A genomewide RNA interference screen for modifiers of aggregates formation by mutant huntingtin in drosophila

Genetics

Volumn 184, Issue 4, 2010, Pages 1165-1179

  Zhang, Sheng ^a   Binari, Richard ^b   Zhou, Rui ^a   Perrimon, Norbert ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 110; HUNTINGTIN; POLYGLUTAMINE; PROTEIN KINASE; PROTEIN TRA1; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HUNTINGTIN PROTEIN, DROSOPHILA; MICROTUBULE ASSOCIATED PROTEIN; MUTANT PROTEIN; PEPTIDE; TRA1 PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CELL LINE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DROSOPHILA; GENE ISOLATION; GENETIC ASSOCIATION; GENETIC SCREENING; IN VIVO STUDY; MUTANT; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; REGULATOR GENE; RNA INTERFERENCE; TRANSGENICS; AGE; ANIMAL; CHEMISTRY; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; GENOME; GENOMICS; HIGH THROUGHPUT SCREENING; HUMAN; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

AGE FACTORS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME, INSECT; GENOMICS; HIGH-THROUGHPUT SCREENING ASSAYS; HSP110 HEAT-SHOCK PROTEINS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MUTANT PROTEINS; MUTATION; PEPTIDES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

EID: 77955870526     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.112516     Document Type: Article

References (69)

1. ANDREW, S. E., Y. P. GOLDBERG, B. KREMER, H. TELENIUS, J. THEILMANN et al., 1993 The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat. Genet. 4: 398-403.
2. ARRASATE, M., S. MITRA, E. S. SCHWEITZER, M. R. SEGAL and S. FINKBEINER, 2004 Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431: 805-810.
3. BILEN, J., and N. M. BONINI, 2005 Drosophila as a model for human neurodegenerative disease. Annu. Rev. Genet. 39: 153-171.
4. BOUTROS, M., A. A. KIGER, S. ARMKNECHT, K. KERR, M. HILD et al., 2004 Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303: 832-835.
5. BRAND, A. H., and N. PERRIMON, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
6. BRUIJN, L. I., T. M. MILLER and D. W. CLEVELAND, 2004 Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27: 723-749.
7. BUKAU, B., J. WEISSMAN and A. HORWICH, 2006 Molecular chaperones and protein quality control. Cell 125: 443-451.
8. CAPLEN, N. J., J. FLEENOR, A. FIRE and R. A. MORGAN, 2000 dsRNA-mediated gene silencing in cultured Drosophila cells: a tissue culture model for the analysis of RNA interference. Gene 252: 95-105.
9. CAUGHEY, B., and P. T. LANSBURY, 2003 Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26: 267-298.
10. CHAN, H. Y., J. M. WARRICK, G. L. GRAY-BOARD, H. L. PAULSON and N. M. BONINI, 2000 Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum. Mol. Genet. 9: 2811-2820.
11. CHAN, H. Y., J. M. WARRICK, I. ANDRIOLA, D. MERRY and N. M. BONINI, 2002 Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila. Hum. Mol. Genet. 11: 2895-2904.
12. CHANG, H. C., S. L. NEWMYER, M. J. HULL, M. EBERSOLD, S. L. SCHMID et al., 2002 Hsc70 is required for endocytosis and clathrin function in Drosophila. J. Cell Biol. 159: 477-487.
13. CHANG, H. C., M. HULL and I. MELLMAN, 2004 The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. J. Cell Biol. 164: 1055-1064.
14. CHEN, H. K., P. FERNANDEZ-FUNEZ, S. F. ACEVEDO, Y. C. LAM, M. D. KAYTOR et al., 2003 Interaction of Akt-phosphorylated ataxin-1 with 14-3-3 mediates neurodegeneration in spinocerebellar ataxia type 1. Cell 113: 457-468.
15. CLEMENS, J. C., C. A. WORBY, N. SIMONSON-LEFF, M. MUDA, T. MAEHAMA et al., 2000 Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA 97: 6499-6503.
16. COOPER, A. A., A. D. GITLER, A. CASHIKAR, C. M. HAYNES, K. J. HILL et al., 2006 Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313: 324-328.
17. CRAIG, E. A., J. S. WEISSMAN and A. L. HORWICH, 1994 Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78: 365-372.
18. DOUMANIS, J., K. WADA, Y. KINO, A. W. MOORE and N. NUKINA, 2009 RNAi screening in Drosophila cells identifies new modifiers of mutant Huntingtin aggregation. PLoS One 4: e7275.
19. DRAGOVIC, Z., S. A. BROADLEY, Y. SHOMURA, A. BRACHER and F. U. HARTL, 2006 Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25: 2519-2528.
20. EASTON, D. P., Y. KANEKO and J. R. SUBJECK, 2000 The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5: 276-290.
21. FERNANDEZ-FUNEZ, P., M. L. NINO-ROSALES, B. DE GOUYON, W. C. SHE, J. M. LUCHAK et al., 2000 Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408: 101-106.
22. FRANCESCHINI, N., 1972 Pupil and pseudopupil in the compound eye of Drosophila, pp. 75-82 in Information Processing in the Visual Sysytem of Arthropods, edited by R. WEHNER. Springer-Verlag, Berlin.
23. FRIEDMAN, A., and N. PERRIMON, 2007 Genetic screening for signal transduction in the era of network biology. Cell 128: 225-231. (Pubitemid 46123521)
24. GARCIA-MATA, R., Z. BEBOK, E. J. SORSCHER and E. S. SZTUL, 1999 Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146: 1239-1254.
25. GATFIELD, D., L. UNTERHOLZNER, F. D. CICCARELLI, P. BORK and E. IZAURRALDE, 2003 Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 22: 3960-3970. (Pubitemid 36975722)
26. GUSELLA, J., and M. MACDONALD, 2002 No post-genetics era in human disease research. Nat. Rev. Genet. 3: 72-79.
27. HAMAMICHI, S., R. N. RIVAS, A. L. KNIGHT, S. CAO, K. A. CALDWELL et al., 2008 Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model. Proc. Natl. Acad. Sci. USA 105: 728-733.
28. HUNTINGTON'S DISEASE COLLABORATIVE RESEARCH GROUP, 1993 A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
29. ISHIHARA, K., N. YAMAGISHI, Y. SAITO, H. ADACHI, Y. KOBAYASHI et al., 2003 Hsp105alpha suppresses the aggregation of truncated androgen receptor with expanded CAG repeats and cell toxicity. J. Biol. Chem. 278: 25143-25150.
30. KANUKA, H., E. KURANAGA, T. HIRATOU, T. IGAKI, B. NELSON et al., 2003 Cytosol-endoplasmic reticulum interplay by Sec61alpha translocon in polyglutamine-mediated neurotoxicity in Drosophila. Proc. Natl. Acad. Sci. USA 100: 11723-11728.
31. KAZANTSEV, A., E. PREISINGER, A. DRANOVSKY, D. GOLDGABER and D. HOUSMAN, 1999 Insoluble detergent-resistant aggregates form between pathological and nonpathological lengths of polyglutamine in mammalian cells. Proc. Natl. Acad. Sci. USA 96: 11404-11409.
32. KAZEMI-ESFARJANI, P., and S. BENZER, 2000 Genetic suppression of polyglutamine toxicity in Drosophila. Science 287: 1837-1840.
33. KULKARNI, M. M., M. BOOKER, S. J. SILVER, A. FRIEDMAN, P. HONG et al., 2006 Evidence of off-target effects associated with long dsRNAs in Drosophila melanogaster cell-based assays. Nat. Methods 3: 833-838.
34. MA, Y., A. CREANGA, L. LUM and P. A. BEACHY, 2006 Prevalence of off-target effects in Drosophila RNA interference screens. Nature 443: 359-363.
35. st Annual Drosophila Research Conference, Pittsburgh, PA 41: 616c.
36. MARSH, J. L., and L. M. THOMPSON, 2006 Drosophila in the study of neurodegenerative disease. Neuron 52: 169-178.
37. MORIMOTO, R. I., 2008 Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22: 1427-1438.
38. NOLLEN, E. A., S. M. GARCIA, G. VAN HAAFTEN, S. KIM, A. CHAVEZ et al., 2004 Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc. Natl. Acad. Sci. USA 101: 6403-6408.
39. OH, H. J., X. CHEN and J. R. SUBJECK, 1997 Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol. Chem. 272: 31636-31640.
40. OH, H. J., D. EASTON, M. MURAWSKI, Y. KANEKO and J. R. SUBJECK, 1999 The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J. Biol. Chem. 274: 15712-15718.
41. PASINELLI, P., and R. H. BROWN, 2006 Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7: 710-723.
42. PENNEY, J. B., JR., J. P. VONSATTEL, M. E. MACDONALD, J. F. GUSELLA and R. H. MYERS, 1997 CAG repeat number governs the development rate of pathology in Huntington's disease. Ann. Neurol. 41: 689-692.
43. POLIER, S., Z. DRAGOVIC, F. U. HARTL and A. BRACHER, 2008 Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133: 1068-1079.
44. PRAHLAD, V., and R. I. MORIMOTO, 2009 Integrating the stress response: lessons for neurodegenerative diseases from C. elegans. Trends Cell Biol. 19: 52-61.
45. PRAHLAD, V., T. CORNELIUS and R. I. MORIMOTO, 2008 Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320: 811-814.
46. RAVIKUMAR, B., C. VACHER, Z. BERGER, J. E. DAVIES, S. LUO 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.
47. RAVIOL, H., H. SADLISH, F. RODRIGUEZ, M. P. MAYER and B. BUKAU, 2006 Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 25: 2510-2518. (Pubitemid 44012233)
48. ROSEN, D. R., T. SIDDIQUE, D. PATTERSON, D. A. FIGLEWICZ, P. SAPP et al., 1993 Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
49. ROSS, C. A., and M. A. POIRIER, 2005 Opinion: What is the role of protein aggregation in neurodegeneration? Nat. Rev. Mol. Cell Biol. 6: 891-898.
50. RUBIN, G. M., M. D. YANDELL, J. R. WORTMAN, G. L. GABOR MIKLOS, C. R. NELSON et al., 2000 Comparative genomics of the eukaryotes. Science 287: 2204-2215.
51. SCHERZINGER, E., R. LURZ, M. TURMAINE, L. MANGIARINI, B. HOLLENBACH et al., 1997 Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90: 549-558.
52. SCHERZINGER, E., A. SITTLER, K. SCHWEIGER, V. HEISER, R. LURZ et al., 1999 Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl. Acad. Sci. USA 96: 4604-4609.
53. SCHUERMANN, J. P., J. JIANG, J. CUELLAR, O. LLORCA, L. WANG et al., 2008 Structure of the Hsp 110:Hsc70 nucleotide exchange machine. Mol. Cell 31: 232-243.
54. SHANER, L., H. WEGELE, J. BUCHNER and K. A. MORANO, 2005 The yeast Hsp110 Sse1 functionally interacts with the Hsp70 chaperones Ssa and Ssb. J. Biol. Chem. 280: 41262-41269.
55. SHULMAN, J. M., and M. B. FEANY, 2003 Genetic modifiers of tauopathy in Drosophila. Genetics 165: 1233-1242.
56. SISODIA, S. S., 1998 Nuclear inclusions in glutamine repeat disorders: Are they pernicious, coincidental, or beneficial? Cell 95: 1-4.
57. SNELL, R. G., J. C. MACMILLAN, J. P. CHEADLE, I. FENTON, L. P. LAZAROU et al., 1993 Relationship between trinucleotide repeat expansion and phenotypic variation in Huntington's disease. Nat. Genet. 4: 393-397.
58. SPILLANTINI, M. G., M. L. SCHMIDT, V. M. LEE, J. Q. TROJANOWSKI, R. JAKES et al., 1997 Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
59. STEFFAN, J. S., L. BODAI, J. PALLOS, M. POELMAN, A. MCCAMPBELL et al., 2001 Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743.
60. STEFFAN, J. S., N. AGRAWAL, J. PALLOS, E. ROCKABRAND, L. C. TROTMAN et al., 2004 SUMO modification of Huntingtin and Huntington's disease pathology. Science 304: 100-104.
61. VALENCIA-SANCHEZ, M. A., and L. E. MAQUAT, 2004 An enemy within: fly reconnaissance deploys an endonuclease to destroy nonsense-containing mRNA. Trends Cell Biol. 14: 594-597.
62. VAN HAM, T. J., K. L. THIJSSEN, R. BREITLING, R. M. HOFSTRA, R. H. PLASTERK et al., 2008 C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. PLoS Genet. 4: e1000027.
63. WANG, J., G. W. FARR, D. H. HALL, F. LI, K. FURTAK et al., 2009a An ALS-linked mutant SOD1 produces a locomotor defect associated with aggregation and synaptic dysfunction when expressed in neurons of Caenorhabditis elegans. PLoS Genet. 5: e1000350.
64. WANG, J., G. W. FARR, C. J. ZEISS, D. J. RODRIGUEZ-GIL, J. H. WILSON et al., 2009b Progressive aggregation despite chaperone associations of a mutant SOD1-YFP in transgenic mice that develop ALS. Proc. Natl. Acad. Sci. USA 106: 1392-1397.
65. WARRICK, J. M., H. Y. CHAN, G. L. GRAY-BOARD, Y. CHAI, H. L. PAULSON et al., 1999 Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23: 425-428.
66. WESTON, C. R., and R. J. DAVIS, 2002 The JNK signal transduction pathway. Curr. Opin. Genet. Dev. 12: 14-21.
67. WHITESELL, L., and S. L. LINDQUIST, 2005 HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5: 761-772.
68. th Annual Drosophila Research Conference, San Diego, CA 46: 923B.
69. YAM, A. Y., V. ALBANESE, H. T. LIN and J. FRYDMAN, 2005 Hsp110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J. Biol. Chem. 280: 41252-41261.