Residues in SRP9/14 essential for elongation arrest activity of the signal recognition particle define a positively charged functional domain on one side of the protein

RNA

Volumn 16, Issue 5, 2010, Pages 969-979

  Mary, Camille ^a   Scherrer, Anne ^a   Huck, Laurent ^a,c   Lakkaraju, Asvin K K ^a,d   Thomas, Yves ^a,e   Johnson, Arthur E ^b   Strub, Katharina ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d EPFL   (Switzerland)

^e GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Alu RNA; Endoplasmic reticulum; RNA protein complexes; SRP; Translation

Indexed keywords

AMINO ACID; LYSINE; PHOSPHATE; PROTEIN; RIBOSOME RNA; SIGNAL RECOGNITION PARTICLE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MAMMAL CELL; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA TRANSLATION; RNA TRANSPORT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BASE SEQUENCE; CELL LINE; CONSERVED SEQUENCE; GENETIC COMPLEMENTATION TEST; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL RECOGNITION PARTICLE; STATIC ELECTRICITY;

EUKARYOTA; MAMMALIA;

EID: 77951199870     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2040410     Document Type: Article

References (46)

1. Andersen ES, Rosenblad MA, Larsen N, Westergaard JC, Burks J, Wower IK, Wower J, Gorodkin J, Samuelsson T, Zwieb C. 2006. The tmRDB and SRPDB resources. Nucleic Acids Res 34: D163-D168.
2. Andreazzoli M, Gerbi SA. 1991. Changes in 7SL RNA conformation during the signal recognition particle cycle. EMBO J 10: 767-777.
3. Bayer TS, Booth LN, Knudsen SM, Ellington AD. 2005. Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA 11: 1848-1857.
4. Birse DE, Kapp U, Strub K, Cusack S, Aberg A. 1997. The crystal structure of the signal recognition particle Alu RNA binding heterodimer, SRP9/14. EMBO J 16: 3757-3766.
5. Blau M, Mullapudi S, Becker T, Dudek J, Zimmermann R, Penczek PA, Beckmann R. 2005. ERj1p uses a universal ribosomal adaptor site to coordinate the 80S ribosome at the membrane. Nat Struct Mol Biol 12: 1015-1016.
6. Bovia F, Bui N, Strub K. 1994. The heterodimeric subunit SRP9/14 of the signal recognition particle functions as permuted single polypeptide chain. Nucleic Acids Res 22: 2028-2035.
7. Bovia F, Fornallaz M, Leffers H, Strub K. 1995. The SRP9/14 subunit of the signal recognition particle (SRP) is present in more than 20-fold excess over SRP in primate cells and exists primarily free but also in complex with small cytoplasmic Alu RNAs. Mol Biol Cell 6: 471-484.
8. Bovia F, Wolff N, Ryser S, Strub K. 1997. The SRP9/14 subunit of the human signal recognition particle binds to a variety of Alu-like RNAs and with higher affinity than its mouse homolog. Nucleic Acids Res 25: 318-326.
9. Brooks MA, Ravelli RB, McCarthy AA, Strub K, Cusack S. 2009. Structure of SRP14 from the Schizosaccharomyces pombe signal recognition particle. Acta Crystallogr D Biol Crystallogr 65: 421-433.
10. Bui N, Wolff N, Cusack S, Strub K. 1997. Mutational analysis of the protein subunits of the signal recognition particle Alu-domain. RNA 3: 748-763.
11. Chang DY, Sasaki-Tozawa N, Green LK, Maraia RJ. 1995. A trinucleotide repeat-associated increase in the level of Alu RNA-binding protein occurred during the same period as the major Alu amplification that accompanied anthropoid evolution. Mol Cell Biol 15: 2109-2116.
12. Chang DY, Newitt JA, Hsu K, Bernstein HD, Maraia RJ. 1997. A highly conserved nucleotide in the Alu domain of SRP RNA mediates translation arrest through high affinity binding to SRP9/14. Nucleic Acids Res 25: 1117-1122.
13. Chen Y, Varani G. 2005. Protein families and RNA recognition. FEBS J 272: 2088-2097.
14. Chevalier M, Rhee H, Elguindi EC, Blond SY. 2000. Interaction of murine BiP/GRP78 with the DnaJ homolog MTJ1. J Biol Chem 275: 19620-19627.
15. Connolly T, Gilmore R. 1986. Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein. J Cell Biol 103: 2253-2261.
16. Connolly T, Rapiejko PJ, Gilmore R. 1991. Requirement of GTP hydrolysis for dissociation of the signal recognition particle from its receptor. Science 252: 1171-1173.
17. Dudek J, Volkmer J, Bies C, Guth S, Muller A, Lerner M, Feick P, Schafer KH, Morgenstern E, Hennessy F, et al. 2002. A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. EMBO J 21: 2958-2967.
18. Gill SC, von Hippel PH. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326.
19. Gilmore R, Blobel G, Walter P. 1982. Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J Cell Biol 95: 463-469. (Pubitemid 13215861)
20. Gomez-Lorenzo MG, Spahn CM, Agrawal RK, Grassucci RA, Penczek P, Chakraburtty K, Ballesta JP, Lavandera JL, Garcia-Bustos JF, Frank J. 2000. Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 Å resolution. EMBO J 19: 2710-2718.
21. Gorlich D, Prehn S, Hartmann E, Herz J, Otto A, Kraft R, Wiedmann M, Knespel S, Dobberstein B, Rapoport TA. 1990. The signal sequence receptor has a second subunit and is part of a translocation complex in the endoplasmic reticulum as probed by bifunctional reagents. J Cell Biol 111: 2283-2294.
22. Gorodkin J, Knudsen B, Zwieb C, Samuelsson T. 2001. SRPDB (Signal Recognition Particle Database). Nucleic Acids Res 29: 169-170.
23. Halic M, Becker T, Pool MR, Spahn CM, Grassucci RA, Frank J, Beckmann R. 2004. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427: 808-814.
24. Huck L, Scherrer A, Terzi L, Johnson AE, Bernstein HD, Cusack S, Weichenrieder O, Strub K. 2004. Conserved tertiary base pairing ensures proper RNA folding and efficient assembly of the signal recognition particle Alu domain. Nucleic Acids Res 32: 4915-4924.
25. Keenan RJ, Freymann DM, Stroud RM, Walter P. 2001. The signal recognition particle. Annu Rev Biochem 70: 755-775.
26. Kroczynska B, Evangelista CM, Samant SS, Elguindi EC, Blond SY. 2004. The SANT2 domain of the murine tumor cell DnaJ-like protein 1 human homologue interacts with a1-antichymotrypsin and kinetically interferes with its serpin inhibitory activity. J Biol Chem 279: 11432-11443.
27. Lakkaraju AK, Luyet PP, Parone P, Falguieres T, Strub K. 2007. Inefficient targeting to the endoplasmic reticulum by the signal recognition particle elicits selective defects in post-ER membrane trafficking. Exp Cell Res 313: 834-847.
28. Lakkaraju AK, Mary C, Scherrer A, Johnson AE, Strub K. 2008. SRP keeps polypeptides translocation-competent by slowing translation to match limiting ER-targeting sites. Cell 133: 440-451.
29. Lustig Y, Goldshmidt H, Uliel S, Michaeli S. 2005. The Trypanosoma brucei signal recognition particle lacks the Alu-domain-binding proteins: Purification and functional analysis of its binding proteins by RNAi. J Cell Sci 118: 4551-4562.
30. Lustig Y, Wachtel C, Safro M, Liu L, Michaeli S. 2010. 'RNA walk' - a novel approach to study RNA-RNA interactions between a small RNA and its target. Nucleic Acids Res 38: e5.
31. Mason N, Ciufo LF, Brown JD. 2000. Elongation arrest is a physiologically important function of signal recognition particle. EMBO J 19: 4164-4174.
32. Meyer DI. 1985. Signal recognition particle (SRP) does not mediate a translational arrest of nascent secretory proteins in mammalian cell-free systems. EMBO J 4: 2031-2033.
33. Ogg SC, Walter P. 1995. SRP samples nascent chains for the presence of signal sequences by interacting with ribosomes at a discrete step during translation elongation. Cell 81: 1075-1084.
34. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
35. Pool MR. 2005. Signal recognition particles in chloroplasts, bacteria, yeast, and mammals. Mol Membr Biol 22: 3-15.
36. Ren YG, Wagner KW, Knee DA, Aza-Blanc P, Nasoff M, Deveraux QL. 2004. Differential regulation of the TRAIL death receptors DR4 and DR5 by the signal recognition particle. Mol Biol Cell 15: 5064-5074.
37. Rosenblad MA, Gorodkin J, Knudsen B, Zwieb C, Samuelsson T. 2003. SRPDB: Signal recognition particle database. Nucleic Acids Res 31: 363-364.
38. Rosenblad MA, Zwieb C, Samuelsson T. 2004. Identification and comparative analysis of components from the signal recognition particle in protozoa and fungi. BMC Genomics 5: 5. doi: 10.1186/1471-2164-5-5.
39. Siegel V, Walter P. 1985. Elongation arrest is not a prerequisite for secretory protein translocation across the microsomal membrane. J Cell Biol 100: 1913-1921.
40. Spahn CM, Gomez-Lorenzo MG, Grassucci RA, Jorgensen R, Andersen GR, Beckmann R, Penczek PA, Ballesta JP, Frank J. 2004. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J 23: 1008-1019.
41. Strub K, Walter P. 1990. Assembly of the Alu domain of the signal recognition particle (SRP): Dimerization of the two protein components is required for efficient binding to SRP RNA. Mol Cell Biol 10: 777-784.
42. Strub K, Fornallaz M, Bui N. 1999. The Alu domain homolog of the yeast signal recognition particle consists of an Srp14p homodimer and a yeast-specific RNA structure. RNA 5: 1333-1347.
43. Terzi L, Pool MR, Dobberstein B, Strub K. 2004. Signal recognition particle Alu domain occupies a defined site at the ribosomal subunit interface upon signal sequence recognition. Biochemistry 43: 107-117.
44. Thomas Y, Bui N, Strub K. 1997. A truncation in the 14 kDa protein of the signal recognition particle leads to tertiary structure changes in the RNA and abolishes the elongation arrest activity of the particle. Nucleic Acids Res 25: 1920-1929.
45. Walter P, Blobel G. 1981. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J Cell Biol 91: 557-561.
46. Weichenrieder O, Wild K, Strub K, Cusack S. 2000. Structure and assembly of the Alu domain of the mammalian signal recognition particle. Nature 408: 167-173.