Role for both DNA and RNA in GTP hydrolysis by the Neisseria gonorrhoeae signal recognition particle receptor

Journal of Bacteriology

Volumn 185, Issue 3, 2003, Pages 801-808

  Frasz, Cody ^a   Arvidson, Cindy Grove ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOCKING PROTEIN; PROTEIN FFH; RNA; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ANALYSIS; IN VITRO STUDY; MOLECULAR CLONING; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; RNA, RIBOSOMAL; SIGNAL RECOGNITION PARTICLE;

ESCHERICHIA COLI; MAMMALIA; NEGIBACTERIA; NEISSERIA; NEISSERIA GONORRHOEAE; PILA; PROKARYOTA;

EID: 0037309133     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.3.801-808.2003     Document Type: Article

References (63)

1. Arvidson, C. G., T. Powers, P. Walter, and M. So. 1999. Neisseria gonorrhoeae PilA is an FtsY homolog. J. Bacteriol. 181:731-739.
2. Arvidson, C. G., and M. So. 1995. Interaction of the Neisseria gonorrhoeae PilA protein with the pile promoter involves multiple sites on the DNA. J. Bacteriol. 177:2497-2504.
3. Arvidson, C. G., and M. So. 1995. The Neisseria transcriptional regulator PilA has a GTPase activity. J. Biol. Chem. 270:26045-26048.
4. Batey, R. T., R. P. Rambo, L. Lucast, B. Rha, and J. A. Doudna. 2000. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 287:1232-1239.
5. Beck, K., L.-F. Wu, J. Brunner, and M. Muller. 2000. Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 19:134-143.
6. 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.
7. Bernstein, H. D., D. Zopf, D. M. Freymann, and P. Walter. 1993. Functional substitution of the signal recognition particle 54-kDa subunit by its Escherichia coli homolog. Proc. Natl. Acad. Sci. USA 90:5229-5233.
8. Brown, S., and M. J. Fournier. 1984. The 4.5S RNA gene of Escherichia coli is essential for cell growth. J. Mol. Biol. 178:533-550.
9. Carey, J. 1991. Gel retardation. Methods Enzymol. 208:103-117.
10. Cornish-Bowden, A., and C. W. Wharton (ed.). 1988 Enzyme kinetics. Information Press Ltd., Oxford, United Kingdom.
11. deGier, J.-W. L., P. Mansournia, Q. A. Valent, G. J. Phillips, J. Luirink, and G. von Heijne. 1996. Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett. 399:307-309.
12. deGier, J.-W. L., P. A. Scotti, A. Saaf, Q. A. Valent, A. Kuhn, J. Luirink, and G. von Heijne. 1998. Differential use of the signal recognition particle translocase targeting pathway for inner membrane protein assembly in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:14646-14651.
13. deLeeuw, E., K. teKaat, C. Moser, G. Menestrina, R. Demel, B. Dekruijff, B. Oudega, J. Luirink, and I. Sinning. 2000. Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity. EMBO J. 19:531-541.
14. Dever, T. E., M. J. Glynias, and W. C. Merrick. 1987. GTP-binding domain: three consensus sequence elements with distinct spacing. Proc. Natl. Acad. Sci. USA 84:1814-1818.
15. 2- GDP. Nat. Struct. Biol. 6:793-801.
16. Gill, D. R., and G. P. C. Salmond. 1990. The identification of the Escherichia coli fisY gene product: an unusual protein. Mol. Microbiol. 4:575-583.
17. Gorodkin, J., B. Knudsen, C. Zweib, and T. Samuelsson. 2001. SRPDB (Signal Recognition Particle Database). Nucleic Acids Res. 29:169-170.
18. Hutchison, C. A., III, S. N. Peterson, S. R. Gill, R. T. Cline, O. White, C. M. Fraser, H. O. Smith, and J. C. Venter. 1999. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286:2165-2169.
19. Jagath, J. R., N. B. Matassova, E. deLeeuw, J. M. Warnecke, G. Lentzen, M. V. Rodnina, J. Luirink, and W. Wintermeyer. 2001. Important role of the tetraloop region of 4.5S RNA in SRP binding to its receptor FtsY. RNA 7:293-301.
20. Jagath, J. R., M. V. Rodnina, and W. Wintermeyer. 2000. Conformational changes in the bacterial SRP receptor FtsY upon binding of guanine nucleotides and SRP. J. Mol. Biol. 295:745-753.
21. Keenan, R. J., D. M. Freymann, R. M. Stroud, and P. Walter. 2001. The signal recognition particle. Annu. Rev. Biochem. 70:755-775 .
22. Keenan, R. J., D. M. Freymann, P. Walter, and R. M. Stroud. 1998. Crystal structure of the signal sequence binding subunit of the signal recognition particle. Cell 94:181-191.
23. Kellogg, D. S., W. L. Peacock, W. E. Deacon, L. Brown, and C. I. Pirkle. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
24. Kusters, R., G. Lentzen, E. Eppens, A. vanGeel, C. C. van der Weijden, W. Wintermeyer, and J. Luirink. 1995. The functioning of the SRP receptor FtsY in protein-targeting in E. coli is correlated with its ability to bind and hydrolyze GTP. FEBS Lett. 372:253-258.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Lee, H. C., and H. D. Bernstein. 2001. 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 98:3471-3476.
27. Leung, S. S., and D. J. Koslowsky. 2001. Interactions of mRNAs and gRNAs involved in trypanosome mitochondrial RNA editing: structure probing of an mRNA bound to its cognate gRNA. RNA 7:1803-1816.
28. Lu, Y., H.-Y. Qi, J. B. Hyndman, N. D. Ulbrandt, A. Teplyakov, N. Tomasevic, and H. D. Bernstein. 2001. Evidence for a novel GTPase priming step in the SRP protein targeting pathway. EMBO J. 20:6724-6734.
29. Luirink, J., S. High, H. Wood, A. Giner, D. Tollervey, and B. Dobberstein. 1992. Signal-sequence recognition by an Escherichia coli ribonucleoprotein complex. Nature 359:741-743.
30. Macao, B., J. Luirink, and T. Samuelsson. 1997. Ffh and FtsY in a Mycoplasma mycoides signal-recognition particle pathway: SRP RNA and M domain of Ffh are not required for stimulation of GTPase activity in vitro. Mol. Microbiol. 24:523-534.
31. MacFarlane, J., and M. Muller. 1995. The functional integration of a polytopic membrane protein of Escherichia coli is dependent on the bacterial signal-recognition particle. Eur. J. Biochem. 233:766-771.
32. Miller, J. D., H. D. Bernstein, and P. Walter. 1994. Interaction of E. coli Ffh/4.5S ribonucleoprotein and FtsY mimics that of the signal recognition particle and its receptor. Nature 367:657-659.
33. 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.
34. Millman, J. S., and D. W. Andrews. 1999. A site-specific, membrane-dependent cleavage event defines the membrane binding domain of FtsY. J. Biol. Chem. 274:33227-33234.
35. Mukherjee, A., K. Dai, and J. Lutkenhaus. 1993. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl. Acad. Sci. USA 90:1053-1057.
36. Neuhard, J., and P. Nygaard. 1987. Purines and pyrimidines, p. 445-473. In J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol. 1. American Society for Microbiology, Washington, D.C.
37. Neumann-Haefelin, C., U. Schafer, M. Muller, and H.-G. Koch. 2000. SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J. 19:6419-6426.
38. Newitt, J. A., N. D. Ulbrandt, and H. D. Bernstein. 1999. The structure of multiple polypeptide domains determines the signal recognition particle requirement of Escherichia coli inner membrane proteins. J. Bacteriol. 181:4561-4567.
39. Peluso, P., D. Herschlag, S. Nock, D. M. Freymann, A. P. Johnson, and P. Walter. 2000. Role of 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor. Science 288:1640-1643.
40. Phillips, G. J., and T. J. Silhavy. 1992. The E. coli ffh gene is necessary for viability and efficient protein transport. Nature 359:744-746.
41. Poritz, M. A., H. D. Bernstein, K. Strub, D. Zopf, H. Wilhelm, and P. Walter. 1990. An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250:1111-1117.
42. Powers, T., and P. Walter. 1997. Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J. 16:4880-4886.
43. Powers, T., and P. Walter. 1995. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 269:1422-1424.
44. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbio. Rev. 57:50-108.
45. Rapoport, T. A., B. Jungnickel, and U. Kutay. 1996. Protein transport across the endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 65:271-303.
46. Romisch, 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.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. Samuelsson, T., M. Olsson, P. M. Witkstrom, and B. R. Johannson. 1995. The GTPase activity of the Escherichia coli Ffh protein is important for normal growth. Biochim. Biophys. Acta 1267:83-91.
49. Schatz, P. J., and J. Beckwith. 1990. Genetic analysis of protein export in Escherichia coli. Annu. Rev. Genet. 24:215-248.
50. Segal, E., E. Billyard, M. So, S. Storzbach, and T. F. Meyer. 1985. Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation. Cell 40:293-300.
51. 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.
52. Studier, F. W., A. H. Rosenberg, and J. J. Dunn. 1990. Use of T7 RNA polymerase to direct the expression of cloned genes. Methods Enzymol. 185:60-89.
53. Suzuma, S., K. Hayashi, K. Nakamura, and K. Yamane. 1999. Analysis of Escherichia coli 4.5S RNA binding affinity to Ffh and EF-G. FEMS Microbiol. Lett. 180:271-277.
54. Taha, M. K., B. Dupuy, W. Saurin, M. So, and C. Marchal. 1991. Control of pilus expression in Neisseria gonorrhoeae as an original system in the family of two-component regulators. Mol. Microbiol. 5:137-148.
55. Ulbrandt, N. D., J. A. Newitt, and H. D. Bernstein. 1997. The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88:187-196.
56. Valent, Q. A., J.-W. L. deGier, G. von Heijne, D. A. Kendall, C. M. ten Hagen-Jongman, B. Oudega, and J. Luirink. 1997. Nascent membrane and presecretory proteins synthesized in Escherichia coli associate with signal recognition particle and trigger factor. Mol. Microbiol. 25:53-64.
57. Valent, Q. A., D. A. Kendall, S. High, R. Kusters, B. Oudega, and J. Luirink. 1995. Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14:5494-5505.
58. Valent, Q. A., P. A. Scotti, S. High, J.-W. L. deGier, G. von Heijne, G. Lentzen, W. Wintermeyer, B. Oudega, and J. Luirink. 1998. The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 17:2504-2512.
59. Walter, P., and A. E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum. Annu. Rev. Cell Biol. 10:87-119.
60. Wickner, W., A. J. M. Driessen, and F.-U. Hartl. 1991. The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu. Rev. Biochem. 60:101-124.
61. Zelazny, A., A. Seluanov, A. Cooper, and E. Bibi. 1997. 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 94:6025-6029.
62. Zheng, N., and L. M. Gierasch. 1997. Domain interactions in E. coli SRP: stabilization of M domain by RNA is required for effective signal sequence modulation of NG domain. Mol. Cell 1:79-87.
63. 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 J. 9:4511-4517.