Topology and boundaries of the aerotaxis receptor Aer in the membrane of Escherichia coli

Journal of Bacteriology

Volumn 188, Issue 3, 2006, Pages 894-901

  Amin, Divya N ^a   Taylor, Barry L ^a   Johnson, Mark S ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; COPPER; CYSTEINE; FLUORESCEIN DERIVATIVE; MACROGOL DERIVATIVE; MEMBRANE RECEPTOR; PHENANTHROLINE DERIVATIVE;

ALGORITHM; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CHEMORECEPTOR; CROSS LINKING; ESCHERICHIA COLI; MEMBRANE VESICLE; NONHUMAN; PLASMID; PREDICTION; PRIORITY JOURNAL;

CARRIER PROTEINS; CHEMOTAXIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 31344454302     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.3.894-901.2006     Document Type: Article

References (68)

1. Bibikov, S. I., L. A. Barnes, Y. Gitin, and J. S. Parkinson. 2000. Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proc. Natl. Acad. Sci. USA 97:5830-5835.
2. Bibikov, S. I., R. Biran, K. E. Rudd, and J. S. Parkinson. 1997. A signal transducer for aerotaxis in Escherichia coli. J. Bacteriol. 179:4075-4079.
3. Boldog, T., and G. L. Hazelbauer. 2004. Accessibility of introduced cysteines in chemoreceptor transmembrane helices reveals boundaries interior to bracketing charged residues. Protein Sci. 13:1466-1475.
4. Butler, S. L., and J. J. Falke. 1998. Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry 37:10746-10756.
5. Chen, C. P., A. Kernytsky, and B. Rost. 2002. Transmembrane helix predictions revisited. Protein Sci. 11:2774-2791.
6. Chen, C. P., and B. Rost. 2002. State-of-the-art in membrane protein prediction. Appl. Bioinformatics 1:21-35.
7. Claras, M. G., and G. von Heijne. 1994. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10:685-686.
8. Cserzo, M., E. Wallin, I. Simon, G. von Heijne, and A. Elofsson. 1997. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10:673-676.
9. Cuff, J. A., M. E. Clamp, A. S. Siddiqui, M. Finlay, and G. J. Barton. 1998. JPred: a consensus secondary structure prediction server. Bioinformatics 14:892-893.
10. Dalbey, R. E. 1990. Positively charged residues are important determinants of membrane protein topology. Trends Biochem. Sci. 15:253-257.
11. Daley, D. O., M. Rapp, E. Granseth, K. Melen, D. Drew, and G. von Heijne. 2005. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308:1321-1323.
12. Deber, C. M., C. Wang, L. P. Liu, A. S. Prior, S. Agrawal, B. L. Muskat, and A. J. Cuticchia. 2001. TM Finder: a prediction program for transmembrane protein segments using a combination of hydrophobicity and nonpolar phase helicity scales. Protein Sci. 10:212-219.
13. Draheim, R. R., A. F. Bormans, R. Z. Lai, and M. D. Manson. 2005. Tryptophan residues flanking the second transmembrane helix (TM2) set the signaling state of the Tar chemoreceptor. Biochemistry 44:1268-1277.
14. Ehrmann, M., D. Boyd, and J. Beckwith. 1990. Genetic analysis of membrane protein topology by a sandwich gene fusion approach. Proc. Natl. Acad. Sci. USA 87:7574-7578.
15. Eilers, M., S. C. Shekar, T. Shieh, S. O. Smith, and P. J. Fleming. 2000. Internal packing of helical membrane proteins. Proc. Natl. Acad. Sci. USA 97:5796-5801.
16. Falke, J. J., A. F. Dernburg, D. A. Sternberg, N. Zalkin, D. L. Milligan, and D. E. Koshland, Jr. 1988. Structure of a bacterial sensory receptor. A site-directed sulfhydryl study. J. Biol. Chem. 263:14850-14858.
17. Guan, L., F. D. Murphy, and H. R. Kaback. 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. USA 99:3475-3480.
18. Herrmann, S., Q. Ma, M. S. Johnson, A. V. Repik, and B. L. Taylor. 2004. PAS domain of the Aer redox sensor requires C-terminal residues for native-fold formation and flavin adenine dinucleotide binding. J. Bacteriol. 186:6782-6791.
19. Hildebrand, P. W., R. Preissner, and C. Frommel. 2004. Structural features of transmembrane helices. FEBS Lett. 559:145-151.
20. Hirokawa, T., S. Boon-Chieng, and S. Mitaku. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379.
21. Hofmann, K., and W. Stoffel. 1993. TMbase - a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374:166.
22. Hughson, A. G., and G. L. Hazelbauer. 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.
23. Iwaki, S., N. Tamura, T. Kimura-Someya, S. Nada, and A. Yamaguchi. 2000. Cysteine-scanning mutagenesis of transmembrane segments 4 and 5 of the Tn10-encoded metal-tetracycline/H+ antiporter reveals a permeability barrier in the middle of a transmembrane water-filled channel. J. Biol. Chem. 275:22704-22712.
24. Javadpour, M. M., M. Eilers, M. Groesbeek, and S. O. Smith. 1999. Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association. Biophys. J. 77:1609-1618.
25. Jones, D. T. 1998. Do transmembrane protein superfolds exist? FEBS Lett. 423:281-285.
26. Jones, D. T. 1999. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:195-202.
27. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1994. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33:3038-3049.
28. Juretic, D., L. Zoranic, and D. Zucic. 2002. Basic charge clusters and predictions of membrane protein topology. J. Chem. Inf. Comput. Sci. 42:620-632.
29. Kimbrough, T. G., and C. Manoil. 1994. Role of a small cytoplasmic domain in the establishment of serine chemoreceptor membrane topology. J. Bacteriol. 176:7118-7120.
30. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
31. Lee, G. F., G. G. Burrows, M. R. Lebert, D. P. Dutton, and G. L. Hazelbauer. 1994. Deducing the organization of a transmembrane domain by disulfide cross-linking. The bacterial chemoreceptor Trg. J. Biol. Chem. 269:29920-29927.
32. Lee, G. F., D. P. Dutton, and G. L. Hazelbauer. 1995. Identification of functionally important helical faces in transmembrane segments by scanning mutagenesis. Proc. Natl. Acad. Sci. USA 92:5416-5420.
33. Lee, G. F., M. R. Lebert, A. A. Lilly, and G. L. Hazelbauer. 1995. Transmembrane signaling characterized in bacterial chemoreceptors by using sulfhydryl cross-linking in vivo. Proc. Natl. Acad. Sci. USA 92:3391-3395.
34. Li, S. C., N. K. Goto, K. A. Williams, and C. M. Deber. 1996. Alpha-helical, but not beta-sheet, propensity of proline is determined by peptide environment. Proc. Natl. Acad. Sci. USA 93:6676-6681.
35. Lu, J., and C. Deutsch. 2001. Pegylation: a method for assessing topological accessibilities in Kv1.3. Biochemistry 40:13288-13301.
36. Ma, Q. 2001. HAMP domain and signaling mechanism of the Aer protein. Ph.D. dissertation. Loma Linda University, Loma Linda, CA.
37. Ma, Q., M. S. Johnson, and B. L. Taylor. 2005. Genetic analysis of the HAMP domain of the Aer aerotaxis sensor localizes flavin adenine dinucleotide-binding determinants to the AS-2 helix. J. Bacteriol. 187:193-201.
38. Ma, Q., F. Roy, S. Herrmann, B. L. Taylor, and M. S. Johnson. 2004. The Aer protein of Escherichia coli forms a homodimer independent of the signaling domain and flavin adenine dinucleotide binding. J. Bacteriol. 186:7456-7459.
39. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
40. McGuffin, L. J., and D. T. Jones. 2003. Benchmarking secondary structure prediction for fold recognition. Proteins 52:166-175.
41. Miller, A. F., and J. J. Falke. 2004. Chemotaxis receptors and signaling. Adv. Protein Chem. 68:393-444.
42. Miller, A. S., and J. J. Falke. 2004. Side chains at the membrane-water interface modulate the signaling state of a transmembrane receptor. Biochemistry 43:1763-1770.
43. Milligan, D. L., and D. E. Koshland, Jr. 1988. Site-directed cross-linking. Establishing the dimeric structure of the aspartate receptor of bacterial chemotaxis. J. Biol. Chem. 263:6268-6275.
44. Nilsson, I., and G. von Heijne. 1998. Breaking the camel's back: proline-induced turns in a model transmembrane helix. J. Mol. Biol. 284:1185-1189.
45. Overath, P., M. Brenner, T. Gulik-Krzywicki, E. Shechter, and L. Letellier. 1975. Lipid phase transitions in cytoplasmic and outer membranes of Escherichia coli. Biochim. Biophys. Acta 389:358-369.
46. Pakula, A. A., and M. I. Simon. 1992. Determination of transmembrane protein structure by disulfide cross-linking: the Escherichia coli Tar receptor. Proc. Natl. Acad. Sci. USA 89:4144-4148.
47. Parkinson, J. S., P. Ames, and C. A. Studdert. 2005. Collaborative signaling by bacterial chemoreceptors. Curr. Opin. Microbiol. 8:116-121.
48. Parkinson, J. S., and S. E. Houts. 1982. Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J. Bacteriol. 151:106-113.
49. Pasquier, C., V. J. Promponas, G. A. Palaios, J. S. Hamodrakas, and S. J. Hamodrakas. 1999. A novel method for predicting transmembrane segments in proteins based on a statistical analysis of the SwissProt database: the PRED-TMR algorithm. Protein Eng. 12:381-385.
50. Persson, B., and P. Argos. 1994. Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol. 237:182-192.
51. Persson, B., and P. Argos. 1996. Topology prediction of membrane proteins. Protein Sci. 5:363-371.
52. Rebbapragada, A., M. S. Johnson, G. P. Harding, A. J. Zuccarelli, H. M. Fletcher, I. B. Zhulin, and B. L. Taylor. 1997. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc. Natl. Acad. Sci. USA 94:10541-10546.
53. Rees, D. C., L. DeAntonio, and D. Eisenberg. 1989. Hydrophobic organization of membrane proteins. Science 245:510-513.
54. Ren, J., S. Lew, J. Wang, and E. London. 1999. Control of the transmembrane orientation and interhelical interactions within membranes by hydrophobic helix length. Biochemistry 38:5905-5912.
55. Ren, J., S. Lew, Z. Wang, and E. London. 1997. Transmembrane orientation of hydrophobic alpha-helices is regulated both by the relationship of helix length to bilayer thickness and by the cholesterol concentration. Biochemistry 36:10213-10220.
56. Repik, A., A. Rebbapragada, M. S. Johnson, J. O. Haznedar, I. B. Zhulin, and B. L. Taylor. 2000. PAS domain residues involved in signal transduction by the Aer redox sensor of Escherichia coli. Mol. Microbiol. 36:806-816.
57. Rost, B. 1996. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 266:525-539.
58. Rost, B., R. Casadio, P. Fariselli, and C. Sander. 1995. Transmembrane helices predicted at 95% accuracy. Protein Sci. 4:521-533.
59. Seligman, L., J. Bailey, and C. Manoil. 1995. Sequences determining the cytoplasmic localization of a chemoreceptor domain. J. Bacteriol. 177:2315-2320.
60. Stultz, C. M., R. Nambudripad, R. H. Lathrop, and J. V. White. 1997. Predicting protein structure with probabilistic models, p. 447-506. In N. Allewell and C. Woodward (ed.), Protein structural biology in bio-medical research, vol. 22B. JAI Press, Greenwich, Conn.
61. Stultz, C. M., J. V. White, and T. F. Smith. 1993. Structural analysis based on state-space modeling. Protein Sci. 2:305-314.
62. Taylor, B. L., and I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
63. Tusnady, G. E., and I. Simon. 2001. The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849-850.
64. von Heijne, G. 1992. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225:487-494.
65. Watts, K. J., Q. Ma, M. S. Johnson, and B. L. Taylor. 2004. Interactions between the PAS and HAMP domains of the Escherichia coli aerotaxis receptor Aer. J. Bacteriol. 186:7440-7449.
66. White, J. V., C. M. Stultz, and T. F. Smith. 1994. Protein classification by stochastic modeling and optimal filtering of amino-acid sequences. Math. Biosci. 119:35-75.
67. Yau, W. M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry 37:14713-14718.
68. Zhulin, I. B., B. L. Taylor, and R. Dixon. 1997. PAS domain S-boxes in Archaea, Bacteria and sensors for oxygen and redox. Trends Biochem. Sci. 22:331-333.