Time-delayed in vivo assembly of subunit a into preformed Escherichia coli FoF1 atp synthase

Journal of Bacteriology

Volumn 195, Issue 18, 2013, Pages 4074-4084

  Brockmann, Britta ^a   Hoppmann, Kim Danielle Koop genannt ^a   Strahl, Henrik ^a,b   Deckers Hebestreit, Gabriele ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; FUCOSE; ISOPROPYL THIOGALACTOSIDE; MESSENGER RNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ALPHA CHAIN; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BIODEGRADATION; COMPLEX FORMATION; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE REPRESSION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; PROTON TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; STOICHIOMETRY; TIME;

ADENOSINE TRIPHOSPHATE; BACTERIOLOGICAL TECHNIQUES; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MUTATION; PROTEIN SUBUNITS; TIME FACTORS;

EID: 84883264018     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00468-13     Document Type: Article

References (68)

1. von Ballmoos C, Cook GM, Dimroth P. 2008. Unique rotary ATP synthase and its biological diversity. Annu. Rev. Biophys. 37:43-64.
2. O ATP synthases. Annu. Rev. Biochem. 78:649-672.
3. O ATP synthase requires YidC and SecYEG for membrane insertion. J. Mol. Biol. 390:893-901.
4. O ATP synthase and SecE of the SecYEG translocase. Biochemistry 42: 10537-10544.
5. O ATP synthase. J. Biol. Chem. 279:39260-39267.
6. + ATP synthase. Interdependence of subunit insertion into the membrane. J. Biol. Chem. 270:2815-2817.
7. Pierson HE, Uhlemann EME, Dmitriev OY. 2011. Interaction with monomeric subunit c drives insertion of ATP synthase subunit a into the membrane and primes a-c complex formation. J. Biol. Chem. 286:38583-38591.
8. Akiyama Y, Ito K. 2003. Reconstitution of membrane proteolysis by FtsH. J. Biol. Chem. 278:18146-18153.
9. O sector is a substrate of the FtsH protease in Escherichia coli. FEBS Lett. 399:26-28.
10. 10 ring stoichiometry in the Escherichia coli ATP synthase analyzed by crosslinking. J. Bacteriol. 191:2400-2404.
11. O-ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc. Natl. Acad. Sci. U. S. A. 104:20776-20781.
12. 1-ATP synthase in vitro. Biochem. Biophys. Res. Commun. 367:663-666.
13. O ATP synthase from Acetobacterium woodii in Escherichia coli requires the native AtpI. J. Bioenerg. Biomembr. 45:15-23.
14. Schneppe B, Deckers-Hebestreit G, Altendorf K. 1990. Overproduction and purification of the uncI gene product of the ATP synthase of Escherichia coli. J. Biol. Chem. 265:389-395.
15. Schneppe B, Deckers-Hebestreit G, Altendorf K. 1991. Detection and localization of the i protein in Escherichia coli cells using antibodies. FEBS Lett. 292:145-147.
16. Gay NJ. 1984. Construction and characterization of an Escherichia coli strain with a uncI mutation. J. Bacteriol. 158:820-825.
17. Liu J, Hicks DB, Krulwich TA. 2013. Roles of AtpI and two YidC-type proteins from alkaliphilic Bacillus pseudofirmus OF4 in ATP synthase assembly and nonfermentative growth. J. Bacteriol. 195:220-230.
18. Rak M, Gokova S, Tzagoloff A. 2011. Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30:920-930.
19. Kucharczyk R, Zick M, Bietenhader M, Rak M, Couplan E, Blondel M, Caubet S-D, di Rago J-P. 2009. Mitochondrial ATP synthase disorders: molecular mechanisms and the quest for curative therapeutic approaches. Biochim. Biophys. Acta 1793:186-199.
20. Koebmann BJ, Westerhoff HV, Snoep JL, Nilsson D, Jensen PR. 2002. The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J. Bacteriol. 184:3909-3916.
21. O-ATP synthase. J. Biol. Chem. 265:5595-5601.
22. 1 subunits is prerequisite for β subunit binding to the N-terminal region of α. Biochemistry 45:15893-15902.
23. 2-subunits as an anchor rail of a rotating c-ring. J. Biol. Chem. 279:33409-33412.
24. O-ATP synthase by in vitro protein synthesis. Biochem. J. 442:631-638.
25. Wittig I, Meyer B, Heide H, Steger M, Bleier L, Wumaier Z, Karas M, Schägger H. 2010. Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochim. Biophys. Acta 1797: 1004-1011.
26. 1-ATPase. J. Biol. Chem. 284:17138-17146.
27. Straffon AFL, Prescott M, Nagley P, Devenish RJ. 1998. The assembly of yeast mitochondrial ATP synthase: subunit depletion in vivo suggests ordered assembly of the stalk subunits b, OSCP and d. Biochim. Biophys. Acta 1371:157-162.
28. Cagnon C, Valverde V, Masson J-M. 1991. A new family of sugarinducible expression vectors for Escherichia coli. Protein Eng. 4:843-847.
29. BAD promoter. J. Bacteriol. 177:4121-4130.
30. Beverin S, Sheppard DE, Park SS. 1971. D-Fucose as a gratuitous inducer of the L-arabinose operon in strains of Escherichia coli B/r mutant in gene araC. J. Bacteriol. 107:79-86.
31. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89.
32. 1 subunit δ of the membrane-bound ATP synthase of Escherichia coli. Mol. Gen. Genet. 184:33-39.
33. 1 ATP synthase from Escherichia coli. FEBS Lett. 426:217-220.
34. 1-ATPase. Biochem. Biophys. Res. Commun. 260:597-599.
35. Klionsky DJ, Brusilow WSA, Simoni RD. 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.
36. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
37. TaKaRa. 2012. Single protein production system (SPP system). TaKaRa Bio Inc., Japan.
38. Neidhardt FC, Ingraham JL, Schaechter M. 1990. Physiology of the bacterial cell. A molecular approach. Sinauer Associates, Sunderland, MA.
39. +. Extremophiles 12:741-752.
40. Krebstakies T, Aldag I, Altendorf K, Greie JC, Deckers-Hebestreit G. 2008. The stoichiometry of subunit c of Escherichia coli ATP synthase is independent of its rate of synthesis. Biochemistry 47:6907-6916.
41. Douglas M, Finkelstein D, Butow RA. 1979. Analysis of products of mitochondrial protein synthesis in yeast: genetic and biochemical aspects. Methods Enzymol. 56:58-66.
42. Schägger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
43. Birkenhäger R, Greie JC, Altendorf K, Deckers-Hebestreit G. 1999. FO complex of the Escherichia coli ATP synthase. Not all monomers of the subunit c oligomer are involved in F1 interaction. Eur. J. Biochem. 264: 385-396.
44. 1-ATPase using monoclonal anti-ε antibody affinity chromatography. Anal. Biochem. 159:35-42.
45. 2 subcomplex. J. Biol. Chem. 278:27068-27071.
46. O complex of the ATP synthase of Escherichia coli. I Effects of subunit b-specific polyclonal antibodies. J. Biol. Chem. 267:12364-12369.
47. 1 ATP synthase: effect of repositioning within helix 4 of subunit a and helix 2 of subunit c. Biochim. Biophys. Acta 1767:998-1005.
48. O complexes. J. Biol. Chem. 262:8340-8346.
49. O-ATPase disrupt ATP-driven proton translocation. Arch. Biochem. Biophys. 274:270-284.
50. 1) a subunit from Escherichia coli. Arch. Biochem. Biophys. 284:71-77.
51. Mertens N, Remaut E, Fiers W. 1995. Tight transcriptional control mechanism ensures stable high-level expression from T7 promoter-based expression plasmids. Biotechnology 13:175-179.
52. Wilcox G. 1974. The interaction of L-arabinose and D-fucose with AraC protein. J. Biol. Chem. 249:6892-6894.
53. Lee SK, Chou HH, Pfleger BF, Newman JD, Yoshikuni Y, Keasling JD. 2007. Directed evolution of AraC for improved compatibility of arabinose-and lactose-inducible promoters. Appl. Environ. Microbiol. 73: 5711-5715.
54. Schramm HC, Schneppe B, Birkenhäger R, McCarthy JEG. 1996. The promoter-proximal, unstable IB region of the atp mRNA of Escherichia coli: an independently degraded region that can act as a destabilizing element. Biochim. Biophys. Acta 1307:162-170.
55. O complex of the ATP synthase of Escherichia coli. II Effects of subunit c-specific polyclonal antibodies. J. Biol. Chem. 267:12370-12374.
56. Solomon KA, Brusilow WSA. 1988. Effect of an uncE ribosome-binding site mutation on the synthesis and assembly of the Escherichia coli protontranslocating ATPase. J. Biol. Chem. 263:5402-5407.
57. 1 ATP synthase for ATP synthesis in membrane vesicles. Eur. J. Biochem. 243:336-343.
58. Matthies D, Haberstock S, Joos F, Dötsch V, Vonck J, Bernhard F, Meier T. 2011. Cell-free expression and assembly of ATP synthase. J. Mol. Biol. 413:593-603.
59. Uhlemann EME, Pierson HE, Fillingame RH, Dmitriev OY. 2012. Cell-free synthesis of membrane subunits of ATP synthase in phospholipid bicelles: NMR shows subunit a fold similar to the protein in the cell membrane. Protein Sci. 21:279-288.
60. 1 mutant cD61N. J. Biol. Chem. 277:31287-31290.
61. Kurzer F, Douraghi-Zadeh K. 1967. Advances in the chemistry of carbodiimides. Chem. Rev. 67:107-152.
62. +-ATPase causes growth inhibition of Escherichia coli. J. Bacteriol. 171:6853-6858.
63. von Meyenburg K, Jørgensen BB, Michelsen O, Sørensen L, McCarthy JEG. 1985. Proton conduction by subunit a of the membrane-bound ATP synthase of Escherichia coli revealed after induced overproduction. EMBO J. 4:2357-2363.
64. O-ATPase subunit a is inhibited by instability of the uncB gene transcript. FEBS Lett. 547:97-100.
65. Matten SR, Schneider TD, Ringquist S, Brusilow WSA. 1998. Identification of an intragenic ribosome binding site that affects expression of the atpB gene of the Escherichia coli proton-translocating ATPase (unc) operon. J. Bacteriol. 180:3940-3945.
66. +-ATPase. J. Biol. Chem. 266:16350-16355.
67. 1) and its reconstitution into liposomes with neurotransmitter transporters. J. Biol. Chem. 266:22141-22146.
68. 1 ATP synthase. J. Biol. Chem., in press.