Crystal structure of the potassium-importing KdpFABC membrane complex

Nature

Volumn 546, Issue 7660, 2017, Pages 681-685

  Huang, Ching Shin ^a   Pedersen, Bjørn Panyella ^b   Stokes, David L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM); COUNTERION; INWARDLY RECTIFYING POTASSIUM CHANNEL; POTASSIUM CHANNEL SUBUNIT KDPA; POTASSIUM CHANNEL SUBUNIT KDPB; POTASSIUM ION; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CATION TRANSPORT PROTEIN; ESCHERICHIA COLI PROTEIN; KDPF PROTEIN, E COLI; MEMBRANE PROTEIN; POTASSIUM; POTASSIUM TRANSLOCATING KDP-ATPASE, E COLI;

BACTERIUM; CHEMICAL REACTION; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME; ENZYME ACTIVITY; HOMEOSTASIS; HYDROLYSIS; OSMOREGULATION; POTASSIUM; PROTEIN;

ARTICLE; AUTOPHOSPHORYLATION; BINDING SITE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; KDPFABC COMPLEX; MEMBRANE; MUTATION; POTASSIUM CELL LEVEL; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATASES; CATION TRANSPORT PROTEINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PHOSPHORYLATION; POTASSIUM;

EID: 85021640979     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22970     Document Type: Article

References (62)

1. Greie, J. C. The KdpFABC complex from Escherichia coli: a chimeric K+ transporter merging ion pumps with ion channels. Eur. J. Cell Biol. 90, 705-710 (2011).
2. Epstein, W. The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 75, 293-320 (2003).
3. Diskowski, M., Mikusevic, V., Stock, C. & Hanelt, I. Functional diversity of the superfamily of K+ transporters to meet various requirements. Biol. Chem. 396, 1003-1014 (2015).
4. Epstein, W., Whitelaw, V. & Hesse, J. A K+ transport ATPase in Escherichia coli. J. Biol. Chem. 253, 6666-6668 (1978).
5. Buurman, E. T., Kim, K. T. & Epstein, W. Genetic evidence for two sequentially occupied K+ binding sites in the Kdp transport ATPase. J. Biol. Chem. 270, 6678-6685 (1995).
6. Dorus, S., Mimura, H. & Epstein, W. Substrate-binding clusters of the K+ -transporting Kdp ATPase of Escherichia coli investigated by amber suppression scanning mutagenesis. J. Biol. Chem. 276, 9590-9598 (2001).
7. Siebers, A. & Altendorf, K. Characterization of the phosphorylated intermediate of the K+-translocating Kdp-ATPase from Escherichia coli. J. Biol. Chem. 264, 5831-5838 (1989).
8. Irzik, K. et al. The KdpC subunit of the Escherichia coli K+ -transporting KdpB P-type ATPase acts as a catalytic chaperone. FEBS J. 278, 3041-3053 (2011).
9. Gassel, M., Mollenkamp, T., Puppe, W. & Altendorf, K. The KdpF subunit is part of the K+-translocating Kdp complex of Escherichia coli and is responsible for stabilization of the complex in vitro. J. Biol. Chem. 274, 37901-37907 (1999).
10. Moller, J. V., Olesen, C., Winther, A. M. & Nissen, P. The sarcoplasmic Ca2+- ATPase: design of a perfect chemi-osmotic pump. Q. Rev. Biophys. 43, 501-566 (2010).
11. Cao, Y. et al. Crystal structure of a potassium ion transporter, TrkH. Nature 471, 336-340 (2011).
12. Vieira-Pires, R. S., Szollosi, A. & Morais-Cabral, J. H. The structure of the KtrAB potassium transporter. Nature 496, 323-328 (2013).
13. Hanelt, I. et al. Gain of function mutations in membrane region M2C2 of KtrB open a gate controlling K+ transport by the KtrAB system from Vibrio alginolyticus. J. Biol. Chem. 285, 10318-10327 (2010).
14. Fendler, K., Drose, S., Epstein, W., Bamberg, E. & Altendorf, K. The Kdp-ATPase of Escherichia coli mediates an ATP-dependent, K+ -independent electrogenic partial reaction. Biochemistry 38, 1850-1856 (1999).
15. Toyoshima, C., Nakasako, M., Nomura, H. & Ogawa, H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405, 647-655 (2000).
16. Bramkamp, M., Altendorf, K. & Greie, J. C. Common patterns and unique features of P-type ATPases: a comparative view on the KdpFABC complex from Escherichia coli (Review). Mol. Membr. Biol. 24, 375-386 (2007).
17. Zhou, Y., Morais-Cabral, J. H., Kaufman, A. & MacKinnon, R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414, 43-48 (2001).
18. Gassel, M., Siebers, A., Epstein, W. & Altendorf, K. Assembly of the Kdp complex, the multi-subunit K+-transport ATPase of Escherichia coli. Biochim. Biophys. Acta 1415, 77-84 (1998).
19. Sitsel, O. et al. Structure and function of Cu(I)- and Zn(II)-ATPases. Biochemistry 54, 5673-5683 (2015).
20. Miller, A. N. & Long, S. B. Crystal structure of the human two-pore domain potassium channel K2P1. Science 335, 432-436 (2012).
21. Payandeh, J., Gamal El-Din, T. M., Scheuer, T., Zheng, N. & Catterall, W. A. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486, 135-139 (2012).
22. Rasaiah, J. C., Garde, S. & Hummer, G. Water in nonpolar confinement: from nanotubes to proteins and beyond. Annu. Rev. Phys. Chem. 59, 713-740 (2008).
23. Cao, Y. et al. Gating of the TrkH ion channel by its associated RCK protein TrkA. Nature 496, 317-322 (2013).
24. Olesen, C., Sorensen, T. L., Nielsen, R. C., Moller, J. V. & Nissen, P. Dephosphorylation of the calcium pump coupled to counterion occlusion. Science 306, 2251-2255 (2004).
25. Puppe, W., Siebers, A. & Altendorf, K. The phosphorylation site of the Kdp-ATPase of Escherichia coli: site-directed mutagenesis of the aspartic acid residues 300 and 307 of the KdpB subunit. Mol. Microbiol. 6, 3511-3520 (1992).
26. Bramkamp, M. & Altendorf, K. Single amino acid substitution in the putative transmembrane helix V in KdpB of the KdpFABC complex of Escherichia coli uncouples ATPase activity and ion transport. Biochemistry 44, 8260-8266 (2005).
27. Becker, D., Fendler, K., Altendorf, K. & Greie, J. C. The conserved dipole in transmembrane helix 5 of KdpB in the Escherichia coli KdpFABC P-type ATPase is crucial for coupling and the electrogenic K+ -translocation step. Biochemistry 46, 13920-13928 (2007).
28. Liu, S. & Lockless, S. W. Equilibrium selectivity alone does not create K+ -selective ion conduction in K+ channels. Nat. Commun. 4, 2746 (2013).
29. Toyoshima, C., Nomura, H. & Tsuda, T. Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432, 361-368 (2004).
30. Moller, J. V., Lenoir, G., Le Maire, M., Juul, B. S. & Champeil, P. Proteolytic studies on the transduction mechanism of sarcoplasmic reticulum Ca2+- ATPase: common features with other P-type ATPases. Ann. NY Acad. Sci. 986, 82-89 (2003).
31. Walderhaug, M. O. et al. KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J. Bacteriol. 174, 2152-2159 (1992).
32. Siebers, A. & Altendorf, K. The K+-translocating Kdp-ATPase from Escherichia coli. Purification, enzymatic properties and production of complex- and subunit-specific antisera. Eur. J. Biochem. 178, 131-140 (1988).
33. Laimins, L. A., Rhoads, D. B. & Epstein, W. Osmotic control of kdp operon expression in Escherichia coli. Proc. Natl Acad. Sci. USA 78, 464-468 (1981).
34. Doublie, S. Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 363, 91-108 (2007).
35. Warren, G. B., Toon, P. A., Birdsall, N. J. M., Lee, A. G. & Metcalfe, J. C. Reversible lipid titrations of the activity of pure adenosine triphosphatase-lipid complexes. Biochemistry 13, 5501-5507 (1974).
36. Wheeler, M. J., Russi, S., Bowler, M. G. & Bowler, M. W. Measurement of the equilibrium relative humidity for common precipitant concentrations: facilitating controlled dehydration experiments. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 68, 111-114 (2012).
37. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
38. Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485 (2010).
39. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M. & Paciorek, W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59, 2023-2030 (2003).
40. Abrahams, J. P. & Leslie, A. G. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 52, 30-42 (1996).
41. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
42. Gourdon, P. et al. Crystal structure of a copper-transporting PIB-type ATPase. Nature 475, 59-64 (2011).
43. van der Laan, M., Gassel, M. & Altendorf, K. Characterization of amino acid substitutions in KdpA, the K+-binding and -translocating subunit of the KdpFABC complex of Escherichia coli. J. Bacteriol. 184, 5491-5494 (2002).
44. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
45. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
46. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
47. Petrek, M. et al. CAVER: a new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics 7, 316 (2006).
48. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
49. Eser, E., Can, T. & Ferhatosmanoǧlu, H. Div-BLAST: diversification of sequence search results. PLoS ONE 9, e115445 (2014).
50. Pei, J., Kim, B. H. & Grishin, N. V. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 36, 2295-2300 (2008).
51. Hu, G. B., Rice, W. J., Drose, S., Altendorf, K. & Stokes, D. L. Three-dimensional structure of the KdpFABC complex of Escherichia coli by electron tomography of two-dimensional crystals. J. Struct. Biol. 161, 411-418 (2008).
52. Heitkamp, T., Bottcher, B. & Greie, J. C. Solution structure of the KdpFABC P-type ATPase from Escherichia coli by electron microscopic single particle analysis. J. Struct. Biol. 166, 295-302 (2009).
53. Heitkamp, T. et al. K+ -translocating KdpFABC P-type ATPase from Escherichia coli acts as a functional and structural dimer. Biochemistry 47, 3564-3575 (2008).
54. Schrader, M. et al. Replacement of glycine 232 by aspartic acid in the KdpA subunit broadens the ion specificity of the K(+)-translocating KdpFABC complex. Biophys. J. 79, 802-813 (2000).
55. Bertrand, J., Altendorf, K. & Bramkamp, M. Amino acid substitutions in putative selectivity filter regions III and IV in KdpA alter ion selectivity of the KdpFABC complex from Escherichia coli. J. Bacteriol. 186, 5519-5522 (2004).
56. Sorensen, T. L., Moller, J. V. & Nissen, P. Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science 304, 1672-1675 (2004).
57. Jensen, A. M., Sorensen, T. L., Olesen, C., Moller, J. V. & Nissen, P. Modulatory and catalytic modes of ATP binding by the calcium pump. EMBO J. 25, 2305-2314 (2006).
58. Toyoshima, C. & Mizutani, T. Crystal structure of the calcium pump with a bound ATP analogue. Nature 430, 529-535 (2004).
59. Bond, C. S. & Schuttelkopf, A. W. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D Biol. Crystallogr. 65, 510-512 (2009).
60. Pedersen, B. P., Buch-Pedersen, M. J., Morth, J. P., Palmgren, M. G. & Nissen, P. Crystal structure of the plasma membrane proton pump. Nature 450, 1111-1114 (2007).
61. Andersson, M. et al. Copper-transporting P-type ATPases use a unique ion-release pathway. Nat. Struct. Mol. Biol. 21, 43-48 (2014).
62. Laursen, M., Yatime, L., Nissen, P. & Fedosova, N. U. Crystal structure of the high-affinity Na+ K+ -ATPase-ouabain complex with Mg2+ bound in the cation binding site. Proc. Natl Acad. Sci. USA 110, 10958-10963 (2013).