Abnormal association of mutant huntingtin with synaptic vesicles inhibits glutamate release

Human Molecular Genetics

Volumn 12, Issue 16, 2003, Pages 2021-2030

  Li, He ^a,b   Wyman, Travis ^a   Yu, Zhao Xue ^a   Li, Shi Hua ^a   Li, Xiao Jiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; HUNTINGTIN; MUTANT PROTEIN; NEUROTRANSMITTER;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; BRAIN REGION; BRAIN SLICE; CELL AGGREGATION; CELL FRACTIONATION; CELL FUNCTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE MUTATION; GENETIC ASSOCIATION; HUNTINGTON CHOREA; MOUSE; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; REVIEW; SYNAPSE VESICLE; TRANSGENIC MOUSE;

ANIMALS; BRAIN CHEMISTRY; GLUTAMIC ACID; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PRESYNAPTIC TERMINALS; RECOMBINANT FUSION PROTEINS; SYNAPTIC VESICLES;

ANIMALIA; MUS MUSCULUS;

EID: 0042921188     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg218     Document Type: Review

References (54)

1. Vonsattel, J.P., Myers, R.H., Stevens, T.J., Ferrante, R.J., Bird, E.D. and Richardson, E.P. Jr (1985) Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol., 44, 559-577.
2. Cudkowicz, M. and Kowall, N.W. (1990) Degeneration of pyramidal projection neurons in Huntington's disease cortex. Ann. Neurol., 27, 200-204.
3. Kremer, H.P., Roos, R.A., Dingjan, G., Marani, E. and Bots, G.T. (1990) Atrophy of the hypothalamic lateral tuberal nucleus in Huntington's disease. J. Neuropathol. Exp. Neurol., 49, 371-382.
4. Mohr, E., Brouwers, P., Claus, J.J., Mann, U.M., Fedio, P. and Chase, T.N. (1991) Visuospatial cognition in Huntington's disease. Mov. Disord., 6, 127-132.
5. Foroud, T., Siemers, E., Kleindorfer, D., Bill, D.J., Hodes, M.E., Norton, J.A., Conneally, P.M. and Christian, J.C. (1995) Cognitive scores in carriers of Huntington's disease gene compared to noncarriers. Ann. Neurol., 37, 657-664.
6. Lange, K.W., Sahakian, B.J., Quinn, N.P., Marsden, C.D. and Robbins, T.W. (1995) Comparison of executive and visuospatial memory function in Huntington's disease and dementia of Alzheimer type matched for degree of dementia. J. Neurol. Neurosurg. Psychiatry, 58, 598-606.
7. Lawrence, A.D., Sahakian, B.J., Hodges, J.R., Rosser, A.E., Lange, K.W. and Robbins, T.W. (1996) Executive and mnemonic functions in early Huntington's disease. Brain, 119, 1633-1645.
8. Davies, S.W., Turmaine, M., Cozens, B.A., DiFiglia, M., Sharp, A.H., Ross, C.A., Scherzinger, E., Wanker, E.E., Mangiarini, L. and Bates, G.P. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell, 90, 537-548.
9. Schilling, G., Becher, M.W., Sharp, A.H., Jinnah, H.A., Duan, K., Kotzuk, J.A., Slunt, H.H., Ratovitski, T., Cooper, J.K., Jenkins, N.A. et al. (1999) Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum. Mol. Genet., 8, 397-407.
10. Carter, R.J., Lione, L.A., Humby, T., Mangiarini, L., Mahal, A., Bates, G.P., Dunnett, S.B. and Morton, A.J. (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J. Neurosci., 19, 3248-3257.
11. Lione, L.A., Carter, R.J., Hunt, M.J., Bates, G.P., Morton, A.J. and Dunnett, S.B. (1999) Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J. Neurosci., 19, 10428-10437.
12. Murphy, K.P., Carter, R.J., Lione, L.A., Mangiarini, L., Mahal, A., Bates, G.P., Dunnett, S.B. and Morton, A.J. (2000) Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human Huntington's disease mutation. J. Neurosci., 20, 5115-5123.
13. Luthi-Carter, R., Strand, A., Peters, N.L., Solano, S.M., Hollingsworth, Z.R., Menon, A.S., Frey, A.S., Spektor, B.S., Penney, E.B., Schilling, G. et al. (2000) Decreased expression of striatal signaling genes in a mouse model of Huntington's disease. Hum. Mol. Genet., 9, 1259-1271.
14. Li, H., Li, S.H., Cheng, A.L., Mangiarini, L., Bates, G.P. and Li, X.J. (1999) Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice. Hum. Mol. Genet., 8, 1227-1236.
15. Lievens, J.C., Woodman, B., Mahal, A., Spasic-Boscovic, O., Samuel, D., Kerkerian-Le Goff, L. and Bates, G.P. (2001) Impaired glutamate uptake in the R6 Huntington's disease transgenic mice. Neurobiol. Dis., 8, 807-821.
16. Li, H., Li, S.H., Johnston, H., Shelbourne, P.F. and Li, X.J. (2000) Amino-terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat. Genet., 25, 385-389.
17. Cepeda, C., Hurst, R.S., Calvert, C.R., Hernandez-Echeagaray, E., Nguyen, O.K., Jocoy, E., Christian, L.J., Ariano, M.A. and Levine, M.S. (2003) Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J. Neurosci., 23, 961-969.
18. Klapstein, G.J., Fisher, R.S., Zanjani, H., Cepeda, C., Jokel, E.S., Chesselet, M.F. and Levine, M.S. (2001) Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J. Neurophysiol., 86, 2667-2677.
19. Laforet, G.A., Sapp, E., Chase, K., McIntyre, C., Boyce, F.M., Campbell, M., Cadigan, B.A., Warzecki, L., Tagle, D.A., Reddy, P.H. et al. (2001) Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease. J. Neurosci., 21, 9112-9123.
20. Nicniocaill, B., Haraldsson, B., Hansson, O., O'Connor, W.T. and Brundin, P. (2001) Altered striatal amino acid neurotransmitter release monitored using microdialysis in R6/1 Huntington transgenic mice. Eur. J. Neurosci., 13, 206-210.
21. Reynolds, G.P., Dalton, C.F., Tillery, C.L., Mangiarini, L., Davies, S.W. and Bates, G.P. (1999) Brain neurotransmitter deficits in mice transgenic for the Huntington's disease mutation. J. Neurochem., 72, 1773-1776.
22. Behrens, P.F., Franz, P., Woodman, B., Lindenberg, K.S. and Landwehrmeyer, G.B. (2002) Impaired glutamate transport and glutamate-glutamine cycling: downstream effects of the Huntington mutation. Brain, 125, 1908-1922.
23. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonsattel, J.P., Carraway, R., Reeves, S.A. et al. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron, 14, 1075-1081.
24. 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. et al. (1995) Widespread expression of Huntington's disease gene (IT15) protein product. Neuron, 14, 1065-1074.
25. Li, X.J., Sharp, A.H., Li, S.H., Dawson, T.M., Snyder, S.H. and Ross, C.A. (1996) Huntingtin-associated protein (HAP1): discrete neuronal localizations in the brain resemble those of neuronal nitric oxide synthase. Proc. Natl Acad. Sci. USA, 93, 4839-4844.
26. Gutekunst, C.A., Li, S.H., Yi, H., Ferrante, R.J., Li, X.J. and Hersch, S.M. (1998) The cellular and subcellular localization of huntingtin-associated protein 1 (HAP1): comparison with huntingtin in rat and human. J. Neurosci., 18, 7674-7686.
27. Martin, E.J., Kim, M., Velier, J., Sapp, E., Lee, H.S., Laforet, G., Won, L., Chase, K., Bhide, P.G., Heller, A., Aronin, N. and Difiglia, M. (1999) Analysis of Huntingtin-associated protein 1 in mouse brain and immortalized striatal neurons. J. Comp. Neurol., 403, 421-430.
28. Lin, C.H., Tallaksen-Greene, S., Chien, W.M., Cearley, J.A., Jackson, W.S., Crouse, A.B., Ren, S., Li, X., Albin, R.L. and Detloff, P.J. (2001) Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum. Mol. Genet., 10, 137-144.
29. Phillips, G.R., Huang, J.K., Wang, Y., Tanaka, H., Shapiro, L., Zhang, W., Shan, W.S., Arndt, K., Frank, M., Gordon, R.E. et al. (2001) The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron, 32, 63-77.
30. Li, S.H., Cheng, A.L., Li, H. and Li, X.J., (1999) Cellular defects and altered gene expression in PC12 cells stably expressing mutant huntingtin. J. Neurosci., 19, 5159-5172.
31. Thiel, G., Sudhof, T.C. and Greengard, P. (1990) Synapsin II. Mapping of a domain in the NH2-terminal region which binds to small synaptic vesicles. J. Biol. Chem., 265, 16527-16533.
32. Chou, J.H. and Jahn, R. (2000) Binding of Rab3A to synaptic vesicles. J. Biol. Chem., 275, 9433-9440.
33. Jennings, P. and Collard, K.J. (1995) Postnatal development of the calcium-dependency of glutamate release from rat cortical synaptosomes: comparison with 5-hydroxytryptamine release. Brain Res. Dev. Brain Res., 89, 120-123.
34. Maneuf, Y.P. and McKnight, A.T. (2001) Calcitonin gene-related peptide-mediated increase in K(+)-induced [(3)H]-dopamine release from rat caudal striatal slices. Neurosci. Lett., 310, 73-76.
35. Patel, D.R., Young, A.M. and Croucher, M.J. (2001) Presynaptic alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor-mediated stimulation of glutamate and GABA release in the rat striatum in vivo: a dual-label microdialysis study. Neuroscience, 102, 101-111.
36. Zhang, W., Yamada, M., Gomeza, J., Basile, A.S. and Wess, J. (2002) Multiple muscarinic acetylcholine receptor subtypes modulate striatal dopamine release, as studied with M1-M5 muscarinic receptor knock-out mice. J. Neurosci., 22, 6347-6352.
37. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P. and Aronin, N. (1997). Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 277, 1990-1993.
38. Morton, A.J. and Edwardson, J.M. (2001) Progressive depletion of complexin II in a transgenic mouse model of Huntington's disease. J. Neurochem., 76, 166-172.
39. Usdin, M.T., Shelbourne, P.F., Myers, R.M. and Madison, D.V. (1999) Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum. Mol. Genet., 8, 839-846.
40. Jenkins, B.G., Klivenyi, P., Kustermann, E., Andreassen, O.A., Ferrante, R.J., Rosen, B.R. and Beal, M.F. (2000) Nonlinear decrease over time in N-acetyl aspartate levels in the absence of neuronal loss and increases in glutamine and glucose in transgenic Huntington's disease mice. J. Neurochem., 74, 2108-2119.
41. Hansson, O., Petersen, A., Leist, M., Nicotera, P., Castilho, R. F. and Brundin, P. (1999) Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. Proc. Natl Acad. Sci. USA, 96, 8727-8732.
42. Li, H., Li, S.H., Yu, Z.X., Shelbourne, P. and Li, X.J. (2001) Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J. Neurosci., 21, 8473-8481.
43. Parker, J.A., Connolly, J.B., Wellington, C., Hayden, M., Dausset, J. and Neri, C. (2001) Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. PG - 13318-23. Proc. Natl Acad. Sci. USA, 98, 13318-13323.
44. Raff, M.C., Whitmore, A. V. and Finn, J.T (2002) Axonal self-destruction and neurodegeneration. Science, 296, 868-871.
45. Metzler, M., Legendre-Guillemin, V., Gan, L., Chopra, V., Kwok, A., McPherson, P.S. and Hayden, M.R. (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J. Biol. Chem., 276, 39271-39276.
46. Rao, D.S., Chang, J.C., Kumar, P.D., Mizukami, I., Smithson, G.M., Bradley, S.V., Parlow, A.F. and Ross, T.S. (2001) Huntingtin interacting protein 1 Is a clathrin coat binding protein required for differentiation of late spermatogenic progenitors. Mol. Cell. Biol., 21, 7796-7806.
47. Waelter, S., Scherzinger, E., Hasenbank, R., Nordhoff, E., Lurz, R., Goehler, H., Gauss, C., Sathasivam, K., Bates, G.P., Lehrach, H. and Wanker, E.E. (2001) The huntingtin interacting protein HIP1 is a clathrin and alpha-adaptin-binding protein involved in receptor-mediated endocytosis. Hum. Mol. Genet., 10, 1807-1817.
48. Chan, E.Y., Nasir, J., Gutekunst, C.A., Coleman, S., Maclean, A., Maas, A., Metzler, M., Gertsenstein, M., Ross, C.A., Nagy, A. and Hayden, M.R. (2002) Targeted disruption of Huntingtin-associated protein-1 (Hap1) results in postnatal death due to depressed feeding behavior. Hum. Mol. Genet., 11, 945-959.
49. Li, S.-H., Yu, Z.-X., Li, C.-L., Nguyen, H.-P., Zhou, Y.-X., Deng, C.X. and Li, X.-J. (2003) Lack of huntingtin-associated protein-1 causes neuronal death resembling hypothalamic degeneration in Huntington disease. J. Neurosci. (in press).
50. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W. and Bates, G.P. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell, 87, 493-506.
51. Li, S.H., Cheng, A.L., Zhou, H., Lam, S., Rao, M., Li, H. and Li, X.J. (2002) Interaction of Huntington disease protein with transcriptional activator Sp1. Mol. Cell. Biol., 22, 1277-1287.
52. Li, H., Ohishi, H., Kinoshita, A., Shigemoto, R., Nomura, S. and Mizuno, N. (1997) Localization of a metabotropic glutamate receptor, mGluR7, in axon terminals of presumed nociceptive, primary afferent fibers in the superficial layers of the spinal dorsal horn: an electron microscope study in the rat. Neurosci. Lett., 223, 153-156.
53. Huttner, W.B., Schiebler, W., Greengard, P. and De Camilli, P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell. Biol., 96, 1374-1388.
54. Cao, F., Levine, J.J., Li, S.H. and Li, X.J. (2001) Nuclear aggregation of huntingtin is not prevented by deletion of chaperone Hsp104. Biochim. Biophys. Acta., 1537, 158-166.