Acidic pH-induced membrane insertion of colicin A into E. Coli natural lipids probed by site-directed Spin labeling

Journal of Molecular Biology

Volumn 425, Issue 10, 2013, Pages 1782-1794

  Pulagam, Lakshmi Padmavathi ^a   Steinhoff, Heinz Jürgen ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

channel activity in liposomes; closed channel state; insertion competent state; Keywords; site directed spin labeling; water soluble pore forming toxin

Indexed keywords

COLICIN A; LIPOSOME;

ARTICLE; CONFORMATION; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ESCHERICHIA COLI; HYDROPHOBICITY; IMMERSION; LIPID MEMBRANE; NONHUMAN; PH; PRIORITY JOURNAL; SPIN LABELING;

ESCHERICHIA COLI;

EID: 84877583096     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.01.037     Document Type: Article

References (66)

1. A. Cancino-Rodezno, H. Porta, M. Soberon, and A. Bravo Defense and death responses to pore forming toxins Biotechnol. Genet. Eng. Rev. 26 2010 65 82
2. S.C. Feil, G. Polekhina, M.A. Gorman, and M.W. Parker Proteins: membrane binding and pore formation. Introduction Adv. Exp. Med. Biol. 677 2010 1 13
3. I. Iacovache, F.G. van der Goot, and L. Pernot Pore formation: an ancient yet complex form of attack Biochim. Biophys. Acta 1778 2008 1611 1623
4. M.W. Parker, J.P. Postma, F. Pattus, A.D. Tucker, and D. Tsernoglou Refined structure of the pore-forming domain of colicin A at 2.4 Å resolution J. Mol. Biol. 224 1992 639 657
5. P.V. Padmavathi, and H.J. Steinhoff Conformation of the closed channel state of colicin A in proteoliposomes: an umbrella model J. Mol. Biol. 378 2008 204 214
6. C. Kleanthous Swimming against the tide: progress and challenges in our understanding of colicin translocation Nat. Rev. Microbiol. 8 2010 843 848
7. H. Ridley, C.L. Johnson, and J.H. Lakey Interfacial interactions of pore-forming colicins Adv. Exp. Med. Biol. 677 2010 81 90
8. J.H. Lakey, D. Duche, J.M. Gonzalez-Manas, D. Baty, and F. Pattus Fluorescence energy transfer distance measurements. The hydrophobic helical hairpin of colicin A in the membrane bound state J. Mol. Biol. 230 1993 1055 1067
9. S. Bohme, P.V. Padmavathi, J. Holterhues, F. Ouchni, J.P. Klare, and H.J. Steinhoff Topology of the amphipathic helices of the colicin A pore-forming domain in E. coli lipid membranes studied by pulse EPR Phys. Chem. Chem. Phys. 11 2009 6770 6777
10. Y. Kim, K. Valentine, S.J. Opella, S.L. Schendel, and W.A. Cramer Solid-state NMR studies of the membrane-bound closed state of the colicin E1 channel domain in lipid bilayers Protein Sci. 7 1998 342 348
11. D. Ho, M.R. Lugo, A.L. Lomize, I.D. Pogozheva, S.P. Singh, A.L. Schwan, and A.R. Merrill Membrane topology of the colicin E1 channel using genetically encoded fluorescence Biochemistry 50 2011 4830 4842
12. S.D. Zakharov, M. Lindeberg, Y. Griko, Z. Salamon, G. Tollin, F.G. Prendergast, and W.A. Cramer Membrane-bound state of the colicin E1 channel domain as an extended two-dimensional helical array Proc. Natl Acad. Sci. USA 95 1998 4282 4287
13. A.P. Todd, J. Cong, F. Levinthal, C. Levinthal, and W.L. Hubbell Site-directed mutagenesis of colicin E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation Proteins 6 1989 294 305
14. P.K. Kienker, X. Qiu, S.L. Slatin, A. Finkelstein, and K.S. Jakes Transmembrane insertion of the colicin Ia hydrophobic hairpin J. Membr. Biol. 157 1997 27 37
15. L. Prieto, and T. Lazaridis Computational studies of colicin insertion into membranes: the closed state Proteins 79 2011 126 141
16. D. Jeanteur, F. Pattus, and P.A. Timmins Membrane-bound form of the pore-forming domain of colicin A. A neutron scattering study J. Mol. Biol. 235 1994 898 907
17. D. Massotte, M. Yamamoto, S. Scianimanico, O. Sorokine, A. van Dorsselaer, and Y. Nakatani Structure of the membrane-bound form of the pore-forming domain of colicin A: a partial proteolysis and mass spectrometry study Biochemistry 32 1993 13787 13794
18. D. Duche, J. Izard, J.M. Gonzalez-Manas, M.W. Parker, M. Crest, M. Chartier, and D. Baty Membrane topology of the colicin A pore-forming domain analyzed by disulfide bond engineering J. Biol. Chem. 271 1996 15401 15406
19. M.K. Anton Savitsky, Denis Duche, Klaus Mobius, and Heinz-Jurgen Steinhoff Spontaneous refolding of the pore-forming colicin a toxin upon membrane association as studied by X-band and W-band high-field electron paramagnetic resonance spectroscopy J. Phys. Chem. B 108 2004 9541 9548
20. K. Mobius, A. Savitsky, C. Wegener, M. Plato, M. Fuchs, and A. Schnegg Combining high-field EPR with site-directed spin labeling reveals unique information on proteins in action Magn. Reson. Chem. 43 2005 S4 S19 Spec no
21. M.C. Tory, and A.R. Merrill Adventures in membrane protein topology. A study of the membrane-bound state of colicin E1 J. Biol. Chem. 274 1999 24539 24549
22. C. Aisenbrey, M. Cusan, S. Lambotte, P. Jasperse, J. Georgescu, U. Harzer, and B. Bechinger Specific isotope labeling of colicin E1 and B channel domains for membrane topological analysis by oriented solid-state NMR spectroscopy ChemBioChem 9 2008 944 951
23. J.O. Bullock Ion selectivity of colicin E1: modulation by pH and membrane composition J. Membr. Biol. 125 1992 255 271
24. S.L. Fridd, and J.H. Lakey Surface aspartate residues are essential for the stability of colicin A P-domain: a mechanism for the formation of an acidic molten-globule Biochemistry 41 2002 1579 1586
25. F.G. van der Goot, J.M. Gonzalez-Manas, J.H. Lakey, and F. Pattus A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A Nature 354 1991 408 410
26. F.G. van der Goot, J.H. Lakey, and F. Pattus The molten globule intermediate for protein insertion or translocation through membranes Trends Cell Biol. 2 1992 343 348
27. N. Poklar, J. Lah, M. Salobir, P. Macek, and G. Vesnaver pH and temperature-induced molten globule-like denatured states of equinatoxin II: a study by UV-melting, DSC, far- and near-UV CD spectroscopy, and ANS fluorescence Biochemistry 36 1997 14345 14352
28. L. Raymond, S.L. Slatin, and A. Finkelstein Channels formed by colicin E1 in planar lipid bilayers are large and exhibit pH-dependent ion selectivity J. Membr. Biol. 84 1985 173 181
29. F. Levinthal, A.P. Todd, W.L. Hubbell, and C. Levinthal A single tryptic fragment of colicin E1 can form an ion channel: stoichiometry confirms kinetics Proteins 11 1991 254 262
30. D.S. Cafiso, and W.L. Hubbell Estimation of transmembrane potentials from phase equilibria of hydrophobic paramagnetic ions Biochemistry 17 1978 187 195
31. Z. Guo, D. Cascio, K. Hideg, and W.L. Hubbell Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme Protein Sci. 17 2008 228 239
32. Z. Guo, D. Cascio, K. Hideg, T. Kalai, and W.L. Hubbell Structural determinants of nitroxide motion in spin-labeled proteins: tertiary contact and solvent-inaccessible sites in helix G of T4 lysozyme Protein Sci. 16 2007 1069 1086
33. H.S. McHaourab, T. Kalai, K. Hideg, and W.L. Hubbell Motion of spin-labeled side chains in T4 lysozyme: effect of side chain structure Biochemistry 38 1999 2947 2955
34. J.P. Klare, and H.J. Steinhoff Spin labeling EPR Photosynth. Res. 102 2009 377 390
35. H.J. Steinhoff Methods for study of protein dynamics and protein-protein interaction in protein-ubiquitination by electron paramagnetic resonance spectroscopy Front. Biosci. 7 2002 c97 c110
36. A. Mulgrew-Nesbitt, K. Diraviyam, J. Wang, S. Singh, P. Murray, and Z. Li The role of electrostatics in protein-membrane interactions Biochim. Biophys. Acta 1761 2006 812 826
37. A. Kyrychenko, M.V. Rodnin, Y.O. Posokhov, A. Holt, B. Pucci, J.A. Killian, and A.S. Ladokhin Thermodynamic measurements of bilayer insertion of a single transmembrane helix chaperoned by fluorinated surfactants J. Mol. Biol. 416 2012 328 334
38. A.S. Ladokhin, and S.H. White Protein chemistry at membrane interfaces: non-additivity of electrostatic and hydrophobic interactions J. Mol. Biol. 309 2001 543 552
39. S. Cohen, S. Albeck, E. Ben-Dov, R. Cahan, M. Firer, A. Zaritsky, and O. Dym Cyt1Aa toxin: crystal structure reveals implications for its membrane-perforating function J. Mol. Biol. 413 2011 804 814
40. S.D. Zakharov, and W.A. Cramer Insertion intermediates of pore-forming colicins in membrane two-dimensional space Biochimie 84 2002 465 475
41. S. Fanucchi, R.J. Adamson, and H.W. Dirr Formation of an unfolding intermediate state of soluble chloride intracellular channel protein CLIC1 at acidic pH Biochemistry 47 2008 11674 11681
42. J.M. Zhao, and L. E. Similarity of the conformation of diphtheria toxin at high temperature to that in the membrane-penetrating low-pH state Proc. Natl Acad. Sci. USA 83 1986 2002 2006
43. R.J. Collier Membrane translocation by anthrax toxin Mol. Aspects Med. 30 2009 413 422
44. V.E. Bychkova, R.H. Pain, and P. OB The 'molten globule' state is involved in the translocation of proteins across membranes? FEBS Lett. 238 1988 231 234
45. V.L. Davidson, K.R. Brunden, and W.A. Cramer 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 1985 1386 1390
46. J.M. Gonzalez-Manas, J.H. Lakey, and F. Pattus Interaction of the colicin-A pore-forming domain with negatively charged phospholipids Eur. J. Biochem. 211 1993 625 633
47. J.H. Lakey, D. Massotte, F. Heitz, J.L. Dasseux, J.F. Faucon, M.W. Parker, and F. Pattus Membrane insertion of the pore-forming domain of colicin A. A spectroscopic study Eur. J. Biochem. 196 1991 599 607
48. J.H. Lakey, J.M. Gonzalez-Manas, F.G. van der Goot, and F. Pattus The membrane insertion of colicins FEBS Lett. 307 1992 26 29
49. J.H. Lakey, D. Baty, and F. Pattus Fluorescence energy transfer distance measurements using site-directed single cysteine mutants. The membrane insertion of colicin A J. Mol. Biol. 218 1991 639 653
50. D. Duche, Y. Corda, V. Geli, and D. Baty Integration of the colicin A pore-forming domain into the cytoplasmic membrane of Escherichia coli J. Mol. Biol. 285 1999 1965 1975
51. M.C. Martinez, C. Lazdunski, and F. Pattus Isolation, molecular and functional properties of the C-terminal domain of colicin A EMBO J. 2 1983 1501 1507
52. H.-J. Steinhoff, A. Savitsky, C. Wegener, M. Pfeiffer, M. Plato, and K. Möbius High-field EPR studies of the structure and conformational changes of site-directed spin labeled bacteriorhodopsin Biochim. Biophys. Acta 1457 2000 253 262
53. Y.K. Shin, C. Levinthal, F. Levinthal, and W.L. Hubbell Colicin E1 binding to membranes: time-resolved studies of spin-labeled mutants Science 259 1993 960 963
54. S.D. Zakharov, J.B. Heymann, Y.L. Zhang, and W.A. Cramer Membrane binding of the colicin E1 channel: activity requires an electrostatic interaction of intermediate magnitude Biophys. J. 70 1996 2774 2783
55. A.A. Musse, and A.R. Merrill The molecular basis for the pH-activation mechanism in the channel-forming bacterial colicin E1 J. Biol. Chem. 278 2003 24491 24499
56. S.D. Zakharov, and W.A. Cramer Colicin crystal structures: pathways and mechanisms for colicin insertion into membranes Biochim. Biophys. Acta 1565 2002 333 346
57. P.A. Elkins, H.Y. Song, W.A. Cramer, and C.V. Stauffacher Crystallization and characterization of colicin E1 channel-forming polypeptides Proteins 19 1994 150 157
58. M. Lindeberg, S.D. Zakharov, and W.A. Cramer Unfolding pathway of the colicin E1 channel protein on a membrane surface J. Mol. Biol. 295 2000 679 692
59. B.M. Kroncke, P.S. Horanyi, and L. Columbus Structural origins of nitroxide side chain dynamics on membrane protein alpha-helical sites Biochemistry 49 2010 10045 10060
60. E. Cascales, S.K. Buchanan, D. Duche, C. Kleanthous, R. Lloubes, and K. Postle Colicin biology Microbiol. Mol. Biol. Rev. 71 2007 158 229
61. S. Morein, A. Andersson, L. Rilfors, and G. Lindblom Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures J. Biol. Chem. 271 1996 6801 6809
62. L. Salwinski, and W.L. Hubbell Structure in the channel forming domain of colicin E1 bound to membranes: the 402-424 sequence Protein Sci. 8 1999 562 572
63. D. Duche, M.W. Parker, J.M. Gonzalez-Manas, F. Pattus, and D. Baty Uncoupled steps of the colicin A pore formation demonstrated by disulfide bond engineering J. Biol. Chem. 269 1994 6332 6339
64. C. Altenbach, W. Froncisz, R. Hemker, H. Mchaourab, and W.L. Hubbell Accessibility of nitroxide side chains: absolute Heisenberg exchange rates from power saturation EPR Biophys. J. 89 2005 2103 2112
65. C. Altenbach, D.A. Greenhalgh, H.G. Khorana, and W.L. Hubbell A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin Proc. Natl Acad. Sci. USA 91 1994 1667 1671
66. N. Radzwill, K. Gerwert, and H.-J. Steinhoff Time-resolved detection of transient movement of helices F and G in doubly spin-labeled bacteriorhodopsin Biophys. J. 80 2001 2856 2866