MscL: channeling membrane tension

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 1, 2015, Pages 15-25

  Walton, Troy A ^a   Idigo, Chinenye A ^a   Herrera, Nadia ^a   Rees, Douglas C ^a,b  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bacterial channels; Hypo osmotic stress response; Mechanosensitive channels; Stretch activated channels; Turgor pressure

Indexed keywords

ESCHERICHIA COLI PROTEIN; ION CHANNEL; MSCL PROTEIN, E COLI;

CELL MEMBRANE; CHANNEL GATING; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; MECHANOTRANSDUCTION; MEMBRANE FLUIDITY; OSMOREGULATION; PHYSIOLOGY; POROSITY; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

CELL MEMBRANE; COMPUTER SIMULATION; ESCHERICHIA COLI PROTEINS; ION CHANNEL GATING; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MODELS, MOLECULAR; OSMOREGULATION; POROSITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84939874102     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1535-x     Document Type: Review

References (53)

1. Anishkin A, Gendel V, Sharifi NA, Chiang CS, Shirinian L, Guy HR, Sukharev S (2003) On the conformation of the COOH-terminal domain of the large mechanosensitive channel MscL. J Gen Physiol 121:227–244
2. Azem A, Shaked I, Rosenbusch JP, Daniel E (1995) Cross-linking of porin with glutardialdehyde: a test for the adequacy of premises of cross-linking theory. Biochim Biophys Acta 1243:151–156
3. Basle A, Iyer R, Delcour AH (2004) Subconductance states in OmpF gating. Biochim Biophys Acta 1664:100–107
4. Beckstein O, Tai K, Sansom MS (2004) Not ions alone: barriers to ion permeation in nanopores and channels. J Amer Chem Soc 126:14694–14695
5. Berrier C, Coulombe A, Houssin C, Ghazi A (1989) A patch-clamp study of ion channels of inner and outer membranes and of contact zones of E. coli, fused into giant liposomes. Pressure-activated channels are localized in the inner membrane. FEBS Lett 259:27–32
6. Blount P, Sukharev SI, Moe PC, Schroeder MJ, Guy HR, Kung C (1996) Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli. EMBO J 15:4798–4805
7. Blount P, Sukharev SI, Schroeder MJ, Nagle SK, 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
8. Booth IR, Louis P (1999) Managing hypoosmotic stress: aquaporins and mechanosensitive channels in Escherichia coli. Curr Opin Microbiol 2:166–169
9. Bosshard HR, Marti DN, Jelesarov I (2004) Protein stabilization by salt bridges: concepts, experimental approaches and clarification of some misunderstandings. J Mol Recogn 17:1–16
10. Chang G, Spencer RH, Lee AT, Barclay MT, Rees DC (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282:2220–2226
11. Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, Dubin AE, Patapoutian A (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330:55–60
12. Coste B, Xiao B, Santos JS, Syeda R, Grandl J, Spencer KS, Kim SE, Schmidt M, Mathur J, Dubin AE, Montal M, Patapoutian A (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483:176–181
13. Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP (1992) Crystal structures explain functional properties of two E. coli porins. Nature 358:727–733
14. Cruickshank CC, Minchin RF, Le Dain AC, Martinac B (1997) Estimation of the pore size of the large-conductance mechanosensitive ion channel of Escherichia coli. Biophys J 73:1925–1931
15. Dorwart MR, Wray R, Brautigam CA, Jiang Y, Blount P (2010) S. aureus MscL is a pentamer in vivo but of variable stoichiometries in vitro: implications for detergent-solubilized membrane proteins. PLoS Biol 8:e1000555
16. Folgering JH, Wolters JC, Poolman B (2005) Engineering covalent oligomers of the mechanosensitive channel of large conductance from Escherichia coli with native conductance and gating characteristics. Protein Sci 14:2947–2954
17. Gandhi CS, Walton TA, Rees DC (2011) OCAM: a new tool for studying the oligomeric diversity of MscL channels. Protein Sci 20:313–326
18. Gunasekar SK, Asnani M, Limbad C, Haghpanah JS, Hom W, Barra H, Nanda S, Lu M, Montclare JK (2009) N-terminal aliphatic residues dictate the structure, stability, assembly, and small molecule binding of the coiled-coil region of cartilage oligomeric matrix protein. Biochemistry 48:8559–8567
19. Hase CC, Le Dain AC, Martinac B (1995) Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 270:18329–18334
20. Hase CC, Minchin RF, Kloda A, Martinac B (1997) Cross-linking studies and membrane localization and assembly of radiolabelled large mechanosensitive ion channel (MscL) of Escherichia coli. Biochem Biophys Res Comm 232:777–782
21. Haswell ES, Meyerowitz EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr Biol 16:1–11
22. Hille B (1968) Pharmacological modifications of the sodium channels of frog nerve. J Gen Physiol 51:199–219
23. Iscla I, Wray R, Blount P (2011) The oligomeric state of the truncated mechanosensitive channel of large conductance shows no variance in vivo. Protein Sci 20:1638–1642
24. Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654
25. Kung C, Martinac B, Sukharev S (2010) Mechanosensitive channels in microbes. Ann Rev Microbiol 64:313–329
26. LeMasurier M, Heginbotham L, Miller C (2001) KcsA: it's a potassium channel. J Gen Physiol 118:303–314
27. Levina N, Totemeyer S, Stokes NR, Louis P, Jones MA, Booth IR (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
28. Liu Z, Gandhi CS, Rees DC (2009) Structure of a tetrameric MscL in an expanded intermediate state. Nature 461:120–124
29. Malashkevich VN, Kammerer RA, Efimov VP, Schulthess T, Engel J (1996) The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel? Science 274:761–765
30. Martinac B, Buechner M, Delcour AH, Adler J, Kung C (1987) Pressure-sensitive ion channel in Escherichia coli. Proc Natl Acad Sci U S A 84:2297–2301
31. Maurer JA, Dougherty DA (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
32. Mika JT, Birkner JP, Poolman B, Kocer A (2013) On the role of individual subunits in MscL gating: "all for one, one for all?". FASEB J 27:882–892
33. Moe PC, Blount P, Kung C (1998) Functional and structural conservation in the mechanosensitive channel MscL implicates elements crucial for mechanosensation. Mol Microbiol 28:583–592
34. Ornatska M, Jones SE, Naik RR, Stone MO, Tsukruk VV (2003) Biomolecular stress-sensitive gauges: surface-mediated immobilization of mechanosensitive membrane protein. J Amer Chem Soc 125:12722–12723
35. Ou X, Blount P, Hoffman RJ, 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
36. Perozo E, Cortes DM, Sompornpisut P, Kloda A, Martinac B (2002) Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature 418:942–948
37. Saint N, Lacapere JJ, Gu LQ, Ghazi A, Martinac B, Rigaud JL (1998) A hexameric transmembrane pore revealed by two-dimensional crystallization of the large mechanosensitive ion channel (MscL) of Escherichia coli. J Biol Chem 273:14667–14670
38. Schrempf H, Schmidt O, Kummerlen R, Hinnah S, Muller D, Betzler M, Steinkamp T, Wagner R (1995) A prokaryotic potassium ion channel with two predicted transmembrane segments from Streptomyces lividans. EMBO J 14:5170–5178
39. Spencer RH, Chang G, Rees DC (1999) 'Feeling the pressure': structural insights into a gated mechanosensitive channel. Curr Opin Struct Biol 9:448–454
40. Steinbacher S, Bass R, Strop P, Rees DC (2007) Structures of the prokaryotic mechanosensitive channels MscL and MscS. Curr Top Membr 58:1–24
41. Sukharev S, Betanzos M, Chiang CS, Guy HR (2001) The gating mechanism of the large mechanosensitive channel MscL. Nature 409:720–724
42. Sukharev S, Durell SR, Guy HR (2001) Structural models of the MscL gating mechanism. Biophys J 81:917–936
43. Sukharev SI, Martinac B, Arshavsky VY, Kung C (1993) Two types of mechanosensitive channels in the Escherichia coli cell envelope: solubilization and functional reconstitution. Biophysical J 65:177–183
44. Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C (1994) A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368:265–268
45. Sukharev SI, Blount P, Martinac B, Kung C (1997) Mechanosensitive channels of Escherichia coli: the MscL gene, protein, and activities. Ann Rev Physiol 59:633–657
46. Sukharev SI, Schroeder MJ, McCaslin DR (1999) Stoichiometry of the large conductance bacterial mechanosensitive channel of E. coli. A biochemical study. J Memb Biol 171:183–193
47. Sukharev SI, Sigurdson WJ, Kung C, Sachs F (1999) Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J Gen Physiol 113:525–540
48. van den Bogaart G, Krasnikov V, Poolman B (2007) Dual-color fluorescence-burst analysis to probe protein efflux through the mechanosensitive channel MscL. Biophys J 92:1233–1240
49. Walton TA, Rees DC (2013) Structure and stability of the C-terminal helical bundle of the E. coli mechanosensitive channel of large conductance. Protein Sci 22:1592–1601
50. Wang LC, Morgan LK, Godakumbura P, Kenney LJ, Anand GS (2012) The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. EMBO J 31:2648–2659
51. Wang Y, Liu Y, Deberg HA, Nomura T, Hoffman MT, Rohde PR, Schulten K, Martinac B, Selvin PR (2014) Single molecule FRET reveals pore size and opening mechanism of a mechano-sensitive ion channel. eLife 3:e01834
52. Yang LM, Wray R, Parker J, Wilson D, Duran RS, Blount P (2012) Three routes to modulate the pore size of the MscL channel/nanovalve. ACS Nano 6:1134–1141
53. Yoshimura K, Usukura J, Sokabe M (2008) Gating-associated conformational changes in the mechanosensitive channel MscL. Proc Natl Acad Sci U S A 105:4033–4038, d