Increasing gene dosage greatly enhances recombinant expression of aquaporins in Pichia pastoris

Wagner S, Bader ML, Drew D, de Gier JW: Rationalizing membrane protein overexpression. Trends Biotechnol. 2006, 24 (8): 364-371. 10.1016/j.tibtech.2006.06.008.

Junge F, Schneider B, Reckel S, Schwarz D, Dotsch V, Bernhard F: Large-scale production of functional membrane proteins. Cell Mol Life Sci. 2008, 65 (11): 1729-1755. 10.1007/s00018-008-8067-5.

Sarramegna V, Talmont F, Demange P, Milon A: Heterologous expression of G-protein-coupled receptors: comparison of expression systems fron the standpoint of large-scale production and purification. Cell Mol Life Sci. 2003, 60 (8): 1529-1546. 10.1007/s00018-003-3168-7.

Yin J, Li G, Ren X, Herrler G: Select what you need: a comparative evaluation of the advantages and limitations of frequently used expression systems for foreign genes. J Biotechnol. 2007, 127 (3): 335-347. 10.1016/j.jbiotec.2006.07.012.

Daly R, Hearn MT: Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J Mol Recognit. 2005, 18 (2): 119-138. 10.1002/jmr.687.

Grisshammer R: Understanding recombinant expression of membrane proteins. Curr Opin Biotechnol. 2006, 17 (4): 337-340. 10.1016/j.copbio.2006.06.001.

Cregg JM, Tolstorukov I, Kusari A, Sunga J, Madden K, Chappell T: Expression in the yeast Pichia pastoris. Methods Enzymol. 2009, 463: 169-189.

Cereghino JL, Cregg JM: Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol Rev. 2000, 24 (1): 45-66. 10.1111/j.1574-6976.2000.tb00532.x.

Doring F, Theis S, Daniel H: Expression and functional characterization of the mammalian intestinal peptide transporter PepT1 in the methylotropic yeast Pichia pastoris. Biochem Biophys Res Commun. 1997, 232 (3): 656-662. 10.1006/bbrc.1997.6351.

Parcej DN, Eckhardt-Strelau L: Structural characterisation of neuronal voltage-sensitive K+ channels heterologously expressed in Pichia pastoris. J Mol Biol. 2003, 333 (1): 103-116. 10.1016/j.jmb.2003.07.009.

Long SB, Campbell EB, Mackinnon R: Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 2005, 309 (5736): 897-903. 10.1126/science.1116269.

Strugatsky D, Gottschalk KE, Goldshleger R, Bibi E, Karlish SJ: Expression of Na+,K+-ATPase in Pichia pastoris: analysis of wild type and D369N mutant proteins by Fe2+-catalyzed oxidative cleavage and molecular modeling. J Biol Chem. 2003, 278 (46): 46064-46073. 10.1074/jbc.M308303200.

Lifshitz Y, Petrovich E, Haviv H, Goldshleger R, Tal DM, Garty H, Karlish SJ: Purification of the human alpha2 Isoform of Na,K-ATPase expressed in Pichia pastoris. Stabilization by lipids and FXYD1. Biochemistry. 2007, 46 (51): 14937-14950. 10.1021/bi701812c.

Talmont F, Sidobre S, Demange P, Milon A, Emorine LJ: Expression and pharmacological characterization of the human mu-opioid receptor in the methylotrophic yeast Pichia pastoris. FEBS Lett. 1996, 394 (3): 268-272. 10.1016/0014-5793(96)00971-4.

Weiss HM, Haase W, Michel H, Reilander H: Comparative biochemical and pharmacological characterization of the mouse 5HT5A 5-hydroxytryptamine receptor and the human beta2-adrenergic receptor produced in the methylotrophic yeast Pichia pastoris. Biochem J. 1998, 330 (Pt 3): 1137-1147.

Hori T, Sato Y, Takahashi N, Takio K, Yokomizo T, Nakamura M, Shimizu T, Miyano M: Expression, purification and characterization of leukotriene B(4) receptor, BLT1 in Pichia pastoris. Protein Expr Purif. 2010, 72 (1): 66-74. 10.1016/j.pep.2010.02.013.

Cai J, Gros P: Overexpression, purification, and functional characterization of ATP-binding cassette transporters in the yeast, Pichia pastoris. Biochim Biophys Acta. 2003, 1610 (1): 63-76. 10.1016/S0005-2736(02)00718-6.

Alisio A, Mueckler M: Purification and characterization of mammalian glucose transporters expressed in Pichia pastoris. Protein Expr Purif. 2010, 70 (1): 81-87. 10.1016/j.pep.2009.10.011.

Tyagi NK, Goyal P, Kumar A, Pandey D, Siess W, Kinne RK: High-yield functional expression of human sodium/d-glucose cotransporter1 in Pichia pastoris and characterization of ligand-induced conformational changes as studied by tryptophan fluorescence. Biochemistry. 2005, 44 (47): 15514-15524. 10.1021/bi051377q.

Sreekrishna K, Brankamp RG, Kropp KE, Blankenship DT, Tsay JT, Smith PL, Wierschke JD, Subramaniam A, Birkenberger LA: Strategies for optimal synthesis and secretion of heterologous proteins in the methylotrophic yeast Pichia pastoris. Gene. 1997, 190 (1): 55-62. 10.1016/S0378-1119(96)00672-5.

Romanos M, Scorer C, Sreekrishna K, Clare J: The generation of multicopy recombinant strains. Methods Mol Biol. 1998, 103: 55-72.

Invitrogen: EasySelect Pichia Expression Kit,version G. 2005, [ http://tools.invitrogen.com/content/sfs/manuals/easyselect_man.pdf ]

Werten MW, van den Bosch TJ, Wind RD, Mooibroek H, de Wolf FA: High-yield secretion of recombinant gelatins by Pichia pastoris. Yeast. 1999, 15 (11): 1087-1096. 10.1002/(SICI)1097-0061(199908)15:11<1087::AID-YEA436>3.0.CO;2-F.

Vedvick T, Buckholz RG, Engel M, Urcan M, Kinney J, Provow S, Siegel RS, Thill GP: High-level secretion of biologically active aprotinin from the yeast Pichia pastoris. J Ind Microbiol. 1991, 7 (3): 197-201. 10.1007/BF01575883.

McGrew JT, Leiske D, Dell B, Klinke R, Krasts D, Wee SF, Abbott N, Armitage R, Harrington K: Expression of trimeric CD40 ligand in Pichia pastoris: use of a rapid method to detect high-level expressing transformants. Gene. 1997, 187 (2): 193-200. 10.1016/S0378-1119(96)00747-0.

Brierley RA: Secretion of recombinant human insulin-like growth factor I (IGF-I). Methods Mol Biol. 1998, 103: 149-177.

Vassileva A, Chugh DA, Swaminathan S, Khanna N: Effect of copy number on the expression levels of hepatitis B surface antigen in the methylotrophic yeast Pichia pastoris. Protein Expr Purif. 2001, 21 (1): 71-80. 10.1006/prep.2000.1335.

Clare JJ, Rayment FB, Ballantine SP, Sreekrishna K, Romanos MA: High-level expression of tetanus toxin fragment C in Pichia pastoris strains containing multiple tandem integrations of the gene. Biotechnology (N Y). 1991, 9 (5): 455-460. 10.1038/nbt0591-455.

Liu SH, Chou WI, Sheu CC, Chang MD: Improved secretory production of glucoamylase in Pichia pastoris by combination of genetic manipulations. Biochem Biophys Res Commun. 2005, 326 (4): 817-824. 10.1016/j.bbrc.2004.11.112.

Mansur M, Cabello C, Hernandez L, Pais J, Varas L, Valdes J, Terrero Y, Hidalgo A, Plana L, Besada V, et al: Multiple gene copy number enhances insulin precursor secretion in the yeast Pichia pastoris. Biotechnol Lett. 2005, 27 (5): 339-345. 10.1007/s10529-005-1007-7.

Clare JJ, Romanos MA, Rayment FB, Rowedder JE, Smith MA, Payne MM, Sreekrishna K, Henwood CA: Production of mouse epidermal growth factor in yeast: high-level secretion using Pichia pastoris strains containing multiple gene copies. Gene. 1991, 105 (2): 205-212. 10.1016/0378-1119(91)90152-2.

Zhu T, Guo M, Tang Z, Zhang M, Zhuang Y, Chu J, Zhang S: Efficient generation of multi-copy strains for optimizing secretory expression of porcine insulin precursor in yeast Pichia pastoris. J Appl Microbiol. 2009, 107 (3): 954-963. 10.1111/j.1365-2672.2009.04279.x.

Sarramegna V, Demange P, Milon A, Talmont F: Optimizing functional versus total expression of the human mu-opioid receptor in Pichia pastoris. Protein Expr Purif. 2002, 24 (2): 212-220. 10.1006/prep.2001.1564.

Horsefield R, Norden K, Fellert M, Backmark A, Tornroth-Horsefield S, Terwisscha van Scheltinga AC, Kvassman J, Kjellbom P, Johanson U, Neutze R: High-resolution x-ray structure of human aquaporin 5. Proc Natl Acad Sci USA. 2008, 105 (36): 13327-13332. 10.1073/pnas.0801466105.

Karlsson M, Fotiadis D, Sjovall S, Johansson I, Hedfalk K, Engel A, Kjellbom P: Reconstitution of water channel function of an aquaporin overexpressed and purified from Pichia pastoris. FEBS Lett. 2003, 537 (1-3): 68-72. 10.1016/S0014-5793(03)00082-6.

Nyblom M, Oberg F, Lindkvist-Petersson K, Hallgren K, Findlay H, Wikstrom J, Karlsson A, Hansson O, Booth PJ, Bill RM, et al: Exceptional overproduction of a functional human membrane protein. Protein Expr Purif. 2007, 56 (1): 110-120. 10.1016/j.pep.2007.07.007.

Daniels MJ, Yeager M: Phosphorylation of aquaporin PvTIP3;1 defined by mass spectrometry and molecular modeling. Biochemistry. 2005, 44 (44): 14443-14454. 10.1021/bi050565d.

Hedfalk K, Pettersson N, Oberg F, Hohmann S, Gordon E: Production, characterization and crystallization of the Plasmodium falciparum aquaporin. Protein Expr Purif. 2008, 59 (1): 69-78. 10.1016/j.pep.2008.01.004.

King LS, Kozono D, Agre P: From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol. 2004, 5 (9): 687-698. 10.1038/nrm1469.

Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F: Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta. 2009, 1788 (6): 1213-1228. 10.1016/j.bbamem.2009.03.009.

Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S: Aquaporin water channels--from atomic structure to clinical medicine. J Physiol. 2002, 542 (Pt 1): 3-16.

Backmark A, Nyblom M, Tornroth-Horsefield S, Kosinska-Eriksson U, Norden K, Fellert M, Kjellbom P, Johanson U, Hedfalk K, Lindkvist-Petersson K, et al: Affinity tags can reduce merohedral twinning of membrane protein crystals. Acta Crystallogr D Biol Crystallogr. 2008, 64 (Pt 11): 1183-1186.

Sunga AJ, Tolstorukov I, Cregg JM: Posttransformational vector amplification in the yeast Pichia pastoris. FEMS Yeast Res. 2008, 8 (6): 870-876. 10.1111/j.1567-1364.2008.00410.x.

Abdelmoula-Souissi S, Rekik L, Gargouri A, Mokdad-Gargouri R: High-level expression of human tumour suppressor P53 in the methylotrophic yeast: Pichia pastoris. Protein Expr Purif. 2007, 54 (2): 283-288. 10.1016/j.pep.2007.03.015.

Maeshima M, Ishikawa F: ER membrane aquaporins in plants. Pflugers Arch. 2008, 456 (4): 709-716. 10.1007/s00424-007-0363-7.

Fotiadis D, Jeno P, Mini T, Wirtz S, Muller SA, Fraysse L, Kjellbom P, Engel A: Structural characterization of two aquaporins isolated from native spinach leaf plasma membranes. J Biol Chem. 2001, 276 (3): 1707-1714. 10.1074/jbc.M009383200.

Abramoff MD, Magelhaes PJ, Ram SJ: Image Processing with ImageJ. Biophotonics International. 2004, 11 (7): 36-42.

Rozen S, Skaletsky H: Primer3 on the www for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.

Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29 (9): e45-10.1093/nar/29.9.e45.