Expression Systems: Pichia pastoris

Production of Membrane Proteins: Strategies for Expression and Isolation

Volumn , Issue , 2011, Pages 75-108

  Alkhalfioui, Fatima ^a   Logez, Christel ^a   Bornert, Olivier ^a   Wagner, Renaud ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Cell lysis; Membrane protein; Methanol utilization; Recombinant expression; Yeast

Indexed keywords

EID: 84868103715     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527634521.ch3     Document Type: Chapter

References (141)

1. Phaff, H.J. and Starmer, W.T. ( 1987 ) Yeasts associated with plants, insects and soil, in The Yeasts, Volume 1: Biology of Yeasts, 2nd edn (eds A.H. Rose and J.S. Harrison ), Academic Press, Orlando, FL, pp. 123-180 .
2. Guilliermond, C.H. ( 1919 ) Seances . Mem. Soc. Biol., 82, 466-470 .
3. Ogata, K., Nishikawa, H., and Ohsugi, M. ( 1969 ) A yeast capable of utilizing methanol . A gric. Biol. Chem., 33, 1519-1520 .
4. Wegner, G.H. ( 1990 ) Emerging applications of methylotrophic yeast . FEMS Microbiol. Rev., 7, 279-284 .
5. Cereghino, J.L. and Cregg, J.M. ( 2000 ) Heterologous protein expression in the methylotrophic yeast Pichia pastoris . FEMS Microbiol. Rev., 24, 45-66 .
6. Macauley-Patrick, S., Fazenda, M.L., McNeil, B., and Harvey, L.M. ( 2005 ) Heterologous protein production using the Pichia pastoris expression system . Yeast, 22, 249-270 .
7. Yamada, Y., Matsuda, M., Maeda, K., and Mikata, K. ( 1995 ) The phylogenetic relationships of methanol-assimilating yeasts based on the partial sequences of 18S and 26S ribosomal RNAs: the proposal of Komagataella gen. nov. (Saccharomycetaceae) . Biosci. Biotechnol. Biochem., 59, 439-444 .
8. Kurtzman, C.P. ( 2009 ) Biotechnological strains of Komagataella ( Pichia ) pastoris are Komagataella phaffii as determined from multigene sequence analysis . J. Ind. Microbiol. Biotechnol., 36, 1435-1438 .
9. De Schutter, K., Lin, Y.C., Tiels, P., Van Hecke, A., Glinka, S., Weber-Lehmann, J., Rouze, P., Van de Peer, Y., and Callewaert, N. ( 2009 ) Genome sequence of the recombinant protein production host Pichia pastoris . Nat. Biotechnol., 27, 561-569 .
10. Cereghino, G.P.L., Cereghino, J.L., Ilgen, C., and Cregg, J.M. ( 2002 ) Production of recombinant proteins in fermenter cultures of the yeast Pichia pastoris . Curr. Opin. Biotechnol., 13, 329-332 .
11. Li, P., Anumanthan, A., Gao, X.G., Ilangovan, K., Suzara, V.V., D ü zg ü nes, N., and Renugopalakrishnan, V. ( 2007 ) Expression of recombinant proteins in Pichia pastoris . Appl. Biochem. Biotechnol., 142, 105-124 .
12. Eckart, M.R. and Bussineau, C.M. ( 1996 ) Quality and authenticity of heterologous proteins synthesized in yeast . Curr. Opin. Biotechnol., 7, 525-530 .
13. Wheatley, M. and Hawtin, S.R. ( 1999 ) Glycosylation of G-protein-coupled receptors for hormones central to normal reproductive functioning: its occurence and role . Hum. Reprod., 5, 356-364 .
14. Duvernay, M.T., Filipeanu, C.M., and Wu, G. ( 2005 ) The regulatory mechanisms of export trafficking of G protein-coupled receptors . Cell. Signal., 17, 1457-1465 .
15. Cohen, D.M. ( 2006 ) Regulation of TRP channels by N-linked glycosylation . Semin. Cell. Dev. Biol., 17, 630-637 .
16. Grinna, L.S. and Tschopp, J.F. ( 1989 ) Size distribution and general structural features of N-linked oligosaccharides from the methylotrophic yeast, Pichia pastoris . Yeast, 5, 107-115 .
17. Wood, M.J. and Komives, E.A. ( 1999 ) Production of large quantities of isotopically labeled protein in Pichia pastoris by fermentation . J. Biomol. NMR, 13, 149-159 .
18. Whittaker, M.M. and Whittaker, J.W. ( 2005 ) Construction and characterization of Pichia pastoris strains for labeling aromatic amino acids in recombinant proteins . Protein Expr. Purif., 41, 266-274 .
19. Weiss, H.M., Haase, W., Michel, H., and Reilander, H. ( 1998 ) Comparative biochemical and pharmacological characterization of the mouse 5HT 5A 5-hydroxytryptamine receptor and the human β 2-adrenergic receptor produced in the methylotrophic yeast Pichia pastoris . Biochem. J., 330, 1137-1147 .
20. Tate, C.G., Haase, J., Baker, C., Boorsma, M., Magnani, F., Vallis, Y., and Williams, D.C. ( 2003 ) Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter . Biochim. Biophys. Acta, 1160, 141-153 .
21. Shukla, A.K., Haase, W., Reinhart, C., and Michel, H. ( 2007 ) Heterologous expression and comparative characterization of the human neuromedin U subtype II receptor using the methylotrophic yeast Pichia pastoris and mammalian cells . Int. J. Biochem. Cell Biol., 39, 931-942 .
22. Yurugi-Kobayashi, T., Asada, H., Shiroishi, M., Shimamura, T., Funamoto, S., Katsuta, N., Ito, K., Sugawara, T., Tokuda, N., Tsujimoto, H., Murata, T., Nomura, N., Haga, K., Haga, T., Iwata, S., and Kobayashi, T. ( 2009 ) Comparison of functional non-glycosylated GPCRs expression in Pichia pastoris . Biochem. Biophys. Res. Commun., 380, 271-276 .
23. Hamilton, S.R. and Gerngross, T.U. ( 2007 ) Glycosylation engineering in yeast: the advent of fully humanized yeast . Curr. Opin. Biotechnol., 18, 387-392 .
24. Opekarova, M. and Tanner, W. ( 2003 ) Specific lipid requirements of membrane proteins-a putative bottleneck in heterologous expression . Biochim. Biophys. Acta, 1610, 11-22 .
25. Lifshitz, Y., Petrovich, E., Haviv, H., Goldshleger, R., Tal, D.M., Garty, H., and Karlish, S.J.D. ( 2007 ) Purification of the human α 2 isoform of Na,K-ATPase expressed in Pichia pastoris. Stabilization by lipids and FXYD1 . Biochemistry, 46, 14937-14950 .
26. Marx, H., Sauer, M., Resina, D., Vai, M., Porro, D., Valero, F., Ferrer, P., and Mattanovich, D. ( 2006 ) Cloning, disruption and protein secretory phenotype of the GAS1 homologue of Pichia pastoris . FEMS Microbiol. Lett., 264, 40-47 .
27. Hopkins, T.R. ( 1991 ) Physical and chemical cell disruption for the recovery of intracellular proteins . Bioprocess Technol., 12, 57-83 .
28. Resina, D., Maurer, M., Cos, O., Arnau, C., Carnicer, M., Marx, H., Gasser, B., Valero, F., Mattanovich, D., and Ferrer, P. ( 2009 ) Engineering of bottlenecks in Rhizopus oryzae lipase production in Pichia pastoris using the nitrogen source-regulated FLD1 promoter . Nat. Biotechnol., 25, 396-403 .
29. Daly, R. and Hearn, M.T.W. ( 2005 ) Expression of heterologous proteins in Pichia pastoris : a useful experimental tool in protein engineering and production . J. Mol. Recognit., 18, 119-138 .
30. Gellisen, G. ( 2000 ) Heterologous protein production in methylotrophic yeasts . Appl. Microbiol. Biotechnol., 54, 741-750 .
31. Hartner, F.S., Ruth, C., Langenegger, D., Johnson, S.N., Hyka, P., Lin-Cereghino, G.P., Lin-Cereghino, J., Kovar, K., Cregg, J.M., and Glieder, A. ( 2008 ) Promoter library designed for fine-tuned gene expression in Pichia pastoris . Nucleic Acids Res., 36, e76 .
32. Cregg, J.M., Barringer, K.J., Hessler, A.Y., and Madden, K.R. ( 1985 ) Pichia pastoris as a host system for transformations . Mol. Cell. Biol., 5, 3376-3385 .
33. Lee, C.C., Williams, T.G., Wong, D.W.S., and Robertson, G.H. ( 2005 ) An episomal expression vector for screening mutant gene libraries in Pichia pastoris . Plasmid, 54, 80-85 .
34. Hong, I.P., Lee, S.J., Kim, Y.S., and Choi, S.G. ( 2007 ) Recombinant expression of human cathelicidin (hCAP18/LL-37) in Pichia pastoris . Biotechnol. Lett., 29, 73-78 .
35. Sandstrom, A.G., Engstrom, K., Nyhlen, J., Kasrayan, A., and Backvall, J.E. ( 2009 ) Directed evolution of Candida antarctica lipase A using an episomal replicating yeast plasmid . Protein Eng. Des. Sel., 22, 413-420 .
36. Pla, I.A., Damasceno, L.M., Vannelli, T., Ritter, G., Batt, C.A., and Shuler, M.L. ( 2006 ) Evaluation of Mut + and Mut S Pichia pastoris phenotypes for high level extracellular scFv expression under feedback control of the methanol concentration . Biotechnol. Prog., 22, 881-888 .
37. Cos, O., Ram ó n, R., Montesinos, J.L., and Valero, F. ( 2006 ) Operational strategies, monitoring and control of heterologous protein production in the methylotrophic yeast Pichia pastoris under different promoters: a review . Microb. Cell Fact., 5, 17 .
38. Weiss, H.M., Haase, W., Michel, H., and Reilander, H. ( 1995 ) Expression of functional mouse 5-HT 5A serotonin receptor in the methylotrophic yeast Pichia pastoris : pharmacological characterization and localization . FEBS Lett., 377, 451-456 .
39. +-ATPase in Pichia pastoris : analysis of wild type and D369N mutant proteins by Fe 2 +-catalyzed oxidative cleavage and molecular modeling . J. Biol. Chem., 278, 46064-46073 .
40. Cohen, E., Goldshleger, R., Shainskaya, A., Tal, D.M., Ebel, C., Le Maire, M., and Karlish, S.J.D. ( 2005 ) Purification of Na,K-ATPase expressed in Pichia pastoris reveals an essential role of phospholipid-protein interactions . J. Biol. Chem., 280, 16610-16618 .
41. +-ATPase purified from Pichia pastoris membranes by specific interactions with lipids . Biochemistry, 46, 12855-12867 .
42. Reina, C., Padoani, G., Carotti, C., Merico, A., Tripodi, G., Ferrari, P., and Popolo, L. ( 2007 ) Expression of the α 3/ β 1 isoform of human Na,K-ATPase in the methylotrophic yeast Pichia pastoris . FEMS Yeast Res., 7, 585-594 .
43. +-ATPase: Purification of α 1/ β 1/PLM complexes expressed in Pichia pastoris . J. Biol. Chem., 281, 15790-15799 .
44. + channels heterologously expressed in Pichia pastoris . J. Mol. Biol., 333, 103-116 .
45. + channel . Science, 309, 897-903 .
46. + channel in a lipid membrane-like environment . Nature, 450, 376-382 .
47. Julien, M., Kajiji, S., Kaback, R.H., and Gros, P. ( 2000 ) Simple purification of highly active biotinylated P-glycoprotein: enantiomer-specific modulation of drug-stimulated ATPase activity . Biochemistry, 39, 75-85 .
48. Urbatsch, I.L., Gimi, K., Wilke-Mounts, S., and Senior, A.E. ( 2000 ) Conserved Walker A Ser residues in the catalytic sites of P-glycoprotein are critical for catalysis and involved primarily at the transition state step . J. Biol. Chem., 275, 25031-25038 .
49. Cai, J., Daoud, R., Georges, E., and Gros, P. ( 2001 ) Functional expression of multidrug resistance protein 1 in Pichia pastoris . Biochemistry, 40, 8307-8316 .
50. Chiou, T.J., Liu, H., and Harrison, M.J. ( 2001 ) The spatial expression patterns of a phosphate transporter ( Mt PT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface . Plant J., 25, 281-293 .
51. Theis, S., Doring, F., and Daniel, H. ( 2001 ) Expression of the Myc/His-tagged human peptide transporter hPEPT1 in yeast for protein purification and functional analysis . Protein Expr. Purif., 22, 436-442 .
52. Urbatsch, I.L., Wilke-Mounts, S., Gimi, K., and Senior, A.E. ( 2001 ) Purification and characterization of N-glycosylation mutant mouse and human P-glycoproteins expressed in Pichia pastoris cells . Arch. Biochem. Biophys., 388, 171-177 .
53. Urbatsch, I.L., Gimi, K., Wilke-Mounts, S., Lerner-Marmarosh, N., Rousseau, M.E., Gros, P., and Senior, A.E. ( 2001 ) Cysteines 431 and 1074 are responsible for inhibitory disulfide cross-linking between the two nucleotide-binding sites in human P-glycoprotein . J. Biol. Chem., 276, 26980-26987 .
54. Zhang, H., Howard, E.M., and Roepe, P.D. ( 2002 ) Analysis of the antimalarial drug resistance protein Pfcrt expressed in yeast . J. Biol. Chem., 277, 49767-49775 .
55. Urbatsch, I.L., Tyndall, G.A., Tombline, G., and Senior, A.E. ( 2003 ) P-glycoprotein catalytic mechanism, studies of the ADP-vanadate inhibited state . J. Biol. Chem., 278, 23171-23179 .
56. Mao, Q., Conseil, G., Gupta, A., Cole, S.P.C., and Unadkat, J.D. ( 2004 ) Functional expression of the human breast cancer resistance protein in Pichia pastoris . Biochem. Biophys. Res. Commun., 320, 730-737 .
57. Tyagi, N.K., Goyal, P., Kumar, A., Pandey, D., Siess, W., and Kinne, R.K.H. ( 2005 ) High-yield functional expression of human sodium/ d-glucose cotransporter 1 in Pichia pastoris and characterization of ligand-induced conformational changes as studied by tryptophan fluorescence . Biochemistry, 44, 15514-15524 .
58. Aller, S.G. and Unger, V.M. ( 2006 ) Projection structure of the human copper transporter CTR1 at 6-Å resolution reveals a compact trimer with a novel channel-like architecture . Proc. Natl. Acad. Sci. USA, 103, 3627-3632 .
59. Diatloff, E., Forde, B.G., and Roberts, S.K. ( 2006 ) Expression and transport characterisation of the wheat low-affinity cation transporter (LCT1) in the methylotrophic yeast Pichia pastoris . Biochem. Biophys. Res. Commun., 344,807-813 .
60. Tan, W., Gou, D.M., Tai, E., Zhao, Y.Z., and Chow, L.M.C. ( 2006 ) Functional reconstitution of purified chloroquine resistance membrane transporter expressed in yeast . Arch. Biochem. Biophys., 452, 119-128 .
61. Tombline, G., Urbatsch, I.L., Virk, N., Muharemagic, A., Bartholomew White, L., and Senior, A.E. ( 2006 ) Expression, purification, and characterization of cysteine-free mouse P-glycoprotein . Arch. Biochem. Biophys., 445, 124-128 .
62. Amoah, L.E., Lekostaj, J.K., and Roepe, P.D. ( 2007 ) Heterologous expression and ATPase activity of mutant versus wild type PfMDR1 protein . Biochemistry, 46, 6060-6073 .
63. Chloupková, M., Pickert, A., Lee, J.Y., Souza, S., Trinh, Y.T., Connelly, S.M., Dumont, M.E., Dean, M., and Urbatsch, I.L. ( 2007 ) Expression of 25 human ABC transporters in the yeast Pichia pastoris and characterization of the purified ABCC3 ATPase activity . Biochemistry, 46, 7992-8003 .
64. Price, D.R.G., Wilkinson, H.S., and Gatehouse, J.A. ( 2007 ) Functional expression and characterisation of a gut facilitative glucose transporter, NlHT1, from the phloem-feeding insect Nilaparvata lugens (rice brown planthopper) . Insect Biochem. Mol. Biol., 37, 1138-1148 .
65. Cox, H.D., Chao, C.K., Patel, S.A., and Thompson, C.M. ( 2008 ) Efficient digestion and mass spectral analysis of vesicular glutamate transporter 1: a recombinant membrane protein expressed in yeast . J. Proteome Res., 7, 570-578.
66. Alisio, A. and Mueckler, M. ( 2010 ) Purification and characterization of mammalian glucose transporters expressed in Pichia pastoris . Protein Expr. Purif., 70, 81-87 .
67. Aller, S.G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P.M., Trinh, Y.T., Zhang, Q., Urbatsch, I.L., and Chang, G. ( 2009 ) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding . Science, 323, 1718-1722 .
68. Beckham, K.S.H., Potter, J.A., and Unkles, S.E. ( 2010 ) Formate-nitrite transporters: optimisation of expression, purification and analysis of prokaryotic and eukaryotic representatives . Protein Expr. Purif., 71, 184-189 .
69. Karlsson, M., Fotiadis, D., Sjovall, S., Johansson, I., Hedfalk, K., Engel, A., and Kjellbom, P. ( 2003 ) Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris . FEBS Lett., 537, 68-72 .
70. Kukulski, W., Schenk, A.D., Johanson, U., Braun, T., de Groot, B.L., Fotiadis, D., Kjellbom, P., and Engel, A. ( 2005 ) The 5 Å structure of heterologously expressed plant aquaporin SoPIP2;1 . J. Mol. Biol., 350, 611-616 .
71. Daniels, M.J., Wood, M.R., and Yeager, M. ( 2006 ) In vivo functional assay of a recombinant aquaporin in Pichia pastoris . Appl. Environ. Microbiol., 72, 1507-1514 .
72. Tornroth-Horsefield, S., Wang, Y., Hedfalk, K., Johanson, U., Karlsson, M., Tajkhorshid, E., Neutze, R., and Kjellbom, P. ( 2006 ) Structural mechanism of plant aquaporin gating . Nature, 439, 688-694 .
73. Eifler, N., Duckely, M., Sumanovski, L.T., Egan, T.M., Oksche, A., Konopka, J.B., Luthi, A., Engel, A., and Werten, P.J.L. ( 2007 ) Functional expression of mammalian receptors and membrane channels in different cells . J. Struct. Biol., 159, 179-193 .
74. Nyblom, M., Oberg, F., Lindkvist-Petersson, K., Hallgren, K., Findlay, H., Wikstrom, J., Karlsson, A., Hansson, O., Booth, P.J., Bill, R.M., Neutze, R., and Hedfalk, K. ( 2007 ) Exceptional overproduction of a functional human membrane protein . Protein Expr. Purif., 56, 110-120 .
75. Hedfalk, K., Pettersson, N., Oberg, F., Hohmann, S., and Gordon, E. ( 2008 ) Production, characterization and crystallization of the Plasmodium falciparum aquaporin . Protein Expr. Purif., 59, 69-78 .
76. Horsefield, R., Nordén, K., Fellert, M., Backmark, A., Tornroth-Horsefield, S., Terwisscha van Scheltinga, A.C., Kvassman, J., Kjellbom, P., Johanson, U., and Neutze, R. ( 2008 ) High-resolution X-ray structure of human aquaporin 5 . Proc. Natl. Acad. Sci. USA, 105, 13327-13332 .
77. Verdoucq, L., Grondin, A., and Maurel, C. ( 2008 ) Structure-function analysis of plant aquaporin At PIP2;1 gating by divalent cations and protons . Biochem. J., 15, 409-416 .
78. Azad, A.K., Sawa, Y., Ishikawa, T., and Shibata, H. ( 2009 ) Heterologous expression of tulip petal plasma membrane aquaporins in Pichia pastoris for water channel analysis . Appl. Environ. Microbiol., 75, 2792-2797 .
79. Fischer, G., Kosinska-Eriksson, U., Aponte-Santamaria, C., Palmgren, M., Geijer, C., Hedfalk, K., Hohmann, S., de Groot, B.L., Neutze, R., and Lindkvist-Petersson, K. ( 2009 ) Crystal structure of a yeast aquaporin at 1.15 Å reveals a novel gating mechanism . PLOS Biol., 7, e1000130 .
80. Ho, J.D., Yeh, R., Sandstrom, A., Chorny, I., Harries, W.E.C., Robbins, R.A., Miercke, L.J.W., and Stroud, R.M. ( 2009 ) Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance . Proc. Natl. Acad. Sci. USA, 106, 7437-7442 .
81. Öberg, F., Ekvall, M., Nyblom, M., Backmark, A., Neutze, R., and Hedfalk, K. ( 2009 ) Insight into factors directing high production of eukaryotic membrane proteins; production of 13 human AQPs in Pichia pastoris . Mol. Membr. Biol., 26, 215-227 .
82. Licata, L., Haase, W., Eckhardt-Strelau, L., and Parcej, D.N. ( 2006 ) Over-expression of a mammalian small conductance calcium-activated K + channel in Pichia pastoris : effects of trafficking signals and subunit fusions . Protein Expr. Purif., 47, 171-178 .
83. Tao, X., Avalos, J.L., Chen, J., and MacKinnon, R. ( 2009 ) Crystal structure of the eukaryotic strong inward-rectifier K + channel Kir2.2 at 3.1 Å resolution . Science, 326, 1668-1674 .
84. Schiller, H., Haase, W., Molsberger, E., Janssen, P., Michel, H., and Reilander, H. ( 2000 ) The human ETB endothelin receptor heterologously produced in the methylotrophic yeast Pichia pastoris shows high-affinity binding and induction of stacked membranes . Receptors Channels, 7, 93-107 .
85. Schiller, H., Molsberger, E., Janssen, P., Michel, H., and Reilander, H. ( 2001 ) Solubilization and purification of the human ETB endothelin receptor produced by high-level fermentation in Pichia pastoris . Receptors Channels, 7, 453-569 .
86. Feng, W., Cai, J., Pierce, W.M., Jr, and Song, Z.H. ( 2002 ) Expression of CB2 cannabinoid receptor in Pichia pastoris . Protein Expr. Purif., 26, 496-505 .
87. 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 .
88. Sarramegna, V., Talmont, F., Seree de Roch, M., Milon, A., and Demange, P. ( 2002 ) Green fluorescent protein as a reporter of human μ-opioid receptor overexpression and localization in the methylotrophic yeast Pichia pastoris . J. Biotechnol., 99, 23-39 .
89. De Jong, L.A.A., Grunewald, S., Franke, J.P., Uges, D.R.A., and Bischoff, R. ( 2004 ) Purification and characterization of the recombinant human dopamine D2S receptor from Pichia pastoris . Protein Expr. Purif., 33, 176-184 .
90. Grunewald, S., Haase, W., Molsberger, E., Michel, H., and Reilander, H. ( 2004 ) Production of the human D2S receptor in the methylotrophic yeast P. pastoris . Receptors Channels, 10, 37-50 .
91. De Rivoyre, M., Bonino, F., Ruel, L., Bidet, M., Thérond, P., and Mus-Veteau, I. ( 2005 ) Human receptor Smoothened, a mediator of Hedgehog signalling, expressed in its native conformation in yeast . FEBS Lett., 579, 1529-1533 .
92. Kim, T.K., Zhang, R., Feng, W., Cai, J., Pierce, W., and Song, Z.H. ( 2005 ) Expression and characterization of human CB1 cannabinoid receptor in methylotrophic yeast Pichia pastoris . Protein Expr. Purif., 40, 60-70 .
93. Sarramegna, V., Muller, I., Mousseau, G., Froment, C., Monsarrat, B., Milon, A., and Talmont, F. ( 2005 ) Solubilization, purification, and mass spectrometry analysis of the human mu-opioid receptor expressed in Pichia pastoris . Protein Expr. Purif., 43, 85-93 .
94. André, N., Cherouati, N., Prual, C., Steffan, T., Zeder-Lutz, G., Magnin, T., Pattus, F., Michel, H., Wagner, R., and Reinhart, C. ( 2006 ) 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, 1115-1126 .
95. Fraser, N.J. ( 2006 ) Expression and functional purification of a glycosylation deficient version of the human adenosine 2a receptor for structural studies . Protein Expr. Purif., 49, 129-137 .
96. Noguchi, S. and Satow, Y. ( 2006 ) Purification of human β 2-adrenergic receptor expressed in methylotrophic yeast Pichia pastoris . J. Biochem., 140, 799-804 .
97. Lundstrom, K., Wagner, R., Reinhart, C., Desmyter, A., Cherouati, N., Magnin, T., Zeder-Lutz, G., Courtot, M., Prual, C., Andr é, N., Hassaine, G., Michel, H., Cambillau, C., and Pattus, F. ( 2006 ) Structural genomics on membrane proteins: comparison of more than 100 GPCRs in 3 expression systems . J. Struct. Funct. Genomics, 7, 77-91 .
98. Yang, G., Liu, T., Peng, W., Sun, X., Zhang, H., Wu, C., and Shen, D. ( 2006 ) Expression and localization of recombinant human EDG-1 receptors in Pichia pastoris . Biotechnol. Lett., 28, 1581-1586 .
99. Yang, G.X., Liu, T.L., Zhang, H., Wu, C.Q., and Shen, D.L. ( 2006 ) Expression and localization of recombinant human B2 receptors in the methylotrophic yeast Pichia pastoris . Genetika, 42, 728-731 .
100. Shukla, A.K., Haase, W., Reinhart, C., and Michel, H. ( 2007 ) Heterologous expression and characterization of the recombinant bradykinin B2 receptor using the methylotrophic yeast Pichia pastoris . Protein Expr. Purif., 55, 1-8 .
101. Zhang, R., Kim, T.K., Qiao, Z.H., Cai, J., Pierce, Jr, W.M., and Song, Z.H. ( 2007 ) Biochemical and mass spectrometric characterization of the human CB2 cannabinoid receptor expressed in Pichia pastoris-importance of correct processing of the N-terminus . Protein Expr. Purif., 55, 225-235 .
102. Magnin, T., Fiez-Vandal, C., Potier, N., Coquard, A., Leray, I., Steffan, T., Logez, C., Alkhalfioui, F., Pattus, F., and Wagner, R. ( 2008 ) A novel, generic and effective method for the rapid purification of G protein-coupled receptors . Protein Expr. Purif., 64, 1-7 .
103. Muller, I., Sarramégna, V., Milon, A., and Talmont, F.J. ( 2010 ) The N-terminal end truncated mu-opioid receptor: from expression to circular dichroism analysis . Appl. Biochem. Biotechnol., 160, 2175-2186 .
104. Talmont, F. ( 2009 ) Monitoring the human β 1, β 2, β 3 adrenergic receptors expression and purification in Pichia pastoris using the fluorescence properties of the enhanced green fluorescent protein . Biotechnol. Lett., 31, 49-55 .
105. Hori, H., Sato, Y., Takahashi, N., Takio, K., Yokomizo, T., Nakamura, M., Shimizu, T., and Miyano, M. ( 2010 ) Expression, purification and characterization of leukotriene B 4 receptor, BLT1 in Pichia pastoris . Protein Expr. Purif., 72, 66-74 .
106. Blum, A., Martin, H.J., and Maser, E. ( 2000 ) Human 11 β-hydroxysteroid dehydrogenase 1/carbonylreductase: recombinant expression in the yeast Pichia pastoris and Escherichia coli . Toxicology, 144, 113-120 .
107. Newton-Vinson, P., Hubalek, F., and Edmondson, D.E. ( 2000 ) High-level expression of human liver monoamine oxidase B in Pichia pastoris . Protein Expr. Purif., 20, 334-345 .
108. Binda, C., Newton-Vinson, P., Hubalek, F., Edmondson, D.E., and Mattevi, A. ( 2002 ) Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders . Nat. Struct. Biol., 9, 22-26 .
109. Li, M., Hubalek, F., Newton-Vinson, P., and Edmondson, D.E. ( 2002 ) High-level expression of human liver monoamine oxidase A in Pichia pastoris : comparison with the enzyme expressed in Saccharomyces cerevisiae . Protein Expr. Purif., 24, 152-162 .
110. Nobel, C.S.I., Dunas, F., and Abrahmsén, L.B. ( 2002 ) Purification of full-length recombinant human and rat type 1 11 β-hydroxysteroid dehydrogenases with retained oxidoreductase activities . Protein Expr. Purif., 26, 349-356 .
111. Binda, C., Li, M., Hubalek, F., Restelli, N., Edmondson, D.E., and Mattevi, A. ( 2003 ) Insights into the mode of inhibition of human mitochondrial monoamine oxidase B from high-resolution crystal structures . Proc. Natl. Acad. Sci. USA, 100, 9750-9755 .
112. Ruf, A., Muller, F., D ' Arcy, B., Stihle, M., Kusznir, E., Handschin, C., Morand, O.H., and Thoma, R. ( 2004 ) The monotopic membrane protein human oxidosqualene cyclase is active as monomer . Biochem. Biophys. Res. Commun., 315, 247-254 .
113. De Colibus, L., Li, M., Binda, C., Lustig, A., Edmondson, D.E., and Mattevi, A. ( 2005 ) Three-dimensional structure of human monoamine oxidase A (MAO A): relation to the structures of rat MAO A and human MAO B . Proc. Natl. Acad. Sci. USA, 102, 12684-12689 .
114. Dietrich, M., Grundmann, L., Kurr, K., Valinotto, L., Saussele, T., Schmid, R.D., and Lange, S. ( 2005 ) Recombinant production of human microsomal cytochrome P450 2D6 in the methylotrophic yeast Pichia pastoris . ChemBioChem., 6, 2014-2022 .
115. Liu, W., Kamensky, Y., Kakkar, R., Foley, E., Kulmacz, R.J., and Palmer, G. ( 2005 ) Purification and characterization of bovine adrenal cytochrome b 561 expressed in insect and yeast cell systems . Protein Expr. Purif., 40, 429-439 .
116. Matsuzaki, F. and Wariishi, H. ( 2005 ) Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium . Biochem. Biophys. Res. Commun., 334, 1184-1190 .
117. Kolar, N.W., Swart, A.C., Mason, J.I., and Swart, P. ( 2007 ) Functional expression and characterisation of human cytochrome P45017 α in Pichia pastoris . J. Biotechnol., 129, 635-644 .
118. Martinez Molina, D., Wetterholm, A., Kohl, A., McCarthy, A.A., Niegowski, D., Ohlson, E., Hammarberg, T., Eshaghi, S., Haeggstrom, J.Z., and Nordlund, P. ( 2007 ) Structural basis for synthesis of inflammatory mediators by human leukotriene C 4 synthase . Nature, 448, 613-617 .
119. Upadhyay, A.K. and Edmondson, D.E. ( 2008 ) Characterization of detergent purified recombinant rat liver monoamine oxidase B expressed in Pichia pastoris . Protein Expr. Purif., 59, 349-356 .
120. Wetterholm, A., Martinez Molina, D., Nordlund, P., Eshaghi, S., and Haeggström, J.Z. ( 2008 ) High-level expression, purification, and crystallization of recombinant rat leukotriene C 4 synthase from the yeast Pichia pastoris . Protein Expr. Purif., 60, 1-6 .
121. Wang, J. and Edmondson, D.E. ( 2010 ) High-level expression and purification of rat monoamine oxidase A (MAO A) in Pichia pastoris : comparison with human MAO A . Protein Expr. Purif., 70, 211-217 .
122. Arslan, B.K. and Edmondson, D.E. ( 2010 ) Expression of zebrafish ( Danio rerio ) monoamine oxidase (MAO) in Pichia pastoris : purification and comparison with human MAO A and MAO B . Protein Expr. Purif., 70, 290-297 .
123. Brucato, C.L., Birr, C.A., Bruguera, P., Ruiz, J.A., and Sanchez-Martinez, D. ( 2002 ) Expression of recombinant rabbit tissue factor in Pichia pastoris, and its application in a prothrombin time reagent . Protein Expr. Purif., 26, 386-393 .
124. Gurkan, C. and Ellar, D.J. ( 2003 ) Expression in Pichia pastoris and purification of a membrane-acting immunotoxin based on a synthetic gene coding for the Bacillus thuringiensis Cyt2Aa1 toxin . Protein Expr. Purif., 29, 103-116 .
125. Huang, Z., Zhang, T., Yang, J., Zhu, P., Du, G., and Cheng, K. ( 2005 ) Cloning and expression of human lectin-like oxidized low density lipoprotein receptor-1 in Pichia pastoris . Biotechnol. Lett., 27, 49-52 .
126. Labarre, C., Van Tilbeurgh, H., and Blondeau, K. ( 2007 ) Pichia pastoris is a valuable host for the expression of genes encoding membrane proteins from the hyperthermophilic Archeon Pyrococcus abyssi . Extremophiles, 11, 403-413 .
127. Jamshad, M., Rajesh, S., Stamataki, Z., McKeating, J.A., Dafforn, T., Overduin, M., and Bill, R.M. ( 2008 ) Structural characterization of recombinant human CD81 produced in Pichia pastoris . Protein Expr. Purif., 57, 206-216 .
128. Egawa, K., Shibata, H., Yamashita, S., Yurimoto, H., Sakai, Y., and Kato, H. ( 2009 ) Overexpression and purification of rat peroxisomal membrane protein 22, PMP22, in Pichia pastoris . Protein Expr. Purif., 64, 47-54 .
129. Vos, W.L., Vaughan, S., Lall, P.Y., McCaffrey, J.G., Wysocka-Kapcinska, M., and Findlay, J.B.C. ( 2010 ) Expression and structural characterization of peripherin/RDS, a membrane protein implicated in photoreceptor outer segment morphology . Eur. Biophys. J., 39, 679-688 .
130. Vlahopoulos, S., Gritzapis, A.D., Perez, S.A., Cacoullos, N., Papamichail, M., and Baxevanis, C.N. ( 2009 ) Mannose addition by yeast Pichia Pastoris on recombinant HER-2 protein inhibits recognition by the monoclonal antibody herceptin . Vaccine, 27, 4704-4708 .
131. Gustafsson, C., Govindarajan, S., and Minshull, J. ( 2004 ) Codon bias and heterologous protein expression . Trends Biotechnol., 22, 346-353 .
132. Singh, S., Gras, A., Fiez-Vandal, C., Ruprecht, J., Rana, R., Martinez, M., Strange, P.G., Wagner, R., and Byrne, B. ( 2008 ) Large-scale functional expression of WT and truncated human adenosine A 2A receptor in Pichia pastoris bioreactor cultures . Microb. Cell Fact., 7, 28 .
133. Talmont, F., Sidobre, S., Demange, P., Milon, A., and Emorine, L.J. ( 1996 ) Expression and pharmacological characterization of the human mu opioid receptor in the methylotrophic yeast Pichia pastoris . FEBS Lett., 394, 268-272 .
134. Cid, G.M., Nugent, P.G., Davenport, A.P., Kuc, R.E., and Wallace, B.A. ( 2000 ) Expression and characterization of the human endothelin-A-receptor in Pichia pastoris : influence of N-terminal epitope tags . J. Cardiovasc. Pharmacol., 36, S55-S57 .
135. Brillet, K., Perret, B.G., Klein, V., Pattus, F., and Wagner, R. ( 2008 ) Using EGFP fusions to monitor the functional expression of GPCRs in the Drosophila Schneider 2 cells . Cytotechnology, 57, 101-109 .
136. Yu, Z.W. and Quinn, P.J. ( 1994 ) Dimethyl sulphoxide: a review of its applications in cell biology . Biosci. Rep., 14, 259-281 .
137. Bernier, V., Lagacé, M., Bichet, D.G., and Bouvier, M. ( 2004 ) Pharmacological chaperones: potential treatment for conformational diseases . Trends Endocrinol. Metab., 15, 222-228 .
138. Zeder-Lutz, G., Cherouati, N., Reinhart, C., Pattus, F., and Wagner, R. ( 2006 ) Dot-blot immunodetection as a versatile and high-throughput assay to evaluate recombinant GPCRs produced in the yeast Pichia pastoris . Protein Expr. Purif., 50, 118-127 .
139. Aguilar-Uscanga, B. and François, J.M. ( 2003 ) A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation . Lett. Appl. Microbiol., 37, 268-274 .
140. Wagner, S., Klepsch, M.M., Schlegel, S., Appel, A., Draheim, R., Tarry, M., Högbom, M., van Wijk, K.J., Slotboom, D.J., Persson, J.O., and de Gier, J.W. ( 2008 ) Tuning Escherichia coli for membrane protein overexpression . Proc. Natl. Acad. Sci. USA, 105, 14371-14376 .
141. Bonander, N., Darby, R.A., Grgic, L., Bora, N., Wen, J., Brogna, S., Poyner, D.R., O ' Neill, M.A., and Bill, R.M. ( 2009 ) Altering the ribosomal subunit ratio in yeast maximizes recombinant protein yield . Microb. Cell. Fact., 8, 10 .