Tuned Escherichia coli as a host for the expression of disulfide-rich proteins

Biotechnology Journal

Volumn 6, Issue 6, 2011, Pages 686-699

  Salinas, Gustavo ^a   Pellizza, Leonardo ^a   Margenat, Mariana ^a   Fló, Martín ^a   Fernández, Cecilia ^a  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Cysteine; Kunitz inhibitors; Oxidative protein folding; Redox compartmentalization; Thiols

Indexed keywords

CYSTEINE; KUNITZ INHIBITORS; OXIDATIVE PROTEIN FOLDING; REDOX COMPARTMENTALIZATION; THIOLS;

AMINO ACIDS; COVALENT BONDS; ENZYME INHIBITION; ESCHERICHIA COLI; PROTEIN FOLDING;

PROTEINS;

CYSTEINE; DISULFIDE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; CYTOPLASM; DISULFIDE BOND; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; ISOMERIZATION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; REVIEW;

CYSTEINE; CYTOPLASM; DISULFIDES; ESCHERICHIA COLI; OXIDOREDUCTASES; PERIPLASM; PROTEASE INHIBITORS; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; SULFHYDRYL COMPOUNDS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 79957793254     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201000335     Document Type: Review

References (56)

1. Hogg, P. J., Disulfide bonds as switches for protein function. Trends Biochem. Sci. 2003, 28, 210-214.
2. Holmgren, A., Johansson, C., Berndt, C., Lonn, M. E. et al., Thiol redox control via thioredoxin and glutaredoxin systems. Biochem. Soc. Trans. 2005, 33, 1375-1377.
3. Tu, B. P., Weissman, J. S., Oxidative protein folding in eukaryotes: Mechanisms and consequences. J. Cell. Biol. 2004, 164, 341-346.
4. Depuydt, M., Messens, J., Collet, J. F., How proteins form disulfide bonds. Antioxid. Redox Signaling 2011, DOI: 10189/ars.20103675.
5. Kemp, M., Go, Y. M., Jones, D. P., Nonequilibrium thermodynamics of thiol/disulfide redox systems: A perspective on redox systems biology. Free Radical Biol. Med. 2008, 44, 921-937.
6. Riemer, J., Bulleid, N., Herrmann, J. M., Disulfide formation in the ER and mitochondria: Two solutions to a common process. Science 2009, 324, 1284-1287.
7. Meyer, Y., Buchanan, B. B., Vignols, F., Reichheld, J. P., Thioredoxins and glutaredoxins: Unifying elements in redox biology. Annu. Rev. Genet. 2009, 43, 335-367.
8. Toledano, M. B., Kumar, C., Le Moan, N., Spector, D. et al., The system biology of thiol redox system in Escherichia coli and yeast: Differential functions in oxidative stress, iron metabolism and DNA synthesis. FEBS Lett. 2007, 581, 3598-3607.
9. Messens, J., Collet, J. F., Pathways of disulfide-bond formation in Escherichia coli. Int. J. Biochem. Cell Biol. 2006, 38, 1050-1062.
10. Schafer, F. Q., Buettner, G. R., Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biol. Med. 2001, 30, 1191-1212.
11. Lillig, C. H., Berndt, C., Holmgren, A., Glutaredoxin systems. Biochim. Biophys. Acta 2008, 1780, 1304-1317.
12. Atkinson, H. J., Babbitt, P. C., An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations. PLoS Comput. Biol. 2009, 5, e1000541.
13. Jurado, P., de Lorenzo, V., Fernandez, L. A., Thioredoxin fusions increase folding of single-chain Fv antibodies in the cytoplasm of Escherichia coli: Evidence that chaperone activity is the prime effect of thioredoxin. J. Mol. Biol. 2006, 357, 49-61.
14. Bardwell, J. C., McGovern, K., Beckwith, J., Identification of a protein required for disulfide-bond formation in vivo. Cell 1991, 67, 581-589.
15. Kadokura, H., Katzen, F., Beckwith, J., Protein disulfide-bond formation in prokaryotes. Annu. Rev. Biochem. 2003, 72, 111-135.
16. Sevier, C. S., Kaiser, C. A., Conservation and diversity of the cellular disulfide-bond formation pathways. Antioxid. Redox Signaling 2006, 8, 797-811.
17. Wunderlich, M., Glockshuber, R., Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci. 1993, 2, 717-726.
18. Guddat, L. W., Bardwell, J. C., Zander, T., Martin, J. L., The uncharged surface features surrounding the active site of Escherichia coli DsbA are conserved and are implicated in peptide binding. Protein Sci. 1997, 6, 1148-1156.
19. Bessette, P. H., Cotto, J. J., Gilbert, H. F., Georgiou, G., In vivo and in vitro function of the Escherichia coli periplasmic cysteine oxidoreductase DsbG. J. Biol. Chem. 1999, 274, 7784-7792.
20. Rietsch, A., Bessette, P., Georgiou, G., Beckwith, J., Reduction of the periplasmic disulfide-bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin. J. Bacteriol. 1997, 179, 6602-6608.
21. Depuydt, M., Leonard, S. E., Vertommen, D., Denoncin, K. et al., A periplasmic reducing system protects single cysteine residues from oxidation. Science 2009, 326, 1109-1111.
22. di Guan, C., Li, P., Riggs, P. D., Inouye, H., Vectors that facilitate the expression and purification of foreign peptides in Escherichia coli by fusion to maltose-binding protein. Gene 1988, 67, 21-30.
23. de Marco, A., Strategies for successful recombinant expression of disulfide-bond-dependent proteins in Escherichia coli. Microb. Cell Fact. 2009, 8, 26.
24. Thie, H., Schirrmann, T., Paschke, M., Dubel, S. et al., SRP and Sec pathway leader peptides for antibody phage display and antibody fragment production in E. coli. N. Biotechnol. 2008, 25, 49-54.
25. Correa, A., Opezzo, P., Tuning different expression parameters to achieve soluble recombinant proteins in E. coli: Advantages of high-throughput screening. Biotechnol. J. 2011, DOI: 10.1002/biot.201100025.
26. Baneyx, F., Mujacic, M., Recombinant protein folding and misfolding in Escherichia coli Nat. Biotechnol. 2004, 22, 1399-1408.
27. Hayhurst, A., Harris, W. J., Escherichia coli skp chaperone coexpression improves solubility and phage display of single-chain antibody fragments. Protein Expression Purif. 1999, 15, 336-343.
28. Faulkner, M. J., Veeravalli, K., Gon, S., Georgiou, G. et al., Functional plasticity of a peroxidase allows evolution of diverse disulfide-reducing pathways. Proc. Natl. Acad. Sci. USA 2008, 105, 6735-6740.
29. Yamamoto, Y., Ritz, D., Planson, A. G., Jonsson, T. J. et al., Mutant AhpC peroxiredoxins suppress thiol-disulfide redox deficiencies and acquire deglutathionylating activity. Mol. Cell 2008, 29, 36-45.
30. Stewart, E. J., Aslund, F., Beckwith, J., Disulfide-bond formation in the Escherichia coli cytoplasm: An in vivo role reversal for the thioredoxins. EMBO J. 1998, 17, 5543-5550.
31. Bessette, P. H., Aslund, F., Beckwith, J., Georgiou, G., Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc. Natl. Acad. Sci. USA 1999, 96, 13703-13708.
32. Gebendorfer, K. M., Winter, J., The periplasm of E. coli-oxidative folding of recombinant proteins, in: Buchner, J. Moroder, L. (Eds.), Oxidative folding of peptides and proteins, Royal Society of Chemistry, Cambridge 2009, pp. 41-66.
33. Vallejo, L. F., Rinas, U., Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb. Cell Fact. 2004, 3, 11.
34. Rawlings, N. D., Tolle, D. P., Barrett, A. J., Evolutionary families of peptidase inhibitors. Biochem. J. 2004, 378, 705-716.
35. Lu, W., Apostol, I., Qasim, M. A., Warne, N. et al., Binding of amino acid side-chains to S1 cavities of serine proteinases. J. Mol. Biol. 1997, 266, 441-461.
36. Arolas, J. L., Lorenzo, J., Rovira, A., Vendrell, J. et al., Secondary binding site of the potato carboxypeptidase inhibitor. Contribution to its structure, folding, and biological properties. Biochemistry 2004, 43, 7973-7982.
37. Arolas, J. L., Lorenzo, J., Rovira, A., Castella, J. et al., A carboxypeptidase inhibitor from the tick Rhipicephalus bursa: Isolation, cDNA cloning, recombinant expression, and characterization. J. Biol. Chem. 2005, 280, 3441-3448.
38. Arolas, J. L., Bronsoms, S., Ventura, S., Aviles, F. X. et al., Characterizing the tick carboxypeptidase inhibitor: Molecular basis for its two-domain nature. J. Biol. Chem. 2006, 281, 22906-22916.
39. Sanglas, L., Aviles, F. X., Huber, R., Gomis-Ruth, F. X. et al., Mammalian metallopeptidase inhibition at the defense barrier of Ascaris parasite. Proc. Natl. Acad. Sci. USA 2009, 106, 1743-1747.
40. Lauber, T., Marx, U. C., Schulz, A., Kreutzmann, P. et al., Accurate disulfide formation in Escherichia coli: Overexpression and characterization of the first domain (HF6478) of the multiple Kazal-type inhibitor LEKTI. Protein Expression Purif. 2001, 22, 108-112.
41. Vitzithum, K., Lauber, T., Kreutzmann, P., Schulz, A. et al., LEKTI domain 15 is a functional Kazal-type proteinase inhibitor. Protein Expression Purif. 2008, 57, 45-56.
42. Gonzalez, S., Flo, M., Margenat, M., Duran, R. et al., A family of diverse Kunitz inhibitors from Echinococcus granulosus potentially involved in host-parasite cross-talk. PLoS One 2009, 4, e7009.
43. Conchillo-Sole, O., de Groot, N. S., Aviles, F. X., Vendrell, J. et al., AGGRESCAN: A server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 2007, 8, 65.
44. Arolas, J. L., Aviles, F. X., Chang, J. Y., Ventura, S., Folding of small disulfide-rich proteins: Clarifying the puzzle. Trends Biochem. Sci. 2006, 31, 292-301.
45. Castillo, V., Graña-Montes, R., Sabate, R., Ventura, S., Prediction of the aggregation propensity of proteins from the primary sequence: Aggregation propensity of proteomes. Biotechnol. J. 2011, DOI: 10.1002/biot.201000331.
46. Mamathambika, B. S., Bardwell, J. C., Disulfide-linked protein folding pathways. Annu. Rev. Cell Dev. Biol. 2008, 24, 211-235.
47. Arolas, J. L., Ventura, S., Protease inhibitors as models for the study of oxidative folding. Antioxid. Redox Signaling 2011, 14, 97-112.
48. Staley, J. P., Kim, P. S., Complete folding of bovine pancreatic trypsin inhibitor with only a single disulfide bond. Proc. Natl. Acad. Sci. USA 1992, 89, 1519-1523.
49. Chang, J. Y., Distinct folding pathways of two homologous disulfide proteins: Bovine pancreatic trypsin inhibitor and tick anticoagulant peptide. Antioxid. Redox Signaling 2011, 14, 127-135.
50. Ostermeier, M., Georgiou, G., The folding of bovine pancreatic trypsin inhibitor in the Escherichia coli periplasm. J. Biol. Chem. 1994, 269, 21072-21077.
51. Foit, L., Mueller-Schickert, A., Mamathambika, B. S., Gleiter, S. et al., Genetic selection for enhanced folding in vivo targets the Cys14-Cys38 disulfide bond in bovine pancreatic trypsin inhibitor. Antioxid. Redox Signaling 2011, 14, 973-984.
52. de Groot, N. S., Sabate, R., Ventura, S., Amyloids in bacterial inclusion bodies. Trends Biochem. Sci. 2009, 34, 408-416.
53. Bardwell, J., Thiol modifications in a snapshot. Nat. Biotechnol. 2005, 23, 42-43.
54. den Blaauwen, T., Driessen, A. J., Sec-dependent preprotein translocation in bacteria. Arch. Microbiol. 1996, 165, 1-8.
55. Luirink, J., Sinning, I., SRP-mediated protein targeting: Structure and function revisited. Biochim. Biophys. Acta 2004, 1694, 17-35.
56. Huber, D., Boyd, D., Xia, Y., Olma, M. H. et al., Use of thioredoxin as a reporter to identify a subset of Escherichia coli signal sequences that promote signal recognition particle-dependent translocation. J. Bacteriol. 2005, 187, 2983-2991.