Physiological impact of intrinsic ADP inhibition of cyanobacterial F oF1 conferred by the inherent sequence inserted into the γ subunit

Plant and Cell Physiology

Volumn 51, Issue 6, 2010, Pages 855-865

  Sunamura, Ei Ichiro ^a   Konno, Hiroki ^a   Imashimizu Kobayashi, Mari ^a   Sugano, Yasushi ^a   Hisabori, Toru ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

subunit; ADP inhibition; ATP synthase; Cyanobacteria; Regulation

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; BIOSYNTHESIS; CYANOBACTERIUM; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CHLOROPLAST PROTON-TRANSLOCATING ATPASES; CYANOBACTERIA; MUTAGENESIS, INSERTIONAL; PROTEIN SUBUNITS; SEQUENCE DELETION;

BACTERIA (MICROORGANISMS); CYANOBACTERIA;

EID: 77953595558     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq061     Document Type: Article

References (60)

1. 1-ATPase from bovine heart mitochondria. Nature 370: 621-628.
2. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130: 309-321.
3. 0-type ATPase. J. Biol. Chem. 271:13888-13891. (Pubitemid 26185436)
4. 1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat Struct. Mol. Biol. 14: 841-846.
5. Avni, A., Anderson, J.D., Holland, N., Rochaix, J.D., Gromet-Elhanan, Z. and Edelman, M. (1992) Tentoxin sensitivity of chloroplasts determined by codon 83 of (3 subunit of proton-ATPase. Science 257: 1245-1247.
6. 1-ATP synthase independent of noncatalytic nucleotide binding sites and insensitive to azide inhibition. J. Biol. Chem. 273:865-870.
7. Bar-Zvi, D. and Shavit, N. (1982) Modulation of the chloroplast ATPase by tight ADP binding. Effect of uncouplers and ATP. J. Bioenerg. Biomembr. 14:467-478.
8. Bottomley, P.J. and Stewart, W.D. (1976) ATP pools and transients in the blue-green alga, Anabaena cylindrica. Arch Microbiol 108:249-258.
9. Boyer, P.D. (1997) The ATP synthase\a splendid molecular machine. Annu. Rev. Biochem. 66:717-749.
10. Digel, J.G., Kishinevsky, A, Ong, A.M. and McCarty, R.E. (1996) Differences between two tight ADP binding sites of the chloroplast coupling factor 1 and their effects on ATPase activity. J. Biol. Chem. 271: 19976-19982.
11. 2 +-induced differences in catalytic site structure and function J. Biol. Chem. 276:11517-11523.
12. 1-ATPase. Proc. Natl Acad. Sci. USA 92:10964-10968.
13. 1-ATPase by lauryldimethylamine oxide and ethylene glycol: relationship of ATPase activity to the interaction of the e and P subunits. Biochemistry 29:4335-4340.
14. 1 adenosine triphosphatase. Correlations of initial velocity, bound intermediate, and oxygen exchange measurements with an alternating three-site model. J. Biol. Chem. 257: 12030-12038.
15. Grimme, L.H. and Boardman, N.K. (1972) Photochemical activities of a particle fraction P1 obtained from the green alga Chlorella fusca. Biochem. Biophys. Res. Commun. 49:1617-1623.
16. 1 motor by external force. Proc. Natl Acad. Sci. USA 102: 4288-4293.
17. 1-ATPase during catalysis. Proc. Natl Acad. Sci. USA 98: 13649-13654.
18. 1-ATPase can rotate in a unidirectional and counterclockwise manner. FEBS Lett. 463: 35-38.
19. 1-ATP synthase for the regulation. Biochim. Biophys. Acta 1555:140-146.
20. Hoppe, S., Bierhoff, H., Cado, I., Weber, A., Tiebe, M., Grummt, I., et al. (2009) AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc. Natl Acad. Sci. USA 106:17781-17786.
21. Jiang, W., Hermolin, J. and Fillingame, R.H. (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc. Natl Acad. Sci. USA 98:4966-4971.
22. Joshi, A.K., Ahmed, S. and Ferro-Luzzi Ames, G. (1989) Energy coupling in bacterial periplasmic transport systems. Studies in intact Escherichia coli cells J. Biol. Chem. 264:2126-2133.
23. 1-ATPase caused by the y subunit generates a high affinity nucleotide binding site. J. Biol. Chem. 271:2433-2438.
24. 1-ATPase J. Biol. Chem. 275: 35746-35750.
25. 1-ATPase is activated without dissociation of an endogenous inhibitor, e subunit. J. Biol. Chem. 272: 24906-24912.
26. Koebmann, B.J., Westerhoff, H.V., SnoepJ.L, Nilsson, D. and Jensen, P.R. (2002) The glycolytic fl ux in Escherichia coli is controlled by the demand for ATP. J. Bacteriol. 184: 3909-3916.
27. 1-ATPase by the e subunit. EMBO J. 25: 4596-4604.
28. Meier, T., Polzer, P., Diederichs, K., Welte, W. and Dimroth, P. (2005) Structure of the rotor ring of F-type Na +-ATPase from Ilyobacter tartaricus. Science 308:659-662.
29. Meiss, E., Konno, H., Groth, G. and Hisabori, T. (2008) Molecular processes of inhibition and stimulation of ATP synthase caused by the phytotoxin tentoxin. J. Biol. Chem. 283:24594-24599.
30. Mills, J.D., Mitchell, P. and Schurmann, P. (1980) Modulation of coupling factor ATPase activity in intact chloroplasts, the role of the thioredoxin system. FEBS Lett. 112:173-177.
31. 1. Biochem. Biophys. Res. Commun. 89:1300-1306.
32. Mitome, N., Suzuki, T., Hayashi, S. and Yoshida, M. (2004) Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H +/ATP ratio and permissive elastic coupling. Proc. Natl Acad. Sci. USA 101: 12159-12164.
33. Nalin, CM. and McCarty, R.E. (1984) Role of a disulfide bond in the y subunit in activation of the ATPase of chloroplast coupling factor 1. J. Biol. Chem. 259: 7275-7280.
34. Nelson, N., Nelson, H. and Racker, E. (1972) Partial resolution of the enzymes catalyzing photophosphorylation. XII. Purifi cation and properties of an inhibitor isolated from chloroplast coupling factor 1. J. Biol. Chem. 247: 7657-7662.
35. Nichols, N.N. and Harwood, C.S. (1997) PcaK, a high-affi nity permease for the aromatic compounds 4-hydroxybenzoate and protocatechuate from Pseudomonas putida.J. Bacteriol 179: 5056-5061.
36. 1-ATPase. Nature 386: 299-302.
37. Nowak, K.F., Tabidze, V. and McCarty, R.E. (2002) The C-terminal domain of the e subunit of the chloroplast ATP synthase is not required for ATP synthesis. Biochemistry 41:15130-15134.
38. 1 from the cyanobacterium Anacystis nidulans. Plant Cell Physiol. 34: 523-529.
39. 1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc. Natl Acad. Sci. USA 96: 7780-7784.
40. 1-ATPase molecules by tentoxin: new properties of the re-activated enzyme. J. Biol. Chem. 279: 9685-9688.
41. Richter, M.L., Patrie, W.J. and McCarty, R.E. (1984) Preparation of the ε subunit and ε subunit-defi cient chloroplast coupling factor 1 in reconstitutively active forms. J. Biol. Chem. 259: 7371-7373.
42. Ross, S.A., Zhang, M.X. and Selman, B.R. (1995) Role of the Chlamydomonas reinhardtii coupling factor 1 γ-subunit cysteine bridge in the regulation of ATP synthase. J. Biol. Chem. 270: 9813-9818.
43. Sabbert, D., Engelbrecht, S. and Junge, W. (1996) Intersubunit rotation in active F-ATPase. Nature 381: 623-625.
44. Samra, H.S., Gao, F., He, F., Hoang, E., Chen, Z., Gegenheimer, P.A., et al. (2006) Structural analysis of the regulatory dithiol-containing domain of the chloroplast ATP synthase γ subunit. J. Biol. Chem. 281: 31041-31049.
45. Scholts, M.J.C., Aardewijn, P. and Walraven, H.S.V. (1996) Membrane vesicles from Synechocystis 6803 showing proton and electron transport and high ATP synthase activities. Photosynth. Res. 47: 301-305.
46. Seelert, H., Poetsch, A., Dencher, N.A., Engel, A., Stahlberg, H. and Muller, D.J. (2000) Structural biology. Proton-powered turbine of a plant motor. Nature 405: 418-419.
47. Senior, A.E. (1990) The proton-translocating ATPase of Escherichia coli. Annu. Rev. Biophys. Biophys. Chem. 19: 7-41.
48. Stanier, R.Y., Kunisawa, R., Mandel, M. and Cohen-Bazire, G. (1971) Purifi cation and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35: 171-205.
49. Stock, D., Leslie, A.G. and Walker, J.E. (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700-1705.
50. 0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme. Proc. Natl Acad. Sci. USA 98: 6560-6564.
51. Vasilyeva, E.A., Minkov, I.B., Fitin, A.F. and Vinogradov, A.D. (1982) Kinetic mechanism of mitochondrial adenosine triphosphatase. ADP-specifi c inhibition as revealed by the steady-state kinetics. Biochem. J. 202: 9-14.
52. 1-ATPase of the cyanobacterium Synechocystis 6803 by mutagenesis of atpC. Mol. Gen. Genet. 244: 144-150.
53. Werner, S., Schumann, J. and Strotmann, H. (1990) The primary structure of the γ-subunit of the ATPase from Synechocystis 6803. FEBS Lett. 261: 204-208.
54. Williams, J. (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 167: 766-778.
55. 1. Proc. Natl Acad. Sci. USA 104: 11233-11238.
56. 1-ATPase is a highly effi cient molecular motor that rotates with discrete 120 degree steps. Cell 93: 1117-1124.
57. 1-ATPase. Nature 410: 898-904.
58. Yoshida, M., Muneyuki, E. and Hisabori, T. (2001) ATP synthase\a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell. Biol. 2: 669-677.
59. Yoshida, M., Sone, N., Hirata, H., Kagawa, Y. and Ui, N. (1979) Subunit structure of adenosine triphosphatase. Comparison of the structure in thermophilic bacterium PS3 with those in mitochondria, chloroplasts, and Escherichia coli. J. Biol. Chem. 254: 9525-9533.
60. Zhou, J.M., Xue, Z.X., Du, Z.Y., Melese, T. and Boyer, P.D. (1988) Relationship of tightly bound ADP and ATP to control and catalysis by chloroplast ATP synthase. Biochemistry 27: 5129-5135.