Functional expression of mammalian receptors and membrane channels in different cells

Journal of Structural Biology

Volumn 159, Issue 2 SPEC. ISS., 2007, Pages 179-193

  Eifler, Nora ^a   Duckely, Myriam ^a   Sumanovski, Lazar T ^a   Egan, Terrance M ^b   Oksche, Alexander ^c   Konopka, James B ^d   Lüthi, Anita ^a   Engel, Andreas ^a   Werten, Paul J L ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

Eukaryotic expression systems; Membrane protein expression; Protein activity; Protein localization; Protein solubility

Indexed keywords

MEMBRANE PROTEIN; MEMBRANE RECEPTOR;

ANIMAL CELL; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; BIOLOGICAL ACTIVITY; CELL STRAIN; CELL STRAIN BHK; CELL STRAIN COS7; CELL STRAIN HEK293; CHO CELL; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; EUKARYOTE; GENE EXPRESSION SYSTEM; HELA CELL; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; INSECT CELL; MAMMAL CELL; MEMBRANE CHANNEL; MOUSE; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN QUALITY; SEMLIKI FOREST ALPHAVIRUS; SOLUBILITY; YEAST;

EUKARYOTA; MAMMALIA; RABBIT FIBROMA VIRUS; SEMLIKI FOREST VIRUS;

EID: 34447645086     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.01.014     Document Type: Article

References (74)

1. Agre P., King L.S., Yasui M., Guggino W.B., Ottersen O.P., Fujiyoshi Y., Engel A., and Nielsen S. Aquaporin water channels-from atomic structure to clinical medicine. J. Physiol. 542 (2002) 3-16
2. 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
3. André N., Cherouati N., Prual C., Steffan T., Zeder-Lutz G., Magnin T., Pattus F., Michel H., Wagner R., and Reinhart C. Enhancing functional production of G protein-coupled receptors in Pichia pastoris to levels required for structural studies via a single expression screen. Protein Sci. 15 (2006) 1115-1126
4. Barbuti A., Gravante B., Riolfo M., Milanesi R., Terragni B., and DiFrancesco D. Localization of pacemaker channels in lipid rafts regulates channel kinetics. Circ. Res. 94 (2004) 1325-1331
5. Borgnia M., Nielsen S., Engel A., and Agre P. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68 (1999) 425-458
6. David N.E., Gee M., Andersen B., Naider F., Thorner J., and Stevens R.C. Expression and purification of the Saccharomyces cerevisiae alpha-factor receptor (Ste2p), a 7-transmembrane-segment G protein-coupled receptor. J. Biol. Chem. 272 (1997) 15553-15561
7. de Ruyter P.G.G.A., Kuipers O.P., and de Vos W.M. Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl. Environ. Microbiol. 62 (1996) 3662-3667
8. DiFrancesco D. Characterization of single pacemaker channels in cardiac sino-atrial node cells. Nature 324 (1986) 470-473
9. Ding S., and Sachs F. Single channel properties of P2X2 purinoceptors. J. Gen. Physiol. 113 (1999) 695-720
10. Dohlman H.G., and Thorner J.W. Regulation of G protein-initiated signal transduction in yeast: paradigms and principles. Annu. Rev. Biochem. 70 (2001) 703-754
11. Dolby V., Collen A., Lundqvist A., and Cronet P. Overexpression and functional characterisation of the human melanocortin 4 receptor in Sf9 cells. Protein Expr. Purif. 37 (2004) 455-461
12. Drew D., Slotboom D.-J., Friso G., Reda T., Genevaux P., Rapp M., Meindl-Beinker N.M., Lambert W., Lerch M., Daley D.O., van Wijk K.-J., Hirst J., Kunji E.R.S., and de Gier J.-W. A scalable, GFP-based pipeline for membrane protein overexpression screening and purification. Protein Sci. 14 (2005) 2011-2017
13. Duvernay M.T., Filipeanu C.M., and Wu G. The regulatory mechanisms of export trafficking of G protein-coupled receptors. Cell Signal. 17 (2005) 1457-1465
14. Egan T.M., and Khakh B.S. Contribution of calcium ions to P2X channel responses. J. Neurosci. 24 (2004) 3413-3420
15. Eroglu C., Cronet P., Panneels V., Beaufils P., and Sinning I. Functional reconstitution of purified metabotropic glutamate receptor expressed in the fly eye. EMBO Rep. 3 (2002) 491-496
16. Farrens D.L., Altenbach C., Yang K., Hubbell W.L., and Khorana H.G. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274 (1996) 768-770
17. Frankland S., Adisa A., Horrocks P., Taraschi T.F., Schneider T., Elliott S.R., Rogerson S.J., Knuepfer E., Cowman A.F., Newbold C.I., and Tilley L. Delivery of the malaria virulence protein PfEMP1 to the erythrocyte surface requires cholesterol-rich domains. Eukaryot. Cell 5 (2006) 849-860
18. Frère S.G.A., Kuisle M., and Lüthi A. Regulation of recombinant and native hyperpolarization-activated cation channels. Mol. Neurobiol. 30 (2004) 279-305
19. Giniger E., Varnum S.M., and Ptashne M. Specific DNA binding of GAL4, a positive regulatory protein of yeast. Cell 40 (1985) 767-774
20. 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
21. Hasslacher M., Schall M., Hayn M., Bona R., Rumbold K., Lückl J., Griengl H., Kohlwein S.D., and Schwab H. High-level intracellular expression of hydroxynitrile lyase from the tropical rubber tree Hevea brasiliensis in microbial hosts. Protein Expr. Purif. 11 (1997) 61-71
22. He Q., Schlich T., Paulsen H., and Vermaas W. Expression of a higher plant light-harvesting chlorophyll a/b-binding protein in Synechocystis sp. PCC 6803. Eur. J. Biochem. 263 (1999) 561-570
23. Heymann J.B., and Engel A. Aquaporins: phylogeny, structure, and physiology of water channels. News Physiol. Sci. 14 (1999) 187-193
24. Hollien J., and Weissman J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 (2006) 104-107
25. Hu Y.C. Baculovirus as a highly efficient expression vector in insect and mammalian cells. Acta Pharmacol. Sin. 26 (2005) 405-416
26. Innamorati G., Sadeghi H., Eberle A.N., and Birnbaumer M. Phosphorylation of the V2 vasopressin receptor. J. Biol. Chem. 272 (1997) 2486-2492
27. Jenness D.D., Burkholder A.C., and Hartwell L.H. Binding of alpha-factor pheromone to Saccharomyces cerevisiae a cells: dissociation constant and number of binding sites. Mol. Cell Biol. 6 (1986) 318-320
28. Jidenko M., Nielsen R.C., Sørensen T.L.-M., Møller J.V., le Maire M., Nissen P., and Jaxel C. Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102 (2005) 11687-11691
29. Karlsson M., Fotiadis D., Sjövall 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
30. Kempf J., Snook L.A., Vonesch J.-L., Dahms T.E.S., Pattus F., and Massotte D. Expression of the human mu opioid receptor in a stable Sf9 cell line. J. Biotechnol. 95 (2002) 181-187
31. Khakh B.S., and North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442 (2006) 527-532
32. Klaassen C.H.W., Bovee-Geurts P.H.M., de Caluwé G.L.J., and de Grip W.J. Large-scale production and purification of functional recombinant bovine rhodopsin with the use of the baculovirus expression system. Biochem. J. 342 Pt. 2 (1999) 293-300
33. Konopka J.B., Margarit S.M., and Dube P. Mutation of Pro-258 in transmembrane domain 6 constitutively activates the G protein-coupled alpha-factor receptor. Proc. Natl. Acad. Sci. USA 93 (1996) 6764-6769
34. 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
35. Kukulski W., Schenk A.D., Johanson U., Braun T., de Groot B.L., Fotiadis D., Kjellbom P., and Engel A. The 5Å structure of heterologously expressed plant aquaporin SoPIP2;1. J. Mol. Biol. 350 (2005) 611-616
36. Kunji E.R.S., Slotboom D.-J., and Poolman B. Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim. Biophys. Acta 1610 (2003) 97-108
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
38. Lagane B., Gaibelet G., Meilhoc E., Masson J.-M., Cézanne L., and Lopez A. Role of sterols in modulating the human mu-opioid receptor function in Saccharomyces cerevisiae. J. Biol. Chem. 275 (2000) 33197-33200
39. Lee B.K., Khare S., Naider F., and Becker J.M. Identification of residues of the Saccharomyces cerevisiae G protein-coupled receptor contributing to alpha-factor pheromone binding. J. Biol. Chem. 276 (2001) 37950-37961
40. Lenoir G., Menguy T., Corre F., Montigny C., Pedersen P.A., Thinès D., le Maire M., and Falson P. Overproduction in yeast and rapid and efficient purification of the rabbit SERCA1a Ca(2+)-ATPase. Biochim. Biophys. Acta 1560 (2002) 67-83
41. Liljestrom P., and Garoff H. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (NY) 9 (1991) 1356-1361
42. Liu K., Kozono D., Kato Y., Agre P., Hazama A., and Yasui M. Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution. Proc. Natl. Acad. Sci. USA 102 (2005) 2192-2197
43. Lu M., Echeverri F., and Moyer B.D. Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic 4 (2003) 416-433
44. Luckow V.A. Baculovirus systems for the expression of human gene products. Curr. Opin. Biotechnol. 4 (1993) 564-572
45. Lundstrom K. Semliki Forest virus vectors for large-scale production of recombinant proteins. Methods Mol. Med. 76 (2003) 525-543
46. 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 2 (2006) 77-91
47. Makuc J., Cappellaro C., and Boles E. Co-expression of a mammalian accessory trafficking protein enables functional expression of the rat MCT1 monocarboxylate transporter in Saccharomyces cerevisiae. FEMS Yeast Res. 4 (2004) 795-801
48. Marquardt T., and Helenius A. Misfolding and aggregation of newly synthesized proteins in the endoplasmic reticulum. J. Cell Biol. 117 (1992) 505-513
49. Menzel R., Vogel F., Kärgel E., and Schunck W.-H. Inducible membranes in yeast: relation to the unfolded-protein-response pathway. Yeast 13 (1997) 1211-1229
50. Monné M., Chan K.W., Slotboom D.-J., and Kunji E.R.S. Functional expression of eukaryotic membrane proteins in Lactococcus lactis. Protein Sci. 14 (2005) 3048-3056
51. O'Reilly D.R., Miller L.K., and Luckow V.A. Baculovirus Expression Vectors: A Laboratory Manual (1988), W.H. Freeman, New York
52. Oksche A., Leder G., Valet S., Platzer M., Hasse K., Geist S., Krause G., Rosenthal A., and Rosenthal W. Variant amino acids in the extracellular loops of murine and human vasopressin V2 receptors account for differences in cell surface expression and ligand affinity. Mol. Endocrinol. 16 (2002) 799-813
53. Oshima A., Doi T., Mitsuoka K., Maeda S., and Fujiyoshi Y. Roles of Met-34, Cys-64, and Arg-75 in the assembly of human connexin 26. Implication for key amino acid residues for channel formation and function. J. Biol. Chem. 278 (2003) 1807-1816
54. Pausch M.H. G-protein-coupled receptors in Saccharomyces cerevisiae: high-throughput screening assays for drug discovery. Trends Biotechnol. 15 (1997) 487-494
55. Puri N., and Roche P.A. Ternary SNARE complexes are enriched in lipid rafts during mast cell exocytosis. Traffic 7 (2006) 1482-1494
56. Ratnala V.R.P., Swarts H.G.P., van Oostrum J., Leurs R., de Groot H.J.M., Bakker R.A., and de Grip W.J. Large-scale overproduction, functional purification and ligand affinities of the His-tagged human histamine H1 receptor. Eur. J. Biochem. 271 (2004) 2636-2646
57. Robben J.H., Knoers N.V.A.M., and Deen P.M.T. Regulation of the vasopressin V2 receptor by vasopressin in polarized renal collecting duct cells. Mol. Biol. Cell 15 (2004) 5693-5699
58. Robinson R.B., and Siegelbaum S.A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65 (2003) 453-480
59. Sadeghi H., Robertson G.L., Bichet D.G., Innamorati G., and Birnbaumer M. Biochemical basis of partial nephrogenic diabetes insipidus phenotypes. Mol. Endocrinol. 11 (1997) 1806-1813
60. Sarramegna V., Muller I., Mousseau G., Froment C., Monsarrat B., Milon A., and Talmont F. Solubilization, purification, and mass spectrometry analysis of the human mu-opioid receptor expressed in Pichia pastoris. Protein Expr. Purif. 43 (2005) 85-93
61. Shukla A.K., Reinhart C., and Michel H. Comparative analysis of the human angiotensin II type 1a receptor heterologously produced in insect cells and mammalian cells. Biochem. Biophys. Res. Commun. 349 (2006) 6-14
62. Shusta E.V., Raines R.T., Plückthun A., and Wittrup K.D. Increasing the secretory capacity of Saccharomyces cerevisiae for production of single-chain antibody fragments. Nat. Biotechnol. 16 (1998) 773-777
63. Stauffer K.A., Kumar N.M., Gilula N.B., and Unwin N. Isolation and purification of gap junction channels. J. Cell Biol. 115 (1991) 141-150
64. Surade S., Klein M., Stolt-Bergner P.C., Muenke C., Roy A., and Michel H. Comparative analysis and "expression space" coverage of the production of prokaryotic membrane proteins for structural genomics. Protein Sci. 15 (2006) 2178-2189
65. Swillens S. How to estimate the total receptor concentration when the specific radioactivity of the ligand is unknown. Trends Pharmacol. Sci. 13 (1992) 430-434
66. Tate C.G. Baculovirus-mediated expression of neurotransmitter transporters. Methods Enzymol. 296 (1998) 443-455
67. 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
68. 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 7077 (2006) 688-694
69. Uozumi N. Escherichia coli as an expression system for K(+) transport systems from plants. Am. J. Physiol. Cell Physiol. 281 (2001) C733-C739
70. Valkonen M., Penttila M., and Saloheimo M. Effects of inactivation and constitutive expression of the unfolded-protein response pathway on protein production in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 69 (2003) 2065-2072
71. Werten P.J.L., Hasler L., Koenderink J.B., Klaassen C.H.W., de Grip W.J., Engel A., and Deen P.M.T. Large-scale purification of functional recombinant human aquaporin-2. FEBS Lett. 504 (2001) 200-205
72. Yasui M., Hazama A., Kwon T.H., Nielsen S., Guggino W.B., and Agre P. Rapid gating and anion permeability of an intracellular aquaporin. Nature 402 (1999) 184-187
73. Yin D., Gavi S., Shumay E., Duell K., Konopka J.B., Malbon C.C., and Wang H.Y. Successful expression of a functional yeast G-protein-coupled receptor (Ste2) in mammalian cells. Biochem. Biophys. Res. Commun. 329 (2005) 281-287
74. Zhang K., and Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66 2 Suppl. 1 (2006) S102-S109