A mechanism for toxin insertion into membranes is suggested by the crystal structure of the channel-forming domain of colicin E1

Structure

Volumn 5, Issue 3, 1997, Pages 443-458

  Elkins, Patricia ^a,b   Bunker, Amy ^a   Cramer, William A ^a   Stauffacher, Cynthia V ^a  

^a PURDUE UNIVERSITY   (United States)

^b GENENTECH INC   (United States)

Author keywords

protein membrane interactions; toxin structure; toxin membrane interactions; voltage gated channel

Indexed keywords

EID: 0031569354     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00200-1     Document Type: Article

References (59)

1. Konisky, J. (1982). Colicins and other bacteriocins with established modes of action. Ann. Rev. Microbiol. 36, 125-144.
2. Cramer, W.A., et al., & Stauffacher, C.V. (1995). Structure-function of the channel-forming colicins. Ann. Rev. Biophys. Biomol. Struct. 24, 611-641.
3. Schein, S.J., Kagan, B.L. & Finkelstein, A. (1978). Colicin K acts by forming voltage-dependent channels in phospholipid bilayer membranes. Nature 276, 159-163.
4. Bullock., J.O., Cohen, F.S., Dankert, J.R. & Cramer, W.A. (1983). Comparison of the macroscopic and single channel conductance properties of colicin E1 and its COOH-terminal tryptic peptide. J. Biol. Chem. 258, 9908-9912.
5. Gould, J.M. & Cramer, W.A. (1977). Studies on the depolarization of the Escherichia coli cell membrane by colicin El. J. Biol. Chem 252, 5491-5497.
6. Cramer, W.A., Dankert, J.R. & Uratani, Y. (1983). The membrane channel-forming bacteriocidal protein, colicin E1. Biochim. Biophys. Acta 737, 173-193.
7. Fields, K.L. & Luria, S.E. (1969). Effects of colicins E1 and K on cellular metabolism. J. Bacteriol. 97, 64-77.
8. Wendt, L. (1970) Mechanism of colicin action: early events. J. Bacteriol. 104, 1236-1241.
9. Phillips, S.K. & Cramer, W.A. (1973). Properties of the fluorescence probe response associated with the transmission mechanism of colicin E1. Biochemistry 12, 1170-1176.
10. Guihard, G., Bénédetti, H., Besnard, M. & Letellier, L. (1993) Phosphate efflux through the channels formed by colicins and phage T5 in Escherichia coli cells is responsible for the fall in cytoplasmic ATP. J. Biol. Chem. 268, 17775-17780.
11. Brunden, K.R., Cramer, W.A. & Cohen, F.S. (1984). Purification of a small receptor-binding peptide from the central region of the colicin E1 molecule. J. Biol. Chem. 259, 190-196.
12. Baty, D., et al., & Lazdunski, C. (1988). Functional domains of colicin A. Mol. Microbiol. 2, 807-811.
13. Bénédetti, H., Frenette, M., Baty, D., Lloublès, R., Geli, V. & Lazdunski, C. (1989) Comparison of the uptake systems for the entry of various BtuB group colicins into Escherichia coli. J. Gen. Microbiol. 135, 3413-3420.
14. Kadner, R.J., Bassford, P.J.J. & Pagsley, A.P. (1979) Colicin receptors and uptake. Zentralb. Bakteriol. Parasiten. Infektion. Hyg. 224, 90-104.
15. 12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4, 2027-2033.
16. Webster, R.E. (1991). The toi gene products and the import of macromolecules into Escherichia coli. Mol. Microbiol. 5, 1005-1011.
17. Levengood, S.K., Beyer, W.F.J. & Webster, R.E. (1991). TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc. Natl. Acad. Sci. USA 88, 5939-5943.
18. Pilsl, H. & Braun, V. (1995). Novel colicin 10: assignment of four domains to TonB- and TolC-dependent uptake via the Tsx receptor and to pore formation. Mol. Microbiol. 16, 57-67.
19. Parker, M.W., Pattus, F., Tucker, A.D. & Tsernoglou, D. (1989). Structure of the membrane-pore-forming fragments of colicin A. Nature 337, 93-96.
20. Parker, M.W., Postma, J.P.M., Pattus, F., Tucker, A.D. & Tsernoglou, D. (1992). Refined structure of the pore-forming domain of colicin A at 2.4 Å resolution. J. Mol. Biol. 224, 639-657.
21. Ghosh, P., Mell, S.F. & Stroud, R.M. (1994). The domain structure of the ion channel-forming protein colicin la. Nat. Struct. Biol. 1, 597-604.
22. Weiner, M., Freymann, D., Ghosh, P. & Stroud, R.M. (1997). Crystal structure of colicin la. Nature 385, 461 -464.
23. Cleveland, M.V., Slatin, S., Finkelstein, A. & Levinthal, C. (1983). Structure-function relationships for a voltage-dependent ion channel: properties of COOH-terminal fragments of colicin A. Proc. Natl. Acad. Sci. USA 80, 3706-3710.
24. Davidson, V.L., Brunden, K.R. & Cramer, W.A. (1985). Acidic pH requirement for insertion of colicin E1 into artificial membrane vesicles: relevance to the mechanism of action of colicins and certain toxins. Proc. Natl. Acad. Sci. USA 82, 1386-1390.
25. van der Goot, F.G., González-Mañas, J.M., Lakey, J.H. & Pattus, F. (1991). A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354, 408-410.
26. Schendel, S.L. & Cramer, W.A. (1994). On the nature of the unfolded intermediate in the in vitro transition of the colicin E1 channel domain from the aqueous to the membrane phase. Protein Sci. 3, 2272-2279.
27. Kagan, B.L., Finkelstein, A. & Colombini, M. (1981). Diphtheria toxin fragment forms large pores in phospholipid bilayer membranes. Proc. Natl. Acad. Sci. USA 78, 4950-4954.
28. Zhang, H., Choe, S., Huynh, P.D., Finkelstein, A., Eisenberg, D. & Collier, R.J. (1994). Dynamic transitions of the transmembrane domain of diphtheria toxin: disulfide trapping and fluorescence proximity studies. Biochemistry 33, 11254-11263.
29. Menestrina, G., Fonti, S. & Gambale, F. (1989). Interaction of tetanus toxin with lipid vesicles. Effects of pH, surface charge, and transmembrane potential on the kinetics of channel formation. Biophys. J. 55, 393-405.
30. Dankert, J.R., Uratani, Y., Grabau, C., Cramer, W.A. & Hermodson, M. (1982). On a domain structure of colicin E1: a COOH-terminal peptide fragment active in membrane depolarization. J. Biol. Chem. 257, 3857-3863.
31. Heymann, J.B., Zakharov, S.D., Zhang, Y.-L. & Cramer, W.A. (1996). Characterization of electrostatic and nonelectrostatic components of protein-membrane binding interactions. Biochemistry 35, 2717-2725.
32. Zakharov, S.D., Heymann, J.B., Zhang, Y.-L. & Cramer, W.A. (1996). Membrane binding of the colicin E1 channel: activity requires an electrostatic interaction of intermediate magnitude. Biophys. J. 70, 2774-2783.
33. Elkins, P., Song, H.Y., Cramer, W.A. & Stauffacher, C.V. (1994). Crystallization and characterization of colicin E1 channel-forming polypeptides. Proteins 19, 150-157.
34. Laskowski, R.A., MacArthus, M.W., Moss, D.S. & Thorton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structure. J. Appl. Cryst 26, 283-291.
35. Nicholls, A.N., Sharp, K.A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.
36. Song, H.Y., Cohen, F.S. & Cramer, W.A. (1991). Membrane topography of ColE1 gene products: the hydrophobic anchor of the colicin E1 channel is a helical hairpin. J. Bacteriol. 173, 2927-2934.
37. Merrill, A.R. & Cramer, W.A. (1990). Identification of a voltage-responsive segment of the potential-gated colicin E1 ion channel. Biochemistry 29, 8529-8534.
38. Parker, M.W. & Pattus, F. (1993). Rendering a membrane protein soluble in water: a common packing motif in bacterial protein toxins. Trends Biochem. Sci. 18, 391-395.
39. Shin, Y.-K., Levinthal, C., Levinthal, F. & Hubbell, W.L. (1993). Colicin E1 binding to membranes: time-resolved studies of spin-label mutants. Science 259, 960-963.
40. Kienker, P.K., Qiu, X.-Q., Slatin, S.L., Finkelstein, A. & Jakes, K.S. (1997). Transmembrane insertion of the colicin la hydrophobic hairpin. J. Gen. Physiol., in press.
41. Jeanteur, D., Pattus, F. & Timmins, P.A. (1994). Membrane-bound form of the pore-forming domain of colicin A. J. Mol. Biol. 235, 898-907.
42. Zhang, Y.-L. & Cramer, W.A. (1992). Constraints imposed by protease accessibility on the trans-membrane and surface topography of the colicin E1 channel. Protein Sci. 1, 1666-1676.
43. Liu, Q.R., Crozel, V., Levinthal, F., Slatin, S., Finkelstein, A. & Levinthal, C. (1986). A very short peptide makes a voltage-dependent ion channel: the critical length of the channel domain of colicin E1. Proteins 1, 218-229.
44. Baty, D., Lakey, J., Pattus, F. & Lazdunski, C. (1990). A 136 residue COOH-terminal fragment of colicin A is endowed with ionophoric activity. Eur. J. Biochem. 189, 409-413.
45. Qui, X.-Q., Jakes, K.S., Kienker, P.K., Finkelstein, A. & Slatin, S.L. (1996). Major transmembrane movement associated with colicin la channel gating. J. Gen. Physiol. 107, 313-321.
46. White, S.H. & Wimley, W.C., (1994). Peptides in lipid bilayers: structural and thermodynamic basis for partitioning and folding. Curr. Opin. Struct. Biol. 4, 79-86.
47. Lakey, J.H., Duch, D., González-Mañas, J.-M., Baty, D. & Pattus, F. (1993). Fluorescence energy transfer distance measurements. The hydrophobic helical hairpin of colicin A in the membrane bound state. J. Mol. Biol. 230, 1055-1067.
48. Otwinowski, Z. (1993). Oscillation Data Reduction Program. In Proceedings of the CCP4 Study Weekend: Data Collection and Processing. (Sawyer, L., Isaacs, N. & Bailey, S., eds), pp. 55-62, SERC Daresbury Laboratory, Warrington, UK.
49. Minor, W. (1993). XDISPLAYF Program. Purdue University, West Lafayette, IN, USA.
50. Collaborative Computational Project No.4. (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D 50, 760-763.
51. Otwinowski, Z. (1991). Maximum likelihood refinement of heavy atom parameters. In Isomorphous Replacement and Anomalous Scattering. (Wolf, W. & Leslie, A.G.W., eds), pp. 80-86, SERC Daresbury Laboratory, Warrington, UK.
52. Read, R.J. (1986). Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Cryst. A 42, 140-149.
53. Jones, T.A., Zou, J.-Y., Cowan, S. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of error in these models. Acta Cryst. A 47, 110-119.
54. Brünger, A.T., Kuriyan, J. & Karplus, M. (1987). Crystallographic R factor refinement by molecular dynamics. Science 235, 458-460.
55. Brünger, A.T. (1992). X-PLOR, Version 3.1: a system for X-ray crystallography and NMR. Yale University Press, New Haven, CT.
56. Brünger, A.T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 335, 472-474.
57. Brünger, A.T. (1993). Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Cryst. D 49, 24-36.
58. QUANTA96: X-ray structure analysis user's reference. (1996). Molecular Simulations, San Diego, CA.
59. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.