A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins

Genes and Development

Volumn 16, Issue 19, 2002, Pages 2497-2508

  Ishizuka, Akira ^a,b   Siomi, Mikiko C ^a   Siomi, Haruhiko ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

FMR1; Fragile X syndrome; MiRNA; RNA helicase; RNAi

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; PROTEIN ARGONAUTE 2; PROTEIN SUBUNIT; RIBOSOME PROTEIN; RIBOSOME PROTEIN L11; RIBOSOME PROTEIN L5; RIBOSOME RNA; RNA; RNA 5S; RNA BINDING PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG;

ARTICLE; DROSOPHILA; GENE SILENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; SEQUENCE HOMOLOGY; TRANSLATION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; DEAD-BOX RNA HELICASES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FRAGILE X MENTAL RETARDATION PROTEIN; GENE SILENCING; HUMANS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN KINASES; RECOMBINANT FUSION PROTEINS; RIBOSOMAL PROTEINS; RNA HELICASES; RNA, RIBOSOMAL, 5S; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ARACHNIDA; HEXAPODA;

EID: 0036791671     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1022002     Document Type: Article

References (79)

1. Bernstein, E., Caudy, A.A., Hammond, S.M., and Hannon, G.J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
2. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. 1998. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17: 170-180.
3. Brown, V., Jin, P., Ceman, S., Darnell, J.C., O'Donnell, W.T., Tenenbaum, S.A., Jin, X., Feng, Y., Wilkinson, K.D., Keene, J.D., et al. 2001. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107: 477-487.
4. Catalanotto, C., Azzalin, G., Macino, G., and Cogoni, C. 2000. Gene silencing in worms and fungi. Nature 404: 245.
5. Clemens, J.C., Worby, C.A., Simonson-Leff, N., Muda, M., Maehama, T., Hemmings, B.A., and Dixon, J.E. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. 97: 6499-6503.
6. Cogoni, C. and Macino, G. 2000. Post-transcriptional gene silencing across kingdoms. Curr. Opin. Genet. Dev. 10: 638-643.
7. Dalmay, T., Horsefield, R., Braunstein, T.H., and Baulcombe, D.C. 2001. SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 20: 2069-2078.
8. Darnell, J.C., Jensen, K.B., Jin, P., Brown, V., Warren, S.T., and Darnell, R.B. 2001. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107: 489-499.
9. de la Cruz, J., Kressler, D., and Linder, P. 1999. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem. Sci. 24: 192-198.
10. Dockendorff, T.C., Su, H.S., McBride, S.M., Yang, Z., Choi, C.H., Siwicki, K.K., Sehgal, A., and Jongens, T.A. 2002. Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34: 973-984.
11. Elbashir, S.M., Lendeckel, W., and Tuschl, T. 2001. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes & Dev. 15: 188-200.
12. Fagard, M., Boutet, S., Morel, J.B., Bellini, C., and Vaucheret, H. 2000. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. 97: 11650-11654.
13. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
14. Ford, M.J., Anton, I.A., and Lane, D.P. 1988. Nuclear protein with sequence homology to translation initiation factor eIF-4A. Nature 332: 736-738.
15. Fortini, M.E. and Bonini, N.M. 2000. Modeling human neurodegenerative diseases in Drosophila: On a wing and a prayer. Trends Genet. 16: 161-167.
16. Gould, E.L., Loesch, D.Z., Martin, M.J., Hagerman, R.J., Armstrong, S.M., and Huggins, R.M. 2000. Melatonin profiles and sleep characteristics in boys with fragile X syndrome: A preliminary study. Am. J. Med. Genet. 95:307-315.
17. Greenough, W.T., Klintsova, A.Y., Irwin, S.A., Galvez, R., Bates, K.E., and Weiler, I.J. 2001. Synaptic regulation of protein synthesis and the fragile X protein. Proc. Natl. Acad. Sci. 98: 7101-7106.
18. Grishok, A., Pasquinelli, A.E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D.L., Fire, A., Ruvkun, G., and Mello, C.C. 2001. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106: 23-34.
19. Hagerman, R.J. 2002. The physical and behavioral phenotype. In Fragile X syndrome, diagnosis, treatment, and research (eds. R.J. Hagerman and P.J. Hagerma), pp. 3-109. John Hopkins University Press, Baltimore, MD.
20. Hammond, S.M., Bernstein, E., Beach, D., and Hannon, G.J. 2000. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404: 293-296.
21. Hammond, S.M., Boettcher, S., Caudy, A.A., Kobayashi, R., and Hannon, G.J. 2001. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293: 1146-1150.
22. Hannon, G.J. 2002. RNA interference. Nature 418: 244-251.
23. Harris, A.N. and Macdonald, P.M. 2001. Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
24. Huang, Y. and Liu, Z.R. 2002. The ATPase, RNA unwinding, and RNA binding activities of recombinant p68 RNA helicase. J. Biol. Chem. 277: 12810-12815.
25. Hutvagner, G. and Zamore, P.D. 2002. RNAi: Nature abhors a double-strand. Curr. Opin. Genet. Dev. 12: 225-232.
26. Hutvagner, G., McLachlan, J., Pasquinelli, A.E., Balint, E., Tuschl, T., and Zamore, P.D. 2001. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838.
27. Iggo, R.D., Jamieson, D.J., MacNeill, S.A., Southgate, J., McPheat, J., and Lane, D.P. 1991. p68 RNA helicase: Identification of a nucleolar form and cloning of related genes containing a conserved intron in yeasts. Mol. Cell. Biol. 11: 1326-1333.
28. Imbert, G., Feng, Y., Nelson, D.L., Warren, S.T., and Mandel, J.-L. 1998. FMR1 and mutations in fragile X syndrome: Molecular biology, biochemistry, and genetics. In Genetic instabilities and hereditary neurological diseases. (eds. R.D. Wells and S.T. Warrenl, pp. 27-53. Academic Press, San Diego, CA.
29. Inoue, S.B., Siomi, M.C., and Siomi, H. 2000. Molecular mechanisms of fragile X syndrome. J. Med. Invest. 47: 101-107.
30. Inoue, S.B., Shimoda, M., Nishinokubi, I., Siomi, M.C., Okamura, M., Nakamura, A., Kobayashi, S., Ishida, N., and Siomi, H. 2002. A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 12: 1331-1335.
31. Irwin, S.A., Patel, B., Idupulapati, M., Harris, J.B., Crisostomo, R.A., Larsen, B.P., Kooy, F., Willems, P.J., Cras, P., Kozlowski, P.B., et al. 2001. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: A quantitative examination. Am. J. Med. Genet. 98: 161-167.
32. Kennerdell, J.R., Yamaguchi, S., and Carthew, R.W. 2002. RNAi is activated during Drosophila oocyte maturation in a manner dependent on aubergine and spindle-E. Genes & Dev. 16: 1884-1889.
33. Ketting, R.F., Fischer, S.E., Bernstein, E., Sijen, T., Hannon, G.J., and Plasterk, R.H. 2001. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes & Dev. 15: 2654-2659.
34. Knight Jr., E. and Darnell, J.E. 1967. Distribution of 5S RNA in HeLa cells. J. Mol. Biol. 28: 491-502.
35. Lafont, F., Lecat, S., Verkade, P., and Simons, K. 1998. Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell. Biol. 142: 1413-1427.
36. Laggerbauer, B., Ostareck, D., Keidel, E.M., Ostareck-Lederer, A., and Fischer, U. 2000. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10: 329-338.
37. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294: 853-858.
38. Lane, D.P. and Hoeffler, W.K. 1980. SV40 large T shares an antigenic determinant with a cellular protein of molecular weight 68,000. Nature 288: 167-170.
39. Lau, N.C., Lim, L.P., Weinstein, E.G., and Bartel, D.P. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294: 858-862.
40. Lee, R.C. and Ambros, V. 2001. An extensive class of small RNAs in Caenorhabditis elegans. Science 294: 862-864.
41. Lee, R.C., Feinbaum, R.L., and Ambros, V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
42. Li, Z., Zhang, Y., Ku, L., Wilkinson, K.D., Warren, S.T., and Feng, Y. 2000. The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 29: 2276-2283.
43. Linder, P., Tanner, N.K., and Banroques, J. 2001. From RNA helicases to RNPases. Trends Biochem. Sci. 26: 339-341.
44. Lorsch, J.R. 2002. RNA chaperones exist and DEAD box proteins get a life. Cell 109: 797-800.
45. Miklos, G.L. and Rubin, G.M. 1996. The role of the genome project in determining gene function: Insights from model organisms. Cell 86: 521-529.
46. Moore, P.B. 1996. The structure and function of 5S ribosomal RNA. In Ribosomal RNA and structure, evolution, processing and function in protein biosynthesis (eds. R.A. Zimmermann and A.E. Dahlberg), pp. 199-236. CRC Press, Boca Raton, FL.
47. Morales, J., Hiesinger, P.R., Schroeder, A.J., Kume. K., Verstreken, P., Jackson, F.R., Nelson, D.L., and Hassan, B.A. 2002. Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34: 961-972.
48. Mourelatos, Z., Dostie, J., Paushkin, S., Sharma, A., Charroux, B., Abel, L., Rappsilber, J., Mann, M., and Dreyfuss, G. 2002. miRNPs: A novel class of ribonucleoproteins containing numerous microRNAs. Genes & Dev. 16: 720-728.
49. Nissen, P., Hansen, J., Ban, N., Moore, P.B., and Steitz, T.A. 2000. The structural basis of ribosome activity in peptide bond synthesis. Science 289: 920-930.
50. Nykanen, A., Haley, B., and Zamore, P.D. 2001. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309-321.
51. O'Donnell, W.T and Warren, S.T. 2002. A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 25: 315-338.
52. Olsen, P.H. and Ambros, V. 1999. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216: 671-680.
53. Pal-Bhadra, M., Bhadra, U., and Birchler, J.A. 2002. RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol Cell. 9: 315-327.
54. Patel, N.H. 1994. Developmental evolution: Insights from studies of insect segmentation. Science 266: 581-590.
55. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906.
56. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Seraphin, B. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17: 1030-1032.
57. Rubin, G.M., Yandell, M.D., Wortman, J.R., Gabor Miklos, G.L., Nelson, C.R., Hariharan, I.K., Fortini, M.E., Li, P.W., Apweiler, R., Fleischmann, W., et al. 2000. Comparative genomics of the eukaryotes. Science 287: 2204-2215.
58. Saxena, A., Padmanabha, R., and Glover, C.V. 1987. Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II. Mol. Cell. Biol. 7: 3409-3417.
59. Schaeffer, C., Bardoni, B., Mandel, J.-L., Ehresmann, B., Ehresmann, C., and Moine, H. 2001. The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20: 4803-4813.
60. Seggerson, K., Tang, L., and Moss, E.G. 2002. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243: 215-225.
61. Siomi, H. and Dreyfuss, G. 1997. RNA-binding proteins as regulators of gene expression. Curr. Opin. Genet. Dev. 7: 345-353.
62. Siomi, H., Siomi, M.C., Nussbaum, R.L., and Dreyfuss, G. 1993. The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74: 291-298.
63. Siomi, M.C., Zhang, Y., Siomi, H., and Dreyfuss, G. 1996. Specific sequences in the fragile X syndrome protein FMR1 and the FXR proteins mediate their binding to 60S ribosomal subunits and the interaction among them. Mol. Cell. Biol. 16: 3825-3832.
64. Steitz, J.A., Berg, C., Hendrick, J.P., La Branche-Chabot, H., Metspalu, A., Rinke, J., and Yario, T. 1988. A 5S rRNA/L5 complex is a precursor to ribosome assembly in mammalian cells. J. Cell. Biol. 106: 545-556.
65. Stevenson, R.J., Hamilton, S.J., MacCallum, D.E., Hall, P.A., and Fuller-Pace, F.V. 1998. Expression of the "dead box" RNA helicase p68 is developmentally and growth regulated and correlates with organ differentiation/maturation in the fetus. J. Pathol. 184: 351-359.
66. Szymanski, M., Barciszewska, M.Z., Barciszewski, J., and Erdmann, V.A. 2000. 5S ribosomal RNA database Y2K. Nucleic Acids Res. 28: 166-167.
67. Tabara, H., Sarkissian, M., Kelly, W.G., Fleenor, J., Grishok, A., Timmons, L., Fire, A., and Mello, C.C. 1999. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99: 123-132.
68. Tabara, H., Yigit, E., Siomi, H., and Mello, C.C. 2002. rde-4 encodes a double-stranded RNA binding protein that interacts in vivo with RDE-1, DCR-1 and a conserved DExH-box helicase to direct RNA interference in C. elegans. Cell 109: 861-871.
69. Tijsterman, M., Ketting, R.F., Okihara, K.L., Sijen, T., and Plasterk, R.H. 2002. RNA helicase MUT-14-dependent gene silencing triggered in C. elegans by short antisense RNAs. Science 295: 694-697.
70. Uchiumi, T. and Kominami, R. 1997. Binding of mammalian ribosomal protein complex P0.P1.P2 and protein L12 to the GTPase-associated domain of 28 S ribosomal RNA and effect on the accessibility to anti-28 S RNA autoantibody. J. Biol. Chem. 272: 3302-3308.
71. Vance, V. and Vaucheret, H. 2001. RNA silencing in plants: Defense and counterdefense. Science 292: 2277-2280.
72. Verheij, C., Bakker, C.E., de Graaff, E., Keulemans, J., Willemsen, R., Verkerk, A.J., Galjaard, H., Reuser, A.J., Hoogeveen, A.T., and Oostra, B.A. 1993. Characterization and localization of the FMR-1 gene product associated with fragile X syndrome. Nature 363: 722-724.
73. Wan, L., Dockendorff, T.C., Jongens, T.A., and Dreyfuss, G. 2000. Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein. Mol. Cell. Biol. 20: 8536-8547.
74. Waterhouse, P.M., Wang, M.B., and Lough, T. 2001. Gene silencing as an adaptive defence against viruses. Nature 411: 834-842.
75. Wightman, B., Ha, I., and Ruvkun, G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.
76. Williams, R.W. and Rubin, G.M. 2002. ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos. Proc. Natl. Acad. Sci. 99: 6889-6894.
77. Wu-Scharf, D., Jeong, B., Zhang, C., and Cerutti, H. 2000. Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science 290: 1159-1162.
78. Zamore, P.D., Tuschl, T., Sharp, P.A., and Bartel, D.P. 2000., RNAi: Double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101: 25-33.
79. Zhang, Y.Q., Bailey, A.M., Matthies, H.J., Renden, R.B., Smith, M.A., Speese, S.D., Rubin, G.M., and Broadie, K. 2001. Drosophila fragile X-related gene regulates the MAP1B homolog futsch to control synaptic structure and function. Cell 107: 591-603.