RNAi for the large non-coding hsrω transcripts suppresses polyglutamine pathogenesis in Drosophila models

RNA Biology

Volumn 6, Issue 4, 2009, Pages

  Mallik, Moushami ^a   Lakhotia, Subhash C ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

CBP; hnRNP; Huntingtin; Neurodegeneration; Non coding RNA; polyQ; SCA

Indexed keywords

DROSOPHILA PROTEIN; MESSENGER RNA; PEPTIDE; POLYGLUTAMINE; UNTRANSLATED RNA;

ALLELE; ANIMAL; ARTICLE; CELL NUCLEUS; CHEMISTRY; DEGENERATIVE DISEASE; DISEASE MODEL; DOWN REGULATION; DROSOPHILA MELANOGASTER; DRUG EFFECT; EYE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NERVOUS SYSTEM; PATHOLOGY; PROTEIN QUATERNARY STRUCTURE; RNA INTERFERENCE; TRANSGENE; ULTRASTRUCTURE;

ALLELES; ANIMALS; CELL NUCLEUS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; NERVOUS SYSTEM; NEURODEGENERATIVE DISEASES; PEPTIDES; PROTEIN STRUCTURE, QUATERNARY; RNA INTERFERENCE; RNA, MESSENGER; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC; TRANSGENES;

EID: 70349588339     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.6.4.9268     Document Type: Article

References (74)

1. Zoghbi HY, Orr HT. Glutamine repeats and neurodegeneration. Annu Rev Neurosci 2000; 23:217-247
2. Nozaki K, Onodera O, Takano H, Tsuji S. Amino acid sequences flanking polyglutamine stretches influence their potential for aggregate formation. Neuroreport 2001; 12:3357-3364 (Pubitemid 33010672)
3. La Spada AR, Taylor JP. Polyglutamines placed into context. Neuron 2003; 38:681-684
4. Masino L. Polyglutamine and neurodegeneration: structural aspects. Protein Pept Lett 2004; 11:239-248
5. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, et al. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 1998; 95:41-53. (Pubitemid 28458023)
6. Saudou F, Finkbeiner S, Devys D, Greenberg ME. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 1998; 95:55-66. (Pubitemid 28458024)
7. Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, et al. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997; 90:537-548 (Pubitemid 27347243)
8. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997; 277:1990-1993 (Pubitemid 27449140)
9. McCampbell A, Taylor JP, Taye AA, Robitschek J, Li M, Walcott J, et al. CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 2000; 9:2197-2202 (Pubitemid 30682297)
10. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL, et al. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 2001; 413:739-743 (Pubitemid 33009952)
11. Perez MK, Paulson HL, Pendse SJ, Saionz SJ, Bonini NM, Pittman RN. Recruitment and the role of nuclear localization in polyglutamine-mediated aggregation. J Cell Biol 1998; 143:1457-1470 (Pubitemid 29006496)
12. Cummings CJ, Mancini MA, Antalffy B, DeFranco DB, Orr HT, Zoghbi HY. Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat Genet 1998; 19:148-154 (Pubitemid 28248795)
13. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292:1552-1555
14. Meriin AB, Zhang X, Miliaras NB, Kazantsev A, Chernoff YO, McCaffery JM, et al. Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol Cell Biol 2003; 23:7554-7565 (Pubitemid 37271456)
15. Ganusova EE, Ozolins LN, Bhagat S, Newnam GP, Wegrzyn RD, Sherman MY, Chernoff YO. Modulation of prion formation, aggregation, and toxicity by the actin cytoskeleton in yeast. Mol Cell Biol 2006; 26:617-629 (Pubitemid 43089773)
16. Iwata A, Christianson JC, Bucci M, Ellerby LM, Nukina N, Forno LS, Kopito RR. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc Natl Acad Sci USA 2005; 102:13135-13140 (Pubitemid 41324991)
17. Fu L, Gao YS, Sztul E. Transcriptional repression and cell death induced by nuclear aggregates of non-polyglutamine protein. Neurobiol Dis 2005; 20:656-665 (Pubitemid 41619342)
18. Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, Martinez P, et al. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 2000; 408:101-106 (Pubitemid 30828268)
19. Sengupta S, Lakhotia SC. Altered expressions of the noncoding hsromega gene enhances poly-Q-induced neurotoxicity in Drosophila. RNA Biol 2006; 3:28-35. (Pubitemid 43754529)
20. Lakhotia SC, Rajendra TK, Prasanth KV. Developmental regulation and complex organization of the promoter of the non-coding hsr(omega) gene of Drosophila melanogaster. J Biosci 2001; 26:25-38.
21. Lakhotia SC. The Non-coding developmentally active and stress inducible hsromega gene of Drosophila melanogaster integrates post-transcriptional processing of other nuclear transcripts. In: Barciszewski J, Erdmann VA, eds. Noncoding RNAs: Molecular Biology and Molecular Medicine. New York: Kluwer Academic/Plenum Publishers 2003; 202-219
22. Lakhotia SC, Ray P, Rajendra TK, Prasanth KV. The non-coding transcripts of hsromega gene in Drosophila: do they regulate trafficking and availability of nuclear RNAprocessing factors? Curr Sci 1999; 77:553-563
23. Prasanth KV, Rajendra TK, Lal AK, Lakhotia SC. Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J Cell Sci 2000; 113:3485-3497
24. Jolly C, Lakhotia SC. Human sat III and Drosophila hsr omega transcripts: a common paradigm for regulation of nuclear RNA processing in stressed cells. Nucleic Acids Res 2006; 34:5508-5514 (Pubitemid 44742439)
25. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401-415 (Pubitemid 23214028)
26. Kazemi-Esfarjani P, Benzer S. Genetic suppression of polyglutamine toxicity in Drosophila. Science 2000; 287:1837-1840 (Pubitemid 30143971)
27. Warrick JM, Paulson HL, Gray-Board GL, Bui QT, Fischbeck KH, Pittman RN, Bonini NM. Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 1998; 93:939-949
28. Taylor JP, Taye AA, Campbell C, Kazemi-Esfarjani P, Fischbeck KH, Min KT. Aberrant histone acetylation, altered transcription, and retinal degeneration in a Drosophila model of polyglutamine disease are rescued by CREB-binding protein. Genes Dev 2003; 17:1463-1468 (Pubitemid 36734703)
29. McCampbell A, Taye AA, Whitty L, Penney E, Steffan JS, Fischbeck KH. Histone deacetylase inhibitors reduce polyglutamine toxicity. Proc Natl Acad Sci USA 2001; 98:15179-15184 (Pubitemid 34013989)
30. 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; 36:585-595 (Pubitemid 38715985)
31. Kim WY, Fayazi Z, Bao X, Higgins D, Kazemi-Esfarjani P. Evidence for sequestration of polyglutamine inclusions by Drosophila myeloid leukemia factor. Mol Cell Neurosci 2005; 29:536-544 (Pubitemid 40984695)
32. Iijima-Ando K, Wu P, Drier EA, Iijima K, Yin JC. cAMP-response element-binding protein and heat-shock protein 70 additively suppress polyglutamine-mediated toxicity in Drosophila. Proc Natl Acad Sci USA 2005; 102:10261-10266 (Pubitemid 41023360)
33. Anne-Laurence B, Caroline R, Irina P, Jean-Philippe L. Chromatin acetylation status in the manifestation of neurodegenerative diseases: HDAC inhibitors as therapeutic tools. Subcell Biochem 2007; 41:263-293
34. Bilen J, Liu N, Burnett BG, Pittman RN, Bonini NM. MicroRNA pathways modulate polyglutamine-induced neurodegeneration. Mol Cell 2006; 24:157-163 (Pubitemid 44466675)
35. Jackson GR, Salecker I, Dong X, Yao X, Arnheim N, Faber PW, et al. Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 1998; 21:633-642 (Pubitemid 28475514)
36. Bilen J, Bonini NM. Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 2007; 3:1950-1964 (Pubitemid 350072059)
37. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, Gordesky-Gold B, et al. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 2003; 40:25-40. (Pubitemid 37222462)
38. Lin DM, Goodman CS. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 1994; 13:507-523 (Pubitemid 24300159)
39. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 1999; 23:425-428
40. Merienne K, Helmlinger D, Perkin GR, Devys D, Trottier Y. Polyglutamine expansion induces a protein-damaging stress connecting heat shock protein 70 to the JNK pathway. J Biol Chem 2003; 278:16957-16967 (Pubitemid 36799570)
41. Qi ML, Tagawa K, Enokido Y, Yoshimura N, Wada Y, Watase K, et al. Proteome analysis of soluble nuclear proteins reveals that HMGB1/2 suppress genotoxic stress in polyglutamine diseases. Nat Cell Biol 2007; 9:402-414 (Pubitemid 46511073)
42. Marsh JL, Walker H, Theisen H, Zhu YZ, Fielder T, Purcell J, Thompson LM. Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila. Hum Mol Genet 2000; 9:13-25. (Pubitemid 30145284)
43. Kazemi-Esfarjani P, Benzer S. Suppression of polyglutamine toxicity by a Drosophila homolog of myeloid leukemia factor 1. Hum Mol Genet 2002; 11:2657-2672 (Pubitemid 35174695)
44. Chai Y, Shao J, Miller VM, Williams A, Paulson HL. Live-cell imaging reveals divergent intracellular dynamics of polyglutamine disease proteins and supports a sequestration model of pathogenesis. Proc Natl Acad Sci USA 2002; 99:9310-9315 (Pubitemid 34764610)
45. Cummings CJ, Orr HT, Zoghbi HY. Progress in pathogenesis studies of spinocerebellar ataxia type 1. Philos Trans R Soc Lond B Biol Sci 1999; 354:1079-1081 (Pubitemid 29477971)
46. Watase K, Weeber EJ, Xu B, Antalffy B, Yuva-Paylor L, Hashimoto K, et al. A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 2002; 34:905-919 (Pubitemid 34722281)
47. Johnson TK, Carrington LB, Hallas RJ, McKechnie SW. Protein synthesis rates in Drosophila associate with levels of the hsr-omega nuclear transcript. Cell Stress Chaperones 2009.
48. Steffan JS, Thompson LM. Targeting aggregation in the development of therapeutics for the treatment of Huntington's disease and other polyglutamine repeat diseases. Expert Opin Ther Targets 2003; 7:201-213
49. Wyttenbach A. Role of heat shock proteins during polyglutamine neurodegeneration: mechanisms and hypothesis. J Mol Neurosci 2004; 23:69-96. (Pubitemid 41359191)
50. Sang TK, Li C, Liu W, Rodriguez A, Abrams JM, Zipursky SL, Jackson GR. Inactivation of Drosophila Apaf-1 related killer suppresses formation of polyglutamine aggregates and blocks polyglutamine pathogenesis. Hum Mol Genet 2005; 14:357-372 (Pubitemid 40227371)
51. Chai Y, Berke SS, Cohen RE, Paulson HL. Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways. J Biol Chem 2004; 279:3605-3611 (Pubitemid 38140601)
52. Kobayashi Y, Kume A, Li M, Doyu M, Hata M, Ohtsuka K, Sobue G. Chaperones Hsp70 and Hsp40 suppress aggregate formation and apoptosis in cultured neuronal cells expressing truncated androgen receptor protein with expanded polyglutamine tract. J Biol Chem 2000; 275:8772-8778 (Pubitemid 30180231)
53. Muchowski PJ, Schaffar G, Sittler A, Wanker EE, Hayer-Hartl MK, Hartl FU. Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 2000; 97:7841-7846 (Pubitemid 30460735)
54. Orr HT, Zoghbi HY. Reversing neurodegeneration: a promise unfolds. Cell 2000; 101:1-4.
55. Sofola OA, Jin P, Qin Y, Duan R, Liu H, de Haro M, et al. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 2007; 55:565-571 (Pubitemid 47223640)
56. Sengupta S. Non-coding RNAs in polyglutamine disorders: friend or foe? J Biosci 2008; 33:303-306
57. Arya R, Mallik M, Lakhotia SC. Heat shock genes - integrating cell survival and death. J Biosci 2007; 32:595-610. (Pubitemid 46708710)
58. Ghosh S, Feany MB. Comparison of pathways controlling toxicity in the eye and brain in Drosophila models of human neurodegenerative diseases. Hum Mol Genet 2004; 13:2011-2018 (Pubitemid 39377825)
59. Mallik M, Lakhotia SC. Noncoding DNA is not "junk" but a necessity for origin and evolution of biological complexity. Proc Natl Acad Sci India 2007; 77:43-50.
60. Zaratiegui M, Irvine DV, Martienssen RA. Noncoding RNAs and gene silencing. Cell 2007; 128:763-776
61. Amaral PP, Dinger ME, Mercer TR, Mattick JS. The eukaryotic genome as an RNA machine. Science 2008; 319:1787-1789
62. Grosshans H, Filipowicz W. Molecular biology: the expanding world of small RNAs. Nature 2008; 451:414-416 (Pubitemid 351158877)
63. Mehler MF, Mattick JS. Non-coding RNAs in the nervous system. J Physiol 2006; 575:333-341
64. Presutti C, Rosati J, Vincenti S, Nasi S. Non coding RNA and brain. BMC Neurosci 2006; 7:5.
65. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ, Gohler H, et al. The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 2000; 97:6763-6768 (Pubitemid 30412788)
66. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 2001; 293:711-714 (Pubitemid 32728676)
67. Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994; 120:2121-2129 (Pubitemid 24232280)
68. Giordano E, Rendina R, Peluso I, Furia M. RNAi triggered by symmetrically transcribed transgenes in Drosophila melanogaster. Genetics 2002; 160:637-648
69. Akanksha, Mallik M, Fatima R, Lakhotia SC. The hsromega(05241) allele of the noncoding hsromega gene of Drosophila melanogaster is not responsible for male sterility as reported earlier. J Genet 2008; 87:87-90.
70. Ellis MC, O'Neill EM, Rubin GM. Expression of Drosophila glass protein and evidence for negative regulation of its activity in non-neuronal cells by another DNA-binding protein. Development 1993; 119:855-865
71. Arya R, Lakhotia SC. A simple nail polish imprint technique for examination of external morphology of Drosophila eyes. Curr Sci 2006; 90:1179-1180 (Pubitemid 43800269)
72. Quinn WG, Harris WA, Benzer S. Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 1974; 71:708-712
73. Velazquez JM, Lindquist S. hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 1984; 36:655-662
74. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: A laboratory manual. New York: Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1989.