Minocycline in phenotypic models of Huntington's disease

Neurobiology of Disease

Volumn 18, Issue 1, 2005, Pages 206-217

  Bantubungi, Kadiombo ^a   Jacquard, Carine ^b   Greco, Anita ^c   Pintor, Annita ^c   Chtarto, Abdelwahed ^a   Tai, Khalid ^a   Galas, Marie Christine ^d   Tenenbaum, Liliane ^a   Déglon, Nicole ^b   Popoli, Patrizia ^c   Minghetti, Luisa ^c   Brouillet, Emmanuel ^b   Brotchi, Jacques ^a   Levivier, Marc ^a   Schiffmann, Serge N ^a   Blum, David ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b DIF   (France)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d INSERM   (France)

Author keywords

3 Nitropropionic acid; Cell death; Huntington's disease; Minocycline; Quinolinic acid; Striatum

Indexed keywords

3 NITROPROPIONIC ACID; CALPAIN; HUNTINGTIN; MINOCYCLINE; QUINOLINIC ACID; STAUROSPORINE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEGENERATION; BRAIN INJURY; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; CORPUS STRIATUM; EMBRYO; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; INFLAMMATION; MALE; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT;

ANIMALS; CALPAIN; CASPASES; CELL DEATH; CELLS, CULTURED; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALITIS; GLUTAMIC ACID; HUNTINGTON DISEASE; MALE; MINOCYCLINE; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; NITRO COMPOUNDS; NUCLEAR PROTEINS; PHENOTYPE; PROPIONIC ACIDS; QUINOLINIC ACID; RATS; RATS, INBRED LEW; RATS, WISTAR; STAUROSPORINE;

EID: 19944428128     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.09.017     Document Type: Article

References (77)

1. A.R. Amin, M.G. Attur, G.D. Thakker, P.D. Patel, P.R. Vyas, R.N. Patel, I.R. Patel, and S.B. Abramson A novel mechanism of action of tetracyclines: effects on nitric oxide synthases Proc. Natl. Acad. Sci. U. S. A. 93 1996 14014 14019
2. M.F. Beal Energetics in the pathogenesis of neurodegenerative diseases Trends Neurosci. 23 2000 298 304
3. M.F. Beal, N.W. Kowall, D.W. Ellison, M.F. Mazurek, K.J. Swartz, and J.B. Martin Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid Nature 321 1986 168 171
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. J.C. Bensadoun, L.P. de Almeida, M. Dreano, P. Aebischer, and N. Deglon Neuroprotective effect of interleukin-6 and IL6/IL6R chimera in the quinolinic acid rat model of Huntington's syndrome Eur. J. Neurosci. 14 2001 1753 1761
6. N. Bizat, J.M. Hermel, F. Boyer, C. Jacquard, C. Creminon, S. Ouary, C. Escartin, P. Hantraye, S. Kajewski, and E. Brouillet Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease J. Neurosci. 23 2003 5020 5030
7. N. Bizat, J.M. Hermel, S. Humbert, C. Jacquard, C. Creminon, C. Escartin, F. Saudou, S. Krajewski, P. Hantraye, and E. Brouillet In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3 J. Biol. Chem. 278 2003 43245 43253
8. D. Blum, D. Gall, L. Cuvelier, and S.N. Schiffmann Topological analysis of striatal lesions induced by 3-nitropropionic acid in the Lewis rat NeuroReport 12 2001 1769 1772
9. D. Blum, M.C. Galas, D. Gall, L. Cuvelier, and S.N. Schiffmann Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease Neurobiol. Dis. 10 2002 410 426
10. D. Blum, D. Gall, M.C. Galas, P. d'Alcantara, K. Bantubungi, and S.N. Schiffmann The adenosine A1 receptor agonist adenosine amine congener exerts a neuroprotective effect against the development of striatal lesions and motor impairments in the 3-nitropropionic acid model of neurotoxicity J. Neurosci. 22 2002 9122 9133
11. D. Blum, R. Hourez, M.C. Galas, P. Popoli, and S.N. Schiffmann Adenosine receptors and Huntington's disease: implications for pathogenesis and therapeutics Lancet Neurol. 2 2003 366 374
12. D. Blum, M.C. Galas, A. Pintor, E. Brouillet, C. Ledent, C.E. Muller, K. Bantubungi, M. Galluzzo, D. Gall, L. Cuvelier, A.S. Rolland, P. Popoli, and S.N. Schiffmann A dual role of adenosine A2A receptors in 3-nitropropionic acid-induced striatal lesions: implications for the neuroprotective potential of A2A antagonists J. Neurosci. 23 2003 5361 5369
13. D. Blum, A. Chtarto, L. Tenenbaum, J. Brotchi, and M. Levivier Clinical potential of minocycline for neurodegenerative disorders Neurobiol. Dis. 17 3 2004 359 366
14. R.M. Bonelli, C. Heuberger, and F. Reisecker Minocycline for Huntington's disease: an open label study Neurology 60 2003 883 884
15. E. Brouillet, M.C. Guyot, V. Mittoux, S. Altairac, F. Conde, S. Palfi, and P. Hantraye Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat J. Neurochem. 70 1998 794 805
16. E. Brouillet, F. Conde, M.F. Beal, and P. Hantraye Replicating Huntington's disease phenotype in experimental animals Prog. Neurobiol. 59 1999 427 468
17. V. Brundula, N.B. Rewcastle, L.M. Metz, C.C. Bernard, and V.W. Yong Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis Brain 125 2002 1297 1308
18. J.H. Cha Transcriptional dysregulation in Huntington's disease Trends Neurosci. 23 2000 387 392
19. M. Chen, V.O. Ona, M. Li, R.J. Ferrante, K.B. Fink, S. Zhu, J. Bian, L. Guo, L.A. Farrell, S.M. Hersch, W. Hobbs, J.P. Vonsattel, J.H. Cha, and R.M. Friedlander Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease Nat. Med. 6 2000 797 801
20. R.E. Coggeshall A consideration of neural counting methods Trends Neurosci. 15 1992 9 13
21. L.P. de Almeida, C.A. Ross, D. Zala, P. Aebischer, and N. Deglon 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
22. E. Diguet, P.O. Fernagut, X. Wei, Y. Du, R. Rouland, C. Gross, E. Bezard, and F. Tison Deleterious effects of minocycline in animal models of Parkinson's disease and Huntington's disease Eur. J. Neurosci. 19 2004 3266 3276
23. E. Diguet, C.E. Gross, F. Tison, and E. Bezard Rise and fall of minocycline in neuroprotection: need to promote publication of negative results Exp. Neurol. 189 2004 1 4
24. M. Dihne, F. Block, H. Korr, and R. Topper Time course of glial proliferation and glial apoptosis following excitotoxic CNS injury Brain Res. 902 2001 178 189
25. M.A. Dommergues, F. Plaisant, C. Verney, and P. Gressens Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection Neuroscience 121 2003 619 628
26. S.C. Fagan, D.J. Edwards, C.V. Borlongan, L. Xu, A. Arora, G. Feuerstein, and D.C. Hess Optimal delivery of minocycline to the brain: implication for human studies of acute neuroprotection Exp. Neurol. 186 2004 248 251
27. J. Gafni, and L.M. Ellerby Calpain activation in Huntington's disease J. Neurosci. 22 2002 4842 4849
28. J. Gafni, E. Hermel, J.E. Young, C.L. Wellington, M.R. Hayden, and L.M. Ellerby Inhibition of calpain cleavage of Huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus J. Biol. Chem. 279 2004 20211 20220
29. M.C. Galas, N. Bizat, L. Cuvelier, K. Bantubungi, E. Brouillet, S.N. Schiffmann, and D. Blum Death of cortical and striatal neurons induced by mitochondrial defect involves differential molecular mechanisms Neurobiol. Dis. 15 2004 152 159
30. Y.P. Goldberg, D.W. Nicholson, D.M. Rasper, M.A. Kalchman, H.B. Koide, R.K. Graham, M. Bromm, P. Kazemi-Esfarjani, N.A. Thornberry, J.P. Vaillancourt, and M.R. Hayden Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract Nat. Genet. 13 1996 442 449
31. A. Gottlieb Safety of minocycline for acne Lancet 349 1997 374
32. 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
33. Y. He, S. Appel, and W. Le Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum Brain Res. 909 2001 187 193
34. 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
35. T. Kiechle, A. Dedeoglu, J. Kubilus, N.W. Kowall, M.F. Beal, R.M. Friedlander, S.M. Hersch, and R.J. Ferrante Cytochrome c and caspase-9 expression in Huntington's disease Neuromol. Med. 1 2002 183 195
36. S.S. Kim, P.J. Kong, B.S. Kim, D.H. Sheen, S.Y. Nam, and W. Chun Inhibitory action of minocycline on lipopolysaccharide-induced release of nitric oxide and prostaglandin E2 in BV2 microglial cells Arch. Pharm. Res. 27 2004 314 318
37. S.R. Knowles, L. Shapiro, and N.H. Shear Serious adverse reactions induced by minocycline. Report of 13 patients and review of the literature Arch. Dermatol. 132 1996 934 939
38. J. Kriz, M.D. Nguyen, and J.P. Julien Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis Neurobiol. Dis. 10 2002 268 278
39. S.M. Lee, T.Y. Yune, S.J. Kim, d.W. Park, Y.K. Lee, Y.C. Kim, Y.J. Oh, G.J. Markelonis, and T.H. Oh Minocycline reduces cell death and improves functional recovery after traumatic spinal cord injury in the rat J. Neurotrauma 20 2003 1017 1027
40. P.L. McGeer, S. Itagaki, and E.G. McGeer Expression of the histocompatibility glycoprotein HLA-DR in neurological disease Acta Neuropathol. (Berl) 76 1988 550 557
41. L. Minghetti, A. Greco, F. Cardone, M. Puopolo, A. Ladogana, S. Almonti, C. Cunningham, V.H. Perry, M. Pocchiari, and G. Levi Increased brain synthesis of prostaglandin E2 and F2-isoprostane in human and experimental transmissible spongiform encephalopathies J. Neuropathol. Exp. Neurol. 59 2000 866 871
42. V. Mittoux, S. Ouary, C. Monville, F. Lisovoski, T. Poyot, F. Conde, C. Escartin, R. Robichon, E. Brouillet, M. Peschanski, and P. Hantraye Corticostriatopallidal neuroprotection by adenovirus-mediated ciliary neurotrophic factor gene transfer in a rat model of progressive striatal degeneration J. Neurosci. 22 2002 4478 4486
43. M. Nakai, Z. Qin, Y. Wang, and T.N. Chase NMDA and non-NMDA receptor-stimulated IkappaB-alpha degradation: differential effects of the caspase-3 inhibitor DEVD.CHO, ethanol and free radical scavenger OPC-14117 Brain Res. 859 2000 207 216
44. V.O. Ona, M. Li, J.P. Vonsattel, L.J. Andrews, S.Q. Khan, W.M. Chung, A.S. Frey, A.S. Menon, X.J. Li, P.E. Stieg, J. Yuan, J.B. Penney, A.B. Young, J.H. Cha, and R.M. Friedlander Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease Nature 399 1999 263 267
45. S. Ouary, N. Bizat, S. Altairac, H. Menetrat, V. Mittoux, F. Conde, P. Hantraye, and E. Brouillet Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionic acid in rats: implications for neuroprotection studies Neuroscience 97 2000 521 530
46. A.V. Panov, C.A. Gutekunst, B.R. Leavitt, M.R. Hayden, J.R. Burke, W.J. Strittmatter, and J.T. Greenamyre Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines Nat. Neurosci. 5 2002 731 736
47. P. Popoli, A. Pintor, M.R. Domenici, C. Frank, M.T. Tebano, A. Pezzola, L. Scarchilli, D. Quarta, R. Reggio, F. Malchiodi-Albedi, M. Falchi, and M. Massotti Blockade of striatal adenosine A2A receptor reduces, through a presynaptic mechanism, quinolinic acid-induced excitotoxicity: possible relevance to neuroprotective interventions in neurodegenerative diseases of the striatum J. Neurosci. 22 2002 1967 1975
48. Z. Qin, Y. Wang, and T.N. Chasea A caspase-3-like protease is involved in NF-kappaB activation induced by stimulation of N-methyl-D-aspartate receptors in rat striatum Brain Res. Mol. Brain Res. 80 2000 111 122
49. J.K. Ryu, A. Nagai, J. Kim, M.C. Lee, J.G. McLarnon, and S.U. Kim Microglial activation and cell death induced by the mitochondrial toxin 3-nitropropionic acid: in vitro and in vivo studies Neurobiol. Dis. 12 2003 121 132
50. E. Sapp, K.B. Kegel, N. Aronin, T. Hashikawa, Y. Uchiyama, K. Tohyama, P.G. Bhide, J.P. Vonsattel, and M. DiFiglia Early and progressive accumulation of reactive microglia in the Huntington disease brain J. Neuropathol. Exp. Neurol. 60 2001 161 172
51. T.M. Scarabelli, A. Stephanou, E. Pasini, G. Gitti, P. Townsend, K. Lawrence, C. Chen-Scarabelli, L. Saravolatz, D. Latchman, R. Knight, and J. Gardin Minocycline inhibits caspase activation and reactivation, increases the ratio of XIAP to smac/DIABLO, and reduces the mitochondrial leakage of cytochrome c and smac/DIABLO J. Am. Coll. Cardiol. 43 2004 865 874
52. D.L. Smith, B. Woodman, A. Mahal, K. Sathasivam, S. Ghazi-Noori, P.A. Lowden, G.P. Bates, and E. Hockly Minocycline and doxycycline are not beneficial in a model of Huntington's disease Ann. Neurol. 54 2003 186 196
53. C. Song, Y. Zhang, C.G. Parsons, and Y.F. Liu Expression of polyglutamine-expanded huntingtin induces tyrosine phosphorylation of N-methyl-d-aspartate receptors J. Biol. Chem. 278 2003 33364 33369
54. D.P. Stirling, K. Khodarahmi, J. Liu, L.T. McPhail, C.B. McBride, J.D. Steeves, M.S. Ramer, and W. Tetzlaff Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury J. Neurosci. 24 2004 2182 2190
55. 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
56. T.S. Tang, H. Tu, E.Y. Chan, A. Maximov, Z. Wang, C.L. Wellington, M.R. Hayden, and I. Bezprozvanny Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1 Neuron 39 2003 227 239
57. 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
58. M. Thomas, T. Ashizawa, and J. Jankovic Minocycline in Huntington's disease: a pilot study Mov. Disord. 19 2004 692 695
59. T.M. Tikka, and J.E. Koistinaho Minocycline provides neuroprotection against N-methyl-d-aspartate neurotoxicity by inhibiting microglia J. Immunol. 166 2001 7527 7533
60. T.M. Tikka, N.E. Vartiainen, G. Goldsteins, S.S. Oja, P.M. Andersen, S.L. Marklund, and J. Koistinaho Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease Brain 125 2002 722 731
61. M. Tomas-Camardiel, I. Rite, A.J. Herrera, R.M. de Pablos, J. Cano, A. Machado, and J.L. Venero Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system Neurobiol. Dis. 16 2004 190 201
62. R. Topper, J. Gehrmann, M. Schwarz, F. Block, J. Noth, and G.W. Kreutzberg Remote microglial activation in the quinolinic acid model of Huntington's disease Exp. Neurol. 123 1993 271 283
63. M. Tsuji, M.A. Wilson, M.S. Lange, and M.V. Johnston Minocycline worsens hypoxic-ischemic brain injury in a neonatal mouse model Exp. Neurol. 189 2004 58 65
64. 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. Natl. Acad. Sci. U. S. A. 97 2000 8093 8097
65. J.P. Vonsattel, R.H. Myers, T.J. Stevens, R.J. Ferrante, E.D. Bird, and E.P. Richardson Jr. Neuropathological classification of Huntington's disease J. Neuropathol. Exp. Neurol. 44 1985 559 577
66. X. Wang, S. Zhu, M. Drozda, W. Zhang, I.G. Stavrovskaya, E. Cattaneo, R.J. Ferrante, B.S. Kristal, and R.M. Friedlander Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease Proc. Natl. Acad. Sci. U. S. A. 100 2003 10483 10487
67. J. Wang, Q. Wei, C.Y. Wang, W.D. Hill, D.C. Hess, and Z. Dong Minocycline up-regulates Bcl-2 and protects against cell death in the mitochondria J. Biol. Chem 279 2004 19948 19954
68. C.L. Wellington, L.M. Ellerby, B.R. Leavitt, S. Roy, D.W. Nicholson, and M.R. Hayden Huntingtin proteolysis in Huntington disease Clin. Neurosci. Res. 3 2003 129 139
69. D.C. Wu, V. Jackson-Lewis, M. Vila, K. Tieu, P. Teismann, C. Vadseth, D.K. Choi, H. Ischiropoulos, and S. Przedborski Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson disease J. Neurosci. 22 2002 1763 1771
70. L. Yang, S. Sugama, J.W. Chirichigno, J. Gregorio, S. Lorenzl, D.H. Shin, S.E. Browne, Y. Shimizu, T.H. Joh, M.F. Beal, and D.S. Albers Minocycline enhances MPTP toxicity to dopaminergic neurons J. Neurosci. Res. 74 2003 278 285
71. J. Yrjanheikki, R. Keinanen, M. Pellikka, T. Hokfelt, and J. Koistinaho Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia Proc. Natl. Acad. Sci. U. S. A. 95 1998 15769 15774
72. J. Yrjanheikki, T. Tikka, R. Keinanen, G. Goldsteins, P.H. Chan, and J. Koistinaho A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window Proc. Natl. Acad. Sci. U. S. A. 96 1999 13496 13500
73. Z.X. Yu, S.H. Li, J. Evans, A. Pillarisetti, H. Li, and X.J. Li Mutant huntingtin causes context-dependent neurodegeneration in mice with Huntington's disease J. Neurosci. 23 2003 2193 2202
74. 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
75. Y. Zhang, V.O. Ona, M. Li, M. Drozda, M. Dubois-Dauphin, S. Przedborski, R.J. Ferrante, and R.M. Friedlander Sequential activation of individual caspases, and of alterations in Bcl-2 proapoptotic signals in a mouse model of Huntington's disease J. Neurochem. 87 2003 1184 1192
76. S. Zhu, I.G. Stavrovskaya, M. Drozda, B.Y. Kim, V. Ona, M. Li, S. Sarang, A.S. Liu, D.M. Hartley, d.C. Wu, S. Gullans, R.J. Ferrante, S. Przedborski, B.S. Kristal, and R.M. Friedlander Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice Nature 417 2002 74 78
77. 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