Disulfide trapping the mechanosensitive channel MscL into a gating-transition state

Biophysical Journal

Volumn 92, Issue 4, 2007, Pages 1224-1232

  Iscla, Irene ^a   Levin, Gal ^a,b   Wray, Robin ^a   Blount, Paul ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; ESCHERICHIA COLI PROTEIN; ION CHANNEL; MECHANOSENSITIVE CHANNEL PROTEIN OF LARGE CONDUCTANCE; UNCLASSIFIED DRUG;

ARTICLE; CHANNEL GATING; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTROPHYSIOLOGY; ESCHERICHIA COLI; NONHUMAN; OXIDATION; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

EID: 33846849245     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.090316     Document Type: Article

References (38)

1. + channels in adult rat atrial myocytes. Prog. Biophys. Mol. Biol. 82:121-135.
2. Tan, J., W. Liu, and D. Saint. 2004. Differential expression of the mechanosensitive potassium channel TREK-1 in epicardial and endocardial myocytes in rat ventricle. Exp. Physiol. 89:237-242.
3. Terrenoire, C., I. Lauritzen, F. Lesage, G. Romey, and M. Lazdunski. 2001. A TREK-1-like potassium channel in atrial cells inhibited by b-adrenergic stimulation and activated by volatile anesthetics. Circ. Res. 89:336-342.
4. Hamill, O. P., and B. Martinac. 2001. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685-740.
5. Sukharev, S., and D. P. Corey. 2004. Mechanosensitive channels: multiplicity of families and gating paradigms. Sci. STKE. 2004:re4.
6. Berrier, C., M. Besnard, B. Ajouz, A. Coulombe, and A. Ghazi. 1996. Multiple mechanosensitive ion channels from Escherichia coli, activated at different thresholds of applied pressure. J. Membr. Biol. 151:175-187.
7. Li, Y., P. C. Moe, S. Chandrasekaran, I. R. Booth, and P. Blount. 2002. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J. 21:5323-5330.
8. McLaggan, D., M. A. Jones, G. Gouesbet, N. Levina, S. Lindey, W. Epstein, and I. R. Booth. 2002. Analysis of the kefA2 mutation suggests that KefA is a cation-specific channel involved in osmotic adaptation in Escherichia coli. Mol. Microbiol. 43:521-536.
9. 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.
10. Sukharev, S. I., P. Blount, B. Martinac, F. R. Blattner, and C. Kung. 1994. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 368:265-268.
11. Blount, P., S. I. Sukharev, P. C. Moe, M. J. Schroeder, H. R. Guy, and C. Kung. 1996. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J. 15:4798-4805.
12. Blount, P., and P. Moe. 1999. Bacterial mechanosensitive channels: integrating physiology, structure and function. Trends Microbiol. 7:420-424.
13. Yoshimura, K., A. Batiza, M. Schroeder, P. Blount, and C. Kung. 1999. Hydrophilicity of a single residue within MscL correlates with increased channel mechanosensitivity. Biophys. J. 77:1960-1972.
14. Chang, G., R. H. Spencer, A. T. Lee, M. T. Barclay, and D. C. Rees. 1998. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science. 282:2220-2226.
15. Sukharev, S., M. Betanzos, C. Chiang, and H. Guy. 2001. The gating mechanism of the large mechanosensitive channel MscL. Nature. 409:720-724.
16. Sukharev, S., S. Durell, and H. Guy. 2001. Structural models of the MscL gating mechanism. Biophys. J. 81:917-936.
17. Perozo, E., D. M. Cortes, P. Sompornpisut, A. Kloda, and B. Martinac. 2002. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 418:942-948.
18. Bartlett, J. L., G. Levin, and P. Blount. 2004. An in vivo assay identifies changes in residue accessibility on mechanosensitive channel gating. Proc. Natl. Acad. Sci. USA. 101:10161-10165.
19. Blount, P., S. I. Sukharev, M. J. Schroeder, S. K. Nagle, and C. Kung. 1996. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc. Natl. Acad. Sci. USA. 93:11652-11657.
20. Ou, X., P. Blount, R. J. Hoffman, and C. Kung. 1998. One face of a transmembrane helix is crucial in mechanosensitive channel gating. Proc. Natl. Acad. Sci. USA. 95:11471-11475.
21. Kumánovics, A., G. Levin, and P. Blount. 2002. Family ties of gated pores: evolution of the sensor module. FASEB J. 16:1623-1629.
22. Levin, G., and P. Blount. 2004. Cysteine scanning of MscL transmembrane domains reveals residues critical for mechanosensitive channel gating. Biophys. J. 86:2862-2870.
23. Moe, P. C., G. Levin, and P. Blount. 2000. Correlating a protein structure with function of a bacterial mechanosensitive channel. J. Biol. Chem. 275:31121-31127.
24. Norman, C., Z. W. Liu, P. Rigby, A. Raso, Y. Petrov, and B. Martinac. 2005. Visualisation of the mechanosensitive channel of large conductance in bacteria using confocal microscopy. Eur. Biophys. J. 34:396-402.
25. Blount, P., S. I. Sukharev, P. C. Moe, B. Martinac, and C. Kung. 1999. Mechanosensitive channels of bacteria. In Methods in Enzymology. P. M. Conn, editor. Academic Press, San Diego, CA. 458-482.
26. Maurer, J. A., and D. A. Dougherty. 2003. Generation and evaluation of a large mutational library from the Escherichia coli mechanosensitive channel of large conductance, MscL: implications for channel gating and evolutionary design. J. Biol. Chem. 278:21076-21082.
27. Ajouz, B., C. Berrier, A. Garrigues, M. Besnard, and A. Ghazi. 1998. Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J. Biol. Chem. 273:26670-26674.
28. Batiza, A. F., M. M. Kuo, K. Yoshimura, and C. Kung. 2002. Gating the bacterial mechanosensitive channel MscL in vivo. Proc. Natl. Acad. Sci. USA. 99:5643-5648.
29. Shapovalov, G., R. Bass, D. C. Rees, and H. A. Lester. 2003. Open-state disulfide crosslinking between mycobacterium tuberculosis mechanosensitive channel subunits. Biophys. J. 84:2357-2365.
30. Falke, J. J., A. F. Dernburg, D. A. Sternberg, N. Zalkin, D. L. Milligan, and D. E. Koshland Jr. 1988. Structure of a bacterial sensory receptor. A site-directed sulfhydryl study. J. Biol. Chem. 263:14850-14858.
31. Srinivasan, N., R. Sowdhamini, C. Ramakrishnan, and P. Balaram. 1990. Conformations of disulfide bridges in proteins. Int. J. Pept. Protein Res. 36:147-155.
32. Perozo, E., A. Kloda, D. M. Cortes, and B. Martinac. 2001. Site-directed spin-labeling analysis of reconstituted Mscl in the closed state. J. Gen. Physiol. 118:193-206.
33. Iscla, I., G. Levin, R. Wray, R. Reynolds, and P. Blount. 2004. Defining the physical gate of a mechanosensitive channel, MscL, by engineering metal-binding sites. Biophys. J. 87:3172-3180.
34. Holmgren, M., K. S. Shin, and G. Yellen. 1998. The activation gate of a voltage-gated K+ channel can be trapped in the open state by an intersubunit metal bridge. Neuron. 21:617-621.
35. + channel. Neuron. 19:175-184.
36. Rothberg, B. S., K. S. Shin, P. S. Phale, and G. Yellen. 2002. Voltage-controlled gating at the intracellular entrance to a hyperpolarization-activated cation channel. J. Gen. Physiol. 119:83-91.
37. Rothberg, B. S., K. S. Shin, and G. Yellen. 2003. Movements near the gate of a hyperpolarization-activated cation channel. J. Gen. Physiol. 122:501-510.
38. Webster, S. M., D. del Camino, J. P. Dekker, and G. Yellen. 2004. Intracellular gate opening in Shaker K+ channels defined by high-affinity metal bridges. Nature. 428:864-868.