Electrophysiological characterization of uncoupled mutants of lacy

Biochemistry

Volumn 52, Issue 46, 2013, Pages 8261-8266

  Gaiko, Olga ^a   Bazzone, Andre ^c   Fendler, Klaus ^c   Ronald Kaback, H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGED RESIDUES; LACTOSE PERMEASE; PROTEOLIPOSOMES; RAPID REACTIONS; RATE LIMITING; SUGAR BINDING; SYMPORTS; WILD TYPES;

ESCHERICHIA COLI;

ELECTROPHYSIOLOGY;

ARGININE; GLUTAMIC ACID; HISTONE; LACTOSE PERMEASE; PROTEOLIPOSOME; SUGAR; TYROSINE;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRIC ACTIVITY; ELECTROPHYSIOLOGY; ESCHERICHIA COLI; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTON TRANSPORT; WILD TYPE;

ELECTROPHYSIOLOGICAL PHENOMENA; ESCHERICHIA COLI PROTEINS; LACTOSE; LIPOSOMES; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEOLIPIDS; SYMPORTERS;

EID: 84888213164     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4013269     Document Type: Article

References (57)

1. Pao, S. S., Paulsen, I. T., and Saier, M. H., Jr. (1998) Major facilitator superfamily Microbiol. Mol. Biol. Rev. 62, 1-32
2. Saier, M. H., Jr. 1999, The major facilitator superfamily J. Mol. Microbiol. Biotechnol. 1, 257-279
3. Kaback, H. R., Sahin-Toth, M., and Weinglass, A. B. (2001) The kamikaze approach to membrane transport Nat. Rev. Mol. Cell Biol. 2, 610-620
4. Guan, L. and Kaback, H. R. (2006) Lessons from lactose permease Annu. Rev. Biophys. Biomol. Struct. 35, 67-91
5. Viitanen, P., Newman, M. J., Foster, D. L., Wilson, T. H., and Kaback, H. R. (1986) Purification, reconstitution, and characterization of the lac permease of Escherichia coli Methods Enzymol 125, 429-452
6. Guan, L., Murphy, F. D., and Kaback, H. R. (2002) Surface-exposed positions in the transmembrane helices of the lactose permease of Escherichia coli determined by intermolecular thiol cross-linking Proc. Natl. Acad. Sci. U.S.A. 99, 3475-3480
7. Ermolova, N., Guan, L., and Kaback, H. R. (2003) Intermolecular thiol cross-linking via loops in the lactose permease of Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 100, 10187-10192
8. Sahin-Tóth, M., Lawrence, M. C., and Kaback, H. R. (1994) Properties of permease dimer, a fusion protein containing two lactose permease molecules from Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 91, 5421-5425
9. Abramson, J. 2003, Structure and mechanism of the lactose permease of Escherichia coli Science 301, 610-615
10. Mirza, O., Guan, L., Verner, G., Iwata, S., and Kaback, H. R. (2006) Structural evidence for induced fit and a mechanism for sugar/H(+) symport in LacY EMBO J. 25, 1177-1183
11. Guan, L., Mirza, O., Verner, G., Iwata, S., and Kaback, H. R. (2007) Structural determination of wild-type lactose permease Proc. Natl. Acad. Sci. U.S.A. 104, 15294-15298
12. Chaptal, V. 2011, Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition Proc. Natl. Acad. Sci. U.S.A. 108, 9361-9366
13. Kaback, H. R. 2007, Site-directed alkylation and the alternating access model for LacY Proc. Natl. Acad. Sci. U.S.A. 104, 491-494
14. Majumdar, D. S. 2007, Single-molecule FRET reveals sugar-induced conformational dynamics in LacY Proc. Natl. Acad. Sci. U.S.A. 104, 12640-12645
15. Smirnova, I. 2007, Sugar binding induces an outward facing conformation of LacY Proc. Natl. Acad. Sci. U.S.A. 104, 16504-16509
16. Nie, Y., Ermolova, N., and Kaback, H. R. (2007) Site-directed alkylation of LacY: Effect of the proton electrochemical gradient J. Mol. Biol. 374, 356-364
17. Nie, Y., Sabetfard, F. E., and Kaback, H. R. (2008) The Cys154→Gly mutation in LacY causes constitutive opening of the hydrophilic periplasmic pathway J. Mol. Biol. 379, 695-703
18. Zhou, Y., Guan, L., Freites, J. A., and Kaback, H. R. (2008) Opening and closing of the periplasmic gate in lactose permease Proc. Natl. Acad. Sci. U.S.A. 105, 3774-3778
19. Nie, Y. and Kaback, H. R. (2010) Sugar binding induces the same global conformational change in purified LacY as in the native bacterial membrane Proc. Natl. Acad. Sci. U.S.A. 107, 9903-9908
20. Jiang, X., Nie, Y., and Kaback, H. R. (2011) Site-directed alkylation studies with LacY provide evidence for the alternating access model of transport Biochemistry 50, 1634-1640
21. Kaback, H. R., Smirnova, I., Kasho, V., Nie, Y., and Zhou, Y. (2011) The alternating access transport mechanism in LacY J. Membr. Biol. 239, 85-93
22. Smirnova, I., Kasho, V., Sugihara, J., and Kaback, H. R. (2011) Opening the periplasmic cavity in lactose permease is the limiting step for sugar binding Proc. Natl. Acad. Sci. U.S.A. 108, 15147-15151
23. Smirnova, I., Kasho, V., Sugihara, J., and Kaback, H. R. (2009) Probing of the rates of alternating access in LacY with Trp fluorescence Proc. Natl. Acad. Sci. U.S.A. 106, 21561-21566
24. Jiang, X. 2012, Evidence for an intermediate conformational state of LacY Proc. Natl. Acad. Sci. U.S.A. 109, 698-704
25. Madej, M. G., Soro, S. N., and Kaback, H. R. (2012) Apo-intermediate in the transport cycle of lactose permease (LacY) Proc. Natl. Acad. Sci. U.S.A. 109, 2970-2978
26. le Coutre, J., Narasimhan, L. R., Patel, C. K., and Kaback, H. R. (1997) The lipid bilayer determines helical tilt angle and function in lactose permease of Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 94, 10167-10171
27. le Coutre, J., Kaback, H. R., Patel, C. K., Heginbotham, L., and Miller, C. (1998) Fourier transform infrared spectroscopy reveals a rigid alpha-helical assembly for the tetrameric Streptomyces lividans K+ channel Proc. Natl. Acad. Sci. U.S.A. 95, 6114-6117
28. Patzlaff, J. S., Moeller, J. A., Barry, B. A., and Brooker, R. J. (1998) Fourier transform infrared analysis of purified lactose permease: a monodisperse lactose permease preparation is stably folded, alpha-helical, and highly accessible to deuterium exchange Biochemistry 37, 15363-15375
29. Nie, Y., Smirnova, I., Kasho, V., and Kaback, H. R. (2006) Energetics of ligand-induced conformational flexibility in the lactose permease of Escherichia coli J. Biol. Chem. 281, 35779-35784
30. Sayeed, W. M. and Baenziger, J. E. (2009) Structural characterization of the osmosensor ProP Biochim. Biophys. Acta 1788, 1108-1115
31. Frillingos, S., Sahin-Toth, M., Wu, J., and Kaback, H. R. (1998) Cys-scanning mutagenesis: A novel approach to structure function relationships in polytopic membrane proteins FASEB J. 12, 1281-1299
32. Venkatesan, P. and Kaback, H. R. (1998) The substrate-binding site in the lactose permease of Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 95, 9802-9807
33. Sahin-Toth, M. 1999, Characterization of Glu126 and Arg144, two residues that are indispensable for substrate binding in the lactose permease of Escherichia coli Biochemistry 38, 813-819
34. Guan, L., Hu, Y., and Kaback, H. R. (2003) Aromatic stacking in the sugar binding site of the lactose permease Biochemistry 42, 1377-1382
35. Smirnova, I. N., Kasho, V., and Kaback, H. R. (2008) Protonation and sugar binding to LacY Proc. Natl. Acad. Sci. U.S.A. 105, 8896-8901
36. Smirnova, I. N., Kasho, V. N., Sugihara, J., Choe, J. Y., and Kaback, H. R. (2009) Residues in the H+ translocation site define the p K a for sugar binding to LacY Biochemistry 48, 8852-8860
37. Smirnova, I., Kasho, V., Sugihara, J., Vazquez-Ibar, J. L., and Kaback, H. R. (2012) Role of protons in sugar binding to LacY Proc. Natl. Acad. Sci. U.S.A. 109, 16835-16840
38. Carrasco, N., Antes, L. M., Poonian, M. S., and Kaback, H. R. (1986) Lac permease of Escherichia coli: Histidine-322 and glutamic acid-325 may be components of a charge-relay system Biochemistry 25, 4486-4488
39. Carrasco, N. 1989, Characterization of site-directed mutants in the lac permease of Escherichia coli. 2. Glutamate-325 replacements Biochemistry 28, 2533-2539
40. Sahin-Tóth, M. and Kaback, H. R. (2001) Arg-302 facilitates deprotonation of Glu-325 in the transport mechanism of the lactose permease from Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 98, 6068-6073
41. Zhou, Y., Jiang, X., and Kaback, H. R. (2012) Role of the irreplaceable residues in the LacY alternating access mechanism Proc. Natl. Acad. Sci. U.S.A. 109, 12438-12442
42. Grewer, C., Gameiro, A., Mager, T., and Fendler, K. (2013) Electrophysiological characterization of membrane transport proteins Annu. Rev. Biophys. 42, 95-120
43. Garcia-Celma, J.-J., Smirnova, I. N., Kaback, H. R., and Fendler, K. (2009) Electrophysiological characterization of LacY Proc. Natl. Acad. Sci. U.S.A. 106, 7373-7378
44. Garcia-Celma, J.-J., Ploch, J., Smirnova, I., Kaback, H. R., and Fendler, K. (2010) Delineating electrogenic reactions during lactose/H+ symport Biochemistry 49, 6115-6121
45. Schultz, P., Garcia-Celma, J.-J., and Fendler, K. (2008) SSM-based electrophysiology Methods Enzymol. 46, 97-103
46. Garcia-Celma, J.-J. 2008, Rapid activation of the melibiose permease MelB immobilized on a solid-supported membrane Langmuir 24, 8119-81128
47. Trumble, W. R., Viitanen, P. V., Sarkar, H. K., Poonian, M. S., and Kaback, H. R. (1984) Site-directed mutagenesis of cys148 in the lac carrier protein of Escherichia coli Biochem. Biophys. Res. Commun. 119, 860-867
48. Viitanen, P. V., Menick, D. R., Sarkar, H. K., Trumble, W. R., and Kaback, H. R. (1985) Site-directed mutagenesis of cysteine-148 in the lac permease of Escherichia coli: Effect on transport, binding, and sulfhydryl inactivation Biochemistry 24, 7628-7635
49. Padan, E., Sarkar, H. K., Viitanen, P. V., Poonian, M. S., and Kaback, H. R. (1985) Site-specific mutagenesis of histidine residues in the lac permease of Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 82, 6765-6768
50. Weinglass, A., Whitelegge, J. P., Faull, K. F., and Kaback, H. R. (2004) Monitoring conformational rearrangements in the substrate-binding site of a membrane transport protein by mass spectrometry J. Biol. Chem. 279, 41858-41865
51. Liu, Z., Madej, M. G., and Kaback, H. R. (2010) Helix dynamics in LacY: Helices II and IV J. Mol. Biol. 396, 617-626
52. Zhang, W., Guan, L., and Kaback, H. R. (2002) Helices VII and X in the lactose permease of Escherichia coli: Proximity and ligand-induced distance changes J. Mol. Biol. 315, 53-62
53. Guan, L. and Kaback, H. R. (2004) Binding affinity of lactose permease is not altered by the H+ electrochemical gradient Proc. Natl. Acad. Sci. U.S.A. 101, 12148-12152
54. Viitanen, P., Garcia, M. L., Foster, D. L., Kaczorowski, G. J., and Kaback, H. R. (1983) Mechanism of lactose translocation in proteoliposomes reconstituted with lac carrier protein purified from Escherichia coli. 2. Deuterium solvent isotope effects Biochemistry 22, 2531-2536
55. Kaczorowski, G. J. and Kaback, H. R. (1979) Mechanism of lactose translocation in membrane vesicles from Escherichia coli. 1. Effect of pH on efflux, exchange, and counterflow Biochemistry 18, 3691-3697
56. Garcia, M. L., Viitanen, P., Foster, D. L., and Kaback, H. R. (1983) Mechanism of lactose translocation in proteoliposomes reconstituted with lac carrier protein purified from Escherichia coli. 1. Effect of pH and imposed membrane potential on efflux, exchange, and counterflow Biochemistry 22, 2524-2531
57. Costello, M. J. 1987, Purified lac permease and cytochrome o oxidase are functional as monomers J. Biol. Chem. 262, 17072-17082