Leber hereditary optic neuropathy: Mitochondrial mutations and degeneration of the optic nerve

Vision Research

Volumn 37, Issue 24, 1997, Pages 3495-3507

  Howell, Neil ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Bioenergetics; Leber hereditary optic neuropathy; Mitochondrial DNA; Neurodegeneration; Neuropathology; Optic nerve

Indexed keywords

LACTIC ACID; MITOCHONDRIAL DNA; PYRUVIC ACID;

APOPTOSIS; BIOENERGY; CELL DEATH; CONTROLLED STUDY; FIBROBLAST CULTURE; GENE MUTATION; HEREDITARY OPTIC ATROPHY; HUMAN; HUMAN CELL; NERVE DEGENERATION; NERVE FIBER; OPTIC NERVE; PEDIGREE ANALYSIS; PENETRANCE; PRIORITY JOURNAL; RESPIRATORY CHAIN; RETINA GANGLION CELL; REVIEW; SEX DIFFERENCE; VISUAL ACUITY; VISUAL IMPAIRMENT;

EID: 0030806721     PISSN: 00426989     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6989(96)00167-8     Document Type: Article

References (108)

1. + transport. Journal of Neuroscience, 12, 840-853.
2. Andersen, S., Bankier, A. T., Barrel, B. G., de Bruijn, M. H., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J., Staden, R. & Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
3. Beal, M. F. (1995). Aging, energy, and oxidative stress in neurodegenerative diseases. Annals of Neurology, 38, 357-366.
4. Bell, J. (1931). Hereditary optic atrophy (Leber's disease). In Pearson, K. (Ed.), The treasury of human inheritance (pp. 325-423). Cambridge: Cambridge University Press.
5. Black, G. C. M., Craig, I. W., Ooostra, R. J., Norby, S., Rosenberg, T., Morten, K., Laborde, A. & Poulton, J. (1995). Leber's hereditary optic neuropathy: Implications of the sex ratio for linkage studies in families with the 3460 ND1 mutation. Eye, 9, 513-516.
6. Bodis-Wollner, I. (1989). Electrophysiological and psychophysical testing of vision in glaucoma. Survey of Ophthalmology, 33(suppl.), 301-307.
7. Brown, M. D., Voljavec, A. S., Lott, M. T., MacDonald, I. & Wallace, D. C. (1992). Leber's hereditary optic neuropathy: A model for mitochondrial neurodegenerative diseases. FASEB Journal, 6, 2791-2799.
8. Brown, M. D. & Wallace, D. C. (1994). Spectrum of mitochondrial DNA mutations in Leber's hereditary optic neuropathy. Clinical Neuroscience, 2, 138-145.
9. Bu, X. & Rotter, J. I. (1991). X chromosomal-linked and mitochondrial gene control of Leber hereditary optic neuropathy: Evidence from segregation analysis for dependence on X chromosome activation. Proceedings of the National Academy of Sciences of the U.S.A., 88, 8198-8202.
10. Burde, R. M. (1993). Optic disk risk factors for nonarteritic anterior ischemic optic neuropathy. American Journal of Ophthalmology, 116, 759-764.
11. Carvalho, M. R. S., Muller, B., Rotzer, E., Berninger, T., Kommerell, G., Blankenagel, A., Savontaus, M.-L., Meitinger, T. & Lorenz, B. (1992). Leber hereditary neuroretinopathy and the X-chromosomal susceptibility factor: No linkage to DXS7. Human Heredity, 42, 316-320.
12. Chan, C., Mackey, D. A. & Byrne, E. (1996). Sporadic Leber hereditary optic neuropathy in Australia and New Zealand. Australian and New Zealand Journal of Ophthalmology, 24, 7-14.
13. Cock, H. R., Cooper, J. M. & Schapira, A. H. V. (1995). The 14484 ND6 mtDNA mutation in Leber hereditary optic neuropathy does not affect fibroblast complex I activity. American Journal of Human Genetics, 57, 1501-1502.
14. Cocke, J. G. Jr, Brown, R. E. & Geppert, L. J. (1966). Optic neuritis with prolonged use of chloramphenicol. Journal of Pediatrics, 68, 27-31.
15. Cornelissen, J. C., Wanders, R. J. A., Bolhuis, P. A., BleekerWagemakers, E., Ooostra, R.-J. & Wijburg, F. A. (1993). Respiratory chain function in Leber's hereditary optic neuropathy: Lack of correlation with clinical disease. Journal of Inherited Metabolic Disorders, 16, 531-533.
16. Cui, Q. & Harvey, A. R. (1995). At least two mechanisms are involved in the death of retinal ganglion cells following target ablation in neonatal rats. Journal of Neuroscience, 15, 8143-8155.
17. Cullom, M. E., Heher, K. L., Miller, N. R., Savino, P. J. & Johns, D. R. (1993). Leber's hereditary optic neuropathy masquerading as tobacco-alcohol amblyopia. Archives of Ophthalmology, 111, 1482-1485.
18. Degli Esposti, M., Carelli, V., Ghelli, A., Ratta, M., Crimi, M., Sangiorgi, S., Montagna, P., Lenaz, G., Lugaresi, E. & Cortelli, P. (1994). Functional alterations of the mitochondrially encoded ND4 subunit associated with Leber's hereditary optic neuropathy. FEBS Letters, 352, 375-379.
19. De Vries, D. D., Went, L. N., Bruyn, G. W., Scholte, H. R., Hofstra, R. M. W., Bolhuis, P. A. & van Oost, B. A. (1996). Genetic and biochemical impairment of mitochondrial complex I activity in a family with Leber hereditary optic neuropathy and hereditary spastic dystonia. American Journal of Human Genetics, 58, 703-711.
20. Dreyer, E. B., Pan, Z.-Ph., Storm, S. & Lipton, S. A. (1994). Greater sensitivity of larger retinal ganglion cells to NMDA-mediated cell death. NeuroReport, 5, 629-631.
21. Dreyer, E. B., Zurakowski, D., Schumer, R. A., Podos, S. M. & Lipton, S. A. (1996). Elevated glutamate levels in the vitreous body of humans and monkeys with glaucoma. Archives of Ophthalmology, 114, 299-305.
22. DuBois, L. G. & Feldon, S. E. (1992). Evidence for a metabolic trigger for Leber's hereditary optic neuropathy. A case report. Journal of Clinical Neuro-ophthalmology, 12, 15-16.
23. Fechtner, R. D. & Weinreb, R. N. (1994). Mechanisms of optic nerve damage in primary open angle glaucoma. Survey of Ophthalmology, 39, 23-42.
24. Flanigan, K. M. & Johns, D. R. (1993). Association of the 11778 mitochondrial DNA mutation and demyelinating disease. Neurology, 43, 2720-2722.
25. Gao, H. & Hollyfield, J. G. (1992). Aging and the human retina. Differential loss of neurons and retinal pigment epithelial cells. Investigative Ophthalmology and Visual Science, 33, 1-17.
26. Ghosh, S. S., Fahy, E., Bodis-Wollner, I., Sherman, J. & Howell, N. (1996). Longitudinal study of a heteroplasmic 3460 Leber hereditary optic neuropathy family by multiplexed primer-extension analysis and nucleotide sequencing. American Journal of Human Genetics, 58, 325-334.
27. Golnik, K. C. & Schaible, E. R. (1994). Folate-responsive optic neuropathy. Journal of Neuro-Ophthalmology, 14, 163-169.
28. de Gottrau, P., Buchi, E. R. & Daicker, B. (1992). Distended optic nerve sheaths in Leber's hereditary optic neuropathy. Journal of Clinical Neuro-ophthalmology, 12, 89-93.
29. Gwag, B. J., Lobner, D., Koh, J.Y., Wie, M. B. & Choi, D. W. (1995). Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience, 68, 615-619.
30. Harding, A. E., Sweeney, M. G., Govan, G. G. & Riordan-Eva, P. (1995). Pedigree analysis in Leber hereditary optic neuropathy families with a pathogenic mtDNA mutation. American Journal of Human Genetics, 57, 77-86.
31. Harley, R. D., Huang, N. N., Macri, C. H. & Green, W. R. (1970). Optic neuritis and optic atrophy following chloramphenicol in cystic fibrosis patients. Transactions of the American Academy of Ophthalmology and Otology, 74, 1011-1029.
32. Hartveit, E., Brandstatter, J. H., Sassoe-Pognetto, M., Laurie, D. J., Seeburg, P. H. & Wassle, H. (1994). Localization and developmental expression of the NMDA receptor subunit NR2A in the mammalian retina. Journal of Comparative Neurology, 348, 570-582.
33. Hirano, M., Lincoff, N. S., Mojon, D. S. & Odel, J. G. (1994). LHON mutations in an outbreak of optic neuropathy in Cuba. Clinical Neuroscience, 2, 173-178.
34. Hollander, H., Makarov, F., Stefani, F. H. & Stone, J. (1995). Evidence of constriction of optic nerve axons at the lamina cribosa in the normotensive eye in humans and other mammals. Ophthalmic Research, 27, 296-309.
35. Howell, N. (1995). Primary LHON mutations: Trying to separate "fruyt" from "chaf". Clinical Neuroscience, 2, 130-137.
36. Howell, N. (1995). Mitochondrial gene mutations and human diseases: A prolegomenon. American Journal of Human Genetics, 55, 219-224.
37. Howell, N., Bindoff, L. A., McCullough, D. A., Kubacka, I., Poulton, J., Mackey, D., Taylor, L. & Turnbull, D. M. (1991). Leber hereditary optic neuropathy: Identification of the same mitochondrial ND1 mutation in six pedigrees. American Journal of Human Genetics, 49, 939-950.
38. Howell, N., Kubacka, I., Halvorson, S. & Mackey, D. (1993a). Leber's hereditary optic neuropathy: The etiological role of a mutation in the mitochondrial cytochrome b gene. Genetics, 133, 133-136.
39. Howell, N., Halvorson, S., Burns, J., McCullough, D A. & Poulton, J. (1993b). When does bilateral optic atrophy become Leber hereditary optic neuropathy? American Journal of Human Genetics, 53, 959-963.
40. Howell, N., Kubacka, I., Halvorson, S., Howell, B., McCullough, D. A. & Mackey, D. (1995). Phylogenetic analysis of mitochondrial genomes from Leber hereditary optic neuropathy pedigrees. Genetics. 140, 285-302.
41. Hrynchak, P. K. & Spafford, M. M. (1994). Visual recovery in a patient with Leber hereditary optic neuropathy and the 14484 mutation. Optometry and Vision Science, 71, 604-612.
42. Huang, N. N., Harley, R. D., Promadhattavedi, V. & Sproul, A. (1966). Visual disturbances in cystic fibrosis following chloramphenicol administration. Journal of Pediatrics, 68, 32-44.
43. Jansen, P. H. P., van der Knaap, M. S. & de Coo, I. F. M. (1996). Leber's hereditary optic neuropathy with the 11 778 mtDNA mutation and white matter disease resembling multiple sclerosis: Clinical, MRI and MRS findings. Journal of Neurological Science, 135, 176-180.
44. Johns, D. R. (1994). Genotype-specific phenotypes in Leber's hereditary optic neuropathy. Clinical Neuroscience, 2, 146-150.
45. Johns, D. R. (1995). Mitochondrial DNA and disease. New England Journal of Medicine, 333, 638-644.
46. Johns, D. R. & Berman, J. (1991). Alternative simultaneous complex I mitochondrial DNA mutations in Leber's hereditary optic neuropathy. Biochemical and Biophysical Research Communication, 174, 1324-1330.
47. Johns, D. R. & Sadun, A. A. (1994). Cuban epidemic optic neuropathy. Mitochondrial DNA analysis. Journal of Neuro-ophthalmology, 14, 130-134.
48. Johns, D. R., Neufeld, M. J. & Hedges, T. R. (1994). Mitochondrial DNA mutations in Cuban optic and peripheral neuropathy. Journal of Neuro-ophthalmology, 14, 135-140.
49. Juvonen, V., Vilkki, J., Aula, P., Nikoskelainen, E. & Savontaus, M.-L. (1993). Reevaluation of the linkage of an optic atrophy susceptibility gene to X-chromosomal markers in Finnish families with Leber hereditary optic neuroretinopathy (LHON). American Journal of Human Genetics, 53, 289-292.
50. Kermode, A. G., Moseley, I. F., Kendall, B. E., Miller, D. H., MacManus, D. G. & McDonald, W. I. (1989). Magnetic resonance imaging in Leber's optic neuropathy. Journal of Neurological and Neurosurgical Psychiatry, 52, 671-674.
51. Kerrison, J. B., Howell, N., Miller, N. R., Hirst, L. & Green, W. R. (1995). Leber hereditary optic neuropathy. Electron microscopy and molecular genetic analysis of a case. Ophthalmology, 102, 15091516.
52. Kothe, A. C., Lovasik, J. V., Pace. R., Hrynchak, P. K. & Flanagan, J. G. (1990). Visual and neural function in Leber's optic neuropathy. Optometry and Vision Science, 67, 138-147.
53. Kwittken, J. & Barest, H. D. (1958). The neuropathology of hereditary optic atrophy (Leber's disease); the first complete anatomic study. American Journal of Pathology, 34, 185-207.
54. Larsson, N.-G., Andersen, O., Holme, E., Oldfors, A. & Wahlstrom, J. (1991). Leber's hereditary optic neuropathy and complex I deficiency in muscle. Annals of Neurology, 30, 701-708.
55. Leber, T. (1871). Uber hereditare und congenital-angelegte Sehnervenleiden. Graefe's Archives of Ophthalmology, 7, 249-291.
56. Levin, L. A. & Louhab, A. (1996). Apoptosis of retinal ganglion cells in anterior ischemic optic neuropathy. Archives in Ophthalmology, 114, 488-491.
57. Lloyd, A. V. C., Grimes, G., Khaw, K.-T. & Schwachman, H. (1963). Chloramphenicol for long-term therapy of cystic fibrosis. Journal of the American Medical Association, 184, 1001-1006.
58. Lowry, O., Roberts, N. R. & Lewis, C. (1956). The quantitative histochemistry of the retina. Journal of Biological Chemistry, 220, 879-892.
59. Ludolph, A. C., Riepe, M. & Ullrich, K. (1993). Excitotoxicity, energy metabolism, neurodegeneration. Journal of Inherited Metabolic Disorders, 16, 716-723.
60. Lundsgard, R. (1944). Leber's disease: A genealogic, genetic and clinical study of 101 cases of retrobulbar optic neuritis in 20 Danish families. Acta Ophthalmology, 21 (Suppl. 3), 3-306.
61. Mackey, D. A. (1993). Blindness in offspring of women blinded by Leber hereditary optic neuropathy. Lancet, 341, 1020-1021.
62. Mackey, D. A. & Buttery, R. G. (1992). Leber hereditary optic neuropathy in Australia. Australian and New Zealand Journal of Ophthalmology, 20, 177-184.
63. Mackey, D. & Howell, N. (1992). A variant of Leber hereditary optic neuropathy characterized by recovery of vision and by an unusual mitochondrial genetic etiology. American Journal of Human Genetics, 51, 1218-1228.
64. Mackey, D. & Howell, N. (1994). Tobacco amblyopia. American Journal of Ophthalmology, 117, 817-818.
65. Mackey, D., Oostra, R.-J., Rosenberg, T., Nikoskelainen, E., BronteStewart, J., Poulton, J., Harding, A. E., Govan, G., Bolhuis, P. A., Norby, S., Bleeker-Wagemakers, E. M., Savontaus, M.-L., Chan, C. & Howell, N. (1996). Primary pathogenic mtDNA mutations in multigeneration pedigrees with Leber hereditary optic neuropathy. American Journal of Human Genetics, 59, 481-485.
66. Majander, A., Huoponen, K., Savontaus, M.-L., Nikoskelainen, E. & Wikstrom, M. (1991). Electron transfer properties of NADH:ubiquinone reductase in the ND1/3460 and ND4/11 778 mutations of the Leber hereditary optic neuroretinopathy (LHON). FEBS Letters, 292, 289-292.
67. Miller, N. R. (1982). The hereditary optic neuropathies. In Walsh and Hoyt's clinical neuro-ophthalmology, 4th Edn (pp. 311-317). Baltimore: Williams & Wilkins.
68. Minckler, D. S., McLean, I. W. & Tso, M. O. M. (1976). Distribution of axonal and glial elements in the Rhesus optic nerve head studied by electron microscopy. American Journal of Ophthalmology, 82, 179-187.
69. Montagna, P., Plazzi, G., Cortelli, P., Carelli, V., Lugaresi, E., Barboni, P. & Fiocchi, M. (1995). Abnormal lactate after effort in healthy carriers of Leber's hereditary optic neuropathy. Journal of Neurology, Neurosurgery & Psychiatry, 58, 640-641.
70. Morrissey, S. P., Borruat, F. X., Miller, D. H., Moseley, I. F., Sweeney, M. G., Govan, G. G., Kelley, M. A., Francis, D. A., Harding, A. E. & McDonald, W. I. (1995). Bilateral simultaneous optic neuropathy in adults: Clinical, imaging, serological, and genetic studies. Journal of Neurology, Neurosurgery & Psychiatry, 58, 70-74.
71. Newman, N. J., Lott, M. T. & Wallace, D. C. (1991). The clinical characteristics of pedigrees of Leber's hereditary optic neuropathy with the 11 778 mutation. American Journal of Ophthalmology, 111, 750-762.
72. Newman, N. J., Torronim, A., Brown, M. D., Lott, M. T., Fernandez, M. M., Wallace, D. C. & The Cuba Neuropathy Field Investigation Team (1994). Epidemic neuropathy in Cuba not associated with mitochondrial DNA mutations found in Leber's hereditary optic neuropathy patients. American Journal of Ophthalmology, 118, 158-168.
73. Nikoskelainen, E. K. (1994). Clinical picture of LHON. Clinical Neuroscience, 2, 115-120.
74. Nikoskelainen, E., Savontaus, M.-L., Wanne, O. P., Katila, M. J. & Nummelin, K. U. (1987). Leber's hereditary optic neuropathy, a maternally inherited disease: A genealogical study in four pedigrees. Archives of Ophthalmology, 105, 665-671.
75. Nikoskelainen, E. K., Marttila, R. J., Huoponen, K., Juvonen, V., Lamminen, T., Sonninen, P. & Savontaus, M.-L. (1995). Leber's "plus": Neurological abnormalities in patients with Leber's hereditary optic neuropathy. Journal of Neurology, Neurosurgery & Psychiatry, 59, 160-164.
76. Nikoskelainen, E. K., Huoponen, K., Juvonen, V., Lamminen, T., Nummelin, K. & Savontaus, M.-L. (1996). Ophthalmologic findings in Leber hereditary optic neuropathy, with special reference to mtDNA mutations. Ophthalmology, 103, 504-514.
77. Ochs, S. (1971). Local supply of energy to the fast axoplasmic transport mechanism. Proceedings of the National Academy of Sciences of the U.S.A., 68, 1279-1282.
78. Oostra, R. J., Bolhuis, P. A., Wijburg, F. A., Zorn-Ende, G. & BleekerWagemakers, E. M. (1994). Leber's hereditary optic neuropathy: Correlations between mitochondrial genotype and visual outcome. Journal of Medical Genetics, 31, 280-286.
79. Oostra, R.-J., Van Galen, M. J. M., Bolhuis, P. A., BleekerWagemakers, E. M. & Van den Bogert, C. (1995). The mitochondrial DNA mutation ND6*14,484C associated with Leber hereditary optic neuropathy, leads to deficiency of complex I of the respiratory chain. Biochemical and Biophysical Research Communication, 215, 1001-1005.
80. Parker, W. D. Jr, Oley, C. A. & Parks, J. K. (1989). A defect in mitochondrial electron-transport activity (NADH-coenzyme Q oxidoreductase) in Leber's hereditary optic neuropathy. New England Journal of Medicine, 320, 1331-1333.
81. Pegoraro, E., Carelli, V., Zeviani, M., Cortelli, P., Montagna, P., Barboni, P., Angelini, C. & Hoffman, E. P. (1996). X-inactivation patterns in female Leber's hereditary optic neuropathy patients do not support a strong X-linked determinant. American Journal of Medical Genetics, 61, 356-362.
82. Quigley, H. A. (1995). Ganglion cell death in glaucoma: Pathology recapitulates ontogeny. Australian and New Zealand Journal of Ophthalmology, 23, 85-91.
83. Quigley, H. A., Dunkelberger, G. R. & Green, W. R. (1988). Chronic human glaucoma causing selectively greater loss of large optic nerve fibers. Ophthalmology, 95, 357-363.
84. Quigley, H. A., Nickells, R. W., Kerrigan, L. A., Pease, M. E., Thibault, D. J. & Zack, D. J. (1995). Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Investigative Ophthalmology and Visual Science, 36, 774-786.
85. Radius, R. L. & Gonzales, M. (1981). Anatomy of the lamina cribosa in human eyes. Archives of Ophthalmology, 99, 2159-2162.
86. Riordan-Eva, P., Sanders, M. D., Govan, G. G., Sweeney, M. G., Da Costa, J. & Harding, A. E. (1995). The clinical features of Leber's hereditary optic neuropathy defined by the presence of a pathogenic mitochondrial DNA mutation. Brain, 118, 319-338.
87. Rizzo, J. F. III (1995). Adenosine triphosphate deficiency: A genre of optic neuropathy. Neurology, 45, 11-16.
88. Sadun, A. A. & Dao, J. (1994). Annual review in neuro-ophthalmology. The anterior visual pathways. Journal of Neuro-ophthalmology, 14, 141-154.
89. Sadun, A. A., Kashima, Y., Wurdeman, A. E., Dao, J., Heller, K. & Sherman, J. (1994). Morphological findings in the visual system in a case of Leber's hereditary optic neuropathy. Clinical Neuroscience, 2, 165-172.
90. Schumer, R. A. & Podos, S. M. (1994). The nerve of glaucoma! Archives of Ophthalmology, 112, 37-44.
91. Seedorff, T. (1970). The inheritance of Leber's disease: A genelogic follow-up study. Acta Ophthalmologica, 163, 133-145.
92. van Senus, A. H. C. (1963). Leber's disease in the Netherlands. Documenta Ophthalmologica, 17, 1-162.
93. Sherman, J. & Kleiner, L. (1994). Visual system dysfunction in Leber's hereditary optic neuropathy. Clinical Neuroscience, 2, 121-129.
94. Smith, K. H., Johns, D. R., Heher, K. L. & Miller, N. R. (1993). Heteroplasmy in Leber's hereditary optic neuropathy. Archives of Ophthalmology, 111, 1486-1490.
95. Smith, J. L., Tse, D. T., Byrne, S. F., Johns, D. R. & Stone, E. M. (1990). Optic nerve sheath distension in Leber's optic neuropathy and the significance of the "Wallace Mutation". Journal of Clinical Neuro-ophthalmology, 10, 231-238.
96. Smith, P. R., Cooper, J. M., Govan, G. G., Harding, A. E. & Schapira, A. H. V. (1994). Platelet mitochondrial function in Leber's hereditary optic neuropathy. Journal of Neurological Sciences, 122, 80-83.
97. Swartz, N. & Savino, P. J. (1994). Is all nondefinable optic atrophy Leber's hereditary optic neuropathy? Survey of Ophthalmology, 39, 146-150.
98. Sweeney, M. G., Davis, M. B., Lashwood, A., Brockington, M., Toscano, A. & Harding, A. E. (1992). Evidence against an X-linked locus close to DXS7 determining visual loss susceptibility in British and Italian families with Leber hereditary optic neuropathy. American Journal of Human Genetics, 51, 741-748.
99. Vergani, L., Martinuzzi, A., Carelli, V., Cortelli, P., Montagna, P., Schievano, G., Carrozzo, R., Angelini, C. & Lugaresi, E. (1995). MtDNA mutations associated with Leber's hereditary optic neuropathy: Studies on cytoplasmic hybrid (cybrid) cells. Biochemical and Biophysical Research Communication, 210, 880-888.
100. Vilkki, J., Ott, J., Savontaus, M.-L., Aula, P. & Nikoskelainen, E. K. (1991). Optic atrophy Leber hereditary optic neuroretinopathy is probably determined by an X-chromosomal gene closely linked to DXS7. American Journal of Human Genetics, 48, 486-491.
101. Wakakura, M. & Yokoe, J. (1995). Evidence for preserved direct pupillary light response in Leber's hereditary optic neuropathy. British Journal of Ophthalmology, 79, 442-446.
102. Wallace, D. C. (1970). A new manifestation of Leber's disease and a new explanation for the agency responsible for its unusual pattern of inheritance. Brain, 93, 121-132.
103. Wallace, D. C. (1995). Mitochondrial DNA variation in human evolution, degenerative disease, and aging. American Journal of Human Genetics, 57, 201-223.
104. Weiner, N. C., Newman, N. J., Lessell, S., Johns, D. R., Lott, M. T. & Wallace, D. C. (1993). Atypical Leber's hereditary optic neuropathy with molecular confirmation. Archives of Neurology, 50, 470-473.
105. Wilson, D. R. & Kline, L. B. (1992). Untitled letter to the editor. Journal of Clinical Neuro-ophthalmology, 12, 73-74.
106. Wilson, J. (1963). Leber's hereditary optic atrophy. Some clinical and aetiological considerations. Brain, 86, 347-362.
107. Wood, K. A. & Youle, R. J. (1995). The role of free radicals and p53 in neuron apoptosis in vivo. Journal of Neuroscience, 15, 5851-5857.
108. Wygnanski, T., Desatnik, H., Quigley, H. A. & Glovinsky, Y. (1995). Comparison of ganglion cell loss and cone loss in experimental glaucoma. American Journal of Ophthalmology, 120, 184-189.