New tools for membrane protein research

Current Protein and Peptide Science

Volumn 11, Issue 2, 2010, Pages 156-165

  Alguel, Yilmaz ^a   Leung, James ^a   Singh, Shweta ^a   Rana, Rohini ^a   Civiero, Laura ^a   Alves, Claudia ^a   Byrne, Bernadette ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Aggregation; Amphiphiles; Conformational thermostabilization; Eukaryotic membrane proteins; High resolution structure determination; High throughput pipelines

Indexed keywords

ALANINE; ANTIBODY; DETERGENT; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LYSOZYME; MEMBRANE PROTEIN;

CRYSTAL STRUCTURE; HUMAN; MUTAGENESIS; NONHUMAN; PROKARYOTE; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SCREENING;

GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; RECOMBINANT FUSION PROTEINS; RESEARCH; RESEARCH DESIGN;

EUKARYOTA; PROKARYOTA;

EID: 77950171265     PISSN: 13892037     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920310790848395     Document Type: Review

References (72)

1. Wallin, E.; Von Heijne, G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci., 1998, 7(4), 1029-1038.
2. Granseth, E.; Daley, D.O.; Rapp, M.; Melen, K.; von Heijne, G. Experimentally constrained topology models for 51,208 bacterial inner membrane proteins. J. Mol. Biol., 2005, 352(3), 489-494.
3. Carpenter, E.P.; Beis, K.; Cameron, A.D.; Iwata, S. Overcoming the challenges of membrane protein crystallography. Curr. Opin. Struct. Biol., 2008, 18(5), 581-586.
4. Granseth, E.; Seppälä, S.; Rapp, M.; Daley, D.O.; Von Heijne, G. Membrane protein structural biology: How far can the bugs take us? Mol. Membr. Biol., 2007, 24(5), 329-332.
5. Midgett, C.R.; Madden, D.R. Breaking the bottleneck: eukaryotic membrane protein expression for high-resolution structural studies. J. Struct. Biol., 2007, 160(3), 265-274.
6. Junge, F.; Schneider, B.; Reckel, S.; Schwarz, D.; Dotsch, V.; Bernhard, F. Large-scale production of functional membrane proteins. Cell Mol. Life Sci., 2008, 65(11), 1729-1755.
7. Sarramegna, V.; Talmont, F.; Demange, P.; Milon, A. Heterologous expression of G-protein-coupled receptors: comparison of expression systems fron the standpoint of large-scale production and purification. Cell Mol. Life Sci., 2003, 60(8), 1529-1546.
8. Grisshammer, R.; White, J.F.; Trinh, L.B.; Shiloach, J. Large-scale expression and purification of a G-protein-coupled receptor for structure determination - an overview. J. Struct. Funct. Genomics, 2005, 6(2-3), 159-163.
9. Ferguson, A.D.; McKeever, B.M.; Xu, S.; Wisniewski, D.; Miller, D.K.; Yamin, T.T.; Spencer, R.H.; Chu, L.; Ujjainwalla, F.; Cunningham, B.R.; Evans, J.F.; Becker, J.W. Crystal structure of inhibitor-bound human 5-lipoxygenase-activating protein. Science, 2007, 317(5837), 510-512.
10. Opekarova, M.; Tanner, W. Specific lipid requirements of membrane proteins - a putative bottleneck in heterologous expression. Biochim. Biophys. Acta, 2003, 1610(1), 11-22.
11. Long, S.B.; Campbell, E.B.; MacKinnon, R. Crystal structure of a mammalian voltage-dependent shaker family K+ channel. Science, 2005, 309(5736), 897-903.
12. Tornroth-Horsefield, S.; Wang, Y.; Hedfalk, K.; Johanson, U.; Karlsson, M.; Tajkhorshid, E.; Neutze, R.; Kjellbom, P. Structural mechanism of plant aquaporin gating. Nature, 2006, 439(7077), 688-694.
13. Martinez Molina, D.; Wetterholm, A.; Kohl, A.; McCarthy, A.A.; Niegowski, D.; Ohlson, E.; Hammarberg, T.; Eshaghi, S.; Haeggstrom, J.Z.; Nordlund, P. Structural basis for synthesis of inflammatory mediators by human leukotriene C4 synthase. Nature, 2007, 448(7153), 613-616.
14. Aller, S.G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P. M.; Trinh, Y. T.; Zhang, Q.; Urbatsch, I.L.; Chang, G. Structure of P-glycoprotein reveals a molecular basis for polyspecific drug binding. Science, 2009, 323(5922), 1718-1722.
15. Pedersen, B.P.; Buch-Pedersen, M.J.; Morth, J.P.; Palmgren, M.G.; Nissen, P. Crystal structure of the plasma membrane proton pump. Nature, 2007, 450 (7172), 1111-1114.
16. Jidenko, M.; Nielsen, R.C.; Sorensen, T.L.; Moller, J.V.; le Maire, M.; Nissen, P.; Jaxel, C. Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 2005, 102(33), 11687-11691.
17. Cherezov, V.; Rosenbaum, D.M.; Hanson, M.A.; Rasmussen, S.G.; Thian, F.S.; Kobilka, T.S.; Choi, H.J.; Kuhn, P.; Weis, W.I.; Kobilka, B.K.; Stevens, R.C. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science, 2007, 318(5854), 1258-1265.
18. Rasmussen, S.G.; Choi, H.J.; Rosenbaum, D.M.; Kobilka, T.S.; Thian, F.S.; Edwards, P.C.; Burghammer, M.; Ratnala, V.R.; Sanishvili, R.; Fischetti, R.F.; Schertler, G.F.; Weis, W.I.; Kobilka, B.K. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature, 2007, 450(7168), 383-387.
19. Warne, T.; Serrano-Vega, M.J.; Baker, J.G.; Moukhametzianov, R.; Edwards, P.C.; Henderson, R.; Leslie, A. G.; Tate, C.G.; Schertler, G.F. Structure of a beta1-adrenergic G-protein-coupled receptor. Nature, 2008, 454(7203), 486-491.
20. Jaakola, V.P.; Griffith, M.T.; Hanson, M.A.; Cherezov, V.; Chien, E.Y.; Lane, J.R.; Ijzerman, A.P.; Stevens, R.C. The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science, 2008, 322(5905), 1211-1217.
21. Jasti, J.; Furukawa, H.; Gonzales, E.B.; Gouaux, E. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature, 2007, 449(7160), 316-323.
22. Lundstrom, K. Semliki Forest virus vectors for rapid and high-level expression of integral membrane proteins. Biochim. Biophys. Acta, 2003, 1610(1), 90-96.
23. Hassaine, G.; Wagner, R.; Kempf, J.; Cherouati, N.; Hassaine, N.; Prual, C.; Andre, N.; Reinhart, C.; Pattus, F.; Lundstrom, K. Semliki Forest virus vectors for overexpression of 101 G protein-coupled receptors in mammalian host cells. Protein Expr. Purif., 2006, 45(2), 343-351.
24. Kunji, E.R.; Chan, K.W.; Slotboom, D.J.; Floyd, S.; O'Connor, R.; Monne, M. Eukaryotic membrane protein overproduction in Lactococcus lactis. Curr. Opin. Biotechnol., 2005, 16(5), 546-551.
25. Tate, C.G.; Haase, J.; Baker, C.; Boorsma, M.; Magnani, F.; Vallis, Y.; Williams, D.C. Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim. Biophys. Acta, 2003, 1610(1), 141-153.
26. Bonander, N.; Hedfalk, K.; Larsson, C.; Mostad, P.; Chang, C.; Gustafsson, L.; Bill, R.M. Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci., 2005, 14(7), 1729-1740.
27. Schwarz, D.; Dötsch, V.; Bernhard, F. Production of membrane proteins using cell-free expression systems. Proteomics, 2008, 8(19), 3933-3946.
28. Liguori, L.; Marques, B.; Villegas-Méndez, A.; Rothe, R.; Lenormand, J.-L. Production of membrane proteins using cell free expression systems. Exp. Rev. Proteomics, 2007, 4(1), 79-90.
29. He, M. Cell-free protein synthesis: applications in proteomics and biotechnology. Nat. Biotechnol., 2008, 25(2-3), 126-132.
30. Jackson, A.M.; Boutell, J.; Cooley, N.; He, M. Cell-free protein synthesis for proteomics. Brief Funct. Genomic Proteomic, 2004, 2(4), 308-319.
31. Kainosho, M.; Torizawa, T.; Iwashita, Y.; Terauchi, T.; Mei Ono, A.; Güntert, P. Optimal isotope labelling for NMR protein structure determinations. Nature, 2006, 440(7080), 52-57.
32. Klammt, C.; Schwarz, D.; Fendler, K.; Haase, W.; Dötsch, V.; Bernhard, F. Evaluation of detergents for the soluble expression of α-helical and β-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J., 2005, 272(23), 6024-6038.
33. Chen, Y.J.; Pornillos, O.; Lieu, S.; Ma, C.; Chen, A.P.; Chang, G. X-ray structure of EmrE supports dual topology model. Proc. Natl. Acad. Sci. USA, 2007, 104(48), 18999-9004.
34. Van den Berg, B.; Clemons, W.M.Jr.; Collinson, I.; Modis, Y.; Hartmann, E.; Harrison, S.C.; Rapoport, T.A. X-ray structure of a protein-conducting channel. Nature, 2004, 427(6969), 36-44.
35. Newstead, S.; Kim, H.; von Heijne, G.; Iwata, S.; Drew, D. High-throughput fluorescent-based optimization of eukaryotic membrane protein overexpression and purification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 2007, 104(35), 13936-13941.
36. Drew, D.; Newstead, S.; Sonoda, Y.; Kim, H.; von Heijne, G.; Iwata, S. GFP-based optimization scheme for the overexpression and purification of eukaryotic membrane proteins in Saccharomyces cerevisiae. Nat. Protoc. 2008, 3(5), 784-798.
37. Kota, J.; Gilstring, C.F.; Ljungdahl, P.O. Membrane chaperone Shr3 assists in folding amino acid permeases preventing precocious ERAD. J. Cell Biol., 2007, 176(5), 617-628.
38. Kawate, T.; Gouaux, E. Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure, 2006, 14(4), 673-681.
39. Li, M.; Hays, F.A.; Roe-Zurz, Z.; Vuong, L.; Kelly, L.; Ho, C.M.; Robbins, R.M.; Pieper, U.; O'Connell, J.D. 3rd; Miercke, L.J.; Giacomini, K.M.; Sali, A.; Stroud, R.M. Selecting optimum eukaryotic integral membrane proteins for structure determination by rapid expression and solubilization screening. J. Mol. Biol., 2009, 385(3), 820-830.
40. Kim, H.; Melén, K.; Osterberg, M.; von Heijne, G. A global topology map of the Saccharomyces cerevisiae membrane proteome. Proc. Natl. Acad. Sci. USA, 2006, 103(30) 11142-1147.
41. Overington, J.P.; Al-Lazikani, B.; Hopkins, A. L. How many drug targets are there? Nat. Rev. Drug Discov., 2006, 5(12), 993-996.
42. Palczewski, K.; Kumasaka, T.; Hori, T.; Behnke, C.A.; Motoshima, H.; Fox, B.A.; Le Trong, I.; Teller, D.C.; Okada, T.; Stenkamp, R.E.; Yamamoto, M.; Miyano, M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science, 2000, 289(5480), 739-745.
43. Klabunde, T.; Hessler, G. Drug design strategies for targeting G-protein-coupled receptors. ChemBioChem., 2002, 3(10), 928-944.
44. McCusker, E.C.; Bane, S.E.; O'Malley, M.A.; Robinson, A.S. Heterologous GPCR expression: a bottleneck to obtaining crystal structures. Biotechnol. Prog., 2007, 23(3), 540-547.
45. Warne, T.; Chirnside, J.; Schertler, G.F. Expression and purification of truncated, non-glycosylated turkey beta-adrenergic receptors for crystallization. Biochim. Biophys. Acta, 2003, 1610(1), 133-140.
46. Grisshammer, R.; Tucker, J. Quantitative evaluation of neurotensin receptor purification by immobilized metal affinity chromatography. Protein Expr. Purif., 1997, 11(1), 53-60.
47. Weiss, H.M.; Grisshammer, R. Purification and characterization of the human adenosine A(2a) receptor functionally expressed in Escherichia coli. Eur. J. Biochem., 2002, 269(1), 82-92.
48. Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature, 1995, 376(6542), 660-669.
49. Hunte, C.; Koepke, J.; Lange, C.; Rossmanith, T.; Michel, H. Structure at 2.3 Å resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure, 2000, 8(6), 669-684.
50. Zhou, Y.; Morais-Cabral, J.H.; Kaufman, A.; MacKinnon, R. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 Å resolution. Nature, 2001, 414(6859), 43-48.
51. Dutzler, R.; Campbell, E.B.; MacKinnon, R. Gating the selectivity filter in ClC chloride channels. Science, 2003, 300(5616), 108-12.
52. Sennhauser, G.; Amstutz, P.; Briand, C.; Storchenegger, O.; Grutter, M.G. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol., 2007, 5(1), e7.
53. Sennhauser, G.; Grutter, M.G. Chaperone-assisted crystallography with DARPins. Structure, 2008, 16(10), 1443-1453.
54. Rosenbaum, D.M.; Cherezov, V.; Hanson, M.A.; Rasmussen, S.G.F.; Thian, F.S.; Kobilka, T.S.; Choi, H.-J.; Yao, X.-J.; Weis, W.I.; Stevens, R.C.; Kobilka, B.K. GPCR Engineering yields high-resolution structural insights into 2-adrenergic receptor function. Science, 2007, 318(5854), 1266-1273.
55. Hanson, M.A.; Cherezov, V.; Griffith, M.T.; Roth, C.B.; Jaakola, V.-P.; Chien, E.Y.T.; Velasquez, J.; Kuhn, P.; Stevens, R.C. A Specific cholesterol binding site is established by the 2.8 Å structure of the human [beta]2-adrenergic receptor. Structure, 2008, 16(6), 897-905.
56. Zhou, Y.; Bowie, J.U. Building a thermostable membrane protein. J. Biol. Chem., 2000, 275(10), 6975-6979.
57. Serrano-Vega, M.J.; Magnani, F.; Shibata, Y.; Tate, C.G. Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form. Proc. Natl. Acad. Sci. USA, 2008, 105(3), 877-882.
58. Magnani, F.; Shibata, Y.; Serrano-Vega, M.J.; Tate, C.G. Co-evolving stability and conformational homogeneity of the human adenosine A2a receptor. Proc. Natl. Acad. Sci. USA, 2008, 105(31), 10744-10749.
59. Shibata, Y.; White, J.F.; Serrano-Vega, M.J.; Magnani, F.; Aloia, A.L.; Grisshammer, R.; Tate, C.G. Thermostabilization of the neurotensin receptor NTS1. J. Mol. Biol., 2009, 390(2), 262-277.
60. Alexandrov, A.I.; Mileni, M.; Chien, E.Y.; Hanson, M.A.; Stevens, R.C. Microscale fluorescent thermal stability assay for membrane proteins. Structure, 2008, 16(3), 351-359.
61. Gutmann, D.A.; Mizohata, E.; Newstead, S.; Ferrandon, S.; Postis, V.; Xia, X.; Henderson, P.J.; van Veen, H.W.; Byrne, B. A high-throughput method for membrane protein solubility screening: the ultracentrifugation dispersity sedimentation assay. Protein Sci., 2007, 16(7), 1422-1428.
62. Privé, G.G. Detergents for the stabilization and crystallization of membrane proteins. Methods, 2007, 41(4), 388-397.
63. Timmins, P.; Pebay-Peyroula, E.; Welte, W. Detergent organisation in solutions and in crystals of membrane proteins. Biophys. Chem., 1994, 53(1-2), 27-36.
64. Popot, J.L.; Berry, E.A.; Charvolin, D.; Creuzenet, C.; Ebel, C.; Engelman, D.M.; Flotenmeyer, M.; Giusti, F.; Gohon, Y.; Hong, Q.; Lakey, J.H.; Leonard, K.; Shuman, H.A.; Timmins, P.; Warschawski, D.E.; Zito, F.; Zoonens, M.; Pucci, B.; Tribet, C. Amphipols: polymeric surfactants for membrane biology research. Cell Mol. Life Sci., 2003, 60(8), 1559-1574.
65. Tribet, C.; Audebert, R.; Popot, J.L. Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc. Natl. Acad. Sci USA, 1996, 93(26), 15047-15050.
66. Yu, S.M.; McQuade, D.T.; Quinn, M.A.; Hackenberger, C.P.; Krebs, M.P.; Polans, A.S.; Gellman, S.H. An improved tripod amphiphile for membrane protein solubilization. Protein Sci., 2000, 9(12), 2518-2527.
67. 2+-ATPase. J. Biol. Chem., 2000, 275(25), 18623-18637.
68. McQuade, D.T.; Seungju, M.A.Q.; Yu, S.M.; Polans, A.S.; Krebs M.P.; Gellman, S.H. Rigid Amphiphiles for membrane protein manipulation. Angew. Chem. Int. Ed. Engl., 2000, 39(4), 758-761.
69. Theisen, M.J.; Potocky, T.B.; McQuade, D.T.; Gellman, S.H.; Chiu, M.L. Crystallization of bacteriorhodopsin solubilized by a tripod amphiphile. Biochim. Biophys. Acta, 2005, 1751(2), 213-216.
70. Scheerer, P.; Park, J.H.; Hildebrand, P.W.; Kim, Y.J.; Krausz, N.; Choe, H.-W.; Hofmann, K.P.; Ernst, O.P. Crystal structure of opsin in its G-protein-interacting conformation. Nature, 2008, 455(7212), 497-502.
71. Singh, S.K.; Piscitelli, C.L.; Yamashita, A.; Gouaux, E. A Competitive inhibitor traps LeuT in an open-to-out conformation. Science, 2008, 322(5908), 1655-1661.
72. Wang, L.; Sigworth, F.J. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature, 2009, 461(7261), 292-295.