Increased calbindin-D28k immunoreactivity in striatal projection neurons of R6/2 Huntington's disease transgenic mice

Neurobiology of Disease

Volumn 20, Issue 3, 2005, Pages 907-917

  Sun, Z ^a   Wang, H B ^a   Deng, Y P ^a   Lei, W L ^a   Xie, J P ^a   Meade, C A ^a   Del Mar, N ^a   Goldowitz, D ^a   Reiner, A ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Calbindin D28k; Huntington's disease; Immunoreactivity

Indexed keywords

CALBINDIN; CALCIUM; EXCITOTOXIN; HUNTINGTIN; N METHYL DEXTRO ASPARTIC ACID; QUINOLINIC ACID; AMINO ACID RECEPTOR STIMULATING AGENT; GLUTAMIC ACID; HD PROTEIN, HUMAN; MESSENGER RNA; NERVE PROTEIN; NEUROTOXIN; NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN REGION; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; CORPUS STRIATUM; EXCITOTOXICITY; EXON; HUNTINGTON CHOREA; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; CALCIUM SIGNALING; DISEASE MODEL; FEMALE; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MUTATION; NEOSTRIATUM; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRINUCLEOTIDE REPEAT; UPREGULATION;

ANIMALS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLUTAMIC ACID; HUMANS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; MUTATION; NEOSTRIATUM; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONS; NEUROTOXINS; NUCLEAR PROTEINS; RNA, MESSENGER; TRINUCLEOTIDE REPEAT EXPANSION; UP-REGULATION;

EID: 27744487206     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.05.023     Document Type: Article

References (86)

1. R.L. Albin, Y. Qin, A.B. Young, J.B. Penney, and M.F. Chesselet Preproenkephalin messenger RNA-containing neurons in striatum of patients with symptomatic and presymptomatic Huntington's disease: an in situ hybridization study Ann. Neurol. 30 1991 542 549
2. M. Arrasate, S. Mitra, E.S. Schweitzer, M.R. Segal, and S. Finkbeiner Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431 2004 805 810
3. T.J. Bazzett, J.B. Becker, R.C. Falic, and R.L. Albin Chronic intrastriatal quinolinic acid produces reversible changes in perikaryal calbindin and parvalbumin immunoreactivity Neuroscience 60 1994 837 841
4. M.F. Beal, E. Brouillet, B.G. Jenkins, R.J. Ferrante, N.W. Kowall, J.M. Miller, E. Storey, R. Srivastava, B.R. Rosen, and B.T. Hyman Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid J. Neurosci. 13 1993 4181 4192
5. P.F. Behrens, P. Franz, B. Woodman, K.S. Lindenberg, and G.B. Landwehrmeyer Impaired glutamate transport and glutamate-glutamine cycling: downstream effects of the Huntington mutation Brain 25 2002 1908 1922
6. J.A. Bibb, Z. Yan, P. Svenningsson, G.L. Snyder, V.A. Pieribone, A. Horiuchi, A.C. Nairn, A. Messer, and P. Greengard Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice Proc. Natl. Acad. Sci. U. S. A. 97 2000 6809 6812
7. 28k immunostaining, following developmental hypoxic-ischemic injury Neuroscience 56 1993 305 315
8. K. Campbell, and A. Björklund Prefrontal corticostriatal afferents maintain increased enkephalin gene expression in the dopamine-denervated rat striatum J. Neurosci. 6 1994 1371 1383
9. 28K and parvalbumin in the rat nervous system Neuroscience 35 1990 373 475
10. C. Cepeda, M.A. Ariano, C.R. Calvert, J. Flores-Hernandez, S.H. Chandler, B.R. Leavitt, M.R. Hayden, and M.S. Levine NMDA receptor function in mouse models of Huntington disease J. Neurosci. Res. 66 2001 525 539
11. C. Cepeda, R.S. Hurst, C.R. Calvert, E. Hernandez-Echeagaray, O.K. Nguyen, E. Jocoy, L.J. Christian, M.A. Ariano, and M.S. Levine Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease J. Neurosci. 23 2003 961 969
12. J.H. Cha, C.M. Kosinski, J.A. Kerner, S.A. Alsdorf, L. Mangiarini, S.W. Davies, J.B. Penney, G.P. Bates, and A.B. Young Altered brain neurotransmitter receptors in transgenic mice expressing a portion of an abnormal human Huntington's disease gene Proc. Natl. Acad. Sci. U. S. A. 95 1998 6480 6485
13. N. Chen, T. Luo, C. Wellington, M. Metzler, K. McCutcheon, M.R. Hayden, and L.A. Raymond Subtype-specific enhancement of NMDA receptor currents by mutant Huntingtin J. Neurochem. 72 1999 1890 1898
14. M.F. Chesselet, L. Weiss, C. Wuenschell, A.J. Tobin, and H.U. Affolter Comparative distribution of mRNAs for glutamic acid decarboxylase, tyrosine hydroxylase, and tachykinins in the basal ganglia: an in situ hybridization study in the rodent brain J. Comp. Neurol. 262 1987 125 140
15. S.W. Davis, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, C.A. Ross, E. Scherzinger, E.E. Wanker, L. Mangiarini, and G.P. Bates Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
16. Y.P. Deng, J.B. Penney, A.B. Young, B.L. Albin, K.D. Anderson, and A. Reiner Differential loss of striatal projection neurons in Huntington's disease: a quantitative immunohistochemical study J. Chem. Neuroanat. 27 2004 143 164
17. E.M. Denovan-Wright, and H.A. Robertson Cannabinoid receptor messenger RNA levels decrease in a subset of neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington's disease mice Neuroscience 98 2000 705 713
18. 28k in the rat and monkey basal ganglia, including subcellular distribution with colloidal gold labeling J. Comp. Neurol. 279 1989 653 665
19. M. DiFiglia, E. Sapp, K. Chase, C. Schwarz, A. Meloni, C. Young, E. Martin, J.-P. Vonsattel, R. Carraway, S.A. Reeves, F.M. Royee, and N.A. Aronin Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons Neuron 14 1995 1075 1081
20. M. DiFiglia, E. Sapp, K.O. Chase, S.W. Davies, G.P. Bates, J.P. Vonsattel, and N. Aronin Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain Science 277 1997 1990 1993
21. 28k immmunocytochemistry J. Neurosci. 11 1991 3877 3887
22. G. Figueredo-Cardenas, C.L. Harris, K.D. Anderson, and A. Reiner Relative resistance of striatal neurons containing calbindin or parvalbumin to quinolinic acid-mediated excitotoxicity compared to other striatal neuron types Exp. Neurol. 149 1998 356 372
23. F.R. Fusco, Q. Chen, W.J. Lamoreaux, G. Figueredo-Cardenas, Y. Jiao, J. Coffman, D.J. Surmeier, M.G. Honig, L.R. Carlock, and A. Reiner Cellular localization of huntingtin in striatal and cortical neurons in rats: lack of correlation with neuronal vulnerability in Huntington's disease J. Neurosci. 19 1999 1189 1202
24. C.R. Gerfen, and C.J. Wilson The basal ganglia L.W. Swanson A. Bjorklund T. Hokfelt Handbook of Chemical Neuroanatomy Integrated Systems of the CNS, Part III vol. 12 1996 Elsevier Science Amsterdam
25. C.R. Gerfen, K.G. Baimbridge, and J.J. Miller The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey Proc. Nat. Acad. Sci. U. S. A. 82 1985 8780 8784
26. C.R. Gerfen, M. Herkenham, and J. Thibault The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems J. Neurosci. 7 1987 3915 3934
27. M. Glass, M. Dragunow, and R.L.M. Faull The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine, adenosine and GABAa receptor alterations in the human basal ganglia in Huntington's disease Neuroscience 97 2000 505 519
28. A.M. Graybiel Neurotransmitters and neuromodulators in the basal ganglia Trends Neurosci. 13 1990 244 253
29. O. Hansson, A. Peters, M. Leist, P. Nicotera, R.F. Castilho, and P. Brundin Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity Proc. Natl. Acad. U. S. A. 96 1999 8727 8732
30. O. Hansson, E. Guatteo, N.B. Mercuri, G. Bernardi, X.J. Li, R.F. Castilho, and P. Brundin Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioral deficits, and changes in calcium homeostasis in mice transgenic for exon 1 of the huntingtin gene Eur. J. Neurosci. 14 2001 1492 1504
31. O. Hansson, R.F. Castilho, L. Korhonen, D. Lindholm, G.P. Bates, and P. Brundin Partial resistance to malonate-induced striatal cell death in transgenic mouse models of Huntington's disease is dependent on age and CAG repeat length J. Neurochem. 78 2001 694 703
32. J.C. Hedreen, and S.E. Folstein Early loss of neostriatal striosome neurons in Huntington's disease J. Neuropathol. Exp. Neurol. 54 1995 105 120
33. M.A. Hickey, and A.J. Morton Mice transgenic for Huntington's disease are resistant to chronic 3-nitropropionic acid-induced striatal toxicity J. Neurochem. 75 2000 2163 2171
34. M.A. Hickey, G.P. Reynolds, and A.J. Morton The role of dopamine in motor symptoms in the R6/2 transgenic mouse model of Huntington's disease J. Neurochem. 81 2002 46 59
35. 28k immunoreactivity in rat striatal neurons in vivo and in vitro mimic the pattern seen in Huntington's disease Neuroscience 65 1995 397 407
36. 28k-containing neurons in animal models of neurodegeneration: possible protection from excitotoxicity Mol. Brain Res. 13 1992 251 261
37. C. Iannicola, S. Moreno, S. Oliverio, R. Nardacci, A. Ciof-Luzzatto, and M. Piacentini Early alterations in gene expression and cell morphology in a mouse model of Huntington's disease J. Neurochem. 75 2000 830 839
38. 28k Neuroscience 97 2000 495 504
39. G.J. Klapstein, R.S. Fisher, H. Zanjani, C. Cepeda, E.S. Jokel, M.-F. Chesselet, and M.S. Levine Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice J. Neurophysiol. 86 2001 2667 2677
40. G.A. Laforet, E. Sapp, K. Chase, C. McIntyre, F.M. Boyce, M. Campbell, B.A. Cadigan, L. Warzecki, D.A. Tagle, P.H. Reddy, C. Cepeda, C.R. Calvert, E.S. Jokel, G.J. Klapstein, M.A. Ariano, M.S. Levine, M. DiFiglia, and N. Aronin Changes in cortical striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease J. Neurosci. 21 2001 9112 9123
41. M.S. Levine, G.J. Klapstein, A. Koppel, E. Gruen, C. Cepeda, M.E. Vargas, E.S. Jokel, E.M. Carpenter, H. Zanjani, R.S. Hurst, A. Efstratiadis, S. Zeitlin, and M.F. Chesselet Enhanced sensitivity to N-methyl-d-aspartate receptor activation in transgenic and knock-in mouse models of Huntington's disease J. Neurosci. Res. 58 1999 515 532
42. L. Li, M. Fan, C.D. Icton, N. Chen, B.R. Leavitt, M.R. Hayden, T.H. Murphy, and L.A. Raymond Role of NR2B-type NMDA receptors in selective neurodegeneration in Huntington disease Neurobiol. Aging 24 2003 1113 1121
43. L. Li, T.H. Murphy, M.R. Hayden, and L.A. Raymond Enhanced striatal NR2B-containing N-methyl-d-aspartate receptor-mediated synaptic currents in a mouse model of Huntington disease J. Neurophysiol. 92 2004 2738 2746
44. J.C. Lievens, B. Woodman, A. Mahal, O. Spasic-Boscovic, D. Samuel, L. Kerkerian-Le Goff, and G.P. Bates Impaired glutamate uptake in the R6 Huntington's disease transgenic mice Neurobiol. Dis. 8 2001 807 821
45. J.C. Lievens, B. Woodman, A. Mahal, and G.P. Bates Abnormal phosphorylation of synapsin I predicts a neuronal transmission impairment in the R6/2 Huntington's disease transgenic mice Mol. Cell. Neurosci. 20 2002 638 648
46. 28k expression in the striatal matrix J. Comp. Neurol. 320 1992 304 322
47. 28k in the rat hippocampus following focal stimulation of the perforant path Neuron 6 1991 627 633
48. R. Luthi-Carter, A. Strand, N.L. Peters, S.M. Solano, Z.R. Hollingsworth, A.S. Menon, A.S. Frey, B.S. Spektor, J. Penney, G. Schilling, C.A. Ross, D.R. Borchelt, S.J. Tapscott, A.B. Young, J.H. Cha, and J.M. Olson Decreased expression of striatal signaling genes in a mouse model of Huntington's disease Hum. Mol. Genet. 9 2000 1259 1271
49. R. Luthi-Carter, S. Hanson, A.D. Strand, D.A. Bergstrom, W. Chun, N.L. Peters, A.M. Woods, E.Y. Chan, C. Kooperberg, D. Krainc, A.B. Young, S.J. Tapscott, and J.M. Olson Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain Hum. Mol. Genet. 11 2002 1911 1926
50. L. Mangiarini, K. Sathasivam, M. Seller, B. Cozens, A. Harper, C. Hetherington, M. Lawton, Y. Trottier, H. Lehrach, S.W. Davies, and G.P. Bates 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 493 506
51. 28k in cultured hippocampal neurons Neuron 6 1991 41 51
52. C.A. Meade, Y.P. Deng, F. Fusco, N. Del Mar, S. Hersch, D. Goldowitz, and A. Reiner Cellular localization and development of neuronal intranuclear inclusions (NIIs) in striatum and cortical neurons in R6/2 transgenic mice J. Comp. Neurol. 449 2002 241 269
53. 28k via herpes simplex virus amplicon vector decreases calcium ion mobilization and enhances neuronal survival after hypoglycemic challenge J. Neurochem. 69 1997 1039 1047
54. L. Menalled, H. Zanjani, L. MacKenzie, A. Koppel, E. Carpenter, S. Zeitlin, and M.F. Chesselet Decrease in striatal enkephalin mRNA in mouse models of Huntington's disease Exp. Neurol. 162 2000 328 342
55. M.L. Monje, R. Phillips, and R. Sapolsky Calbindin overexpression buffers hippocampal cultures from the energetic impairments caused by glutamate Brain Res. 911 2001 37 42
56. 28k localization in stratum pyramidale of rat hippocampus Hippocampus 5 1995 25 39
57. A.J. Morton, and W. Leavens Mice transgenic for the human Huntington's disease mutation have reduced sensitivity to kainic acid toxicity Brain Res. Bull. 52 2000 51 59
58. B. NicNiocaill, B. Haraldsson, O. Hansson, W.T. O'Connor, and P. Brundin Altered striatal amino acid neurotransmitter release monitored using microdialysis in R6/1 Huntington transgenic mice Eur. J. Neurosci. 13 2001 206 210
59. W. Paschen Glutamate excitotoxicity in transient global cerebral ischemia Acta Neurobiol. Exp. 56 1996 313 322
60. A. Petersen, Z. Puschban, J. Lotharius, B. NicNiocaill, P. Wiekop, W.T. O'Connor, and P. Brundin Evidence for dysfunction of the nigrostriatal pathway in the R6/1 line of transgenic Huntington's disease mice Neurobiol. Dis. 11 2002 134 146
61. 28k gene transfer via herpes simplex virus amplicon vector decrease hippocampal damage in vivo following neurotoxic insults J. Neurochem. 73 1999 1200 1205
62. 28k and GABA in the matrix compartment of the rat caudate-putamen nuclei Neuroscience 71 1996 167 178
63. A.E. Pollack, J.L. Bird, E.B. Lambert, Z.P. Florin, and V.L. Castellar Role of NMDA glutamate receptors in regulating D2 dopamine-dependent Fos induction in the rat striatopallidal pathway Brain Res. 818 1999 543 547
64. L. Prensa, J.M. Gimenez-Amaya, and A. Parent Chemical heterogeneity of the striosomal compartment in the human striatum J. Comp. Neurol. 413 1999 603 618
65. G.V. Rebec, S.J. Barton, and M.D. Ennis Dysregulation of ascorbate release in the striatum of behaving mice expressing the Huntington's disease gene J. Neurosci. 22 2002 1 5
66. A. Reiner, I. Dragatsis, S. Zeitlin, and D. Goldowitz Wild-type Huntingtin plays a role in brain development and neuronal survival Mol. Neurobiol. 28 2003 259 275
67. E.K. Richfield, and M. Herkenham Selective vulnerability in Huntington's disease: preferential loss of cannabinoid receptors in lateral globus pallidus Ann. Neurol. 36 1994 577 584
68. E.K. Richfield, K.A. Maguire-Zeiss, H.E. Vonkeman, and P. Voorn Preferential loss of preproenkephalin versus preprotachykinin neurons from the striatum of Huntington's disease patients Ann. Neurol. 38 1995 852 861
69. 28k in HEK 293 cells Cell Calcium 29 2001 277 287
70. C.A. Ross Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative disease? Neuron 19 1997 1147 1150
71. C.A. Ross, R.L. Margolis, A. Rosenblatt, N.G. Ranen, M. Becher, and E. Aylward Huntington disease and the related disorder, dentatorubral- pallidoluysian atrophy (DRPLA) Medicine 76 1996 305 338
72. E. Sapp, J. Penney, A. Young, N. Aronin, J.P. Vonsattel, and M. DiFiglia Axonal transport of N-terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease J. Neuropathol. Exp. Neurol. 58 1999 165 173
73. F. Saudou, S. Finkbeiner, D. Devys, and M.E. Greenberg Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions Cell 95 1998 55 56
74. J. Schiefer, A. Alberty, T. Dose, S. Oliva, J. Noth, and C.M. Kosinski Huntington's disease transgenic mice are resistant to global cerebral ischemia Neurosci. Lett. 334 2002 99 102
75. R. Schwarcz, A.C. Foster, E.D. French, W.O. Whetsell Jr., and C. Kohler Excitotoxic models for neurodegenerative disorders Life Sci. 35 1984 19 32
76. G. Szebenyi, G.A. Morfini, A. Babcock, M. Gould, K. Selkoe, D.L. Stenoien, M. Young, P.W. Faber, M.E. MacDonald, M.J. McPhaul, and S.T. Brady Neuropathogenic forms of huntingtin and androgen receptor inhibit fast axonal transport Neuron 40 2003 41 52
77. Z. Sun, N. Del Mar, C. Meade, D. Goldowitz, and A. Reiner Differential changes in striatal projection neurons in R6/2 transgenic mice for Huntington's disease Neurobiol. Dis. 11 2003 369 385
78. H. Takano, and J.F. Gusella The predominantly HEAT-like motif structure of huntingtin and its association and coincident nuclear entry with dorsal, an NF-kB/Rel/dorsal family transcription factor BMC Neurosci. 3 2002 3 15
79. The 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
80. M. Turmaine, A. Raza, A. Mahal, L. Mangiarini, G.P. Bates, and S.W. Davies Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease Proc. Nat. Aced. Sci. U. S. A. 97 2000 8093 8097
81. M. Tymianski, M.C. Wallace, I. Spigelman, M. Uno, P.L. Carlen, C.H. Tator, and M.P. Charlton Cell-permeant calcium chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo Neuron 11 1993 221 235
82. J.P. Vonsattel, and M. DiFiglia Huntington disease J. Neuropathol. Exp. Neurol. 57 1998 369 384
83. 28k overexpression protects striatal neurons from transient focal cerebral ischemia Stroke 32 2001 1028 1035
84. M.M. Zeron, N. Chen, A. Moshaver, A. Ting-Chun Lee, C.L. Wellington, M.R. Hayden, and L.A. Raymond Mutant Huntingtin enhances excitotoxic cell death Mol. Cell. Neurosci. 17 2001 41 53
85. M.M. Zeron, O. Hansson, N. Chen, C.L. Wellington, B.R. Leavitt, P. Brundin, M.R. Hayden, and L.A. Raymond Increased sensitivity to N-methyl-d-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease Neuron 33 2002 849 860
86. M.M. Zeron, H.B. Fernandes, C. Krebs, J. Shehadeh, C.L. Wellington, B.R. Leavitt, K.G. Baimbridge, M.R. Hayden, and L.A. Raymond Potentiation of NMDA receptor-mediated excitotoxicity linked with intrinsic apoptotic pathway in YAC transgenic mouse model of Huntington's disease Mol. Cell. Neurosci. 25 2004 469 479