Neuronal degeneration in the basal ganglia and loss of pallido- subthalamic synapses in mice with targeted disruption of the Huntington's disease gene

Brain Research

Volumn 818, Issue 2, 1999, Pages 468-479

  O'Kusky, John R ^a   Nasir, Jamal ^a   Cicchetti, Francesca ^b   Parent, Andre ^b   Hayden, Michael R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

Author keywords

Apoptosis; Huntingtin protein; Huntington's disease; Subthalamic nucleus

Indexed keywords

ENKEPHALIN; HUNTINGTIN; SUBSTANCE P;

ADOLESCENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASAL GANGLION; CELL LOSS; CELL ULTRASTRUCTURE; CONTROLLED STUDY; GENE DISRUPTION; GLOBUS PALLIDUS; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; STEREOLOGY; SUBTHALAMIC NUCLEUS;

AFFERENT PATHWAYS; ANIMALS; BASAL GANGLIA; ENKEPHALINS; GENE TARGETING; GLOBUS PALLIDUS; HETEROZYGOTE; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEUROGLIA; NEURONS; SUBSTANCE P; SYNAPSES; THALAMIC NUCLEI;

EID: 0033550705     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(98)01312-2     Document Type: Article

References (40)

1. Andrew S.E., Goldberg Y.P., Kremer B., Telenius H., Theilmann J., Adam S., Starr E., Squitieri F., Lin B., Kalchman M., Graham R.K., Hayden M.R. The relationship between trinucleotide repeat length and clinical features of Huntington's disease. Nat. Genet. 4:1993;398-403.
2. Carpenter M.B., Whittier J.R., Mettler F.A. Analysis of choreoid hyperkinesia in the rhesus monkey: surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus of Luys. J. Comp. Neurol. 92:1950;293-331.
3. Cicchetti F., Parent A. Striatal interneurons in Huntington's disease: selective increase in the density of calretinin-immunoreactive medium-sized neurons. Mov. Disord. 11:1996;619-626.
4. J.K. Cooper, G. Schilling, M.F. Peters, W.J. Herring, A.H. Sharp, Z. Kaminsky, J. Masone, F.A. Khan, M. Delanoy, D.R. Borchelt, V.L. Dawson, T.M. Dawson, C.A. Ross, Truncated N-terminal fragments of huntingtin with expanded glutamine repeats form nuclear and cytoplasmic aggregates in cell culture, Hum. Mol. Genet., (1998) 783-790.
5. Cunningham T.J. Naturally occurring neuron death and its regulation by developing neural pathways. Int. Rev. Cytol. 74:1982;163-186.
6. Duyao M., Ambrose C., Myers R., Noveletto A., Persichetti F., Frontali M., Dolstein S., Ross C., Franz M., Abbot M.et al. Trinucleotide repeat length instability and age of onset of Huntington's disease. Nat. Genet. 4:1993;387-392.
7. 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. Inactivation of the mouse Huntington's disease gene homolog Hdh. Science. 269:1995;407-410.
8. Hackam A.S., Singaraja R., Wellington C.L., Metzler M., McCutcheon K., Zhang T., Kalchman M., Hayden M.R. The influence of huntingtin protein size on nuclear localization and cellular toxicity. J. Cell Biol. 141:1998;1097-1105.
9. P.S. Harper, Huntington's Disease, Saunders, London, 1991.
10. M.R. Hayden, Huntington's Chorea, Springer-Verlag, London, 1981.
11. Hsu S.M., Raine L., Fanger A. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedure. J. Histochem. 29:1981;577-580.
12. Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 72:1993;971-983.
13. Kerr J.F.R., Gobe G.C., Winterford C.M., Harmon B.V. Anatomical methods in cell death. Methods Cell Biol. 46:1995;1-27.
14. Lange H., Thorner G., Hopf A.V., Schroder K.F. Morphometric studies of the neuropathological process in choreatic diseases. J. Neurol. Sci. 28:1976;401-425.
15. Li S.H., Li X.J. Aggregation of N-terminal huntingtin is dependent on the length of its glutamine repeats. Hum. Mol. Genet. 7:1998;777-782.
16. Li S.H., Schilling G., Young W.S., Li X.-J., Margolis R.L., Stine O.C., Wagster M.V., Abbott M.H., Franz M.L., Ranen N.G.et al. Huntington's disease gene (IT15) is widely expressed in human and rat tissues. Neuron. 11:1993;985-993.
17. Lin B., Nasir J., MacDonald H., Hutchinson G.B., Graham R.K., Rommens J.M., Hayden M.R. Sequence of the murine Huntington disease gene: evidence for conservation, alternate splicing and polymorphism in a triplet (CCG) repeat. Hum. Mol. Genet. 3:1994;85-92.
18. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 87:1996;456-493.
19. Martindale D., Hackam A., Wieczorek A., Ellerby L., Wellington C., McCutcheon K., Singaraja R.R., Kazemi-Esfarjani P., Devon R., Kim S.U., Bredesen D., Tufaro F., Hayden M.R. Length of huntingtin and its polyglutamine tract influences location and frequency of intracellular aggregates. Nat. Genet. 18:1998;150-154.
20. Milstein C., Cuello A.C. Hybrid hybridomas and their use in immunohistochemistry. Nature. 305(5934):1983;537-540.
21. Moriizumi T., Nakamura Y., Kitao Y., Kudo M. Ultrastructural analysis of afferent terminals in the subthalamic nucleus of the cat with a combined degeneration and horseradish peroxidase tracing method. J. Comp. Neurol. 265:1987;159-174.
22. Nasir J., Lin B.-Y., Bucan M., Nadeau J., Hayden M.R. The murine homolog of the Huntington disease gene (Hdh) maps to mouse chromosome 5 within a region of conserved synteny with human chromosome 4p16.3. Genomics. 22:1994;198-201.
23. 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. Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell. 81:1995;811-823.
24. O'Kusky J.R., Norman M.G. Sudden infant death syndrome: increased synaptic density in the central reticular nucleus of the medulla. J. Neuropathol. Exp. Neurol. 53:1994;263-271.
25. O'Kusky J.R., Norman M.G. Sudden infant death syndrome: increased number of synapses in the hypoglossal nucleus. J. Neuropathol. Exp. Neurol. 54:1995;627-634.
26. O'Kusky J.R., Akers M.A., Vinters H.V. Synaptogenesis in hemimegalencephaly: the numerical density of asymmetric and symmetric synapses in the cerebral cortex. Acta Neuropathol. 92:1996;156-163.
27. Oorshcot D.E. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical dissector methods. J. Comp. Neurol. 366:1996;580-599.
28. Oppenheim R.W. Cell death during development of the nervous system. Ann. Rev. Neurosci. 14:1991;453-501.
29. Parent A., Hazrati L. Functional anatomy of the basal ganglia: II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Rev. 20:1995;128-154.
30. Portera-Cailliau C., Hedreen J.C., Price D.L., Koliatsos V.E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15:1995;3775-3787.
31. Ribeiro-da-Silva A., Pioro E.P., Cuello A.C. Substance P- and enkephalin-like immunoreactivities are colocalized in certain neurons of the substance gelatinosa of the rat spinal cord: an ultrastructural double-labeling study. J. Neurosci. 11:1991;1068-1080.
32. Romansky K.V., Usunoff K.G., Ivanov D.P., Galabov G.P. Corticosubthalamic projection in the cat: an electron microscopic study. Brain Res. 163:1979;319-322.
33. 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. Widespread expression of Huntington's disease gene (IT15) protein product. Neuron. 14:1995;1065-1074.
34. Strong T.V., Tagel D.A., Vades J.M., Elmer L.W., Boehm K., Swaroop M., Kaatz K.W., Collings F.S., Albin R.L. Widespread expression of the human and rat Huntington's disease gene in brain and nonneural tissues. Nat. Genet. 5:1993;259-265.
35. Thomas L.B., Gates D.J., Richfield E.K., O'Brien T.F., Schweltzer J.B., Steindler D.A. DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp. Neurol. 133:1995;265-272.
36. Trottier Y., Devys D., Imbert G., Saudou F., An I., Lutz Y., Weber C., Agid Y., Hirsch E.C., Mandel J.-L. Cellular localisation of the Huntington's disease protein and discrimination of the normal and mutated form. Nat. Genet. 10:1995;104-110.
37. Vonsattel J.-P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44:1985;559-577.
38. Wellington C.L., Brinkman R.R., O'Kusky J.R., Hayden M.R. Toward understanding the molecular pathology of Huntington's disease. Brain Pathol. 7:1997;979-1002.
39. Whittier J.R. Ballism and the subthalamic nucleus (nucleus hypothalamus corpus Luysi). Arch. Neurol. Psychol. 58:1947;672-692.
40. Zeitlin S., Liu J.-P., Chapman D.L., Papaioannou V.E., Efstratiadis A. Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet. 11:1995;155-163.