International
Tables for
Crystallography
Volume F
Crystallography of biological macromolecules
Edited by M. G. Rossmann and E. Arnold

International Tables for Crystallography (2006). Vol. F, ch. 3.1, pp. 65-80   | 1 | 2 |
https://doi.org/10.1107/97809553602060000659

Chapter 3.1. Preparing recombinant proteins for X-ray crystallography

S. H. Hughesa and A. M. Stockb*

aNational Cancer Institute, Frederick Cancer R&D Center, Frederick, MD 21702-1201, USA, and bCenter for Advanced Biotechnology and Medicine, Howard Hughes Medical Institute and University of Medicine and Dentistry of New Jersey – Robert Wood Johnson Medical School, 679 Hoes Lane, Piscataway, NJ 08854–5627, USA
Correspondence e-mail:  stock@cabm.rutgers.edu

References

Abelson, J. N. & Simon, M. I. (1990). Guide to protein purification. Methods Enzymol. 182, 1–894.Google Scholar
Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1995). Short protocols in molecular biology: a compendium of methods from current protocols in molecular biology, 3rd ed. New York: Greene Publishing Associates and Wiley.Google Scholar
Beggs, J. D. (1978). Transformation of yeast by a replicating hybrid plasmid. Nature (London), 275, 104–109.Google Scholar
Bhandari, P. & Gowrishankar, J. (1997). An Escherichia coli host strain useful for efficient overproduction of cloned gene products with NaCl as the inducer. J. Bacteriol. 179, 4403–4406.Google Scholar
Biswas, E. E., Fricke, W. M., Chen, P. H. & Biswas, S. B. (1997). Yeast DNA helicase A: cloning, expression, purification, and enzymatic characterization. Biochemistry, 36, 13277–13284.Google Scholar
Bollag, D. M., Rozycki, M. D. & Edelstein, S. J. (1996). Protein methods. New York: Wiley-Liss.Google Scholar
Boyer, P. L. & Hughes, S. H. (1996). Site-directed mutagenic analysis of viral polymerases and related proteins. Methods Enzymol. 275, 538–555.Google Scholar
Brinkmann, U., Mattes, R. E. & Buckel, P. (1989). High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene, 85, 109–114.Google Scholar
Broach, J. R. (1983). Construction of high copy number yeast vectors using 2 µm circle sequences. Methods Enzymol. 101, 307–325.Google Scholar
Chong, S., Mersha, F. B., Comb, D. G., Scott, M. E., Landry, D., Vence, L. M., Perler, F. B., Benner, J., Kucera, R. B., Hirvonen, C. A., Pelletier, J. J., Paulus, H. & Xu, M. Q. (1997). Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene, 192, 271–281.Google Scholar
Chong, S., Shao, Y., Paulus, H., Benner, J., Perler, F. B. & Xu, M. Q. (1996). Protein splicing involving the Saccharomyces cerevisiae VMA intein. The steps in the splicing pathway, side reactions leading to protein cleavage, and establishment of an in vitro splicing system. J. Biol. Chem. 271, 22159–22168.Google Scholar
Cohen, S. L., Ferre-D'Amare, A. R., Burley, S. K. & Chait, B. T. (1995). Probing the solution structure of the DNA-binding protein Max by a combination of proteolysis and mass spectrometry. Protein Sci. 46, 1088–1099.Google Scholar
Cole, P. A. (1996). Chaperone-assisted protein expression. Structure, 4, 239–242.Google Scholar
Cregg, J. M., Vedick, T. S. & Raschke, W. C. (1993). Recent advances in the expression of foreign genes in Pichia pastoris. Biotechnology, 11, 905–910.Google Scholar
De Bernardez Clark, E. (1998). Refolding of recombinant proteins. Curr. Opin. Biotechnol. 9, 157–163.Google Scholar
De Boer, H. A. & Kastelein, R. A. (1986). Biased codon usage: an exploration of its role in optimization of translation. In Maximizing gene expression, edited by W. S. Reznikioff & L. Gold, pp. 225–285. Boston: Butterworths.Google Scholar
Del Tito, B. J. Jr, Ward, J. M., Hodgson, J., Gershater, C. J. L., Edwards, H., Wysocki, L. A., Watson, F. A., Sathe, G. & Kane, J. F. (1995). Effects of a minor isoleucyl tRNA on heterologous protein translation in Escherichia coli. J. Bacteriol. 177, 7086–7091.Google Scholar
Enfors, S.-O. (1992). Control of in vivo proteolysis in the production of recombinant proteins. Trends Biotechnol. 10, 310–315.Google Scholar
Ernst, J. F. & Kawashima, E. (1988). Variations in codon usage are not correlated with heterologous gene expression in Saccharomyces cerevisiae and Escherichia coli. J. Biotechnol. 7, 1–9.Google Scholar
Ferré-D'Amaré, A. R. & Burley, S. K. (1994). Use of dynamic light scattering to assess crystallizability of macromolecules and macromolecular assemblies. Structure, 2, 357–359.Google Scholar
Fischer, B., Sumner, I. & Goodenough, P. (1993). Isolation, renaturation, and formation of disulfide bonds of eukaryotic proteins expressed in Escherichia coli as inclusion bodies. Biotechnol. Bioeng. 41, 3–13.Google Scholar
Georgiou, G. & Valax, P. (1996). Expression of correctly folded proteins in Escherichia coli. Curr. Opin. Biotechnol. 7, 190–197.Google Scholar
Gold, L., Pribnow, D., Schneider, T., Shinedling, S., Singer, B. S. & Stormo, G. (1981). Translational initiation in prokaryotes. Annu. Rev. Microbiol. 35, 365–403.Google Scholar
Goldman, E., Rosenberg, A. H., Zubay, G. & Studier, F. W. (1995). Consecutive low-usage leucine codons block translation only when near the 5′ end of a message in Escherichia coli. J. Mol. Biol. 245, 467–473.Google Scholar
Gottesman, S. (1990). Minimizing proteolysis in Escherichia coli: genetic solutions. Methods Enzymol. 185, 119–129.Google Scholar
Grinna, L. S. & Tschopp, J. F. (1989). Size distribution and general structural features of N-linked oligosaccharides from the methylotrophic yeast, Pichia pastoris. Yeast, 5, 107–115.Google Scholar
Guise, A. D., West, S. M. & Chaudhuri, J. B. (1996). Protein folding in vivo and renaturation of recombinant proteins from inclusion bodies. Mol. Biotechnol. 6, 53–64.Google Scholar
Hendrickson, W. A., Horton, J. R. & LeMaster, D. M. (1990). Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9, 1665–1672.Google Scholar
Hernan, R. A., Hui, H. L., Andracki, M. E., Noble, R. W., Sligar, S. G., Walder, J. A. & Walder, R. Y. (1992). Human hemoglobin expression in Escherichia coli: importance of optimal codon usage. Biochemistry, 31, 8619–8628.Google Scholar
Higgins, D. R. & Cregg, J. (1998). Methods in molecular biology, Vol. 103. Pichia protocols. Totowa: Humana Press.Google Scholar
Hirel, P. H., Schmitter, M. J., Dessen, P., Fayat, G. & Blanquet, S. (1989). Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc. Natl Acad. Sci. USA, 86, 8247–8251.Google Scholar
Hockney, R. C. (1994). Recent developments in heterologous protein production in Escherichia coli. Trends Biotechnol. 12, 456–463.Google Scholar
Hofmann, A., Tai, M., Wong, W. & Glabe, C. G. (1995). A sparse matrix screen to establish initial conditions for protein renaturation. Anal. Biochem. 230, 8–15.Google Scholar
Hollenberg, C. P. & Gellissen, G. (1997). Production of recombinant proteins by methylotrophic yeasts. Curr. Opin. Biotechnol. 8, 554–560.Google Scholar
Hubbard, S. J. (1998). The structural aspects of limited proteolysis of native proteins. Biochim. Biophys. Acta, 1382, 191–206.Google Scholar
Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (1990). PCR protocols: a guide to methods and applications. San Diego: Academic Press.Google Scholar
Jarvis, D. L., Kawar, Z. S. & Hollister, J. R. (1998). Engineering N-glycosylation pathways in the baculovirus-insect cell system. Curr. Opin. Biotechnol. 9, 528–533.Google Scholar
Jones, I. & Morikawa, Y. (1996). Baculovirus vectors for expression in insect cells. Curr. Opin. Biotechnol. 7, 512–516.Google Scholar
Kane, J. F. (1995). Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6, 494–500.Google Scholar
Kaufman, R. J. (1990). Selection and coamplification of heterologous genes in mammalian cells. Methods Enzymol. 185, 537–566.Google Scholar
Kim, R., Sandler, S. J., Goldman, S., Yokota, H., Clark, A. J. & Kim, S.-H. (1998). Overexpression of archaeal proteins in Escherichia coli. Biotechnol. Lett. 20, 207–210.Google Scholar
Krueger, J. K., Kulke, M. H., Schutt, C. & Stock, J. (1989). Protein inclusion body formation and purification. BioPharm, March issue, 40–45.Google Scholar
Kwong, P. D., Wyatt, R., Robinson, J., Sweet, R. W., Sodroski, J. & Hendrickson, W. A. (1998). Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature (London), 393, 648–659.Google Scholar
LaVallie, E. R., DiBlasio, E. A., Kovacic, S., Grant, K. L., Schendel, P. F. & McCoy, J. M. (1993). A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology, 11, 187–193.Google Scholar
LaVallie, E. R. & McCoy, J. M. (1995). Gene fusion expression systems in Esherichia coli. Curr. Opin. Biotechnol. 6, 501–506.Google Scholar
Lee, H. W., Joo, J.-H., Kang, S., Song, L.-S., Kwon, J.-B., Han, M. H. & Na, D. S. (1992). Expression of human interleukin-2 from native and synthetic genes in E. coli: no correlation between major codon bias and high level expression. Biotechnol. Lett. 14, 653–658.Google Scholar
Lu, A. & Miller, L. K. (1996). Generation of recombinant baculoviruses by direct cloning. Biotechniques, 21, 63–68.Google Scholar
McCarroll, L. & King, L. A. (1997). Stable insect cell cultures for recombinant protein production. Curr. Opin. Biotechnol. 8, 590–594.Google Scholar
McPherson, M. J., Hames, B. D. & Taylor, G. R. (1995). PCR 2: a practical approach. Oxford, New York: IRL Press at Oxford University Press.Google Scholar
Makrides, S. C. (1996). Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 60, 512–538.Google Scholar
Marston, F. A. (1986). The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem. J. 240, 1–12.Google Scholar
Merrington, C. L., Bailey, M. J. & Possee, R. D. (1997). Manipulation of baculovirus vectors. Mol. Biotechnol. 8, 283–297.Google Scholar
Mitraki, A. & King, J. (1989). Protein folding intermediates and inclusion body formation. Biotechnology, 7, 690–697.Google Scholar
Mohsen, A.-W. A. & Vockley, J. (1995). High-level expression of an altered cDNA encoding human isovaleryl-CoA dehydrogenase in Escherichia coli. Gene, 160, 263–267.Google Scholar
Murby, M., Uhlén, M. & Ståhl, S. (1996). Upstream strategies to minimize proteolytic degradation upon recombinant production in Escherichia coli. Protein Expr. Purif. 7, 129–136.Google Scholar
Nilsson, B., Forsberg, G., Moks, T., Hartmanis, M. & Uhlén, M. (1992). Fusion proteins in biotechnology and structural biology. Curr. Opin. Struct. Biol. 2, 569–575.Google Scholar
O'Reilly, D. R., Miller, L. K. & Luckow, V. A. (1992). Baculovirus expression vectors: A laboratory manual. New York: W. H. Freeman & Co.Google Scholar
Pfeifer, T. A. (1998). Expression of heterologous proteins in stable insect culture. Curr. Opin. Biotechnol. 9, 518–521.Google Scholar
Possee, R. D. (1997). Baculoviruses as expression vectors. Curr. Opin. Biotechnol. 7, 569–572. Google Scholar
Richardson, C. D. (1995). Methods in molecular biology, Vol. 39. Baculovirus expression protocols. Totowa: Humana Press.Google Scholar
Richarme, G. & Caldas, T. D. (1997). Chaperone properties of the bacterial periplasmic substrate-binding proteins. J. Biol. Chem. 272, 15607–15612.Google Scholar
Ringquist, S., Shinedling, S., Barrick, D., Green, L., Binkley, J., Stormo, G. D. & Gold, L. (1992). Translational initiation in Escherichia coli: sequences within the ribosome-binding site. Mol. Microbiol. 6, 1219–1229.Google Scholar
Romanos, M. (1995). Advances in the use of Pichia pastoris for high-level gene expression. Curr. Opin. Biotechnol. 6, 527–533.Google Scholar
Romanos, M. A., Scorer, C. A. & Clare, J. J. (1992). Foreign gene expression in yeast: a review. Yeast, 8, 423–488.Google Scholar
Rossi, F. M. & Blau, H. M. (1998). Recent advances in inducible expression systems. Curr. Opin. Biotechnol. 9, 451–456.Google Scholar
Sachdev, D. & 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.Google Scholar
Saez, E., No, D., West, A. & Evans, R. M. (1997). Inducible expression in mammalian cells and transgenic mice. Curr. Opin. Biotechnol. 8, 608–616.Google Scholar
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular cloning: A laboratory manual, 2nd ed. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Samuelsson, E., Moks, T., Nilsson, B. & Uhlén, M. (1994). Enhanced in vitro refolding of insulin-like growth factor I using a solubilizing fusion partner. Biochemistry, 33, 4207–4211.Google Scholar
Schein, C. H. & Noteborn, M. H. M. (1988). Formation of soluble recombinant proteins in Escherichia coli is favored by lower growth temperature. Biotechnology, 6, 291–294.Google Scholar
Schenk, P. M., Baumann, S., Mattes, R. & Steinbiss, H.-H. (1995). Improved high-level expression system for eukaryotic genes in Escherichia coli using T7 RNA polymerase and rare ArgtRNAs. Biotechniques, 19, 196–198.Google Scholar
Sclimenti, C. R. & Calos, M. P. (1998). Epstein–Barr virus vectors for gene expression and transfer. Curr. Opin. Biotechnol. 9, 476–479.Google Scholar
Scopes, R. K. (1994). Protein purification: principles and practice. New York: Springer-Verlag.Google Scholar
Shimotohno, K. & Temin, H. M. (1982). Loss of intervening sequences in mouse α-globin DNA inserted in an infectious retrovirus vector. Nature (London), 299, 265–268.Google Scholar
Sorge, J. & Hughes, S. H. (1982). Splicing of intervening sequences introduced into an infectious retroviral vector. J. Mol. Appl. Genet. 1, 547–559.Google Scholar
Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113–130.Google Scholar
Studier, F. W., Rosenberg, A. H., Dunn, J. J. & Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185, 60–89.Google Scholar
Tabor, S. & Richardson, C. C. (1985). A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA, 82, 1074–1078.Google Scholar
Tobias, J. W., Shrader, T. E., Rocap, G. & Varshavsky, A. (1991). The N-end rule in bacteria. Science, 254, 1374–1377.Google Scholar
Tsunasawa, S., Stewart, J. W. & Sherman, F. S. (1985). Amino-terminal processing of mutant forms of yeast iso-1-cytochrome c. The specificities of methionine aminopeptidase and acetyltransferase. J. Biol. Chem. 260, 5382–5391.Google Scholar
Unger, T. F. (1997). Show me the money: prokaryotic expression vectors and purification systems. The Scientist, 11, 20–23.Google Scholar
Wall, J. G. & Plückthun, A. (1995). Effects of overexpressing folding modulators on the in vivo folding of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6, 507–516.Google Scholar
Waller, J.-P. (1963). The NH2-terminal residues of the proteins from cell-free extracts of E. coli. J. Mol. Biol. 7, 483–496.Google Scholar
Werner, M. H., Clore, G. M., Gronenborn, A. M., Kondoh, A. & Fisher, R. J. (1994). Refolding proteins by gel filtration chromatography. FEBS Lett. 345, 125–130.Google Scholar
Wilkinson, D. L., Ma, N. T., Haught, C. & Harrison, R. G. A. (1995). Purification by immobilized metal affinity chromatography of human atrial natriuretic peptide expressed in a novel thioredoxin fusion protein. Biotechnol. Prog. 11, 265–269.Google Scholar
Yasukawa, T., Kanei-Ishii, C., Maekawa, T., Fujimoto, J., Yamamoto, T. & Ishii, S. (1995). Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin. J. Biol. Chem. 270, 25328–25331.Google Scholar
Yonemoto, W. M., McGlone, M. L., Slice, L. W. & Taylor, S. S. (1998). Prokaryotic expression of catalytic subunit of adenosine cyclic monophosphate-dependent protein kinase. In Protein phosphorylation, edited by B. M. Sefton & T. Hunter, pp. 419–434. San Diego: Academic Press. Google Scholar
Zhang, S. P., Zubay, G. & Goldman, E. (1991). Low usage codons in Escherichia coli, yeast, fruit fly and primates. Gene, 105, 61–72.Google Scholar