Revealing the ligand binding site of NhaA Na+/H+ antiporter and its pH dependence

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 38150-38157

  Maes, Michal ^a   Rimon, Abraham ^a   Kozachkov Magrisso, Lena ^a   Friedler, Assaf ^a   Padan, Etana ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPORTERS; LIGAND-BINDING SITES; MUTATIONAL ANALYSIS; PH DEPENDENCE; PH-DEPENDENT; SINGLE BINDING SITES;

LIGANDS;

SODIUM;

SODIUM PROTON EXCHANGE PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL PH; CONTROLLED STUDY; ENTHALPY; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; BINDING SITES; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; KINETICS; LIGANDS; LITHIUM; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SODIUM-HYDROGEN ANTIPORTER; THERMODYNAMICS;

EID: 84868306588     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.391128     Document Type: Article

References (45)

1. West, I. C., and Mitchell, P. (1974) Proton/sodium ion antiport in Escherichia coli. Biochem. J. 144, 87-90
2. Padan, E., Bibi, E., Ito, M., and Krulwich, T. A. (2005) Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717, 67-88 (Pubitemid 41682429)
3. Padan, E. (2008) The enlightening encounter between structure and function in the NhaA Na+-H+ antiporter. Trends Biochem. Sci. 33, 435-443
4. Krulwich, T. A., Sachs, G., and Padan, E. (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat. Rev. Microbiol. 9, 330-343
5. + exchanger. J. Mol. Cell. Cardiol. 44, 228-237
6. Brett, C. L., Donowitz, M., and Rao, R. (2005) Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 288, C223-C239 (Pubitemid 40105332)
7. + antiporter sharing evolutionary origins with bacterial NhaA may be a candidate gene for essential hypertension. Proc. Natl. Acad. Sci. U.S.A. 104, 18677-18681 (Pubitemid 350210756)
8. + antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266, 11289-11294 (Pubitemid 21906945)
9. Taglicht, D., Padan, E., and Schuldiner, S. (1993) Proton-sodium stoichiometry of NhaA, an electrogenic antiporter from Escherichia coli. J. Biol. Chem. 268, 5382-5387 (Pubitemid 23090853)
10. Orlowski, J., and Grinstein, S. (2007) Emerging roles of alkali cation/proton exchangers in organellar homeostasis. Curr. Opin. Cell Biol. 19, 483-492 (Pubitemid 47271963)
11. + antiporter and insights into mechanism of action and regulation by pH. Nature 435, 1197-1202 (Pubitemid 40943079)
12. Schushan, M., Rimon, A., Haliloglu, T., Forrest, L. R., Padan, E., and Ben- Tal, N. (2012) A model structure of a periplasm-facing state of the NhaA antiporter suggests the molecular underpinnings of pH-induced conformational changes. J. Biol. Chem. 287, 18249-18261
13. Schushan, M., Xiang, M., Bogomiakov, P., Padan, E., Rao, R., and Ben-Tal, N. (2010) Model-guided mutagenesis drives functional studies of human NHA2, implicated in hypertension. J. Mol. Biol. 396, 1181-1196
14. Padan, E., Kozachkov, L., Herz, K., and Rimon, A. (2009) NhaA crystal structure: functional-structural insights. J. Exp. Biol. 212, 1593-1603
15. Hu, N. J., Iwata, S., Cameron, A. D., and Drew, D. (2011) Crystal structure of a bacterial homologue of the bile acid sodium symporter ASBT. Nature 478, 408-411
16. + exchanger 1 (NHE1): functional and clinical implications. J. Biol. Chem. 282, 37854-37863
17. + antiporter of Escherichia coli, at physiological pH. Biochemistry 46, 2419-2430 (Pubitemid 46362416)
18. + antiporter (NhaA) from Escherichia coli. FEBS Lett. 363, 264-268
19. + antiporter (NhaA) from Escherichia coli by random mutagenesis. J. Biochem. 121, 661-670 (Pubitemid 27170848)
20. + antiporter of Escherichia coli. Biochemistry 41, 609-617 (Pubitemid 34062032)
21. + antiporter in Escherichia coli. J. Biol. Chem. 268, 1729-1734 (Pubitemid 23033565)
22. + antiporter system(s). J. Biol. Chem. 264, 20297-20302 (Pubitemid 20009210)
23. + antiporter of Escherichia coli, is exposed and faces the cell exterior. J. Biol. Chem. 272, 1761-1768 (Pubitemid 27043265)
24. +. J. Biol. Chem. 282, 26810-26821 (Pubitemid 47501951)
25. Rothman, A. (1997) A Study of the Structure/Function Relation of NhaA, a Sodium Proton Antiporter from Escherichia coli. Ph.D. dissertation, Hebrew University of Jerusalem, Jerusalem
26. + antiporter. J. Biol. Chem. 284, 6337-6347
27. Fisher, C. L., and Pei, G. K. (1997) Modification of a PCR-based sitedirected mutagenesis method. BioTechniques 23, 570-571, 574
28. Rosen, B. P. (1986) Ion extrusion systems in Escherichia coli. Methods Enzymol. 125, 328-336 (Pubitemid 16072648)
29. + antiporter gene of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 84, 2615-2619 (Pubitemid 17064703)
30. Schuldiner, S., and Fishkes, H. (1978) Sodium-proton antiport in isolated membrane vesicles of Escherichia coli. Biochemistry 17, 706-711 (Pubitemid 8295115)
31. + antiporter (NhaA) protein from Helicobacter pylori required for ion transport and pH sensing. J. Biol. Chem. 278, 21467-21473 (Pubitemid 36792543)
32. + antiporter of Escherichia coli involves loop VIII-IX, plays a role in the pH response of the protein, and is maintained by the pure protein in dodecyl maltoside. J. Biol. Chem. 274, 24617-24624
33. + antiporter as well as the growth phenotype of Escherichia coli. J. Biol. Chem. 273, 26470-26476 (Pubitemid 28471655)
34. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
35. + antiporter of Escherichia coli. J. Biol. Chem. 279, 23104-23113 (Pubitemid 38685615)
36. + and H+ circulation in cells. J. Bioenerg. Biomembr. 25, 647-669 (Pubitemid 24012898)
37. 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 (Pubitemid 46041309)
38. + antiporter NhaA of Escherichia coli. Biochim. Biophys. Acta 1709, 240-250 (Pubitemid 41254217)
39. Williams, K. A., Geldmacher-Kaufer, U., Padan, E., Schuldiner, S., and Kühlbrandt, W. (1999) Projection structure of NhaA, a secondary transporter from Escherichia coli, at 4.0 Ä resolution. EMBO J. 18, 3558-3563 (Pubitemid 29308836)
40. + antiporter of Escherichia coli, in the membrane and its functional and structural consequences. Biochemistry 40, 3403-3412 (Pubitemid 32221644)
41. + antiporter of Helicobacter pylori: topology and function of the residues, including two consecutive essential aspartate residues. Biochemistry 45, 14834-14842 (Pubitemid 44907000)
42. Screpanti, E., and Hunte, C. (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J. Struct. Biol. 159, 261-267 (Pubitemid 47095395)
43. Olkhova, E., Padan, E., and Michel, H. (2007) The influence of protonation states on the dynamics of the NhaA antiporter from Escherichia coli. Biophys. J. 92, 3784-3791 (Pubitemid 46910566)
44. Harms, M. J., Schlessman, J. L., Sue, G. R., and García-Moreno, B. (2011) Arginine residues at internal positions in a protein are always charged. Proc. Natl. Acad. Sci. U.S.A. 108, 18954-18959
45. + antiporters constructed from NhaA of Helicobacter pylori and Escherichia coli: implications for domains of NhaA for pH sensing. J. Biochem. 129, 569-576 (Pubitemid 32299278)