A functional GTPase domain, but not its transmembrane domain, is required for function of the SRP receptor β-subunit

Journal of Cell Biology

Volumn 142, Issue 2, 1998, Pages 341-354

  Ogg, Stephen C ^a,b   Barz, Wolfgang P ^a,c   Walter, Peter ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Endoplasmic reticulum; GTPase; Protein targeting; Saccharomyces cerevisiae; Signal recognition particle

Indexed keywords

GUANOSINE TRIPHOSPHATASE;

AMINO ACID SUBSTITUTION; ARTICLE; BETA CHAIN; BINDING SITE; CYTOSOL; ENDOPLASMIC RETICULUM; GENE MUTATION; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; BINDING SITES; CLONING, MOLECULAR; DNA, FUNGAL; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GENES, FUNGAL; GTP PHOSPHOHYDROLASES; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PEPTIDE; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION; SIGNAL RECOGNITION PARTICLE;

EID: 0032572527     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.2.341     Document Type: Article

References (57)

1. Bacher, G., H. Lütcke, B. Jungnickel, T.A. Rapoport, and B. Dobberstein. 1996. Regulation by the ribosome of the GTPase cycle of the signal-recognition particle during protein targeting. Nature. 381:248-251.
2. Barbacid, M. 1987. ras Genes. Annu. Rev. Biochem. 56:779-827.
3. Bernstein, H.D., M.A. Poritz, K. Strub, P.J. Hoben, S. Brenner, and P. Walter. 1989. Model for signal sequence recognition from amino-acid sequence of 54k subunit of signal recognition particle. Nature. 340:482-486.
4. Bourne, H.R., D.A. Sanders, and F. McCormick. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 349:117-127.
5. Brown, J.D., B.C. Hann, K.F. Medzihradszky, M. Niwa, A.L. Burlingame, and P. Walter. 1994. Subunits of the Saccharomyces cerevisiae signal recognition particle required for its functional expression. EMBO (Eur. Mol. Biol. Organ) J. 13:4390-4400.
6. Brown, J.D., D.T.W. Ng, S.C. Ogg, and P. Walter. 1995. Targeting Pathways to the Endoplasmic Reticulum Membrane. Cold Spring Harb. Symp. Quant. Biol. 60:23-30.
7. Bult, C.J., O. White, G.J. Olsen, L. Zhou, R.D. Fleischmann, G.G. Sutton, J.A. Blake, L.M. FitzGerald, R.A. Clayton, J.D. Gocayne, et al. 1996. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 273:1058-1073.
8. Camonis, J.H., and M. Jacquet. 1988. A new RAS mutation that suppresses the CDC25 gene requirement for growth of Saccharomyces cerevisiae. Mol. Cell Biol. 8:2980-2983.
9. Christianson, T.W., R.S. Sikorski, M. Dante, J.H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene. 110:119-122.
10. Connolly, T., and R. Gilmore. 1986. Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein. J. Cell Biol. 103:2253-2261.
11. Connolly, T., and R. Gilmore. 1989. The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell. 57:599-610.
12. Davis, R.W., M. Thomas, J. Cameron, T.P. St. John, S. Scherer, and R.A. Padgett. 1980. Rapid DNA isolations for enzymatic and hybridization analysis. Methods Enzymology. 65:404-406.
13. Deshaies, R.J., and R. Schekman. 1987. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J. Cell Biol. 105:633-645.
14. Deshaies, R.J., and R. Schekman. 1990. Structural and functional dissection of Sec62p, a membrane-bound component of the yeast endoplasmic reticulum protein import machinery. Mol. Cell. Biol. 10:6024-6035.
15. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
16. Field, J., J. Nikawa, D. Broek, B. MacDonald, L. Rodgers, I.A. Wilson, R.A. Lerner, and M. Wigler. 1988. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8:2159-2165.
17. Freymann, D.M., R.J. Keenan, R.M. Stroud, and P. Walter. 1997. Structure of the conserved GTPase domain of the signal recognition particle. Nature. 385: 361-364.
18. Geitz, R.D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 74:527-534.
19. Gilmore, R., G. Blobel, and P. Walter. 1982a. 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.
20. Gilmore, R., P. Walter, and G. Blobel. 1982b. Protein translocation across the endoplasmic reticulum. II. Isolation and characterization of the signal recognition particle receptor. J. Cell Biol. 95:470-477.
21. Görlich, D., and T.A. Rapoport. 1993. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell. 75:615-630.
22. Hanein, D., K.E. Matlack, B. Jungnickel, K. Plath, K.U. Kalies, K.R. Miller, T.A. Rapoport, and C.W. Akey. 1996. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell. 87:721-732.
23. Hann, B.C., and P. Walter. 1991. The Signal Recognition Particle in S. cerevisiae. Cell. 67:131-144.
24. Higuchi, R., B. Krummel, and R.K. Saiki. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:7351-7367.
25. Hortsch, M., D. Avossa, and D.I. Meyer. 1985. A structural and functional analysis of the docking protein. J. Biol. Chem. 260:9137-9145.
26. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
27. Jonak, J., P.H. Anborgh, and A. Parmeggiani. 1994. Histidine-118 of elongation factor Tu: its role in aminoacyl-tRNA binding and regulation of the GTPase activity. FEBS Lett. 343:94-98.
28. Krieg, U.C., P. Walter, and A.E. Johnson. 1986. Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc. Natl. Acad. Sci. USA. 83:8604-8608.
29. Kunkel, T.A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA. 82:488-492.
30. Kunkel, T.A., J.D. Roberts, and R.A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods. Enzymol. 154: 367-382.
31. Kurzchalia, T.V., M. Wiedmann, A.S. Girshovich, E.S. Bochkareva, H. Bielka, and T.A. Rapoport. 1986. The signal sequence of nascent preprolactin interacts with the 54K polypeptide of the signal recognition particle. Nature. 320: 634-636.
32. Lauffer, L., P.D. Garcia, R.N. Harkins, L. Coussens, A. Ullrich, and P. Walter. 1985. Topology of the SRP receptor in the endoplasmic reticulum membrane. Nature. 318:334-338.
33. Meyer, D.I., D. Louvard, and B. Dobberstein. 1982. Characterization of molecules involved in protein translocation using a specific antibody. J. Cell Biol. 92:579-583.
34. Miller, J.D., S. Tajima, L. Lauffer, and P. Walter. 1995. The β-subunit of the signal recognition particle receptor is a transmembrane GTPase that anchors the α-subunit, a peripheral membrane GTPase, to the endoplasmic reticulum membrane. J. Cell Biol. 128:273-282.
35. Miller, J.D., H. Wilhelm, L. Gierasch, R. Gilmore, and P. Walter. 1993. GTP binding and hydrolysis by the signal recognition particle during initiation of protein translocation. Nature. 366:351-354.
36. Montoya, G., C. Svensson, J. Luirink, and I. Sinning. 1997. Crystal structure of the NG domain from the signal-recognition particle receptor FtsY. Nature. 385:365-368.
37. Ng, D.T.W., J.D. Brown, and P. Walter. 1996. Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134:269-278.
38. Ogg, S., M. Poritz, and P. Walter. 1992. The signal recognition particle receptor is important for growth and protein secretion in Saccharomyces cerevisiae. Mol. Biol. Cell. 3:895-911.
39. Powers, T., and P. Walter. 1995. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science. 269:1422-1424.
40. Pringle, J.R., R.A. Preston, A.E.M. Adams, T. Stearns, D.G. Drubin, B.K. Haarer, and E.W. Jones. 1989. Fluorescence microscopy methods for yeast. Methods Cell Biol. 31:358-435.
41. Rapiejko, P.J., and R. Gilmore. 1997. Empty site forms of the SRP54 and SR alpha GTPases mediate targeting of ribosome-nascent chain complexes to the endoplasmic reticulum. Cell. 89:703-713.
42. Rapoport, T.A., B. Jungnickel, and U. Kutay. 1996. Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65:271-303.
43. Römisch, K., J. Webb, J. Herz, S. Prehn, R. Frank, M. Vingron, and B. Dobberstein. 1989. Homology of the 54K Protein of signal recognition particle, docking protein, and two E. coli proteins with putative GTP-binding domains. Nature. 340:478-482.
44. Rose, M.D., L.M. Misra, and J.P. Vogel. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell. 57:1211-1221.
45. Rose, M.D., P. Novick, J.H. Thomas, D. Botstein, and G.R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 60:237-243.
46. Sambrook, J., E.M. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Plainview, New York. 545 pp.
47. Seluanov, A., and E. Bibi. 1997. FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J. Biol. Chem. 272:2053-2055.
48. Sherman, F., and C. Lawrence. 1974. Saccharomyces. In Handbook of Genetics. R.C. King, editor. Plenum Press, New York. 359-393.
49. Siegel, V., and P. Walter. 1988. Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP. Cell. 52:39-49.
50. Sikorski, R.S., and P. Heiter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
51. Smith, D.B., and K.S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 67:31-40.
52. Tajima, S., L. Lauffer, V.L. Rath, and P. Walter. 1986. The signal recognition particle receptor is a complex that contains two distinct polypeptide chains. J. Cell Biol. 103:1167-1178.
53. Ulbrandt, N.D., J.A. Newitt, and H.D. Bernstein. 1997. The E. coli signal recognition particle is required of the insertion of a subset of inner membrane proteins. Cell. 88:187-196.
54. Walter, P., and G. Blobel. 1980. Purification of membrane-associated protein complex required for protein translocation across the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 77:7112-7116.
55. Walter, P., and G. Blobel. 1982. Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature. 299:691-698.
56. Walter, P., and A.E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10: 87-119.
57. Zopf, D., H.D. Bernstein, A.E. Johnson, and P. Walter. 1990. The methionine-rich domain of the 54 kd protein subunit of the signal recognition particle contains an RNA binding site and can be crosslinked to a signal sequence. EMBO (Eur. Mol. Biol. Organ.) J. 9:4511-4517.