Progressive and selective striatal degeneration in primary neuronal cultures using lentiviral vector coding for a mutant huntingtin fragment

Neurobiology of Disease

Volumn 20, Issue 3, 2005, Pages 785-798

  Zala, Diana ^a   Benchoua, Alexandra ^b   Brouillet, Emmanuel ^b   Perrin, Valérie ^a   Gaillard, Marie Claude ^b   Zurn, Anne D ^c   Aebischer, Patrick ^a   Déglon, Nicole ^a,b  

^a EPFL   (Switzerland)

^b DIF   (France)

^c University of Lausanne Medical Center   (Switzerland)

Author keywords

Lentiviral vector; Mutant huntingtin; Striatal degeneration

Indexed keywords

BIOCHEMICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; HEAT SHOCK PROTEIN 70; HUNTINGTIN; LENTIVIRUS VECTOR; MICROTUBULE ASSOCIATED PROTEIN 2; MUTANT PROTEIN; NEUROFILAMENT PROTEIN; NUCLEAR PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL DEATH; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; CORPUS STRIATUM; EMBRYO; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; NERVE CELL CULTURE; NERVE DEGENERATION; NEURITE; NEUROPROTECTION; NICK END LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; TRANSGENE; WESTERN BLOTTING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CELLS, CULTURED; CILIARY NEUROTROPHIC FACTOR; CORPUS STRIATUM; GENETIC VECTORS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HUNTINGTON DISEASE; INCLUSION BODIES; LENTIVIRUS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; NEURONS; NUCLEAR PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TRANSFECTION; TRANSGENES;

EID: 27744443276     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.05.017     Document Type: Article

References (69)

1. J. Alberch, E. Perez-Navarro, and J.M. Canals Neurotrophic factors in Huntington's disease Prog. Brain Res. 146 2004 195 229
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. A.C. Bachoud-Levi, N. Déglon, J.P. Nguyen, J. Bloch, C. Bourdet, L. Winkel, P. Remy, M. Goddard, J.P. Lefaucheur, P. Brugieres, S. Baudic, P. Cesaro, M. Peschanski, and P. Aebischer Neuroprotective gene therapy for Huntington's disease using a polymer encapsulated BHK cell line engineered to secrete human CNTF Hum. Gene Ther. 11 2000 1723 1729
4. G. Bates Huntingtin aggregation and toxicity in Huntington's disease Lancet 361 2003 1642 1644
5. A.P. Bemelmans, P. Horellou, L. Pradier, I. Brunet, P. Colin, and J. Mallet Brain-derived neurotrophic factor-mediated protection of striatal neurons in an excitotoxic rat model of Huntington's disease, as demonstrated by adenoviral gene transfer Hum. Gene Ther. 10 1999 2987 2997
6. J.M. Canals, J.R. Pineda, J.F. Torres-Peraza, M. Bosch, R. Martin-Ibanez, M.T. Munoz, G. Mengod, P. Ernfors, and J. Alberch Brain-derived neurotrophic factor regulates the onset and severity of motor dysfunction associated with enkephalinergic neuronal degeneration in Huntington's disease J. Neurosci. 24 2004 7727 7739
7. Y. Chai, S.L. Koppenhafer, N.M. Bonini, and H.L. Paulson Analysis of the role of heat shock protein (Hsp) molecular chaperones in polyglutamine disease J. Neurosci. 19 1999 10338 10347
8. Y. Chai, J. Shao, V.M. Miller, A. Williams, and H.L. Paulson Live-cell imaging reveals divergent intracellular dynamics of polyglutamine disease proteins and supports a sequestration model of pathogenesis Proc. Natl. Acad. Sci. U. S. A. 99 2002 9310 9315
9. E.Y. Chan, R. Luthi-Carter, A. Strand, S.M. Solano, S.A. Hanson, M.M. DeJohn, C. Kooperberg, K.O. Chase, M. DiFiglia, A.B. Young, B.R. Leavitt, J.H. Cha, N. Aronin, M.R. Hayden, and J.M. Olson Increased huntingtin protein length reduces the number of polyglutamine-induced gene expression changes in mouse models of Huntington's disease Hum. Mol. Genet. 11 2002 1939 1951
10. 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, and C.A. Ross Truncated N-terminal fragments of huntingtin with expanded glutamine repeats form nuclear and cytoplasmic aggregates in cell culture Hum. Mol. Genet. 7 1998 783 790
11. C.J. Cummings, M.A. Mancini, B. Antalffy, D.B. DeFranco, H.T. Orr, and H.Y. Zoghbi Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1 Nat. Genet. 19 1998 148 154
12. L.P. de Almeida, D. Zala, and P. Aebischer Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease Neurobiol. Dis. 8 2001 433 446
13. L.P. de Almeida, C.A. Ross, D. Zala, and P. Aebischer Lentiviral-mediated delivery of mutant huntingtin in the striatum of rats induces a selective neuropathology modulated by polyglutamine repeat size, huntingtin expression levels, and protein length J. Neurosci. 22 2002 3473 3483
14. N. Déglon, J.L. Tseng, J.C. Bensadoun, A.D. Zurn, Y. Arsenijevic, L. Pereira de Almeida, R. Zufferey, D. Trono, and P. Aebischer Self-inactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease Hum. Gene Ther. 11 2000 179 190
15. M. DiFiglia, E. Sapp, K. Chase, C. Schwarz, A. Meloni, C. Young, E. Martin, J.P. Vonsattel, R. Carraway, and S.A. Reeves Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons Neuron 14 1995 1075 1081
16. 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
17. A.W. Dunah, H. Jeong, A. Griffin, Y.M. Kim, D.G. Standaert, S.M. Hersch, M.M. Mouradian, A.B. Young, N. Tanese, and D. Krainc Sp1 and TAFII130 transcriptional activity disrupted in early Huntington's disease Science 296 2002 2238 2243
18. D.F. Emerich, C.K. Cain, C. Greco, J.A. Saydoff, Z.Y. Hu, H. Liu, and M.D. Lindner Cellular delivery of human CNTF prevents motor and cognitive dysfunction in a rodent model of Huntington's disease Cell Transplant. 6 1997 249 266
19. R.J. Ferrante, C.A. Gutekunst, F. Persichetti, S.M. McNeil, N.W. Kowall, J.F. Gusella, M.E. MacDonald, M.F. Beal, and S.M. Hersch Heterogeneous topographic and cellular distribution of huntingtin expression in the normal human neostriatum J. Neurosci. 17 1997 3052 3063
20. I. Ferrer, E. Goutan, C. Marin, M.J. Rey, and T. Ribalta Brain-derived neurotrophic factor in Huntington disease Brain Res. 866 2000 257 261
21. F.R. Fusco, Q. Chen, W.J. Lamoreaux, G. Figueredo-Cardenas, Y. Jiao, J.A. 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
22. F.R. Fusco, A. Martorana, Z. De March, M.T. Viscomi, G. Sancesario, and G. Bernardi Huntingtin distribution among striatal output neurons of normal rat brain Neurosci. Lett. 339 2003 53 56
23. J. Gafni, and L.M. Ellerby Calpain activation in Huntington's disease J. Neurosci. 22 2002 4842 4849
24. L.R. Gauthier, B.C. Charrin, M. Borrell-Pages, J.P. Dompierre, H. Rangone, F.P. Cordelieres, J. De Mey, M.E. MacDonald, V. Lessmann, S. Humbert, and F. Saudou Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules Cell 118 2004 127 138
25. D. Goffredo, D. Rigamonti, M. Tartari, A. De Micheli, C. Verderio, M. Matteoli, C. Zuccato, and E. Cattaneo Calcium-dependent cleavage of endogenous wild-type huntingtin in primary cortical neurons J. Biol. Chem. 277 2002 39594 39598
26. S. Gunawardena, L.S. Her, R.G. Brusch, R.A. Laymon, I.R. Niesman, B. Gordesky-Gold, L. Sintasath, N.M. Bonini, and L.S. Goldstein Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila Neuron 40 2003 25 40
27. C.A. Gutekunst, S.H. Li, H. Yi, J.S. Mulroy, S. Kuemmerle, R. Jones, D. Rye, R.J. Ferrante, S.M. Hersch, and X.J. Li Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology J. Neurosci. 19 1999 2522 2534
28. A.S. Hackam, R. Singaraja, C.L. Wellington, M. Metzler, K. McCutcheon, T. Zhang, M. Kalchman, and M.R. Hayden The influence of huntingtin protein size on nuclear localization and cellular toxicity J. Cell Biol. 141 1998 1097 1105
29. H. Heinsen, M. Strik, M. Bauer, K. Luther, G. Ulmar, D. Gangnus, G. Jungkunz, W. Eisenmenger, and M. Gotz Cortical and striatal neurone number in Huntington's disease Acta Neuropathol. (Berl.) 88 1994 320 333
30. E. Hermel, J. Gafni, S.S. Propp, B.R. Leavitt, C.L. Wellington, J.E. Young, A.S. Hackam, A.V. Logvinova, A.L. Peel, S.F. Chen, V. Hook, R. Singaraja, S. Krajewski, P.C. Goldsmith, H.M. Ellerby, M.R. Hayden, D.E. Bredesen, and L.M. Ellerby Specific caspase interactions and amplification are involved in selective neuronal vulnerability in Huntington's disease Cell Death Differ. 11 2004 424 438
31. A.F. Hottinger, M. Azzouz, N. Déglon, P. Aebischer, and A.D. Zurn Complete and long-term rescue of lesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neurotrophic factor in the facial nucleus J. Neurosci. 20 2000 5587 5593
32. N.R. Jana, M. Tanaka, G. Wang, and N. Nukina Polyglutamine length-dependent interaction of Hsp40 and Hsp70 family chaperones with truncated N-terminal huntingtin: their role in suppression of aggregation and cellular toxicity Hum. Mol. Genet. 9 2000 2009 2018
33. Y. Kobayashi, A. Kume, M. Li, M. Doyu, M. Hata, K. Ohtsuka, and G. Sobue Chaperones Hsp70 and Hsp40 suppress aggregate formation and apoptosis in cultured neuronal cells expressing truncated androgen receptor protein with expanded polyglutamine tract J. Biol. Chem. 275 2000 8772 8778
34. S. Kuemmerle, C.A. Gutekunst, A.M. Klein, X.J. Li, S.H. Li, M.F. Beal, S.M. Hersch, and R.J. Ferrante Huntington aggregates may not predict neuronal death in Huntington's disease Ann. Neurol. 46 1999 842 849
35. G.B. Landwehrmeyer, S.M. McNeil, L.S.t. Dure, P. Ge, H. Aizawa, Q. Huang, C.M. Ambrose, M.P. Duyao, E.D. Bird, and E. Bonilla Huntington's disease gene: regional and cellular expression in brain of normal and affected individuals Ann. Neurol. 37 1995 218 230
36. S.H. Li, A.L. Cheng, H. Li, and X.J. Li Cellular defects and altered gene expression in PC12 cells stably expressing mutant huntingtin J. Neurosci. 19 1999 5159 5172
37. H. Li, S.H. Li, Z.X. Yu, P. Shelbourne, and X.J. Li Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice J. Neurosci. 21 2001 8473 8481
38. Y.F. Liu Expression of polyglutamine-expanded Huntingtin activates the SEK1-JNK pathway and induces apoptosis in a hippocampal neuronal cell line J. Biol. Chem. 273 1998 28873 28877
39. A. Lunkes, and J.L. Mandel A cellular model that recapitulates major pathogenic steps of Huntington's disease Hum. Mol. Genet. 7 1998 1355 1361
40. A. Lunkes, K.S. Lindenberg, L. Ben-Haiem, C. Weber, D. Devys, G.B. Landwehrmeyer, J.L. Mandel, and Y. Trottier Proteases acting on mutant huntingtin generate cleaved products that differentially build up cytoplasmic and nuclear inclusions Mol. Cell 10 2002 259 269
41. R. Luthi-Carter, A. Strand, N.L. Peters, S.M. Solano, Z.R. Hollingsworth, A.S. Menon, A.S. Frey, B.S. Spektor, E.B. 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
42. F.C. Nucifora Jr., M. Sasaki, M.F. Peters, H. Huang, J.K. Cooper, M. Yamada, H. Takahashi, S. Tsuji, J. Troncoso, V.L. Dawson, T.M. Dawson, and C.A. Ross Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity Science 291 2001 2423 2428
43. J.A. Parker, J.B. Connolly, C. Wellington, M. Hayden, J. Dausset, and C. Neri Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death Proc. Natl. Acad. Sci. U. S. A. 98 2001 13318 13323
44. A. Petersen, K.E. Larsen, G.G. Behr, N. Romero, S. Przedborski, P. Brundin, and D. Sulzer Expanded CAG repeats in exon 1 of the Huntington's disease gene stimulate dopamine-mediated striatal neuron autophagy and degeneration Hum. Mol. Genet. 10 2001 1243 1254
45. E. Régulier, Y. Trottier, V. Perrin, P. Aebischer, and N. Déglon Early and reversible neuropathology induced by tetracycline-regulated lentiviral overexpression of mutant huntingtin in rat striatum Hum. Mol. Genet. 12 2003 2827 2836
46. D. Rigamonti, S. Sipione, D. Goffredo, C. Zuccato, E. Fossale, and E. Cattaneo Huntingtin's neuroprotective activity occurs via inhibition of procaspase-9 processing J. Biol. Chem. 276 2001 14545 14548
47. C.A. Ross Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders Neuron 35 2002 819 822
48. I. Sanchez, C.J. Xu, P. Juo, A. Kakizaka, J. Blenis, and J. Yuan Caspase-8 is required for cell death induced by expanded polyglutamine repeats Neuron 22 1999 623 633
49. R.O. Sanchez Mejia, and R.M. Friedlander Caspases in Huntington's disease Neuroscientist 7 2001 480 489
50. E. Sapp, C. Schwarz, K. Chase, P.G. Bhide, A.B. Young, J. Penney, J.P. Vonsattel, N. Aronin, and M. DiFiglia Huntingtin localization in brains of normal and Huntington's disease patients Ann. Neurol. 42 1997 604 612
51. 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 66
52. G. Schaffar, P. Breuer, R. Boteva, C. Behrends, N. Tzvetkov, N. Strippel, H. Sakahira, K. Siegers, M. Hayer-Hartl, and F.U. Hartl Cellular toxicity of polyglutamine expansion proteins; mechanism of transcription factor deactivation Mol. Cell 15 2004 95 105
53. A.R. Schroder, P. Shinn, H. Chen, C. Berry, J.R. Ecker, and F. Bushman HIV-1 integration in the human genome favors active genes and local hotspots Cell 110 2002 521 529
54. S. Sipione, D. Rigamonti, M. Valenza, C. Zuccato, L. Conti, J. Pritchard, C. Kooperberg, J.M. Olson, and E. Cattaneo Early transcriptional profiles in huntingtin-inducible striatal cells by microarray analyses Hum. Mol. Genet. 11 2002 1953 1965
55. B.J. Snider, J.L. Moss, F.J. Revilla, C.S. Lee, V.C. Wheeler, M.E. Macdonald, and D.W. Choi Neocortical neurons cultured from mice with expanded CAG repeats in the huntingtin gene: unaltered vulnerability to excitotoxins and other insults Neuroscience 120 2003 617 625
56. J.S. Steffan, A. Kazantsev, O. Spasic-Boskovic, M. Greenwald, Y.Z. Zhu, H. Gohler, E.E. Wanker, G.P. Bates, D.E. Housman, and L.M. Thompson The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription Proc. Natl. Acad. Sci. U. S. A. 97 2000 6763 6768
57. D.L. Stenoien, C.J. Cummings, H.P. Adams, M.G. Mancini, K. Patel, G.N. DeMartino, M. Marcelli, N.L. Weigel, and M.A. Mancini Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone Hum. Mol. Genet. 8 1999 731 741
58. K.L. Sugars, and D.C. Rubinsztein Transcriptional abnormalities in Huntington disease Trends Genet. 19 2003 233 238
59. The Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group Cell 72 1993 971 983
60. F. Trettel, D. Rigamonti, P. Hilditch-Maguire, V.C. Wheeler, A.H. Sharp, F. Persichetti, E. Cattaneo, and M.E. MacDonald Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells Hum. Mol. Genet. 9 2000 2799 2809
61. J.P. Vonsattel, H. Aizawa, P. Ge, M. DiFiglia, A.C. McKee, M. MacDonald, J.F. Gusella, G.B. Landwehrmeyer, E.D. Bird, and E.P. Richardson Jr. An improved approach to prepare human brains for research J. Neuropathol. Exp. Neurol. 54 1995 42 56
62. Y. Wu, and J.W. Marsh Gene transcription in HIV infection Microbes Infect. 5 2003 1023 1027
63. A. Wyttenbach, J. Carmichael, J. Swartz, R.A. Furlong, Y. Narain, J. Rankin, and D.C. Rubinsztein Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease Proc. Natl. Acad. Sci. U. S. A. 97 2000 2898 2903
64. A. Wyttenbach, J. Swartz, H. Kita, T. Thykjaer, J. Carmichael, J. Bradley, R. Brown, M. Maxwell, A. Schapira, T.F. Orntoft, K. Kato, and D.C. Rubinsztein Polyglutamine expansions cause decreased CRE-mediated transcription and early gene expression changes prior to cell death in an inducible cell model of Huntington's disease Hum. Mol. Genet. 10 2001 1829 1845
65. A. Wyttenbach, O. Sauvageot, J. Carmichael, C. Diaz-Latoud, A.P. Arrigo, and D.C. Rubinsztein Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin Hum. Mol. Genet. 11 2002 1137 1151
66. D. Zala, J.C. Bensadoun, L. Pereira de Almeida, B.R. Leavitt, C.A. Gutekunst, P. Aebischer, M.R. Hayden, and N. Déglon Long-term lentiviral-mediated expression of ciliary neurotrophic factor in the striatum of Huntington's disease transgenic mice Exp. Neurol. 185 2004 26 35
67. 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
68. C. Zuccato, A. Ciammola, D. Rigamonti, B.R. Leavitt, D. Goffredo, L. Conti, M.E. MacDonald, R.M. Friedlander, V. Silani, M.R. Hayden, T. Timmusk, S. Sipione, and E. Cattaneo Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease Science 293 2001 493 498
69. C. Zuccato, M. Tartari, A. Crotti, D. Goffredo, M. Valenza, L. Conti, T. Cataudella, B.R. Leavitt, M.R. Hayden, T. Timmusk, D. Rigamonti, and E. Cattaneo Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes Nat. Genet. 35 2003 76 83