dAtaxin-2 mediates expanded ataxin-1-induced neurodegeneration in a Drosophila model of SCA1

PLoS Genetics

Volumn 3, Issue 12, 2007, Pages 2551-2564

  Al Ramahi, Ismael ^a,b   Pérez, Alma M ^a   Lim, Janghoo ^a   Zhang, Minghang ^a   Sorensen, Rie ^a   De Haro, Maria ^a   Branco, Joana ^a   Pulst, Stefan M ^c,d   Zoghbi, Huda Y ^a   Botas, Juan ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; ATAXIN 2; HUNTINGTIN; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; ATAXIN-1; NERVE PROTEIN; NUCLEAR PROTEIN; SCA2 PROTEIN;

ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DNA MODIFICATION; DROSOPHILA; EYE TOXICITY; GENE DELETION; HUMAN; HUMAN CELL; MECHANORECEPTOR; NERVE DEGENERATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; DEGENERATIVE DISEASE; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DROSOPHILA; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NUCLEAR PROTEINS;

EID: 37749039120     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0030234     Document Type: Article

References (55)

1. Taroni F, DiDonato S (2004) Pathways to motor incoordination: the inherited ataxias. Nat Rev Neurosci 5: 641-655.
2. Koeppen AH (2005) The pathogenesis of spinocerebellar ataxia. Cerebellum 4: 62-73.
3. Soong BW, Paulson HL (2007) Spinocerebellar ataxias: an update. Curr Opin Neurol 20: 438-446.
4. Lim J, Hao T, Shaw C, Patel AJ, Szabo G, et al. (2006) A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 125: 801-814.
5. Orr HT, Zoghbi HY (2001) SCA1 molecular genetics: a history of a 13 year collaboration against glutamines. Hum Mol Genet 10: 2307-2311.
6. Okazawa H, Rich T, Chang A, Lin X, Waragai M, et al. (2002) Interaction between mutant ataxin-1 and PQBP-1 affects transcription and cell death. Neuron 34: 701-713.
7. Al-Ramahi I, Lam YC, Chen HK, de Gouyon B, Zhang M, et al. (2006) CHIP protects from the neurotoxicity of expanded and wild-type ataxin-1 and promotes their ubiquitination and degradation. J Biol Chem 281: 26714-26724.
8. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, et al. (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat Genet 19: 148-154.
9. Tsai CC, Kao HY, Mitzutani A, Banayo E, Rajan H, et al. (2004) Ataxin 1, a SCA1 neurodegenerative disorder protein, is functionally linked to the silencing mediator of retinoid and thyroid hormone receptors. Proc Natl Acad Sci U S A 101: 4047-4052.
10. Uchihara T, Fujigasaki H, Koyano S, Nakamura A, Yagishita S, et al. (2001) Non-expanded polyglutamine proteins in intranuclear inclusions of hereditary ataxias-triple-labeling immunofluorescence study. Acta Neuropathol (Berl) 102: 149-152.
11. Warrick JM, Morabito LM, Bilen J, Gordesky-Gold B, Faust LZ, et al. (2005) Ataxin-3 suppresses polyglutamine neurodegeneration in Drosophila by a ubiquitin-associated mechanism. Mol Cell 18: 37-48.
12. Orr HT, Zoghbi HY (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
13. Riley BE, Orr HT (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev 20: 2183-2192.
14. Duenas AM, Goold R, Giunti P (2006) Molecular pathogenesis of spinocerebellar ataxias. Brain 129: 1357-1370.
15. Gatchel JR, Zoghbi HY (2005) Diseases of unstable repeat expansion: mechanisms and common principles. Nat Rev Genet 6: 743-755.
16. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, et al. (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95: 41-53.
17. Emamian ES, Kaytor MD, Duvick LA, Zu T, Tousey SK, et al. (2003) Serine 776 of ataxin-1 is critical for polyglutamine-induced disease in SCA1 transgenic mice. Neuron 38: 375-387.
18. Tsuda H, Jafar-Nejad H, Patel AJ, Sun Y, Chen HK, et al. (2005) The AXH domain of Ataxin-1 mediates neurodegeneration through its interaction with Gfi-1/Senseless proteins. Cell 122: 633-644.
19. Mizutani A, Wang L, Rajan H, Vig PJ, Alaynick WA, et al. (2005) Boat, an AXH domain protein, suppresses the cytotoxicity of mutant ataxin-1. Embo J 24: 3339-3351.
20. Nolo R, Abbott LA, Bellen HJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102: 349-362.
21. Li SH, Li XJ (2004) Huntingtin-protein interactions and the pathogenesis of Huntington's disease. Trends Genet 20: 146-154.
22. Bilen J, Bonini NM (2005) Drosophila as a model for human neurodegenerative disease. Annu Rev Genet 39: 153-171.
23. Zoghbi HY, Botas J (2002) Mouse and fly models of neurodegeneration. Trends Genet 18: 463-471.
24. Marsh JL, Thompson LM (2006) Drosophila in the study of neurodegenerative disease. Neuron 52: 169-178.
25. Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, et al. (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408: 101-106.
26. Nonhoff U, Ralser M, Welzel F, Piccini I, Balzereit D, et al. (2007) Ataxin-2 interacts with the DEAD/H-box RNA helicase DDX6 and interferes with P-bodies and stress granules. Mol Biol Cell 18: 1385-1396.
27. He W, Parker R (2000) Functions of Lsm proteins in mRNA degradation and splicing. Curr Opin Cell Biol 12: 346-350.
28. Ralser M, Albrecht M, Nonhoff U, Lengauer T, Lehrach H, et al. (2005) An integrative approach to gain insights into the cellular function of human ataxin-2. J Mol Biol 346: 203-214.
29. Dunn CD, Jensen RE (2003) Suppression of a defect in mitochondrial protein import identifies cytosolic proteins required for viability of yeast cells lacking mitochondrial DNA. Genetics 165: 35-45.
30. Mangus DA, Amrani N, Jacobson A (1998) Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation. Mol Cell Biol 18: 7383-7396.
31. Ciosk R, DePalma M, Priess JR (2004) ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline. Development 131: 4831-4841.
32. Satterfield TF, Pallanck LJ (2006) Ataxin-2 and its Drosophila homolog, ATX2, physically assemble with polyribosomes. Hum Mol Genet 15: 2523-2532.
33. Satterfield TF, Jackson SM, Pallanck LJ (2002) A Drosophila homolog of the polyglutamine disease gene SCA2 is a dosage-sensitive regulator of actin filament formation. Genetics 162: 1687-1702.
34. Pulst SM, Nechiporuk A, Nechiporuk T, Gispert S, Chen XN, et al. (1996) Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet 14: 269-276.
35. Sanpei K, Takano H, Igarashi S, Sato T, Oyake M, et al. (1996) Identification of the spinocerebellar ataxia type 2 gene using a direct identification of repeat expansion and cloning technique, DIRECT. Nat Genet 14: 277-284.
36. Imbert G, Saudou F, Yvert G, Devys D, Trottier Y, et al. (1996) Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats. Nat Genet 14: 285-291.
37. Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, et al. (1998) Systematic gain-of-function genetics in Drosophila. Development 125: 1049-1057.
38. Ghosh S, Feany MB (2004) Comparison of pathways controlling toxicity in the eye and brain in Drosophila models of human neurodegenerative diseases. Hum Mol Genet 13: 2011-2018.
39. Shulman JM, Feany MB (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165: 1233-1242.
40. Ganetzky B, Flanagan JR (1978) On the relationship between senescence and age-related changes in two wild-type strains of Drosophila melanogaster. Exp Gerontol 13: 189-196.
41. Feany MB, Bender WW (2000) A Drosophila model of Parkinson's disease. Nature 404: 394-398.
42. Iijima K, Liu HP, Chiang AS, Hearn SA, Konsolaki M, et al. (2004) Dissecting the pathological effects of human Abeta40 and Abeta42 in Drosophila: a potential model for Alzheimer's disease. Proc Natl Acad Sci U S A 101: 6623-6628.
43. Kaltenbach LS, Romero E, Becklin RR, Chettier R, Bell R, et al. (2007) Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet 3: e82. doi:10.1371/journal.pgen.0030082
44. Huynh DP, Figueroa K, Hoang N, Pulst SM (2000) Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet 26: 44-50.
45. Huynh DP, Yang HT, Vakharia H, Nguyen D, Pulst SM (2003) Expansion of the polyQ repeat in ataxin-2 alters its Golgi localization, disrupts the Golgi complex and causes cell death. Hum Mol Genet 12: 1485-1496.
46. Kiehl TR, Nechiporuk A, Figueroa KP, Keating MT, Huynh DP, et al. (2006) Generation and characterization of Sca2 (ataxin-2) knockout mice. Biochem Biophys Res Commun 339: 17-24.
47. Koyano S, Uchihara T, Fujigasaki H, Nakamura A, Yagishita S, et al. (1999) Neuronal intranuclear inclusions in spinocerebellar ataxia type 2: triple-labeling immunofluorescent study. Neurosci Lett 273: 117-120.
48. Pang JT, Giunti P, Chamberlain S, An SF, Vitaliani R, et al. (2002) Neuronal intranuclear inclusions in SCA2: a genetic, morphological and immunohistochemical study of two cases. Brain 125: 656-663.
49. Armstrong J, Bonaventura I, Rojo A, Gonzalez G, Corral J, et al. (2005) Spinocerebellar ataxia type 2 (SCA2) with white matter involvement. Neurosci Lett 381: 247-251.
50. Li SH, Li XJ (2004) Huntingtin and its role in neuronal degeneration. Neuroscientist 10: 467-475.
51. Hackam AS, Hodgson JG, Singaraja R, Zhang T, Gan L, et al. (1999) Evidence for both the nucleus and cytoplasm as subcellular sites of pathogenesis in Huntington's disease in cell culture and in transgenic mice expressing mutant huntingtin. Philos Trans R Soc Lond B Biol Sci 354: 1047-1055.
52. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, et al. (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40: 25-40.
53. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
54. Weihe U, Milan M, Cohen SM (2001) Regulation of Apterous activity in Drosophila wing development. Development 128: 4615-4622.
55. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, et al. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437: 1173-1178.