Understanding the relationship between the primary structure of proteins and its propensity to be soluble on overexpression in Escherichia coli

Protein Science

Volumn 14, Issue 3, 2005, Pages 582-592

  Idicula Thomas, Susan ^a   Balaji, Petety V ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

Aliphatic index; Inclusion body; Instability index; Solubility index; Thermostability; Tripeptide frequency

Indexed keywords

AMINO ACID; DIPEPTIDE; ESCHERICHIA COLI PROTEIN; RECOMBINANT PROTEIN; TRIPEPTIDE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GROWTH; CELL INCLUSION; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; SOLUBILITY; THERMOSTABILITY;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; ESCHERICHIA COLI; HEAT; MOLECULAR WEIGHT; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SOLUBILITY;

EID: 14144255127     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041009005     Document Type: Article

References (72)

1. Bertone, P., Kluger, Y., Lan, N., Zheng, D., Christendat, D., Yee, A., Edwards, A.M., Arrowsmith, C.H., Montelione, G.T., and Gerstein, M. 2001. SPINE: An integrated tracking database and data mining approach for identifying feasible targets in high-throughput structural proteomics. Nucleic Acids Res. 29: 2884-2898.
2. Boeggeman, E.E., Ramakrishnan, B., and Qasba, P.K. 2003. The N-terminal stem region of bovine and human β1,4-galactosyltransferase 1 increases the in vitro folding efficiency of their catalytic domain from inclusion bodies. Protein Expr. Purif. 30: 219-229.
3. Carrio, M.M. and Villaverde, A. 2001. Protein aggregation as bacterial inclusion bodies is reversible. FEBS Lett. 489: 29-33.
4. Cha, H.J., Wu, C.F., Valdes, J.J., Rao, G., and Bentley, W.E. 2000. Observations of green fluorescent protein as a fusion partner in genetically engineered Escherichia coli: Monitoring protein expression and solubility. Biotechnol. Bioeng. 67: 565-574.
5. Chan, H.S. and Dill, K.A. 1994. Transition states and folding dynamics of proteins and heteropolymers. J. Chem. Phys. 100: 9238-9257.
6. Chen, J., Acton, T.B., Basu, S.K., Montelione, G.T., and Inouye, M. 2002. Enhancement of the solubility of proteins overexpressed in Escherichia coli by heat shock. J. Mol. Microbiol. Biotechnol. 4: 519-524.
7. Clark, E.D.B. 1998. Refolding of recombinant proteins. Curr. Opin. Biotechnol. 9: 157-163.
8. Cortazzo, P., Cervenansky, C., Marin, M., Reiss, C., Ehrlich, R., and Deana, A. 2002. Silent mutations affect in vivo protein folding in Escherichia coli. Biochem. Biophys. Res. Commun. 293: 537-541.
9. Dale, G.E., Broger, C., Langen, H., D'Arcy, A., and Stuber, D. 1994. Improving protein solubility through rationally designed amino acid replacements: Solubilization of the trimethoprim-resistant type S1 dihydrofolate reductase. Protein Eng. 7: 933-939.
10. Davis, G.D., Elisee, C., Newham, D.M., and Harrison, R.G. 1999. New fusion protein systems designed to give soluble expression in Escherichia coli. Biotechnol. Bioeng. 65: 382-388.
11. Doray, B., Chen, C.D., and Kemper, B. 2001. N-terminal deletions and His-tag fusions dramatically affect expression of cytochrome p450 2C2 in bacteria. Arch. Biochem. Biophys. 393: 143-153.
12. Fink, A.L. 1998. Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold Des. 3: R9-R23.
13. Folkers, G.E., van Buuren, B.N., and Kaptein, R. 2004. Expression screening, protein purification and NMR analysis of human protein domains for structural genomics. J. Struct. Funct. Genomics 5: 119-131.
14. Forrer, P. and Jaussi, R. 1998. High-level expression of soluble heterologous proteins in the cytoplasm of Escherichia coli by fusion to the bacteriophage λ head protein D. Gene 224: 45-52.
15. Fox, J.D., Kapust, R.B., and Waugh, D.S. 2001. Single amino acid substitutions on the surface of Escherichia coli maltose-binding protein can have a profound impact on the solubility of fusion proteins. Protein Sci. 10: 622-630.
16. Georgiou, G. and Valax, P. 1999. Isolating inclusion bodies from bacteria. Methods Enzymol. 309: 48-58.
17. Goh, C.S., Lan, N., Douglas, S.M., Wu, B., Echols, N., Smith, A., Milburn, D., Montelione, G.T., Zhao, H., and Gerstein, M. 2004. Mining the structural genomics pipeline: Identification of protein properties that affect high-throughput experimental analysis. J. Mol. Biol. 336:115-130.
18. Gromiha, M.M., Oobatake, M., and Sarai, A. 1999. Important amino acid properties for enhanced thermostability from mesophilic to thermophilic proteins. Biophys. Chem. 82: 51-67.
19. Guruprasad, K., Reddy, B.V., and Pandit, M.W. 1990. Correlation between stability of a protein and its dipeptide composition: A novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng. 4: 155-161.
20. Hammarstrom, M., Hellgren, N., van Den Berg, S., Berglund, H., and Hard, T. 2002. Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli. Protein Sci. 11: 313-321.
21. Ikai, A. 1980. Thermostability and aliphatic index of globular proteins. J. Biochem. 88: 1895-1898.
22. Jenkins, T.M., Hickman, A.B., Dyda, F., Ghirlando, R., Davies, D.R., and Craigie, R. 1995. Catalytic domain of human immunodeficiency virus type 1 integrase: Identification of a soluble mutant by systematic replacement of hydrophobic residues. Proc. Natl. Acad. Sci. 92: 6057-6061.
23. Kallberg, Y., Gustafsson, M., Persson, B., Thyberg, J., and Johansson, J. 2001. Prediction of amyloid fibril-forming proteins. J. Biol. Chem. 276: 12945-12950.
24. Kapust, R.B. and Waugh, D.S. 1999. Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 8: 1668-1674.
25. Katzav-Gozansky, T., Hanan, E., and Solomon, B. 1996. Effect of monoclonal antibodies in preventing carboxypeptidase A aggregation. Biotechnol. Appl. Biochem. 23: 227-230.
26. King, J., Haase-Pettingell, C., Robinson, A.S., Speed, M., and Mitraki, A. 1996. Thermolabile folding intermediates: Inclusion body precursors and chaperonin substrates. FASEB J. 10: 57-66.
27. Knaust, R.K. and Nordlund, P. 2001. Screening for soluble expression of recombinant proteins in a 96-well format. Anal. Biochem. 297: 79-85.
28. Komar, A.A., Lesnik, T., and Reiss, C. 1999. Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation. FEBS Lett. 462: 387-391.
29. 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.
30. Lilie, H., Schwarz, E., and Rudolph, R. 1998. Advances in refolding of proteins produced in E. coli. Curr. Opin. Biotechnol. 9: 497-501.
31. Lin, Z., Thorsen, T., and Arnold, F.H. 1999. Functional expression of horse-radish peroxidase in E. coli by directed evolution. Biotechnol. Prog. 15: 467-471.
32. Luan, C.H., Qiu, S., Finley, J.B., Carson, M., Gray, R.J., Huang, W., Johnson, D., Tsao, J., Reboul, J., Vaglio, P., et al. 2004. High-throughput expression of C. elegans proteins. Genome Res. 14: 2102-2110.
33. Malissard, M. and Berger, E.G. 2001. Improving solubility of catalytic domain of human β-1,4-galactosyltransferase 1 through rationally designed amino acid replacements. Eur. J. Biochem. 268: 4352-4358.
34. Makrides, S.C. 1996. Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60: 512-538.
35. Mogk, A., Mayer, M.P., and Deuerling, E. 2002. Mechanisms of protein folding: Molecular chaperones and their application in biotechnology. Chembiochem. 3: 807-814.
36. Murby, M., Samuelsson, E., Nguyen, T.N., Mignard, L., Power, U., Binz, H., Uhlen, M., and Stahl, S. 1995. Hydrophobicity engineering to increase solubility and stability of a recombinant protein from respiratory syncytial virus. Eur. J. Biochem. 230: 38-44.
37. Ni, L., Zhou, J., Hurley, T.D., and Weiner, H. 1999. Human liver mitochondrial aldehyde dehydrogenase: Three-dimensional structure and the restoration of solubility and activity of chimeric forms. Protein Sci. 8: 2784-2790.
38. Nygaard, F.B. and Harlow, K.W. 2001. Heterologous expression of soluble, active proteins in Escherichia coli: The human estrogen receptor hormone-binding domain as paradigm. Protein Expr. Purif. 21: 500-509.
39. Oberg, K., Chrunyk, B.A., Wetzel, R., and Fink, A.L. 1994. Nativelike secondary structure in interleukin-1 β inclusion bodies by attenuated total reflectance FTIR. Biochemistry 33: 2628-2634.
40. Oswald, T., Wende, W., Pingoud, A., and Rinas, U. 1994. Comparison of N-terminal affinity fusion domains: Effect on expression level and product heterogeneity of recombinant restriction endonuclease EcoR V. Appl. Microbiol. Biotechnol. 42: 73-77.
41. Pedelacq, J.D., Piltch, E., Liong, E.C., Berendzen, J., Kim, C.Y., Rho, B.S., Park, M.S., Terwilliger, T.C., and Waldo, G.S. 2002. Engineering soluble proteins for structural genomics. Nat. Biotechnol. 20: 927-932.
42. Przybycien, T.M., Dunn, J.P., Valax, P., and Georgiou, G. 1994. Secondary structure characterization of β-lactamase inclusion bodies. Protein Eng. 7: 131-136.
43. Ramachandiran, V., Willms, C., Kramer, G., and Hardesty, B. 2000. Fluorophores at the N-terminus of nascent chloramphenicol acetyltransferase peptides affect translation and movement through the ribosome. J. Biol. Chem. 275: 1781-1786.
44. Rogers, S., Wells, R., and Rechsteiner, M. 1986. Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234: 364-368.
45. Rosen, R., Biran, D., Gur, E., Becher, D., Hecker, M., and Ron, E.Z. 2002. Protein aggregation in Escherichia coli: Role of proteases. FEMS Microbiol. Lett. 207: 9-12.
46. Rudolph, R. 1990. Renaturation of recombinant, disulfide-bonded proteins from inclusion bodies. In Modern methods in protein and nucleic acid research (ed. H. Tschesche), pp. 149-172. Walter de Gruyter, Berlin.
47. Rudolph, R. and Lilie, H. 1996. In vitro folding of inclusion body proteins. FASEB J. 10: 49-56.
48. Sachdev, D. and Chirgwin, J.M. 1998. Solubility of proteins isolated from inclusion bodies is enhanced by fusion to maltose-binding protein or thioredoxin. Protein Expr. Purif. 12: 122-132.
49. Sati, S.P., Singh, S.K., Kumar, N., and Sharma, A. 2002. Extra terminal residues have a profound effect on the folding and solubility of a Plasmodium falciparum sexual stage-specific protein over-expressed in Escherichia coli. Eur. J. Biochem. 269: 5259-5263.
50. Schein, C.H. 1990. Solubility as a function of protein structure and solvent components. Biotechnology 8: 308-317.
51. Schein, C.H. and Noteborn, M.H.M. 1988. Formation of soluble recombinant proteins in Escherichia coli is favored by lower growth temperature. Biotechnology 6: 291-294.
52. Shakhnovich, E.I. and Gutin, A.M. 1993. Engineering of stable and fast-folding sequences of model proteins. Proc. Natl. Acad. Sci. 90: 7195-7199.
53. Shin, Y.P., Kung, W.M., Chen, J.C., Yeh, C.H., Wang, A.H., and Wang, T.F. 2002. High-throughput screening of soluble recombinant proteins. Protein Sci. 11: 1714-1719.
54. Socci, N.D. and Onuchic, J.N. 1994. Folding kinetics of protein-like heteropolymers. J. Chem. Phys. 100: 1519-1528.
55. Stevens, R.C. 2000. Design of high-throughput methods of protein production for structural biology. Structure 8:R177-R185.
56. Tandon, S. and Horowitz, P. 1988. The effects of lauryl maltoside on the reactivation of several enzymes after treatment with guanidinium chloride. Biochim. Biophys. Acta 955:19-25.
57. Timson, D.J. and Reece, R.J. 2003. Functional analysis of disease-causing mutations in human galactokinase. Eur. J. Biochem. 270: 1767-1774.
58. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27: 527-533.
59. Tresaugues, L., Collinet, B., Minard, P., Henckes, G., Aufrere, R., Blondeau, K., Liger, D., Zhou, C.Z., Janin, J., Van Tilbeurgh, H., et al. 2004. Refolding strategies from inclusion bodies in a structural genomics project. J. Struct. Funct. Genomics 5: 195-204.
60. 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:I383-1386.
61. Uversky, V.N., Gillespie, J.R., and Fink, A.L. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427.
62. Waldo, G.S. 2003. Genetic screens and directed evolution for protein solubility. Curr. Opin. Chem. Biol. 7: 33-38.
63. Wetzel, R., Perry, L.J., and Veilleux, C. 1991. Mutations in human interferon γ affecting inclusion body formation identified by a general immunochemical screen. Biotechnology 9: 731-737.
64. 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.
65. Wilkinson, D.L. and Harrison, R.G. 1991. Predicting the solubility of recombinant proteins in Escherichia coli. Biotechnology 9: 443-448.
66. Williams, R.M., Obradovi, Z., Mathura, V., Braun, W., Garner, E.C., Young, J., Takayama, S., Brown, C.J., and Dunker, A.K. 2001. The protein non-folding problem: Amino acid determinants of intrinsic order and disorder. Pac. Symp. Biocomput. 6: 89-100.
67. Winter, J., Neubauer, P., Glockshuber, R., and Rudolph, R. 2001. Increased production of human proinsulin in the periplasmic space of Escherichia coli by fusion to DsbA. J. Biotechnol. 84: 175-185.
68. Woestenenk, E.A., Hammarstrom, M., van den Berg, S., Hard, T., and Berglund, H. 2004. His tag effect on solubility of human proteins produced in Escherichia coli: A comparison between four expression vectors. J. Struct. Funct. Genomics. 5: 217-229.
69. Yakhnin, A.V. and Babitzke, P. 2002. NusA-stimulated RNA polymerase pausing and termination participates in the Bacillus subtilis trp operon attenuation mechanism in vitro. Proc. Natl. Acad. Sci. 99: 11067-11072.
70. Zaccaria, D., Greco, R., MacWilliams, H., Bozzaro, S., and Ceccarelli, A. 1998. UGUS, a reporter for use with destabilizing N-termini. Nucleic Acids Res. 26: 1128-1129.
71. Zhang, Y., Olsen, D.R., Nguyen, K.B., Olson, P.S., Rhodes, E.T., and Mascarenhas. D. 1998. Expression of eukaryotic proteins in soluble form in Escherichia coli. Protein Expr. Purif. 12: 159-165.
72. Zhou, P., Lugovskoy, A.A., and Wagner, G. 2001. A solubility-enhancement tag (SET) for NMR studies of poorly behaving proteins. J. Biomol. NMR 20: 11-14.