Chimeras Reveal a Single Lipid-Interface Residue that Controls MscL Channel Kinetics as well as Mechanosensitivity

Cell Reports

Volumn 3, Issue 2, 2013, Pages 520-527

  Yang, Li Min ^a   Zhong, Dalian ^a   Blount, Paul ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ION CHANNEL; LIPID; MS CHANNEL OF LARGE CONDUCTANCE; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; CELL MEMBRANE; CHANNEL GATING; CHIMERA; CONTROLLED STUDY; CYTOPLASM; ENZYME KINETICS; ESCHERICHIA COLI; HYDROPHOBICITY; HYSTERESIS; LIPID ANALYSIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; STAPHYLOCOCCUS AUREUS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; DNA MUTATIONAL ANALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ION CHANNEL GATING; ION CHANNELS; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PERIPLASM; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

EID: 84874238162     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.01.018     Document Type: Article

References (38)

1. Ajouz B., Berrier C., Besnard M., Martinac B., Ghazi A. Contributions of the different extramembranous domains of the mechanosensitive ion channel MscL to its response to membrane tension. J. Biol. Chem. 2000, 275:1015-1022.
2. Balleza D., Gómez-Lagunas F. Conserved motifs in mechanosensitive channels MscL and MscS. Eur. Biophys. J. 2009, 38:1013-1027.
3. Blount P., Krause J.E. Functional nonequivalence of structurally homologous domains of neurokinin-1 and neurokinin-2 type tachykinin receptors. J. Biol. Chem. 1993, 268:16388-16395.
4. Blount P., Moe P.C. Bacterial mechanosensitive channels: integrating physiology, structure and function. Trends Microbiol. 1999, 7:420-424.
5. Blount P., Sukharev S.I., Moe P.C., Schroeder M.J., Guy H.R., Kung C. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J. 1996, 15:4798-4805.
6. Blount P., Sukharev S.I., Schroeder M.J., Nagle S.K., Kung C. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli. Proc. Natl. Acad. Sci. USA 1996, 93:11652-11657.
7. Blount P., Sukharev S.I., Moe P.C., Martinac B., Kung C. Mechanosensitive channels of bacteria. Meth Enzymol 1999, 458-482. Academic Press, San Diego, CA. P.M. Conn (Ed.).
8. Blount P., Iscla I., Moe P.C., Li Y. MscL: the bacterial mechanosensitive channel of large conductance. Mechanosensitive Ion Channels (a volume in the Current Topics in Membranes series) 2007, 202-233. Elsievier Press, St. Louis, MO. O.P. Hamill (Ed.).
9. Blount P., Iscla I., Li Y. Mechanosensitive channels and sensing osmotic stimuli in bacteria. Sensing with Ion Channels 2008, 25-47. Springer-Verlag Press, Berlin. B. Martinac (Ed.).
10. Blount P., Li Y., Moe P.C., Iscla I. Mechanosensitive channels gated by membrane tension: bacteria and beyond. Mechanosensitive Ion Channels (a volume in the Mechanosensitivity in Cells and Tissues, Moscow Academia series) 2008, 71-101. Springer Press, New York. A. Kamkin, I. Kiseleva (Eds.).
11. Booth I.R., Blount P. The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J. Bacteriol. 2012, 194:4802-4809.
12. Chang G., Spencer R.H., Lee A.T., Barclay M.T., Rees D.C. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 1998, 282:2220-2226.
13. Cruickshank C.C., Minchin R.F., Le Dain A.C., Martinac B. Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys. J. 1997, 73:1925-1931.
14. Deplazes E., Louhivuori M., Jayatilaka D., Marrink S.J., Corry B. Structural investigation of MscL gating using experimental data and coarse grained MD simulations. PLoS Comput. Biol. 2012, 8:e1002683.
15. Dorwart M.R., Wray R., Brautigam C.A., Jiang Y., Blount P. S. aureus MscL is a pentamer in vivo but of variable stoichiometries in vitro: implications for detergent-solubilized membrane proteins. PLoS Biol. 2010, 8:e1000555.
16. Doyle D.A., Morais Cabral J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., Chait B.T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280:69-77.
17. Folgering J.H., Moe P.C., Schuurman-Wolters G.K., Blount P., Poolman B. Lactococcus lactis uses MscL as its principal mechanosensitive channel. J. Biol. Chem. 2005, 280:8784-8792.
18. Innis M.A., Gelfand D.H., Sninsky J.J., White T.J. PCR Protocols. A Guide to Methods and Applications 1990, Academic Press, Inc., San Diego.
19. Iscla I., Wray R., Blount P. The oligomeric state of the truncated mechanosensitive channel of large conductance shows no variance in vivo. Protein Sci. 2011, 20:1638-1642.
20. Jeon J., Voth G.A. Gating of the mechanosensitive channel protein MscL: the interplay of membrane and protein. Biophys. J. 2008, 94:3497-3511.
21. Kamaraju K., Gottlieb P.A., Sachs F., Sukharev S. Effects of GsMTx4 on bacterial mechanosensitive channels in inside-out patches from giant spheroplasts. Biophys. J. 2010, 99:2870-2878.
22. Levin G., Blount P. Cysteine scanning of MscL transmembrane domains reveals residues critical for mechanosensitive channel gating. Biophys. J. 2004, 86:2862-2870.
23. Levina N., Tötemeyer S., Stokes N.R., Louis P., Jones M.A., Booth I.R. 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. 1999, 18:1730-1737.
24. Liu Z., Gandhi C.S., Rees D.C. Structure of a tetrameric MscL in an expanded intermediate state. Nature 2009, 461:120-124.
25. Martinac B., Buechner M., Delcour A.H., Adler J., Kung C. Pressure-sensitive ion channel in Escherichia coli. Proc. Natl. Acad. Sci. USA 1987, 84:2297-2301.
26. Maurer J.A., Dougherty D.A. 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. 2003, 278:21076-21082.
27. Maurer J.A., Elmore D.E., Lester H.A., Dougherty D.A. Comparing and contrasting Escherichia coli and Mycobacterium tuberculosis mechanosensitive channels (MscL). New gain of function mutations in the loop region. J. Biol. Chem. 2000, 275:22238-22244.
28. Moe P.C., Blount P., Kung C. Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol. Microbiol. 1998, 28:583-592.
29. Moe P.C., Levin G., Blount P. Correlating a protein structure with function of a bacterial mechanosensitive channel. J. Biol. Chem. 2000, 275:31121-31127.
30. Ou X., Blount P., Hoffman R.J., Kung C. One face of a transmembrane helix is crucial in mechanosensitive channel gating. Proc. Natl. Acad. Sci. USA 1998, 95:11471-11475.
31. Park K.H., Berrier C., Martinac B., Ghazi A. Purification and functional reconstitution of N- and C-halves of the MscL channel. Biophys. J. 2004, 86:2129-2136.
32. Pivetti C.D., Yen M.R., Miller S., Busch W., Tseng Y.H., Booth I.R., Saier M.H. Two families of mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 2003, 67:66-85.
33. Sawada Y., Murase M., Sokabe M. The gating mechanism of the bacterial mechanosensitive channel MscL revealed by molecular dynamics simulations: from tension sensing to channel opening. Channels (Austin) 2012, 6:317-331.
34. Steinbacher S., Bass R., Strop P., Rees D.C. Structures of the prokaryotic mechanosensitive channels MscL and MscS. Mechanosensitive Ion Channels (a volume in the Current Topics in Membranes series) 2007, 1-20. Elsievier Press, St. Louis, MO. O.P. Hamill (Ed.).
35. Su Z., Zhou X., Haynes W.J., Loukin S.H., Anishkin A., Saimi Y., Kung C. Yeast gain-of-function mutations reveal structure-function relationships conserved among different subfamilies of transient receptor potential channels. Proc. Natl. Acad. Sci. USA 2007, 104:19607-19612.
36. Tsai I.J., Liu Z.W., Rayment J., Norman C., McKinley A., Martinac B. The role of the periplasmic loop residue glutamine 65 for MscL mechanosensitivity. Eur. Biophys. J. 2005, 34:403-412.
37. Yoshimura K., Batiza A., Schroeder M., Blount P., Kung C. Hydrophilicity of a single residue within MscL correlates with increased channel mechanosensitivity. Biophys. J. 1999, 77:1960-1972.
38. Zhou X., Su Z., Anishkin A., Haynes W.J., Friske E.M., Loukin S.H., Kung C., Saimi Y. Yeast screens show aromatic residues at the end of the sixth helix anchor transient receptor potential channel gate. Proc. Natl. Acad. Sci. USA 2007, 104:15555-15559.