Molecular basis of transport and regulation in the Na+/betaine symporter BetP

Nature

Volumn 458, Issue 7234, 2009, Pages 47-52

  Ressl, Susanne ^a   Terwisscha Van Scheltinga, Anke C ^a   Vonrhein, Clemens ^b   Ott, Vera ^c   Ziegler, Christine ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b GLOBAL PHASING LTD   (United Kingdom)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETAINE; PROTEIN BETP; SODIUM; UNCLASSIFIED DRUG;

CYTOLOGY; HYDRATION; MEMBRANE; MOLECULAR ANALYSIS; OSMOREGULATION; PRESSURE;

ARTICLE; CORYNEBACTERIUM GLUTAMICUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TRANSPORT;

BACTERIAL PROTEINS; BETAINE; BINDING SITES; CARRIER PROTEINS; CORYNEBACTERIUM GLUTAMICUM; CRYSTALLOGRAPHY, X-RAY; ION TRANSPORT; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SODIUM; STRUCTURE-ACTIVITY RELATIONSHIP;

CORYNEBACTERIUM GLUTAMICUM;

EID: 61949479923     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature07819     Document Type: Article

References (59)

1. Burg, M. B. Molecular basis of osmotic regulation. Am. J. Physiol. 268, F983-F996 (1995).
2. Kinne, R. K. The role of organic osmolytes in osmoregulation: from bacteria to mammals. J. Exp. Zool. 265, 346-355 (1993).
3. Yancey, P. H. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830 (2005).
4. Burg, M. B. & Ferraris, J. D. Intracellular organic osmolytes: function and regulation. J. Biol. Chem. 283, 7309-7313 (2008).
5. Wood, J. M. et al. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp. Biochem. Physiol. A 130, 437-460 (2001).
6. Wood, J. M. Bacterial osmosensing transporters. Methods Enzymol. 428, 77-107 (2007).
7. da Costa, M. S., Santos, H. & Galinski, E. A. An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv. Biochem. Eng. Biotechnol. 61, 117-153 (1998).
8. Roberts, M. F. Osmoadaptation and osmoregulation in archaea. Front. Biosci. 5, D796-D812 (2000).
9. Pflüger, K. & Müller, V. Transport of compatible solutes in extremophiles. J. Bioenerg. Biomembr. 36, 17-24 (2004).
10. Blomberg, A. Osmoresponsive proteins and functional assessment strategies in Saccharomyces cerevisiae. Electrophoresis 18, 1429-1440 (1997).
11. Tuteja, N. Mechanisms of high salinity tolerance in plants. Methods Enzymol. 428, 419-438 (2007).
12. Beck, F. X. & Neuhofer, W. Response of renal medullary cells to osmotic stress. Contrib. Nephrol. 148, 21-34 (2005).
13. Lang, F. Mechanisms and significance of cell volume regulation. J. Am. Coll. Nutr. 26, 613S-623S (2007).
14. Lim, C. H., Bot, A. G., de Jonge, H. R. & Tilly, B. C. Osmosignaling and volume regulation in intestinal epithelial cells. Methods Enzymol. 428, 325-342 (2007).
15. Rösgen, J. Molecular basis of osmolyte effects on protein and metabolites. Methods Enzymol. 428, 459-486 (2007).
16. Garcia-Perez, A. & Burg, M. B. Importance of organic osmolytes for osmoregulation by renal medullary cells. Hypertension 16, 595-602 (1990).
17. Kempf, B. & Bremer, E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319-330 (1998).
18. Empadinhas, N. & da Costa, M. S. Diversity and biosynthesis of compatible solutes in hyper/thermophiles. Int. Microbiol. 9, 199-206 (2006).
19. Athawale, M. V., Dordick, J. S. & Garde, S. Osmolyte trimethylamine-N-oxide does not affect the strength of hydrophobic interactions: origin of osmolyte compatibility. Biophys. J. 89, 858-866 (2005).
20. Peter, H., Burkovski, A. & Krämer, R. Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute betaine. J. Bacteriol. 178, 5229-5234 (1996).
21. Kappes, R. M., Kempf, B. & Bremer, E. Three transport systems for the osmoprotectant betaine operate in Bacillus subtilis: characterization of OpuD. J. Bacteriol. 178, 5071-5079 (1996).
22. Farwick, M., Siewe, R. M. & Krämer, R. Betaine uptake after hyperosmotic shift in Corynebacterium glutamicum. J. Bacteriol. 177, 4690-4695 (1995).
23. Schiller, D., Krämer, R. & Morbach, S. Cation specificity of osmosensing by the betaine carrier BetP of Corynebacterium glutamicum. FEBS Lett. 563, 108-112 (2004).
24. Peter, H., Burkovski, A. & Krämer, R. Osmo-sensing by N- and C-terminal extensions of the betaine uptake system BetP of Corynebacterium glutamicum. J. Biol. Chem. 273, 2567-2574 (1998).
25. Ziegler, C. et al. Projection structure and oligomeric state of the osmoregulated sodium/betaine symporter BetP of Corynebacterium glutamicum. J. Mol. Biol. 337, 1137-1147 (2004).
26. --dependent neurotransmitter transporters. Nature 437, 215-223 (2005).
27. Chang, A. B., Lin, R., Studley, W. K., Tran, C. V. & Saier, M. H. Jr. Phylogeny as a guide to structure and function of membrane transport proteins. Mol. Membr. Biol. 21, 171-181 (2004).
28. +/sugar symport. Science 321, 810-814 (2008).
29. Saier, M. H. J. Families of transmembrane sugar transport proteins. Mol. Microbiol. 35, 699-710 (2000).
30. Weyand, S. et al. Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322, 709-713 (2008).
31. Schiefner, A. et al. Cation-π interactions as determinants for binding of the compatible solutes betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli. J. Biol. Chem. 279, 5588-5596 (2004).
32. Kempson, S. A. & Montrose, M. H. Osmotic regulation of renal betaine transport: transcription and beyond. Pflugers Arch. 449, 227-234 (2004).
33. Borden, L. A. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem. Int. 29, 335-356 (1996).
34. Rapp, M. G. E., Seppälä, S. & von Heijne, G. Identification and evolution of dual-topology membrane proteins. Nature Struct. Mol. Biol. 13, 112-116 (2006).
35. Schiefner, A., Holtmann, G., Diederichs, K., Welte, W. & Bremer, E. Structural basis for the binding of compatible solutes by ProX from the hyperthermophilic archaeon Archaeoglobus fulgidus. J. Biol. Chem. 279, 48270-48281 (2004).
36. Horn, C. et al. Molecular determinants for substrate specificity of the ligand-binding protein OpuAC from Bacillus subtilis for the compatible solutes betaine and proline betaine. J. Mol. Biol. 357, 592-606 (2006).
37. Jardetzky, O. Simple allosteric model for membrane pumps. Nature 211, 969-970 (1966).
38. Bolen, D. W. & Rose, G. D. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem. 77, 339-362 (2008).
39. Tanford, C. Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv. Protein Chem. 24, 1-95 (1970).
40. Kuhlmann, S. I., Terwisscha van Scheltinga, A. C., Bienert, R., Kunte, H. J. & Ziegler, C. Osmoregulated transport of compatible solutes in the halophilic bacterium Halomonas elongata: 1.55 Å high-resolution structure of the periplasmic ectoine-binding protein from TRAP-transporter TeaABC. Biochemistry 47, 9475-9485 (2008).
41. Yernool, D., Boudker, O., Jin, Y. & Gouaux, E. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818 (2004).
42. Forrest, L. R. et al. Mechanism for alternating access in neurotransmitter transporters. Proc. Natl Acad. Sci. USA 105, 10338-10343 (2008).
43. +-leucine transporters. Mol. Membr. Biol. 25, 567-570 (2008).
44. Smicun, Y., Campbell, S. D., Chen, M. A., Gu, H. & Rudnick, G. The role of external loop regions in serotonin transport. Loop scanning mutagenesis of the serotonin transporter external domain. J. Biol. Chem. 274, 36058-36064 (1999).
45. Stephan, M. M., Chen, M. A., Penado, K. M. & Rudnick, G. An extracellular loop region of the serotonin transporter may be involved in the translocation mechanism. Biochemistry 36, 1322-1330 (1997).
46. Palsdottir, H. & Hunte, C. Lipids in membrane protein structures. Biochim. Biophys. Acta 1666, 2-18 (2004).
47. Ott, V., Koch, J., Späte, K., Morbach, S. & Krämer, R. Regulatory properties and interaction of the C- and N-terminal domains of BetP, an osmoregulated betaine transporter from Corynebacterium glutamicum. Biochemistry 47, 12208-12218 (2008).
48. + as an osmotic stimulus. Biochemistry 43, 5583-5591 (2004).
49. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
50. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D 62, 72-82 (2006).
51. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
52. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
53. 1 ATPase. Acta Crystallogr. D 52, 30-42 (1996).
54. Cowtan, K. dm: An automated procedure for phase improvement by density modification. CCP4/ESF-EACBM Newslett. Protein Crystallogr. 31, 34-38 (1994).
55. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
56. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
57. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004).
58. Terwilliger, T. C. et al. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D 64, 61-69 (2008).
59. Lovell, S. C. et al. Structure validation by C-alpha geometry: phi, psi, and C-beta deviation. Proteins Struct. Funct. Genet. 50, 437-450 (2003).