Beclin 1 mitigates motor and neuropathological deficits in genetic mouse models of Machado-Joseph disease

Brain

Volumn 136, Issue 7, 2013, Pages 2173-2188

  Nascimento Ferreira, Isabel ^a,b,c   Nóbrega, Clévio ^a   Vasconcelos Ferreira, Ana ^a,b   Onofre, Isabel ^a,b   Albuquerque, David ^d   Aveleira, Célia ^a   Hirai, Hirokazu ^e   Déglon, Nicole ^f   Pereira De Almeida, Luís ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

ataxin 3; autophagy; beclin 1, Machado Joseph disease, spinocerebellar ataxia type 3

Indexed keywords

BECLIN 1; POLYGLUTAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY EQUILIBRIUM; CEREBELLUM; CONTROLLED STUDY; DISEASE COURSE; EXPERIMENTAL MODEL; FEMALE; GAIT; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MACHADO JOSEPH DISEASE; MALE; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL;

EID: 84879899999     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt144     Document Type: Article

References (42)

1. Alves S, Regulier E, Nascimento-Ferreira I, Hassig R, Dufour N, Koeppen A, et al. Striatal and nigral pathology in a lentiviral rat model of Machado-Joseph disease. Hum Mol Genet 2008; 17: 2071-83
2. Bauer PO, Nukina N. The pathogenic mechanisms of polyglutamine diseases and current therapeutic strategies. J Neurochem 2009; 110: 1737-65
3. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292: 1552-5
4. Boy J, Schmidt T, Wolburg H, Mack A, Nuber S, Bottcher M, et al. Reversibility of symptoms in a conditional mouse model of spinocerebellar ataxia type 3. Hum Mol Genet 2009; 18: 4282-95
5. Can G, Ekiz HA, Baran Y. Imatinib induces autophagy through BECLIN-1 and ATG5 genes in chronic myeloid leukemia cells. Hematology 2011; 16: 95-9
6. Carlson KM, Andresen JM, Orr HT. Emerging pathogenic pathways in the spinocerebellar ataxias. Curr Opin Genet Dev 2009; 19: 247-53
7. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, et al. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 1999; 19: 3248-57
8. Chen X, Tang TS, Tu H, Nelson O, Pook M, Hammer R, et al. Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 3. J Neurosci 2008; 28: 12713-24
9. Cuervo AM. Autophagy: In sickness and in health. Trends Cell Biol 2004; 14: 70-7
10. de Almeida LP, Ross CA, Zala D, Aebischer P, Deglon N. Lentiviralmediated 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 2002; 22: 3473-83
11. de Almeida LP, Zala D, Aebischer P, Deglon N. Neuroprotective effect of a CNTF-expressing lentiviral vector in the quinolinic acid rat model of Huntington's disease. Neurobiol Dis 2001; 8: 433-46
12. Duenas AM, Goold R, Giunti P. Molecular pathogenesis of spinocerebellar ataxias. Brain 2006; 129: 1357-70
13. Goti D, Katzen SM, Mez J, Kurtis N, Kiluk J, Ben-Haiem L, et al. A mutant ataxin-3 putative-cleavage fragment in brains of Machado-Joseph disease patients and transgenic mice is cytotoxic above a critical concentration. J Neurosci 2004; 24: 10266-79
14. Huang HL, Chen YC, Huang YC, Yang KC, Pan H, Shih SP, et al. Lapatinib induces autophagy, apoptosis and megakaryocytic differentiation in chronic myelogenous leukemia K562 cells. PLoS One 2011; 6: E29014
15. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19: 5360-72
16. Jaeger PA, Pickford F, Sun CH, Lucin KM, Masliah E, Wyss-Coray T. Regulation of amyloid precursor protein processing by the Beclin 1 complex. PLoS One 2010; 5: E11102
17. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S, et al. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 1994; 8: 221-8
18. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 1998; 72: 8586-96
19. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11: 385-96
20. Nascimento-Ferreira I, Santos-Ferreira T, Sousa-Ferreira L, Auregan G, Onofre I, Alves S, et al. Overexpression of the autophagic beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease. Brain 2011; 134: 1400-15
21. Nobrega C, Nascimento-Ferreira I, Onofre I, Albuquerque D, Conceicao M, Deglon N, et al. Overexpression of mutant ataxin-3 in mouse cerebellum induces ataxia and cerebellar neuropathology. Cerebellum 2012. Advance Access published on December 15, 2012, doi: 10.1007/s12311-012-0432-0
22. Oue M, Mitsumura K, Torashima T, Koyama C, Yamaguchi H, Furuya N, et al. Characterization of mutant mice that express polyglutamine in cerebellar Purkinje cells. Brain Res 2009; 1255: 9-17
23. Paulson HL, Perez MK, Trottier Y, Trojanowski JQ, Subramony SH, Das SS, et al. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 1997; 19: 333-44
24. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 2008; 118: 2190-9
25. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112: 1809-20
26. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36: 585-95
27. Regulier E, Pereira de Almeida L, Sommer B, Aebischer P, Deglon N. Dose-Dependent neuroprotective effect of ciliary neurotrophic factor delivered via tetracycline-regulated lentiviral vectors in the quinolinic acid rat model of Huntington's disease. Hum Gene Ther 2002; 13: 1981-90
28. Rosenberg RN. Machado-Joseph disease: An autosomal dominant motor system degeneration. Mov Disord 1992; 7: 193-203
29. Schols L, Bauer P, Schmidt T, Schulte T, Riess O. Autosomal dominant cerebellar ataxias: Clinical features, genetics, and pathogenesis. Lancet Neurol 2004; 3: 291-304
30. Shibata M, Lu T, Furuya T, Degterev A, Mizushima N, Yoshimori T, et al. Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem 2006; 281: 14474-85
31. Shintani T, Klionsky DJ. Autophagy in health and disease: A doubleedged sword. Science 2004; 306: 990-5
32. Spencer B, Potkar R, Trejo M, Rockenstein E, Patrick C, Gindi R, et al. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases. J Neurosci 2009; 29: 13578-13588
33. Sudarsky L, Coutinho P. Machado-Joseph disease. Clin Neurosci 1995; 3: 17-22
34. Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q. Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 2008; 105: 19211-6
35. Torashima T, Koyama C, Iizuka A, Mitsumura K, Takayama K, Yanagi S, et al. Lentivector-mediated rescue from cerebellar ataxia in a mouse model of spinocerebellar ataxia. EMBO Rep 2008; 9: 393-9
36. Venkatraman P, Wetzel R, Tanaka M, Nukina N, Goldberg AL. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol Cell 2004; 14: 95-104
37. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010; 13: 805-11
38. Yamamoto A, Lucas JJ, Hen R. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 2000; 101: 57-66
39. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 2003; 100: 15077-82
40. Zhao Y, Xue T, Yang X, Zhu H, Ding X, Lou L, et al. Autophagy plays an important role in sunitinib-mediated cell death in H9c2 cardiac muscle cells. Toxicol Appl Pharmacol 2010; 248: 20-7
41. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 2009; 11: 468-76
42. Zu T, Duvick LA, Kaytor MD, Berlinger MS, Zoghbi HY, Clark HB, et al. Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J Neurosci 2004; 24: 8853-61 Technology