From gene to protein: A review of new and enabling technologies for multi-parallel protein expression

Protein Expression and Purification

Volumn 40, Issue 1, 2005, Pages 1-22

  Hunt, Ian ^a,b  

^a NOVARTIS HORSHAM RESEARCH CENTRE   (United Kingdom)

^b Millennium Pharmaceut 75 Sidney S   (United States)

Author keywords

Baculovirus; Deep well block protein expression; High throughput

Indexed keywords

UNIDENTIFIED BACULOVIRUS;

EID: 13844271129     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2004.10.018     Document Type: Review

References (106)

1. A.J.M. Walhout, G.F. Temple, M.A. Brasch, J.L. Hartley, M.A. Lorson, J. Thorner, and M. Vidal Gateway recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes Methods Enzymol. 328 2000 575 592
2. J.L. Hartley, G.F. Temple, and M.A. Brasch DNA cloning using in vitro site-specific recombination Genome Res. 10 2000 1788 1795
3. A. Landy Dynamic, structural, and regulatory aspects of lambda site-specific recombination Annu. Rev. Biochem. 58 1989 913 949
4. Q. Liu, M.Z. Li, D. Leibham, D. Cortez, and S.J. Elledge The univector plasmid-fusion system, a method for rapid construction of recombinant DNA without restriction enzymes Curr. Biol. 8 1998 1300 1309
5. L. Stols, M. Gu, L. Dieckman, R. Raffen, F.R. Collart, and M.I. Donnelly A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site Protein Expr. Purif. 25 2002 8 15
6. L. Dieckman, M. Gu, L. Stols, M.I. Donnelly, and F.R. Collart High throughput methods for gene cloning and expression Protein Expr. Purif. 25 2002 1 7
7. S.P. Chambers, D.A. Austen, J.R. Fulghum, and W.M. Kim High-throughput screening for soluble recombinant expressed kinases in Escherichia coli and insect cells Protein Expr. Purif. 36 2004 40 47
8. R.C. Stevens Design of high-throughput methods of protein production for structural biology Struct. Fold Des. 8 2000 R177 R185
9. K. Terpe Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems Appl. Microbiol. Biotechnol. 60 2003 523 533
10. D.B. Smith, and J. Thorner Generating fusions to glutathione S-transferase for protein studies Gene 326 2000 254 270
11. D.B. Smith, and K.S. Johnson Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase Gene 67 1988 31 40
12. E. Hochuli Purification of recombinant proteins with metal chelate adsorbent Genet. Eng. 12 1990 87 98
13. E. Hochuli Large-scale chromatography of recombinant proteins J. Chromatogr. 444 1988 293 302
14. E. Hochuli, H. Dobeli, and A. Schacher New metal chelate adsorbent selective for proteins and peptides containing neighbouring histidine residues J. Chromatogr. 411 1987 177 184
15. A.K. Mohanty, and M.C. Wiener Membrane protein expression and production: effects of polyhistidine tag length and position Protein Express. Purif. 33 2004 311 325
16. M.E. Kimple, and J. Sondek Affinity purifcation, Section 9.9.1-9.9.19 Current Protocols in Protein Science 2004 Wiley USA
17. G. Chaga, D.E. Bochkariov, G.G. Jokhadze, J. Hopp, and P. Nelson Natural poly-histidine affinity tag for purification of recombinant proteins on cobalt(II)-carboxymethylaspartate crosslinked agarose J. Chromatogr. A 864 1999 247 256
18. P. Braun, and J. LaBaer High throughput protein production for functional proteomics Trends Biotechnol. 21 2003 383 388
19. J.D. Fox, R.B. Kapust, and D.S. Waugh 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 2001 622 630
20. R.B. Kapust, and D.S. Waugh Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused Protein Sci. 8 1999 1668 1674
21. M. Hammarstrom, N. Hellgren, B.S. Van den, H. Berglund, and T. Hard Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli Protein Sci. 11 2002 313 321
22. Y.P. Shih, W.M. Kung, J.C. Chen, C.H. Yeh, A.H.J. Wang, and T.F. Wang High-throughput screening of soluble recombinant proteins Protein Sci. 11 2002 1714 1719
23. P. Braun, Y.H. Hu, B.H. Shen, A. Halleck, M. Koundinya, E. Harlow, and J. LaBaer Proteome-scale purification of human proteins from bacteria Proc. Natl. Acad. Sci. USA 99 2002 2654 2659
24. R.T. Baker Protein expression using ubiquitin fusion and cleavage Curr. Opin. Biotechnol. 7 1996 541 546
25. R.T. Baker, and P.G. Board The human ubiquitin-52 amino acid fusion protein gene shares several structural features with mammalian ribosomal protein genes Nucleic Acids Res. 19 1991 1035 1040
26. J.L. Wittliff, L.L. Wenz, J. Dong, Z. Nawaz, and T.R. Butt Expression and characterization of an active human estrogen receptor as a ubiquitin fusion protein from Escherichia coli J. Biol. Chem. 265 1990 22016 22022
27. T.R. Butt, S. Jonnalagadda, B.P. Monia, E.J. Sternberg, J.A. Marsh, J.M. Stadel, D.J. Ecker, and S.T. Crooke Ubiquitin fusion augments the yield of cloned gene products in Escherichia coli Proc. Natl. Acad. Sci. USA 86 1989 2540 2544
28. A. Varshavsky Ubiquitin fusion technique and its descendants Methods Enzymol. 327 2000 578 593
29. A.M. Catanzariti, T.A. Soboleva, D.A. Jans, P.G. Board, and R.T. Baker An efficient system for high-level expression and easy purification of authentic recombinant proteins Protein Sci. 13 2004 1331 1339
30. M.P. Malakhov, M.R. Mattern, O.A. Malakhova, M. Drinker, S.D. Weeks, and T.R. Butt SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins J. Struct. Funct. Genomics 5 2004 75 86
31. G.S. Waldo Improving protein folding efficiency by directed evolution using the GFP folding reporter Methods Mol. Biol. 230 2003 343 359
32. R.T. Raines, M. McCormick, T.R. Van Oosbree, and R.C. Mierendorf The S.Tag fusion system for protein purification Methods Enzymol. 326 2000 362 376
33. S. Chong, and M.Q. Xu Protein splicing of the Saccharomyces cerevisiae VMA intein without the endonuclease motifs J. Biol. Chem. 272 1997 15587 15590
34. S. Chong, F.B. Mersha, D.G. Comb, M.E. Scott, D. Landry, L.M. Vence, F.B. Perler, J. Benner, R.B. Kucera, C.A. Hirvonen, J.J. Pelletier, H. Paulus, and M.Q. Xu Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element Gene 192 1997 271 281
35. S. Chong, Y. Shao, H. Paulus, J. Benner, F.B. Perler, and M.Q. Xu 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 1996 22159 22168
36. F. Baneyx Recombinant protein expression in Escherichia coli Curr. Opin. Biotechnol. 10 1999 411 421
37. G. Hannig, and S.C. Makrides Strategies for optimizing heterologous protein expression in Escherichia coli Trends Biotechnol. 16 1998 54 60
38. S.C. Makrides Strategies for achieving high-level expression of genes in Escherichia coli Microbiol. Rev. 60 1996 512 538
39. W.A. Prinz, F. Aslund, A. Holmgren, and J. Beckwith The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm J. Biol. Chem. 272 1997 15661 15667
40. P.H. Bessette, F. Aslund, J. Beckwith, and G. Georgiou Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm Proc. Natl. Acad. Sci. USA 96 1999 13703 13708
41. E. Mossner, M. Huber-Wunderlich, A. Rietsch, J. Beckwith, R. Glockshuber, and F. Aslund Importance of redox potential for the in vivo function of the cytoplasmic disulfide reductant thioredoxin from Escherichia coli J. Biol. Chem. 274 1999 25254 25259
42. E.J. Stewart, F. Aslund, and J. Beckwith Disulfide bond formation in the Escherichia coli cytoplasm: an in vivo role reversal for the thioredoxins EMBO J. 17 1998 5543 5550
43. C. Gustafsson, S. Govindarajan, and J. Minshull Codon bias and heterologous protein expression Trends Biotechnol. 22 2004 346 353
44. G.S. Waldo Genetic screens and directed evolution for protein solubility Curr. Opin. Chem. Biol. 7 2003 33 38
45. S.A. Lesley, J. Graziano, C.Y. Cho, M.W. Knuth, and H.E. Klock Gene expression response to misfolded protein as a screen for soluble recombinant protein Protein Eng. 15 2002 153 160
46. W.C. Wigley, R.D. Stidham, N.M. Smith, J.F. Hunt, and P.J. Thomas Protein solubility and folding monitored in vivo by structural complementation of a genetic marker protein Nat. Biotechnol. 19 2001 131 136
47. R.K. Knaust, and P. Nordlund Screening for soluble expression of recombinant proteins in a 96-well format Anal. Biochem. 297 2001 79 85
48. D. Busso, R. Kim, and S.H. Kim Expression of soluble recombinant proteins in a cell-free system using a 96-well format J. Biochem. Biophys. Methods 55 2003 233 240
49. M.R. Chance, A.R. Bresnick, S.K. Burley, J.S. Jiang, C.D. Lima, A. Sali, S.C. Almo, J.B. Bonanno, J.A. Buglino, S. Boulton, H. Chen, N. Eswar, G. He, R. Huang, V. Ilyin, L. McMahan, U. Pieper, S. Ray, M. Vidal, and L.K. Wang Structural genomics: a pipeline for providing structures for the biologist Protein Sci. 11 2002 723 738
50. S.A. Lesley High-throughput proteomics: protein expression and purification in the postgenomic world Protein Expr. Purif. 22 2001 159 164
51. C.S. Millard, L. Stols, P. Quartey, Y. Kim, I. Dementieva, and M.I. Donnelly A less laborious approach to the high-throughput production of recombinant proteins in Escherichia coli using 2-liter plastic bottles Protein Expr. Purif. 29 2003 311 320
52. P. Rucker, F.M. Torti, and S.V. Torti Recombinant ferritin: modulation of subunit stoichiometry in bacterial expression systems Protein Eng. 10 1997 967 973
53. K. Johnston, A. Clements, R.N. Venkataramani, R.C. Trievel, and R. Marmorstein Coexpression of proteins in bacteria using T7-based expression plasmids: expression of heteromeric cell-cycle and transcriptional regulatory complexes Protein Expr. Purif. 20 2000 435 443
54. K.J. Kim, H.E. Kim, K.H. Lee, W. Han, M.J. Yi, J. Jeong, and B.H. Oh Two-promoter vector is highly efficient for overproduction of protein complexes Protein Sci. 13 2004 1698 1703
55. P.A. Kitts, and R.D. Possee A method for producing recombinant baculovirus expression vectors at high frequency Biotechniques 14 1993 810 817
56. V.A. Luckow, S.C. Lee, G.F. Barry, and P.O. Olins Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli J. Virol. 67 1993 4566 4579
57. G.P. Pijlman, J.E. van Schijndel, and J.M. Vlak Spontaneous excision of BAC vector sequences from bacmid-derived baculovirus expression vectors upon passage in insect cells J. Gen. Virol. 84 2003 2669 2678
58. W.F. Hink, D.R. Thomsen, D.J. Davidson, A.L. Meyer, and F.J. Castellano Expression of three recombinant proteins using baculovirus vectors in 23 insect cell lines Biotechnol. Prog. 7 2004 9 14
59. D.R. O'Reilly, L.K. Miller, and V.A. Luckow Baculovirus Expression Vectors: A Laboratory Manual 2004 WH Freeman NY
60. J.L. Vaughn, R.H. Goodwin, G.J. Tompkins, and P. McCawley The establishment of two cell lines from the insect Spodoptera frugiperda In Vitro 13 1977 213 217
61. R.A. Taticek, C. Choi, S.E. Phan, L.A. Palomares, and M.L. Shuler Comparison of growth and recombinant protein expression in two different insect cell lines in attached and suspension culture Biotechnol. Prog. 17 2001 676 684
62. D.L. Jarvis Developing baculovirus-insect cell expression systems for humanized recombinant glycoprotein production Virology 310 2003 1 7
63. J. Hollister, E. Grabenhorst, M. Nimtz, H. Conradt, and D.L. Jarvis Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans Biochemistry 41 2002 15093 15104
64. M.A. Sommerfelt, and E.J. Sorscher Use of fluorescence-activated cell sorting for rapid isolation of insect cells harboring recombinant baculovirus Methods Cell Biol. 42 Pt. B 1994 563 574
65. B. Philipps, M. Forstner, and L.M. Mayr Baculovirus expression system for magnetic sorting of infected cells and enhanced titer determination Biotechniques 36 2004 80 83
66. P. Farrell, and K. Iatrou Transfected insect cells in suspension culture rapidly yield moderate quantities of recombinant proteins in protein-free culture medium Protein Expr. Purif. 36 2004 177 185
67. S.P. Chambers High-throughput protein expression for the post-genomic era Drug Discov. Today 7 2002 759 765
68. D. Bahia, R. Cheung, M. Buchs, S. Geisse, I. Hunt, Optimisation of insect cell growth in deep-well blocks: development of a high-throughput insect cell expression system, Protein Expr. Purif. (2004), in press
69. V. Singh Disposable bioreactor for cell culture using wave-induced agitation Cytotechnology 30 1999 149 158
70. W. Weber, E. Weber, S. Geisse, and K. Memmert Optimisation of protein expression and establishment of the Wave Bioreactor for Baculovirus/insect cell culture Cytotechnology 38 2002 77 85
71. W.F. Hink, and P.V. Vail A plaque assay for titration of alfalfa looper nuclear polyhydrosis virus in a cabbage looper TN-368 cell line J. Invertebr. Pathol. 22 1973 168 174
72. L.E. Volkman, and P.A. Goldsmith Baculovirus bioassay not dependent upon polyhedra production J. Gen. Virol. 56 1981 203 206
73. M.S. Kwon, T. Dojima, M. Toriyama, and E.Y. Park Development of an antibody-based assay for determination of baculovirus titers in 10 hours Biotechnol. Prog. 18 2002 647 651
74. D.J. Sussman 24-hour assay for estimating the titer of beta-galactosidase-expressing baculovirus Biotechniques 18 1995 50 51
75. T. Yahata, S. Andriole, K.J. Isselbacher, and T. Shioda Estimation of baculovirus titer by beta-galactosidase activity assay of virus preparations Biotechniques 29 2000 214 215
76. S. Eriksson, E. Raivio, J.P. Kukkonen, K. Eriksson, and C. Lindqvist Green fluorescent protein as a tool for screening recombinant baculoviruses J. Virol. Methods 59 1996 127 133
77. H.J. Cha, T. Gotoh, and W.E. Bentley Simplification of titer determination for recombinant baculovirus by green fluorescent protein marker Biotechniques 23 1997 782 786
78. V. Malde, and I. Hunt Calculation of baculovirus titer using a microfluidic-based bioanalyzer Biotechniques 36 2004 942 946
79. M.J. Espy, F.R. Cockerill III, R.F. Meyer, M.D. Bowen, G.A. Poland, T.L. Hadfield, and T.F. Smith Detection of smallpox virus DNA by LightCycler PCR J. Clin. Microbiol. 40 2002 1985 1988
80. M.J. Espy, P.N. Rys, A.D. Wold, J.R. Uhl, L.M. Sloan, G.D. Jenkins, D.M. Ilstrup, F.R. Cockerill III, R. Patel, J.E. Rosenblatt, and T.F. Smith Detection of herpes simplex virus DNA in genital and dermal specimens by LightCycler PCR after extraction using the IsoQuick, MagNA Pure, and BioRobot 9604 methods J. Clin. Microbiol. 39 2001 2233 2236
81. C.J. Gerard, M.J. Arboleda, G. Solar, J.J. Mule, and W.G. Kerr A rapid and quantitative assay to estimate gene transfer into retrovirally transduced hematopoietic stem/progenitor cells using a 96-well format PCR and fluorescent detection system universal for MMLV-based proviruses Hum. Gene Ther. 7 1996 343 354
82. H.R. Lo, and Y.C. Chao Rapid titer determination of baculovirus by quantitative real-time polymerase chain reaction Biotechnol. Prog. 20 2004 354 360
83. J. Benting, S. Lecat, D. Zacchetti, and K. Simons Protein expression in Drosophila Schneider cells Anal. Biochem. 278 2000 59 68
84. D.F. Lee, C.C. Chen, T.A. Hsu, and J.L. Juang A baculovirus superinfection system: efficient vehicle for gene transfer into Drosophila S2 cells J. Virol. 74 2000 11873 11880
85. R.V. Merrihew, T.A. Kost, and J.P. Condreay Baculovirus-mediated gene delivery into mammalian cells Methods Mol. Biol. 246 2004 355 365
86. C. Holz, O. Hesse, N. Bolotina, U. Stahl, and C. Lang A micro-scale process for high-throughput expression of cDNAs in the yeast Saccharomyces cerevisiae Protein Expr. Purif. 25 2002 372 378
87. M. Boettner, B. Prinz, C. Holz, U. Stahl, and C. Lang High-throughput screening for expression of heterologous proteins in the yeast Pichia pastoris J. Biotechnol. 99 2002 51 62
88. G. Van Heeke, T.L. Ott, A. Strauss, D. Ammaturo, and F.W. Bazer High yield expression and secretion of the ovine pregnancy recognition hormone interferon-tau by Pichia pastoris J. Interferon Cytokine Res. 16 1996 119 126
89. A.J. Austin, C.E. Jones, and G.V. Heeke Production of human tissue factor using the Pichia pastoris expression system Protein Expr. Purif. 13 1998 136 142
90. F. Wurm, and A. Bernard Large-scale transient expression in mammalian cells for recombinant protein production Curr. Opin. Biotechnol. 10 1999 156 159
91. P.L. Pham, S. Perret, H.C. Doan, B. Cass, G. St Laurent, A. Kamen, and Y. Durocher Large-scale transient transfection of serum-free suspension-growing HEK293 EBNA1 cells: peptone additives improve cell growth and transfection efficiency Biotechnol. Bioeng. 84 2003 332 342
92. Y. Durocher, S. Perret, and A. Kamen High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells Nucleic Acids Res. 30 2002 E9
93. S. Geisse, and H.P. Kocher Protein expression in mammalian and insect cell systems Methods Enzymol. 306 1999 19 41
94. K. Lundstrom Semliki Forest virus vectors for rapid and high-level expression of integral membrane proteins Biochim. Biophys. Acta 1610 2003 90 96
95. K. Lundstrom Semliki Forest virus vectors for large-scale production of recombinant proteins Methods Mol. Med. 76 2003 525 543
96. K. Lundstrom Semliki forest virus-based expression for versatile use in receptor research J. Recept. Signal Transduct. Res. 22 2002 229 240
97. K. Madin, T. Sawasaki, N. Kamura, K. Takai, T. Ogasawara, K. Yazaki, T. Takei, K. Miura, and Y. Endo Formation of circular polyribosomes in wheat germ cell-free protein synthesis system FEBS Lett. 562 2004 155 159
98. T. Kawasaki, M.D. Gouda, T. Sawasaki, K. Takai, and Y. Endo Efficient synthesis of a disulfide-containing protein through a batch cell-free system from wheat germ Eur. J. Biochem. 270 2003 4780 4786
99. T. Sawasaki, M. Seki, K. Sinozaki, and Y. Endo High-throughput expression of proteins from cDNAs catalogue from Arabidopsis in wheat germ cell-free protein synthesis system Tanpakushitsu Kakusan Koso 47 2002 1003 1008
100. M. Hino, Y. Shinohara, K. Kajimoto, H. Terada, and Y. Baba Requirement of continuous transcription for the synthesis of sufficient amounts of protein by a cell-free rapid translation system Protein Expr. Purif. 24 2002 255 259
101. T. Kigawa, and S. Yokoyama High-throughput cell-free protein expression system for structural genomics and proteomics studies Tanpakushitsu Kakusan Koso 47 2002 1014 1019
102. Y. Endo, and T. Sawasaki High-throughput, genome-scale protein production method based on the wheat germ cell-free expression system Biotechnol. Adv. 21 2003 695 713
103. R.C. Stevens, S. Yokoyama, and I.A. Wilson Global efforts in structural genomics Science 294 2001 89 92
104. S. Yokoyama, H. Hirota, T. Kigawa, T. Yabuki, M. Shirouzu, T. Terada, Y. Ito, Y. Matsuo, Y. Kuroda, Y. Nishimura, Y. Kyogoku, K. Miki, R. Masui, and S. Kuramitsu Structural genomics projects in Japan Nat. Struct. Biol. 7 Suppl. 2000 943 945
105. T. Lanio, A. Jeltsch, and A. Pingoud High-throughput purification of polyHis-tagged recombinant fusion proteins Methods Mol. Biol. 205 2003 199 203
106. J. Drees, J. Smith, F. Schafer, and K. Steinert High-throughput expression and purification of 6×His-tagged proteins in a 96-well format Methods Mol. Med. 94 2004 179 190