Development of a minimal cell-free translation system for the synthesis of presecretory and integral membrane proteins

Biotechnology Progress

Volumn 21, Issue 4, 2005, Pages 1243-1251

  Kuruma, Yutetsu ^a   Nishiyama, Ken Ichi ^a,b   Shimizu, Yoshihiro ^a   Müller, Matthias ^b   Ueda, Takuya ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ESCHERICHIA COLI; SYNTHESIS (CHEMICAL);

CELL-FREE SYSTEMS; INTERACTION MECHANISMS; TRANSLATION FACTORS; TRANSLOCATIONS;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CARRIER PROTEIN; CELL RECEPTOR; CHAPERONE; ESCHERICHIA COLI PROTEIN; FFH PROTEIN, E COLI; FTSQ PROTEIN, E COLI; FTSY PROTEIN, BACTERIA; MEMBRANE PROTEIN; OMP ALPHA PROTEIN, BACTERIA; OMP-ALPHA PROTEIN, BACTERIA; OUTER MEMBRANE PROTEIN; SECA PROTEIN, BACTERIA; SECB PROTEIN, BACTERIA; SIGNAL RECOGNITION PARTICLE;

ARTICLE; CELL FREE SYSTEM; CHEMISTRY; ESCHERICHIA COLI; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR BIOLOGY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SECRETION; SOLUBILITY; TRANSPORT VESICLE;

ADENOSINE TRIPHOSPHATASES; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL-FREE SYSTEM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR BIOLOGY; MOLECULAR CHAPERONES; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL RECOGNITION PARTICLE; SOLUBILITY; TRANSPORT VESICLES;

ESCHERICHIA COLI;

EID: 23244445172     PISSN: 87567938     EISSN: None     Source Type: Journal    
DOI: 10.1021/bp049553u     Document Type: Article

References (57)

1. Jermutus, L.; Ryabova, L. A.; Pluckthun, A. Recent advances in producing and selecting functional proteins by using cell-free translation. Curr. Opin. Biotechnol. 1998, 9, 534-548.
2. Stiege, W.; Erdmann, V. A. The potentials of the in vitro protein biosynthesis system. J. Biotechnol. 1995, 41, 81-90.
3. Shimizu, Y.; Inoue, A.; Tomari, Y.; Suzuki, T.; Yokogawa, T.; Nishikawa, K.; Ueda, T. Cell-free translation reconstituted with purified components. Nat. Biotechnol. 2001, 19, 751-755.
4. Koch, H. G.; Moser, M.; Muller, M. Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev. Physiol. Biochem. Pharmacol. 2003, 146, 55-94
5. de Keyzer, J.; van der Does, C.; Driessen, A. J. The bacterial translocase: a dynamic protein channel complex. Cell. Mol. Life Sci. 2003, 60, 2034-2052
6. Mori, H.; Ito, K. The Sec protein-translocation pathway. Trends Microbiol. 2001, 9, 494-500.
7. Muller, M.; Koch, H. G.; Beck, K.; Schafer, U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 2001, 66, 107-157.
8. Pugsley, A. P.; Francetic, O.; Driessen, A. J.; de Lorenzo, V. Getting out: protein traffic in prokaryotes. Mol. Microbiol. 2004, 52, 3-11.
9. Economou, A.; Wickner, W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 1994, 78, 835-843.
10. Economou, A.; Pogliano, J. A.; Beckwith, J.; Oliver, D. B.; Wickner, W. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 1995, 83, 1171-1181.
11. Eichler, J.; Wickner, W. Both an N-terminal 65-kDa domain and a C-terminal 30-kDa domain of SecA cycle into the membrane at SecYEG during translocation. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 5574-5581.
12. Nishiyama, K.; Suzuki, T.; Tokuda, H. Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 1996, 85, 71-81.
13. Suzuki, H.; Nishiyama, K.; Tokuda, H. Coupled structure changes of SecA and SecG revealed by the synthetic lethality of the secAcsR11 and delta secG:: kan double mutant. Mol. Microbiol. 1998, 29, 331-341.
14. Werner, P. K.; Saier, M. H., Jr.; Muller, M. Membrane insertion of the mannitol permease of Escherichia coli occurs under conditions of impaired SecA function. J. Biol. Chem. 1992, 267, 24523-24532.
15. Koch, H. G.; Hengelage, T.; Neumann-Haefelin, C.; MacFarlane, J.; Hoffschulte, H. K.; Schimz, K. L.; Mechler, B.; Muller, M. In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol. Biol. Cell 1999, 10, 2163-2173.
16. Scotti, P. A.; Valent, Q. A.; Manting, E. H.; Urbanus, M. L.; Driessen, A. J.; Oudega, B.; Luirink, J. SecA is not required for signal recognition particle-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J. Biol. Chem. 1999, 274, 29883-29888.
17. Koch, H. G.; Muller, M. Dissecting the translocase and integrase functions of the Escherichia coli SecYEG translocon. J. Cell Biol. 2000, 150, 689-694.
18. Qi, H. Y.; Bernstein, H. D. SecA is required for the insertion of inner membrane proteins targeted by the Escherichia coli signal recognition particle. J. Biol. Chem. 1999, 274, 8993-8997.
19. Tian, H.; Boyd, D.; Beckwith, J. A mutant hunt for defects in membrane protein assembly yields mutations affecting the bacterial signal recognition particle and Sec machinery. Proc. Natl. Acad. Sci. U.S.A 2000, 97, 4730-4735.
20. Urbanus, M. L.; Scotti, P. A.; Froderberg, L.; Saaf, A.; de Gier, J. W.; Brunner, J.; Samuelson, J. C.; Dalbey, R. E.; Oudega, B.; Luirink, J. Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep. 2001, 2, 524-529.
21. Koch, H. G.; Moser, M.; Schimz, K. L.; Muller, M. The integration of YidC into the cytoplasmic membrane of Escherichia coli requires the signal recognition particle, SecA and SecYEG. J. Biol. Chem. 2002, 277, 5715-5718.
22. Stuart, R. Insertion of proteins into the inner membrane of mitochondria: the role of the Oxa1 complex. Biochim. Biophys. Acta 2002, 1592, 79-87.
23. Sundberg, E.; Slagter, J. G.; Fridborg, I.; Cleary, S. P.; Robinson, C.; Coupland, G. ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 1997, 9, 717-730.
24. Samuelson, J. C.; Chen, M.; Jiang, F.; Moller, I.; Wiedmann, M.; Kuhn, A.; Phillips, G. J.; Dalbey, R. E. YidC mediates membrane protein insertion in bacteria. Nature 2000, 406, 637-641.
25. Chen, M.; Xie, K.; Nouwen, N.; Driessen, A. J.; Dalbey, R. E. Conditional lethal mutations separate the M13 procoat and Pf3 coat functions of YidC: different YIDC structural requirements for membrane protein insertion. J. Biol. Chem. 2003, 278, 23295-23300.
26. Geller, B. L.; Wickner, W. M13 procoat inserts into liposomes in the absence of other membrane proteins. J. Biol. Chem. 1985, 260, 13281-13285.
27. Kuhn, A.; Rohrer, J.; Gallusser, A. Bacteriophages M13 and Pf3 tell us how proteins insert into the membrane. J. Struct. Biol. 1990, 104, 38-43.
28. Robinson, C.; Bolhuis, A. Protein targeting by the twin-arginine translocation pathway. Nat. Rev. Mol. Cell Biol. 2001, 2, 350-356.
29. Walter, P.; Blobel, G. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 1981, 91, 557-561.
30. Raine, A.; Ullers, R.; Pavlov, M.; Luirink, J.; Wikberg, J. E.; Ehrenberg, M. Targeting and insertion of heterologous membrane proteins in E. coli. Biochimie 2003, 85, 659-668.
31. Nagai, K.; Oubridge, C.; Kuglstatter, A.; Menichelli, E.; Isel, C.; Jovine, L. Structure, function and evolution of the signal recognition particle. EMBO J. 2003, 22, 3479-3485.
32. Kawasaki, H.; Matsuyama, S.; Sasaki, S.; Akita, M.; Mizushima, S. SecA protein is directly involved in protein secretion in Escherichia coli. FEBS Lett. 1989, 242, 431-434.
33. Studier, F. W.; Moffatt, B. A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 1986, 189, 113-130.
34. Yanisch-Perron, C.; Vieira, J.; Messing, J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985, 33, 103-119.
35. Casadaban, M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 1976, 104, 541-555.
36. Akita, M.; Sasaki, S.; Matsuyama, S.; Mizushima, S. SecA interacts with secretory proteins by recognizing the positive charge at the amino terminus of the signal peptide in Escherichia coli. J. Biol. Chem. 1990, 265, 8164-8169.
37. Muller, M.; Blobel, G. In vitro translocation of bacterial proteins across the plasma membrane of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A 1984, 81, 7421-7425.
38. Helde, R.; Wiesler, B.; Wachter, E.; Neubuser, A.; Hoffschulte, H. K.; Hengelage, T.; Schimz, K. L.; Stuart, R. A.; Muller, M. Comparative characterization of SecA from the alpha-subclass purple bacterium Rhodobacter capsulatus and Escherichia coli reveals differences in membrane and precursor specificity. J. Bacteriol. 1997, 179, 4003-4012.
39. Ying, B. W.; Taguchi, H.; Ueda, H.; Ueda, T. Chaperone-assisted folding of a single-chain antibody in a reconstituted translation system. Biochem. Biophys. Res. Commun. 2004, 320, 1359-1364.
40. Neumann-Haefelin, C.; Schafer, U.; Muller, M.; Koch, H. G. SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J. 2000, 19, 6419-6426.
41. Cabelli, R. J.; Chen, L.; Tai, P. C.; Oliver, D. B. SecA protein is required for secretory protein translocation into E. coli membrane vesicles. Cell 1988, 55, 683-692.
42. Kawasaki, S.; Mizushima, S.; Tokuda, H. Membrane vesicles containing overproduced SecY and SecE exhibit high translocation ATPase activity and countermovement of protons in a SecA- and presecretory protein-dependent manner. J. Biol. Chem. 1993, 268, 8193-8198.
43. Sugiyama, J. E.; Mahmoodian, S.; Jacobson, G. R. Membrane topology analysis of Escherichia coli mannitol permease by using a nested-deletion method to create mtlA-phoA fusions. Proc. Natl. Acad. Sci. U.S.A 1991, 88, 9603-9607.
44. van der Laan, M.; Nouwen, N.; Driessen, A. J. SecYEG proteoliposomes catalyze the Deltaphi-dependent membrane insertion of FtsQ. J. Biol. Chem. 2004, 279, 1659-1664.
45. Chen, L.; Tai, P. C. ATP is essential for protein translocation into Escherichia coli membrane vesicles. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4384-4388.
46. Geller, B. L.; Movva, N. R.; Wickner, W. Both ATP and the electrochemical potential are required for optimal assembly of pro-OmpA into Escherichia coli inner membrane vesicles. Proc. Natl. Acad. Sci. U.S.A 1986, 83, 4219-4222.
47. Nishiyama, K.; Fukuda, A.; Morita, K.; Tokuda, H. Membrane deinsertion of SecA underlying proton motive force-dependent stimulation of protein translocation. EMBO J. 1999, 18, 1049-1058.
48. Nishiyama, K.; Hanada, M.; Tokuda, H. Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J. 1994, 13, 3272-3277.
49. Randall, L. L. Translocation of domains of nascent periplasmic proteins across the cytoplasmic membrane is independent of elongation. Cell 1983, 33, 231-240.
50. Lecker, S. H.; Driessen, A. J.; Wickner, W. ProOmpA contains secondary and tertiary structure prior to translocation and is shielded from aggregation by association with SecB protein. EMBO J. 1990, 9, 2309-2314.
51. Wild, J.; Rossmeissl, P.; Walter, W. A.; Gross, C. A. Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J. Bacteriol. 1996, 178, 3608-3613.
52. Crooke, E.; Guthrie, B.; Lecker, S.; Lill, R.; Wickner, W. ProOmpA is stabilized for membrane translocation by either purified E. coli trigger factor or canine signal recognition particle. Cell 1988, 54, 1003-1011.
53. Lecker, S.; Lill, R.; Ziegelhoffer, T.; Georgopoulos, C.; Bassford, P. J., Jr.; Kumamoto, C. A.; Wickner, W. Three pure chaperone proteins of Escherichia coli-SecB, trigger factor and GroEL-form soluble complexes with precursor proteins in vitro. EMBO J. 1989, 8, 2703-2709.
54. Fekkes, P.; van der Does, C.; Driessen, A. J. The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J. 1997, 16, 6105-6113.
55. Kumamoto, C. A.; Beckwith, J. Evidence for specificity at an early step in protein export in Escherichia coli. J. Bacteriol. 1985, 163, 267-274.
56. Shimizu, H.; Nishiyama, K.; Tokuda, H. Expression of gpsA encoding biosynthetic sn-glycerol 3-phosphate dehydrogenase suppresses both the LB-phenotype of a secB null mutant and the cold-sensitive phenotype of a secG null mutant. Mol. Microbiol. 1997, 26, 1013-1021.
57. Yamada, H.; Tokuda, H.; Mizushima, S. Proton motive force-dependent and -independent protein translocation revealed by an efficient in vitro assay system of Escherichia coli. J. Biol. Chem. 1989, 264, 1723-1728.