Huntingtin inclusion bodies are iron-dependent centers of oxidative events

FEBS Journal

Volumn 273, Issue 23, 2006, Pages 5428-5441

  Firdaus, Wance J J ^b   Wyttenbach, Andreas ^c   Giuliano, Paola ^d   Kretz Remy, Carole ^b   Currie, R William ^b,e   Arrigo, André Patrick ^a,b  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d NATIONAL CANCER INSTITUTE   (Italy)

^e DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Hsps; Huntingtin; Inclusion bodies; Iron; ROS

Indexed keywords

DEFEROXAMINE; DICHLOROFLUORESCEIN; HUNTINGTIN; HYDROETHIDINE; IRON; IRON CHELATING AGENT; POLYGLUTAMINE; POLYPEPTIDE;

ANIMAL CELL; ARTICLE; CELL INCLUSION; CELL STRAIN; CELL STRAIN COS7; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; INCUBATION TIME; MORPHOLOGY; NONHUMAN; OXIDATION; PRIORITY JOURNAL;

EID: 33751080354     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05537.x     Document Type: Article

References (67)

1. Ambrose CM, Duyao MP, Barnes G, Bates GP, Lin CS, Srinidhi J, Baxendale S, Hummerich H, Lehrach H, Altherr M et al. (1994) Structure and expression of the Huntington's disease gene: evidence against simple inactivation due to an expanded CAG repeat. Somat Cell Mol Genet 20, 27-38.
2. Ross CA (1997) Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases? Neuron 19, 1147-1150.
3. Perutz MF (1999) Glutamine repeats and neurodegenerative diseases: molecular aspects. Trends Biochem Sci 24, 58-63.
4. Hilditch-Maguire P, Trettel F, Passani LA, Auerbach A, Persichetti F & MacDonald ME (2000) Huntingtin: an iron-regulated protein essential for normal nuclear and perinuclear organelles. Hum Mol Genet 9, 2789-2797.
5. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N & DiFiglia M (2000) Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J Neurosci 20, 7268-7278.
6. Sherman MY & Goldberg AL (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32.
7. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L & Bates GP (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548.
8. Petersen A, Mani K & Brundin P (1999) Recent advances on the pathogenesis of Huntington's disease. Exp Neurol 157, 1-18.
9. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ, Gohler H, Wanker EE, Bates GP, Housman DE & Thompson LM (2000) The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 97, 6763-6768.
10. Bates G (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361, 1642-1644.
11. Wyttenbach A, Sauvageot O, Carmichael J, Diaz-Latoud C, Arrigo A-P & Rubinsztein DC (2002) Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum Mol Genet 11, 1137-1151.
12. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, Zoghbi HY & Orr HT (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamineinduced disease in SCA1 transgenic mice. Cell 95, 41-53.
13. Saudou F, Finkbeiner S, Devys D & Greenberg ME (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95, 55-66.
14. Carmichael J, Chatellier J, Woolfson A, Milstein C, Fersht AR & Rubinsztein DC (2000) Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease. Proc Natl Acad Sci USA 97, 9701-9705.
15. Marsh JL, Walker H, Theisen H, Zhu YZ, Fielder T, Purcell J & Thompson LM (2000) Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila. Hum Mol Genet 9, 13-25.
16. Arrasate M, Mitra S, Schweitzer ES, Segal MR & Finkbeiner S (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810.
17. Kopito RR (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10, 524-530.
18. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ et al. (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36, 585-595.
19. Jana NR, Zemskov EA, Wang G & Nukina N (2001) Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10, 1049-1059.
20. Sakahira H, Breuer P, Hayer-Hartl MK & Hartl FU (2002) Molecular chaperones as modulators of polyglutamine protein aggregation and toxicity. Proc Natl Acad Sci USA 99, 16412-16418.
21. Wyttenbach A (2004) Role of heat shock proteins during polyglutamine neurodegeneration: mechanisms and hypothesis. J Mol Neurosci 23, 69-96.
22. Muchowski PJ, Schaffar G, Sittler A, Wanker EE, Hayer-Hartl MK & Hartl FU (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97, 7841-7846.
23. Wyttenbach A, Carmichael J, Swartz J, Furlong RA, Narain Y, Rankin J & Rubinsztein DC (2000) 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 USA 97, 2898-2903.
24. Muchowski PJ (2002) Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron 35, 9-12.
25. Mehlen P, Coronas V, Ljubic-Thibal V, Ducasse C, Granger L, Jourdan F & Arrigo A-P (1999) Small stress protein Hsp27 accumulation during dopamine-mediated differentiation of rat olfactory neurons counteracts apoptosis. Cell Death Differ 6, 227-233.
26. Wagstaff MJ, Collaco-Moraes Y, Smith J, de Belleroche JS, Coffin RS & Latchman DS (1999) Protection of neuronal cells from apoptosis by Hsp27 delivered with a herpes simplex virus-based vector. J Biol Chem 274, 5061-5069.
27. Halliwell B & Jenner P (1998) Impaired clearance of oxidised proteins in neurodegenerative diseases. Lancet 351, 1510-1520.
28. Pettmann B & Henderson CE (1998) Neuronal cell death. Neuron 20, 633-647.
29. Facchinetti F, Dawson VL & Dawson TM (1998) Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18, 667-682.
30. Browne SE, Ferrante RJ & Beal MF (1999) Oxidative stress in Huntington's disease. Brain Pathol 9, 147-163.
31. Bogdanov MB, Andreassen OA, Dedeoglu A, Ferrante RJ & Beal MF (2001) Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. J Neurochem 79, 1246-1249.
32. Halliwell B (2001) Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18, 685-716.
33. Tabrizi SJ, Workman J, Hart PE, Mangiarini L, Mahal A, Bates G, Cooper JM & Schapira AH (2000) Mitochondrial dysfunction and free radical damage in the Huntington R6/2 transgenic mouse. Ann Neurol 47, 80-86.
34. Giuliano P, De Cristofaro T, Affaitati A, Pizzulo GM, Feliciello A, Criscuolo C, De Michele G, Filla A, Avvedimento EV & Varrone S (2003) DNA damage induced by polyglutamine-expanded proteins. Hum Mol Genet 12, 2301-2309.
35. Sokolov S, Pozniakovsky A, Bocharova N, Knorre D & Severin F (2006) Expression of an expanded polyglutamine domain in yeast causes death with apoptotic markers. Biochim Biophys Acta 12, 12-19.
36. Firdaus WJ, Wyttenbach A, Diaz-Latoud C, Currie RW & Arrigo A-P (2006) Analysis of oxidative events induced by expanded polyglutamine huntingtin exon 1 that are differentially restored by expression of heat shock proteins or treatment with an antioxidant. FEBS J 273, 3076-3093.
37. Perluigi M, Poon HF, Maragon W, Pierce WM, Klein JB, Calabrese V, Cini C, De Marco C & Butterfield DA (2005) Proteomic analysis of protein expression and oxidative modification in R6/2 transgenic mice - a model of Huntington's disease. Mol Cell Proteomics 20, 20-30.
38. Sawa A (2001) Mechanisms for neuronal cell death and dysfunction in Huntington's disease: pathological cross-talk between the nucleus and the mitochondria? J Mol Med 79, 375-381.
39. Panov AV, Gutekunst CA, Leavitt BR, Hayden MR, Burke JR, Strittmatter WJ & Greenamyre JT (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat Neurosci 5, 731-736.
40. Panov AV, Burke JR, Strittmatter WJ & Greenamyre JT (2003) In vitro effects of polyglutamine tracts on Ca2+-dependent depolarization of rat and human mitochondria: relevance to Huntington's disease. Arch Biochem Biophys 410, 1-6.
41. Sun J & Trumpower BL (2003) Superoxide anion generation by the cytochrome bc1 complex. Arch Biochem Biophys 419, 198-206.
42. Demasi M & Davies KJ (2003) Proteasome inhibitors induce intracellular protein aggregation and cell death by an oxygen-dependent mechanism. FEBS Lett 542, 89-94.
43. Rottkamp CA, Nunomura A, Hirai K, Sayre LM, Perry G & Smith MA (2000) Will antioxidants fulfill their expectations for the treatment of Alzheimer disease? Mech Ageing Dev 116, 169-179.
44. Rottkamp CA, Nunomura A, Raina AK, Sayre LM, Perry G & Smith MA (2000) Oxidative stress, antioxidants, and Alzheimer disease. Alzheimer Dis Assoc Disord 14, S62-S66.
45. Turnbull S, Tabner BJ, El-Agnaf OM, Moore S, Davies Y & Allsop D (2001) alpha-Synuclein implicated in Parkinson's disease catalyses the formation of hydrogen peroxide in vitro. Free Radic Biol Med 30, 1163-1170.
46. Tabner BJ, Turnbull S, El-Agnaf O & Allsop D (2001) Production of reactive oxygen species from aggregating proteins implicated in Alzheimer's disease, Parkinson's disease and other neurodegenerative diseases. Curr Top Med Chem 1, 507-517.
47. Tabner BJ, Turnbull S, El-Agnaf OM & Allsop D (2002) Formation of hydrogen peroxide and hydroxyl radicals from A (beta) and alpha-synuclein as a possible mechanism of cell death in Alzheimer's disease and Parkinson's disease. Free Radic Biol Med 32, 1076-1083.
48. Turnbull S, Tabner BJ, Brown DR & Allsop D (2003) Copper-dependent generation of hydrogen peroxide from the toxic prion protein fragment PrP106-126. Neurosci Lett 336, 159-162.
49. Beal MF (1998) Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366, 211-223.
50. Muchowski PJ, Ning K, D'Souza-Schorey C & Fields S (2002) Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment. Proc Natl Acad Sci USA 99, 727-732.
51. Waelter S, Boeddrich A, Lurz R, Scherzinger E, Lueder G, Lehrach H & Wanker EE (2001) Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol Biol Cell 12, 1393-1407.
52. Preville X, Salvemini F, Giraud S, Chaufour S, Paul C, Stepien G, Ursini MV & Arrigo A-P (1999) Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp Cell Res 247, 61-78.
53. Arrigo A-P (2001) Hsp27: novel regulator of intracellular redox state. IUBMB Life 52, 303-307.
54. Arrigo A-P, Firdaus WJ, Mellier G, Moulin M, Paul C, Diaz-Latoud C & Kretz-Remy C (2005) Cytotoxic effects induced by oxidative stress in cultured mammalian cells and protection provided by Hsp27 expression. Methods 35, 126-138.
55. Arrigo AP, Virot S, Chaufour S, Firdaus W, Kretz-Remy C & Diaz-Latoud C (2005) Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 7, 414-422.
56. Chen H, Zheng C, Zhang Y, Chang YZ, Qian ZM & Shen X (2006) Heat shock protein 27 downregulates the transferrin receptor 1-mediated iron uptake. Int J Biochem Cell Biol 38, 1402-1416.
57. Sayre LM, Perry G, Atwood CS & Smith MA (2000) The role of metals in neurodegenerative diseases. Cell Mol Biol 46, 731-741.
58. Sayre LM, Smith MA & Perry G (2001) Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr Med Chem 8, 721-738.
59. Fernandes Leite J (2001) Huntington s disease: a bimolecular vision. Rev Neurol 32, 762-767.
60. Mattson MP (2004) Metal-catalyzed disruption of membrane protein and lipid signaling in the pathogenesis of neurodegenerative disorders. Ann NY Acad Sci 1012, 37-50.
61. Turnbull S, Tabner BJ, El-Agnaf OM, Twyman LJ & Allsop D (2001) New evidence that the Alzheimer betaamyloid peptide does not spontaneously form free radicals: an ESR study using a series of spin-traps. Free Radic Biol Med 30, 1154-1162.
62. Holmberg CI, Staniszewski KE, Mensah KN, Matouschek A & Morimoto RI (2004) Inefficient degradation of truncated polyglutamine proteins by the proteasome. EMBO J 23, 4307-4318.
63. Venkatraman P, Wetzel R, Tanaka M, Nukina N & Goldberg AL (2004) Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol Cell 14, 95-104.
64. Diaz-Hernandez M, Valera AG, Moran MA, Gomez-Ramos P, Alvarez-Castelao B, Castano JG, Hernandez F & Lucas JJ (2006) Inhibition of 26S proteasome activity by huntingtin filaments but not inclusion bodies isolated from mouse and human brain. J Neurochem 19, 19-25.
65. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S & Arrigo A-P (2002) Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 22, 816-834.
66. Mitsui K, Nakayama H, Akagi T, Nekooki M, Ohtawa K, Takio K, Hashikawa T & Nukina N (2002) Purification of polyglutamine aggregates and identification of elongation factor-1alpha and heat shock protein 84 as aggregate- interacting proteins. J Neurosci 22, 9267-9277.
67. Levine RL, Williams JA, Stadtman ER & Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233, 346-357.