Enhancing functional production of G protein-coupled receptors in Pichia pastoris to levels required for structural studies via a single expression screen

Protein Science

Volumn 15, Issue 5, 2006, Pages 1115-1126

  André, Nicolas ^a   Cherouati, Nadia ^b   Prual, Cécile ^a   Steffan, Tania ^b   Zeder Lutz, Gabrielle ^b   Magnin, Thierry ^b   Pattus, Franc ^b   Michel, Hartmut ^a   Wagner, Renaud ^b   Reinhart, Christoph ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Binding assay; Expression screening; G protein coupled receptor; GPCR; Optimization; Pichia pastoris

Indexed keywords

DIMETHYL SULFOXIDE; G PROTEIN COUPLED RECEPTOR; HISTIDINE;

AMINO ACID SEQUENCE; ARTICLE; BINDING ASSAY; CONTROLLED STUDY; CULTURE MEDIUM; FUNGUS GROWTH; LIGAND BINDING; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; TEMPERATURE; YEAST;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION; IMMUNOBLOTTING; KINETICS; LIGANDS; MOLECULAR SEQUENCE DATA; PICHIA; PROTEIN BINDING; RADIOLIGAND ASSAY; RECEPTORS, G-PROTEIN-COUPLED; TISSUE CULTURE TECHNIQUES;

FUNGI; MAMMALIA; PICHIA; PICHIA PASTORIS;

EID: 33646155331     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062098206     Document Type: Article

References (52)

1. Akermoun, M., Koglin, M., Zvalova-Iooss, D., Folschweiller, N., Dowell, S.J., and Gearing, K.L. 2005. Characterization of 16 human G protein-coupled receptors expressed in baculovirus-infected insect cells. Protein Expr. Purif. 44: 65-74.
2. Audinot, V., Newman-Tancredi, A., Cussac, D., and Milla, N.M.J. 2001. Inverse agonist properties of antipsychotic agents at cloned, human (h) serotonin (5-HT)(1B) and h5-HT(1D) receptors. Neuropsychopharmacology 25: 410-422.
3. Befort, K., Tabbara, L., Kling, D., Maigret, B., and Kieffer, B.L. 1996. Role of aromatic transmembrane residues of the δ-opioid receptor in ligand recognition. J. Biol. Chem. 271: 10161-10168.
4. Bernier, V., Bichet, D.G., and Bouvier, M. 2004. Pharmacological chaperon action on G-protein-coupled receptors. Curr. Opin. Pharmacol. 4: 528-533.
5. Bockaert, J. and Pin, J.P. 1999. Molecular tinkering of G protein-coupled receptors: An evolutionary success. EMBO J. 18: 1723-1729.
6. Boettner, M., Prinz, B., Holz, C., Stahl, U., and Lang, C. 2002. High-throughput screening for expression of heterologous proteins in the yeast Pichia pastoris. J. Biotechnol. 99: 51-62.
7. Cabrele, C., Wieland, H.A., Langer, M., Stidsen, C.E., and Beck-Sickinger, A.G. 2001. Y-receptor affinity modulation by the design of pancreatic polypeptide/neuropeptide Y chimera led to Y(5)-receptor ligands with picomolar affinity. Peptides 22: 365-378.
8. Domenech, T., Beleta, J., and Palacios, J.M. 1997. Characterization of human serotonin 1D and 1B receptors using [3H]-GR-125743, a novel radiolabelled serotonin 5HT1D/1B receptor antagonist. Naunyn Schmiedebergs Arch. Pharmacol. 356: 328-334.
9. Drew, D., Froderberg, L., Baars, L., and de Gier, J.W. 2003. Assembly and overexpression of membrane proteins in Escherichia coli. Biochim. Biophys. Acta 1610: 3-10.
10. Grisshammer, R., Little, J., and Aharony, D. 1994. Expression of rat NK-2 (neurokinin A) receptor in E. coli. Receptors Channels 2: 295-302.
11. Grünewald, S., Haase, W., Molsberger, E., Michel, H., and Reiländer, H. 2004. Production of the human D2S receptor in the methylotrophic yeast. P. pastoris. Recept. Channels 10: 37-50.
12. Hill, P., Lai, Y., Hnilo, J., Lin, C.C., Karla, M., Bounds, S., Herz, J., and Mitchell, R. 1996. Cloning, expression, and comparison of the binding characteristics of the known human dopamine receptors. Adv. Neurol. 69: 41-52.
13. Homma, T., Iwahashi, H., and Komatsu, Y. 2003. Yeast gene expression during growth at low temperature. Cryobiology 46: 230-237.
14. Hong, F., Meinander, N.Q., and Jonsson, L.J. 2002. Fermentation strategies for improved heterologous expression of laccase in Pichia pastoris. Biotechnol. Bioeng. 79: 438-449.
15. Inouye, M., and Phadtare, S. 2004. Cold shock response and adaptation at nearfreezing temperature in microorganisms. Sci. STKE 237: pe26.
16. Ivanovic, A. 2001. "Klonierung rekombinanter Histamin H1-rezeptoren und deren charakterisierung; solubilisierung und reinigung nach heterologer produktion." Ph.D. thesis, Johann-Wolfgang-Goethe-Universität, Frankfurt am Main, Germany.
17. Jahic, M., Gustavsson, M., Jansen, A.K., Martinelle, M., and Enfors, S.O. 2003a. Analysis and control of proteolysis of a fusion protein in Pichia pastoris fed-batch processes. J. Biotechnol. 102: 45-53.
18. Jahic, M., Wallberg, F., Bollok, M., Garcia, P., and Enfors, S.O. 2003b. Temperature limited fed-batch technique for control of proteolysis in Pichia pastoris bioreactor cultures. Microb. Cell Fact. 18: 6.
19. King, K., Dohlman, H.G., Thorner, J., Caron, M.G., and Lefkowitz, R.J. 1990. Control of yeast mating signal transduction by a mammalian β 2-adrenergic receptor and Gs α subunit. Science 250: 121-123 [Erratum: Science 1991 251: 144].
20. Klabunde, T. and Hessler, G. 2002. Drug design strategies for targeting G-protein-coupled receptors. ChemBioChem 3: 928-944.
21. Koganesawa, N., Aizawa, T., Shimojo, H., Miura, K., Ohnishi, A., Demura, M., Hayakawa, Y., Nitta, K., and Kawano, K. 2002. Expression and purification of a small cytokine growth-blocking peptide from armyworm Pseudaletia separata by an optimized fermentation method using the methylotrophic yeast Pichia pastoris. Protein Expr. Purif. 25: 416-425.
22. Kuhn, P., Wilson, K., Patch, M.G., and Stevens, R.C. 2002. The genesis of highthroughput structure-based drug discovery using protein crystallography. Curr. Opin. Chem. Biol. 6: 704-710.
23. Leurs, R., Smit, M.J., Menge, W.M., and Timmerman, H. 1994. Pharmacological characterization of the human histamine H2 receptor stably expressed in Chinese hamster ovary cells. Br. J. Pharmacol. 112: 847-854.
24. Li, J., Edwards, P.C., Burghammer, M., Villa, C., and Schertler, G.F. 2004. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343: 1409-1438.
25. Lundstrom, K. 2003. Semliki Forest virus vectors for rapid and high-level expression of integral membrane proteins. Biochim. Biophys. Acta 1610: 90-96.
26. _. 2005. Structural genomics of GPCRs. Trends Biotechnol. 23: 103-108.
27. Lundstrom, K., Hawcock, A.B., Vargas, A., Ward, P., Thomas, P., and Naylor, A. 1997. Effect of single point mutations of the human tachykinin NK1 receptor on antagonist affinity. Eur. J. Pharmacol. 337: 73-81.
28. Massotte, D. 2003. G protein-coupled receptor overexpression with the baculovirus-insect cell system: A tool for structural and functional studies. Biochim. Biophys. Acta 1610: 77-89.
29. Millan, M.J., Newman-Tancredi, A., Audinot, V., Cussac, D., Lejeune, F., Nicolas, J.P., Coge, F., Galizzi, J.P., Boutin, J.A., Rivet, J.M., et al. 2000. Agonist and antagonist actions of yohimbine as compared to fluparoxan at α(2)-adrenergic receptors (AR)s, serotonin (5-HT)(1A), 5-HT(1B), 5-HT(1D) and dopamine D(2) and D(3) receptors. Significance for the modulation of frontocortical monoaminergic transmission and depressive states. Synapse 35: 79-95.
30. Murakami, K., Onoda, Y., Kimura, J., and Yoshino, M. 1997. Protection by histidine against oxidative inactivation of AMP deaminase in yeast. Biochem. Mol. Biol. Int. 42: 1063-1069.
31. Murata, Y., Watanabe, T., Sato, M., Momose, Y., Nakahara, T., Oka, S., and Iwahashi, H. 2003. Dimethyl sulfoxide exposure facilitates phospholipid biosynthesis and cellular membrane proliferation in yeast cells. J. Biol. Chem. 278: 33185-33193.
32. Opekarová, M. and Tanner, W. 2003. Specific lipid requirements of membrane proteins - a putative bottleneck in heterologous expression. Biochim. Biophys. Acta 1160: 11-22.
33. Oury-Donat, F., Carayon, P., Thurneyssen, O., Pailhon, V., Emonds-Alt, X., Soubrie, P., and Le Fur, G. 1995. Functional characterization of the nonpeptide neurokinin3 (NK3) receptor antagonist, SR142801 on the human NK3 receptor expressed in Chinese hamster ovary cells. J. Pharmacol. Exp. Ther. 274: 148-154.
34. 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., et al. 2000. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289: 739-745.
35. Parker, E.M., Babij, C.K., Balasubramaniam, A., Burrier, R.E., Guzzi, M., Hamud, F., Mukhopadhyay, G., Rudinski, M.S., Tao, Z., Tice, M., et al. 1998. GR231118 (1229U91) and other analogues of the C-terminus of neuropeptide Y are potent neuropeptide Y Y1 receptor antagonists and neuropeptide Y Y4 receptor agonists. Eur. J. Pharmacol. 349: 97-105.
36. Peralta, E.G., Ashkenazi, A., Winslow, J.W., Smith, D.H., Ramachandran, J., and Capon, D.J. 1987. Distinct primary structures, ligand-binding properties and tissue-specific expression of four human muscarinic acetylcholine receptors. EMBO J. 6: 3923-3929.
37. Petäjä-Repo, U.E., Hogu, E.M., Bhalla, S., Laperriere, A., Morello, J.-P., and Bouvier, M. 2002. Ligands act as pharmacological chaperones and increase the efficiency of δ opioid receptor maturation. EMBO J. 21: 1628-1637.
38. Rees, S., den Daas, I., Foord, S., Goodson, S., Bull, D., Kilpatrick, G., and Lee, M. 1994. Cloning and characterisation of the human 5-HT5A serotonin receptor. FEBS Lett. 355: 242-246.
39. Reinhart, C. and Krettler, C. 2006. Expression of membrane proteins in yeasts. In Structural genomics and rational drug design in membrane proteins (ed. K. Lundstrom), pp. 115-152. Marcel Dekker, New York. (in press).
40. Sarau, H.M., Griswold, D.E., Bush, B., Potts, W., Sandhu, P., Lundberg, D., Foley, J.J., Schmidt, D.B., Webb, E.F., Martin, L.D., et al. 2000. Nonpeptide tachykinin receptor antagonists. II. Pharmacological and pharmacokinetic profile of SB-222200, a central nervous system penetrant, potent and selective NK-3 receptor antagonist. J. Pharmacol. Exp. Ther. 295: 373-381.
41. Sarramegna, V., Demange, P., Milon, A., and Talmont, F. 2002. Optimizing functional versus total expression of the human μ-opioid receptor in Pichia pastoris. Protein Expr. Purif. 24: 212-220.
42. Sarramegna, V., Talmont, F., Demange, P., and Milon, A. 2003. 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: 1529-1546.
43. Schiller, H., Haase, W., Molsberger, E., Janssen, P., Michel, H., and Reiländer, H. 2000. The human ET(B) endothelin receptor heterologously produced in the methylotrophic yeast Pichia pastoris shows high-affinity binding and induction of stacked membranes. Recept. Channels 7: 93-107.
44. Scorer, C.A., Clare, J.J., McCombie, W.R., Romanos, M.A., and Sreekrishna, K. 1994. Rapid selection using G418 of high copy number transformants of Pichia pastoris for high-level foreign gene expression. Biotechnology (N.Y.) 12: 181-184.
45. Sizmann, D., Kuusinen, H., Keranen, S., Lomasney, J., Caron, M.G., Lefkowitz, R.J., and Keinanen, K. 1996. Production of adrenergic receptors in yeast. Recept. Channels 4: 197-203.
46. Tate, C.G. 2001. Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett. 504: 94-98.
47. Walter, S. and Buchner, J. 2002. Molecular chaperons - Cellular machines for protein folding. Angew. Chem. Int. Ed. Engl. 41: 1098-1113.
48. Weiss, H.M., Haase, W., Michel, H., and Reiländer, H. 1998a. Comparative biochemical and pharmacological characterization of the mouse 5HT5A 5-hydroxytryptamine receptor and the human β2-adrenergic receptor produced in the methylotrophic yeast Pichia pastoris. Biochem. J. 330: 1137-1147.
49. Weiss, H.M., Haase, W., and Reiländer, H. 1998b. Expression of an integral membrane protein, the 5HT5A receptor. Methods Mol. Biol. 103: 227-239.
50. 2a receptor functionally expressed in Escherichia coli. Eur. J. Biochem. 269: 82-92.
51. Yu, Z.W. and Quinn, P.J. 1994. Dimethyl sulphoxide: A review of its applications in cell biology. Biosci. Rep. 14: 259-281.
52. Zhang, W., Needham, D.L., Coffin, M., Rooker, A., Hurban, P., Tanzer, M.M., and Shuster, J.R. 2003. Microarray analyses of the metabolic responses of Saccharomyces cerevisiae to organic solvent dimethyl sulfoxide. J. Ind. Microbiol. Biotechnol. 30: 57-69.