Detecting molecular interactions that stabilize, activate and guide ligand-binding of the sodium/proton antiporter MjNhaP1 from Methanococcus jannaschii

Journal of Structural Biology

Volumn 159, Issue 2 SPEC. ISS., 2007, Pages 290-301

  Kedrov, Alexej ^a   Wegmann, Susanne ^a   Smits, Sander H J ^b   Goswami, Panchali ^b   Baumann, Hella ^a   Muller, Daniel J ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Activation; Atomic force microscopy; Membrane proteins; MjNhaP1; Molecular interactions; Single molecule force spectroscopy

Indexed keywords

METHANOCALDOCOCCUS JANNASCHII; VERTEBRATA;

EID: 34447642312     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.02.010     Document Type: Article

References (59)

1. Abramson J., Iwata S., and Kaback H.R. Lactose permease as a paradigm for membrane transport proteins. Mol. Membr. Biol. 21 (2004) 227-236
2. Abramson J., Smirnova I., Kasho V., Verner G., Kaback H.R., and Iwata S. Structure and mechanism of the lactose permease of Escherichia coli. Science 301 (2003) 610-615
3. Agre P., and Kozono D. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 555 (2003) 72-78
4. Albrecht C., et al. DNA: a programmable force sensor. Science 301 (2003) 367-370
5. Arteca G.A., and Li Z. Effect of proline kinks on the mechanical unfolding of alpha-helices. Chem. Phys. Lett. 399 (2004) 496-502
6. Böckmann R.A., Hac A., Heimburg T., and Grubmüller H. Effect of sodium chloride on a lipid bilayer. Biophys. J. 85 (2003) 1647-1655
7. Bowie J.U. Solving the membrane protein folding problem. Nature 438 (2005) 581-589
8. Bult C.J., et al. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273 (1996) 1058-1073
9. Butt H.J., and Jaschke M. Calculation of thermal noise in atomic force microscopy. Nanotechnology 6 (1995) 1-7
10. Caffrey M. Membrane protein crystallization. J. Struct. Biol. 142 (2003) 108-132
11. Cisneros D.A., Oesterhelt D., and Müller D.J. Probing origins of molecular interactions stabilizing the membrane proteins halorhodopsin and bacteriorhodopsin. Structure (Camb) 13 (2005) 235-242
12. Dibrov P., Young P.G., and Fliegel L. Functional analysis of amino acid residues essential for activity in the Na+/H+ exchanger of fission yeast. Biochemistry 37 (1998) 8282-8288
13. Engel A., and Müller D.J. Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7 (2000) 715-718
14. Engelman D.M., et al. Membrane protein folding: beyond the two stage model. FEBS Lett. 555 (2003) 122-125
15. Frederix P.L., Akiyama T., Staufer U., Gerber C., Fotiadis D., Müller D.J., and Engel A. Atomic force bio-analytics. Curr. Opin. Chem. Biol. 7 (2003) 641-647
16. Garidel P., and Blume A. 1,2-Dimyristoyl-sn-glycero-3-phosphoglycerol (DMPG) monolayers: influence of temperature, pH, ionic strength and binding of alkaline earth cations. Chem. Phys. Lipids 138 (2005) 50-59
17. Hellmer J., Patzold R., and Zeilinger C. Identification of a pH regulated Na(+)/H(+) antiporter of Methanococcus jannaschii. FEBS Lett. 527 (2002) 245-249
18. Hellmer J., Teubner A., and Zeilinger C. Conserved arginine and aspartate residues are critical for function of MjNhaP1, a Na+/H+ antiporter of M. jannaschii. FEBS Lett. 542 (2003) 32-36
19. Hunte C., Screpanti E., Venturi M., Rimon A., Padan E., and Michel H. Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435 (2005) 1197-1202
20. Inoue H., Noumi T., Tsuchiya T., and Kanazawa H. Essential aspartic acid residues, Asp-133, Asp-163 and Asp-164, in the transmembrane helices of a Na+/H+ antiporter (NhaA) from Escherichia coli. FEBS Lett. 363 (1995) 264-268
21. Janovjak H., Kedrov A., Cisneros D.A., Sapra T., and Müller D.J. Imaging and detecting molecular interactions of single transmembrane proteins. Neurobiol. Aging 27 (2006) 546-561
22. Janovjak H., Kessler M., Oesterhelt D., Gaub H., and Müller D.J. Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 22 (2003) 5220-5229
23. Janshoff A., Neitzert M., Oberdorfer Y., and Fuchs H. Force spectroscopy of molecular systems-single molecule spectroscopy of polymers and biomolecules. Angew. Chem. Int. Ed. Engl. 39 (2000) 3212-3237
24. Junker J.P., Hell K., Schlierf M., Neupert W., and Rief M. Influence of substrate binding on the mechanical stability of mouse dihydrofolate reductase. Biophys. J. 89 (2005) L46-L48
25. Kaback H.R., Sahin-Toth M., and Weinglass A.B. The kamikaze approach to membrane transport. Nat. Rev. Mol. Cell Biol. 2 (2001) 610-620
26. Karmazyn M., Gan X.T., Humphreys R.A., Yoshida H., and Kusumoto K. The myocardial Na(+)-H(+) exchange: structure, regulation, and its role in heart disease. Circ. Res. 85 (1999) 777-786
27. Karmazyn M., Sawyer M., and Fliegel L. The Na(+)/H(+) exchanger: a target for cardiac therapeutic intervention. Curr. Drug Targets Cardiovasc. Haematol. Disord. 5 (2005) 323-335
28. Kedrov A., Janovjak H., Sapra K.T., and Müller D.J. Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 233-260
29. Kedrov A., Krieg M., Ziegler C., Kühlbrandt W., and Müller D.J. Locating ligand binding and activation of a single antiporter. EMBO Rep. 6 (2005) 668-674
30. Kedrov A., Ziegler C., Janovjak H., Kühlbrandt W., and Müller D.J. Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy. J. Mol. Biol. 340 (2004) 1143-1152
31. Kedrov A., Ziegler C., and Müller D.J. Differentiating ligand and inhibitor interactions of a single antiporter. J. Mol. Biol. 362 (2006) 925-932
32. Kessler M., and Gaub H. Unfolding barriers in bacteriorhodopsin probed from the cytoplasmic and the extracellular side by AFM. Structure 14 (2006) 521-527
33. Kozachkov L., Herz K., and Padan E. Functional and structural interactions of the transmembrane domain X of NhaA, Na(+)/H(+) antiporter of Escherichia coli, at physiological pH. Biochemistry. 46 (2007) 2419-2430
34. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature 227 (1970) 680-685
35. Leavitt S., and Freire E. Direct measurement of protein binding energetics by isothermal titration calorimetry. Curr. Opin. Struct. Biol. 11 (2001) 560-566
36. Leckband D. Force as a probe of membrane protein structure and function. Curr. Opin. Struct. Biol. 11 (2001) 433-439
37. MacKinnon R. Potassium channels. FEBS Lett. 555 (2003) 62-65
38. Marko J.F., and Siggia E.D. Stretching DNA. Macromolecules 28 (1995) 8759-8770
39. Müller D.J., Kessler M., Oesterhelt F., Möller C., Oesterhelt D., and Gaub H. Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 83 (2002) 3578-3588
40. Müller D.J., Sapra T., Scheuring S., Kedrov A., Frederix P.L., Fotiadis D., and Engel A. Single-molecule studies of membrane proteins. Curr. Opin. Struct. Biol. 16 (2006) 489-495
41. Murga M.L.F., Bernik D., de Valdez G.F., and Disalvo A.E. Permeability and stability properties of membranes formed by lipids extracted from Lactobacillus acidophilus grown at different temperatures. Arch. Biochem. Biophys. 364 (1999) 115-121
42. Nury H., Dahout-Gonzalez C., Trezeguet V., Lauquin G.J., Brandolin G., and Pebay-Peyroula E. Relations between structure and function of the mitochondrial ADP/ATP carrier. Annu. Rev. Biochem. 75 (2006) 713-741
43. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H.E., and Müller D.J. Unfolding pathways of individual bacteriorhodopsins. Science 288 (2000) 143-146
44. Padan E., Bibi E., Ito M., and Krulwich T.A. Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717 (2005) 67-88
45. Padan E., Tzubery T., Herz K., Kozachkov L., Rimon A., and Galili L. NhaA of Escherichia coli, as a model of a pH-regulated Na+/H+ antiporter. Biochim. Biophys. Acta 1658 (2004) 2-13
46. Padan E., Venturi M., Gerchman Y., and Dover N. Na(+)/H(+) antiporters. Biochim. Biophys. Acta 1505 (2001) 144-157
47. Rief M., and Grubmuller H. Force spectroscopy of single biomolecules. Chemphyschem 3 (2002) 255-261
48. Sapra K.T., Besir H., Oesterhelt D., and Müller D.J. Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J. Mol. Biol. 355 (2006) 640-650
49. Sapra T., Park P.S., Filipek S., Engel A., Müller D.J., and Palczewski K. Detecting molecular interactions that stabilize native bovine rhodopsin. J. Mol. Biol. 358 (2006) 255-269
50. Scheuring S. AFM studies of the supramolecular assembly of bacterial photosynthetic core-complexes. Curr. Opin. Chem. Biol. 10 (2006) 387-393
51. Scheuring S., Müller D.J., Stahlberg H., Engel H.A., and Engel A. Sampling the conformational space of membrane protein surfaces with the AFM. Eur. Biophys. J. Biophys. Lett. 31 (2002) 172-178
52. Simon E., Clotet J., Calero F., Ramos J., and Arino J. A screening for high copy supressors of the sit4 hal3 synthetically lethal phenotype revelas a role for the yeast Nha1 antipoter in cell cycle regulation. J. Biol. Chem. 276 (2001) 29740-29747
53. Spink C.H., and Wellman S.E. Thermal denaturation as tool to study DNA-ligand interactions. Methods Enzymol. 340 (2001) 193-211
54. Stahlberg H., Engel A., and Philippsen A. Assessing the structure of membrane proteins: combining different methods gives the full picture. Biochem. Cell Biol. 80 (2002) 563-568
55. Taglicht D., Padan E., and Schuldiner S. Overproduction and purification of a functional Na+/H+ antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266 (1991) 11289-11294
56. Vinothkumar K.R., Smits S.H., and Kühlbrandt W. pH-induced structural change in a sodium/proton antiporter from Methanococcus jannaschii. EMBO J. 24 (2005) 2720-2729
57. Werten P.J., Remigy H.W., de Groot B.L., Fotiadis D., Philippsen A., Stahlberg H., Grubmuller H., and Engel A. Progress in the analysis of membrane protein structure and function. FEBS Lett. 529 (2002) 65-72
58. Wiebe C.A., DiBattista E.R., and Fliegel L. Functional role of polar amino acid residues in Na+/H+ exchangers. Biochem. J. 357 (2001) 1-10
59. Yamashita A., Singh S.K., Kawate T., Jin Y., and Gouaux E. Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437 (2005) 215-223