Abstract
Proteins with internal repeats (Pir) in the Baker’s yeast are located on the cell wall and include four highly homologous members. Recently, Pir proteins have become increasingly used as anchor proteins in yeast cell surface display systems. These display systems are classified into three types: N-terminal fusion, C-terminal fusion, and inserted fusion. In addition to the GPI (glycosylphosphatidyl inositol) and the FL/FS anchor proteins, these three Pir-based systems significantly increase the choices for target proteins to be displayed. Furthermore, Pir proteins can also be used as a fusion partner for target proteins to be effectively secreted into culture medium. Here, we summarize the development and application of Pir proteins as anchor proteins.
Similar content being viewed by others
References
Abe H (2003) In vitio oligosaccharide synthesis using intact yeast cell that display glucisylteansferases at the cell surface through cell wall-anchored protein Pir. Glycobiology 13(2):87–95
Abe H, Ohba M, Shimma Y, Jigami Y (2004) Yeast cells harboring human α-1,3-fucosyltransferase at the cell surface engineered using Pir, a cell wall-anchored protein. FEMS Yeast Res 4(4–5):417–425. doi:10.1016/s1567-1356(03)00193-4
Andres I, Gallardo O, Parascandola P, Javier Pastor FI, Zueco J (2005) Use of the cell wall protein Pir4 as a fusion partner for the expression of Bacillus sp. BP-7 xylanase A in Saccharomyces cerevisiae. Biotechnol Bioeng 89(6):690–697. doi:10.1002/bit.20375
Andres I, Rodriguez-Diaz J, Buesa J, Zueco J (2006) Yeast expression of the VP8* fragment of the rotavirus spike protein and its use as immunogen in mice. Biotechnol Bioeng 93(1):89–98. doi:10.1002/bit.20696
Boder ET, Wittrup KD (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 15(6):553–557
Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459(7247):657–662
Castillo L, Martinez AI, Garcera A, Elorza MV, Valentin E, Sentandreu R (2003) Functional analysis of the cysteine residues and the repetitive sequence of Saccharomyces cerevisiae Pir4/Cis3: the repetitive sequence is needed for binding to the cell wall beta-1,3-glucan. Yeast 20(11):973–983. doi:10.1002/yea.1016
Charbit A, Boulain JC, Ryter A, Hofnung M (1986) Probing the topology of a bacterial membrane protein by genetic insertion of a foreign epitope; expression at the cell surface. EMBO J 5(11):3029
De Groot PW, Ram AF, Klis FM (2005) Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 42(8):657–675. doi:10.1016/j.fgb.2005.04.002
Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuvéglise C, Talla E (2004) Genome evolution in yeasts. Nature 430(6995):35–44
Ecker M, Deutzmann R, Lehle L, Mrsa V, Tanner W (2006) Pir proteins of Saccharomyces cerevisiae are attached to β-1, 3-glucan by a new protein–carbohydrate linkage. J Biol Chem 281(17):11523–11529
Efimov VP, Nepluev IV, Mesyanzhinov VV (1995) Bacteriophage T4 as a surface display vector. Virus Genes 10(2):173–177
Ernst WJ, Spenger A, Toellner L, Katinger H, Grabherr RM (2000) Expanding baculovirus surface display. Eur J Biochem 267(13):4033–4039
Goossens KVY, Stassen C, Stals I, Donohue DS, Devreese B, De Greve H, Willaert RG (2011) The N-terminal domain of the Flo1 flocculation protein from Saccharomyces cerevisiae binds specifically to mannose carbohydrates. Eukaryot Cell 10(1):110–117
Gordon JL, Armisén D, Proux-Wéra E, ÓhÉigeartaigh SS, Byrne KP, Wolfe KH (2011) Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. Proc Natl Acad Sci U S A 108(50):20024–20029
Jaafar L, Moukadiri I, Zueco J (2003) Characterization of a disulphide-bound Pir-cell wall protein (Pir-CWP) of Yarrowia lipolytica. Yeast 20(5):417–426. doi:10.1002/yea.973
Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, Magee BB, Newport G, Thorstenson YR, Agabian N, Magee PT (2004) The diploid genome sequence of Candida albicans. Proc Natl Acad Sci USA 101(19):7329–7334. doi:10.1073/pnas.0401648101
Khasa YP, Conrad S, Sengul M, Plautz S, Meagher MM, Inan M (2011) Isolation of Pichia pastoris PIR genes and their utilization for cell surface display and recombinant protein secretion. Yeast 28(3):213–226. doi:10.1002/yea.1832
Kondo A, Ueda M (2004) Yeast cell-surface display—applications of molecular display. Appl Microbiol Biotechnol 64(1):28–40
Lattemann CT, Maurer J, Gerland E, Meyer TF (2000) Autodisplay: functional display of active β-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J Bacteriol 182(13):3726–3733
Liu W-S, Pan X-X, Jia B, Zhao H-Y, Xu L, Liu Y, Yan Y-J (2010) Surface display of active lipases Lip7 and Lip8 from Yarrowia lipolytica on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 88(4):885–891
Louis VL, Despons L, Friedrich A, Martin T, Durrens P, Casarégola S, Neuvéglise C, Fairhead C, Marck C, Cruz JA (2012) Pichia sorbitophila, an interspecies yeast hybrid, reveals early steps of genome resolution after polyploidization. G3: Genes Genomes Genet 2(2):299–311
Martínez AI, Castillo L, Garcerá A, Elorza MV, Valentín E, Sentandreu R (2004) Role of Pir1 in the construction of the Candida albicans cell wall. Microbiology 150(10):3151–3161
Matsumoto T, Fukuda H, Ueda M, Tanaka A, Kondo A (2002) Construction of yeast strains with high cell surface lipase activity by using novel display systems based on the Flo1p flocculation functional domain. Appl Environ Microbiol 68(9):4517–4522. doi:10.1128/aem.68.9.4517-4522.2002
Mormeneo M, Andrés I, Bofill C, Díaz P, Zueco J (2008) Efficient secretion of Bacillus subtilis lipase A in Saccharomyces cerevisiae by translational fusion to the Pir4 cell wall protein. Appl Microbiol Biotechnol 80(3):437–445
Mormeneo M, Pastor FJ, Zueco J (2012) Efficient expression of a Paenibacillus barcinonensis endoglucanase in Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 39(1):115–123
Moukadiri I, Zueco J (2001a) Evidence for the attachment of Hsp150/Pir2 to the cell wall of Saccharomyces cerevisiae through disulfide bridges. FEMS Yeast Res 1(3):241–245
Moukadiri I, Zueco J (2001b) YJL159w does encode Pir2/Hsp150. Yeast 18(4):323–324
Moukadiri I, Jaafar L, Zueco J (1999) Identification of two mannoproteins released from cell walls of a Saccharomyces cerevisiae mnn1 mnn9 double mutant by reducing agents. J Bacteriol 181(16):4741–4745
Mrsă V, Seidl T, Gentzsch M, Tanner W (1997) Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13(12):1145–1154
Paciello L, Andrès I, Zueco J, Bianchi MM, de Alteriis E, Parascandola P (2010) Expression of human interleukin-1β in Saccharomyces cerevisiae using PIR4 as fusion partner and production in aerated fed-batch reactor. Ann Microbiol 60(4):719–728
Pepper LR, Cho YK, Boder ET, Shusta EV (2008) A decade of yeast surface display technology: where are we now? Comb Chem High Throughput Screen 11(2):127
Russo P, Kalkkinen N, Sareneva H, Paakkola J, Makarow M (1992) A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc Natl Acad Sci 89(9):3671–3675
Scannell DR, Frank AC, Conant GC, Byrne KP, Woolfit M, Wolfe KH (2007) Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc Natl Acad Sci 104(20):8397–8402
Shimma Y-i, Jigami Y (2004) Expression of human glycosyltransferase genes in yeast as a tool for enzymatic synthesis of sugar chain. Glycoconj J 21(1–2):75–78
Shimma Y, Saito F, Oosawa F, Jigami Y (2006) Construction of a library of human glycosyltransferases immobilized in the cell wall of Saccharomyces cerevisiae. Appl Environ Microbiol 72(11):7003–7012. doi:10.1128/AEM.01378-06
Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228(4705):1315–1317
Souciet J-L, Aigle M, Artiguenave F, Blandin G, Bolotin-Fukuhara M, Bon E, Brottier P, Casaregola S, de Montigny J, Dujon B (2000) Genomic exploration of the hemiascomycetous yeasts: 1. A set of yeast species for molecular evolution studies. FEBS Lett 487(1):3–12
Starwalt SE, Masteller EL, Bluestone JA, Kranz DM (2003) Directed evolution of a single-chain class II MHC product by yeast display. Protein Eng Des Sel 16(2):147–156. doi:10.1093/proeng/gzg018
Sumita T, Yoko-o T, Shimma Y, Jigami Y (2005) Comparison of cell wall localization among Pir family proteins and functional dissection of the region required for cell wall binding and bud scar recruitment of Pir1p. Eukaryot Cell 4(11):1872–1881
Tanaka T, Yamada R, Ogino C, Kondo A (2012) Recent developments in yeast cell surface display toward extended applications in biotechnology. Appl Microbiol Biotechnol 95(3):577–591. doi:10.1007/s00253-012-4175-0
Toh-E A, Oguchi T, Matsui Y, Yasunaga S, Nisogi H, Tanaka K (1993) Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock. Yeast 9(5):481–494
van der Vaart JM, Caro L, Chapman JW, Klis FM, Verrips CT (1995) Identification of three mannoproteins in the cell wall of Saccharomyces cerevisiae. J Bacteriol 177(11):3104–3110
Van der Vaart JM, Te Biesebeke R, Chapman JW, Toschka HY, Klis FM, Verrips CT (1997) Comparison of cell wall proteins of Saccharomyces cerevisiae as anchors for cell surface expression of heterologous proteins. Appl Environ Microbiol 63(2):615–620
Wang Q, Li L, Chen M, Qi Q, Wang PG (2008) Construction of a novel Pichia pastoris cell-surface display system based on the cell wall protein Pir1. Curr Microbiol 56(4):352–357. doi:10.1007/s00284-007-9089-1
Watari J, Takata Y, Ogawa M, Sahara H, Koshino S, Onnela ML, Airaksinen U, Jaatinen R, Penttilä M, Keränen S (1994) Molecular cloning and analysis of the yeast flocculation gene FLO1. Yeast 10(2):211–225
Yin QY, de Groot PW, Dekker HL, de Jong L, Klis FM, de Koster CG (2005) Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls identification of proteins covalently attached via glycosylphosphatidylinosotol remnants or mild alkali-sensitive linkages. J Biol Chem 280(21):20894–20901
Acknowledgments
This work was supported by the National Key Basic Research Development Plan (973 Project) (no. 2013CB127506), by The National Natural Science Foundation (no.31360130), by Hi-tech Research Development Plan of Yunnan Province (approval nos. 2009YG-3B), by Yunnan University (grant no. 2005Z004B), and by Tobacco’s Hi-tech Plan of Yunnan Province tobacco company (grant no. 2012YN06).
Conflict of interest
The authors declare that they have no conflict of interest. Na Yang and Zefen Yu contributed equally to this paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yang, N., Yu, Z., Jia, D. et al. The contribution of Pir protein family to yeast cell surface display. Appl Microbiol Biotechnol 98, 2897–2905 (2014). https://doi.org/10.1007/s00253-014-5538-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-014-5538-5