Trp replacements for tightly interacting Gly-Gly pairs in LacY stabilize an outward-facing conformation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 22, 2013, Pages 8876-8881

  Smirnova, Irina ^a   Kasho, Vladimir ^a   Sugihara, Junichi ^a   Kaback, H Ronald ^a,b,c  

^a The Departments of Physiology and Biophysics   (United States)

^b Immunology   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alternating access; Fluorescence; Major facilitator superfamily; Permease; Symport

Indexed keywords

CYSTEINE; GLYCINE; LACTOSE PERMEASE; PROTEOLIPOSOME; SUGAR;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ESCHERICHIA COLI; FLOW KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION;

ALTERNATING ACCESS; FLUORESCENCE; MAJOR FACILITATOR SUPERFAMILY; PERMEASE; SYMPORT;

BIOLOGICAL TRANSPORT, ACTIVE; ESCHERICHIA COLI; GLYCINE; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS; OLIGONUCLEOTIDES; PROTEIN CONFORMATION; PROTEOLIPIDS; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

EID: 84878464140     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306849110     Document Type: Article

References (63)

1. Saier MH, Jr., et al. (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1(2):257-279.
2. Saier MH, Jr. (2000) Families of transmembrane sugar transport proteins. Mol Microbiol 35(4):699-710.
3. West IC, Mitchell P (1973) Stoicheiometry of lactose-H+ symport across the plasma membrane of Escherichia coli. Biochem J 132(3):587-592.
4. Patel L, Garcia ML, Kaback HR (1982) Direct measurement of lactose/proton symport in Escherichia coli membrane vesicles: Further evidence for the involvement of histidine residue(s). Biochemistry 21(23):5805-5810.
5. Garcia-Celma JJ, Smirnova IN, Kaback HR, Fendler K (2009) Electrophysiological characterization of LacY. Proc Natl Acad Sci USA 106(18):7373-7378.
6. Smirnova I, Kasho V, Kaback HR (2011) Lactose permease and the alternating access mechanism. Biochemistry 50(45):9684-9693.
7. Abramson J, et al. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301(5633):610-615.
8. Mirza O, Guan L, Verner G, Iwata S, Kaback HR (2006) Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J 25(6):1177-1183.
9. Guan L, Mirza O, Verner G, Iwata S, Kaback HR (2007) Structural determination of wild-type lactose permease. Proc Natl Acad Sci USA 104(39):15294-15298.
10. Chaptal V, et al. (2011) Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. Proc Natl Acad Sci USA 108(23):9361-9366.
11. Kaback HR, et al. (2007) Site-directed alkylation and the alternating access model for LacY. Proc Natl Acad Sci USA 104(2):491-494.
12. Nie Y, Ermolova N, Kaback HR (2007) Site-directed alkylation of LacY: Effect of the proton electrochemical gradient. J Mol Biol 374(2):356-364.
13. Nie Y, Sabetfard FE, Kaback HR (2008) The Cys154->Gly mutation in LacY causes constitutive opening of the hydrophilic periplasmic pathway. J Mol Biol 379(4): 695-703.
14. Nie Y, Kaback HR (2010) Sugar binding induces the same global conformational change in purified LacY as in the native bacterial membrane. Proc Natl Acad Sci USA 107(21):9903-9908.
15. Jiang X, Nie Y, Kaback HR (2011) Site-directed alkylation studies with LacY provide evidence for the alternating access model of transport. Biochemistry 50(10): 1634-1640.
16. Jiang X, et al. (2012) Evidence for an intermediate conformational state of LacY. Proc Natl Acad Sci USA 109(12):E698-E704.
17. Majumdar DS, et al. (2007) Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc Natl Acad Sci USA 104(31):12640-12645.
18. Smirnova I, et al. (2007) Sugar binding induces an outward facing conformation of LacY. Proc Natl Acad Sci USA 104(42):16504-16509.
19. Zhou Y, Guan L, Freites JA, Kaback HR (2008) Opening and closing of the periplasmic gate in lactose permease. Proc Natl Acad Sci USA 105(10):3774-3778.
20. Smirnova IN, Kasho VN, Kaback HR (2006) Direct sugar binding to LacY measured by resonance energy transfer. Biochemistry 45(51):15279-15287.
21. Smirnova I, Kasho V, Sugihara J, Kaback HR (2009) Probing of the rates of alternating access in LacY with Trp fluorescence. Proc Natl Acad Sci USA 106(51):21561-21566.
22. Smirnova I, Kasho V, Sugihara J, Kaback HR (2011) Opening the periplasmic cavity in lactose permease is the limiting step for sugar binding. Proc Natl Acad Sci USA 108(37): 15147-15151.
23. Kaback HR, Smirnova I, Kasho V, Nie Y, Zhou Y (2011) The alternating access transport mechanism in LacY. J Membr Biol 239(1-2):85-93.
24. Radestock S, Forrest LR (2011) The alternating-access mechanism of MFS transporters arises from inverted-topology repeats. J Mol Biol 407(5):698-715.
25. Madej MG, Soro SN, Kaback HR (2012) Apo-intermediate in the transport cycle of lactose permease (LacY). Proc Natl Acad Sci USA 109(44):E2970-E2978.
26. Sugihara J, Sun L, Yan N, Kaback HR (2012) Dynamics of the L-fucose/H+ symporter revealed by fluorescence spectroscopy. Proc Natl Acad Sci USA 109(37):14847-14851.
27. le Coutre J, Kaback HR, Patel CK, Heginbotham L, Miller C (1998) Fourier transform infrared spectroscopy reveals a rigid alpha-helical assembly for the tetrameric Streptomyces lividans K+ channel. Proc Natl Acad Sci USA 95(11):6114-6117.
28. Sayeed WM, Baenziger JE (2009) Structural characterization of the osmosensor ProP. Biochim Biophys Acta 1788(5):1108-1115.
29. Patzlaff JS, Moeller JA, Barry BA, Brooker RJ (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(44): 15363-15375.
30. Nie Y, Smirnova I, Kasho V, Kaback HR (2006) Energetics of ligand-induced conformational flexibility in the lactose permease of Escherichia coli. J Biol Chem 281(47): 35779-35784.
31. Kaczorowski GJ, Kaback HR (1979) Mechanism of lactose translocation in membrane vesicles from Escherichia coli. 1. Effect of pH on efflux, exchange, and counterflow. Biochemistry 18(17):3691-3697.
32. Kaback HR, Sahin-Tóth M, Weinglass AB (2001) The kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2(8):610-620.
33. Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67-91.
34. Smirnova IN, Kasho V, Kaback HR (2008) Protonation and sugar binding to LacY. Proc Natl Acad Sci USA 105(26):8896-8901.
35. Smirnova I, Kasho V, Sugihara J, Vázquez-Ibar JL, Kaback HR (2012) Role of protons in sugar binding to LacY. Proc Natl Acad Sci USA 109(42):16835-16840.
36. Smirnova IN, Kasho VN, Sugihara J, Choe JY, Kaback HR (2009) Residues in the H+ translocation site define the pKa for sugar binding to LacY. Biochemistry 48(37): 8852-8860.
37. Carrasco N, Antes LM, Poonian MS, Kaback HR (1986) lac permease of Escherichia coli: Histidine-322 and glutamic acid-325 may be components of a charge-relay system. Biochemistry 25(16):4486-4488.
38. Persson B, Roepe PD, Patel L, Lee J, Kaback HR (1992) Site-directed mutagenesis of lysine 319 in the lactose permease of Escherichia coli. Biochemistry 31(37):8892-8897.
39. Sahin-Toth M, Kaback HR (2001) Arg-302 facilitates deprotonation of Glu-325 in the transport mechanism of the lactose permease from Escherichiacoli. Proc Natl Acad Sci USA 98(11):6068-6073.
40. Menick DR, Sarkar HK, Poonian MS, Kaback HR (1985) cys154 Is important for lac permease activity in Escherichia coli. Biochem Biophys Res Commun 132(1):162-170.
41. van Iwaarden PR, Driessen AJ, Lolkema JS, Kaback HR, Konings WN (1993) Exchange, efflux, and substrate binding by cysteine mutants of the lactose permease of Escherichia coli. Biochemistry 32(20):5419-5424.
42. Smirnova IN, Kaback HR (2003) A mutation in the lactose permease of Escherichia coli that decreases conformational flexibility and increases protein stability. Biochemistry 42(10):3025-3031.
43. Ermolova NV, Smirnova IN, Kasho VN, Kaback HR (2005) Interhelical packing modulates conformational flexibility in the lactose permease of Escherichia coli. Biochemistry 44(21):7669-7677.
44. Zhou Y, Madej MG, Guan L, Nie Y, Kaback HR (2011) An early event in the transport mechanism of LacY: Interaction between helices V and I. J Biol Chem 286(35):30415-304212.
45. Jung K, Jung H, Colacurcio P, Kaback HR (1995) Role of glycine residues in the structure and function of lactose permease, an Escherichia coli membrane transport protein. Biochemistry 34(3):1030-1039.
46. Consler TG, Tsolas O, Kaback HR (1991) Role of proline residues in the structure and function of a membrane transport protein. Biochemistry 30(5):1291-1298.
47. Kasho VN, Smirnova IN, Kaback HR (2006) Sequence alignment and homology threading reveals prokaryotic and eukaryotic proteins similar to lactose permease. J Mol Biol 358(4):1060-1070.
48. Senes A, Ubarretxena-Belandia I, Engelman DM (2001) The Calpha-H.O hydrogen bond: A determinant of stability and specificity in transmembrane helix interactions. Proc Natl Acad Sci USA 98(16):9056-9061.
49. Liu W, Eilers M, Patel AB, Smith SO (2004) Helix packing moments reveal diversity and conservation in membrane protein structure. J Mol Biol 337(3):713-729.
50. Weinglass AB, Kaback HR (1999) Conformational flexibility at the substrate binding site in the lactose permease of Escherichia coli. Proc Natl Acad Sci USA 96(20): 11178-11182.
51. Weinglass AB, Smirnova IN, Kaback HR (2001) Engineering conformational flexibility in the lactose permease of Escherichia coli: Use of glycine-scanning mutagenesis to rescue mutant Glu325->Asp. Biochemistry 40(3):769-776.
52. Russell RB, Eggleston DS (2000) New roles for structure in biology and drug discovery. Nat Struct Biol 7(Suppl):928-930.
53. Kleiger G, Grothe R, Mallick P, Eisenberg D (2002) GXXXG and AXXXA: Common alpha-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41(19):5990-5997.
54. Frillingos S, Sahin-Tóth M, Wu J, Kaback HR (1998) Cys-scanning mutagenesis: A novel approach to structure function relationships in polytopic membrane proteins. FASEB J 12(13):1281-1299.
55. Weitzman C, Kaback HR (1995) Cysteine scanning mutagenesis of helix V in the lactose permease of Escherichia coli. Biochemistry 34(29):9374-9379.
56. He MM, Sun J, Kaback HR (1996) Cysteine scanning mutagenesis of putative helix XII in the lactose permease of Escherichia coli. Biochemistry 35:12909-12914.
57. Frillingos S, Sun J, Gonzalez A, Kaback HR (1997) Cysteine-scanning mutagenesis of helix II and flanking hydrophilic domains in the lactose permease of Escherichia coli. Biochemistry 36(1):269-273.
58. Frillingos S, Kaback HR (1997) The role of helix VIII in the lactose permease of Escherichia coli: II. Site-directed sulfhydryl modification. Protein Sci 6(2):438-443.
59. Venkatesan P, Liu Z, Hu Y, Kaback HR (2000) Site-directed sulfhydryl labeling of the lactose permease of Escherichia coli: Helix II. Biochemistry 39:10649-10655.
60. Viitanen P, Newman MJ, Foster DL, Wilson TH, Kaback HR (1986) Purification, reconstitution, and characterization of the lac permease of Escherichia coli. Methods Enzymol 125:429-452.
61. Kaback HR (1974) Transport in isolated bacterial membrane vesicles. Methods Enzymol 31(Pt A):698-709.
62. Kaback HR (1971) Bacterial Membranes. Methods in Enzymol, eds Kaplan NP, Jakoby WB, & Colowick NP (Elsevier, New York), Vol XXII, pp 99-120.
63. Short SA, Kaback HR, Kohn LD (1975) Localization of D-lactate dehydrogenase in native and reconstituted Escherichia coli membrane vesicles. J Biol Chem 250(11): 4291-4296.