The role of tryptophan residues in the function and stability of the mechanosensitive channel MscS from Escherichia coli

Biochemistry

Volumn 46, Issue 38, 2007, Pages 10899-10908

  Rasmussen, Akiko ^a   Rasmussen, Tim ^a   Edwards, Michelle D ^a   Schauer, Daniela ^a   Schumann, Ulrike ^a   Miller, Samantha ^a   Booth, Ian R ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MECHANOSENSITIVE CHANNELS; PHENYLALANINE; QUENCHING AGENTS; TRYPTOPHAN;

ESCHERICHIA COLI; FLUORESCENCE; MUTAGENESIS; OLIGOMERS; PROTEINS;

AMINO ACIDS;

BACTERIAL PROTEIN; PROTEIN MSCS; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CHANNEL GATING; ESCHERICHIA COLI; FLUORESCENCE; MEMBRANE CHANNEL; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; MODELS, CHEMICAL; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

ESCHERICHIA COLI;

EID: 34648828239     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701056k     Document Type: Article

References (37)

1. Burley, S. K., and Petsko, G. A. (1986) Amino-aromatic interactions in proteins, FEBS Lett. 203, 139-143.
2. Zacharias, N., and Dougherty, D. A. (2002) Cation-[pi] interactions in ligand recognition and catalysis, Trends Pharmacol. Sci. 23, 281-287.
3. Andersen, O. S., Greathouse, D. V., Providence, L. L., Becker, M. D., and Koeppe, R. E. (1998) Importance of Tryptophan Dipoles for Protein Function: 5-Fluorination of Tryptophans in Gramicidin A Channels, J. Am. Chem. Soc. 120, 5142-5146.
4. Killian, J. A., and von Heijne, G. (2000) How proteins adapt to a membrane-water interface, Trends Biochem. Sci. 25, 429-434.
5. Bogan, A. A., and Thorn, K. S. (1998) Anatomy of hot spots in protein interfaces, J. Mol. Biol. 280, 1-9.
6. Booth, I. R., Edwards, M. D., Black, S., Schumann, U., and Miller, S. (2007) Mechanosensitive channels in bacteria: signs of closure?, Nat. Rev. Microbiol. 5, 431-440.
7. Berrier, C., Coulombe, A., Szabo, I., Zoratti, M., and Ghazi, A. (1992) Gadolinium Ion Inhibits Loss of Metabolites Induced by Osmotic Shock and Large Stretch-Activated Channels in Bacteria, Eur. J. Biochem. 206, 559-565.
8. Levina, N., Totemeyer, S., Stokes, N. R., Louis, P., Jones, M. A., and Booth, I. R. (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.
9. Schleyer, M., Schmid, R., and Bakker, E. P. (1993) Transient, specific and extremely rapid release of osmolytes from growing cells of Escherichia coli K-12 exposed to hypoosmotic shock, Arch. Microbiol. 160, 424-431.
10. Berrier, C., Besnard, M., Ajouz, B., Coulombe, A., and Ghazi, A. (1996) Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J. Membr. Biol. 151, 175-187.
11. Li, Y., Moe, P. C., Chandrasekaran, S., Booth, I. R., and Blount, P. (2002) Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli, EMBO J. 21, 5323-5330.
12. Sukharev, S. I., Sigurdson, W. J., Kung, C., and Sachs, F. (1999) Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL, J. Gen. Physiol. 113, 525-540.
13. Chiang, C. S., Shirinian, L., and Sukharev, S. (2005) Capping transmembrane helices of MscL with aromatic residues changes channel response to membrane stretch, Biochemistry 44, 12589-12597.
14. Bass, R. B., Strop, P., Barclay, M., and Rees, D. C. (2002) Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel, Science 298, 1582-1587.
15. Steinbacher, S., Bass, R., Strop, P., and Rees, D. C. (2007) Structures of the Prokaryotic Mechanosensitive Channels MscL and MscS, Curr. Topics Membr. 58, 1-24.
16. Miller, S., Bartlett, W., Chandrasekaran, S., Simpson, S., Edwards, M., and Booth, I. R. (2003) Domain organization of the MscS mechanosensitive channel of Escherichia coli, EMBO J. 22, 36-46.
17. Booth, I. R., Edwards, M. D., Black, S., Schumann, U., Bartlett, W., Rasmussen, T., Rasmussen, A., and Miller, S. (2007) Physiological Analysis of Bacterial Mechanosensitive Channels, in Methods in Enzymology (Sies, M., and Haeussinger, D., Eds.) pp 47-61, Elsevier, New York.
18. Schumann, U., Edwards, M. D., Li, C., and Booth, I. R. (2004) The conserved carboxy-terminus of the MscS mechanosensitive channel is not essential but increases stability and activity, FEBS Lett. 572, 233-237.
19. Edwards, M. D., Li, Y., Kim, S., Miller, S., Bartlett, W., Black, S., Dennison, S., Iscla, I., Blount, P., Bowie, J. U., and Booth, I. R. (2005) Pivotal role of the glycine-rich TM3 helix in gating the MscS mechanosensitive channel, Nat. Struct. Mol. Biol. 12, 113-119.
20. Vasquez, V., Cortes, D. M., Furukawa, H., and Perozo, E. (2007) An Optimized Purification and Reconstitution Method for the MscS Channel: Strategies for Spectroscopical Analysis, Biochemistry 46, 6766-6773.
21. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
22. Kirby, E. P., and Steiner, R. F. (1970) The tryptophan microenvironments in apomyoglobin, J. Biol. Chem. 245, 6300-6306.
23. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res. 25, 3389-3402.
24. Blount, P., Sukharev, S. I., Schroeder, M. J., Nagle, S. K., and Kung, C. (1996) Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli, Proc. Natl. Acad. Sci.U.S.A. 93, 11652-11657.
25. Blount, P., Schroeder, M. J., and Kung, C. (1997) Mutations in a bacterial mechanosensitive channel change the cellular response to osmotic stress, J. Biol. Chem. 272, 32150-32157.
26. Ou, X., Blount, P., Hoffman, R. J., and Kung, C. (1998) One face of a transmembrane helix is crucial in mechanosensitive channel gating, Proc. Natl. Acad. Sci. U.S.A. 95, 11471-11475.
27. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H., and Poolman, B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation, J. Mol. Biol. 317, 591-600.
28. Callis, P. R., and Liu, T. (2004) Quantitative prediction of fluorescence quantum yields for tryptophan in proteins, J. Phys. Chem. B 108, 4248-4259.
29. Eftink, M. R. (1991) Fluorescence techniques for studying protein structure, Methods Biochem. Anal. 35, 127-205.
30. Stryer, L., and Haugland, R. P. (1967) Energy Transfer: A Spectroscopic Ruler, PNAS 58, 719-726.
31. Miller, S., Edwards, M. D., Ozdemir, C., and Booth, I. R. (2003) The closed structure of the MscS mechanosensitive channel - Cross-linking of single cysteine mutants, J. Biol. Chem. 278, 32246-32250.
32. Kadokura, H., Katzen, F., and Beckwith, J. (2003) Protein disulfide bond formation in prokaryotes, Annu. Rev. Biochem. 72, 111-135.
33. Gallivan, J. P., and Dougherty, D. A. (1999) Cation-pi interactions in structural biology, PNAS 96, 9459-9464.
34. Clackson, T., and Wells, J. A. (1995) A hot spot of binding energy in a hormone-receptor interface, Science 267, 383-386.
35. Powl, A. M., Carney, J., Marius, P., East, J. M., and Lee, A. G. (2005) Lipid interactions with bacterial channels: fluorescence studies, Biochem. Soc. Trans. 33, 905-909.
36. Powl, A. M., East, J. M., and Lee, A. G. (2003) Lipid-protein interactions studied by introduction of a tryptophan residue: The mechanosensitive channel MscL, Biochemistry 42, 14306-14317.
37. Powl, A. M., East, J. M., and Lee, A. G. (2005) Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation, Biochemistry 44, 5873-5883.