68. Bodeutsch N, Thanos S. Migration of phagocytic cells and development of the murine intraretinal microglial network: an in vivo study using fluorescent dyes. Glia. 2000;32:91-101.
69. Sorenson JC, Dalmau I, Zimmer J, Finsen B. Microglial reactions to retrograde degeneration of tracer-identified thalamic neurons after frontal sensorimotor cortex lesions in adult rats. Exp Brain Res. 1996;112:203-212.
70. Kerrigan-Baumrind LA, Quigley HA, Pease ME, Kerrigan DF, Mitchell RS. The 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.