Recombinant production of the human aquaporins in the yeast Pichia pastoris (Invited Review)

References

• Baim SB, Sherman F. mRNA structures influencing translation in the yeast Saccharomyces cerevisiae. Mol Cell Biol 1988;8:1591–1601.
   PubMed Web of Science ®Google Scholar
• Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T. 2006. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci USA 103:269–274.
   PubMed Web of Science ®Google Scholar
• Bill RM, Henderson PJ, Iwata S, Kunji ER, Michel H, Neutze R, 2011. Overcoming barriers to membrane protein structure determination. Nat Biotechnol 29:335–340.
   PubMed Web of Science ®Google Scholar
• Bleasby A. 2001. EMBOSS: cai [Online] Accessed 25 March 2011 from. http://emboss.bioinformatics.nl/cgi-bin/emboss/cai.
   Google Scholar
• Bonander N, Bill RM. 2009. Relieving the first bottleneck in the drug discovery pipeline: Using array technologies to rationalize membrane protein production. Expert Rev Proteomics 6:501–505.
   PubMed Web of Science ®Google Scholar
• Bonander N, Hedfalk K, Larsson C, Mostad P, Chang C, Gustafsson L, 2005. Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci 14:1729–1740.
   PubMedGoogle Scholar
• Buck TM, Wagner J, Grund S, Skach WR. 2007. A novel tripartite motif involved in aquaporin topogenesis, monomer folding and tetramerization. Nat Struct Mol Biol 14:762–769.
   PubMedGoogle Scholar
• Chepelinsky AB. 2009. Structural function of MIP/aquaporin 0 in the eye lens; genetic defects lead to congenital inherited cataracts. Handb Exp Pharmacol 190:265–97.
   Google Scholar
• Cigan AM, Donahue TF. 1987. Sequence and structural features associated with translational initiator regions in yeast – a review. Gene 59:1–18.
   PubMed Web of Science ®Google Scholar
• Cregg JM, Barringer KJ. 1990. Pichia transformation. United States patent application 07/110148.
   Google Scholar
• Cregg JM, Cereghino JL, Shi J, Higgins DR. 2000. Recombinant protein expression in Pichia pastoris. Mol Biotechnol 16:23–52.
   PubMed Web of Science ®Google Scholar
• De Schutter K, Lin YC, Tiels P, Van Hecke A, Glinka S, Weber-Lehmann J, 2009. Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 27:561–566.
   PubMed Web of Science ®Google Scholar
• Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S. 2000. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276:1118–1128.
   PubMed Web of Science ®Google Scholar
• Fantoni A, Bill RM, Gustafsson L, Hedfalk K. 2007. Improved yields of full-length functional human FGF1 can be achieved using the methylotrophic yeast Pichia pastoris. Protein Expr Purif 52:31–39.
   PubMed Web of Science ®Google Scholar
• Forstner M, Leder L, Mayr LM. 2007. Optimization of protein expression systems for modern drug discovery. Expert Rev Proteomics 4:67–78.
   PubMed Web of Science ®Google Scholar
• Foster W, Helm A, Turnbull I, Gulati H, Yang B, Verkman AS, 2000. Identification of sequence determinants that direct different intracellular folding pathways for aquaporin-1 and aquaporin-4. J Biol Chem 275:34157–34165.
   PubMedGoogle Scholar
• Garcia F, Kierbel A, Larocca MC, Gradilone SA, Splinter P, LaRusso NF, 2001. The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J Biol Chem 276:12147–12152.
   PubMed Web of Science ®Google Scholar
• GeneArt. 2011. Gene Synthesis [Online] Accessed 25 March 2011 from. http://www.geneart.com/english/products-services/gene-synthesis/index.html.
   Google Scholar
• GenScript. 2011. Gene Synthesis [Online] Accessed 25 March 2011 from. http://www.genscript.com/gene_synthesis.html.
   Google Scholar
• Grisshammer R. 2006. Understanding recombinant expression of membrane proteins. Curr Opin Biotechnol 17:337–340.
   PubMed Web of Science ®Google Scholar
• Grisshammer R, Tate CG. 1995. Overexpression of integral membrane proteins for structural studies. Q Rev Biophys 28:315–422.
   PubMed Web of Science ®Google Scholar
• Grote A, Hiller K, Scheer M, Munch R, Nortemann B, Hempel DC, 2005. JCat: a novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Res 33:W526–W531.
   PubMed Web of Science ®Google Scholar
• Gustafsson C, Govindarajan S, Minshull J. 2004. Codon bias and heterologous protein expression. Trends Biotechnol 22:346–353.
   PubMed Web of Science ®Google Scholar
• Hedfalk K, Pettersson N, Oberg F, Hohmann S, Gordon E. 2008. Production, characterization and crystallization of the Plasmodium falciparum aquaporin. Protein Expr Purif 59:69–78.
   PubMedGoogle Scholar
• Hennig L, Schafer E. 1998. Protein purification with C-terminal fusion of maltose binding protein. Protein Expr Purif 14:367–370.
   PubMedGoogle Scholar
• Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, Andersson H, 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377–381.
   PubMed Web of Science ®Google Scholar
• Hessa T, Meindl-Beinker NM, Bernsel A, Kim H, Sato Y, Lerch-Bader M, 2007. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450:1026–1030.
   PubMed Web of Science ®Google Scholar
• Holmes WJ, Darby RA, Wilks MD, Smith R, Bill RM. 2009. Developing a scalable model of recombinant protein yield from Pichia pastoris: the influence of culture conditions, biomass and induction regime. Microb Cell Fact 8:35.
   PubMedGoogle Scholar
• Invitrogen. 2002. Pichia Fermentation Process Guidelines [Online] Accessed 5 February 2008 from. http://tools.invitrogen.com/content/sfs/manuals/pichiaferm_prot.pdf.
   Google Scholar
• Invitrogen. 2005. EasySelect Pichia Expression Kit, version G [Online] Accessed 14 February 2005 from. http://www.invitrogen.com/content/sfs/manuals/easyselect_man.pdf.
   Google Scholar
• Invitrogen. 2010. EasySelect Pichia Expression Kit, Version MAN0000042 [Online] Accessed 18 June 2010 from. http://www.invitrogen.com/content/sfs/manuals/easyselect_man.pdf.
   Google Scholar
• Itoh T, Rai T, Kuwahara M, Ko SB, Uchida S, Sasaki S, Ishibashi K. 2005. Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem Biophys Res Commun 330:832–838.
   PubMed Web of Science ®Google Scholar
• Jungo C, Marison I, von Stockar U. 2007a. Mixed feeds of glycerol and methanol can improve the performance of Pichia pastoris cultures: A quantitative study based on concentration gradients in transient continuous cultures. J Biotechnol 128:824–837.
   PubMed Web of Science ®Google Scholar
• Jungo C, Schenk J, Pasquier M, Marison IW, von Stockar U. 2007b. A quantitative analysis of the benefits of mixed feeds of sorbitol and methanol for the production of recombinant avidin with Pichia pastoris. J Biotechnol 131:57–66.
   PubMed Web of Science ®Google Scholar
• Karabasil MR, Hasegawa T, Azlina A, Purevjav J, Purwanti N, Yao C, Akamatsu T, Hosoi K. 2009. Trafficking of GFP-AQP5 chimeric proteins conferred with unphosphorylated amino acids at their PKA-target motif ((152)SRRTS) in MDCK-II cells. J Med Invest 56:55–63.
   PubMedGoogle Scholar
• King LS, Kozono D, Agre P. 2004. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698.
   PubMed Web of Science ®Google Scholar
• Kazusa. 2007. Avilable from: http://www.kazusa.or.jp/codon
   Google Scholar
• Kozak M. 1981. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res 9:5233–5252.
   PubMed Web of Science ®Google Scholar
• Lian J, Ding S, Cai J, Zhang D, Xu Z, Wang X. 2009. Improving aquaporin Z expression in Escherichia coli by fusion partners and subsequent condition optimization. Appl Microbiol Biotechnol 82:463–470.
   PubMed Web of Science ®Google Scholar
• Lu Y, Turnbull IR, Bragin A, Carveth K, Verkman AS, Skach WR. 2000. Reorientation of aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol Biol Cell 11:2973–2985.
   PubMedGoogle Scholar
• Lundstrom K. 2006. Structural genomics: The ultimate approach for rational drug design. Mol Biotechnol 34:205–212.
   PubMedGoogle Scholar
• Mobasheri A, Shakibaei M, Marples D. 2004. Immunohistochemical localization of aquaporin 10 in the apical membranes of the human ileum: a potential pathway for luminal water and small solute absorption. Histochem Cell Biol 121:463–471.
   PubMedGoogle Scholar
• Morishita Y, Matsuzaki T, Hara-chikuma M, Andoo A, Shimono M, Matsuki A, Kobayashi K, Ikeda M, Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol Cell Biol 2005;25:7770–7779.
   PubMed Web of Science ®Google Scholar
• Mus-Veteau I. 2002. Heterologous expression and purification systems for structural proteomics of mammalian membrane proteins. Comp Funct Genomics 3:511–517.
   PubMedGoogle Scholar
• Nedvetsky PI, Tamma G, Beulshausen S, Valenti G, Rosenthal W, Klussmann E. 2009. Regulation of aquaporin-2 trafficking. Handb Exp Pharmacol 190:133–157.
   Google Scholar
• Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME. 2001. Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci SA 98:14108–14113.
   PubMed Web of Science ®Google Scholar
• Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. 1997. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171–180.
   PubMed Web of Science ®Google Scholar
• Nielsen S, Smith BL, Christensen EI, Agre P. 1993. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci USA 90:7275–7279.
   PubMedGoogle Scholar
• Nyblom M, Oberg F, Lindkvist-Petersson K, Hallgren K, Findlay H, Wikstrom J, 2007. Exceptional overproduction of a functional human membrane protein. Protein Expr Purif 56:110–120.
   PubMedGoogle Scholar
• Oberg F, Ekvall M, Nyblom M, Backmark A, Neutze R, 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.
   PubMed Web of Science ®Google Scholar
• Oberg F, Sjohamn J, Conner MT, Bill RM, Hedfalk K. 2011a. Improving recombinant eukaryotic membrane protein yields in Pichia pastoris: the importance of codon optimization and clone selection. Mol Membr Biol 28:398–411.
   PubMed Web of Science ®Google Scholar
• Oberg F, Sjohamn J, Fischer G, Moberg A, Pedersen A, Neutze R, 2011b. Glycosylation increases the thermostability of human aquaporin 10. J Biol Chem 286:31915–31923.
   PubMedGoogle Scholar
• Perez-Martin J, Cases I, de Lorenzo V. 1997. Design of a solubilization pathway for recombinant polypeptides in vivo through processing of a bi-protein with a viral protease. Protein Eng 10:725–730.
   PubMedGoogle Scholar
• Petrovskaya LE, Shulga AA, Bocharova OV, Ermolyuk YS, Kryukova EA, Chupin VV, 2010. Expression of G-protein coupled receptors in Escherichia coli for structural studies. Biochemistry (Mosc) 75:881–891.
   PubMedGoogle Scholar
• Puigbo P, Bravo IG, Garcia-Vallve S. 2008. CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 3:38.
   PubMed Web of Science ®Google Scholar
• Rai T, Sasaki S, Uchida S. 2006. Polarized trafficking of the aquaporin-3 water channel is mediated by an NH2-terminal sorting signal. American journal of physiology. Cell physiology 290:C298–C304.
   Google Scholar
• Rice P. 2011. EMBOSS:isochore [Online] Accessed 28 March 2011 from. http://emboss.bioinformatics.nl/cgi-bin/emboss/isochore.
   Google Scholar
• Romanos MA, Scorer CA, Clare JJ. 1992. Foreign gene expression in yeast: A review. Yeast 8:423–488.
   PubMed Web of Science ®Google Scholar
• Roosild TP, Greenwald J, Vega M, Castronovo S, Riek R, Choe S. 2005. NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307:1317–1321
   PubMed Web of Science ®Google Scholar
• Sadlish H, Pitonzo D, Johnson AE, Skach WR. 2005. Sequential triage of transmembrane segments by Sec61alpha during biogenesis of a native multispanning membrane protein. Nat Struct Mol Biol 12:870–878.
   PubMedGoogle Scholar
• Sharp PM, Li WH. 1987. The codon Adaptation Index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295.
   PubMed Web of Science ®Google Scholar
• Shi LB, Skach WR, Ma T, Verkman AS. 1995. Distinct biogenesis mechanisms for the water channels MIWC and CHIP28 at the endoplasmic reticulum. Biochemistry 34:8250–8256.
   PubMed Web of Science ®Google Scholar
• Sinclair G, Choy FY. 2002. Synonymous codon usage bias and the expression of human glucocerebrosidase in the methylotrophic yeast, Pichia pastoris. Protein Expr Purif 26:96–105.
   PubMed Web of Science ®Google Scholar
• Skach WR, Shi LB, Calayag MC, Frigeri A, Lingappa VR, Verkman AS. 1994. Biogenesis and transmembrane topology of the CHIP28 water channel at the endoplasmic reticulum. J Cell Biol 125:803–815.
   PubMedGoogle Scholar
• Skowronski MT, Lebeck J, Rojek A, Praetorius J, Fuchtbauer EM, Frokiaer J, Nielsen S. 2007. AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am J Physiol Renal Physiol 292:F956–F965.
   PubMed Web of Science ®Google Scholar
• Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P. 1999. Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–187.
   PubMed Web of Science ®Google Scholar
• Tate CG. 2001. Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett 504:94–98.
   PubMed Web of Science ®Google Scholar
• Tate CG, Haase J, Baker C, Boorsma M, Magnani F, Vallis Y, 2003. Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim Biophys Acta 1610:141–153.
   PubMed Web of Science ®Google Scholar
• Tornroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, 2006. Structural mechanism of plant aquaporin gating. Nature 439:688–694.
   PubMed Web of Science ®Google Scholar
• Wang A, Clapper J, Guderian JA, Foy TM, Fanger GR, Retter MW, 2003. A novel method for increasing the expression level of recombinant proteins. Protein Expr Purif 30:124–133.
   PubMedGoogle Scholar
• White S. 2011. Database of Membrane Proteins of Known Structure [Online] Accessed 8 April 2011 from. http://blanco.biomol.uci.edu/Membrane_Proteins_xtal.html.
   Google Scholar
• Wright F. 1990. The 'effective number of codons' used in a gene. Gene 87:23–29.
   PubMed Web of Science ®Google Scholar
• Wu G, Culley DE, Zhang W. 2005. Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187.
   PubMed Web of Science ®Google Scholar
• Xia X. 2007. The +4G site in Kozak consensus is not related to the efficiency of translation initiation. PLoS One 2:e188.
   PubMed Web of Science ®Google Scholar