Review
You have full text access to this OnlineOpen article
A synergistic approach to protein crystallization: Combination of a fixed-arm carrier with surface entropy reduction
Article first published online: 1 MAR 2010
DOI: 10.1002/pro.368
Copyright © 2010 The Protein Society
Additional Information
How to Cite
Moon, A. F., Mueller, G. A., Zhong, X. and Pedersen, L. C. (2010), A synergistic approach to protein crystallization: Combination of a fixed-arm carrier with surface entropy reduction. Protein Science, 19: 901–913. doi: 10.1002/pro.368
Publication History
- Issue published online: 23 APR 2010
- Article first published online: 1 MAR 2010
- Accepted manuscript online: 1 MAR 2010 12:00AM EST
- Manuscript Accepted: 8 FEB 2010
- Manuscript Revised: 5 FEB 2010
- Manuscript Received: 15 JAN 2010
Funded by
- Intramural Research Program of the National Institutes of Health (NIH)
- National Institute of Environmental Health Sciences (NIEHS)
References
- 1, ( 1995) Reductive alkylation of proteins. Anal Biochem 224: 1–16.
- 2( 1997) Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol 276: 171–179.
- 3, , , , , , , , , ( 2006) Lysine methylation as a routine rescue strategy for protein crystallization. Structure 14: 1617–1622.
- 4, , , , , , ( 1996) Carboxymethylation of the human estrogen receptor ligand-binding domain-estradiol complex: HPLC/ESMS peptide mapping shows that cysteine 447 does not react with iodoacetic acid. Steroids 61: 367–373.
- 5, , , , , , ( 1998) The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95: 927–937.
- 6, , ( 2007) In situ proteolysis for protein crystallization and structure determination. Nat Methods 4: 1019–1021.
- 7, ( 2009) In situ proteolysis to generate crystals for structure determination: an update. PLoS ONE 4( 4): e5094.
- 8, , , , , , , , , , , , ( 1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc Natl Acad Sci USA 90: 6320–6324.
- 9, , , , , ( 1994) Fullerene-like organization of HIV gag-protein shell in virus-like particles produced by recombinant baculovirus. Virology 198: 288–296.
- 10, , , ( 1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660–669.
- 11, , , ( 1995) Fv fragment-mediated crystallization of the membrane protein bacterial cytochrome c oxidase. Nat Struct Biol 2: 842–846.
- 12, , , ( 1997) Structure at 2.7 A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc Natl Acad Sci USA 94: 10547–10553.
- 13, , , ( 2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414: 43–48.
- 14, ( 2002) Crystallisation of membrane proteins mediated by antibody fragments. Curr Opin Struct Biol 12: 503–508.
- 15, , , , ( 2006) Crystal structure of the TCR co-receptor CD8alphaalpha in complex with monoclonal antibody YTS 105.18 Fab fragment at 2.88 A resolution. J Mol Biol 358: 347–354.
- 16, , , , ( 2008) The crystal structure of CD8 in complex with YTS156.7.7 Fab and interaction with other CD8 antibodies define the binding mode of CD8 αβ to MHC class I. J Mol Biol 384: 1190–1202.
- 17, ( 2008) Structure of complex III with bound cytochrome c in reduced state and definition of a minimal core interface for electron transfer. J Biol Chem 283: 17542–17549.
- 18, , ( 1995) The use of antibody fragments for crystallization and structure determinations. Structure 3: 1291–1293.
- 19
- 20, , , , ( 2009) Nanobody-aided structure determination of the EpsI: EpsJ pseudopilin heterodimer from Vibrio vulnificus. J Struct Biol 166: 8–15.
- 21, ( 2003) Monoclonal antibodies for the structural analysis of the Na+/H+ antiporter NhaA from Escherichia coli. Biochim Biophys Acta 1610: 46–50.
- 22, , ( 2004) An antibody library for stabilizing and crystallizing membrane proteins—selecting binders to the citrate carrier CitS. FEBS Lett 564: 340–348.
- 23, , , , ( 2003) Crystal structures of fusion proteins with large-affinity tags. Protein Sci 12: 1313–1322.Direct Link:
- 24, , , ( 1997) Crystal structure of a recombinant form of the maltodextrin-binding protein carrying an inserted sequence of a B-cell epitope from the preS2 region of hepatitis B virus. Proteins 27: 1–8.Direct Link:
- 25, , , ( 2009) Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process. Protein Sci 18: 1521–1530.Direct Link:
- 26, , ( 2007) Escherichia coli MutS tetramerization domain structure reveals that stable dimers but not tetramers are essential for DNA mismatch repair in vivo. J Biol Chem 282: 16345–16354.
- 27, ( 2003) Insights into binding cooperativity of MATa1/MATalpha2 from the crystal structure of a MATa1 homeodomain-maltose binding protein chimera. Protein Sci 12: 306–312.Direct Link:
- 28, , , , ( 2009) Secondary structure of Huntingtin amino-terminal region. Structure 17: 1205–1212.
- 29, , , , , , , ( 2009) Structural basis of yeast Tim40/Mia40 as an oxidative translocator in the mitochondrial intermembrane space. Proc Natl Acad Sci USA 106: 14403–14407.
- 30, , , ( 1999) Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteins. Proc Natl Acad Sci USA 96: 4319–4324.
- 31, , , , ( 2008) A dominant conformational role for amino acid diversity in minimalist protein-protein interfaces. J Mol Biol 381: 407–418.
- 32, , ( 2008) Crystal structure of human IPS-1/MAVS/VISA/Cardif caspase activation recruitment domain. BMC Struct Biol 8: 11.
- 33, , , ( 2008) Molecular recognition of corticotropin-releasing factor by its G-protein-coupled receptor CRFR1. J Biol Chem 283: 32900–32912.
- 34, , , , ( 2008) Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456: 653–657.
- 35, , , , ( 2003) Inherent protein structural flexibility at the RNA-binding interface of L30e. J Mol Biol 326: 999–1004.
- 36, , , , , , ( 1998) Crystallization of a trimeric human T cell leukemia virus type 1 gp21 ectodomain fragment as a chimera with maltose-binding protein. Protein Sci 7: 1612–1619.Direct Link:
- 37, , , , , ( 2005) De novo design of an IL-4 antagonist and its structure at 1.9 A. Proc Natl Acad Sci USA 102: 1889–1894.
- 38, , , , , , ( 2001) Crystal structure of the SarR protein from Staphylococcus aureus. Proc Natl Acad Sci USA 98: 6877–6882.
- 39, , , , , , , ( 2003) The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat Struct Biol 10: 1026–1032.
- 40, ( 2008) Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc Natl Acad Sci USA 105: 5034–5039.
- 41, , , , , , , , ( 2000) Crystallization and preliminary X-ray diffraction analysis of the extracellular domain of the cell surface antigen CD38 complexed with ganglioside. J Biochem 127: 181–184.
- 42, , , ( 2008) Redirecting the substrate specificity of heparan sulfate 2-O-sulfotransferase by structurally guided mutagenesis. Proc Natl Acad Sci USA 105: 18724–18729.
- 43, , , , , ( 2008) Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Sci 17: 1771–1780.Direct Link:
- 44, , , , , ( 2007) Basis for a ubiquitin-like protein thioester switch toggling E1-E2 affinity. Nature 445: 394–398.
- 45, , , , , , ( 1994) Three-dimensional structure of Schistosoma japonicum glutathione S-transferase fused with a six-amino acid conserved neutralizing epitope of gp41 from HIV. Protein Sci 3: 2233–2244.Direct Link:
- 46, , , ( 1999) Structure of the fibrinogen gamma-chain integrin binding and factor XIIIa cross-linking sites obtained through carrier protein driven crystallization. Protein Sci 8: 2663–2671.Direct Link:
- 47, , , ( 1998) Structure of the ankyrin-binding domain of α-Na, K-ATPase. J Biol Chem 273: 18681–18684.
- 48, , , , , , , , , ( 1999) Crystal structure of the nuclear matrix targeting signal of the transcription factor acute myelogenous leukemia-1/polyoma enhancer-binding protein 2alphaB/core binding factor α2. J Biol Chem 274: 33580–33586.
- 49, , , , , ( 1997) Use of a fusion protein to obtain crystals suitable for X-ray analysis: crystallization of a GST-fused protein containing the DNA-binding domain of DNA replication-related element-binding factor, DREF. Protein Sci 6: 1783–1786.Direct Link:
- 50, , , , , ( 2007) Polymer-driven crystallization. Protein Sci 16: 2542–2551.Direct Link:
- 51, , , , , , , , ( 2008) A specific cholesterol binding site is established by the 2.8 A structure of the human β2-adrenergic receptor. Structure 16: 897–905.
- 52, , , , , , , , , , ( 2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318: 1258–1265.
- 53, , , , , , , ( 2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322: 1211–1217.
- 54, , , , ( 2008) Thioredoxin as a fusion tag for carrier-driven crystallization. Protein Sci 17: 2070–2079.Direct Link:
- 55, , , , , ( 1998) A thioredoxin fusion protein of VanH, a D-lactate dehydrogenase from Enterococcus faecium: cloning, expression, purification, kinetic analysis, and crystallization. Protein Sci 7: 1147–1155.Direct Link:
- 56, , , , , , , , , , ( 2007) GPCR engineering yields high-resolution structural insights into β-adrenergic receptor function. Science 318: 1266–1273.
- 57, , , , , , ( 2002) Proteome-scale purification of human proteins from bacteria. Proc Natl Acad Sci USA 99: 2654–2659.
- 58, , , , ( 2002) Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli. Protein Sci 11: 313–321.Direct Link:
- 59, , , , , ( 2002) High-throughput screening of soluble recombinant proteins. Protein Sci 11: 1714–1719.Direct Link:
- 60, ( 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.Direct Link:
- 61, ( 2000) Fusions to maltose-binding protein: control of folding and solubility in protein purification. Methods Enzymol 326: 312–321.
- 62, , , , , , ( 2000) Protein production: feeding the crystallographers and NMR spectroscopists. Nat Struct Biol Suppl 7: 970–972.
- 63( 2000) Design of high-throughput methods of protein production for structural biology. Structure 8: R177–R185.
- 64, , ( 1994) Expression of rat NK-2 (neurokinin A) receptor in E. coli. Receptors Channels 2: 295–302.
- 65, ( 1996) Overexpression of bacterio-opsin in Escherichia coli as a water-soluble fusion to maltose binding protein: efficient regeneration of the fusion protein and selective cleavage with trypsin. Protein Sci 5: 456–467.
- 66, , , ( 1999) Overexpression of the alanine carrier protein gene from thermophilic bacterium PS3 in Escherichia coli. J Biochem 125: 454–459.
- 67, , , ( 2004) Automated large-scale purification of a G protein-coupled receptor for neurotensin. FEBS Lett 564: 289–293.
- 68( 2004) Rational protein crystallization by mutational surface engineering. Structure 12: 529–535.
- 69, ( 2006) Entropy and surface engineering in protein crystallization. Acta Crystallogr D Biol Crystallogr 62: 116–124.Direct Link:
- 70, , , , , , ( 2007) Protein crystallization by surface entropy reduction: optimization of the SER strategy. Acta Crystallogr D Biol Crystallogr 63: 636–645.Direct Link:
- 71, , , ( 2002) Solvent entropy contribution to the free energy of protein crystallization. Acta Crystallogr D Biol Crystallogr 58: 1611–1616.Direct Link:
- 72( 2003) Solvent entropy effects in the formation of protein solid phases. Methods Enzymol 368: 84–105.
- 73, ( 1998) Role of main-chain electrostatics, hydrophobic effect and side-chain conformational entropy in determining the secondary structure of proteins. J Mol Biol 279: 665–684.
- 74, , , , , , ( 2002) The impact of Glu-->Ala and Glu-->Asp mutations on the crystallization properties of RhoGDI: the structure of RhoGDI at 1.3 A resolution. Acta Crystallogr D Biol Crystallogr 58: 1983–1991.Direct Link:
- 75( 1991) MOLSCRIPT: a program to produce both detailed and schematic plots of proteins. J Appl Crystallogr 24: 946–950.Direct Link:
- 76, , ( 1991) The 2.3-A resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J Biol Chem 266: 5202–5219.
- 77, , , ( 1992) Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. Biochemistry 31: 10657–10663.
- 78, , , , , , , ( 2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild Wizard. Acta Crystallogr D Biol Crystallogr 64: 61–69.Direct Link:
- 79, , , , , , , , , ( 2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948–1954.Direct Link:
- 80, , ( 2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030–1037.
- 81, , , , ( 2001) Substrate specificity of the heparan sulfate hexuronic acid 2-O-sulfotransferase. Biochemistry 40: 5548–5555.
- 82, , , , ( 2001) Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J Biol Chem 276: 30744–30752.
- 83( 1998) Comparative studies of protein crystallization by vapour-diffusion and microbatch techniques. Acta Crystallogr D Biol Crystallogr 54: 8–15.Direct Link:
- 84( 1997) MOLREP: An automated program for molecular replacement. J Appl Crystallogr 30: 1022–1025.Direct Link:
- 85, , , , ( 1997) Crystal structure of estrogen sulphotransferase. Nat Struct Biol 4: 904–908.
- 86, , , , , , , , , , , , , ( 1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905–921.Direct Link:
- 87( 2002) The PyMOL molecular graphics system. DeLano Scientific: San Carlos, CA.
- 88, , , , , ( 2001) Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc Natl Acad Sci USA 98: 12984–12989.
- 89, , , , ( 2002) The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 62: 1261–1273.
- 90, , , ( 2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 5: 1137–1141.
- 91, , , ( 2007) Nomenclature and structural biology of allergens. J Allergy Clin Immunol 119: 414–420.
- 92( 1993) Mite allergens groups I-VII. A catalogue of enzymes. Clin Exp Allergy 23: 350–353.Direct Link:
- 93, , , , ( 1993) Molecular cloning of a house dust mite allergen with common antibody binding specificities with multiple components in mite extracts. Clin Exp Allergy 23: 934–940.Direct Link:
- 94, , , , , ( 1996) IgE and monoclonal antibody binding by the mite allergen Der p 7. Clin Exp Allergy 26: 308–315.Direct Link:
- 95( 1999) GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J Mol Biol 287: 797–815.
- 96, , , , ( 2000) The 1.7 A crystal structure of BPI: a study of how two dissimilar amino acid sequences can adopt the same fold. J Mol Biol 299: 1019–1034.
- 97, , , , ( 2009) Crystal structure of Epiphyas postvittana takeout 1 with bound ubiquinone supports a role as ligand carriers for takeout proteins in insects. J Biol Chem 284: 3496–3503.
- 98, , , , , , , , , , ( 2009) Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457: 585–588.

1469-896X/asset/olbannerleft.gif?v=1&s=d218899ae53b2862ab119790ed504b8d72122fb3)
1469-896X/asset/olbannerright.gif?v=1&s=59470eb9a1d9b7b13b1be75e9445e6c46ee2214f)
1469-896X/asset/cover.gif?v=1&s=0ff483325083001100314f63c633a394aff24478)