An improved definition of the RNA-binding specificity of SECIS-binding protein 2, an essential component of the selenocysteine incorporation machinery

Nucleic Acids Research

Volumn 35, Issue 6, 2007, Pages 1868-1884

  Clery A ^a   Bourguignon Igel, V ^a   Allmang, C ^b   Krol, A ^b   Branlant, Christiane ^a  

^a Biopôle de l Université de Lorraine   (France)

^b INST DE BIOL MOLEC ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; GUANINE; MESSENGER RNA; RNA; SELENIUM BINDING PROTEIN; SELENOCYSTEINE; SELENOPROTEIN; RNA BINDING PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SECISBP2 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SNU13 PROTEIN, S CEREVISIAE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; RNA BINDING; RNA STRUCTURE; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BINDING SITES; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SELENOCYSTEINE;

EID: 34247894065     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm066     Document Type: Article

References (63)

1. Klein,D.J., Schmeing,T.M., Moore,P.B. and Steitz,T.A. (2001) The kink-turn: A new RNA secondary structure motif. EMBO J., 20, 4214-4221.
2. Wimberly,B.T., Brodersen,D.E., Clemons,W.M.Jr, Morgan-Warren,R.J., Carter,A.P., Vonrhein,C., Hartsch,T. and Ramakrishnan,V. (2000) Structure of the 30S ribosomal subunit. Nature, 407, 327-339.
3. Schluenzen,F., Tocilj,A., Zarivach,R., Harms,J., Gluehmann,M., Janell,D., Bashan,A., Bartels,H., Agmon,I. et al. (2000) Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell, 102, 615-623.
4. Ban,N., Nissen,P., Hansen,J., Moore,P.B. and Steitz,T.A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science, 289, 905-920.
5. Vidovic,I., Nottrott,S., Hartmuth,K., Luhrmann,R. and Ficner,R. (2000) Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment. Mol. Cell, 6, 1331-1342.
6. Nottrott,S., Hartmuth,K., Fabrizio,P., Urlaub,H., Vidovic,I., Ficner,R. and Luhrmann,R. (1999) Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J. 18, 6119-6133.
7. Watkins,N.J., Segault,V., Charpentier,B., Nottrott,S., Fabrizio,P., Bachi,A., Wilm,M., Rosbash,M., Branlant,C. et al. (2000) A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell, 103, 457-466.
8. Terns,M.P. and Terns,R.M. (2002) Small nucleolar RNAs: Versatile trans-acting molecules of ancient evolutionary origin. Gene Expr., 10, 17-39.
9. Charpentier,B., Muller,S. and Branlant,C. (2005) Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res., 33, 3133-3144.
10. Omer,A.D., Ziesche,S., Ebhardt,H. and Dennis,P.P. (2002) In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proc. Natl. Acad. Sci. U.S.A., 99 5289-5294.
11. Rozhdestvensky,T.S., Tang,T.H., Tchirkova,I.V., Brosius,J., Bachellerie,J.P. and Huttenhofer,A. (2003) Binding of L7Ae protein to the K-turn of archaeal snoRNAs: A shared RNA binding motif for C/D and H/ ACA box snoRNAs in Archaea. Nucleic Acids Res., 31, 869-877.
12. Granneman,S., Pruijn,G.J., Horstman,W., van Venrooij,W.J., Luhrmann,R. and Watkins,N.J. (2002) The hU3-55K protein requires 15.5K binding to the box B/C motif as well as flanking RNA elements for its association with the U3 small nucleolar RNA in Vitro. J. Biol. Chem., 277 48490-48500.
13. Nottrott,S., Urlaub,H. and Luhrmann,R. (2002) Hierarchical, clustered protein interactions with U4/U6 snRNA: A biochemical role for U4/U6 proteins. EMBO J., 21, 5527-5538.
14. Watkins,N.J., Dickmanns,A. and Luhrmann,R. (2002) Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol., 22, 8342-8352.
15. Baker,D.L., Youssef,O.A., Chastkofsky,M.I., Dy,D.A., Terns,R.M. and Terns,M.P. (2005) RNA-guided RNA modification: Functional organization of the archaeal H/ACA RNP. Genes Dev., 19, 1238-1248.
16. Tran,E.J., Zhang,X. and Maxwell,E.S. (2003) Efficient RNA 2′-O-methylation requires juxtaposed and symmetrically assembled archaeal box C/D and C'/D' RNPs. EMBO J., 22, 3930-3940.
17. Rashid,R., Aittaleb,M., Chen,Q., Spiegel,K., Demeler,B. and Li,H. (2003) Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles. J. Mol. Biol., 333, 295-306.
18. Bortolin,M.L., Bachellerie,J.P. and Clouet-d'Orval,B. (2003) In vitro RNP assembly and methylation guide activity of an unusual box C/D RNA, cis-acting archaeal pre-tRNA(Trp). Nucleic Acids Res., 31, 6524-6535.
19. Schultz,A., Nottrott,S., Hartmuth,K. and Luhrmann,R. (2006) RNA structural requirements for the association of the spliceosomal hPrp31 protein with the U4 and U4atac small nuclear ribonucleoproteins. J. Biol. Chem., 281, 28278-28286.
20. Koonin,E.V., Bork,P. and Sander,C. (1994) A novel RNA-binding motif in omnipotent suppressors of translation termination, ribosomal proteins and a ribosome modification enzyme? Nucleic Acids Res., 22, 2166-2167.
21. Vilardell,J. and Warner,J.R. (1994) Regulation of splicing at an intermediate step in the formation of the spliceosome. Genes Dev., 8, 211-220.
22. Chao,J.A. and Williamson,J.R. (2004) Joint X-ray and NMR refinement of the yeast L30e-mRNA complex. Structure, 12, 1165-1176.
23. Mao,H., White,S.A. and Williamson,J.R. (1999) A novel loop-loop recognition motif in the yeast ribosomal protein L30 autoregulatory RNA complex. Nat. Struct. Biol., 6, 1139-1147.
24. Kuhn,J.F., Tran,E.J. and Maxwell,E.S. (2002) Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein. Nucleic Acids Res., 30, 931-941.
25. Charron,C., Manival,X., Clery,A., Senty-Segault,V., Charpentier,B., Marmier-Gourrier,N., Branlant,C. and Aubry,A. (2004) The archaeal sRNA binding protein L7Ae has a 3D structure very similar to that of its eukaryal counterpart while having a broader RNA-binding specificity. J. Mol. Biol., 342, 757-773.
26. Marmier-Gourrier,N., Clery,A., Senty-Segault,V., Charpentier,B., Schlotter,F., Leclerc,F., Fournier,R. and Branlant,C. (2003) A structural, phylogenetic, and functional study of 15.5-kD/Snu13 protein binding on U3 small nucleolar RNA. RNA, 9, 821-838.
27. Li,H. and White,S.A. (1997) RNA apatamers for yeast ribosomal protein L32 have a conserved purine-rich internal loop. RNA, 3, 245-254.
28. White,S.A., Hoeger,M., Schweppe,J.J., Shillingford,A., Shipilov,V. and Zarutskie,J. (2004) Internal loop mutations in the ribosomal protein L30 binding site of the yeast L30 RNA transcript. RNA, 10, 369-377.
29. Allmang,C., Carbon,P. and Krol,A. (2002) The SBP2 and 15.5 kD/Snu13p proteins share the same RNA binding domain: Identification of SBP2 amino acids important to SECIS RNA binding. RNA, 8, 1308-1318.
30. Fletcher,J.E., Copeland,P.R., Driscoll,D.M. and Krol,A. (2001) The selenocysteine incorporation machinery: Interactions between the SECIS RNA and the SECIS-binding protein SBP2. RNA, 7, 1442-1453.
31. Walczak,R., Carbon,P. and Krol,A. (1998) An essential non-Watson-Crick base pair motif in 3′UTR to mediate selenoprotein translation. RNA 4, 74-84.
32. Allmang,C. and Krol,A. (2006) Selenoprotein synthesis: UGA does not end the story. Biochimie, 88, 1561-1571.
33. Krol,A. (2002) Evolutionarily different RNA motifs and RNA-protein complexes to achieve selenoprotein synthesis. Biochimie, 84, 765-774.
34. Gladyshev,V.N. (2001). Selenium in biology and human health: controversies and perspectives. In Hatfield,D.L. (ed), Selenium: Its Molecular Biology and Role in Human Health. Kluwer, Boston, pp. 313-317.
35. Flohe,L., Andreesen,J.R., Brigelius-Flohe,R., Maiorino,M. and Ursini,F. (2000) Selenium, the element of the moon, in life on earth. IUBMB Life, 49, 411-420.
36. Rayman,M.P. (2000) The importance of selenium to human health. Lancet 356, 233-241.
37. Rederstorff,M., Krol,A. and Lescure,A. (2006) Understanding the importance of selenium and selenoproteins in muscle function. Cell Mol. Life Sci., 63, 52-59.
38. Martin,G.W.III, Harney,J.W. and Berry,M.J. (1998) Functionality of mutations at conserved nucleotides in eukaryotic SECIS elements is determined by the identity of a single nonconserved nucleotide. RNA 4, 65-73.
39. Tujebajeva,R.M., Copeland,P.R., Xu,X.M., Carlson,B.A., Harney,J.W., Driscoll,D.M., Hatfield,D.L. and Berry,M.J. (2000) Decoding apparatus for eukaryotic selenocysteine insertion. EMBO Rep., 1, 158-163.
40. Fagegaltier,D., Hubert,N., Yamada,K., Mizutani,T., Carbon,P. and Krol,A. (2000) Characterization of mSelB, a novel mammalian elongation factor for selenoprotein translation. EMBO J., 19, 4796-4805.
41. Zavacki,A.M., Mansell,J.B., Chung,M., Klimovitsky,B., Harney,J.W. and Berry,M.J. (2003) Coupled tRNA(Sec)-dependent assembly of the selenocysteine decoding apparatus. Mol. Cell, 11, 773-781.
42. Chavatte,L., Brown,B.A. and Driscoll,D.M. (2005) Ribosomal protein L30 is a component of the UGA-selenocysteine recoding machinery in eukaryotes. Nat. Struct. Mol. Biol., 12, 408-416.
43. Mougin,A., Gottschalk,A., Fabrizio,P., Luhrmann,R. and Branlant,C. (2002) Direct probing of RNA structure and RNA-protein interactions in purified HeLa cells and yeast spliceosomal U4/U6.U5 tri-snRNP particles. J. Mol. Biol., 317, 631-649.
44. Charron,C., Manival,X., Charpentier,B., Branlant,C. and Aubry,A. (2004) Purification, crystallization and preliminary X-ray diffraction data of L7Ae sRNP core protein from Pyrococcus abyssii. Acta Crystallogr. D Biol. Crystallogr., 60, 122-124.
45. Lescure,A., Allmang,C., Yamada,K., Carbon,P. and Krol,A. (2002) cDNA cloning, expression pattern and RNA binding analysis of human selenocysteine insertion sequence (SECIS) binding protein 2. Gene, 291, 279-285.
46. Mathews,D.H., Sabina,J., Zuker,M. and Turner,D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
47. Clery,A., Senty-Segault,V., Leclerc,F., Raue,H.A. and Branlant,C. (2007) Analysis of sequence and structural features that identify the B/C motif of U3 small nucleolar RNA as the recognition site for the Snu13p-Rrp9p protein pair. Mol. Cell. Biol., 27, 1191-1206.
48. Nolivos,S., Carpousis,A.J. and Clouet-d'Orval,B. (2005) The K-loop, a general feature of the Pyrococcus C/D guide RNAs, is an RNA structural motif related to the K-turn. Nucleic Acids Res., 33, 6507-6514.
49. Copeland,P.R. and Driscoll,D.M. (1999) Purification, redox sensitivity, and RNA binding properties of SECIS-binding protein 2, a protein involved in selenoprotein biosynthesis. J. Biol. Chem., 274, 25447-25454.
50. Matsumura,S., Ikawa,Y. and Inoue,T. (2003) Biochemical characterization of the kink-turn RNA motif. Nucleic Acids Res., 31, 5544-5551.
51. Kryukov,G.V., Castellano,S., Novoselov,S.V., Lobanov,A.V., Zehtab,O., Guigo,R. and Gladyshev,V.N. (2003) Characterization of mammalian selenoproteomes. Science, 300, 1439-1443.
52. Fagegaltier,D., Lescure,A., Walczak,R., Carbon,P. and Krol,A. (2000) Structural analysis of new local features in SECIS RNA hairpins. Nucleic Acids Res., 28, 2679-2689.
53. Lescure,A., Gautheret,D., Carbon,P. and Krol,A. (1999) Novel selenoproteins identified in silico and in vivo by using a conserved RNA structural motif. J. Biol. Chem., 274, 38147-38154.
54. Szewczak,L.B., DeGregorio,S.J., Strobel,S.A. and Steitz,J.A. (2002) Exclusive interaction of the 15.5 kD protein with the terminal box C/D motif of a methylation guide snoRNP. Chem. Biol., 9, 1095-1107.
55. Szewczak,L.B., Gabrielsen,J.S., Degregorio,S.J., Strobel,S.A. and Steitz,J.A. (2005) Molecular basis for RNA kink-turn recognition by the h15.5K small RNP protein. RNA, 11, 1407-1419.
56. Moore,T., Zhang,Y., Fenley,M.O. and Li,H. (2004) Molecular basis of box C/D RNA-protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure, 12, 807-818.
57. Razga,F., Spackova,N., Reblova,K., Koca,J., Leontis,N.B. and Sponer,J. (2004) Ribosomal RNA kink-turn motif - a flexible molecular hinge. J. Biomol. Struct. Dyn., 22, 183-194.
58. Tuerk,C. and Gold,L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science, 249, 505-510.
59. Klug,S.J. and Famulok,M. (1994) All you wanted to know about SELEX. Mol. Biol. Rep., 20, 97-107.
60. Hamma,T. and Ferre-D'Amare,A.R. (2004) Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8A resolution. Structure, 12, 893-903.
61. Wozniak,A.K., Nottrott,S., Kuhn-Holsken,E., Schroder,G.F., Grubmuller,H., Luhrmann,R., Seidel,C.A. and Oesterhelt,F. (2005) Detecting protein-induced folding of the U4 snRNA kink-turn by single-molecule multiparameter FRET measurements. RNA, 11, 1545-1554.
62. Allamand,V., Richard,P., Lescure,A., Ledeuil,C., Desjardin,D., Petit,N., Gartioux,C., Ferreiro,A., Krol,A. et al. (2006) A single homozygous point mutation in a 3′ untranslated region motif of selenoprotein N mRNA causes SEPN1-related myopathy. EMBO Rep., 7, 450-454.
63. de Jesus,L.A., Hoffmann,P.R., Michaud,T., Forry,E.P., Small-Howard,A., Stillwell,R.J., Morozova,N., Harney,J.W. and Berry,M.J. (2006) Nuclear assembly of UGA decoding complexes on selenoprotein mRNAs: A mechanism for eluding nonsense-mediated decay? Mol. Cell. Biol., 26, 1795-1805.