The RRM domain of poly(A)-specific ribonuclease has a noncanonical binding site for mRNA cap analog recognition

Nucleic Acids Research

Volumn 36, Issue 14, 2008, Pages 4754-4767

  Nagata, Takashi ^a,d   Suzuki, Sakura ^a   Endo, Ryuta ^a   Shirouzu, Mikako ^a   Terada, Takaho ^a   Inoue, Makoto ^a   Kigawa, Takanori ^a,b   Kobayashi, Naohiro ^a   Güntert, Peter ^a,e   Tanaka, Akiko ^a   Hayashizaki, Yoshihide ^a   Muto, Yutaka ^a   Yokoyama, Shigeyuki ^a,c  

^a RIKEN YOKOHAMA INSTITUTE   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

7 METHYLGUANOSINE; CAPPED RNA; MESSENGER RNA; RIBONUCLEASE A; TRYPTOPHAN;

ALPHA HELIX; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN RNA BINDING; RNA RECOGNITION MOTIF; SEQUENCE ANALYSIS; SOLVENT EXTRACTION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; DINUCLEOSIDE PHOSPHATES; EXORIBONUCLEASES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RNA CAP ANALOGS; SEQUENCE ALIGNMENT;

MAMMALIA;

EID: 49249117189     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn458     Document Type: Article

References (70)

1. Isken,O. and Maquat,L.E. (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev., 21 1833-1856.
2. Maquat,L.E. and Carmichael,G.G. (2001) Quality control of mRNA function. Cell, 104, 173-176.
3. Mitchell,P. and Tollervey,D. (2001) mRNA turnover. Curr. Opin. Cell Biol., 13, 320-325.
4. Meyer,S., Temme,C. and Wahle,E. (2004) Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit. Rev. Biochem. Mol. Biol., 39, 197-216.
5. Parker,R. and Song,H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol., 11, 121-127.
6. Wilusz,C.J., Wormington,M. and Peltz,S.W. (2001) The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol., 2, 237-246.
7. von der Haar,T., Gross,J.D., Wagner,G. and McCarthy,J.E. (2004) The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat. Struct. Mol. Biol., 11, 503-511.
8. Coller,J. and Parker,R. (2004) Eukaryotic mRNA decapping. Annu. Rev. Biochem., 73, 861-890.
9. Mitchell,P. and Tollervey,D. (2000) mRNA stability in eukaryotes. Curr. Opin. Genet. Dev., 10, 193-198.
10. Åström,J., Åström,A. and Virtanen,A. (1991) In vitro deadenylation of mammalian mRNA by a HeLa cell 3′ exonuclease. EMBO J., 10, 3067-3071.
11. Åström J., Åström,A. and Virtanen,A. (1992) Properties of a HeLa cell 3′ exonuclease specific for degrading poly(A) tails of mammalian mRNA. J. Biol. Chem., 267, 18154-18159.
12. Körner,C.G., Wormington,M., Muckenthaler,M., Schneider,S., Dehlin,E. and Wahle,E. (1998) The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J., 17, 5427-5437.
13. Kömer,C.G.. and Wahle,E. (1997) Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J. Biol. Chem., 272, 10448-10456.
14. Martínez,J., Ren,Y.G., Thuresson,A.C., Hellman,U., Åström,J. and Virtanen,A. (2000) A 54-kDa fragment of the Poly(A)-specific ribonuclease is an oligomeric, processive, and cap-interacting Poly(A)-specific 3′ exonuclease. J. Biol. Chem., 275, 24222-24230.
15. Chiba,Y., Johnson,M.A., Lidder,P., Vogel,J.T., van Erp,H. and Green,P.J. (2004) AtPARN is an essential poly(A) ribonuclease in Arabídopsis. Gene, 328, 95-102.
16. Copeland,P.R. and Wormington,M. (2001) The mechanism and regulation of deadenylation: Identification and characterization of Xenopus PARN. RNA, 7, 875-886.
17. Kim,J.H. and Richter,J.D. (2006) Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell, 24 173-183.
18. Ren,Y.G., Kirsebom,L.A. and Virtanen.A. (2004) Coordination of divalent metal ions in the active site of poly(A)-specific ribonuclease. J. Biol. Chem., 279, 48702-48706.
19. Dchlin.E.. Wormington.M., Körner,C.G. and Wahle.E. (2000) Cap-dependent deadenylation of mRNA. EMBO J., 19. 1079-1086.
20. Gao,M., Fritz,D.T., Ford,L.P. and Wilusz,J. (2000) Interaction between a poly(A)-specific ribonuclease and the 5′ cap influences mRNA deadenylation rates in vitro. Mol. Cell, 5, 479-488.
21. Martínz,J., Ren,Y.G., Nilsson,P., Ehrenberg.M. and Virtanen.A. (2001) The mRNA cap structure stimulates rate of poly(A) removal and amplifies processivity of degradation. J. Biol. Chem., 276, 27923--27929.
22. Zuo,Y. and Deutscher,M.P. (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29, 1017-1026.
23. Wu,M., Reuter,M., Lilic,H., Liu,Y., Wahle,E. and Song,H. (2005) Structural insight into poly(A) binding and catalytic mechanism of human PARN. EMBO J., 24, 4082-4093.
24. Liepinsh,E., Leonchiks,A., Sharipo,A., Guignard,L. and Otting.G. (2003) Solution structure of the R3H domain from human Sμbp-2. J. Mol. Biol., 326, 217-223.
25. Okazaki,Y., Furuno,M., Kasukawa,T., Adachi,J., Bono,H., Kondo,S., Nikaido,I., Osato,N., Saito,R., Suzuki,H. et al. (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature, 420, 563-573.
26. Kigawa,T., Yabuki.T., Matsuda,N., Matsuda,T., Nakajima,R., Tanaka,A. and Yokoyama,S. (2004) Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. J. Struct. Funct. Genomics, 5, 63-68.
27. Clore,G.M. and Gronenborn,A.M. (1998) Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol., 16, 22-34.
28. Bax,A. (1994) Multidimensional nuclear magnetic resonance methods for Protein studies. Curr. Opin. Struct. Biol., 4, 738-744.
29. Cavanaph,J., Fairbrother,W.J., Palmer,A.G.J. and Skelton,N.J. (1996) Protein NMR Spectroscopy: Principles and Practice. Academic Press, San Diego, CA, USA.
30. Clowes,R.T., Crawford,A., Raine,A.R., Smith,B.O. and Laue,E.D. (1995) Improved methods for structural studies of proteins using nuclear magnetic resonance spectroscopy. Curr. Opin. Biotechnol., 6, 81-88.
31. Iwahara,J., Wojciak,J.M. and Clubb,R.T. (2001) Improved NMR spectra of a protein-DNA complex through rational mutagenesis and the application of a sensitivity optimized isotope-filtered NOESY experiment. J. Biomol. NMR, 19, 231-241.
32. Zwahlen,C., Legault,P., Vincent,S.J.F., Greenblatt,J., Konrat,R. and Kay,L.E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: Application to a bacteriophage 1 N-peptide/boxB RNA complex. J. Am. Chem. Soc., 119, 6711-6721.
33. Delaglio,F., Grzesick,S., Vuister,G.W., Zhu,G., Pfeifer,J. and Bax,A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
34. Kobayashi,N., Iwahara,L, Koshiba,S., Tomizawa,T., Tochio,N., Güntert,P., Kigawa,T. and Yokoyama,S. (2007) KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J. Biomol. NMR, 39, 31-52.
35. Johnson,B.A. and Blevins,R.A. (1994) NMRView: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 4, 603-614.
36. Güntert,P. (2004) Automated NMR structure calculation with CYANA. Meth. Mol. Biol., 278, 353-378.
37. Güntert,P., Mumenthaler,C. and Wüthrich,K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 273, 283-298.
38. Herrmann,T., Güntert,P. and Wüthrich,K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227.
39. Cornilescu,G., Delaglio,F. and Bax,A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302.
40. Powers,R., Garrett,D.S., March,C.J., Frieden,E.A., Gronenborn,A.M. and Clore,G.M. (1993) The high-resolution, three-dimensional solution structure of human interleukin-4 determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry, 32 6744-6762.
41. Güntert,P. Braun,W and Wüthrich,K. (1991) Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol., 217, 517-530.
42. Machida,M., Yokoyama,S., Matsuzawa,H.. Miyazawa,T. and Ohta,T. (1985) Allosteric effect of fructose 1,6-bisphosphate on the conformation of NAD+ as bound to L-lactate dehydrogenase from Thermus caldophilus GK24. J. Biol. Chem., 260, 16143-16147.
43. Koide,S., Yokoyama,S., Matsuzawa,H., Miyazawa,T. and Ohta,T. (1989) Conformation of NAD+ bound to allosteric L-lactate dehydrogenase activated by chemical modification. J. Biol. Chem., 264, 8676-8679.
44. Xia,B., Tsui,V., Case,D.A., Dyson,H.J. and Wright,P.E. (2002) Comparison of protein solution structures refined by molecular dynamics simulation in vacuum, with a generalized Born model, and with explicit water. J. Biomol. NMR, 22, 317-331.
45. Koradi,R., Billeter,M. and Wüthrich,K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51 -55.
46. Laskowski,R.A., Rullmann,J.A., MacArthur,M.W., Kaptein,R. and Thornton,J.M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8 477-486.
47. Goddard,T.D. and Kneller,D.G. SPARKY 3. University of California, San Francisco, 2006.
48. 5N NMR relaxation. Biochemistry, 33, 5984-6003.
49. Dreyfuss,G., Swanson,M.S. and Pinol-Roma,S. (1988) Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem. Sci., 13, 86-91.
50. Adam,S.A., Nakagawa,T., Swanson,M.S., Woodruff,T.K. and Dreyfuss,G. (1986) mRNA polyadenylate-binding protein: Gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell Biol., 6, 2932-2943.
51. Swanson,M.S., Nakagawa,T.Y., LeVan,K. and Dreyfuss,G. (1987) Primary structure of human nuclear ribonucleoprotein particle C proteins: conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and pre-rRNA-binding proteins. Mol. Cell Biol., 7 1731-1739.
52. Maris,C., Dominguez,C. and Allain,F.H. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 272, 2118-2131.
53. Nilsson,P., Henriksson,N., Niedzwiecka,A., Balatsos,N.A., Kokkoris,K., Eriksson,J. and Virtanen,A. (2007) A multifunctional RNA recognition motif (RRM) in poly(A)-specific ribonuclease (PARN) with cap and poly(A) binding properties. J. Biol. Chem., 282, 32902-32911.
54. Avis,J., Allain,F.H.-T., Howe,P. W. A., Varani,G., Neuhaus,D. and Nagai,K. (1996) Solution structure of the N-terminal RNP domain of U1A protein: The role of C-terminal residues in structure stability and RNA binding. J. Mol. Biol., 257, 398-411.
55. Allain,F.-H.T., Gubser,C. C., Howe,P. W. A., Nagai,K., Neuhaus,D. and Varani,G. (1996) Specificity of ribonucleoprotein interaction determined by RNA folding during complex formation. Nature, 380, 646-650.
56. Mittermaier,A., Kay,L.E. and Forman-Kay,J.D. (1999) Analysis of deuterium relaxation-derived methyl axis order parameters and correlation with local structure. J. Biomol. NMR, 13, 181-185.
57. Scherly,D., Kambach,C., Boelens,W., van Venrooij,W. J. and Mattaj,I. W. (1991) Conserved amino acid residues within and outside of the N-terminal ribonucleoprotein involved in U1 RNA binding. J. Mol. Biol., 219, 577-584.
58. Izaurralde,E., Lewis,J., McGuigan,C., Jankowska,M., Darzynkiewicz,E. and Mattaj,I.W. (1994) A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell, 78, 657-668.
59. Izaurralde,E., Lewis,J., Gamberi,C., Jarmolowski,A., McGuigan,C. and Mattaj,I.W. (1995) A cap-binding protein complex mediating U snRNA export. Nature, 376, 709-712.
60. 7GpppG binding to the nuclear cap-binding protein complex. Nat. Struct. Biol., 9, 912-917.
61. 7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J., 21, 5548-5557.
62. Ishida,T., Doi,M., Ueda,H., Inoue,M. and Sheldrick,G.M. (1988) Specific ring stacking interaction on the tryptophan-7-methylguanine system: comparative crystallographic studies of indole derivatives-7-methylguanine base, nucleoside nucleotide complexes. J. Am. Chem. Soc., 110, 2286-2294.
63. Allain,F.H., Howe,P.W., Neuhaus,D. and Varani,G. (1997) Structural basis of the RNA-binding specificity of human U1A protein. EMBO J., 16, 5764-5772.
64. Nagai,K., Oubridge,C., Jessen,T.H., Li,J. and Evans,P.R. (1990) Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature, 348, 515-520.
65. Handa,N., Nureki,O., Kurimoto,K., Kim,I., Sakamoto,H., Shimura,Y., Muto,Y. and Yokoyama,S. (1999) Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature, 398, 579-585.
66. Nagata,T., Kurihara,Y., Matsuda,G., Saeki,J., Kohno,T., Yanagida,Y., Ishikawa,F., Uesugi,S. and Katahira,M. (1999) Structure and interactions with RNA of the N-terminal UUAG-specific RNA-binding domain of hnRNP D0. J. Mol. Biol., 287, 221-237.
67. Nagata,T., Kanno,R., Kurihara,Y., Uesugi,S., Imai,T., Sakakibara,S., Okano,H. and Katahira,M. (1999) Structure, backbone dynamics and interactions with RNA of the C-terminal RNA-binding domain of a mouse neural RNA-binding protein, Musashi1. J. Mol. Biol., 287, 315-330.
68. Deo,R.C., Bonanno,J.B., Sonenberg,N. and Burley,S.K. (1999) Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell, 98 835-845.
69. OH 3′ termini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol. Cell, 21, 75-85.
70. Mulder,F.A., Schipper,D., Bott,R. and Boelens,R. (1999) Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292, 111-123.