Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay

Cell

Volumn 120, Issue 2, 2005, Pages 195-208

  Kim, Yoon Ki ^a   Furic, Luc ^b   DesGroseillers, Luc ^b   Maquat, Lynne E ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; MESSENGER RNA; PROTEIN; PROTEIN STAUFEN1; PROTEIN UPF1; PROTEIN UPF2; PROTEIN UPF3X; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CODON; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; RNA DEGRADATION; RNA SPLICING; RNA STABILITY;

ANIMALIA; MAMMALIA;

EID: 12944327374     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2004.11.050     Document Type: Article

References (74)

1. Bachand F., Triki I., Autexier C. Human telomerase RNA-protein interactions. Nucleic Acids Res. 29:2001;3385-3393
2. Belanger G., Stocksley M.A., Vandromme M., Schaeffer L., Furic L., DesGroseillers L., Jasmin B.J. Localization of the RNA-binding proteins Staufen1 and Staufen2 at the mammalian neuromuscular junction. J. Neurochem. 86:2003;669-677
3. Belgrader P., Maquat L.E. Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol. Cell. Biol. 14:1994;6326-6336
4. Bono F., Ebert J., Unterholzner L., Guttler T., Izaurralde E., Conti E. Molecular insights into the interaction of PYM with the Mago-Y14 core of the exon junction complex. EMBO Rep. 5:2004;304-310
5. Broadus J., Fuerstenberg S., Doe C.Q. Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature. 391:1998;792-795
6. Chan C.C., Dostie J., Diem M.D., Feng W., Mann M., Rappsilber J., Dreyfuss G. eIF4A3 is a novel component of the exon junction complex. RNA. 10:2004;200-209
7. Chiu S.Y., Lejeune F., Ranganathan A.C., Maquat L.E. The pioneer translation initiation complex is functionally distinct from but structurally overlaps with the steady-state translation initiation complex. Genes Dev. 18:2004;745-754
8. Degot S., Le Hir H., Alpy F., Kedinger V., Stoll I., Wendling C., Seraphin B., Rio M.C., Tomasetto C. Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J. Biol. Chem. 279:2004;33702-33715
9. Donaldson J.G., Jackson C.L. Regulators and effectors of the ARF GTPases. Curr. Opin. Cell Biol. 12:2000;475-482
10. Ephrussi A., Dickinson L.K., Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 66:1991;37-50
11. Ferraiuolo M.A., Lee C.S., Ler L.W., Hsu J.L., Costa-Mattioli M., Luo M.J., Reed R., Sonenberg N. A nuclear translation-like factor eIF4AIII is recruited to the mRNA during splicing and functions in nonsense-mediated decay. Proc. Natl. Acad. Sci. USA. 101:2004;4118-4123
12. Gehring N.H., Neu-Yilik G., Schell T., Hentze M.W., Kulozik A.E. Y14 and hUpf3b form an NMD-activating complex. Mol. Cell. 11:2003;939-949
13. Goodrich J.S., Clouse K.N., Schupbach T. Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development. 131:2004;1949-1958
14. Grentzmann G., Ingram J.A., Kelly P.J., Gesteland R.F., Atkins J.F. A dual-luciferase reporter system for studying recoding signals. RNA. 4:1998;479-486
15. Hachet O., Ephrussi A. Drosophila Y14 shuttles to the posterior of the oocyte and is required for oskar mRNA transport. Curr. Biol. 11:2001;1666-1674
16. Hachet O., Ephrussi A. Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature. 428:2004;959-963
17. Hammond L.E., Rudner D.Z., Kanaar R., Rio D.C. Mutations in the hrp48 gene, which encodes a Drosophila heterogeneous nuclear ribonucleoprotein particle protein, cause lethality and developmental defects and affect P-element third-intron splicing in vivo. Mol. Cell. Biol. 17:1997;7260-7267
18. Hentze M.W., Kulozik A.E. A perfect message. RNA surveillance and nonsense-mediated decay Cell. 96:1999;307-310
19. Hillman R.T., Green R.E., Brenner S.E. An unappreciated role for RNA surveillance. Genome Biol. 5:2004;R8. Published online February 2, 2004.
20. Inoue K., Khajavi M., Ohyama T., Hirabayashi S., Wilson J., Reggin J.D., Mancias P., Butler I.J., Wilkinson M.F., Wegner M., Lupski J.R. Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat. Genet. 36:2004;361-369
21. Ishigaki Y., Li X., Serin G., Maquat L.E. Evidence for a pioneer round of mRNA translation. mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20 Cell. 106:2001;607-617
22. Iwahana H., Honda S., Tsujisawa T., Takahashi Y., Adzuma K., Katashima R., Yamaoka T., Moritani M., Yoshimoto K., Itakura M. Rat genomic structure of amidophosphoribosyltransferase, cDNA sequence of aminoimidazole ribonucleotide carboxylase, and cell cycle-dependent expression of these two physically linked genes. Biochim. Biophys. Acta. 1261:1995;369-380
23. Kanai Y., Dohmae N., Hirokawa N. Kinesin transports RNA. isolation and characterization of an RNA-transporting granule Neuron. 43:2004;513-525
24. Kataoka N., Yong J., Kim V.N., Velazquez F., Perkinson R.A., Wang F., Dreyfuss G. Pre-mRNA splicing imprints mRNA in the nucleus with a novel RNA-binding protein that persists in the cytoplasm. Mol. Cell. 6:2000;673-682
25. Kiebler M.A., Hemraj I., Verkade P., Kohrmann M., Fortes P., Marion R.M., Ortin J., Dotti C.G. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons. implications for its involvement in mRNA transport J. Neurosci. 19:1999;288-297
26. Kielkopf C.L., Burley S.K. X-ray structures of threonine aldolase complexes. structural basis of substrate recognition Biochemistry. 41:2002;11711-11720
27. Kim V.N., Kataoka N., Dreyfuss G. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science. 293:2001;1832-1836
28. Kim-Ha J., Smith J.L., Macdonald P.M. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell. 66:1991;23-35
29. Kim-Ha J., Kerr K., Macdonald P.M. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell. 81:1995;403-412
30. Kohrmann M., Luo M., Kaether C., DesGroseillers L., Dotti C.G., Kiebler M.A. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell. 10:1999;2945-2953
31. Krichevsky A.M., Kosik K.S. Neuronal RNA granules. a link between RNA localization and stimulation-dependent translation Neuron. 32:2001;683-696
32. Lau C.K., Diem M.D., Dreyfuss G., Van Duyne G.D. Structure of the Y14-Magoh core of the exon junction complex. Curr. Biol. 13:2003;933-941
33. Le S., Sternglanz R., Greider C.W. Identification of two RNA-binding proteins associated with human telomerase RNA. Mol. Biol. Cell. 11:2000;999-1010
34. Lee C.M., Haun R.S., Tsai S.C., Moss J., Vaughan M. Characterization of the human gene encoding ADP-ribosylation factor 1, a guanine nucleotide-binding activator of cholera toxin. J. Biol. Chem. 267:1992;9028-9034
35. Le Hir H., Izaurralde E., Maquat L.E., Moore M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19:2000;6860-6869. a
36. Le Hir H., Moore M.J., Maquat L.E. Pre-mRNA splicing alters mRNP composition. evidence for stable association of proteins at exon-exon junctions Genes Dev. 14:2000;1098-1108. b
37. Le Hir H., Gatfield D., Izaurralde E., Moore M.J. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20:2001;4987-4997
38. Lejeune F., Ishigaki Y., Li X., Maquat L.E. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells. dynamics of mRNP remodeling EMBO J. 21:2002;3536-3545
39. Lejeune F., Li X., Maquat L.E. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell. 12:2003;675-687
40. Lejeune F., Ranganathan A.C., Maquat L.E. eIF4G is required for the pioneer round of translation in mammalian cells. Nat. Struct. Mol. Biol. 11:2004;992-1000
41. Li P., Yang X., Wasser M., Cai Y., Chia W. Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions. Cell. 90:1997;437-447
42. Li C., Lin R.I., Lai M.C., Ouyang P., Tarn W.Y. Nuclear Pnn/DRS protein binds to spliced mRNPs and participates in mRNA processing and export via interaction with RNPS1. Mol. Cell. Biol. 23:2003;7363-7376
43. Luo M.L., Zhou Z., Magni K., Christoforides C., Rappsilber J., Mann M., Reed R. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature. 413:2001;644-647
44. Luo M., Duchaine T.F., DesGroseillers L. Molecular mapping of the determinants involved in human Staufen-ribosome association. Biochem. J. 365:2002;817-824
45. Lykke-Andersen J., Shu M.D., Steitz J.A. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell. 103:2000;1121-1131
46. Lykke-Andersen J., Shu M.D., Steitz J.A. Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science. 293:2001;1836-1839
47. Macchi P., Kroening S., Palacios I.M., Baldassa S., Grunewald B., Ambrosino C., Goetze B., Lupas A., St Johnston D., Kiebler M. Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner. J. Neurosci. 23:2003;5778-5788
48. Mallardo M., Deitinghoff A., Muller J., Goetze B., Macchi P., Peters C., Kiebler M.A. Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. USA. 100:2003;2100-2105
49. Maquat L.E. Nonsense-mediated mRNA decay. a comparative analysis of different species Curr. Genomics. 5:2004;175-190. a
50. Maquat L.E. Nonsense-mediated mRNA decay. splicing, translation and mRNP dynamics Nat. Rev. Mol. Cell Biol. 5:2004;89-99. b
51. Marion R.M., Fortes P., Beloso A., Dotti C., Ortin J. A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:1999;2212-2219
52. Matsuzaki F., Ohshiro T., Ikeshima-Kataoka H., Izumi H. miranda localizes staufen and prospero asymmetrically in mitotic neuroblasts and epithelial cells in early Drosophila embryogenesis. Development. 125:1998;4089-4098
53. Mendell J.T., Sharifi N.A., Meyers J.L., Martinez-Murillo F., Dietz H.C. Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36:2004;1073-1078
54. Micklem D.R., Adams J., Grunert S., St Johnston D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 19:2000;1366-1377
55. Mohr S.E., Dillon S.T., Boswell R.E. The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis. Genes Dev. 15:2001;2886-2899
56. Monshausen M., Putz U., Rehbein M., Schweizer M., DesGroseillers L., Kuhl D., Richter D., Kindler S. Two rat brain staufen isoforms differentially bind RNA. J. Neurochem. 76:2001;155-165
57. Monshausen M., Rehbein M., Richter D., Kindler S. The RNA-binding protein Staufen from rat brain interacts with protein phosphatase-1. J. Neurochem. 81:2002;557-564
58. Moriarty P.M., Reddy C.C., Maquat L.E. Selenium deficiency reduces the abundance of mRNA for Se-dependent glutathione peroxidase 1 by a UGA-dependent mechanism likely to be nonsense codon-mediated decay of cytoplasmic mRNA. Mol. Cell. Biol. 18:1998;2932-2939
59. Mouland A.J., Mercier J., Luo M., Bernier L., DesGroseillers L., Cohen E.A. The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1. evidence for a role in genomic RNA encapsidation J. Virol. 74:2000;5441-5451
60. Nagy E., Maquat L.E. A rule for termination-codon position within intron-containing genes. when nonsense affects RNA abundance Trends Biochem. Sci. 23:1998;198-199
61. Ohashi S., Koike K., Omori A., Ichinose S., Ohara S., Kobayashi S., Sato T.A., Anzai K. Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem. 277:2002;37804-37810
62. Ohnishi T., Yamashita A., Kashima I., Schell T., Anders K.R., Grimson A., Hachiya T., Hentze M.W., Anderson P., Ohno S. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell. 12:2003;1187-1200
63. Pal M., Ishigaki Y., Nagy E., Maquat L.E. Evidence that phosphorylation of human Upfl protein varies with intracellular location and is mediated by a wortmannin-sensitive and rapamycin-sensitive PI 3-kinase-related kinase signaling pathway. RNA. 7:2001;5-15
64. Palacios I.M., Gatfield D., St Johnston D., Izaurralde E. An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature. 427:2004;753-757
65. Schuldt A.J., Adams J.H., Davidson C.M., Micklem D.R., Haseloff J., St Johnston D., Brand A.H. Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12:1998;1847-1857
66. Shen C.P., Knoblich J.A., Chan Y.M., Jiang M.M., Jan L.Y., Jan Y.N. Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes Dev. 12:1998;1837-1846
67. Shibuya T., Tange T.O., Sonenberg N., Moore M.J. eIF4AIII binds spliced mRNA in the exon junction complex and is essential for nonsense-mediated decay. Nat. Struct. Mol. Biol. 11:2004;346-351
68. Siebel C.W., Kanaar R., Rio D.C. Regulation of tissue-specific P-element pre-mRNA splicing requires the RNA-binding protein PSI. Genes Dev. 8:1994;1713-1725
69. St Johnston D. The intracellular localization of messenger RNAs. Cell. 81:1995;161-170
70. Sun X., Perlick H.A., Dietz H.C., Maquat L.E. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc. Natl. Acad. Sci. USA. 95:1998;10009-10014
71. van Eeden F.J., Palacios I.M., Petronczki M., Weston M.J., St Johnston D. Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J. Cell Biol. 154:2001;511-523
72. Wickham L., Duchaine T., Luo M., Nabi I.R., DesGroseillers L. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:1999;2220-2230
73. Wilusz C.J., Wang W., Peltz S.W. Curbing the nonsense. the activation and regulation of mRNA surveillance Genes Dev. 15:2001;2781-2785
74. Zhang J., Sun X., Qian Y., Maquat L.E. Intron function in the nonsense-mediated decay of beta-globin mRNA. indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm RNA. 4:1998;801-815