Signal recognition particles in chloroplasts, bacteria, yeast and mammals

Molecular Membrane Biology

Volumn 22, Issue 1-2, 2005, Pages 3-15

  Pool, Martin R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

GTPase; Ribosome; Signal recognition particle; Structure function; Targeting

Indexed keywords

MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; RNA; SECY PROTEIN; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIAL MEMBRANE; BACTERIUM; CELL SECRETION; CHLOROPLAST; ENDOPLASMIC RETICULUM; EUKARYOTE; GENETIC CONSERVATION; MAMMAL; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; RNA BINDING; RNA STRUCTURE; SPECIES DIFFERENCE; YEAST;

ANIMALS; BACTERIA; CHLOROPLASTS; MAMMALS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PEPTIDE; SIGNAL RECOGNITION PARTICLE; YEASTS;

EUKARYOTA; FUNGI; MAMMALIA;

EID: 18844387083     PISSN: 09687688     EISSN: None     Source Type: Journal    
DOI: 10.1080/09687860400026348     Document Type: Review

References (106)

1. Keenan RJ, Freymann DM, Stroud RM, Walter P. The signal recognition particle. Ann Rev Biochem 2001;70: 755-775.
2. Gundelfinger ED, Krause E, Melli M, Dobberstein B. The organization of the 7SL RNA in the signal recognition particle. Nucleic Acids Res 1983;11:7363-7374.
3. Brown JD, Hann BC, Medzihradszky KF, Niwa M, Burlingame AL, Walter P. Subunits of the Saccharomyces cerevisiae signal recognition particle required for its functional expression. EMBO J 1994;13:4390-4400.
4. Van Nues RW, Brown JD. Saccharomyces SRP RNA secondary structures: A conserved S-domain and extended Alu-domain. RNA 2004;10:75-89.
5. Rosenblad MA, Zwieb C, Samuelsson T. Identification and comparative analysis of components from the signal recognition particle in protozoa and fungi. BMC Genomics 2004;5:5.
6. Ribes V, Römisch K, Giner A, Dobberstein B, Tollervey D. E. coli 4.5S RNA is part of a ribonucleoprotein particle that has properties related to signal recognition particle. Cell 1990;63:591-600.
7. Nakamura K, Yahagi S, Yamazaki T, Yamane K. Bacillus subtilis histone-like protein, HBsu, is an integral component of a SRP-like particle that can bind the Alu domain of small cytoplasmic RNA. J Biol Chem 1999;274:13569-13576.
8. Zwieb C, Eichler J. Getting on target: The archaeal signal recognition particle. Archaea 2002;1:27-34.
9. Siegel V, Walter P. Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: Analysis of biochemical mutants of SRP. Cell 1988;52:39-49.
10. Brown S, Fournier MJ. The 4.5S RNA gene of Escherichia coli is essential for cell growth. J Cell Biol 1984;178:533-550.
11. Phillips GJ, Silhavy TJ. The E. coli ffh gene is necessary for viability and efficient protein export. Nature 1992;359: 744-746.
12. Freymann DM, Keenan RJ, Stroud RN, Walter P. Structure of the conserved GTPase domain of the signal recognition particle. Nature 1997;385:361-364.
13. Zheng N, Gierasch LM. Domain interactions in E. coli SRP: Stabilization of M domain by RNA is required for effective signal sequence modulation of NG domain. Mol Cell 1999;1:79-87.
14. Kurzchalia TV, Wiedmann M, Girshovich AS, Bochkareva ES, Bielka H, Rapoport TA. The signal sequence of nascent preprolactin interacts with the 54 K polypeptide of signal recognition particle. Nature 1986;320:634-636.
15. High S, Dobberstein B. The signal sequence interacts with the methionine-rich domain of the 54-kD protein of signal recognition particle. J Cell Biol 1991;113:229-233.
16. Zopf D, Bernstein HD, Johnson AE, Walter P. 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 J 1990;9:4511-4517.
17. Keenan RJ, Freymann DM, Walter P, Stroud RM. Crystal structure of the signal sequence binding protein of the signal recognition particle. Cell 1998;94:181-191.
18. Batey RT, Rambo RP, Lucast L, Rha B, Doudna JA. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 2000;287:1232-1239.
19. Römisch K, Webb J, Lingelbach K, Gausepohl H, Dobberstein B. The 54-kD protein of signal recognition particle contains a methionine-rich RNA binding domain. J Cell Biol 1990;111:1793-1802.
20. Siegel V, Walter P. Binding sites of the 19-kDa and 68/72-kDa signal recognition particle (SRP) proteins on SRP RNA as determined by protein-RNA 'footprinting'. Proc Natl Acad Sci USA 1998;85:1801-1805.
21. Oubridge C, Kuglstatter A, Jovine L, Nagai K. Crystal structure of SRP19 in complex with the S domain of SRP RNA and its implication for the assembly of the signal recognition particle. Mol Cell 2002;9:1251-1261.
22. Hainzl T, Huang S, Sauer-Eriksson AE. Structure of the SRP19 RNA complex and implications for signal recognition particle assembly. Nature 2002;417:767-771.
23. Luirink J, High S, Wood H, Giner A, Tollervey D, Dobberstein B. Signal sequence recognition by an E. coli ribonucleoprotein particle. Nature 1992;359:741-743.
24. Walter P, Ibrahimi I, Blobel G. Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in vitro assembled polysomes synthesizing secretory protein. J Cell Biol 1981;91:545-550.
25. Flanagan JJ, Chen JC, Miao Y, Shao Y, Lin J, Bock PE, Johnson AE. SRP binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J Biol Chem 2003;278:18628-18637.
26. Ogg SC, Walter P. SRP samples nascent chains for the presence of signal sequences by interacting with the ribosome at a discrete step during translation elongation. Cell 1995;81:1075-1084.
27. Pool MR, Stumm J, Fulga TA, Sinning I, Dobberstein B. Distinct modes of signal recognition particle interaction with the ribosome. Science 2002;297:1345-1348.
28. Halic M, Becker T, Pool MR, Spann CM, Grassucci RA, Frank J, Beckmann R. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 2004;427:808-814.
29. Ullers RS, Houben ENG, Raine A, ten Hagen-Jongman CM, Ehrenberg M, Brunner J, Oudega B, Harms N, Luirink J. Interplay of SRP and Trigger Factor at L23 near the nascent chain exit site on the E. coli ribosome. J Cell Biol 2003;161:679-684.
30. Gu SQ, Peske F, Wieden HJ, Rodnina MV, Wintermeyer W. The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 2003;9:566-573.
31. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. The structural basis of ribosome activity in peptide bond synthesis. Science 2000;289:920-930.
32. Wild K, Rosendal KR, Sinning I. A structural step into the SRP cycle. Mol Microbiol 2004;53:357-363.
33. Wiedmann M, Kurzchalia TV, Bielka H, Rapoport TA. Direct probing of the interaction between the signal sequence of nascent preprolactin and the signal recognition particle by specific cross-linking. J Cell Biol 1987;104:201-208.
34. Bacher G, Lütcke H, Jungnickel B, Rapoport TA, Dobberstein B. Regulation by the ribosome of the GTPase of the signal recognition particle during protein targeting. Nature 1996;381:248-251.
35. Montoya G, Svensson C, Luirink J, Sinning I. Crystal structure of the NG domain from the signal recognition particle receptor FtsY. Nature 1997;385:365-368.
36. Young JC, Ursini J, Legate KR, Miller JD, Walter P, Andrews DW. An amino-terminal domain containing hydrophobic and hydrophilic sequences binds the signal recognition particle receptor α subunit to the β subunit on the endoplasmic reticulum membrane. J Biol Chem 1995;270:15650-15657.
37. Miller JD, Tajima S, Lauffer L, Walter P. 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 1995;128:273-282.
38. Legate K, Falcone D, Andrews D. Nucleotide-dependent binding of the GTPase domain of the signal recognition particle receptor β-subunit to the α-subunit. J Biol Chem 2000;275:27439-27446.
39. Schwartz T, Blobel G. Structural basis for the function of the beta subunit of the eukaryotic signal recognition particle receptor. Cell 2003;112:793-803.
40. Zelazny A, Seluanov A, Cooper A, Bibi E. The NG domain of the prokaryotic signal recognition particle receptor, FtsY, is fully functional when fused to an unrelated integral membrane polypeptide. Proc Natl Acad Sci USA 1997;94: 6025-6029.
41. Bibi E, Herskovits AA, Bochkareva ES, Zelazny A. Putative integral membrane SRP receptors. Trends Biochem Sci 2001;26:15-16.
42. Herskovits AA, Shimoni E, Minsky A, Bibi E. Accumulation of endoplasmic membranes and novel membrane-bound ribosome-signal recognition particle receptor complexes in Escherichia coli. J Cell Biol 2002;159:403-410.
43. Mandon EC, Jiang Y, Gilmore R. Dual recognition of the ribosome and the signal recognition particle by the SRP receptor during protein targeting to the endoplasmic reticulum. J Cell Biol 2003;162:575-585.
44. Rapiejko PJ, Gilmore R. Empty site forms of SRP54 and SRalpha GTPases mediate targeting of ribosome-nascent chain complexes to the endoplasmic reticulum. Cell 1997; 89:703-713.
45. Focia PJ, Shepotinovskaya IV, Seidler JA, Freymann DM. Heterodimeric GTPase core of the SRP targeting complex. Science 2004;303:373-377.
46. Egea PF, Shan SO, Napetschnig J, Savage DF, Walter P, Stroud RM. Substrate twinning activates the signal recognition particle and its receptor. Nature 2004;427:215-221.
47. Peluso P, Herschlag D, Nock S, Freymann D, Johnson AE, Walter P. Role of the 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor. Science 2000;288.
48. Jagath JR, Matassova NB, de Leeuw E, Warnecke JM, Lentzen G, Rodnina MV, Luirink J, Wintermeyer W Important role of the tetraloop region of 4.5S RNA in SRP binding to its receptor FtsY. RNA 2001;7:293-301.
49. Connolly T, Rapiejko PJ, Gilmore R. Requirement of GTP hydrolysis for dissociation of the signal recognition particle from its receptor. Science 1991;252:1171-1173.
50. Song W, Raden D, Mandon EC, Gilmore R. Role of Sec61α in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell 2000;100:333-343.
51. de Leeuw E, te Kaat K, Moser C, Menestrina G, Demel R, de Kruijff B, Oudega B, Luirink J, Sinning I. Anionic phospholipds are involved in membrane association of FtsY and stimulate its GTPase activity. EMBO J 2000;19:531-541.
52. Eitan A, Bibi E. The core Escherichia coli signal recognition particle receptor contains only the N and G domains of FtsY. J Bacteriol 2004;186:2492-2494.
53. Lu Y, Hai-Yuan Q, Hyndman JB, Ulbrandt ND, Teplyakov A, Tomasevic N, Bernstein HD. Evidence for a novel GTPase priming step in the SRP protein targeting patchway. EMBO J 2001;20:6724-6734.
54. Lütcke H, High S, Römisch K, Ashford AJ, Dobberstein B. The methionine-rich domain of the 54 kDa subunit of signal recognition particle is sufficient for the interaction with signal sequences. EMBO J 1992;11:1543-1551.
55. Powers T, Walter P. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 1995;269:1422-1424.
56. Shan SO, Stroud RM, Walter P. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol 2004;2:e320.
57. Powers T, Walter P. Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J 1997;16:4880-4886.
58. Walter P, Blobel G. 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 1981;91:557-561.
59. Mason N, Ciufo LF, Brown JD. Elongation arrest is a physiologically important function of the signal recognition particle. EMBO J 2000;19:4164-4174.
60. Thomas Y, Bui N, Strub K. 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 1997;25:1920-1929.
61. Weichenrieder O, Wild K, Strub K, Cusack S. Structure and assembly of the Alu domain of the mammalian signal recognition particle. Nature 2000;408:167-173.
62. Huck L, Scherrer A, Terzi L, Johnson AE, Bernstein HD, Cusack S, Weichenrieder O, Strub K. Conserved tertiary base pairing ensures proper RNA folding and efficient assembly of the signal recognition particle Alu domain. Nucleic Acids Res 2004;32:4915-4924.
63. Terzi L, Pool MR, Dobberstein B, Strub K. Signal recognition particle Alu domain occupies a defined site at the ribosomal subunit interface upon signal sequence recognition. Biochemistry 2004;43:107-117.
64. Liao X, Selinger D, Althoff S, Chiang A, Hamilton D, Ma M, Wise JA. Random mutagenesis of Schizosaccharomyces pombe SRP RNA: Lethal and conditional lesions cluster in presumptive protein binding sites. Nucleic Acids Res 1992;20:1607-1615.
65. Ben-Shlomo H, Levitan A, Beja O, Michaeli S. The trypanosomatid Leptomonas collosoma 7SL RNA gene. Analysis of elements controlling its expression. Nucleic Acids Res 1997;25:4977-4984.
66. Liu L, Ben-Shlomo H, Xu YX, Stern MZ, Goncharov I, Zhang Y, Michaeli S. The trypanosomatid signal recognition particle consists of two RNA molecules, a 7SL RNA homologue and a novel tRNA-like molecule. J Biol Chem 2003;278:18271-18280.
67. Sagar MB, Lucast L, Doudna JA. Conserved but non-essential interaction of SRP RNA with translation factor EF-G. RNA 2004;10:772-778.
68. Nakamura K, Imai Y, Nakamura A, Yamane K. Small cytoplasmic RNA of Bacillus subtilis: Functional relationship with human signal recognition particle 7S RNA and Escherichia coli 4.5S RNA. J. Bacteriol 1992;174:2185-2192.
69. Nishiguchi M, Honda K, Amikura R, Nakamura K, Yamane K. Structural requirements of Bacillus subtilis small cytoplasmic RNA for cell growth, sporulation, and extracellular enzyme production. J Bacteriol 1994;176:157-165.
70. Schuenemann D, Amin P, Hoffman NE. Functional divergence of the plastid and cytosolic forms of the 54-kDa subunit of signal recognition particle. Biochem Biophys Res Commun 1994;254:253-258.
71. Groves MR, Mant A, Kuhn A, Koch J, Dubel S, Robinson C, Sinning I. Functional characterization of recombinant chloroplast signal recognition particle. J Biol Chem 2001;276:27778-27786.
72. Packer JC, Howe CJ. Algal plastid genomes encode homologues of the SRP-associated RNA. Mol Microbiol 1998;27:508-510.
73. Rosenblad MA, Samuelsson T. Identification of chloroplast signal recognition particle genes. Plant Cell Physiol 2004;45:1633-1639.
74. Franklin AE, Hoffmann NE. Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J Biol Chem 1993;268:22175-22180.
75. Tu CJ, Schuenemann D, Hoffman NE. Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J Biol Chem 1999;274:27219-27224.
76. Klimyuk VI, Persello-Cartieaux F, Havaux M, Contard-David P, Schuenemann D, Meiherhoff K, Gouet P, Jones JD, Hoffman NE, Nussaume L. A chromodomain protein encoded by the arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 1999;11:87-99.
77. Goforth RL, Peterson EC, Yuan J, Moore M, Knight AD, Lohse MB, Sakon J, Henry RL. Regulation of the GTPase cycle in posttranslational signal recognition particle based protein targeting involves cpSRP43. J Biol Chem 2004;279:43077-43084.
78. Jonas-Straube E, Hutin C, Hoffman NE, Schunemann D. Functional analysis of the protein-interacting domains of chloroplast SRP43. J Biol Chem 2001;276:24654-24660.
79. Tu CJ, Peterson EC, Henry R, Hoffman NE. The L18 domain of light-harvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J Biol Chem 2000;275:13187-13190.
80. Hutin C, Havaux M, Garde JP, Kloppstech K, Meiherhoff K, Hoffman N, Nussaume L. Double mutation cpSRP43 - /cpSRP54 - is necessary to abolish the cpSRP pathway required for thylakoid targeting of the light-harvesting chlorophyll proteins. Plant J 2002;29:531-543.
81. Moore M, Goforth RL, Mori H, Henry R. Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required. J Cell Biol 2003;162:1245-1254.
82. Moore M, Harrison MS, Peterson EC, Henry R. Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 2000;275:1529-1532.
83. Samuelson JC, Jiang F, Yi L, Chen M, de Gier JW, Kuhn A, Dalbey RE. Function of YidC for the insertion of M13 procoat protein in Escherichia coli: Translocation of mutants that show differences in their membrane potential dependence and Sec requirement. J Biol Chem 2001;276:34847-34852.
84. Amin P, Sy DA, Pilgrim ML, Parry DH, Nussaume L, Hoffman NE. Arabidopsis mutants lacking the 43- and 54-kilodalton subunits of the chloroplast signal recognition particle have distinct phenotypes. Plant Physiol 1999;121:61-70.
85. Nilsson R, van Wijk KJ. Transient interaction of cpSRP54 with elongating nascent chains of the chloroplast-encoded D1 protein; 'cpSRP54 caught in the act'. FEBS Lett 2002;524:127-133.
86. Zhang L, Paakkarinen V, Suorsa M, Aro EM. A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J Biol Chem 2001;276:37809-37814.
87. Kutay U, Ahnert-Hilger G, Hartmann E, Wiedenmann B, Rapoport TA. Transport route for synaptobrevin via a novel transport pathway of insertion into the endoplasmic reticulum membrane. EMBO J 1995;14:217-223.
88. Schlenstedt G, Gudmundsson GH, Boman HG, Zimmermann R. A large presecretory protein translocates both cotranslationally, using signal recognition particle and ribosome, and posttranslationally, without these ribonucleoparticles, when synthesized in the presence of mammalian microsomes. J Biol Chem 1990;265:13960-13968.
89. Borgese N, Brambillasca S, Soffientini P, Yabal M, Makarow M. Biogenesis of tail-anchored proteins. Biochem Soc Trans 2003;31:1238-1242.
90. Abell BM, Pool MR, Schlenker O, Sinning I, High S. Signal recognition particle mediates post-translational targeting in eukaryotes. EMBO J 2004;23:2755-2764.
91. Ng DT, Brown JD, Walter P. Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J Cell Biol 1996;134:269-278.
92. Hann BC, Walter P. The signal recognition particle in S. cerevisiae. Cell 1991;67:131-144.
93. Mutka SC, Walter P. Multifaceted physiological response allows yeast to adapt to the loss of the signal recognition particle-dependent protein-targeting pathway. Mol Biol Cell 2001;12:577-588.
94. Bassford P, Beckwith J, Ito K, Kumamoto C, Mizushima S, Oliver D, Randall L, Silhavy T, Tai PC, Wickner B. The primary pathway of protein export in E. coli. Cell 1991;65:367-368.
95. de Keyzer J, van der Does C, Driessen AJ. The bacterial translocase: A dynamic protein channel complex. Cell Mol Life Sci 2003;60:2034-2052.
96. Ulbrandt ND, Newitt JA, Bernstein HD. The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 1997;88:187-196.
97. Seluanov A, Bibi E. FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J Biol Chem 1997;272:2053-2055.
98. Beha D, Deitermann S, Muller M, Koch HG. Export of beta-lactamase is independent of the signal recognition particle. J Biol Chem 2003;278:22161- 22167.
99. Lee HC, Bernstein HD. The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc Natl Acad Sci USA 2001;98:3471-3476.
100. Peterson JH, Woolhead CA, Bernstein HD. Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J Biol Chem 2003;278:46155-46162.
101. Yang AJ, Mulligan RM. Identification of a 4.5S-like ribonucleoprotein in maize mitochondria. Nucleic Acids Res 1996;24:3601-3606.
102. Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM. Ribosome binding to the Oxa1 complex facilitates cotranslational protein insertion in mitochondria. EMBO J 2003;22:6448-6457.
103. Jia L, Dienhart M, Schramp M, McCauley M, Hell K, Stuart RA. Yeast Oxal interacts with mitochondrial ribosomes: The importance of the C-terminal region of Oxa1. EMBO J 2003;22:6438-6447.
104. Schierle CF, Berkmen M, Huber D, Kumamoto C, Boyd D, Beckwith J. The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J Bacteriol 2003;185:5706-5713.
105. Bowers CW, Lau F, Silhavy TJ. Secretion of LamB-LacZ by the signal recognition particle pathway of Escherichia coli. J Bacteriol 2003;185:5697-5705.
106. Larsen N, Zwieb C. SRP-RNA sequence alignment and secondary structure. Nucleic Acids Res 1991;19:209-215.