Genetic selection for protein solubility enabled by the folding quality control feature of the twin-arginine translocation pathway

Protein Science

Volumn 15, Issue 3, 2006, Pages 449-458

  Fisher, Adam C ^a   Kim, Woojin ^b   Delisa, Matthew P ^a,c  

^a School of Chemical and Molecular Engineering   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c Department of Molecular Biology and Genetics   (United States)

Author keywords

cDNA; Cloning; Peptide fragment isolation; Protein structure folding; Protein trafficking sorting; Stability and mutagenesis; Synthesis of peptides and proteins

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; ARGININE; BETA LACTAMASE; HYBRID PROTEIN; TRANSACTIVATOR PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORRELATION ANALYSIS; GENETIC SELECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEIN VARIANT; REPORTER GENE; SOLUBILITY;

AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; BETA-LACTAMASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE LIBRARY; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SOLUBILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33644536727     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.051902606     Document Type: Article

References (55)

1. Baneyx, F. and Mujacic, M. 2004. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol. 22: 1399-1408.
2. Berks, B.C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22: 393-404.
3. Berks, B.C., Sargent, F., and Palmer, T. 2000. The Tat protein export pathway. Mol. Microbiol. 35: 260-274.
4. Betton, J. and Hofnung, M. 1996. Folding of a mutant maltose-binding protein of Escherichia coli which forms inclusion bodies. J. Biol. Chem. 271: 8046-8052.
5. Bogsch, E.G., Sargent, F., Stanley, N.R., Berks, B.C., Robinson, C., and Palmer, T. 1998. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273: 18003-18006.
6. Bowden, G.A., Baneyx, F., and Georgiou, G. 1992. Abnormal fractionation of β-lactamase in Escherichia coli: Evidence for an interaction with the inner membrane in the absence of a leader peptide. J. Bacteriol. 174: 3407-3410.
7. Cabantous, S., Terwilliger, T.C., and Waldo, G.S. 2005. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23: 102-107.
8. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. 99: 7877-7882.
9. Chen, Y.T., Scanlan, M.J., Sahin, U., Tureci, O., Gure, A.O., Tsang, S., Williamson, B., Stockert, E., Pfreundschuh, M., and Old, L.J. 1997. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. 94: 1914-1918.
10. DeLisa, M.P., Samuelson, P., Palmer, T., and Georgiou, G. 2002. Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J. Biol. Chem. 277: 29825-29831.
11. DeLisa, M.P., Tullman, D., and Georgiou, G. 2003. Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc. Natl. Acad. Sci. 100: 6115-6120.
12. Ellis, R.J. and Minton, A.P. 2003. Cell biology: Join the crowd. Nature 425: 27-28.
13. Feilmeier, B.J., Iseminger, G., Schroeder, D., Webber, H., and Phillips, G.J. 2000. Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J. Bacteriol. 182: 4068-4076.
14. Fisher, A.C. and DeLisa, M.P. 2004. A little help from my friends: Quality control of presecretory proteins in bacteria. J. Bacteriol. 186: 7467-7473.
15. Friedler, A., Veprintsev, D.B., Hansson, L.O., and Fersht, A.R. 2003. Kinetic instability of p53 core domain mutants: Implications for rescue by small molecules. J. Biol. Chem. 278: 24108-24112.
16. Galarneau, A., Primeau, M., Trudeau, L.E., and Michnick, S.W. 2002. β-lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein protein interactions. Nat. Biotechnol. 20: 619-622.
17. Georgiou, G. and Valax, P. 1996. Expression of correctly folded proteins in Escherichia coli. Curr. Opin. Biotechnol. 7: 190-197.
18. Gerth, M.L., Patrick, W.M., and Lutz, S. 2004. A second-generation system for unbiased reading frame selection. Protein Eng. Des. Sel. 17: 595-602.
19. Gohlke, U., Pullan, L., McDevitt, C.A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H.R., and Berks, B.C. 2005. The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. 102: 10482-10486.
20. Jack, R.L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T., and Sargent, F. 2004. Coordinating assembly and export of complex bacterial proteins. EMBO J. 23: 3962-3972.
21. Kipping, M., Lilie, H., Lindenstrauss, U., Andreesen, J.R., Griesinger, C., Carlomagno, T., and Bruser, T. 2003. Structural studies on a twin-arginine signal sequence. FEBS Lett. 550: 18-22.
22. Kuhlman, B., Dantas, G., Ireton, G.C., Varani, G., Stoddard, B.L., and Baker, D. 2003. Design of a novel globular protein fold with atomiclevel accuracy. Science 302: 1364-1368.
23. Lansbury Jr., P.T. 2001. Following nature's anti-amyloid strategy. Nat. Biotechnol. 19: 112-113.
24. Lesley, S.A., Graziano, J., Cho, C.Y., Knuth, M.W., and Klock, H.E. 2002. Gene expression response to misfolded protein as a screen for soluble recombinant protein. Protein Eng. 15: 153-160.
25. Lorimer, G.H. 1996. A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J. 10: 5-9.
26. Lutz, S., Fast, W., and Benkovic, S.J. 2002. A universal, vector-based system for nucleic acid reading-frame selection. Protein Eng. 15: 1025-1030.
27. Makrides, S.C. 1996. Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60: 512-538.
28. Maxwell, K.L., Mittermaier, A.K., Forman-Kay, J.D., and Davidson, A.R. 1999. A simple in vivo assay for increased protein solubility. Protein Sci. 8: 1908-1911.
29. Murphy, R., Green, S., Ritter, G., Cohen, L., Ryan, D., Woods, W., Rubira, M., Cebon, J., Davis, I.D., Sjolander, A., et al. 2005. Recombinant NY-ESO-1 cancer antigen: Production and purification under cGMP conditions. Prep. Biochem. Biotechnol. 35: 119-134.
30. Nurizzo, D., Halbig, D., Sprenger, G.A., and Baker, E.N. 2001. Crystal structures of the precursor form of glucose-fructose oxidoreductase from Zymomonas mobilis and its complexes with bound ligands. Biochemistry 40: 13857-13867.
31. Philibert, P. and Martineau, P. 2004. Directed evolution of single-chain Fv for cytoplasmic expression using the β-galactosidase complementation assay results in proteins highly susceptible to protease degradation and aggregation. Microb. Cell. Fact. 3: 16.
32. Radford, S.E. and Dobson, C.M. 1999. From computer simulations to human disease: Emerging themes in protein folding. Cell 97: 291-298.
33. Rodrigue, A., Chanal, A., Beck, K., Muller, M., and Wu, L.F. 1999. Cotranslocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem. 274: 13223-13228.
34. Roodveldt, C., Aharoni, A., and Tawfik, D.S. 2005. Directed evolution of proteins for heterologous expression and solubility. Curr. Opin. Struct. Biol. 15: 50-56.
35. Ross, C.A. and Poirier, M.A. 2004. Protein aggregation and neurodegenerative disease. Nat. Med. 10 (Suppl.): S10-S17.
36. Sanders, C., Wethkamp, N., and Lill, H. 2001. Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol. Microbiol. 41: 241-246.
37. Santini, C.L., Ize, B., Chanal, A., Muller, M., Giordano, G., and Wu, L.F. 1998. A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17: 101-112.
38. Santini, C.L., Bernadac, A., Zhang, M., Chanal, A., Ize, B., Blanco, C., and Wu, L.F. 2001. Translocation of jellyfish green fluorescent protein via the Tat system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J. Biol. Chem. 276: 8159-8164.
39. Sargent, F., Bogsch, E.G., Stanley, N.R., Wexler, M., Robinson, C., Berks, B.C., and Palmer, T. 1998. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17: 3640-3650.
40. Sargent, F., Gohlke, U., De Leeuw, E., Stanley, N.R., Palmer, T., Saibil, H.R., and Berks, B.C. 2001. Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268: 3361-3367.
41. Selkoe, D.J. 2001. Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev. 81: 741-766.
42. Settles, A.M., Yonetani, A., Baron, A., Bush, D.R., Cline, K., and Martienssen, R. 1997. Sec-independent protein translocation by the maize Hcf106 protein. Science 278: 1467-1470.
43. Shuman, H.A. 1982. Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J. Biol. Chem. 257: 5455-5461.
44. Sone, M., Kishigami, S., Yoshihisa, T., and Ito, K. 1997. Roles of disulfide bonds in bacterial alkaline phosphatase. J. Biol. Chem. 272: 6174-6178.
45. Thomas, J.D., Daniel, R.A., Errington, J., and Robinson, C. 2001. Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol. Microbiol. 39: 47-53.
46. Tsumoto, K., Umetsu, M., Kumagai, I., Ejima, D., and Arakawa, T. 2003. Solubilization of active green fluorescent protein from insoluble particles by guanidine and arginine. Biochem. Biophys. Res. Commun. 312: 1383-1386.
47. Waldo, G.S., Standish, B.M., Berendzen, J., and Terwilliger, T.C. 1999. Rapid protein-folding assay using green fluorescent protein. Nat. Biotechnol. 17: 691-695.
48. Wall, J.G. and Pluckthun, A. 1995. Effects of overexpressing folding modulators on the in vivo folding of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6: 507-516.
49. Weiner, J.H., Bilous, P.T., Shaw, G.M., Lubitz, S.P., Frost, L., Thomas, G.H., Cole, J.A., and Turner, R.J. 1998. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93: 93-101.
50. Wigley, W.C., Stidham, R.D., Smith, N.M., Hunt, J.F., and Thomas, P.J. 2001. Protein solubility and folding monitored in vivo by structural complementation of a genetic marker protein. Nat. Biotechnol. 19: 131-136.
51. Williams, A.D., Sega, M., Chen, M., Kheterpal, I., Geva, M., Berthelier, V., Kaleta, D.T., Cook, K.D., and Wetzel, R. 2005. Structural properties of Ab protofibrils stabilized by a small molecule. Proc. Natl. Acad. Sci. 102: 7115-7120.
52. Wood, S.J., Wetzel, R., Martin, J.D., and Hurle, M.R. 1995. Prolines and amyloidogenicity in fragments of the Alzheimer's peptide β/A4. Biochemistry 34: 724-730.
53. Wurth, C., Guimard, N.K., and Hecht, M.H. 2002. Mutations that reduce aggregation of the Alzheimer's Aβ42 peptide: An unbiased search for the sequence determinants of Aβ amyloidogenesis. J. Mol. Biol. 319: 1279-1290.
54. Zaccolo, M., Williams, D.M., Brown, D.M., and Gherardi, E. 1996. An approach to random mutagenesis of DNA using mixtures of triphosphate derivatives of nucleoside analogues. J. Mol. Biol. 255: 589-603.
55. Zhu, J. and Winans, S.C. 2001. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc. Natl. Acad. Sci. 98: 1507-1512.