Significance of αthr-349 in the catalytic sites of Escherichia coli ATP synthase

Biochemistry

Volumn 53, Issue 47, 2014, Pages 7376-7385

  Ahmad, Zulfiqar ^a   Winjobi, Mumeenat ^a   Kabir, M Anaul ^b  

^a A T STILL UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF TECHNOLOGY CALICUT   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; X RAYS;

ATP-ASE ACTIVITY; CATALYTIC SITES; DOUBLE MUTATION; OXIDATIVE PHOSPHORYLATION; PHOSPHATE BINDING; TRANSITION STATE STABILIZATION; X RAY STRUCTURE ANALYSIS; X-RAY STRUCTURE;

BINDING SITES;

4 CHLORO 7 NITROBENZOFURAZAN; ADENOSINE TRIPHOSPHATASE; AZIDE; DICYCLOHEXYLCARBODIIMIDE; FLUOROALUMINATE; MUTANT PROTEIN; PHOSPHATE; PHOSPHATE BINDING PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SCANDIUM; THREONINE; 7-CHLORO-4-NITROBENZ-2-OXA-1,3-DIAZOLE; ADENOSINE DIPHOSPHATE; ALUMINUM; DITHIOTHREITOL; ENZYME INHIBITOR; F1F0-ATP SYNTHASE; FLUORINE; FLUOROALUMINUM; NITROBENZENE DERIVATIVE; OXAZOLE DERIVATIVE;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM MUTANT; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME STRUCTURE; ESCHERICHIA COLI; MUTATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; WILD TYPE; X RAY; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MUTAGENESIS;

ESCHERICHIA COLI;

ADENOSINE DIPHOSPHATE; ALUMINUM; AZIDES; CATALYTIC DOMAIN; CELL MEMBRANE; DICYCLOHEXYLCARBODIIMIDE; DITHIOTHREITOL; ENZYME INHIBITORS; ESCHERICHIA COLI; FLUORINE; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; NITROBENZENES; OXAZOLES; THREONINE;

EID: 84915750331     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5013063     Document Type: Article

References (61)

1. Senior, A. E. (2012) Two ATPases J. Biol. Chem. 287, 30049-30062
2. Ahmad, Z. and Cox, J. L. (2014) ATP Synthase: The Right Size Base Model for Nanomotors in Nanomedicine Sci. World J. 2014, 10
3. 1: From catalysis to γεc(10-12) subunit assembly rotation Biochim. Biophys. Acta 1459, 499-505
4. Roy, A., Hutcheon, M. L., Duncan, T. M., and Cingolani, G. (2012) Improved crystallization of Escherichia coli ATP synthase catalytic complex (F1) by introducing a phosphomimetic mutation in subunit ε Acta Crystallogr. F68, 1229-1233
5. Senior, A. E. (1988) ATP synthesis by oxidative phosphorylation Physiol. Rev. 68, 177-231
6. Karrasch, S. and Walker, J. E. (1999) Novel features in the structure of bovine ATP synthase J. Mol. Biol. 290, 379-384
7. Devenish, R. J., Prescott, M., Roucou, X., and Nagley, P. (2000) Insights into ATP synthase assembly and function through the molecular genetic manipulation of subunits of the yeast mitochondrial enzyme complex Biochim. Biophys. Acta 1458, 428-442
8. Abrahams, J. P., Leslie, A. G. W., Lutter, R., and Walker, J. E. (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria Nature 370, 621-628
9. Senior, A. E., Nadanaciva, S., and Weber, J. (2002) The molecular mechanism of ATP synthesis by F1F0-ATP synthase Biochim. Biophys. Acta 1553, 188-211
10. Noji, H. and Yoshida, M. (2001) The rotary machine in the cell, ATP synthase J. Biol. Chem. 276, 1665-1668
11. Weber, J. and Senior, A. E. (2003) ATP synthesis driven by proton transport in F1F0-ATP synthase FEBS Lett. 545, 61-70
12. 1-ATPase Biochim. Biophys. Acta 1458, 310-325
13. Pedersen, P. L. (2007) Transport ATPases into the year 2008: A brief overview related to types, structures, functions and roles in health and disease J. Bioenerg. Biomembr. 39, 349-355
14. Ahmad, Z., Okafor, F., and Laughlin, T. F. (2011) Role of Charged Residues in the Catalytic Sites of Escherichia coli ATP Synthase J. Amino Acids 2011, 785741
15. Ahmad, Z. and Laughlin, T. F. (2010) Medicinal chemistry of ATP synthase: A potential drug target of dietary polyphenols and amphibian antimicrobial peptides Curr. Med. Chem. 17, 2822-2836
16. Senior, A. E. (2007) ATP synthase: Motoring to the finish line Cell 130, 220-221
17. Martin, J. L., Ishmukhametov, R., Hornung, T., Ahmad, Z., and Frasch, W. D. (2014) Anatomy of F1-ATPase powered rotation Proc. Natl. Acad. Sci. U.S.A. 111, 3715-3720
18. Cingolani, G. and Duncan, T. M. (2011) Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation Nat. Struct. Mol. Biol. 18, 701-707
19. Li, W., Brudecki, L. E., Senior, A. E., and Ahmad, Z. (2009) Role of α-subunit VISIT-DG sequence residues Ser-347 and Gly-351 in the catalytic sites of Escherichia coli ATP synthase J. Biol. Chem. 284, 10747-10754
20. Boyer, P. D. (1989) A perspective of the binding change mechanism for ATP synthesis FASEB J. 3, 2164-2178
21. al-Shawi, M. K. and Senior, A. E. (1992) Effects of dimethyl sulfoxide on catalysis in Escherichia coli F1-ATPase Biochemistry 31, 886-891
22. Al-Shawi, M. K., Ketchum, C. J., and Nakamoto, R. K. (1997) The Escherichia coli FOF1 γM23K uncoupling mutant has a higher K0.5 for Pi. Transition state analysis of this mutant and others reveals that synthesis and hydrolysis utilize the same kinetic pathway Biochemistry 36, 12961-12969
23. Lobau, S., Weber, J., and Senior, A. E. (1998) Catalytic site nucleotide binding and hydrolysis in F1F0-ATP synthase Biochemistry 37, 10846-10853
24. Weber, J. and Senior, A. E. (1995) Location and properties of pyrophosphate-binding sites in Escherichia coli F1-ATPase J. Biol. Chem. 270, 12653-12658
25. Perez, J. A., Greenfield, A. J., Sutton, R., and Ferguson, S. J. (1986) Characterisation of phosphate binding to mitochondrial and bacterial membrane-bound ATP synthase by studies of inhibition with 4-chloro-7-nitrobenzofurazan FEBS Lett. 198, 113-118
26. Orriss, G. L., Leslie, A. G., Braig, K., and Walker, J. E. (1998) Bovine F1-ATPase covalently inhibited with 4-chloro-7-nitrobenzofurazan: The structure provides further support for a rotary catalytic mechanism Structure 6, 831-837
27. 2+ADP and aluminium fluoride Structure 8, 567-573
28. 1-ATPase with nucleotide bound to all three catalytic sites: Implications for the mechanism of rotary catalysis Cell 106, 331-341
29. Ahmad, Z. and Senior, A. E. (2005) Modulation of charge in the phosphate binding site of Escherichia coli ATP synthase J. Biol. Chem. 280, 27981-27989
30. Ahmad, Z. and Senior, A. E. (2004) Mutagenesis of residue βArg-246 in the phosphate-binding subdomain of catalytic sites of Escherichia coli F1-ATPase J. Biol. Chem. 279, 31505-31513
31. 1-ATPase J. Biol. Chem. 279, 46057-46064
32. Ahmad, Z. and Senior, A. E. (2005) Identification of phosphate binding residues of Escherichia coli ATP synthase J. Bioenerg. Biomembr. 37, 437-440
33. Ahmad, Z. and Senior, A. E. (2005) Involvement of ATP synthase residues αArg-376, βArg-182, and βLys-155 in Pi binding FEBS Lett. 579, 523-528
34. Ahmad, Z. and Senior, A. E. (2006) Inhibition of the ATPase activity of Escherichia coli ATP synthase by magnesium fluoride FEBS Lett. 580, 517-520
35. Brudecki, L. E., Grindstaff, J. J., and Ahmad, Z. (2008) Role of αPhe-291 residue in the phosphate-binding subdomain of catalytic sites of Escherichia coli ATP synthase Arch. Biochem. Biophys. 471, 168-175
36. Chen, C., Saxena, A. K., Simcoke, W. N., Garboczi, D. N., Pedersen, P. L., and Ko, Y. H. (2006) Mitochondrial ATP synthase. Crystal structure of the catalytic F1 unit in a vanadate-induced transition-like state and implications for mechanism J. Biol. Chem. 281, 13777-13783
37. Andries, K., Verhasselt, P., Guillemont, J., Gohlmann, H. W., Neefs, J. M., Winkler, H., Van Gestel, J., Timmerman, P., Zhu, M., Lee, E., Williams, P., de Chaffoy, D., Huitric, E., Hoffner, S., Cambau, E., Truffot-Pernot, C., Lounis, N., and Jarlier, V. (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis Science 307, 223-227
38. Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold EMBO J. 1, 945-951
39. Ketchum, C. J., Al-Shawi, M. K., and Nakamoto, R. K. (1998) Intergenic suppression of the γM23K uncoupling mutation in F0F1 ATP synthase by βGlu-381 substitutions: The role of the β380DELSEED386 segment in energy coupling Biochem. J. 330, 707-712
40. Vandeyar, M. A., Weiner, M. P., Hutton, C. J., and Batt, C. A. (1988) A simple and rapid method for the selection of oligodeoxynucleotide-directed mutants Gene 65, 129-133
41. Weber, J., Wilke-Mounts, S., Lee, R. S., Grell, E., and Senior, A. E. (1993) Specific placement of tryptophan in the catalytic sites of Escherichia coli F1-ATPase provides a direct probe of nucleotide binding: Maximal ATP hydrolysis occurs with three sites occupied J. Biol. Chem. 268, 20126-20133
42. Klionsky, D. J., Brusilow, W. S., and Simoni, R. D. (1984) In vivo evidence for the role of the ε subunit as an inhibitor of the proton-translocating ATPase of Escherichia coli J. Bacteriol. 160, 1055-1060
43. Senior, A. E., Langman, L., Cox, G. B., and Gibson, F. (1983) Oxidative phosphorylation in Escherichia coli. Characterization of mutant strains in which F1-ATPase contains abnormal β-subunits Biochem. J. 210, 395-403
44. Senior, A. E., Latchney, L. R., Ferguson, A. M., and Wise, J. G. (1984) Purification of F1-ATPase with impaired catalytic activity from partial revertants of Escherichia coli uncA mutant strains Arch. Biochem. Biophys. 228, 49-53
45. Taussky, H. H. and Shorr, E. (1953) A microcolorimetric method for the determination of inorganic phosphorus J. Biol. Chem. 202, 675-685
46. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680-685
47. Rao, R., Perlin, D. S., and Senior, A. E. (1987) The defective proton-ATPase of uncA mutants of Escherichia coli: ATP-binding and ATP-induced conformational change in mutant α-subunits Arch. Biochem. Biophys. 255, 309-315
48. Weber, J., Wilke-Mounts, S., and Senior, A. E. (1994) Cooperativity and stoichiometry of substrate binding to the catalytic sites of Escherichia coli F1-ATPase. Effects of magnesium, inhibitors, and mutation J. Biol. Chem. 269, 20462-20467
49. Chinnam, N., Dadi, P. K., Sabri, S. A., Ahmad, M., Kabir, M. A., and Ahmad, Z. (2010) Dietary bioflavonoids inhibit Escherichia coli ATP synthase in a differential manner Int. J. Biol. Macromol. 46, 478-486
50. Dadi, P. K., Ahmad, M., and Ahmad, Z. (2009) Inhibition of ATPase activity of Escherichia coli ATP synthase by polyphenols Int. J. Biol. Macromol. 45, 72-79
51. Laughlin, T. F. and Ahmad, Z. (2010) Inhibition of Escherichia coli ATP synthase by amphibian antimicrobial peptides Int. J. Biol. Macromol. 46, 367-374
52. Ahmad, Z., Ahmad, M., Okafor, F., Jones, J., Abunameh, A., Cheniya, R. P., and Kady, I. O. (2012) Effect of structural modulation of polyphenolic compounds on the inhibition of Escherichia coli ATP synthase Int. J. Biol. Macromol. 50, 476-486
53. Ferguson, S. J., Lloyd, W. J., and Radda, G. K. (1975) The mitochondrial ATPase. Selective modification of a nitrogen residue in the β subunit Eur. J. Biochem. 54, 127-133
54. Ferguson, S. J., Lloyd, W. J., Lyons, M. H., and Radda, G. K. (1975) The mitochondrial ATPase. Evidence for a single essential tyrosine residue Eur. J. Biochem. 54, 117-126
55. Nadanaciva, S., Weber, J., and Senior, A. E. (2000) New probes of the F1-ATPase catalytic transition state reveal that two of the three catalytic sites can assume a transition state conformation simultaneously Biochemistry 39, 9583-9590
56. Nadanaciva, S., Weber, J., and Senior, A. E. (1999) Binding of the transition state analog MgADP-fluoroaluminate to F1-ATPase J. Biol. Chem. 274, 7052-7058
57. Bowler, M. W., Montgomery, M. G., Leslie, A. G., and Walker, J. E. (2006) How azide inhibits ATP hydrolysis by the F-ATPases Proc. Natl. Acad. Sci. U.S.A. 103, 8646-8649
58. 14C]carbodiimide J. Biol. Chem. 257, 10033-10037
59. +-ATPase activity of Escherichia coli F1F0 is blocked after reaction of dicyclohexylcarbodiimide with a single proteolipid (subunit c) of the F0 complex J. Biol. Chem. 264, 3896-3903
60. 1-ATPase revealed by single-molecule imaging and manipulation Cell 130, 309-321
61. Tombline, G., Bartholomew, L., Gimi, K., Tyndall, G. A., and Senior, A. E. (2004) Synergy between conserved ABC signature Ser residues in P-glycoprotein catalysis J. Biol. Chem. 279, 5363-5373