Cerebral PET imaging and histological evidence of transglutaminase inhibitor cystamine induced neuroprotection in transgenic R6/2 mouse model of Huntington's disease

Journal of the Neurological Sciences

Volumn 231, Issue 1-2, 2005, Pages 57-66

  Wang, Xukui ^a   Sarkar, Aparajita ^a   Cicchetti, Francesca ^b   Yu, Meixiang ^a   Zhu, Aijun ^a   Jokivarsi, Kimmo ^a   Saint Pierre, Martine ^b   Brownell, Anna Liisa ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Centre de Recherche en Neurosciences   (Canada)

Author keywords

Cellular inclusion; Cystamine; Dopamine D2 receptor; Glucose metabolism; Huntington's disease; Neuroprotection

Indexed keywords

AMINOTRANSFERASE INHIBITOR; CARBON 11; CYSTAMINE; DOPAMINE 2 RECEPTOR; FLUORODEOXYGLUCOSE F 18; GLUCOSE; RACLOPRIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEGENERATION; BRAIN METABOLISM; CALCULATION; CELL INCLUSION; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DOSE RESPONSE; GLUCOSE BRAIN LEVEL; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; HISTOLOGY; HUNTINGTON CHOREA; MALE; MOUSE; NEUROPROTECTION; NISSL SUBSTANCE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; STAINING; STATISTICAL SIGNIFICANCE; TRANSGENIC MOUSE;

EID: 15944409947     PISSN: 0022510X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jns.2004.12.011     Document Type: Article

References (71)

1. A. Young, and J.B. Penney Neurochemical anatomy and movement disorders Neurol. Clin. 2 3 1984 417 433
2. C. Ross, R.L. Margolis, A. Rosenblatt, N.G. Ranen, M.W. Becher, and E. Aylward Huntington disease and the related disorder, dentatorubral- pallidoluysian atrophy (DRPLA) Medicine (Baltimore) 76 1997 305 338
3. M. Witjes-Ane, M. Vegter-van der Vlis, J.P. van Vugt, J.B. Lanser, J. Hermans, and A.H. Zwinderman Cognitive and motor functioning in gene carriers for Huntington's disease: a baseline study J. Neuropsychiatry Clin. Neurosci. 15 1 2003 7 16
4. R. Albin, and D.A. Tagle Genetics and molecular biology of Huntington's disease Trends Neurosci. 18 1995 11 14
5. C. Heizmann, and K. Braun Changes in Ca(2+)-binding proteins in human neurodegenerative disorders Trends Neurosci. 15 7 1992 259 264
6. The Huntington's Disease Collaborative Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes Cell 72 1993 971 983
7. M. MacDonald, S. Gines, J.F. Gusella, and V.C. Wheeler Huntington's disease Neuromol. Med. 4 2003 7 20
8. H. Green Human genetic diseases due to codon reiteration: relationship to an evolutionary mechanism Cell 74 1993 955 956
9. J. Burke, J.J. Enghild, M.E. Martin, Y.S. Jou, R.M. Myers, and A.D. Roses Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH Nat. Med. 2 1996 347 350
10. M. DiFiglia, E. Sapp, K.O. Chase, S.W. Davies, G.P. Bates, and J.P. Vonsattel Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain Science 277 1997 1990 1993
11. M. Kim, H.S. Lee, G. LaForet, C. McIntyre, E.J. Martin, and P. Chang Mutant huntingtin expression in clonal striatal cells: dissociation of inclusion formation and neuronal survival by caspase inhibition J. Neurosci. 19 1999 964 973
12. C. Meade, Y.P. Deng, F.R. Fusco, N. Del Mar, S. Hersch, and D. Goldowitz Cellular localization and development of neuronal intranuclear inclusions in striatal and cortical neurons in R6/2 transgenic mice J. Comp. Neurol. 449 2002 241 269
13. S. Taniguchi, A.M. McDonagh, S.M. Pickering-Brown, Y. Umeda, T. Iwatsubo, and M. Hasegawa The neuropathology of frontotemporal lobar degeneration with respect to the cytological and biochemical characteristics of tau protein Neuropathol. Appl. Neurobiol. 30 1 2004 1 18
14. E. Zemskov, N.R. Jana, M. Kurosawa, H. Miyazaki, N. Sakamoto, and M. Nekooki Pro-apoptotic protein kinase C delta is associated with intranuclear inclusions in a transgenic model of Huntington's disease J. Neurochem. 87 2 2003 395 406
15. L. Mangiarini, K. Sathasivam, M. Seller, B. Cozens, A. Harper, and C. Hetherington Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice Cell 87 3 1996 493 506
16. S. Davies, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, and C.A. Ross Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
17. M. Becher, J.A. Kotzuk, A.H. Sharp, S.W. Davies, G.P. Bates, and D.L. Price Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length Neurobiol. Dis. 4 1998 387 397
18. M. Karpuj, H. Garren, H. Slunt, D.L. Price, J. Gusella, and M.W. Becher Transglutaminase aggregates huntingtin into nonamyloidogenic polymers, and its enzymatic activity increases in Huntington's disease brain nuclei Proc. Natl. Acad. Sci. U. S. A. 96 1999 7388 7393
19. G. Zainelli, C.A. Ross, J.C. Troncoso, and N.A. Muma Transglutaminase cross-links in intranuclear inclusions in Huntington disease J. Neuropathol. Exp. Neurol. 62 2003 14 24
20. J. Folk Transglutaminases Annu. Rev. Biochem. 49 1980 517 531
21. L. Lorand DRPLA aggregation and transglutaminase, revisited Nat. Genet. 20 1998 231
22. A. Dedeoglu, J.K. Kubilus, T.M. Jeitner, S.A. Matson, M. Bogdanov, and N.W. Kowall Therapeutic effects of cystamine in a murine model of Huntington's disease J. Neurosci. 22 2002 8942 8950
23. M. Karpuj, M.W. Becher, J.E. Springer, D. Chabas, S. Youssef, and R. Pedotti Prolonged survival and decreased abnormal movements in transgenic model of Huntington disease, with administration of the transglutaminase inhibitor cystamine Nat. Med. 8 2002 143 149
24. D. Kuhl, M.E. Phelps, C.H. Markham, E.J. Metter, W.H. Riege, and J. Winter Cerebral metabolism and atrophy in Huntington's disease determined by 18FDG and computed tomographic scan Ann. Neurol. 12 5 1982 425 434
25. T. Kuwert, H.W. Lange, K.J. Langen, H. Herzog, A. Aulich, and L.E. Feinendegen Cortical and subcortical glucose consumption measured by PET in patients with Huntington's disease Brain 113 Pt 5 1990 1405 1423
26. A. Feigin, K.L. Leenders, J.R. Moeller, J. Missimer, G. Kuenig, and P. Spetsieris Metabolic network abnormalities in early Huntington's disease: an [(18)F]FDG PET study J. Nucl. Med. 42 2001 1591 1595
27. M.D. Araujo, S.R. Cherry, K.J. Tatsukawa, T. Toyokuni, and H.I. Kornblum Deficits in striatal dopamine D2 receptors and energy metabolism detected by in vivo mirco PET imaging in a rat model of Huntington's disease Exp. Neurol. 166 2000 287 297
28. M. Ariano, N. Aronin, M. Difiglia, D.A. Tagle, D.R. Sibley, and B.R. Leavitt Striatal neurochemical changes in transgenic models of Huntington's disease J. Neurosci. Res. 68 2002 716 729
29. A.-L. Brownell, P. Hantraye, U. Wullner, L. Hamberg, T. Shoup, and T. Shoup PET- and MRI-based assessment of glucose utilization, dopamine receptor binding, and hemodynamic changes after lesions to the caudate-putamen in primates Exp. Neurol. 125 1994 41 51
30. A.-L. Brownell, I.Y. Chen, X. Wang, M. Yu, and B.G. Jenkins Neurotoxicity-induced changes in striatal dopamine receptor function Ann. N. Y. Acad. Sci. 991 2003 281 283
31. G. Paxinos, and K.B.G. Franklin The mouse brain in stereotaxic coordinates 2nd edition 2001 Academic Press San Diego (CA)
32. U. Scherer-Singler, S.R. Vincent, H. Kimura, and E.G. McGeer Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry J. Neurosci. Methods 9 3 1983 229 234
33. S. Vincent, and O. Johansson Striatal neurons containing both somatostatin- and Avian Pancreatic Polypeptide (APP)-like immunoreactivities and NADPH-diaphorase activity: a light and electron microscopy study J. Comp. Neurol. 217 3 1983 264 270
34. J.R. Glaser, and E.M. Glaser Stereology, morphometry, and mapping: the whole is greater than the sum of its parts J. Chem. Neuroanat. 20 2000 115 126
35. N. Pavese, T.C. Andrews, D.J. Brooks, A.K. Ho, A.E. Rosser, and R.A. Barker Progressive striatal and cortical dopamine receptor dysfunction in Huntington's disease: a PET study Brain 126 2003 1127 1135
36. F. Cicchetti, P.V. Gould, and A. Parent Sparing of striatal neurons coexpressing calretinin and substance P (NK1) receptor in Huntington's disease Brain Res. 730 1996 232 237
37. F. Cicchetti, and A. Parent Striatal interneurons in Huntington's disease: selective increase in the density of calretinin-immunoreactive medium-sized neurons Mov. Disord. 11 1996 619 626
38. A. Antonini, K.L. Leenders, R. Spiegel, D. Meier, P. Vontobel, and M. Weigell-Weber Striatal glucose metabolism and dopamine D2 receptor binding in asymptomatic gene carriers and patients with Huntington's disease Brain 119 1996 2085 2095
39. P. Kelly, D.I. Graham, and J. McCulloch Specific alterations in local cerebral glucose utilization following striatal lesions Brain Res. 233 1 1982 157 172
40. B. Agranoff, and K.A. Frey A regional metabolic contrast method for the study of brain pathology Ann. Neurol., Suppl. 15 1984 S93 S97
41. A. Bokde, P. Pietrini, V. Ibanez, M.L. Furey, G.E. Alexander, and N.R. Graff-Radford The effect of brain atrophy on cerebral hypometabolism in the visual variant of Alzheimer disease Arch. Neurol. 58 2001 480 486
42. E. Palombo, L.J. Porrino, K.S. Bankiewicz, A.M. Crane, L. Sokoloff, and I.J. Kopin Local cerebral glucose utilization in monkeys with hemiparkinsonism induced by intracarotid infusion of the neurotoxin MPTP J. Neurosci. 10 3 1990 860 869
43. J. Eberling, B.C. Richardson, B.R. Reed, N. Wolfe, and W.J. Jagust Cortical glucose metabolism in Parkinson's disease without dementia Neurobiol. Aging 15 3 1994 329 335
44. R. Vannucci, and S.J. Vannucci Glucose metabolism in the developing brain Semin. Perinatol. 24 2000 107 115
45. A.-L. Brownell, Y.I. Chen, M. Yu., X. Wang, A. Dedeoglu, and C. Cicchetti 3-Nitropropionic acid induced neurotoxicity-assessed by ultra high resolution PET with comparison to MRS J. Neurochem. 89 2004 1206 1214
46. M. Beal, E. Brouillet, B.G. Jenkins, R.J. Ferrante, N.W. Kowall, and J.M. Miller Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid J. Neurosci. 13 10 1993 4181 4192
47. M. Garcia, P. Vanhoutte, C. Pages, M.J. Besson, E. Brouillet, and J. Caboche The mitochondrial toxin 3-nitropropionic acid induces striatal neurodegeneration via a c-Jun N-terminal kinase/c-Jun module J. Neurosci. 22 6 2002 2174 2184
48. B. Ravikumar, A. Steward, H. Kita, K. Kato, R. Duden, and D.C. Rubinsztein Raised intracellular glucose concentrations reduce aggregation and cell death caused by mutant huntingtin exon 1 by decreasing mTOR phosphorylation and inducing autophagy Hum. Mol. Genet. 12 9 2003 985 994
49. W. O'Connor Functional neuroanatomy of the basal ganglia as studied by dual-probe microdialysis Nucl. Med. Biol. 25 1998 743 746
50. K. Ostergaard, N.A. Sunde, and E. Dupont Basal ganglia disease. Functional neuroanatomy and therapeutic perspectives Ugeskr. Laeger 162 2000 5480 5483
51. A. Cross, and M. Rossor Dopamine D-1 and D-2 receptors in Huntington's disease Eur. J. Pharmacol. 88 1983 223 229
52. S. Hume, A.A. Lammertsma, R. Myers, S. Rajeswaran, P.M. Bloomfield, and S. Ashworth The potential of high-resolution positron emission tomography to monitor striatal dopaminergic function in rat models of disease J. Neurosci. Methods 67 1996 103 112
53. B. Spektor, D.W. Miller, Z.R. Hollingsworth, Y.A. Kaneko, S.M. Solano, and J.M. Johnson Differential D1 and D2 receptor-mediated effects on immediate early gene induction in a transgenic mouse model of Huntington's disease Brain Res. Mol. Brain Res. 102 2002 118 128
54. J. Brandt, S.E. Folstein, D.F. Wong, J. Links, R.F. Dannals, and A. McDonnell-Sill D2 receptors in Huntington's disease: positron emission tomography findings and clinical correlates J. Neuropsychiatry Clin. Neurosci. 2 1990 20 27
55. S. Augood, R.L. Faull, and P.C. Emson Dopamine D1 and D2 receptor gene expression in the striatum in Huntington's disease Ann. Neurol. 42 1997 215 221
56. L. Lorand Neurodegenerative diseases and transglutaminase Proc. Natl. Acad. Sci. U. S. A. 93 1996 14310 14313
57. A. Cooper, K.F. Sheu, J.R. Burke, O. Onodera, W.J. Strittmatter, and A.D. Roses Polyglutamine domains are substrates of tissue transglutaminase: does transglutaminase play a role in expanded CAG/poly-Q neurodegenerative diseases? J. Neurochem. 69 1997 431 434
58. V. Gentile, C. Sepe, M. Calvani, M.A. Melone, R. Cotrufo, and A.J. Cooper Tissue transglutaminase-catalyzed formation of high-molecular-weight aggregates in vitro is favored with long polyglutamine domains: a possible mechanism contributing to CAG-triplet diseases Arch. Biochem. Biophys. 352 1998 314 321
59. A. Cooper, T.M. Jeitner, V. Gentile, and J.P. Blass Cross linking of polyglutamine domains catalyzed by tissue transglutaminase is greatly favored with pathological-length repeats: does transglutaminase activity play a role in (CAG)(n)/Q(n)-expansion diseases? Neurochem. Int. 40 2002 53 67
60. M. Lesort, W. Chun, G.V. Johnson, and R.J. Ferrante Tissue transglutaminase is increased in Huntington's disease brain J. Neurochem. 73 1999 2018 2027
61. M. Karpuj, M.W. Becher, and L. Steinman Evidence for a role for transglutaminase in Huntington's disease and the potential therapeutic implications Neurochem. Int. 40 2002 31 36
62. L. Lorand, and S.M. Conrad Transglutaminases Mol. Cell. Biochem. 58 1984 9 35
63. C. Greenberg, P.J. Birckbichler, and R.H. Rice Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues FASEB J. 5 1991 3071 3077
64. S. Igarashi, R. Koide, T. Shimohata, M. Yamada, Y. Hayashi, and H. Takano Suppression of aggregate formation and apoptosis by transglutaminase inhibitors in cells expressing truncated DRPLA protein with an expanded polyglutamine stretch Nat. Genet. 18 1998 111 117
65. S. Oliverio, A. Amendola, C. Rodolfo, A. Spinedi, and M. Piacentini Inhibition of "tissue" transglutaminase increases cell survival by preventing apoptosis J. Biol. Chem. 274 1999 34123 34128
66. 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
67. I. Sánchez, C. Mahlke, and J. Yuan Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders Nature 421 2003 373 379
68. B.L. Apostol, A. Kazantsev, S. Raffioni, K. Illes, J. Pallos, and L. Bodai A cell-based assay for aggregation inhibitors as therapeutics of polyglutamine-repeat disease and validation in Drosophila Proc. Natl. Acad. Sci. 100 2003 5950 5955
69. M. Tanaka, Y. Machida, S. Niu, T. Ikeda, N.R. Jana, and H. Doi Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease Nat. Med. 10 2004 148 154
70. M. Lesort, M. Lee, J. Tucholski, and G.V. Johnson Cystamine inhibits caspase activity. Implications for the treatment of polyglutamine disorders J. Biol. Chem. 278 2003 3825 3830
71. H.G. Lüesse, J. Schiefer, A. Spruenken, C. Puls, F. Block, and C.M. Kosinski Evaluation of R6/2 HD transgenic mice for therapeutic studies in Huntington's disease: behavioral testing and impact of diabetes mellitus Behav. Brain Res. 126 2001 185 195