Library methods for structural biology of challenging proteins and their complexes

Current Opinion in Structural Biology

Volumn 23, Issue 3, 2013, Pages 403-408

  Hart, Darren J ^a   Waldo, Geoffrey S ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ARYLDIALKYLPHOSPHATASE; ARYLDIALKYLPHOSPHATASE 1; ARYLDIALKYLPHOSPHATASE 3; DNA DIRECTED DNA POLYMERASE BETA; ENOYL REDUCTASE; G PROTEIN COUPLED RECEPTOR; GLUCOCORTICOID RECEPTOR; GREEN FLUORESCENT PROTEIN; HYDROLYASE; NUCLEOPORIN; OXIDOREDUCTASE; RNA DIRECTED DNA POLYMERASE; TRANSPOSASE; UNCLASSIFIED DRUG;

BIOINFORMATICS; CRYSTALLIZATION; DIFFRACTION; ESCHERICHIA COLI; GENE EXPRESSION; GENE LIBRARY; GENE MUTATION; GENETIC ENGINEERING; GENETIC SCREENING; GENETIC SELECTION; GENETIC VARIABILITY; HUMAN; HUMAN CYTOMEGALOVIRUS; INFLUENZA VIRUS; LIGAND BINDING; MOLECULAR CLONING; MUTATIONAL ANALYSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; QUALITY CONTROL; REVIEW; SITE DIRECTED MUTAGENESIS;

DIRECTED MOLECULAR EVOLUTION; MULTIPROTEIN COMPLEXES; PEPTIDE LIBRARY; PROTEIN CONFORMATION; PROTEIN ENGINEERING; SOLUBILITY;

EID: 84879169708     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.03.004     Document Type: Review

References (66)

1. Goldsmith M., Tawfik D.S. Directed enzyme evolution: beyond the low-hanging fruit. Curr Opin Struct Biol 2012, 22:406-412.
2. Lonberg N. Fully human antibodies from transgenic mouse and phage display platforms. Curr Opin Immunol 2008, 20:450-459.
3. Pabo C.O., Peisach E., Grant R.A. Design and selection of novel Cys2His2 zinc finger proteins. Annu Rev Biochem 2001, 70:313-340.
4. Perez-Pinera P., Ousterout D.G., Gersbach C.A. Advances in targeted genome editing. Curr Opin Chem Biol 2012, 16:268-277.
5. Dalby P.A. Strategy and success for the directed evolution of enzymes. Curr Opin Struct Biol 2011, 21:473-480.
6. Ness J.E., Kim S., Gottman A., Pak R., Krebber A., Borchert T.V., Govindarajan S., Mundorff E.C., Minshull J. Synthetic shuffling expands functional protein diversity by allowing amino acids to recombine independently. Nat Biotechnol 2002, 20:1251-1255.
7. Keenan R.J. DNA shuffling as a tool for protein crystallization. Proc Natl Acad Sci U S A 2005, 102:8887-8892.
8. Yumerefendi H., Tarendeau F., Mas P.J., Hart D.J. ESPRIT: an automated, library-based method for mapping and soluble expression of protein domains from challenging targets. J Struct Biol 2010, 172:66-74.
9. Cornvik T., Dahlroth S.-L., Magnusdottir A., Flodin S., Engvall B., Lieu V., Ekberg M., Nordlund P. An efficient and generic strategy for producing soluble human proteins and domains in E. coli by screening construct libraries. Proteins 2006, 65:266-273.
10. Dahlroth S.-L., Lieu V., Haas J., Nordlund P. Screening colonies of pooled ORFeomes (SCOOP): a rapid and efficient strategy for expression screening ORFeomes in Escherichia coli. Protein Exp Purif 2009, 68:121-127.
11. Guilligay D., Tarendeau F., Resa-Infante P., Coloma R., Crepin T., Sehr P., Lewis J., Ruigrok R.W.H., Ortin J., Hart D.J., et al. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 2008, 15:500-506.
12. Dyson M.R., Perera R.L., Shadbolt S.P., Biderman L., Bromek K., Murzina N.V., McCafferty J. Identification of soluble protein fragments by gene fragmentation and genetic selection. Nucleic Acids Res 2008, 36:e51.
13. Reich S., Puckey L.H., Cheetham C.L., Harris R., Ali A.A.E., Bhattacharyya U., Maclagan K., Powell K.A., Prodromou C., Pearl L.H., et al. Combinatorial domain hunting: an effective approach for the identification of soluble protein domains adaptable to high-throughput applications. Protein Sci 2006, 15:2356-2365.
14. Thorstenson Y.R., Hunicke-Smith S.P., Oefner P.J., Davis R.W. An automated hydrodynamic process for controlled, unbiased DNA shearing. Genome Res 1998, 8:848-855.
15. Kawasaki M., Inagaki F. Random PCR-based screening for soluble domains using green fluorescent protein. Biochem Biophys Res Commun 2001, 280:842-844.
16. An Y., Yumerefendi H., Mas P.J., Chesneau A., Hart D.J. ORF-selector ESPRIT: a second generation library screen for soluble protein expression employing precise open reading frame selection. J Struct Biol 2011, 175:189-197.
17. Gerth M.L., Patrick W.M., Lutz S. A second-generation system for unbiased reading frame selection. Protein Eng Des Sel 2004, 17:595-602.
18. Pedelacq J.-D., Nguyen H.B., Cabantous S., Mark B.L., Listwan P., Bell C., Friedland N., Lockard M., Faille A., Mourey L., et al. Experimental mapping of soluble protein domains using a hierarchical approach. Nucleic Acids Res 2011, 39:e125.
19. Muteeb G., Sen R. Random mutagenesis using a mutator strain. Methods Mol Biol 2010, 634:411-419.
20. Cadwell R.C., Joyce G.F. Mutagenic PCR. Genome Res 1994, 3:S136-S140.
21. Aguinaldo A.M., Arnold F. Staggered extension process (StEP) in vitro recombination. Methods Mol Biol 2002, 192:235-239.
22. Zhao H., Zha W. In vitro 'sexual' evolution through the PCR-based staggered extension process (StEP). Nat Protoc 2006, 1:1865-1871.
23. Stemmer W.P. Rapid evolution of a protein in vitro by DNA shuffling. Nature 1994, 370:389-391.
24. Crameri A., Raillard S.A., Bermudez E., Stemmer W.P. DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 1998, 391:288-291.
25. Van den Brulle J., Fischer M., Langmann T., Horn G., Waldmann T., Arnold S., Fuhrmann M., Schatz O., O'Connell T., O'Connell D., et al. A novel solid phase technology for high-throughput gene synthesis. Biotechniques 2008, 45:340-343.
26. Heddle C., Mazaleyrat S.L. Development of a screening platform for directed evolution using the reef coral fluorescent protein ZsGreen as a solubility reporter. Protein Eng Des Sel 2007, 20:327-337.
27. Cabantous S., Rogers Y., Terwilliger T.C., Waldo G.S. New molecular reporters for rapid protein folding assays. PLoS ONE 2008, 3:e2387.
28. Maxwell K.L., Mittermaier A.K., Forman-Kay J.D., Davidson A.R. A simple in vivo assay for increased protein solubility. Protein Sci 1999, 8:1908-1911.
29. Liu J.-W., Boucher Y., Stokes H.W., Ollis D.L. Improving protein solubility: the use of the Escherichia coli dihydrofolate reductase gene as a fusion reporter. Protein Exp Purif 2006, 47:258-263.
30. Cabantous S., Terwilliger T.C., Waldo G.S. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat Biotechnol 2005, 23:102-107.
31. Yumerefendi H., Desravines D.C., Hart D.J. Library-based methods for identification of soluble expression constructs. Methods 2011, 55:38-43.
32. Listwan P., Pédelacq J.-D., Lockard M., Bell C., Terwilliger T.C., Waldo G.S. The optimization of in vitro high-throughput chemical lysis of Escherichia coli. Application to ACP domain of the polyketide synthase ppsC from Mycobacterium tuberculosis. J Struct Funct Genomics 2010, 11:41-49.
33. Cornvik T., Dahlroth S.-L., Magnusdottir A., Herman M.D., Knaust R., Ekberg M., Nordlund P. Colony filtration blot: a new screening method for soluble protein expression in Escherichia coli. Nat Methods 2005, 2:507-509.
34. Christ D., Winter G. Identification of protein domains by shotgun proteolysis. J Mol Biol 2006, 358:364-371.
35. Sieber V., Plückthun A., Schmid F.X. Selecting proteins with improved stability by a phage-based method. Nat Biotechnol 1998, 16:955-960.
36. Speck J., Arndt K.M., Muller K.M. Efficient phage display of intracellularly folded proteins mediated by the TAT pathway. Protein Eng Des Sel 2011, 24:473-484.
37. Maclagan K., Tommasi R., Laurine E., Prodromou C., Driscoll P.C., Pearl L.H., Reich S., Savva R. A combinatorial method to enable detailed investigation of protein-protein interactions. Future Med Chem 2011, 3:271-282.
38. An Y., Meresse P., Mas P.J., Hart D.J. CoESPRIT: a library-based construct screening method for identification and expression of soluble protein complexes. PLoS ONE 2011, 6:e16261.
39. Lockard M.A., Listwan P., Pedelacq J.-D., Cabantous S., Nguyen H.B., Terwilliger T.C., Waldo G.S. A high-throughput immobilized bead screen for stable proteins and multi-protein complexes. Protein Eng Des Sel 2011, 24:565-578.
40. Eshaghi S. An efficient strategy for high-throughput expression screening of recombinant integral membrane proteins. Protein Sci 2005, 14:676-683.
41. Molina D.M., Cornvik T., Eshaghi S., Haeggström J.Z., Nordlund P., Sabet M.I. Engineering membrane protein overproduction in Escherichia coli. Protein Sci 2008, 17:673-680.
42. Drew D., Lerch M., Kunji E., Slotboom D.-J., De Gier J.-W. Optimization of membrane protein overexpression and purification using GFP fusions. Nat Methods 2006, 3:303-313.
43. Hammon J., Palanivelu D.V., Chen J., Patel C., Minor D.L. A green fluorescent protein screen for identification of well-expressed membrane proteins from a cohort of extremophilic organisms. Protein Sci 2009, 18:121-133.
44. Sarkar C.A., Dodevski I., Kenig M., Dudli S., Mohr A., Hermans E., Pluckthun A. Directed evolution of a G protein-coupled receptor for expression, stability, and binding selectivity. Proc Natl Acad Sci U S A 2008, 105:14808-14813.
45. Schlinkmann K.M., Hillenbrand M., Rittner A., Künz M., Strohner R., Plückthun A. Maximizing detergent stability and functional expression of a GPCR by exhaustive recombination and evolution. J Mol Biol 2012, 422:414-428.
46. Tarendeau F., Crepin T., Guilligay D., Ruigrok R.W.H., Cusack S., Hart D.J. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog 2008, 4:e1000136.
47. Tarendeau F., Boudet J., Guilligay D., Mas P.J., Bougault C.M., Boulo S., Baudin F., Ruigrok R.W.H., Daigle N., Ellenberg J., et al. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 2007, 14:229-233.
48. Nadal M., Mas P.J., Blanco A.G., Arnan C., Solà M., Hart D.J., Coll M. Structure and inhibition of herpesvirus DNA packaging terminase nuclease domain. Proc Natl Acad Sci U S A 2010, 107:16078-16083.
49. Rawlings A.E., Levdikov V.M., Blagova E., Colledge V.L., Mas P.J., Tunaley J., Vavrova L., Wilson K.S., Barak I., Hart D.J., et al. Expression of soluble, active fragments of the morphogenetic protein SpoIIE from Bacillus subtilis using a library-based construct screen. Protein Eng Des Sel 2010, 23:817-825.
50. Levdikov V.M., Blagova E.V., Rawlings A.E., Jameson K., Tunaley J., Hart D.J., Barak I., Wilkinson A.J. Structure of the phosphatase domain of the cell fate determinant SpoIIE from Bacillus subtilis. J Mol Biol 2012, 415:343-358.
51. Meier C., Brookings D.C., Ceska T.A., Doyle C., Gong H., McMillan D., Saville G.P., Mushtaq A., Knight D., Reich S., et al. Engineering human MEK-1 for structural studies: a case study of combinatorial domain hunting. J Struct Biol 2012, 177:329-334.
52. Jacobs S.A., Podell E.R., Wuttke D.S., Cech T.R. Soluble domains of telomerase reverse transciptase identified by high-throughput screening. Protein Sci 2005, 14:2051-2058.
53. Hodel A.E., Hodel M.R., Griffis E.R., Hennig K.A., Ratner G.A., Xu S., Powers M.A. The three-dimensional structure of the autoproteolytic, nuclear pore-targeting domain of the human nucleoporin Nup98. Mol Cell 2002, 10:347-358.
54. Sabogal A., Rio D.C. A green fluorescent protein solubility screen in E. coli reveals domain boundaries of the GTP-binding domain in the P element transposase. Protein Sci 2010, 19:2210-2218.
55. Seitz T., Thoma R., Schoch G.A., Stihle M., Benz J., D'Arcy B., Wiget A., Ruf A., Hennig M., Sterner R. Enhancing the stability and solubility of the glucocorticoid receptor ligand-binding domain by high-throughput library screening. J Mol Biol 2010, 403:562-577.
56. Aharoni A., Gaidukov L., Yagur S., Toker L., Silman I., Tawfik D.S. Directed evolution of mammalian paraoxonases PON1 and PON3 for bacterial expression and catalytic specialization. Proc Natl Acad Sci U S A 2004, 101:482-487.
57. Harel M., Aharoni A., Gaidukov L., Brumshtein B., Khersonsky O., Meged R., Dvir H., Ravelli R.B.G., McCarthy A., Toker L., et al. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat Struct Mol Biol 2004, 11:412-419.
58. Van Engelenburg S.B., Palmer A.E. Imaging type-III secretion reveals dynamics and spatial segregation of Salmonella effectors. Nat Methods 2010, 7:325-330.
59. Feinberg E.H., VanHoven M.K., Bendesky A., Wang G., Fetter R.D., Shen K., Bargmann C.I. GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57:353-363.
60. Ishikawa H., Meng F., Kondo N., Iwamoto A., Matsuda Z. Generation of a dual-functional split-reporter protein for monitoring membrane fusion using self-associating split GFP. Protein Eng Des Sel 2012, 25:813-820.
61. D'Angelo S., Velappan N., Mignone F., Santoro C., Sblattero D., Kiss C., Bradbury A.R. Filtering 'genic' open reading frames from genomic DNA samples for advanced annotation. BMC Genomics 2011, 12:S5.
62. Richter F., Leaver-Fay A., Khare S.D., Bjelic S., Baker D. De novo enzyme design using rosetta3. PLoS ONE 2011, 6:e19230.
63. Borovkov A.Y., Loskutov A.V., Robida M.D., Day K.M., Cano J.A., Le Olson T., Patel H., Brown K., Hunter P.D., Sykes K.F. High-quality gene assembly directly from unpurified mixtures of microarray-synthesized oligonucleotides. Nucleic Acids Res 2010, 38:e180.
64. Kong D.S., Carr P.A., Chen L., Zhang S., Jacobson J.M. Parallel gene synthesis in a microfluidic device. Nucleic Acids Res 2007, 35:e61.
65. Fallah-Araghi A., Baret J.-C., Ryckelynck M., Griffiths A.D. A completely in vitro ultrahigh-throughput droplet-based microfluidic screening system for protein engineering and directed evolution. Lab Chip 2012, 12:882.
66. Agresti J.J., Antipov E., Abate A.R., Ahn K., Rowat A.C., Baret J.-C., Marquez M., Klibanov A.M., Griffiths A.D., Weitz D.A. Ultrahigh-throughput screening in drop-based microfluidics for directed evolution. Proc Natl Acad Sci U S A 2010, 107:4004-4009.