Evaluation of cell-free protein synthesis for the crystallization of membrane proteins - A case study on a member of the glutamate transporter family from Staphylothermus marinus

FEBS Journal

Volumn 280, Issue 4, 2013, Pages 1112-1125

  Jaehme, Michael ^a   Michel, Hartmut ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

cell free protein synthesis; crystallization; Foscholine 12; glutamate transporter; membrane proteins

Indexed keywords

GLUTAMATE TRANSPORTER; GREEN FLUORESCENT PROTEIN; PROTEIN FOS; PROTEIN FOS 12; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CELL DENSITY; CELL FREE SYSTEM; CONTROLLED STUDY; CRYSTALLIZATION; CRYSTALLOGRAPHY; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; PARTICLE SIZE; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; PYROCOCCUS HORIKOSHII; STAPHYLOTHERMUS MARINUS;

AMINO ACID TRANSPORT SYSTEM X-AG; ARCHAEAL PROTEINS; CROSS-LINKING REAGENTS; CRYSTALLIZATION; DESULFUROCOCCACEAE; DETERGENTS; ESCHERICHIA COLI; GLUCOSIDES; GLUTARAL; PHOSPHORYLCHOLINE; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STAPHYLOTHERMUS MARINUS;

EID: 84874117105     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12105     Document Type: Article

References (64)

1. Deisenhofer J, Epp O, Miki K, Huber R, &, Michel H, (1985) Structure of the protein subunits in the photosynthetic reaction center of rhodopseudomonas-viridis at 3a resolution. Nature 318, 618-624.
2. White SH, (2009) Biophysical dissection of membrane proteins. Nature 459, 344-346.
3. Geertsma ER, Groeneveld M, Slotboom DJ, &, Poolman B, (2008) Quality control of overexpressed membrane proteins. Proc Natl Acad Sci USA 105, 5722-5727.
4. Bernaudat F, Frelet-Barrand A, Pochon N, Dementin S, Hivin P, Boutigny S, Rioux JB, Salvi D, Seigneurin-Berny D, Richaud P, et al,. (2011) Heterologous expression of membrane proteins: choosing the appropriate host. PLoS One 6, e29191.
5. Shimizu Y, Kanamori T, &, Ueda T, (2005) Protein synthesis by pure translation systems. Methods 36, 299-304.
6. Klammt C, Lohr F, Schafer B, Haase W, Dotsch V, Ruterjans H, Glaubitz C, &, Bernhard F, (2004) High level cell-free expression and specific labeling of integral membrane proteins. Eur J Biochem/FEBS 271, 568-580.
7. Klammt C, Schwarz D, Fendler K, Haase W, Dotsch V, &, Bernhard F, (2005) Evaluation of detergents for the soluble expression of alpha-helical and beta-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J 272, 6024-6038.
8. Berrier C, Park KH, Abes S, Bibonne A, Betton JM, &, Ghazi A, (2004) Cell-free synthesis of a functional ion channel in the absence of a membrane and in the presence of detergent. Biochemistry 43, 12585-12591.
9. Kalmbach R, Chizhov I, Schumacher MC, Friedrich T, Bamberg E, &, Engelhard M, (2007) Functional cell-free synthesis of a seven helix membrane protein: in situ insertion of bacteriorhodopsin into liposomes. J Mol Biol 371, 639-648.
10. Cappuccio JA, Blanchette CD, Sulchek TA, Arroyo ES, Kralj JM, Hinz AK, Kuhn EA, Chromy BA, Segelke BW, Rothschild KJ, et al,. (2008) Cell-free co-expression of functional membrane proteins and apolipoprotein, forming soluble nanolipoprotein particles. Mol Cell Proteomics 7, 2246-2253.
11. Koglin A, Klammt C, Trbovic N, Schwarz D, Schneider B, Schafer B, Lohr F, Bernhard F, &, Dotsch V, (2006) Combination of cell-free expression and NMR spectroscopy as a new approach for structural investigation of membrane proteins. Magn Reson Chem/MRC 44, S17-S23.
12. Chen YJ, Pornillos O, Lieu S, Ma C, Chen AP, &, Chang G, (2007) X-ray structure of EmrE supports dual topology model. Proc Natl Acad Sci USA 104, 18999-19004.
13. Deniaud A, Liguori L, Blesneac I, Lenormand JL, &, Pebay-Peyroula E, (2010) Crystallization of the membrane protein hVDAC1 produced in cell-free system. BBA-Biomembranes 1798, 1540-1546.
14. Nguyen TA, Lieu SS, &, Chang G, (2010) An Escherichia coli-based cell-free system for large-scale production of functional mammalian membrane proteins suitable for X-ray crystallography. J Mol Microbiol Biotechnol 18, 85-91.
15. Vandenberg RJ, Handford CA, Campbell EM, Ryan RM, &, Yool AJ, (2011) Water and urea permeation pathways of the human excitatory amino acid transporter EAAT1. Biochem J 439, 333-340.
16. Kanai Y, &, Hediger MA, (2004) The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch Eur J Phy 447, 469-479.
17. Ryan RM, &, Mindell JA, (2007) The uncoupled chloride conductance of a bacterial glutamate transporter homolog. Nat Struct Mol Biol 14, 365-371.
18. Slotboom DJ, Konings WN, &, Lolkema JS, (1999) Structural features of the glutamate transporter family. Microbiol Mol Biol R 63, 293.
19. Yernool D, Boudker O, Jin Y, &, Gouaux E, (2004) Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431, 811-818.
20. Boudker O, Ryan RM, Yernool D, Shimamoto K, &, Gouaux E, (2007) Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter. Nature 445, 387-393.
21. Reyes N, Ginter C, &, Boudker O, (2009) Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462, 880-885.
22. Verdon G, &, Boudker O, (2012) Crystal structure of an asymmetric trimer of a bacterial glutamate transporter homolog. Nat Struct Mol Biol 19, 355-357.
23. Ishihara G, Goto M, Saeki M, Ito K, Hori T, Kigawa T, Shirouzu M, &, Yokoyama S, (2005) Expression of G protein coupled receptors in a cell-free translational system using detergents and thioredoxin-fusion vectors. Protein Expr Purif 41, 27-37.
24. Katayama Y, Shimokata K, Suematsu M, Ogura T, Tsukihara T, Yoshikawa S, &, Shimada H, (2010) Cell-free synthesis of cytochrome c oxidase, a multicomponent membrane protein. J Bioenerg Biomembr 42, 235-240.
25. Kim DM, &, Choi CY, (1996) A semicontinuous prokaryotic coupled transcription/translation system using a dialysis membrane. Biotechnol Prog 12, 645-649.
26. Schwarz D, Junge F, Durst F, Frolich N, Schneider B, Reckel S, Sobhanifar S, Dotsch V, &, Bernhard F, (2007) Preparative scale expression of membrane proteins in Escherichia coli-based continuous exchange cell-free systems. Nat Protoc 2, 2945-2957.
27. Underwood KA, Swartz JR, &, Puglisi JD, (2005) Quantitative polysome analysis identifies limitations in bacterial cell-free protein synthesis. Biotechnol Bioeng 91, 425-435.
28. Drew D, Lerch M, Kunji E, Slotboom DJ, &, de Gier JW, (2006) Optimization of membrane protein overexpression and purification using GFP fusions. Nat Methods 3, 303-313.
29. Slotboom DJ, Sobczak I, Konings WN, &, Lolkema JS, (1999) A conserved serine-rich stretch in the glutamate transporter family forms a substrate-sensitive reentrant loop. Proc Natl Acad Sci USA 96, 14282-14287.
30. Yernool D, Boudker O, Folta-Stogniew E, &, Gouaux E, (2003) Trimeric subunit stoichiometry of the glutamate transporters from Bacillus caldotenax and Bacillus stearothermophilus. Biochemistry 42, 12981-12988.
31. Guzman LM, Belin D, Carson MJ, &, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177, 4121-4130.
32. Ryan RM, Compton EL, &, Mindell JA, (2009) Functional characterization of a Na+-dependent aspartate transporter from Pyrococcus horikoshii. J Biol Chem 284, 17540-17548.
33. Gendreau S, Voswinkel S, Torres-Salazar D, Lang N, Heidtmann H, Detro-Dassen S, Schmalzing G, Hidalgo P, &, Fahlke C, (2004) A trimeric quaternary structure is conserved in bacterial and human glutamate transporters. J Biol Chem 279, 39505-39512.
34. Migneault I, Dartiguenave C, Bertrand MJ, &, Waldron KC, (2004) Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. Biotechniques 37, 790-796, 798-802.
35. Quick M, Winther AML, Shi L, Nissen P, Weinstein H, &, Javitch JA, (2009) Binding of an octylglucoside detergent molecule in the second substrate (S2) site of LeuT establishes an inhibitor-bound conformation. Proc Natl Acad Sci USA 106, 5563-5568.
36. Palladino P, Rossi F, &, Ragone R, (2010) Effective critical micellar concentration of a zwitterionic detergent: a fluorimetric study on n-dodecyl phosphocholine. J Fluoresc 20, 191-196.
37. Serrano-Vega MJ, Magnani F, Shibata Y, &, Tate CG, (2008) Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form. Proc Natl Acad Sci USA 105, 877-882.
38. Wuu JJ, &, Swartz JR, (2008) High yield cell-free production of integral membrane proteins without refolding or detergents. Biochim Biophys Acta 1778, 1237-1250.
39. Ma Y, Munch D, Schneider T, Sahl HG, Bouhss A, Ghoshdastider U, Wang J, Dotsch V, Wang X, &, Bernhard F, (2011) Preparative scale cell-free production and quality optimization of MraY homologues in different expression modes. J Biol Chem 286, 38844-38853.
40. Yu H, (1999) Extending the size limit of protein nuclear magnetic resonance. Proc Natl Acad Sci USA 96, 332-334.
41. Raunser S, Appel M, Ganea C, Geldmacher-Kaufer U, Fendler K, &, Kuhlbrandt W, (2006) Structure and function of prokaryotic glutamate transporters from Escherichia coli and Pyrococcus horikoshii. Biochemistry 45, 12796-12805.
42. Drew DE, von Heijne G, Nordlund P, &, de Gier JW, (2001) Green fluorescent protein as an indicator to monitor membrane protein overexpression in Escherichia coli. FEBS Lett 507, 220-224.
43. Groeneveld M, &, Slotboom DJ, (2007) Rigidity of the subunit interfaces of the trimeric glutamate transporter GltT during translocation. J Mol Biol 372, 565-570.
44. Lipfert J, Columbus L, Chu VB, Lesley SA, &, Doniach S, (2007) Size and shape of detergent micelles determined by small-angle x-ray scattering. J Phys Chem B 111, 12427-12438.
45. Keller T, Egenberger B, Gorboulev V, Bernhard F, Uzelac Z, Gorbunov D, Wirth C, Koppatz S, Dotsch V, Hunte C, et al,. (2011) The large extracellular loop of organic cation transporter 1 influences substrate affinity and is pivotal for oligomerization. J Biol Chem 286, 37874-37886.
46. Elbaz Y, Danieli T, Kanner BI, &, Schuldiner S, (2010) Expression of neurotransmitter transporters for structural and biochemical studies. Protein Expr Purif 73, 152-160.
47. Kauko A, Hedin LE, Thebaud E, Cristobal S, Elofsson A, &, von Heijne G, (2010) Repositioning of transmembrane alpha-helices during membrane protein folding. J Mol Biol 397, 190-201.
48. Matthies D, Haberstock S, Joos F, Dotsch V, Vonck J, Bernhard F, &, Meier T, (2011) Cell-free expression and assembly of ATP synthase. J Mol Biol 413, 593-603.
49. Studier FW, &, Moffatt BA, (1986) Use of bacteriophage-T7 RNA-polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113-130.
50. Tegel H, Ottosson J, &, Hober S, (2011) Enhancing the protein production levels in Escherichia coli with a strong promoter. FEBS J 278, 729-739.
51. Brosius J, Erfle M, &, Storella J, (1985) Spacing of the -10 and -35 regions in the tac promoter. Effect on its in vivo activity. J Biol Chem 260, 3539-3541.
52. Terpe K, (2006) Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 72, 211-222.
53. Quick M, Shi L, Zehnpfennig B, Weinstein H, &, Javitch JA, (2012) Experimental conditions can obscure the second high-affinity site in LeuT. Nat Struct Mol Biol 19, 207-211.
54. Hwang PM, Bishop RE, &, Kay LE, (2004) The integral membrane enzyme PagP alternates between two dynamically distinct states. Proc Natl Acad Sci USA 101, 9618-9623.
55. Ahn VE, Lo EI, Engel CK, Chen L, Hwang PM, Kay LE, Bishop RE, &, Prive GG, (2004) A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J 23, 2931-2941.
56. Rukhman V, Lerner N, &, Adir N, (2000) Analysis of the role of detergent mixtures on the crystallization of the reaction center of Photosystem II. Photosynth Res 65, 249-259.
57. Columbus L, Lipfert J, Jambunathan K, Fox DA, Sim AY, Doniach S, &, Lesley SA, (2009) Mixing and matching detergents for membrane protein NMR structure determination. J Am Chem Soc 131, 7320-7326.
58. Adam Y, Edwards RH, &, Schuldiner S, (2008) Expression and function of the rat vesicular monoamine transporter 2. Am J Physiol-Cell Ph 294, C1004-C1011.
59. Lyukmanova EN, Shenkarev ZO, Khabibullina NF, Kopeina GS, Shulepko MA, Paramonov AS, Mineev KS, Tikhonov RV, Shingarova LN, Petrovskaya LE, et al,. (2012) Lipid-protein nanodiscs for cell-free production of integral membrane proteins in a soluble and folded state: comparison with detergent micelles, bicelles and liposomes. Biochim Biophys Acta 1818, 349-358.
60. Groeneveld M, &, Slotboom DJ, (2010) Na(+):aspartate coupling stoichiometry in the glutamate transporter homologue Glt(Ph). Biochemistry 49, 3511-3513.
61. Tropea JE, Cherry S, &, Waugh DS, (2009) Expression and purification of soluble His(6)-tagged TEV protease. Methods Mol Biol 498, 297-307.
62. Gruegelsiepe H, Schoen A, Kirsebom LA, &, Hartmann RK, (2005) Enzymatic RNA synthesis using bacteriophage T7 RNA polymerase. In Handbook of RNA Biochemistry (, Hartmann RK, Schoen ABA, &, Westhof E, eds), pp. 3-21. Wiley-VCH, Weinheim.
63. Geertsma ER, Mahmood NABN, Schuurman-Wolters GK, &, Poolman B, (2008) Membrane reconstitution of ABC transporters and assays of translocator function. Nat Protoc 3, 256-266.
64. Schmid FX, (1998) Optical spectroscopy to characterize protein conformation and conformational changes and measuring the conformational stability of a protein. In Protein Structure: A Practical Approach (, pp. Creighton TE, ed.), pp. 261-322. Oxford University Press, Oxford, UK.