PH-triggered conformational switching of the diphtheria toxin T-domain: The roles of N-terminal histidines

Journal of Molecular Biology

Volumn 425, Issue 15, 2013, Pages 2752-2764

  Kurnikov, Igor V ^a   Kyrychenko, Alexander ^b   Flores Canales, Jose C ^a   Rodnin, Mykola V ^b   Simakov, Nikolay ^c   Vargas Uribe, Mauricio ^b   Posokhov, Yevgen O ^b   Kurnikova, Maria ^a   Ladokhin, Alexey S ^b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

acid induced conformational; change membrane protein insertion; fluorescence; histidine protonation; molecular dynamics

Indexed keywords

DIPHTHERIA TOXIN; HISTIDINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROPHOBICITY; MOLECULAR DYNAMICS; MUTAGENESIS; PH; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING; PROTON TRANSPORT; STATIC ELECTRICITY;

EID: 84879946745     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.04.030     Document Type: Article

References (54)

1. X.I. Ambroggio, and B. Kuhlman Design of protein conformational switches Curr. Opin. Struct. Biol. 16 2006 525 530
2. D.H. Hoch, M. Romero-Mira, B.E. Ehrlich, A. Finkelstein, B.R. DasGupta, and L.L. Simpson Channels formed by botulinum, tetanus, and diphtheria toxins in planar lipid bilayers: relevance to translocation of proteins Proc. Natl Acad. Sci. USA 82 1985 1692 1696
3. 2-terminal region across planar bilayers J. Gen. Physiol. 112 1998 317 324
4. S.S. Arnon, R. Schechter, T.V. Inglesby, D.A. Henderson, J.G. Bartlett, and M.S. Ascher Botulinum toxin as a biological weapon: medical and public health management JAMA, J. Am. Med. Assoc. 285 2001 1059 1070
5. E.A. Neale Moving across membranes Nat. Struct. Biol. 10 2003 2 3
6. L.K. Koriazova, and M. Montal Translocation of botulinum neurotoxin light chain protease through the heavy chain channel Nat. Struct. Biol. 10 2003 13 18
7. R.J. Collier, and J.A. Young Anthrax toxin Annu. Rev. Cell Dev. Biol. 19 2003 45 70
8. T. Kampmann, D.S. Mueller, A.E. Mark, P.R. Young, and B. Kobe The role of histidine residues in low-pH-mediated viral membrane fusion Structure 14 2006 1481 1487
9. Z.L. Qin, Y. Zheng, and M. Kielian Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein J. Virol. 83 2009 4670 4677
10. Y.T. Hsu, K.G. Wolter, and R.J. Youle Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis Proc. Natl Acad. Sci. USA 94 1997 3668 3672
11. A. Antignani, and R.J. Youle How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18 2006 685 689
12. R.J. Youle, and A. Strasser The BCL-2 protein family: opposing activities that mediate cell death Nat. Rev., Mol. Cell Biol. 9 2008 47 59
13. D.E. Shaw, K.J. Bowers, E. Chow, M.P. Eastwood, D.J. Ierardi, and J.L. Klepeis Millisecond-scale molecular dynamics simulations on Anton Proceedings of the Conference on High Performance Computing Networking, Storage and Analysis - SC '09 2009 ACM Press New York, NY 1
14. Shaw, D. E., Chao, J. C., Eastwood, M. P., Gagliardo, J., Grossman, J. P., Ho, C. R., et al. (2007). Anton, a special-purpose machine for molecular dynamics simulation. ACM SIGARCH Computer Architecture News 35, pp. 1-12.
15. K.J. Oh, L. Senzel, R.J. Collier, and A. Finkelstein Translocation of the catalytic domain of diphtheria toxin across planar phospholipid bilayers by its own T domain Proc. Natl Acad. Sci. USA 96 1999 8467 8470
16. M.J. Bennett, and D. Eisenberg Refined structure of monomeric diphtheria toxin at 2.3 Å resolution Protein Sci. 3 1994 1464 1475
17. K.J. Oh, H. Zhan, C. Cui, K. Hideg, R.J. Collier, and W.L. Hubbell Organization of diphtheria toxin T domain in bilayers: a site-directed spin labeling study Science 273 1996 810 812
18. K. Kachel, J.H. Ren, R.J. Collier, and E. London Identifying transmembrane states and defining the membrane insertion boundaries of hydrophobic helices in membrane-inserted diphtheria toxin T domain J. Biol. Chem. 273 1998 22950 22956
19. L. Senzel, M. Gordon, R.O. Blaustein, K.J. Oh, R.J. Collier, and A. Finkelstein Topography of diphtheria toxin's T domain in the open channel state J. Gen. Physiol. 115 2000 421 434
20. A. Kyrychenko, Y.O. Posokhov, M.V. Rodnin, and A.S. Ladokhin Kinetic intermediate reveals staggered pH-dependent transitions along the membrane insertion pathway of the diphtheria toxin T-domain Biochemistry 48 2009 7584 7594
21. A. Perier, A. Chassaing, S. Raffestin, S. Pichard, M. Masella, and A. Menez Concerted protonation of key histidines triggers membrane interaction of the diphtheria toxin T domain J. Biol. Chem. 282 2007 24239 24245
22. M.V. Rodnin, A. Kyrychenko, P. Kienker, O. Sharma, Y.O. Posokhov, and R.J. Collier Conformational switching of the diphtheria toxin T domain J. Mol. Biol. 402 2010 1 7
23. M.V. Rodnin, A. Kyrychenko, P. Kienker, O. Sharma, M. Vargas-Uribe, and R.J. Collier Replacement of C-terminal histidines uncouples membrane insertion and translocation in diphtheria toxin T-domain Biophys. J. 101 2011 L41 L43
24. A. Nicholls, and B. Honig A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation J. Comput. Chem. 12 1991 435 445
25. as in proteins Proteins 15 1993 252 265
26. I.V. Kurnikov, M.A. Ratner, and A.A. Pacheco Redox equilibria in hydroxylamine oxidoreductase. Electrostatic control of electron redistribution in multielectron oxidative processes. Biochemistry 44 2005 1856 1863
27. I.V. Kurnikov, N Simakov, K Speranskiy, and M.G. Kurnikova HARLEM, Molecular Modeling Package 1997-2012 http://harlemprog.org/
28. S.S. Palchevskyy, Y.O. Posokhov, B. Olivier, J.L. Popot, B. Pucci, and A.S. Ladokhin Chaperoning of insertion of membrane proteins into lipid bilayers by hemifluorinated surfactants: application to diphtheria toxin Biochemistry 45 2006 2629 2635
29. M.V. Rodnin, Y.O. Posokhov, C. Contino-Pepin, J. Brettmann, A. Kyrychenko, and S.S. Palchevskyy Interactions of fluorinated surfactants with diphtheria toxin T-domain: testing new media for studies of membrane proteins Biophys. J. 94 2008 4348 4357
30. A.S. Ladokhin, and S.H. White Folding of amphipathic α-helices on membranes: energetics of helix formation by melittin J. Mol. Biol. 285 1999 1363 1369
31. S.E. Mansoor, H.S. Mchaourab, and D.L. Farrens Mapping proximity within proteins using fluorescence spectroscopy. A study of T4 lysozyme showing that tryptophan residues quench bimane fluorescence Biochemistry 41 2002 2475 2484
32. T. Mamonova, M.J. Yonkunas, and M.G. Kurnikova Energetics of the cleft closing transition and the role of electrostatic interactions in conformational rearrangements of the glutamate receptor ligand binding domain Biochemistry 47 2008 11077 11085
33. A. Nicholls, K.A. Sharp, and B. Honig Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons Proteins 11 1991 281 296
34. D. Sitkoff, K.A. Sharp, and B. Honig Accurate calculation of hydration free energies using macroscopic solvent models J. Phys. Chem. 98 1994 1978 1988
35. R.F. Murphy, S. Powers, and C.R. Cantor Endosome pH measured in single cells by dual fluorescence flow cytometry: rapid acidification of insulin to pH 6 J. Cell Biol. 98 1984 1757 1762
36. D.J. Yamashiro, and F.R. Maxfield Kinetics of endosome acidification in mutant and wild-type Chinese hamster ovary cells J. Cell Biol. 105 1987 2713 2721
37. J. Huotari, and A. Helenius Endosome maturation EMBO J. 30 2011 3481 3500
38. L.T. Dang, A.R. Purvis, R.H. Huang, L.A. Westfield, and J.E. Sadler Phylogenetic and functional analysis of histidine residues essential for pH-dependent multimerization of von Willebrand factor J. Biol. Chem. 286 2011 25763 25769
39. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
40. M. Vihinen, E. Torkkila, and P. Riikonen Accuracy of protein flexibility predictions Proteins 19 1994 141 149
41. Steere, B. (2001). Characterization of high-order oligomerization and energetics in diptheria toxin, PhD Thesis, University of California, Los Angeles.
42. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
43. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725
44. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
45. Case, D. A., Darden, T. A., Cheatham III, T. E., Simmerling, C. L., Wang, J., Duke, R. E., et al. (2006). AMBER 9, University of California, San Francisco.
46. J.-P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1977 327 341
47. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, A. DiNola, and J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
48. R.W. Pastor, B.R. Brooks, and A. Szabo An analysis of the accuracy of Langevin and molecular dynamics algorithms Mol. Phys. 65 1988 1409 1419
49. Y. Shan, J.L. Klepeis, M.P. Eastwood, R.O. Dror, and D.E. Shaw Gaussian split Ewald: a fast Ewald mesh method for molecular simulation J. Chem. Phys. 122 2005 054101
50. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graphics 14 1996 33 38
51. D.A. Case, T.A. Darden, T.E. Cheatham III, C. Simmerling, J. Wang, and R.E. Duke AMBER 11, University of California 2010 University of California, San Francisco San Francisco, CA
52. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded geometrical feature Biopolymers 22 1983 2577 2637
53. W.D. Cornell, P. Cieplak, C.I. Bayly, I.R. Gould, K.M. Merz, and D.M. Ferguson A second generation force field for the simulation of proteins, nucleic acids, and organic molecules J. Am. Chem. Soc. 117 1995 5179 5197
54. D. Bashford, and M. Karplus Multiple-site titration curves of proteins: an analysis of exact and approximate methods for their calculation J. Phys. Chem. 95 1991 9556 9561