Neurobiology of Huntington's disease

Neurobiology of Disease

Volumn 3, Issue 1, 1996, Pages 3-15

  Sharp, Alan H ^a   Ross, Christopher A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITOTOXIN; FREE RADICAL; TRINUCLEOTIDE;

APOPTOSIS; GENE EXPRESSION; HUMAN; HUNTINGTON CHOREA; NERVE DEGENERATION; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; REVIEW;

EID: 0029991245     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.1996.0002     Document Type: Review

References (129)

1. 2+ signal transduction. J Biol. Chem. 267, 13361-13368.
2. Adler, A. J., Danielsen, M., & Robins, D. M. (1992) Androgen-specific gene activation via a consensus glutocorticoid response element is determined by interaction with nonreceptor factors. Proc. Natl. Acad. Sci. USA 89, 11660-11663.
3. Albin, R. L., & Greenamyre, J. T. (1992) Alternative excitotoxic hypotheses. Neurology 42, 733-738.
4. Albin, R. L. (1995) Selective neurodegeneration in Huntington's disease. Ann. Neurol. 38, 835-836.
5. Albin, R. L., & Tagle, D. A. (1995) Genetics and molecular biology of Huntington's disease. Trends Neurosci. 18, 11-14.
6. Albin, R. I., Young, A. B., & Penney, J. B. (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 365-375.
7. Albin, R. L., Reiner, A., Anderson, K. D., Dure, L. S., IV, Handelin, B., Balfour, R., Whetsell, W. O., Penney, J. B., & Young, A. B. (1992) Preferential loss of striato-external pallidal projection neurons in presymptomatic Huntington's disease. Ann. Neurol. 31, 425-430.
8. Ambrose, C. M., Duyao, M. P., Barnes, G., Bates, G. P., Lin, C. S., Srinidhi, J., Baxendale, S., Hummerich, H., Lehrach, H., Altherr, M., Wasmuth, J., Buckler, A., Church, D., Housman, D., Berks, M., Micklem, G., Durbin, R., Dodge, A., Read, A., Gusella, J., & MacDonald, M. E. (1994) Structure and expression of the Huntington's disease gene: Evidence against simple inactivation due to an expanded CAG repeat. Somat. Cell Mol. Genet. 20, 27-38.
9. Andrade, M. A., & Bork, P. (1995) HEAT repeats in the Huntington's disease protein. Nature Genet. 11, 115-116.
10. Aronin, N., Chase, K., Young, C., Sapp, E., Schwartz, C., Matta, N., Kornreich, R., Landwehrmeyer, B., Bird, E., Beal, M. F., Vonsattel, J.-P., Smith, T., Carraway, R., Boyee, F. M., Young, A. B., Penney, J. B., & DiFiglia, M. (1995) CAG expansion affects the expression of mutant huntingtin in the Huntington's disease brain. Neuron 15, 1193-1201.
11. Aronin, N., & DiFiglia, M. (1995) Clues to Huntington's normal and abnormal function. J. NIH Res. 7, 55-56.
12. Aylward, E. H., Brandt, J., Codori, A. M., Mangus, R. S., Barta, P. E., & Harris, G. J. (1994) Reduced basal ganglia volume associated with the gene for Huntington's disease in asymptomatic at-risk persons. Neurology 44, 823-828.
13. Bao, J., Sharp, A. H., Wagster, M. V., Becher, M., Schilling, G., Ross, C. A., Dawson, V. L., & Dawson, T. M. (1996) Expansion of polyglutamine repeat in huntingtin leads to abnormal protein interactions involving calmodulin. Proc. Natl. Acad. Sci. USA, in press.
14. Barnes, G. T., Duyao, M. P., Ambrose, C. M., McNeil, S., Persichetti, F., Srinidhi, J., Gusella, J. F., & MacDonald, M. E. (1994) Mouse Huntington's disease gene homolog (Hdh). Somat. Cell Mol. Genet. 20, 87-97.
15. Baxendale, S., Abdulla, S., Elgar, G., Buck, D., Berks, M., Micklem, G., Durbin, R., Bates, G., Brenner, S., Beck, S., & Lehrach, H. (1995) Comparative sequence analysis of the human and pufferfish Huntington's disease genes. Nature Genet. 10, 67-76.
16. Beal, M. F., Kowall, N. W., Ellison, D. W., Mazurek, M. F., Swartz, K. J., & Martin, J. B. (1986) Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature 321, 168-171.
17. Beal, M. F., Ferrante, R. J., Swartz, K. J., & Kowall, N. W. (1991) Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J. Neurosci. 11, 1649-1659.
18. Beal, M. F., Brouillet, E., Jenkins, B., Henshaw, R., Rosen, B., & Hyman, B. T. (1993a) Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J. Neurochem. 61, 1147-1150.
19. Beal, M. F., Brouillet, E., Jenkins, B. G., Ferrante, R. J., Kowall, N. W., Miller, J. M., Storey, E., Srivastava, R., Rosen, B. R., & Hyman, B. T. (1993b) Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13(10), 4181-4192.
20. Beal, M. F., Hyman, B. T., & Koroshetz, W. (1993c) Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases? Trends Neurosci. 16, 125-131.
21. Beal, M. F., Finn, S. E, & Brouillet, E. (1993d) Evidence for the involvement of metabotropic glutamate receptors in striatal excitotoxin lesions in vivo. Neurodegeneration 2, 81-91.
22. Beal, M. F., (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann. Neurol. 38, 357-366.
23. Bredesen, D. E. (1995) Neural apoptosis. Ann. Neurol. 38, 839-851.
24. Bredt, D. S., & Snyder, S. H. (1992) Nitric oxide, a novel neuronal messenger. Neuron 8, 3-11.
25. Brenman, J. E., Chao, D. S., Xia, H., Aldape, K., & Bredt, D. S. (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in duchenne muscular dystrophy. Cell 82, 743-752.
26. Brouillet, E., Jenkins, B. G., Hyman, B. T., Ferrante, R. J., Kowall, N. W., Srivastava, R., Roy, D. S., Rosen, B. R., & Beal, M. F. (1993) Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J. Neurochem. 60, 356-369.
27. Brouillet, E., Hantraye, P., Ferrante, R. J., Dolan, R., Leroy-Willig, A., Kowall, N. W., & Beal, M. F. (1995) Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc. Natl. Acad. Sci. USA 92, 7105-7109.
28. Burke, J. R., Enghild, J. J., Martin, M. E., Jou, Y. S., Myers, R. M., Roses, A. D., Vance, J. M., & Strittmatter, W. J. (1996) Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nature Med. 2, 347-350.
29. Choi, D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
30. Choi, D. W. (1992) Bench to bedside: The glutamate connection. Science 258, 241-243.
31. Copp, A. J. (1995) Death before birth: Clues from gene knockouts and mutations. Trends Genet. 11, 87-93.
32. Corral-Debrinski, M., Horton, T., Lott, M. T., Shoffner, J. M., Beal, M. F., & Wallace, D. C. (1992) Mitochondrial DNA deletions in human brain: Regional variability and increase with advanced age. Nature Genet. 2, 324-329.
33. Cotman, C. W., Monaghan, D. T., Ottersen, O. P., & Storm-Mathisen, J. (1987) Anatomical organization of excitatory amino acid receptors and their pathways. Trends Neurosci. 10, 273-280.
34. Coyle, J. T., & Schwarcz, R. (1976) Lesion of striatal neurones with kainic acid provides a model for Huntington's chorea. Nature 263, 244-246.
35. Coyle, J. T., & Puttfarcken, P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.
36. Cudkowicz, M., & Kowall, N. W. (1990) Degeneration of pyramidal projection neurons in Huntington's disease cortex. Ann. Neurol. 27, 200-204.
37. Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S., & Snyder, S. H. (1991a) Nitric oxide mediates glutamate neurotoxicity in primary cortical culture. Proc. Natl. Acad. Sci. USA 88, 6368-6371.
38. Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M., & Snyder, S. H. (1991b) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Nat/. Acad. Sci. USA 88, 7797-7801.
39. Dawson, T. M., Dawson, V. L., & Snyder, S. H. (1992) A novel neuronal messenger molecule in brain: The free radical, nitric oxide. Ann. Neurol. 32, 297-311.
40. Dawson, T. M., & Snyder, S. H. (1994) Gases as biological messengers: Nitric oxide and carbon monoxide in the brain. J. Neurosci. 14, 5147-5159.
41. Dawson, V. L., Dawson, T. M., Bartley D. A., Uhl, G. R., & Snyder, S. H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661.
42. Dawson, V. L., Huang, P. L., Fishman, M. C., Snyder, S. H., & Dawson, T. M. (1995) Primary cortical neuronal cultures from neuronal NOS null mics are resistant to glutamate neurotoxicity. Soc. Neurosci. 21, 520.
43. de la Monte, S. M., Vonsattel, J-P., & Richardson, E. P. (1988) Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. J. Neuropathol. Exp. Neurol. 47, 516-525.
44. DiFiglia, M., & Carey, J. (1986) Large neurons in the primate neostriatum examined with the combined Golgi-electron microscopic method. J. Comp. Neurol. 244, 36-52.
45. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonsattel, J-P., Carraway, R., Reeves, S. A., Boyce, F. M., & Aronin, N. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14, 1075-1081.
46. Dom, R., Malfroid, M., & Baro, F. (1976) Neuropathology of Huntington's chorea. Studies of the ventrobasal complex of the thalamus. Neurology 26, 64-68.
47. Dragunow, M., Faull, R. L. M., Lawlor, P., Beilharz, E. J., Singleton, K., Walker, E. B., & Mee, E. (1995) In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimer's disease temporal lobes. Neuroreport 6, 1053-1057.
48. Dugan, L. L., Sensi, S. L., Canzoniero, L. M. T., Handran, S. D., Rothman, S. M., Lin, T.-S., Goldberg, M. P., & Choi, D. W. (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.
49. Duyao, M. P., Auerbach, A. B., Ryan, A., Persichetti, F., Barnes, G. T., McNeil, S. M., Ge, P., Vonsattel, J.-P., Gusella, J. F., Joyner, A. L., & MacDonald, M. E. (1995) Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269, 407-410.
50. Faber, P. W., King, A., van Rooji, H. C. J., Brinkmann, A. O., de Both, N. J., & Trapman, J. (1991) The mouse androgen receptor: Functional analysis of the protein and characterization of the gene. Biochem J. 278, 269-278.
51. Ferrante, R. J., Kowall, N. W., Beal, M. F., Richardson, E. P., Jr., Bird, E. D., & Martin, J. B. (1985) Selective sparing of a class of striatal neurons in Huntington's disease. Science 230, 561-563.
52. Ferrante, R. J., Kowall, N. W., Beal, M. F., Martin, J. B., Bird, E. D., & Richardson, E. P. Jr. (1987) Morphologic and histochemical characteristics of a spared subset of striatal neurons in Huntington's disease. J. Neuropathol. Exp. Neurol. 46, 12-27.
53. Folstein, S. E. (1989) Huntington's Disease. A Disorder of Families. The Johns Hopkins Press, Baltimore, MD.
54. Gerber, H.-P., Seipel, K., Georgiev, O., Höfferer, M., Hug, M., Rusconi, S., & Schaffner, W. (1994) Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263, 808-811.
55. Graveland, G. A., Williams, R. S., & DiFiglia, M. (1985a) A Golgi study of the human neostriatum: Neurons and afferent fibers. J. Comp. Neurol. 234, 317-333.
56. Graveland, G. A., Williams, R. S., & DiFiglia, M. (1985b) Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 227, 770-773.
57. Green, H. (1993) Human genetic diseases due to codon reiteration: Relationship to an evolutionary mechanism. Cell 74, 955-956.
58. Green, H., & Wang, N. (1994) Codon reiteration and the evolution of proteins. Proc. Natl. Acad. Sci. USA 91, 4298-4302.
59. Greene, J. C., & Greenamyre, J. T. (1995) Manipulation of membrane potential modulates malonate-induced striatal excitotoxicity in vivo. Soc. Neurosci. Abst. 21, 1039.
60. Gutekunst, C.-A., Levey, A. I., Heilman, C. J., Whaley, W. L., Yi, H., Nash, N. R., Rees, H. D., Madden, J. J., & Hersch, S. M. (1995) Identification and localization of huntingtin in brain and human lymphoblastoid cell lines with anti-fusion protein antibodies. Proc. Natl. Acad. Sci. USA 92, 8710-8714.
61. Harper, P. S. (1991) Huntington's Disease. W. B. Saunders, London.
62. Hayden, M. R. (1981) Huntington's Chorea. Springer-Verlag, Berlin.
63. Hedreen, J. C., Peyser, C. B., Folstein, S. B., & Ross, C. A. (1991) Neuronal loss in layers V and VI of cerebral cortex in Huntington's disease. Neurosci. Lett. 133, 257-261.
64. Hedreen, J. C., & Folstein, S. E. (1995) Early loss of neostriatal striosome neurons in Huntington's disease. J. Neuropathol. Exp. Neurol. 54, 105-120.
65. Hedreen, J. C., & Ross, C. A. (1995) Huntington's Disease. In: The Primary Degenerative Dementias Other Than Alzheimer's Disease, (A. W. Clark & D. W. Dickson, Eds.), Carolina Academic Press, Durham, NC.
66. Hoogeveen, A. T., Willemsen, R., Meyer, N., de Rooij, K. E., Roos, R. A. C., van Ommen, G.-J. B., & Galjaard, H. (1993) Characterization and localization of the Huntington disease gene product. Hum. Mol. Genet. 2, 2069-2073.
67. 28k immunoactivity in rat striatal neurons in vivo and in vitro mimic the pattern seen in Huntington's disease. Neuroscience 65, 397-407.
68. Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983.
69. Huntington, G. (1872) On chorea. Med. Surg. Rep. 26, 317-321.
70. Huttner, W. B., Schiebler, W., Greengard, P, & De Camilli, P. (1983) Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. ni. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374-1388.
71. Ide, K., Nukina, N., Masuda, N., Goto, J., & Kanazawa, I. (1995) Abnormal gene product identified in Huntington's disease lymphocytes and brain. Biochem. Biophys. Res. Commun. 209, 1119-1125.
72. Jackson, M., Gentleman, S., Lennox, G., Ward, L., Gray, T., Randall, K., Morrel, K., & Lowe, J. (1995) The cortical neuritic pathology of Huntington's disease. Neuropathol. Appl. Neurobiol. 21, 18-26.
73. Jou, Y.-S., & Myers, R. M. (1995) Evidence from antibody studies that the CAG repeat in the Huntington disease gene is expressed in the protein. Hum. Mol. Genet. 4, 465-469.
74. Kowall, N. W., Ferrante, R. J., & Martin, J. B. (1987) Patterns of cell loss in Huntington's disease. Trends Neurosci. 10, 24-29.
75. Kremer, B., Swaab, D., Bots, G., Fisser, B., Ravid, R., & Roos, R. (1991) The hypothalamic lateral tuberal nucleus in Alzheimer's disease. Ann. Neurol. 29, 279-284.
76. Kremer, B., Tallaksen-Green, S. J., & Albin, R. L. (1993) AMPA & NMDA binding sites in the hypothalamic lateral tuberal nucleus: Implications for Huntington's disease. Neurology, 43, 1593-1595.
77. Kremer, H. P. H., Roos, R. A. C., Dingjan, G., Marani, E., & Bots, G. T. A. M. (1990) Atrophy of the hypothalamic lateral tuberal nucleus in Huntington's disease. J. Neuropathol. Exp. Neurol. 49, 371-382.
78. La Spada, A. R., Wilson, E. M., Lubahn, D. B., Harding, A. E., & Fischbeck, K. H. (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352, 77-79.
79. La Spada, A. R., Paulson, H. L., & Fischbeck, K. H. (1994) Trinucleotide repeat expansion in neurological disease. Ann. Neurol. 36, 814-822.
80. Landwehrmeyer, G. B., McNeil, S. M., Dure, L. S., Ge, P., Aizawa, H., Huang, Q., Ambrose, C. M., Duyao, M. P., Bird, E. D., Bonilla, E., de Young, M., Avila-Gonzales, A. J., Wexler, N. S., DiFiglia, M., Gusella, J. F., MacDonald, M. D., Penney, J. B., Young, A. B., & Vonsattel, J.-P. (1995) Huntington's disease gene: Regional and cellular expression in brain of normal and affected individuals. Ann. Neurol. 37, 218-230.
81. Lange, H., Thörner, G., Hopf, A., & Schröder, K. F. (1976) Morphometric studies of the neuropathological changes in choreatic diseases. J. Neurol. Sci. 28, 401-425.
82. Lasek, R. J. (1981) Cytoskeletons and cell motility in the nervous system. In: Basic Neurochemistry (G. J. Siegel, R. W. Albers, B. W. Agranoff, & R. Katzman, Eds.), pp. 403-412. Little, Brown & Co., Boston, MA.
83. Li, X-J., Li, S-H., Sharp, A. H., Nucifora, F. C., Jr., Schilling, G., Lanahan, A., Worley, P., Snyder, S. H., & Ross, C. A. (1995) A Huntingtin-associated protein enriched in brain with implications for pathology. Nature 378, 398-402.
84. Li, X.-J., Sharp, A. H., Li, S.-H., Dawson, T. M., Snyder, S. H., & Ross, C. A. Huntingtin associated protein (HAP1): Discrete neuronal localizations in the brain resemble neuronal nitric oxide synthase. Proc. Natl. Acad. Sci. USA, in press.
85. Lin, B., Nasir, J., MacDonald, H., Hutchinson, G., Graham, R. K., Rommens, J. M., & Hayden, M. R. (1994) Sequence of the murine Huntington disease gene: Evidence for conversation, and polymorphism in a triplet (CCG) repeat alternate splicing. Hum. Mol. Genet. 3, 85-92.
86. Ludolph, A. C., He, F., Spencer, P. S., Hammerstad, J., & Sabri, M. (1991) 3-Nitropropionic acid-exogenous animal neurotoxin and possible human striatal toxin. Can. J. Neurol. Sci. 18, 492-498.
87. McGeer, E. G., McGeer, P. L., & Singh, K. (1978) Kainate-induced degeneration of neostriatal neurons: Dependency upon corticostriatal tract. Brain Res. 139, 381-383.
88. McPherson, P. S., Takei, K., Schmid, S. L., & De Camilli, P. (1994) p145, a major Grb2-binding protein in brain, is co-localized with dynamin in nerve terminals where it undergoes activity-dependent dephosphorylation. J. Biol. Chem. 48, 30132-30139.
89. 3H]glutamate-binding sites in rat brain. J. Neurosci. 5, 2909-2919.
90. Monaghan, D. T., Bridges, R. J., & Cotman, C. W. (1989) The excitatory amino acid receptors: Their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29, 365-402.
91. Myers, R. H., Vonsattel, J. P., Stevens, T. J., Cupples, L. A., Richardson, E. P., Martin, J. B., & Bird, E. D. (1988) Clinical and neuropathologic assessment of severity in Huntington's disease. Neurology 38, 341-347.
92. Nasir, J., Floresco, S. B., O'Kusky, J. R., Diewert, V. M., Richman, J. M., Zeisler, J., Borowski, A., Marth, J. D., Phillips, A. G., & Hayden, M. R. (1995) Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81, 811-823.
93. Okamoto, N., Hori, S., Akazawa, C., Hayashi, Y., Shigemoto, R., Mizuno, N., & Nakanishi, S. (1994) Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J. Biol. Chem. 269, 1231-1236.
94. Persichetti, F., Ambrose, C. M., Ge, P., McNeil, S. M., Srinidhi, J., Anderson, M. A., Jenkins, B., Barnes, G. T., Duyao, M. P., Kanaley, L., Wexler, N. S., Myers, R. H., Bird, E. D., Vonsattel, J.-P., MacDonald, M. E., & Gusella, J. F. (1995) Normal and expanded Huntington's disease gene alleles produce distinguishable proteins due to translation across the CAG repeat. Mol. Med. 1, 374-383.
95. Perutz, M., Johnson, T., Suzuki, M., & Finch, J. T. (1994) Glutamine repeats as polar zippers: Their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 91, 5355-5358.
96. Perutz, M. (1994) Polar zippers: Their role in human disease. Protein Sci. 3, 1629-1637.
97. Portera-Cailliau, C., Hedreen, J. C., Price, D. L., & Koliatsos, V. E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. j. Neurosci. 15(5), 3775-3787.
98. Reiner, A., Albin, R. L., Anderson, K. D., D'Amato, C. J., Penney, J. B., & Young, A. B. (1988) Differential loss of striatal projection neurons in Huntington disease. Proc. Natl. Acad. Sci. USA 85, 5733-5737.
99. Richfield, E. K., Maguire-Zeiss, K. A., Vonkeman, H. E., & Voorn, P. (1995) Preferential loss of preproenkephalin versus preprotachykinin neurons from the striatum of Huntington's disease patients. Ann. Neurol. 38, 852-861.
100. Ross, C. A., McInnis, M. G., Margolis, R. L., & Li, S-H. (1993) Genes with triplet repeats: Candidate mediators of neuropsychiatrie disorders. Trends Neurosci. 16, 254-260.
101. Ross, C. A. (1995) When more is less: Pathogenesis of glutamine repeat neurodegenerative diseases. Neuron 15, 493-496.
102. Sapp, E., Ge, P., Aizawa, H., Bird, E., Penney, J., Young, A. B., Vonsattell, J.-P., & DiFiglia, M. (1995) Evidence for a preferential loss of enkephalin immunoreactivity in the external globus pallidus in low grade Huntington's disease using high resolution image analysis. Neuroscience 64, 397-404.
103. Schilling, G., Sharp, A. H., Loev, S. J., Wagster, M. V., Li, S.-H., Stine, O. C., & Ross, C. A. (1995) Expression of the Huntington's disease (IT15) protein product in HD patients. Hum. Mol. Genet. 4, 1365-1371.
104. Schmitt, I., Bächner, D., Megow, D., Henklein, P., Hameister, H., Epplen, J. T., & Riess, O. (1995) Expression of the Huntington disease gene in rodents: Cloning of the rat homologue and evidence for downregulation of non-neuronal tissues during development. Hum. Mol. Genet. 4, 1173-1182.
105. Schulz, J. B., Henshaw, D. R., Siwek, D., Jenkins, B. G., Ferrante, R. J., Cipolloni, P. B., Kowal, N. W., Rosen, B. R., & Beal, M. F. (1995) Involvement of free radicals in excitotoxicity in vivo. J. Neurochem. 64, 2239-2247.
106. Schulz, J. B., Matthews, R. T., Jenkins, B. G., Ferrante, R. J., Siwek, D., Henshaw, D. R., Cipolloni, P. B., Mecocci, P., Kowall, N. W., Rosen, B. R., & Beal, M. F. (1995) Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J. Neurosci. 15, 8419-8429.
107. Sharp, A. H., Loev, S. J., Schilling, G., Li, S-H., Li, X-J., Bao, J., Wagster, M. V., Kotzuk, J. A., Steiner, J. P., Lo, A., Hedreen, J., Sisodia, S., Snyder, S. H., Dawson, T. M., Ryugo, D. K., & Ross, C. A. (1995) Widespread expression of the Huntington's disease gene (IT-15) protein product. Neuron 14, 1065-1074.
108. Shoffner, J. M., Brown, M. D., Stugard, C., Jun, A. S., Pollock, S., Haas, R. H., Kaufman, A., Koontz, D., Kim, Y., Graham, J. R., Smith, E., Dixon, J., & Wallace, D. C. (1995) Leber's hereditary optic neuropathy plus dystonia is caused by a mitochondrial DNA point mutation. Ann. Neurol. 38, 163-169.
109. Sotrel, A., Paskevich, P. A., Kiely, D. K., Bird, E. D., Williams, R. S., & Myers, R. H. (1991) Morphometric analysis of the prefrontal cortex in Huntington's disease. Neurology 41, 1117-1123.
110. Stine, O. C., Li, S-H., Pleasant, N., Wagster, M. V., Hedreen, J. C., & Ross, C. A. (1995) Expression of the mutant allele of IT-15 (the HD gene) in striatum and cortex of Huntington's disease patients. Hum. Mol. Genet. 4(1), 15-18.
111. Stott, K., Blackburn, J. M., Butler, P. J. G., & Perutz, M. (1995) Incorporation of glutamine repeats makes protein oligomerize: Implications for neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 92, 6509-6513.
112. Strong, T. V., Tagle, D. A., Valdes, J. M., Elmer, L. W., Boehm, K., Swaroop, M., Kaatz, K. W., Collins, F. S., & Albin, R. L. (1993) Widespread expression of the human and rat Huntington's disease gene in brain and nonneuronal tissues. Nature Genet. 5, 259-265.
113. Takel, K., McPherson, P. S., Schmid, S. L., & De Camilli, P. (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature 374, 186-192.
114. Testa, C. M., Standaert, D. G., Young, A. B., & Penney, J. B., Jr. (1994) Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J. Neurosci. 14, 3005-3018.
115. Testa, C. M., Standaert, D. G., Landwehrmeyer, G. B., Penney, J. B., Jr., & Young, A. B. (1995) Differential expression of mGluRS metabotropic glutamate receptor mRNA by rat striatal neurons. J. Comp. Neurol. 354, 241-252.
116. Thomas, L. B., Gates, D. J., Ridifield, E. K., O'Brien, T E, Schweitzer, J. B., & Steindler, D. A. (1995) DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp. Neurol. 133, 265-272.
117. Trottier, Y., Devys, D., Imbert, G., Saudou, F., An, I., Lutz, Y., Weber, C., Agid, Y., Hirsch, E. C., & Mandel, J-L. (1995a) Cellular localization of the Huntington's disease protein and discrimination of the normal and mutated form. Nature Genet. 10, 104-110.
118. Trottier, Y., Lutz, Y., Stevanin, G., Imbert, G., Devys, D., Cancel, G., Saudou, F., Weber, C., David, G., Tora, L., Agid, Y., Brice, A., & Mondel, J.-L. (1995b) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378, 403-406.
119. 3H]kainic acid binding sites in the rat forebrain. Eur. J. Pharmacol. 86, 361-371.
120. Vonsattel, J-P., Myers, R. H., Stevens, T. J., Ferrante, R. J., Bird, E. D., & Richardson, E. P., Jr. (1985) Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44, 559-577.
121. 3H]AMPA binding in layer VI of frontal cortex in Huntington's disease. Exp. Neurol. 127, 70-75.
122. Wexler, N. S., Young, A. B., Tanzi, R. E., Travers, H., StarostaRuubinstein, S., Penney, J. B., Snodgrass, S. R., Shoulson, I., Gomez, F., Arroyo, M. A. R., Penchaszadeh, G. K., Moreno, H., Gibbons, K., Faryniarz, A., Hobbs, W., Anderson, M. A., Bonilla, E., Conneally, P. M., & Gusella, J. F. (1987) Homozygotes for Huntington's disease. Nature 326, 194-197.
123. Wullner, U., Young, A. B., Penney, J. B., & Beal, M. F. (1994) 3-nitropropionic acid toxicity in the striatum. J. Neurochem. 63, 1772-1781.
124. Wyllie, A. H. (1981) Cell death: A new classification separating apoptosis from necrosis. In: Cell Death in Biology and Pathology (I. D. Bowen & R. A. Lockshin, Eds.), pp. 9-34. Chapman and Hall, New York.
125. Young, A. B., Greenamyre, J. T., Hollingsworth, Z., Albin, R., D'Amato, C., Shoulson, I., & Penney, J. B. (1988) NMDA receptor losses in putamen from patients with Huntington's disease. Science 241, 981-983.
126. Young, A. B., & Fagg, G. E. (1990) Excitatory amino acid receptors in the brain: Membrane binding and receptor autoradiographic approaches. Trends Pharmacol. Sci. 11, 126-133.
127. Zech, M., Roberts, G. W., Bogerts, B., Crow, T. J., & Polak, J. M. (1986) Neuropeptides in the amygdala of controls, schizophrenics and patients suffering from Huntington's chorea: An immunohistochemical study. Acta Neuropathol (Berlin) 71, 259-266.
128. Zeitlin, S., Liu, J-P., Chapman, D. L., Papaioannou, V. E., & Efstratiadis, A. (1995) Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nature Genet. 11, 155-163.
129. Zweig, R. M., Koven, S. J., Hedreen, J. C., Maestri, N. E., Kazazian, H. H., & Folstein, S. E. (1989) Linkage to the Huntington's disease locus in a family with unusual clinical and pathological features. Ann. Neurol. 26, 78-84.