Inhibition of ATP hydrolysis by thermoalkaliphilic F1F 0-ATP synthase is controlled by the C terminus of the ε subunit

Journal of Bacteriology

Volumn 188, Issue 11, 2006, Pages 3796-3804

  Keis, Stefanie ^a   Stocker, Achim ^b   Dimroth, Peter ^b   Cook, Gregory M ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ALANINE; HOLOENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RECOMBINANT ENZYME; TRYPSIN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME SUBUNIT; ESCHERICHIA COLI; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DETERGENTS; DIMETHYLAMINES; DNA PRIMERS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; KINETICS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PLASMIDS; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

BACILLUS SP.; ESCHERICHIA COLI;

EID: 33744767457     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00040-06     Document Type: Article

References (62)

1. 1-ATPase from bovine heart mitochondria. Nature 370:621-628.
2. Boyer, P. D. 1997. The ATP synthase - a splendid molecular machine. Annu. Rev. Biochem. 66:717-749.
3. Brusilow, W. S. A., M. A. Scarpetta, C. A. Hawthorne, and W. P. Clark. 1989. Organization and sequence of the genes coding for the proton-translocating ATPase of Bacillus megaterium. J. Biol. Chem. 264:1528-1533.
4. 0 ATPases. Structure, arrangement, and role of the ε subunit in energy coupling within the complex. Biochim. Biophys. Acta 1458:263-269.
5. Cipriano, D. J., Y. Bi, and S. D. Dunn. 2002. Genetic fusions of globular proteins to the ε subunit of the Escherichia coli ATP synthase: implications for in vivo rotational catalysis and ε subunit function. J. Biol. Chem. 277: 16782-16790.
6. Cipriano, D. J., and S. D. Dunn. 2006. The role of the ε subunit in Escherichia coli ATP synthase: the C-terminal domain is required for efficient energy coupling. J. Biol. Chem. 281:501-507.
7. 0-ATP synthase from thermoalkaliphilic Bacillus sp. strain TA2.A1. J. Bacteriol. 185:4442-4449.
8. Digel, J. G., N. D. Moore, and R. E. McCarty. 1998. Influence of divalent cations on nucleotide exchange and ATPase activity of chloroplast coupling factor 1. Biochemistry 37:17209-17215.
9. +-coupled ATP synthases operating at low electrochemical potential. Adv. Microb. Physiol. 49:175-218.
10. 1-ATPase at 2.4 Å resolution. Nat. Struct. Biol. 7:1055-1061.
11. Hanahan, D., J. Jessee, and F. R. Bloom. 1991. Plasmid transformation of Escherichia coli and other bacteria. Methods Enzymol. 204:63-113.
12. t-ATPase: propagation of the inhibitory effect of the ε subunit. J. Biol. Chem. 276:23969-23973.
13. Harris, D. A., P. John, and G. K. Radda. 1977. Tightly bound nucleotides of the energy-transducing ATPase, and their role in oxidative phosphorylation. I. The Paracoccus denitrificans system. Biochim. Biophys. Acta 459:546-559.
14. 0 ATP synthase from Bacillus subtilis. J. Bacteriol. 176:4192-4195.
15. +. J. Biol. Chem. 265:20547-20554.
16. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
17. Hoffmann, A., and P. Dimroth. 1990. The ATPase of Bacillus alcalophilus. Purification and properties of the enzyme. Eur. J. Biochem. 194:423-430.
18. Hoffmann, A., and P. Dimroth. 1991. The ATPase of Bacillus alcalophilus. Reconstitution of energy-transducing functions. Eur. J. Biochem. 196:493-497.
19. 1-ATPase. J. Biol. Chem. 280:4013-40134.
20. Ivey, D. M., and T. A. Krulwich. 1991. Organization and nucleotide sequence of the atp genes encoding the ATP synthase from alkaliphilic Bacillus firmus OF4. Mol. Gen. Genet. 229:292-300.
21. 1 β-subunit. FEBS Lett. 229:224-228.
22. Johnson, E. A., Y. Evron, and R. E. McCarty. 2001. Resonance energy transfer between tryptophan 57 in the ε subunit and pyrene maleimide labeled γ subunit of the chloroplast ATP synthase. Biochemistry 40:1804-1811.
23. Johnson, E. A., and R. E. McCarty. 2002. The carboxyl terminus of the ε subunit of the chloroplast ATP synthase is exposed during illumination. Biochemistry 41:2446-2451.
24. 1-ATPase is activated without dissociation of an endogenous inhibitor, ε subunit. J. Biol. Chem. 272:24906-24912.
25. 1-ATPase. J. Biol. Chem. 274:33991-33994.
26. 1-ATPase binds ATP. J. Biol. Chem. 278:36013-36016.
27. 0-ATP synthase from a thermoalkaliphilic Bacillus sp. strain TA2.A1. Biochim. Biophys. Acta 1676:112-117.
28. Klionsky, D. J., W. S. A. Brusilow, and R. D. Simoni. 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.
29. 1). J. Biol. Chem. 263:17437-17442.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. 1 ATPase. Arch. Biochem. Biophys. 197: 83-89.
32. 1 by the detergent lauryldimethylamine oxide. Biochemistry 23:4140-4143.
33. 0-ATP synthase. Biochemistry 44:7275-7281.
34. Maurer, L. M., E. Yohannes, S. S. Bondurant, M. Radmacher, and J. L. Slonczewski. 2005. pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J. Bacteriol. 187:304-319.
35. Nakagawa, H., S. H. Lee, V. K. Kalra, and A. F. Brodie. 1977. Trypsin-induced changes in the orientation of latent ATPase in protoplast ghosts from Mycobacterium phlei. J. Biol. Chem. 252:8229-8234.
36. 1 ATP synthase. J. Membr. Biol. 151:101-111.
37. Nalin, C. M., and R. E. McCarty. 1984. Role of a disulfide bond in the γ subunit in activation of the ATPase of chloroplast coupling factor 1. J. Biol. Chem. 259:7275-7280.
38. Nowak, K. F., and R. E. McCarty. 2004. Regulatory role of the C-terminus of the ε subunit from the chloroplast ATP synthase. Biochemistry 43:3273-3279.
39. Nowak, K. F., V. Tabidze, and R. E. McCarty. 2002. The C-terminal domain of the ε subunit of the chloroplast ATP synthase is not required for ATP synthesis. Biochemistry 41:15130-15134.
40. Ohta, S., M. Yohda, M. Ishizuka, H. Hirata, T. Hamamoto, Y. Otawara-Hamamoto, K. Matsuda, and Y. Kagawa. 1988. Sequence and over-expression of subunits of adenosine triphosphate synthase in thermophilic bacterium PS3. Biochim. Biophys. Acta 933:141-155.
41. Olsson, K., S. Keis, H. W. Morgan, P. Dimroth, and G. M. Cook. 2003. Bioenergetic properties of the thermoalkaliphilic Bacillus sp. strain TA2.A1. J. Bacteriol. 185:461-465.
42. Richter, M. L., W. J. Patrie, and R. E. McCarty. 1984. Preparation of the ε subunit and ε subunit-deflcient chloroplast coupling factor 1 in reconstitutively active forms. J. Biol. Chem. 259:7371-7373.
43. Rodgers, A. J. W., and M. C. J. Wilce. 2000. Structure of the γ-ε complex of ATP synthase. Nat. Struct. Biol. 7:1051-1054.
44. 1-ATPase single molecules. Nature 433:773-777.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
46. 1, ATPase: DNA sequence of the atp operon and characterization of atp mutants. J. Bacteriol. 176:6802-6811.
47. Senior, A. E. 1988. ATP synthesis by oxidative phosphorylation. Physiol. Rev. 68:177-231.
48. Smith, J. B., and P. C. Sternweis. 1977. Purification of membrane attachment and inhibitory subunits of the proton translocating adenosine triphosphatase from Escherichia coli. Biochemistry 16:306-311.
49. Smith, J. B., and P. C. Sternweis. 1982. Subunit specific antisera to the Escherichia coli ATP synthase: effects on ATPase activity, energy transduction, and enzyme assembly. Arch. Biochem. Biophys. 217:376-387.
50. 1-ATPase complexes from the thermoalkaliphilic Bacillus sp. strain TA2.A1. J. Struct. Biol. 152:140-145.
51. 1-ATPase/synthase is geared to the synthesis mode by conformational rearrangement of ε subunit in response to proton motive force and ADP/ATP balance. J. Biol. Chem. 278:46840-46846.
52. 0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme. Proc. Natl. Acad. Sci. USA 98:6560-6564.
53. Uhlin, U., G. B. Cox, and J. M. Guss. 1997. Crystal structure of the ε subunit of the proton-translocating ATP synthase from Escherichia coli. Structure 5:1219-1230.
54. Walker, J. E., M. Saraste, and N. J. Gay. 1984. The unc operon: nucleotide sequence, regulation and structure of ATP-synthase. Biochim. Biophys. Acta 768:164-200.
55. Wang, Z., D. B. Hicks, A. A. Guffanti, K. Baldwin, and T. A. Krulwich. 2004. Replacement of amino acid sequence features of a- and c-subunits of ATP synthases of alkaliphilic Bacillus with the Bacillus consensus sequence results in defective oxidative phosphorylation and non-fermentative growth at pH 10.5. J. Biol. Chem. 279:26546-26554.
56. 1-ATPase catalytic sites. J. Biol. Chem. 274:19124-19128.
57. 1,-ATPase. Biochim. Biophys. Acta 1319:19-58.
58. 1-ATPase from Escherichia coli and interactions of this subunit with β subunits in the complex. J. Biol. Chem. 273:26645-26651.
59. Wilkens, S., F. W. Dahlquist, L. P. McIntosh, L. W. Donaldson, and R. A. Capaldi. 1995. Structural features of the ε subunit of the Escherichia coli ATP synthase determined by NMR spectroscopy. Nat. Struct. Biol. 2:961-967.
60. Xiong, H., D. Zhang, and S. B. Vik. 1998. Subunit ε of the Escherichia coli ATP synthase: novel insights into structure and function by analysis of thirteen mutant forms. Biochemistry 37:16423-16429.
61. Yoshida, M., E. Muneyuki, and T. Hisabori. 2001. ATP synthase - a marvelous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2:669-677.
62. 1-ATPase in Paracoccus denitrificans plasma membranes. J. Biol. Chem. 279:12319-12324.