Enhanced sensitivity to N-methyl-D-aspartate receptor activation in transgenic and knockin mouse models of Huntington's disease

Journal of Neuroscience Research

Volumn 58, Issue 4, 1999, Pages 515-532

  Levine, Michael S ^a   Klapstein, Gloria J ^a   Koppel, Ahrin ^a   Gruen, Ehud ^a   Cepeda, Carlos ^a   Vargas, Mauricio E ^a   Jokel, Eve S ^a   Carpenter, Ellen M ^a   Zanjani, Hadi ^b   Hurst, Raymond S ^a   Efstratiadis, Argiris ^c   Zeitlin, Scott ^c   Chesselet, Marie Françoise ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Department of Neurology Univ of California at Los Angeles ^*  (United States)

Author keywords

Electrophysiology; Excitotoxicity; Huntington's disease; Knockin mice; NMDA; Nuclear inclusions; Striatum; Transgenic mice

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMATE RECEPTOR; GLUTAMIC ACID; KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL SWELLING; CORPUS STRIATUM; ELECTROPHYSIOLOGY; HISTOPATHOLOGY; HUNTINGTON CHOREA; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; TRANSGENIC MOUSE;

EID: 0033571743     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19991115)58:4<515::AID-JNR5>3.0.CO;2-F     Document Type: Article

References (74)

1. Beal MF, Kowall NW, Ellison DW, Mazurek MF, Swartz KJ, Martin JB. 1986. Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature 321:168-171.
2. Beal MF, Ferrante RJ, Swartz KJ, Kowall NW. 1991. Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J Neurosci 11:1649-1659.
3. Beal MF, Bradley TH, Koroshetz W. 1993. Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases? Trends Neurosci 16:125-131.
4. Bogdanov MB, Ferrante RJ, Kuemmerle S, Klivenyi P, Beal MF. 1998. Increased vulnerability to 3-nitoproprionic acid in an animal model of Huntington's disease. J Neurochem 71:2642-2644.
5. Bordelon YM, Chesselet M-F. 1999. Early effects of intrastriatal injections of quinolinic acid on microtubule-associated protein-2 and neuropeptides in rat basal ganglia. Neuroscience 93:843-853.
6. Bradley A. 1987. Production and analysis of chimeric mice. In: Robertson EJ, editor. Teratocarcinomas and embryonic stem cells: a practical approach. Oxford: IRL Press. p. 131-151.
7. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton, AJ. 1999. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19:3248-3257.
8. Cepeda C, Colwell CS, Itri JN, Chandler SH, Levine MS. 1998a. Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons: contribution of calcium conductances. J Neurophysiol 79:82-94.
9. Cepeda C, Colwell CS, Itri JN, Gruen E, Levine MS. 1998b. Dopaminergic modulation of early signs of excitotoxicity in visualized rat neostriatal neurons. Eur J Neurosci 10:3491-3497.
10. Cepeda, C, Itri JN, Levine MS. 1998c. Differential sensitivity of medium and large striatal neurons to NMDA receptor activation. Neurosci Abst 24:1644.
11. Cha J H J, Kosinski CM, Kerner JA, Alsdorf SA, Mangiarini L, Davies SW, Penney JB, Bates GP, Young AB. 1998. Altered brain neurotransmitter receptors in trans-genic mice expressing a portion of an abnormal human Huntington disease gene. Proc Nail Acad Sci USA 95:6480-6485.
12. Chen N, Luo T, Wellington C, Metzler M, McCutcheon K, Hayden MR, Raymond LA. 1999. Subtype-specific enhancement of NMDA receptor currents by mutant huntingtin. J Neurochem 72:1890-1898.
13. Cherubini E, Herrling PL, Lanfumey L, Stanzione P. 1988. Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. J Physiol Lond 400:677-690.
14. Choi DW. 1985. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci Lett 58:293-297.
15. Choi DW. 1987. Ionic dependence of glutamate neurotoxicity. J Neurosci 7:369-379.
16. Choi DW. 1988. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
17. Colwell CS, Levine MS. 1996. Glutamate receptor-induced toxicity in neostriatal cells. Brain Res 724:205-212.
18. Colwell CS, Altemus KL, Cepeda C, Levine MS. 1996. Regulation of NMDA-induced toxicity in the neostriatum: a role for metabotropic glutamate receptors. Proc Natl Acad Sci USA 93:1200-1204.
19. Colwell CS, Cepeda C, Crawford CA, Levine MS. 1998. Postnatal development of glutamate receptor-mediated responses in the neostriatum. Dev Neurosci 20:154-163.
20. Coyle JT. 1979. An animal model for Huntington's disease. Biol Psychiatry 14:251-276.
21. Davies SW, Turmaine M, Cozens BA, DiFiglia M. Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L, Bates GP. 1997. Formation of neuronal intranuclear inclusions (NII) underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90:537-548.
22. DiFiglia M. 1990. Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci 13:863-873.
23. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel J-P, Aronin N. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:1990-1993.
24. DiFiglia M., Sapp E, Chase K, Schwarz C, Meloni A, Young C, Martin E, Vonsattel J-P, Carraway R, Reeves SA, Boyce FM, Aronin N. 1995. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14:1075-1081.
25. Dodt HU. Zieglgänsberger W. 1990. Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res 537:333-336.
26. Dodt HU, Zieglgänsberger W. 1994. Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci 11:453-458.
27. Dodt HU, Hager G, Zieglgänsberger W. 1993. Direct observation of neurotoxicity in brain slices with infrared videomicroscopy. J Neurosci Meth 50:165-171.
28. Duyao MP, Auerbach AB, Ryan A, Persichetti F, Barnes GT, McNeil SM, Ge P, Vonsattel J-P, Gusella JF, Joyner AL, MacDonald ME. 1995. Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269:407-410.
29. Ferrante RJ, Gutenkust CA, Persichetti F, McNeil SM, Kowall NW, Gusella JF, MacDonald ME, Beal MF, Hersch SM. 1997. Heterogeneous topographic and cellular distribution of Huntingtin expression in the normal human neostriatum. J Neurosci 17:3052-3063.
30. Freese A, DiFiglia M, Koroshetz WJ, Beal MF, Martin JB, 1990. Characterisation and mechanism of glutamate neurotoxicity in primary striatal cultures. Brain Res 521:254-264.
31. Fonnum F, Storm-Mathisen J, Divac I. 1981. Biochemical evidence for glutamate as a neurotransmitter in cortico-striatal and corticothalamic fibers in the rat brain. Neuroscience 6:863-873.
32. Fusco FR, Chen Q, Lamoreaux WJ, Figueredo-Cardenas G, Jiao Y, Coffman JA, Surmeier DJ, Honig MG, Carlock LR, Reiner A. 1999. Cellular localisation of huntingtin in striatal and cortical neurons in rats: lack of correlation with neuronal vulnerability in Huntington's disease. J Neurosci 19:1189-1202.
33. Gagne J, Milot M, Gelinas S, Lahsaini A, Trudeau F, Martinoli M-G, Massicotte G. 1997. Binding properties of glutamate receptors in streptozotocin-induced diabetes in rats. Diabetes 46:841-846.
34. Goldberg YP, Kalchman MA, Metzler M, Nasir J, Zeisler J, Graham R, Koide K, O'Kusky JR, Sharp AH, Ross CA, Jirik F, Hayden MR. 1996. Absence of disease phenolype and intergenerational stability of the CAG repeat in transgenic mice expressing the human Huntington disease transcript. Hum Mol Genet 5:77-185.
35. Gourfinkel-An I, Cancel G, Trottier Y, Devys D, Tora L, Lutz Y, Imbert G, Saudou F, Stevanin G, Agid Y, Brice A, Mandel JL, Hirsch EC. 1997. Differential distribution of the normal and mutated forms of huntingtin in the human brain. Ann Neurol 42:712-719.
36. Gutekunst CA, Levey AI, Heilman CJ, Whaley WL, Yi H, Nash NR, Rees HD, Madden JJ, Hersh SM. 1995. Identification and localization on huntingtin in brain and human lymphoblastoid cell lines with anti-f usion protein antibodies. Proc Natl Acad Sei USA 92:8710-8714.
37. Gutekunst C-A, Li S-H, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li X-J. 1999. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 19:2522-2534.
38. Harper P. 1996. Huntington's disease. London: W.B. Saunders.
39. Hille B. 1992. Ionic channels of excitable membranes. Sunderland MA: Sinauer Associates, p. 607
40. 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.
41. Hurlbert MS, Zhou W, Wasmeier C, Kaddis FG, Hutton JC, Freed CR. 1999. Mice transgenic for an expanded CAG repeat in Huntington's disease gene develop diabetes. Diabetes 48:649-651.
42. Iino M, Ozawa S, Tzuzuki K. 1990. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol 424:151-165.
43. Jack JJB, Noble D, Tsein RW. 1975. Electric current flow in excitable cells. Oxford: Clarendon.
44. Jiang ZG, North RA. 1991. Membrane properties and synaptic responses of rat striatal neurones in vitro. J. Physiol. Lond. 443:533-553.
45. Jones E. 1987. The thalamus. New York, NY: Plenum.
46. Kim M, Lee H-S, LaForet G, McIntyre C, Martin EJ, Chang P, Kim TW, Williams M, Reddy PH, Tagle D, Boyce FM, Won L, Heller A, Aronin N, DiFiglia M. 1999. Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition. J Neurosci 19:964-973.
47. Koroshetz WJ, Freese A, DiFiglia M. 1990. The correlation between excitatory amino acid-induced current responses and excitotoxicity in striatal cultures Brain Res 521:265-272.
48. Kosinski CM, Cha JH, Young AB, Persichetti F, MacDonald M, Gusella JF, Penney JB Jr, Standaert DG. 1997. Huntingtin immunoreactivity in the rat neostriatum: differential accumulation in projection and interneurons. Exp Neurol 144:239-247.
49. Landwehrmeyer GB, McNeil SM, Dure IV LS, Ge P, Aizawa H, Huang Q, Ambrose CM, Duyao MP, Bird ED, Bonilla E, de Young M, Avila-Gonzales AJ, Wexler NS, DiFiglia M, Gusella JF, MacDonald ME, Penney JB, Young AB, Vonsattel JP. 1995. Huntington's disease gene: regional and cellular expression in brain of normal and affected individuals. Ann Neurol 37:218-230.
50. Levine MS, Li Z, Cepeda C, Cromwell HC, Altemus KL. 1996. Neuromodulatory actions of dopamine on synaptically-evoked neostriatal responses in slices. Synapse 24:65-78.
51. Levine MS, Chesselet M-F. Koppel A, Gruen E, Cepeda C, Carpenter EM, Zanjani H, Hurst RS, Altemus KL, Murai JS, Efstratiadis A, Zeitlin S. 1998. Enhanced sensitivity to glutamate receptor activation in mouse models of Huntington's Disease. Neurosci Abst 24:972.
52. Mangiurini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. 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.
53. Mansour SL, Thomas KR, Cappecchi MR. 1988. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336:348-352.
54. McGeer PL, McGeer EG, Shorer V, Singh K. 1977. A glutamatergic corticostriatal path? Brain Res 128:369-373.
55. Menalled LB, Mackenzie L, Zanjani H, Zeitlin S, Chesselet M-F. 1999. Selective impairment of enkephalinergic striatal neurons in two mouse models of Huntington's disease. Neurosci Abst 25:588.
56. Meshul CK, Stallbaumer RK, Taylor B, Janowsky A. 1994. Haloperidol-induced morphological changes in striatum are associated with glutamate synapses. Brain Res 648:181-195.
57. Nasir J, Floresco SB, O'Kusky JR, Diewert VM, Richman JM, Zeisler J, Borowski A, Marth JD, Phillips AG, Hayden MR. 1995. Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81:811-823.
58. Persichetti F, Ambrose CM, Ge P, McNeil SM, Srinidhi J, Anderson MA, Jenkins B, Barnes GT, Duyao MP, Kanaley N, Wexler NS, Myers RH, Bird ED, Vonsattel J-P, MacDonald ME, Gusella JF. 1995. Normal and expanded Huntington's disease gene alleles produce distinguishable proteins due to translation across the CAG repeat. Mol Med 1:374-383.
59. Phillips HJ. 1973. Dye exclusion tests for cell viability. In: Kruse PK, Patterson MK, editors. Tissue culture: methods and applications. New York: Academic Press, p. 406-408.
60. Price MT, Olney JW, Samson L, Labruyere J. 1985. Calcium influx accompanies but does not cause excitotoxin-induced neuronal necrosis in retina. Brain Res Bull 14:369-376.
61. Reddy PH, Williams M, Charles V, Garrett L, Pike-Buchanan L, Whetsell WO Jr, Miller G, Tagle DA. 1998, Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nature Genet 20:98-202.
62. Richfield EK, Maguire-Zeiss KA, Vonkeman HE, Voorn P. 1995. Preferential loss of preproenkephalin versus preprotachykinin neurons from the striatum of Huntington's disease patients. Ann Neurol 38:852-861.
63. Rothman SM. 1985. The neurotoxicity of excitatory amino acids is produced by passive chloride influx. J Neurosci 5:1483-1489.
64. Rothman SM. 1992. Excitotoxins: possible mechanisms of action. Ann NY Acad Sci 648:132-139.
65. Sapp E, Penney J, Young A, Aronin N, Vonsattel J-P, DiFiglia M. 1999. Axonal transport of N-terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease. J Neuropathol Exp Neurol 58:165-173.
66. Saudou F, Finkbeiner S, Devys D, Greenberg ME. 1998. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
67. Schilling G, Becher MW, Sharp AH, Jinnah HA, Duan K, Kotzuk JA, Slunt HH, Ratovitski T, Cooper JK, Jenkins NA, Copeland NG, Price DL, Ross CA, Borchelt DR. 1999. Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet 8:397-407.
68. Schneggenburger R, Zhou Z, Konnerth A, Neher E. 1993. Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron 11:133-143.
69. Schwarcz R, Foster AC, French ED, Whetsel WO Jr, Köhler C. 1984. Excitotoxic models for neurodegenerative disorders. Life Sci 35:19-32.
70. Trottier Y, Devys D, Imbert G, Saudou F, An I, Lutz Y, Weber C, Agid Y, Hirsch EC, Mandel JL. 1995. Cellular localization of the Hunting-ton's disease protein and discrimination of the normal and mutated form. Nature Genet 10:104-110.
71. Vonsattel JPG, DiFiglia M. 1998. Huntington's disease. J Neuropath Exp Neurol 57:369-384.
72. White JK, Auerbach W, Duyao M P, Vonsattel JP, Gusella JF, Joyner AL, MacDonald ME. 1997. Huntingtin is required for neurogenesis and is not impaired by the Huntington's disease CAG expansion. Nature Genet 17:404-410.
73. Zeitlin S, Liu JP, Chapman DL, Papaioannou VE, Efstratiadis A. 1995. Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nature Genet 11:155-163.
74. Zukin RS, Bennett MVL. 1995. Alternatively spliced isoforms of the NMDAR1 receptor subunit. Trends Neurosci 18:306-313.