Breaking the bottleneck: Eukaryotic membrane protein expression for high-resolution structural studies

Journal of Structural Biology

Volumn 160, Issue 3, 2007, Pages 265-274

  Midgett, Charles R ^a   Madden, Dean R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Baculovirus expression system; Co expression; Crystallization; Electron crystallography; Eukaryotic integral membrane proteins; Large scale transient transfection; Mammalian cells; Pichia; Protein structure; Purification; Recombinant expression; Saccharomyces; X ray crystallography

Indexed keywords

MEMBRANE PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; CRYSTALLIZATION; DISULFIDE BOND; ELECTRON DIFFRACTION; ESCHERICHIA COLI; EUKARYOTE; HOMOLOGOUS RECOMBINATION; HUMAN; INSECT CELL; LIPID COMPOSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; X RAY CRYSTALLOGRAPHY; YEAST;

ANIMALS; BACULOVIRIDAE; CELL LINE; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; CRYSTALLOGRAPHY; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENETIC VECTORS; HUMANS; INSECTS; MAMMALS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; TRANSFECTION; YEASTS;

EUKARYOTA; MAMMALIA; PICHIA; SACCHAROMYCES;

EID: 36148942092     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.07.001     Document Type: Article

References (117)

1. Abdulaev N.G., Popp M.P., Smith W.C., and Ridge K.D. Functional expression of bovine opsin in the methylotrophic yeast Pichia pastoris. Protein Expr. Purif. 10 (1997) 61-69
2. Airenne K.J., Peltomaa E., Hytonen V.P., Laitinen O.H., and Yla-Herttuala S. Improved generation of recombinant baculovirus genomes in Escherichia coli. Nucleic Acids Res. 31 (2003) e101
3. Akermoun M., Koglin M., Zvalova-Iooss D., Folschweiller N., Dowell S.J., and Gearing K.L. Characterization of 16 human G protein-coupled receptors expressed in baculovirus-infected insect cells. Protein Expr. Purif. 44 (2005) 65-74
4. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92 (1998) 291-294
5. Ames R., Fornwald J., Nuthulaganti P., Trill J., Foley J., Buckley P., Kost T., Wu Z., and Romanos M. BacMam recombinant baculoviruses in G protein-coupled receptor drug discovery. Receptors Channels 10 (2004) 99-107
6. Aricescu A.R., Assenberg R., Bill R.M., Busso D., Chang V.T., Davis S.J., Dubrovsky A., Gustafsson L., Hedfalk K., Heinemann U., Jones I.M., Ksiazek D., Lang C., Maskos K., Messerschmidt A., Macieira S., Peleg Y., Perrakis A., Poterszman A., Schneider G., Sixma T.K., Sussman J.L., Sutton G., Tarboureich N., Zeev-Ben-Mordehai T., and Jones E.Y. Eukaryotic expression: developments for structural proteomics. Acta Crystallogr. D Biol. Crystallogr. 62 (2006) 1114-1124
7. Aricescu A.R., Lu W., and Jones E.Y. A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr. D Biol. Crystallogr. 62 (2006) 1243-1250
8. Bach M., Grigat S., Pawlik B., Fork C., Utermohlen O., Pal S., Banczyk D., Lazar A., Schomig E., and Grundemann D. Fast set-up of doxycycline-inducible protein expression in human cell lines with a single plasmid based on Epstein-Barr virus replication and the simple tetracycline repressor. FEBS J. 274 (2007) 783-790
9. Baldi L., Hacker D.L., Adam M., and Wurm F.M. Recombinant protein production by large-scale transient gene expression in mammalian cells: state of the art and future perspectives. Biotechnol. Lett. (2007) 10.1007/s10529-006-9297-y
10. Bateman A., Coin L., Durbin R., Finn R.D., Hollich V., Griffiths-Jones S., Khanna A., Marshall M., Moxon S., Sonnhammer E.L., Studholme D.J., Yeats C., and Eddy S.R. The Pfam protein families database. Nucleic Acids Res. 32 (2004) D138-D141
11. Berrow N.S., Alderton D., Sainsbury S., Nettleship J., Assenberg R., Rahman N., Stuart D.I., and Owens R.J. A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Res. 35 (2007) e45
12. Bonander N., Hedfalk K., Larsson C., Mostad P., Chang C., Gustafsson L., and Bill R.M. Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci. 14 (2005) 1729-1740
13. Brisson A., and Unwin P.N. Tubular crystals of acetylcholine receptor. J. Cell Biol. 99 (1984) 1202-1211
14. Buck B., Zamoon J., Kirby T.L., DeSilva T.M., Karim C., Thomas D., and Veglia G. Overexpression, purification, and characterization of recombinant Ca-ATPase regulators for high-resolution solution and solid-state NMR studies. Protein Expr. Purif. 30 (2003) 253-261
15. Cadigan K.M., and Liu Y.I. Wnt signaling: complexity at the surface. J. Cell Sci. 119 (2006) 395-402
16. Chang G., Spencer R.H., Lee A.T., Barclay M.T., and Rees D.C. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282 (1998) 2220-2226
17. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
18. Condreay J.P., Witherspoon S.M., Clay W.C., and Kost T.A. Transient and stable gene expression in mammalian cells transduced with a recombinant baculovirus vector. PNAS 96 (1999) 127-132
19. Derouazi M., Girard P., Van Tilborgh F., Iglesias K., Muller N., Bertschinger M., and Wurm F.M. Serum-free large-scale transient transfection of CHO cells. Biotechnol. Bioeng. 87 (2004) 537-545
20. 2+-ATPase regulatory proteins for high-resolution structural studies. Protein Expr. Purif. 40 (2005) 118-125
21. + conduction and selectivity. Science 280 (1998) 69-77
22. Eifler N., Duckely M., Sumanovsky L.T., Egan T.M., Oksche A., Konopka J.B., Luthi A., Engel A., and Werten P.J. Functional expression of mammalian receptors and membrane channels in different cells. J. Struct. Biol. (2007)
23. Farrell P.J., Lu M., Prevost J., Brown C., Behie L., and Iatrou K. High-level expression of secreted glycoproteins in transformed lepidopteran insect cells using a novel expression vector. Biotechnol. Bioeng. 60 (1998) 656-663
24. Fleishman S.J., Unger V.M., and Ben-Tal N. Transmembrane protein structures without X-rays. Trends Biochem. Sci. 31 (2006) 106-113
25. Fourneau J.-M., Cohen H., and van Endert P.M.J.o.I.M. A chaperone-assisted high yield system for the production of HLA-DR4 tetramers in insect cells. J. Immunol. Methods 285 (2004) 253-264
26. Geisse S., Jordan M., and Wurm F.M. Large-scale transient expression of therapeutic proteins in mammalian cells. Methods Mol. Biol. 308 (2005) 87-98
27. Greger I.H., Akamine P., Khatri L., and Ziff E.B. Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron 51 (2006) 85-97
28. Griffith D.A., Delipala C., Leadsham J., Jarvis S.M., and Oesterhelt D. A novel yeast expression system for the overproduction of quality-controlled membrane proteins. FEBS Lett. 553 (2003) 45-50
29. Grisshammer R. Understanding recombinant expression of membrane proteins. Curr. Opin. Biotechnol. 17 (2006) 337-340
30. Grisshammer R., White J.F., Trinh L.B., and Shiloach J. Large-scale expression and purification of a G-protein-coupled receptor for structure determination-an overview. J. Struct. Funct. Genomics 6 (2005) 159-163
31. Hamilton S.R., Bobrowicz P., Bobrowicz B., Davidson R.C., Li H., Mitchell T., Nett J.H., Rausch S., Stadheim T.A., Wischnewski H., Wildt S., and Gerngross T.U. Production of complex human glycoproteins in yeast. Science 301 (2003) 1244-1246
32. Hamilton S.R., Davidson R.C., Sethuraman N., Nett J.H., Jiang Y., Rios S., Bobrowicz P., Stadheim T.A., Li H., Choi B.K., Hopkins D., Wischnewski H., Roser J., Mitchell T., Strawbridge R.R., Hoopes J., Wildt S., and Gerngross T.U. Humanization of yeast to produce complex terminally sialylated glycoproteins. Science 313 (2006) 1441-1443
33. Harrison R.L., and Jarvis D.L. Protein N-glycosylation in the baculovirus-insect cell expression system and engineering of insect cells to produce "mammalianized" recombinant glycoproteins. Adv. Virus Res. 68 (2006) 159-191
34. Hassan N.J., Pountney D.J., Ellis C., and Mossakowska D.E. BacMam recombinant baculovirus in transporter expression: a study of BCRP and OATP1B1. Protein Expr. Purif. 47 (2006) 591-598
35. Helenius A., and Aebi M. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73 (2004) 1019-1049
36. Higgins M.K., Demir M., and Tate C.G. Calnexin co-expression and the use of weaker promoters increase the expression of correctly assembled Shaker potassium channel in insect cells. Biochim. Biophys. Acta 1610 (2003) 124-132
37. Hiroaki Y., Tani K., Kamegawa A., Gyobu N., Nishikawa K., Suzuki H., Walz T., Sasaki S., Mitsuoka K., Kimura K., Mizoguchi A., and Fujiyoshi Y. Implications of the aquaporin-4 structure on array formation and cell adhesion. J. Mol. Biol. 355 (2006) 628-639
38. Hofmann C., Sandig V., Jennings G., Rudolph M., Schlag P., and Strauss M. Efficient gene transfer into human hepatocytes by baculovirus vectors. PNAS 92 (1995) 10099-10103
39. Hunt I. From gene to protein: a review of new and enabling technologies for multi-parallel protein expression. Protein Expr. Purif. 40 (2005) 1-22
40. Ishihara G., Goto M., Saeki M., Ito K., Hori T., Kigawa T., Shirouzu M., and Yokoyama S. Expression of G protein coupled receptors in a cell-free translational system using detergents and thioredoxin-fusion vectors. Protein Expr. Purif. 41 (2005) 27-37
41. Ivanova L., Brandli J., Saudan P., and Bachmann M.F. Hybrid Sindbis/Epstein-Barr virus episomal expression vector for inducible production of proteins. Biotechniques 39 (2005) 209-212
42. Janssen J.J., Bovee-Geurts P.H., Merkx M., and DeGrip W.J. Histidine tagging both allows convenient single-step purification of bovine rhodopsin and exerts ionic strength-dependent effects on its photochemistry. J. Biol. Chem. 270 (1995) 11222-11229
43. Janssen J.J., van de Ven W.J., van Groningen-Luyben W.A., Roosien J., Vlak J.M., and de Grip W.J. Synthesis of functional bovine opsin in insect cells under control of the baculovirus polyhedrin promoter. Mol. Biol. Rep. 13 (1988) 65-71
44. Je Y.H., Chang J.H., Choi J.Y., Roh J.Y., Jin B.R., O'Reilly D., and Kang S.K. A defective viral genome maintained in Escherichia Coli for the generation of baculovirus expression vectors. Biotechnol. Lett. 23 (2001) 575-582
45. Jidenko M., Nielsen R.C., Sorensen T.L., Moller J.V., le Maire M., Nissen P., and Jaxel C. Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. PNAS 102 (2005) 11687-11691
46. Jones J., Nivitchanyong T., Giblin C., Ciccarone V., Judd D., Gorfien S., Krag S.S., and Betenbaugh M.J. Optimization of tetracycline-responsive recombinant protein production and effect on cell growth and ER stress in mammalian cells. Biotechnol. Bioeng. 91 (2005) 722-732
47. Karlsson M., Fotiadis D., Sjovall S., Johansson I., Hedfalk K., Engel A., and Kjellbom P. Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett. 537 (2003) 68-72
48. Kiselyov K., Shin D.M., Kim J.Y., Yuan J.P., and Muallem S. TRPC channels: interacting proteins. Handb. Exp. Pharmacol. (2007) 559-574
49. + channels in a baculovirus-infected insect cell line. Neuron 5 (1990) 221-226
50. Klammt, C., Srivastava, A., Eifler, N., Junge, F., Beyermann, M., Schwarz, D., Michel, H., Doetsch, V., Bernhard, F., 2007. Functional analysis of cell-free-produced human endothelin B receptor reveals transmembrane segment 1 as an essential area for ET-1 binding and homodimer formation. FEBS J. doi:10.1111/j.1742-4658.2007.05854.x.
51. Kost T.A., Condreay J.P., and Jarvis D.L. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat. Biotechnol. 23 (2005) 567-575
52. Kost T.A., Ignar D.M., Clay W.C., Andrews J., Leray J.D., Overton L., Hoffman C.R., Kilpatrick K.E., Ellis B., and Emerson D.L. Production of a urokinase plasminogen activator-IgG fusion protein (uPA-IgG) in the baculovirus expression system. Gene 190 (1997) 139-144
53. Kunji E.R., Slotboom D.J., and Poolman B. Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim. Biophys. Acta 1610 (2003) 97-108
54. Lee A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666 (2004) 62-87
55. 2+-ATPase. Biochim. Biophys. Acta 1560 (2002) 67-83
56. Liguori L., Marques B., Villegas-Mendez A., Rothe R., and Lenormand J.L. Production of membrane proteins using cell-free expression systems. Expert Rev. Proteomics 4 (2007) 79-90
57. Lipscomb M.L., Mowry M.C., and Kompala D.S. Production of a secreted glycoprotein from an inducible promoter system in a perfusion bioreactor. Biotechnol. Prog. 20 (2004) 1402-1407
58. Liu J., and Rost B. Comparing function and structure between entire proteomes. Protein Sci. 10 (2001) 1970-1979
59. Locher K.P., Lee A.T., and Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296 (2002) 1091-1098
60. + channel. Science 309 (2005) 897-903
61. Luckow V.A., and Summers M.D. Signals important for high-level expression of foreign genes in Autographa californica nuclear polyhedrosis virus expression vectors. Virology 167 (1988) 56-71
62. Lundstrom K. Semliki Forest virus vectors for rapid and high-level expression of integral membrane proteins. Biochim. Biophys. Acta 1610 (2003) 90-96
63. Lundstrom K. Structural genomics for membrane proteins. Cell. Mol. Life Sci. 63 (2006) 2597-2607
64. Lundstrom K., Wagner R., Reinhart C., Desmyter A., Cherouati N., Magnin T., Zeder-Lutz G., Courtot M., Prual C., Andre N., Hassaine G., Michel H., Cambillau C., and Pattus F. Structural genomics on membrane proteins: comparison of more than 100 GPCRs in 3 expression systems. J. Struct. Funct. Genomics 7 (2006) 77-91
65. Madden D.R. The structure and function of glutamate receptor ion channels. Nat. Rev. Neurosci. 3 (2002) 91-101
66. Madden D.R., Abele R., Andersson A., and Keinänen K. Large-scale expression and thermodynamic characterization of a glutamate receptor agonist-binding domain. Eur. J. Biochem. 267 (2000) 4281-4289
67. Mancia F., Patel S.D., Rajala M.W., Scherer P.E., Nemes A., Schieren I., Hendrickson W.A., and Shapiro L. Optimization of protein production in mammalian cells with a coexpressed fluorescent marker. Structure 12 (2004) 1355-1360
68. Mollaaghababa R., Davidson F.F., Kaiser C., and Khorana H.G. Structure and function in rhodopsin: expression of functional mammalian opsin in Saccharomyces cerevisiae. PNAS 93 (1996) 11482-11486
69. Monne M., Chan K.W., Slotboom D.J., and Kunji E.R. Functional expression of eukaryotic membrane proteins in Lactococcus lactis. Protein Sci. 14 (2005) 3048-3056
70. Neddermann P., Gargioli C., Muraglia E., Sambucini S., Bonelli F., De Francesco R., and Cortese R. A novel, inducible, eukaryotic gene expression system based on the quorum-sensing transcription factor TraR. EMBO Rep. 4 (2003) 159-165
71. Nussberger S., Dorr K., Wang D.N., and Kühlbrandt W. Lipid-protein interactions in crystals of plant light-harvesting complex. J. Mol. Biol. 234 (1993) 347-356
72. O'Reilly D., Miller L.K., and Luckow V.A. Baculovirus Expression Vectors A Laboratory Manual (1992), Oxford University Press, New York
73. Oprian D.D., Molday R.S., Kaufman R.J., and Khorana H.G. Expression of a synthetic bovine rhodopsin gene in monkey kidney cells. PNAS 84 (1987) 8874-8878
74. Orlean P. Biogenesis of yeast wall and surface components. In: Pringle J.R., Broach J.R., and Jones E.W. (Eds). The Molecular and Cellular Biology of the Yeast Saccharomyces: Cell Cycle and Cell Biology vol. 3 (1997), Cold Spring Harbor Press, NY 229-362
75. Pajot-Augy E., Bozon V., Remy J.J., Couture L., and Salesse R. Critical relationship between glycosylation of recombinant lutropin receptor ectodomain and its secretion from baculovirus-infected insect cells. Eur. J. Biochem. 260 (1999) 635-648
76. Palanivelu D.V., Kozono D.E., Engel A., Suda K., Lustig A., Agre P., and Schirmer T. Co-axial association of recombinant eye lens aquaporin-0 observed in loosely packed 3D crystals. J. Mol. Biol. 355 (2006) 605-611
77. 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., and Miyano M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000) 739-745
78. + channels heterologously expressed in Pichia pastoris. J. Mol. Biol. 333 (2003) 103-116
79. ATP channel expression in mammalian cells utilizing recombinant baculovirus transduction. Receptors Channels 8 (2002) 99-111
80. Pham P.L., Perret S., Cass B., Carpentier E., St-Laurent G., Bisson L., Kamen A., and Durocher Y. Transient gene expression in HEK293 cells: peptone addition posttransfection improves recombinant protein synthesis. Biotechnol. Bioeng. 90 (2005) 332-344
81. Pham P.L., Perret S., Doan H.C., Cass B., St-Laurent G., Kamen A., and Durocher Y. 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
82. Philipps B., Rotmann D., Wicki M., Mayr L.M., and Forstner M. Time reduction and process optimization of the baculovirus expression system for more efficient recombinant protein production in insect cells. Protein Expr. Purif. 42 (2005) 211-218
83. Raunser S., Haase W., Bostina M., Parcej D.N., and Kuhlbrandt W. High-yield expression, reconstitution and structure of the recombinant, fully functional glutamate transporter GLT-1 from Rattus norvegicus. J. Mol. Biol. 351 (2005) 598-613
84. Reeves P.J., Thurmond R.L., and Khorana H.G. Structure and function in rhodopsin: high level expression of a synthetic bovine opsin gene and its mutants in stable mammalian cell lines. PNAS 93 (1996) 11487-11492
85. Roosild T.P., Greenwald J., Vega M., Castronovo S., Riek R., and Choe S. NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307 (2005) 1317-1321
86. Rosenbusch J.P. Stability of membrane proteins: relevance for the selection of appropriate methods for high-resolution structure determinations. J. Struct. Biol. 136 (2001) 144-157
87. Sarramegna V., Talmont F., Demange P., and Milon A. Heterologous expression of G-protein-coupled receptors: comparison of expression systems from the standpoint of large-scale production and purification. Cell. Mol. Life Sci. 60 (2003) 1529-1546
88. Scanlon S.M., Williams D.C., and Schloss P. Membrane cholesterol modulates serotonin transporter activity. Biochemistry 40 (2001) 10507-10513
89. Scott M.J., Modha S.S., Rhodes A.D., Broadway N.M., Hardwicke P.I., Zhao H.J., Kennedy-Wilson K.M., Sweitzer S.M., and Martin S.L. Efficient expression of secreted proteases via recombinant BacMam virus. Protein Expr. Purif. 52 (2007) 104-116
90. Seddon A.M., Curnow P., and Booth P.J. Membrane proteins, lipids and detergents: not just a soap opera. Biochim. Biophys. Acta 1666 (2004) 105-117
91. Seth G., Hossler P., Yee J.C., and Hu W.S. Engineering cells for cell culture bioprocessing-physiological fundamentals. Adv. Biochem. Eng. Biotechnol. 101 (2006) 119-164
92. Shamotienko O., Akhtar S., Sidera C., Meunier F.A., Ink B., Weir M., and Dolly J.O. Recreation of neuronal Kv1 channel oligomers by expression in mammalian cells using Semliki Forest virus. Biochemistry 38 (1999) 16766-16776
93. + channel surface expression through effects early in biosynthesis. Neuron 16 (1996) 843-852
94. Shoji I., Aizaki H., Tani H., Ishii K., Chiba T., Saito I., Miyamura T., and Matsuura Y. Efficient gene transfer into various mammalian cells, including non-hepatic cells, by baculovirus vectors. J. Gen. Virol. 78 Pt. 10 (1997) 2657-2664
95. Smith G.E., Summers M.D., and Fraser M.J. Production of human beta interferon in insect cells infected with a baculovirus expression vector. Mol. Cell. Biol. 3 (1983) 2156-2165
96. Sokolova O., Kolmakova-Partensky L., and Grigorieff N. Three-dimensional structure of a voltage-gated potassium channel at 2.5 nm resolution. Structure 9 (2001) 215-220
97. Standfuss J., Xie G., Edwards P.C., Burghammer M., Oprian D.D., and Schertler G.F.X. Crystal Structure of a thermally stable rhodopsin mutant. J. Mol. Biol. (2007) 10.1016/j.jmb.2007.03.007
98. Stock D., Leslie A.G., and Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science 286 (1999) 1700-1705
99. Tate C.G. Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett. 504 (2001) 94-98
100. Tate C.G., Haase J., Baker C., Boorsma M., Magnani F., Vallis Y., and Williams D.C. Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim. Biophys. Acta 1610 (2003) 141-153
101. Toyoshima C., Nakasako M., Nomura H., and Ogawa H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405 (2000) 647-655
102. Tucker J., and Grisshammer R. Purification of a rat neurotensin receptor expressed in Escherichia coli. Biochem. J. 317 Pt. 3 (1996) 891-899
103. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., and Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 439 (2006) 688-694
104. Unger V.M., Kumar N.M., Gilula N.B., and Yeager M. Three-dimensional structure of a recombinant gap junction membrane channel. Science 283 (1999) 1176-1180
105. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J. Mol. Biol. 346 (2005) 967-989
106. Wagner S., Bader M.L., Drew D., and de Gier J.W. Rationalizing membrane protein overexpression. Trends Biotechnol. 24 (2006) 364-371
107. Wang Z., Stalcup L.D., Harvey B.J., Weber J., Chloupkova M., Dumont M.E., Dean M., and Urbatsch I.L. Purification and ATP hydrolysis of the putative cholesterol transporters ABCG5 and ABCG8. Biochemistry 45 (2006) 9929-9939
108. Weber W., Rimann M., Spielmann M., Keller B., Daoud-El Baba M., Aubel D., Weber C.C., and Fussenegger M. Gas-inducible transgene expression in mammalian cells and mice. Nat. Biotechnol. 22 (2004) 1440-1444
109. Weber W., Weber E., Geisse S., and Memmert K. Optimisation of protein expression and establishment of the Wave Bioreactor for Baculovirus/insect cell culture. Cytotechnology 38 (2002) 77-85
110. Weiss H.M., and Grisshammer R. Purification and characterization of the human adenosine A(2a) receptor functionally expressed in Escherichia coli. Eur. J. Biochem. 269 (2002) 82-92
111. Werner N.S., Weber W., Fussenegger M., and Geisse S. A gas-inducible expression system in HEK.EBNA cells applied to controlled proliferation studies by expression of p27(Kip1). Biotechnol. Bioeng. 96 (2007) 1155-1166
112. White S.H. The progress of membrane protein structure determination. Protein Sci. 13 (2004) 1948-1949
113. Wiener M.C. A pedestrian guide to membrane protein crystallization. Methods 34 (2004) 364-372
114. Zhang H., Kurisu G., Smith J.L., and Cramer W.A. A defined protein-detergent-lipid complex for crystallization of integral membrane proteins: the cytochrome b6f complex of oxygenic photosynthesis. PNAS 100 (2003) 5160-5163
115. Zhang L., Wu G., Tate C.G., Lookene A., and Olivecrona G. Calreticulin promotes folding/dimerization of human lipoprotein lipase expressed in insect cells (Sf21). J. Biol. Chem. 278 (2003) 29344-29351
116. Zhao Y., Chapman D.A., and Jones I.M. Improving baculovirus recombination. Nucleic Acids Res. 31 (2003) e6
117. Zhuang J., Prive G.G., Werner G.E., Ringler P., Kaback H.R., and Engel A. Two-dimensional crystallization of Escherichia coli lactose permease. J. Struct. Biol. 125 (1999) 63-75