Cys-scanning mutagenesis: A novel approach to structure-function relationships in polytopic membrane proteins

FASEB Journal

Volumn 12, Issue 13, 1998, Pages 1281-1299

  Frillingos, Stathis ^a,b   Sahin Tóth, Miklós ^a   Wu, Jianhua ^a   Kaback, H Ronald ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF IOANNINA   (Greece)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Active transport; Bioenergetics; Conformational change; Ligand binding; Membrane protein structure; Site directed mutagenesis

Indexed keywords

ARGININE; BETA GALACTOSIDASE; CYSTEINE; GLUCAGON; LACTOSE PERMEASE; MEMBRANE PROTEIN; MUTANT PROTEIN; N ETHYLMALEIMIDE;

ACTIVE TRANSPORT; ALKYLATION; BIOENERGY; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; LIGAND BINDING; MUTAGENESIS; NONHUMAN; PKA; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON TRANSPORT; REVIEW; SITE DIRECTED MUTAGENESIS;

EID: 0031717187     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.12.13.1281     Document Type: Review

References (118)

1. Deiscnhofer, J. M., and Michel, H. (1989) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. Science 245, 1463-1473
2. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E., and Downing, K. H. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol,. Biol,. 213, 899-929
3. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature (London) 376, 660-669
4. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272, 1136-1144
5. Pebay-Peyroula, E., Rummel, G., Roaenbusch,J. P., and Landau, E. M. (1997) X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 277, 1676-1681
6. Kaback, H. R. (1996) Handbook of Biological Physics: Transport Processes in Eukaryotic and Prokaryotic Organisms, Vol. II (Konings, W. N., Kaback, H. R., and Lolkema, J. S., eds) pp. 203-227, Elsevier, Amsterdam
7. Kaback, H. R. (1997) A molecular mechanism for energy coupling in a membrane transport protein, the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 94, 5539-5543
8. Kaback, H. R., Voss, J., and Wu, J. (1997) Helix packing in polytopic membrane proteins: the lactose permease of Escherichia coli. Curr. Opin. Struct. Biol. 7, 537-542
9. Kaback, H. R., and Wu, J. (1997) From membrane to molecule to the third amino acid from the left with the lactose permease of Escherichia coli Q. Rev. Biophys. 30, 333-364
10. Dunten, R. L., Sahin-Tóth, M., and Kaback, H. R. (1993) Cysteine scanning mutagenesis of putative helix XI in the lactose permease of Escherichia coli. Biochemistry 32., 12644-12650
11. Loo, T. W., and Clarke, D. M. (1995) Membrane topology of a cysteine-less mutant of human p-glycoprotein. J. Biol. Chem. 270, 843-848
12. Sun, J., Wu, J., Carrasco, N., and Kaback, H. R. (1996) Identification of the epitope for monoclonal antibody 4B1 which uncouples lactose and proton translocation in the lactose permease of Escherichia coli. Biochemistry 35, 990-998
13. Sun, J., Li, J., Carrasco, N., and Kaback, H. R. (1997) The last two cytoplasmic loops in the lactose permease of Escherichia coli comprise a discontinuous epitope for a monoclonal antibody. Biochemistry 36, 274-280
14. + antiporter as studied by site-directed chemical labeling. J. Biol. Chem. 272, 580-585
15. Voss, J., Hubbell, W. L., Hernandez, J., and Kaback, H. R. (1997) Site-directed spin-labeling of transmembrane domain VII and the 4B1 antibody epitope in the lactose permease of Escherichia coli Biochemistry 36, 15055-15061
16. Altenbach, C., Marti, T., Khorana, H. G., and Hubbell, W. L. (1990) Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants. Science 248, 1088-1092
17. Akabas, M. H., Stauffer, D. A., Xu, M., and Karlin, A. (1992) Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science 258, 307-310
18. Abrams, F. S., and London, E. (1992) Calibration of the parallax fluorescence quenching method for determination of membrane penetration depth: refinement and comparison of quenching by spin-labeled and brominated lipids. Biochemistry 31, 5312-5322
19. Yan, R., and Maloney, P. (1993) Identification of a residue in thetranslocation pathway of a membrane carrier. Cell 75, 37-44
20. Yan, R., and Maloney, P. (1995) Residues in the pathway through a membrane transporter. Proc. Natl. Acad, Sci. USA 92, 5973-5976
21. Lu, Q., and Miller, C. (1995) Silver as a probe of pore-forming residues in a potassium channel. Science 268, 304
22. Arkin, I. T., MacKenzie, K. R., Fisher, L., Aimoto, S., Engelman, D. M., and Smith, S. O. (1996) Mapping the lipid-exposed surfaces of membrane proteins. Nat. Struct. Biol. 3, 240-243
23. Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A., and Danielson, M. A. (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu, Rev. Cell. Dev. Biol. 13, 457-512
24. Frillingos, S., and Kaback, H. R. (1996) Probing the conformation of the lactose permease of Escherichia coli by in situ sitedirected sulfhydryl modification. Biochemistry 35, 3950-3956
25. Frillingos, S., and Kaback, H. R. (1997) The role of helix VIII in the lactose permease of Escherichia coli II. Site-directed sulfhydryl modification. Protein Sci. 6, 438-443
26. Lynch, B. A., and Koshland, D. E. (1991) Disulfide cross linking studies of the transmembrane regions of the aspartate sensory receptor of Escherichia coli. Proc. Natl. Acad. Sci. USA 88, 10402-10406
27. Pakula, A., and Simon, M. (1992) Determination of transmembrane protein structure by disulfide cross-linking: the Escherichia coli Tar receptor. Proc. Natl. Acad. Sci. USA 89, 4144-4148
28. Chervitz, S. A., and Falke, J. J. (1996) Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc. Natl. Acad. Sci. USA 93, 2545-2550
29. Yu, H., Kono, M., McKee, T. D., and Oprian, D. D. (1995) A general method for mapping tertiary contacts between amino acid residues in membrane-embedded proteins. Biochemistry 34, 14963-14969
30. Hughson, A. G., and Hazelbauer, G. L. (1996) Detecting the conformational change of transmembrane signaling in a bacterial chemoreceptor by measuring effects on disulfide cross-linking in vivo. Proc. Natl. Acad. Sci. USA 93, 11546-11551
31. Wu, J., and Kaback, H. R. (1996) A general method for determining helix packing in membrane proteins in situ: helices I and II are close to helix VII in the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 93, 14498-14502
32. Wu, J., and Kaback, H. R. (1997) Helix proximity and ligand-induced conformational changes in the lactose permease of Escherichia coli determined by site-directed chemical crosslinking. J. Mol. Biol. 270, 285-293
33. Sun, J., and Kaback, H. R. (1997) Proximity of periplasmic loops in the lactose permease of Escherichia coli determined by site-directed crosslinking. Biochemistry 36, 11959-11965
34. 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
35. 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. USA 91, 5421-5425
36. van Iwaarden, P. R., Pastore, J. C., Konings, W. N., and Kaback, H. R. (1991) Construction of a functional lactose permease devoid of cysteine residues. Biochemistry 30, 9595-9600
37. Sahin-Tóth, M., Persson, B., Schwieger, J., Cohan, M., and Kaback, H. R. (1994) Cysteine scanning mutagenesis of the N-terminal 82 amino acid residues in the lactose permease of Escherichia coli, Protein Sci. 3, 240-247
38. '38. Frillingos, S., Sun, J., Gonzalez, A., and Kabuck, H. R. (1997) Cysteine-scanning mutagenesis of helix II and flanking hydrophilic domains in the lactose permease of Escherichia coli. Biochemistry 36, 269-273
39. Sahin-Tóth, M., Frillingos, S., Bibi, E., Gonzalez, A., and Kaback, H. R. (1994) The role of transmembrane domain III in the lactose permease of Escherichia coli. Protein Sci. 3, 2302-2310
40. Frillingos, S., Gonzalez, A., and Kaback, H. R. (1997) Cysteine-scanning mutagenesis of helix IV and the adjoining loops i the lactose permease of Escherichia coli: Glu126 and Arg144 are essential. Biochemistry 47, 14284-14290
41. Weitzman, C., and Kaback, H. R. (1995) Cysteine scanning mutagenesis of helix V in the lactose permease of Escherichia coli. Biochemistry 4, 2310-2318
42. Frillingos, S., and Kaback, H. R. (1996) Cysteine-scanning mutagenesis of helix VI and the flanking hydrophilic domains in the lactose permease of Escherichia coli. Biochemistry 35, 5333-5338
43. Frillingos, S., Sahin-Tóth, M., Persson, B., and Kaback, H. R. (1994) Cysteine-scanning mutagenesis of putative helix VII in the lactose permease of Escherichia coli. Biochemistry 33, 8074-8081
44. Frillingos, S., Ujwal, M. L., Sun. J., and Kaback, H. R. (1997) The role of helix VIII in the lactose permese of Escherichia coli. I. Cys-scanning mutagenesis. Protein Sci. 6, 431-437
45. Sahin-Tóth, M., and Kaback, H. R. (1993) Cysteine scanning mutagenesis of putative transmembrane helices IX and X in the lactose permease of Escherichia coli. Protein Sci. 2, 1024-1033
46. He, M. M., Sun, J., and Kaback, H. R. (1996) Cysteine scanning mutagenesis of putative helix XII in the lactose permease of Escherichia coli. Biochemistry 35, 12909-12914
47. Roepe, P. D., Zbar, R. I., Sarkar, H. K., and Kaback, H. R. (1989) A five-residue sequence near the carboxyl terminus of the polytopic membrane protein lac permease is required for stability within the membrane. Proc. Natl. Acad. Sci. USA 86, 3992-3996
48. McKenna, E., Hardy, D., Pasture, J. C., and Kaback, H. R. (1991) Sequential truncation of the lactose permease over a three-amino acid sequence near the carboxyl terminus leads to progressive loss of activity and stability. Proc. Natl. Acad. Sci. USA 88, 2969-2973
49. McKenna, E., Hardy, D., and Kaback, H. R. (1992) Evidence that the final turn of the last transmembrane helix in the lactose permease is required for folding. J. Biol. Chem. 267, 6471-6474
50. 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
51. Menick, D. R., Sarkar, H. K., Poonian, M. S., and Kaback, H. R. (1985) Cys154 is important for lac permease activity in Escherichia coli. Biochem. Biophys. Res. Commun. 132, 162-170
52. Brooker, R. J., and Wilson, T. H. (1986) Site-specific alteration of cysteine 176 and cysteine 234 in the lactose carrier of Escherichia coli. J. Biol. Chem. 261, 11765-11771
53. Menick, D. R., Lee, J. A., Brooker, R. J., Wilson, T. H., and Kaback, H. R. (1987) Role of cysteine residues in the lac permease of Escherichia coli. Biochemistry 26, 1132-1136
54. van Iwaarden, P. R., Driessen, A. J., Menick, D. R., Kaback, H. R., and Konings, W. N. (1991) Characterization of purified, reconstituted site-directed cysteine mutants of the lactose permease of Escherichia coli. J. Biol. Chem. 266, 15688-15692
55. Jung, H.,Jung, K., and Kaback, H. R. (1994) Cysteine 148 in the lactose permease of Escherichia coli is a component of a substrate binding site. I. Site-directed mutagenesis studies. Biochemistry 33/12160-12165
56. Wu, J., Frillingos, S., and Kaback, H. R. (1905) Dynamics of lactose permease of Escherichia coli determined by site-directed chemical labeling and fluorescence spectroscopy. Biochemistry 34, 8257-8263
57. Wu, J., and Kaback, H. R. (1994) Cysteine 148 in the lactose permease of Escherichia coli is a component of a substrate binding site. 2. Site-directed fluorescence studies. Biochemistry 33, 12166-12171
58. Wu, J., Frillingos, S., Voss, J., and Kaback, H. R. (1994) Ligand-induced conformation changes in the lactose permease of Escherichia coli: evidence for two binding sites. Protein Sci. 3, 2294-2301
59. Jung, H., Jung, K., and Kaback, H. R. (1994) A conformational change in the lactose permease of Escherichia coli is induced by ligand binding or membrane potential. Protein Sci. 3, 1052-1057
60. Wu, J., Perrin, D., Sigman, D., and Kaback, H. (1995) Helix packing of lactose permease in Escherichia coli studied by sitedirected chemical cleavage. Proc. Natl. Acad. Sci. USA 92, 9186-9190
61. Wu, J., Voss, J., Hubbell, W. L., and Kaback, H. R. (1996) Sitedirected spin labeling and chemical crosslinking demonstrate that helix V is close to helicies VII and VIII in the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 93, 10123-10127
62. King, S. C., Hansen, C. L., and Wilson, T. H. (1991) The interaction between aspartic acid 237 and lysine 358 in the lactose carrier of Escherichia coli. Biochem. Biophys. Acta 1062, 177-186
63. Sahin-Tóth, M., Dun ten, R. L., Gonzalez, A., and Kaback, H. R. (1992) Functional interactions between putative intramembrane charged residues in the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 89, 10547-10551
64. Lee, J. L., Hwang, P. P., Hansen, C., and Wilson, T. H. (1992) Possible salt bridges between transmembranc α-helices of the lactose carrier of Escherichia coli. J. Biol. Chem. 207, 20758-20764
65. Dunten, R. L., Sahin-Tóth, M., and Kaback, H. R. (1993) Role of the charge pair formed by aspartic acid 237 and lysine 358 in the lactose permease of Escherichia coli. Biochemistry 32, 3139-3145
66. Sahin-Tóth, M., and Kaback, H. R. (1993) Properties of interacting aspartic acid and lysine residues in the lactose permease of Escherichia coli. Biochemistry 32, 10027-10035
67. Frillingos, S., and Kaback, H. R. (1996) Chemical rescue of Asp237→Ala and Lys358→Ala mutants in the lactose permease of Escherichia coli. Biochemistry 35, 13363-13367
68. Jessen-Marshall, A. E., and Brooker, R. J. (1996) Evidence that transmembrane segment 2 of the lactose permease is part of a conformationally sensitive interface between the two halves of the protein. J. Biol. Chem. 271, 1400-1404
69. Jessen-Marshall, A. E., Parker, N. J., and Brooker, R. J. (1997) Suppressor analysis of mutations in the loop 2-3 motif of lactose permease: evidence that glycine-64 is an important residue for conformational changes. J. Bacteriol. 179, 2616-2622
70. Consler, T. G., Persson, B. L., Jung, H., Zen, K. H., Jung, K., Prive, G. G., Verner, G. E., and Kaback, H. R. (1993) Properties and purification of an active biotinylated lactose permease from Escherichia coli. Proc. Natl. Acad. Sci. USA 90, 6934-6938
71. Voss, J., Sun, J., and Kaback, H. R. (1998) Sulfhydryl oxidation of mutants with cysteine in place of acidic residues in the lactose permease. Biochemistry 37, 8191-8196
72. Jung, K., Jung, H., Wu, J., Privé, G. G., and Kaback, H. R. (1993) Use of site-directed fluorescence labeling to study proximity relationships in the lactose permease of Escherichia coli. Biochemistry 32, 12273-12278
73. Wang, Q., Voss, J., Hubbell W. L., and Kaback, H. R. (1998) Proximity of helices VIII (Ala2373) and IX (Met299) in the lactose permease of Escherichia coli. Biochemistry 37, 4910-4915
74. Jung, K., Voss, J., He, M., Hubbell, W. L., and Kaback, H. R. (1995) Engineering a metal binding site within a polytopic membrane protein, the lactose permease of Escherichia coli Biochemistry 34, 6272-6277
75. He, M. M., Voss, J., Hubbell, W. L., and Kaback, H. R. (1995) Use of designed metal-binding sites to study helix proximity in the lactose permease of Escherichia coli: 1. proximity of helix VII (Asp237 and Asp240) with helices X (Lys319) and XI (Lys358). Biochemistry 34, 15661-15666
76. He, M. M., Voss, J., Hubbell, W. L., and Kaback, H. R. (1995) Use of designed metal binding sites to study helix proximity in the lactose permease of Escherichia coli. 2. proximity of helix IX (Arg302) with helix X (His322 and Glu325). Biochemistry 34, 15667-15670
77. He, M., Voss, J., Hubbell, W. L., and Kaback, H. R. (1997) Arginine 302 (Helix X) in the lactose permease of Escherichia coli is in close proximity to glutamate 269 (helix VIII) as well as glutamate 325 (helix X). Biochemistry 36, 13682-13087
78. Voss, J., Salwinski, L., Kaback, H. R., and Hubbell, W. L. (1995) A method for distance determination in proteins using a designed metal ion binding site and site-directed spin labeling: evaluation with T4 lysozyme. Proc. Natl. Acad. Sci. USA 92, 12295-12299
79. Voss, J., Hubbell, W. L., and Kaback, H. R. (1995) Distance determination in proteins using designed metal ion binding sites and site-directed spin labeling: application to the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 92, 12300-12303
80. Voss, J., Hubbell, W. L., and Kaback, H. R. (1997) Helix packing in the lactose permease determined by metal-nitroxide interaction. Biochemistry 37, 211-216
81. Wu, J., Hardy, D., and Kaback, H. R. (1998) Transmembrane helix tilting and ligand-induced conformational changes in the lactose permease determined by site-directed chemical crosslinking in situ. J. Mol. Biol. In press
82. Frillingos, S., Wu, J., Venkatesan, P., and Kaback, H. R. (1997) Binding of ligand or monoclonal antibody 4B1 induces discrete structural changes in the lactose permease of Escherichia coli. Biochemistry 36, 6408-6414
83. Kimura, T., Suzuki, M., Sawai, T., and Yamaguchi, A. (1996) Determination of a transmembrane segment using cyteine-scanning mutants of transposon Tn10-encoded metal-tetracycline/H+ antiporter. Biochemistry 35, 15896-15899
84. + antiporter. J. Biol. Chem. 273, 5243-5247
85. Foster, D. L., Boublik, M., and Kaback, H. R. (1983) Structure of the lac carrier protein of Escherichia coli. J. Biol. Chem. 258, 31-34
86. McKenna, E., Hardy, D., and Kaback, H. R. (1992) Insertional mutagenesis of hydrophilic domains in the lactose permease of Escherichia coli. Proc. Natl. Acad. Sci. USA 89, 11954-11958
87. 86a. Venkatesan, P., and Kaback, H. R. (1998) The substrate binding site in the lactose permease of Escherichia coli Proc. Natl. Acad. Sci. USA In press
88. Varela, M. F., and Wilson, T. H. (1996) Molecular biology of the lactose carrier of Escherichia coli. Biochim Biophys Acta 1276, 21-34
89. McMorrow, I., Chin, D. T., Fiebig, K., Pierce, J. L., Wilson, D. M., Reeve, E.C.R., & Wilson, T.H. (1988) The lactose carrier of Klebsiella pneumoniae M5a1: the physiology of transport and nucleotide sequence of the lac Y gene. Biochim. Biophys. Acta 945, 315-323
90. Lee, J., Okazaki, N., Tsuchiya, T., and Wilson, T. H. (1994) Cloning and sequencing of the gene for the lactose carrier of Citrobacter freundii. Biochem. Biophys. Res. Commun. 203, 1882-1888
91. Aslanidis, C., Schmid, K., and Schmitt, R. (1989) Nucleotide sequences and operon structure of plasmid-borne genes mediating uptake and utilization of raffinose in Escherichia coli. J. Bacteriol. 171, 6753-6763
92. Jung, K., Jung, H., and Kaback, H. R. (1994) Dynamics of lactose permease of Eacherichia coli determined by site-directed fluorescence labeling. Biochemistry 33, 3980-3985
93. Sun, J., Kemp, C. R., and Kaback, H. R. (1998) Ligand-induced changes in periplasmic loops in the lactose permease of Escherichia coli Biochemistry 37, 8020-8026
94. 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. USA 94, 10167-10171
95. Dornmair, K., Corni, A. F., Wright, J. K., and Jähnig, F. (1985) The size of the lactose permease derived from rotational diffusion measurements. EMBOJ. 4, 3633-3638
96. Costello, M. J., Escaig, J., Matsushita, K., Viitanen, P. V., Menick, D. R., and Kaback, H. R. (1987) Purified lac permease and cytochrome o oxidase are functional as monomers. J. Biol. Chem. 262, 17072-17082
97. Lis, L. J., McAlister, M., Fuller, N., Rand, R. P., and Parsegian, V. A. (1982) Measurement of the lateral compressibility of several phospholipid bilayers. Biophys. J. 37, 667-672
98. + channel. Proc. Natl. Acad. Sci. USA 95, 6114-6117
99. Alvarez, J., Lee, D. C., Baldwin, S. A., and Chapman, D. (1987) Fourier transform infrared spectroscopic study of the structure and conformational changes of the human crythrocyte glucose, transporter. J. Biol. Chem. 262, 3502-3509
100. Arkin, I. T., RUSS, W. P., Lebendiker, M., and Schuldiner, S. (1996) Determining the secondary structure and orientation of EmrE, a multi-drug transporter, indicates a transmembrane four-helix bundle. Biochemistry 35, 7233-7238
101. Downer, N. W., Bruchman, T. J., and Hazzard, J. H. (1986) Infrared spectroscopic study of photoreceptor membrane and purple membrane. Protein secondary structure and hydrogen deuterium exchange. J. Biol. Chem. 261, 3640-3647
102. 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
103. +. Biochemistry 18, 3697-3704
104. Kaback, H. R. (1987) Use of site-directed mutagenesis to study the mechanism of a membrane transport protein. Biochemistry 26, 2071-2076
105. 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
106. Carrasco, N., Viitanen, P., Herzlinger, D., and Kaback, H. R. (1984) Monoclonal antibodies against the lac carrier protein from Escherichia coli. 1. Functional studies. Biochemistry 23, 3681-3687
107. a of a carboxylic acid at position 325 (helix X) of the lactose permease of Escherichia coli, Biochemistry 35, 10166-10171
108. King, S. C., and Wilson, T. H. (1989) Galactoside-dependent proton transport by mutants of the Escherichia coli lactose carrier. Replacement of histidine 322 by tyrosine or phenylalanine. J. Biol. Chem. 264, 7390-7394
109. King, S. C., and Wilson, T. H. (1989) Galactoside-dependent proton transport by mutants of the Escherichia coli lactose carrier: substitution of tyrosine for histidine-322 and of leucine for serine-306. Biochim. Biophys. Acta 982, 253-264
110. King, S. C., and Wilson, T. H. (1990) Sensitivity of efflux-driven carrier turnover to external pH in mutants of the Escherichia coli lactose carrier that have tyrosine or phenylalanine substituted for histidine-322. A comparison of lactose and melibiose. J. Biol. Chem. 265, 3153-3160
111. Brooker, R. J. (1990) Characterization of the double mutant, Val-177/Asn-322, of the lactose permease. J. Biol. Chem. 265, 4155-4160
112. Menick, D. R., Carrasco, N., Antes, L. M., Patel, L., and Kaback, H. R. (1987) Lac permease of Escherichia coli: arginine-302 as a component of the postulated proton relay. Biochemistry 26, 6638-6644
113. Matzke, E. A., Stephenson, L. J., and Brooker, R. J. (1992) Functional role of arginine 302 within the lactose permease of Escherichia coli, J. Biol. Chem. 267, 19095-19100
114. Ujwal, M. L., Sahin-Tóth, M., Persson, B., and Kaback, H. R. (1994) Role of glutamate-269 in the lactose permease of Escherichia coli, Mol. Membr. Biol. 1, 9-16
115. Franco, P. J., and Brooker, R. J. (1994) Functional rules of Glu-269 and Glu-325 within the lactose permease of Escherichia coli, J. Biol. Chem. 269, 7379-7386
116. Wang, Q., Matsushita, K., de Foresta, B., LeMaire, M., and Kaback, H. R. (1997) Ligand-induced movement of helix X in the lactose permease of Escherichia coli: a fluorescence quenching study. Biochemistry 36, 14120-14127
117. He, M., and Kaback, H. R. (1997) Interaction between residues Glu269 (Helix VIII) and His322 (Helix X) of the lactose permease of Escherichia coli is essential for substrate binding. Biochemistry 36, 13688-13692
118. Holman, C. M., and Benisek, W. F. (1994) Extent of proton transfer in the transition states of the reaction catalyzed by the D5-3-ketosteroid isomerase of Comamonas (Psuedomonas) testeroni: site-specific replacement of the active site base, aspartate 38, by the weaker base alanine-3-sulfinate. Biochemistry 33, 2672-2681