2,2,2-Trifluoroethanol changes the transition kinetics and subunit interactions in the small bacterial mechanosensitive channel MscS

Biophysical Journal

Volumn 92, Issue 8, 2007, Pages 2771-2784

  Akitake, Bradley ^a   Spelbrink, Robin E J ^b   Anishkin, Andriy ^a   Killian, J Antoinette ^b   De Kruijff, Ben ^b   Sukharev, Sergei ^a  

^a Bldg 142   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; DODECYL SULFATE; ION CHANNEL; LITHIUM; PROTEIN SUBUNIT; SMALL CONDUCTANCE MECHANOSENSITIVE CHANNEL; TRIFLUOROETHANOL; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GEL ELECTROPHORESIS; NONHUMAN; OLIGOMERIZATION; PATCH CLAMP; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPHEROPLAST;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 34147178808     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.098715     Document Type: Article

References (54)

1. Hong, D. P., M. Hoshino, R. Kuboi, and Y. Goto. 1999. Clustering of fluorine-substituted alcohols as a factor responsible for their marked effects on proteins and peptides. J. Am. Chem. Soc. 121:8427-8433.
2. Nelson, J. W., and N. R. Kallenbach. 1986. Stabilization of the ribonuclease S-peptide α-helix by trifluoroethanol. Proteins. 1:211-217.
3. Sonnichsen, F. D., J. E. Van Eyk, R. S. Hodges, and B. D. Sykes. 1992. Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide. Biochemistry. 31:8790-8798.
4. Wienk, H. L., M. Czisch, and B. de Kruijff. 1999. The structural flexibility of the preferredoxin transit peptide. FEBS Lett. 453:318-326.
5. Jasanoff, A., and A. R. Fersht. 1994. Quantitative determination of helical propensities from trifluoroethanol titration curves. Biochemistry. 33:2129-2135.
6. Luo, P., and R. L. Baldwin. 1999. Interaction between water and polar groups of the helix backbone: an important determinant of helix propensities. Proc. Natl. Acad. Sci. USA. 96:4930-4935.
7. Lu, H., M. Buck, S. E. Radford, and C. M. Dobson. 1997. Acceleration of the folding of hen lysozyme by trifluoroethanol. J. Mol. Biol. 265:112-117.
8. Kumar, Y., S. Muzammil, and S. Tayyab. 2005. Influence of fluoro, chloro and alkyl alcohols on the folding pathway of human serum albumin. J. Biochem. (Tokyo). 138:335-341.
9. Chitra, R., and P. E. Smith. 2001. Properties of 2,2,2-trifluoroethanol and water mixtures. J. Chem. Phys. 114:426-435.
10. Cammers-Goodwin, A., T. J. Allen, S. L. Oslick, K. F. McClure, J. H. Lee, and D. S. Kemp. 1996. Mechanism of stabilization of helical conformations of polypeptides by water containing trifluoroethanol. J. Am. Chem. Soc. 118:3082-3090.
11. Kentsis, A., and T. R. Sosnick. 1998. Trifluoroethanol promotes helix formation by destabilizing backbone exposure: desolvation rather than native hydrogen bonding defines the kinetic pathway of dimeric coiled coil folding. Biochemistry. 37:14613-14622.
12. Bodkin, M. J., and J. M. Goodfellow. 1996. Hydrophobic solvation in aqueous trifluoroethanol solution. Biopolymers. 39:43-50.
13. Rajan, R., and P. Balaram. 1996. A model for the interaction of trifluoroethanol with peptides and proteins. Int. J. Pept. Protein Res. 48:328-336.
14. Reiersen, H., and A. R. Rees. 2000. Trifluoroethanol may form a solvent matrix for assisted hydrophobic interactions between peptide side chains. Protein Eng. 13:739-743.
15. Banerjee, T., and N. Kishore. 2005. Does the anesthetic 2,2,2-trifluoroethanol interact with bovine serum albumin by direct binding or by solvent-mediated effects? A calorimetric and spectroscopic investigation. Biopolymers. 78:78-86.
16. + channel (SKC1): oligomeric stoichiometry and stability. Biochemistry. 36:10343-10352.
17. van den Brink-van der Laan, V., J. Chupin, A. Killian, and B. de Kruijff. 2004. Stability of KcsA tetramer depends on membrane lateral pressure. Biochemistry. 43:4240-4250.
18. Barrera, F. N., M. L. Renart, M. L. Molina, J. A. Poveda, J. A. Encinar, A. M. Fernandez, J. L. Neira, and J. M. Gonzalez-Ros. 2005. Unfolding and refolding in vitro of a tetrameric, α-helical membrane protein: the prokaryotic potassium channel KcsA. Biochemistry. 44:14344-14352.
19. Deshusses, J. M., J. A. Burgess, A. Scherl, Y. Wenger, N. Walter, V. Converset, S. Paesano, G. L. Corthals, D. F. Hochstrasser, and J. C. Sanchez. 2003. Exploitation of specific properties of trifluoroethanol for extraction and separation of membrane proteins. Proteomics. 3:1418-1424.
20. Zuobi-Hasona, K., P. J. Crowley, A. Hasona, A. S. Bleiweis, and L. J. Brady. 2005. Solubilization of cellular membrane proteins from Streptococcus mutans for two-dimensional gel electrophoresis. Electrophoresis. 26:1200-1205.
21. Spelbrink, R. E., A. Kolkman, M. Slijper, J. A. Killian, and B. de Kruijff. 2005. Detection and identification of stable oligomeric protein complexes in Escherichia coli inner membranes: a proteomics approach. J. Biol. Chem. 280:28742-28748.
22. Levina, N., S. Totemeyer, N. R. Stokes, P. Louis, M. A. Jones, and I. R. Booth. 1999. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 18:1730-1737.
23. Sukharev, S. 2002. Purification of the small mechanosensitive channel of Escherichia coli (MscS): the subunit structure, conduction, and gating characteristics in liposomes. Biophys. J. 83:290-298.
24. Okada, K., P. C. Moe, and P. Blount. 2002. Functional design of bacterial mechanosensitive channels. Comparisons and contrasts illuminated by random mutagenesis. J. Biol. Chem. 277:27682-27688.
25. Koprowski, P., and A. Kubalski. 1998. Voltage-independent adaptation of mechanosensitive channels in Escherichia coli protoplasts. J. Membr. Biol. 164:253-262.
26. Akitake, B., A. Anishkin, and S. Sukharev. 2005. The "dashpot" mechanism of stretch-dependent gating in MscS. J. Gen. Physiol. 125:143-154.
27. Bass, R. B., P. Strop, M. Barclay, and D. C. Rees. 2002. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 298:1582-1587.
28. Edwards, M. D., Y. Li, S. Kim, S. Miller, W. Bartlett, S. Black, S. Dennison, I. Iscla, P. Blount, J. U. Bowie, and I. R. Booth. 2005. Pivotal role of the glycine-rich TM3 helix in gating the MscS mechanosensitive channel. Nat. Struct. Mol. Biol. 12:113-119.
29. Anishkin, A., and S. Sukharev. 2004. Water dynamics and dewetting transitions in the small mechanosensitive channel MscS. Biophys. J. 86:2883-2895.
30. Sotomayor, M., and K. Schulten. 2004. Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87:3050-3065.
31. Fraczkiewicz, R., and W. Braun. 1998. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19:319-333.
32. Eisenberg, D., E. Schwarz, M. Komaromy, and R. Wall. 1984. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179:125-142.
33. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
34. Kanjilal, S., N. Taulier, J. Y. Le Huerou, M. Gindre, W. Urbach, and M. Waks. 2003. Ultrasonic studies of alcohol-induced transconformation in β-lactoglobulin: the intermediate state. Biophys. J. 85:3928-3934.
35. Stenberg, F., P. Chovanec, S. L. Maslen, C. V. Robinson, L. L. Ilag, G. von Hippel, and D. O. Daley. 2005. Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 280:34409-34419.
36. Roccatano, D., G. Colombo, M. Fioroni, and A. E. Mark. 2002. Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc. Natl. Acad. Sci. USA. 99:12179-12184.
37. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365.
38. Popot, J. L., and D. M. Engelman. 2000. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:881-922.
39. Ozdirekcan, S., D. T. Rijkers, R. M. Liskamp, and J. A. Killian. 2005. Influence of flanking residues on tilt and rotation angles of transmembrane peptides in lipid bilayers. A solid-state 2H NMR study. Biochemistry. 44:1004-1012.
40. Strandberg, E., S. Ozdirekcan, D. T. Rijkers, P. C. van der Wel, R. E. Koeppe, R. M. Liskamp, and J. A. Killian. 2004. Tilt angles of transmembrane model peptides in oriented and nonoriented lipid bilayers as determined by 2H solid-state NMR. Biophys. J. 86:3709-3721.
41. Spronk, S. A., D. E. Elmore, and D. A. Dougherty. 2006. Voltage-dependent hydration and conduction properties of the hydrophobic pore of the mechanosensitive channel of small conductance. Biophys. J. 90:3555-3569.
42. Miller, S., M. D. Edwards, C. Ozdemir, and I. R. Booth. 2003. The closed structure of the MscS mechanosensitive channel. Cross-linking of single cysteine mutants. J. Biol. Chem. 278:32246-32250.
43. Edwards, M. D., I. R. Booth, and S. Miller. 2004. Gating the bacterial mechanosensitive channels: MscS a new paradigm? Curr. Opin. Microbiol. 7:163-167.
44. Barry, J. A., and K. Gawrisch. 1994. Direct NMR evidence for ethanol binding to the lipid-water interface of phospholipid bilayers. Biochemistry. 33:8082-8088.
45. Koenig, B. W., and K. Gawrisch. 2005. Lipid-ethanol interaction studied by NMR on bicelles. J. Phys. Chem. B. 109:7540-7547.
46. Sheetz, M. P., and S. J. Singer. 1974. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA. 71:4457-4461.
47. Heerklotz, H. 2001. Membrane stress and permeabilization induced by asymmetric incorporation of compounds. Biophys. J. 81:184-195.
48. Martinac, B., J. Adler, and C. Kung. 1990. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 348:261-263.
49. Perozo, E., A. Kloda, D. M. Cortes, and B. Martinac. 2002. Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9:696-703.
50. Schumann, U., M. D. Edwards, C. Li, and I. R. Booth. 2004. The conserved carboxy-terminus of the MscS mechanosensitive channel is not essential but increases stability and activity. FEBS Lett. 572:233-237.
51. Grajkowski, W., A. Kubalski, and P. Koprowski. 2005. Surface changes of the mechanosensitive channel MscS upon its activation, inactivation, and closing. Biophys. J. 88:3050-3059.
52. 81 in vertebrate calmodulin. Biophys. J. 81:2908-2918.
53. Main, E. R., and S. E. Jackson. 1999. Does trifluoroethanol affect folding pathways and can it be used as a probe of structure in transition states? Nat. Struct. Biol. 6:831-835.
54. Chitra, R., and P. E. Smith. 2001. A comparison of the properties of 2,2,2-trifluoroethanol and 2,2,2-trifluoroethanol/water mixtures using different force fields. J. Chem. Phys. 115:5521-5530.