Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity

EMBO Journal

Volumn 19, Issue 4, 2000, Pages 531-541

  De Leeuw, E ^a   Te Kaat, K ^b   Moser, C ^c,e   Menestrina, G ^c   Demel, R ^d   De Kruijff, B ^d   Oudega, B ^a   Luirink, J ^a   Sinning, I ^b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c CNR   (Italy)

^d UTRECHT UNIVERSITY   (Netherlands)

^e GSK   (Italy)

Author keywords

E.coli; FtsY; Protein targeting; Signal recognition particle

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PHOSPHOLIPID; SIGNAL RECOGNITION PARTICLE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL;

ESCHERICHIA COLI; EUKARYOTA;

EID: 0034651525     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.4.531     Document Type: Article

References (47)

1. Arkin, I.T., Rothman, M., Ludlam, C.F.C., Aimoto, S., Engelman, D.M., Rothschild, K.J. and Smith, S.O. (1995) Structural model of the phospholamban ion channel complex in phospholipid membranes. J. Mol. Biol., 248, 824-834.
2. Breukink, E., Demel, R.A., de Korte-Kool, G. and de Kruijff, B. (1992) SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochemistry, 31, 1119-1124.
3. Byler, D.M. and Susi, H. (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers, 25, 469-487.
4. Cabelli, R.J., Dolan, K.M., Qian, L. and Oliver, D.B. (1991) Characterization of membrane-associated and soluble states of SecA protein from wild-type and SecA51 (TS) mutant strains of Escherichia coli. J. Biol. Chem., 266, 24420-24427.
5. Cabiaux, V., Buckley, J.T., Wattiez, R., Ruysschaert, J.M., Parker, M.W. and van der Goot, F.G. (1997) Conformational changes in aerolysin during the transition from the water-soluble protoxin to the membrane channel. Biochemistry, 36, 15224-15232.
6. Cullis, P.R. and de Kruijff, B. (1979) Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta, 559, 399-120.
7. De Gier, J.W.L., Mansournia, P., Valent, Q.A., Phillips, G.J., Luirink, J. and von Heijne, G. (1996) Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett., 399, 307-309.
8. De Leeuw, E., Poland, D., Mol, O., Sinning, I., ten Hagen-Jongman, C.M., Oudega, B. and Luirink, J. (1997) Membrane association of FtsY, the E.coli SRP receptor. FEBS Lett., 416, 225-229.
9. Demel, R.A. (1994) Monomolecular layers in the study of biomembranes. Subcell. Biochem., 23, 83-120.
10. Driessen, A.J.M. (1996) Translocation of proteins across the bacterial cytoplasmic membrane. In Konings, W.N., Kaback, H.R. and Lolkema, J.S. (eds), Handbook of Biophysics, 2. Transport Processes in Membranes. Elsevier, Amsterdam, The Netherlands, pp. 759-790.
11. Driessen, A.J.M., Fekkes, P. and van der Wolk, J.P.W. (1998) The Sec system. Curr. Opin. Microbiol., 2, 216-222.
12. Ellens, H., Bentz, J. and Szoka, F.C. (1986) Fusion of phosphatidyl-ethanolamine-containing liposomes and mechanism of the L alpha-HII phase transition. Biochemistry, 25, 285-294.
13. Fringeli, U.P. and Günthard, H.H. (1981) Infrared membrane spectroscopy. Mol. Biol. Biochem. Biophys., 31, 270-332.
14. Gill, D.R., Hatfull ,G.F. and Salmond, G.P.C. (1986) A new cell division operon in Escherichia coli. Mol. Gen. Genet., 205, 134-145.
15. Goormaghtigh, E., Cabiaux, V. and Ruysschaert, J.-M. (1990) Secondary structure and dosage of soluble and membrane proteins by attenuated total reflection Fourier-transform infrared spectroscopy on hydrated films. Eur. J. Biochem., 193, 409-420.
16. Hartl, F.-U., Lecker, S., Schiebel, E., Hendrick, J.P. and Wickner, W. (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E.coli plasma membrane. Cell, 63, 269-279.
17. Hope, M.J., Bally, M.B., Webb, G. and Cullis, P.R. (1985) Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta, 812, 55-65.
18. Kusters, R., Dowhan, W. and de Kruijff, B. (1991) Negatively charged phospholipids restore prePhoE translocation across phosphatidyl-glycerol-depleted Escherichia coli inner membrane vesicles. J. Biol. Chem., 266, 8659-8662.
19. Kusters, R., Lentzen, G., Eppens, E., van Geel, A., van der Weijden, C.C., Wintermeyer, W. and Luirink, J. (1995) The functioning of the SRP receptor FtsY in protein targeting in E.coli is correlated with its ability to bind and hydrolyse GTP. FEBS Lett., 372, 253-258.
20. Luirink, J. and Dobberstein, B. (1994) Mammalian and Escherichia coli signal recognition particles. Mol. Microbiol., 11, 9-13.
21. Luirink, J., ten Hagen-Jongman, C.M., van der Weijden, C.C., Oudega, B., High, S., Dobberstein, B. and Kusters, R. (1994) An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J., 13, 2289-2296.
22. MacFarlane, J. and Milller, M. (1995) Functional integration of a polytopic membrane protein of E.coli requires the bacterial signal recognition particle. Eur. J. Biochem., 223, 766-771.
23. Menestrina, G., Cabiaux, V. and Tejuca, M. (1999) Secondary structure of sea anemone cytolysins in soluble and membrane bound form by infrared spectroscopy. Biochem. Biophys. Res. Commun., 254, 174-180.
24. Miller, J.D., Bernstein, H.D. and Walter, P. (1994) Interaction of E.coli Ffh/4.5S ribonucleoprotein and FtsY mimics that of mammalian signal recognition particle and its receptor. Nature, 367, 657-659.
25. Mitchell, C. and Oliver, D. (1993) Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase. Mol. Micobiol., 10, 483-497.
26. Monloya, G., Svensson, C., Luirink, J. and Sinning, I. (1997a) Crystal structure of the NG domain from the signal recognition particle receptor FtsY. Nature, 385, 365-368.
27. Montoya, G., Svensson, C., Luirink, J. and Sinning, I. (1997b) Expression, crystallization and preliminary X-ray diffraction study of FtsY, the docking protein of the signal recognition particle of E.coli. Proteins, 28, 285-288.
28. Morein, S., Andersson, A., Rilfors, L. and Lindblom, G. (1996) Wild-type Escherichia coli cells regulate the membrane lipid composition in a 'window' between gel and non-lamellar structures. J. Biol. Chem., 271, 6801-6809.
29. Moser, C. (1998) Functional studies on the receptor of the signal recognition particle. PhD thesis. University of Heidelberg.
30. Moser, C., Mol,O., Goody, R.S. and Sinning, I. (1997) The signal recognition particle receptor of Escherichia coli (FtsY) has a nucleotide exchange factor built into the GTPase domain. Proc. Natl Acad. Sci. USA, 94, 11339-11344.
31. Powers, T. and Walter, P. (1995) Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science, 269, 1422-1424.
32. Powers, T. and Walter, P. (1997) Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J., 16, 4880-4886.
33. Rapoport, T.A., Jungnickel, B. and Kutay, U. (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem., 65, 271-303.
34. Samuelsson, T. and Olsson, M. (1993) GTPase activity of a bacterial SRP-like complex. Nucleic Acids Res., 21, 847-853.
35. Samuelsson, T. and Zwieb, C. (1999) The signal recognition particle database (SRPDB). Nucleic Acids Res., 27, 169-170.
36. Scotti, P.A., Valent, Q.A., Manting, E.H., Urbanus, M.L., Driessen, A.J.M., Oudega, B. and Luirink, J. (1999) SecA is not required for SRP-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J. Biol. Chem., 274, 29883-29888.
37. Seluanov, A. and Bibi, E. (1997) FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J. Biol. Chem., 272, 2053-2055.
38. Studier, F.W., Rosenberg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
39. Tamm, L.K. and Tatulian, S.A. (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers. Rev. Biophys., 30, 365-429.
40. Tatulian, S.A., Hinterdorfer, P., Baber, G. and Tamm, L.K. (1995) Influenza hemagglutinin assumes a tilted conformation during membrane fusion as determined by attenuated total reflection FTIR spectroscopy. EMBO J., 14, 5514-5523.
41. Ulbrandt, N.D., London, E. and Oliver, D.B. (1992) Deep penetration of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic phospholipids and by partial unfolding. J. Biol. Chem., 267, 15184-15192.
42. Ulbrandt, N.D., Newitt, J.A. and Bernstein, H.D. (1997) The E.coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell, 88, 187-196.
43. Valent, Q.A., de Gier, J.-W.L., van Heijne, G., Kendall, D.A., ten Hagen-Jongman, C.M., Oudega, B. and Luirink, J. (1997) Nascent membrane and presecretory proteins synthesised in Escherichia coli associate with signal recognition particle and trigger factor. Mol. Microbiol., 25, 53-64.
44. Valent, Q.A., Scotti, P.A., High, S., de Gier, J.-W.L., von Heijne, G., Lentzen, G., Wintermeyer, W., Oudega, B. and Luirink, J. (1998) The E.coli SRP and SecB targeting pathways converge at the translocon. EMBO J., 17, 2504-2512.
45. Wolin, S.L. (1994) From the elephant to E.coli: SRP-dependent protein targeting. Cell, 77, 787-790.
46. Young, J.C. and Andrews, D.W. (1996) The signal recognition particle receptor α subunit assembles co-translationally on the endoplasmic reticulum membrane during an mRNA-encoded translation pause in vitro. EMBO J., 15, 172-181.
47. Young, J.C., Ursini, J., Legate, K.R., Miller, J.D., Walter, P., and Andrews, D.W. (1995) 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., 270, 15650-15657.