Applications of yeast surface display for protein engineering

Methods in Molecular Biology

Volumn 1319, Issue , 2015, Pages 155-175

  Cherf, Gerald M ^a   Cochran, Jennifer R ^a  

^a NONE

Author keywords

Affinity maturation; DNA shuffling; Enzyme engineering; Protein engineering; Protein stability engineering; Random mutagenesis; Yeast surface display

Indexed keywords

CELL MEMBRANE PROTEIN; HEMAGGLUTININ; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; CELL SURFACE; CELL SURFACE DISPLAY; DISSOCIATION CONSTANT; DNA SHUFFLING; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME SUBSTRATE; EPITOPE MAPPING; HEAT STRESS; MUTAGENESIS; NONHUMAN; PHAGE DISPLAY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; THERMOSTABILITY; YEAST CELL; BIOSYNTHESIS; GENETICS; METABOLISM; PROCEDURES;

SACCHAROMYCES CEREVISIAE;

CELL SURFACE DISPLAY TECHNIQUES; EPITOPE MAPPING; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN STABILITY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE;

BIOCHEMICAL ENGINEERING; CELL ENGINEERING; EPITOPES; GENETIC ENGINEERING; MEDICAL APPLICATIONS; YEAST;

AFFINITY MATURATION; DNA SHUFFLING; ENZYME ENGINEERING; PROTEIN ENGINEERING; PROTEIN STABILITY; RANDOM MUTAGENESIS; YEAST SURFACE DISPLAYS;

RECOMBINANT PROTEINS;

EID: 85011757987     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-2748-7_8     Document Type: Article

References (130)

1. He M, Taussig MJ (1997) Antibodyribosome- mRNA (ARM) complexes as efficient selection particles for in vitro display and evolution of antibody combining sites. Nucleic Acids Res 25:5132–5134
2. Hanes J, Plückthun A (1997) In vitro selection and evolution of functional proteins by using ribosome display. Proc Natl Acad Sci U S A 94:4937–4942
3. Roberts RW, Szostak JW (1997) RNApeptide fusions for the in vitro selection of peptides and proteins. Proc Natl Acad Sci U S A 94:12297–12302
4. Mattheakis LC, Bhatt RR, Dower WJ (1994) An in vitro polysome display system for identifying ligands from very large peptide libraries. Proc Natl Acad Sci U S A 91: 9022–9026
5. Mattheakis LC, Dias JM, Dower WJ (1996) Cell-free synthesis of peptide libraries displayed on polysomes. Methods Enzymol 267:195–207
6. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–1317
7. McCafferty J, Griffiths AD, Winter G, Chiswell DJ (1990) Phage antibodies: filamentous phage displaying antibody variable domains. Nature 348:552–554
8. Francisco JA, Campbell R, Iverson BL, Georgiou G (1993) Production and fluorescence- activated cell sorting of Escherichia coli expressing a functional antibody fragment on the external surface. Proc Natl Acad Sci U S A 90:10444–10448
9. Ho M, Nagata S, Pastan I (2006) Isolation of anti-CD22 Fv with high affinity by Fv display on human cells. Proc Natl Acad Sci U S A 103:9637–9642
10. Beerli RR et al (2008) Isolation of human monoclonal antibodies by mammalian cell display. Proc Natl Acad Sci U S A 105: 14336–14341
11. Ernst W et al (1998) Baculovirus surface display: construction and screening of a eukaryotic epitope library. Nucleic Acids Res 26:1718–1723
12. Boder ET, Wittrup KD (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 15: 553–557
13. Kondo A, Ueda M (2004) Yeast cell-surface display—applications of molecular display. Appl Microbiol Biotechnol 64:28–40
14. Boder ET, Wittrup KD (2000) Yeast surface display for directed evolution of protein expression, affinity, and stability. Methods Enzymol 328:430–444
15. Kapteyn JC, Van Den Ende H, Klis FM (1999) The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 1426:373–383
16. Roy A, Lu CF, Marykwas DL, Lipke PN, Kurjan J (1991) The AGA1 product is involved in cell surface attachment of the Saccharomyces cerevisiae cell adhesion glycoprotein a-agglutinin. Mol Cell Biol 11:4196–4206
17. Lu CF et al (1995) Glycosyl phosphatidylinositoldependent cross-linking of alpha-agglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J Cell Biol 128:333–340
18. Koide S, Koide A, Lipovšek D (2012) Targetbinding proteins based on the 10th human fibronectin type III domain (10 Fn3). Methods Enzymol 503:135–156
19. Scholler N (2012) Selection of antibody fragments by yeast display. Methods Mol Biol 907:259–280
20. Zhao Q, Zhu Z, Dimitrov DS (2012) Yeast display of engineered antibody domains. Methods Mol Biol 899:73–84
21. Chao G et al (2006) Isolating and engineering human antibodies using yeast surface display. Nat Protoc 1:755–768
22. Feldhaus MJ et al (2003) Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library. Nat Biotechnol 21:163–170
23. Miller KD, Pefaur NB, Baird CL (2008) Construction and screening of antigen targeted immune yeast surface display antibody libraries. Curr Protoc Cytom Chapter 4:Unit4.7
24. Wildt S, Gerngross TU (2005) The humanization of N-glycosylation pathways in yeast. Nat Rev Microbiol 3:119–128
25. De Pourcq K, De Schutter K, Callewaert N (2010) Engineering of glycosylation in yeast and other fungi: current state and perspectives. Appl Microbiol Biotechnol 87: 1617–1631
26. Gerngross TU (2004) Advances in the production of human therapeutic proteins in yeasts and filamentous fungi. Nat Biotechnol 22:1409–1414
27. VanAntwerp JJ, Wittrup KD (2000) Fine affinity discrimination by yeast surface display and flow cytometry. Biotechnol Prog 16: 31–37
28. Kieke MC, Cho BK, Boder ET, Kranz DM, Wittrup KD (1997) Isolation of anti-T cell receptor scFv mutants by yeast surface display. Protein Eng 10:1303–1310
29. Hackel BJ, Kapila A, Wittrup KD (2008) Picomolar affinity fibronectin domains engineered utilizing loop length diversity, recursive mutagenesis, and loop shuffling. J Mol Biol 381:1238–1252
30. Boder ET, Midelfort KS, Wittrup KD (2000) Directed evolution of antibody fragments with monovalent femtomolar antigen- binding affinity. Proc Natl Acad Sci U S A 97:10701–10705
31. Stemmer WP (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370:389–391
32. Lipovsek D et al (2007) Evolution of an interloop disulfide bond in high-affinity antibody mimics based on fibronectin type III domain and selected by yeast surface display: molecular convergence with single-domain camelid and shark antibodies. J Mol Biol 368:1024–1041
33. Holler PD et al (2000) In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc Natl Acad Sci U S A 97:5387–5392
34. Cochran JR, Kim Y-S, Lippow SM, Rao B, Wittrup KD (2006) Improved mutants from directed evolution are biased to orthologous substitutions. Protein Eng Des Sel 19:245–253
35. Rao BM, Girvin AT, Ciardelli T, Lauffenburger DA, Wittrup KD (2003) Interleukin-2 mutants with enhanced alpha-receptor subunit binding affinity. Protein Eng 16:1081–1087
36. Rao BM, Driver I, Lauffenburger DA, Wittrup KD (2005) High-affinity CD25- binding IL-2 mutants potently stimulate persistent T cell growth. Biochemistry 44:10696–10701
37. Shpilman M et al (2011) Development and characterization of high affinity leptins and leptin antagonists. J Biol Chem 286:4429–4442
38. Kariolis MS et al (2014) An engineered Axl “decoy receptor” effectively silences the Gas6-Axl signaling axis. Nat Chem Biol 10:977–983
39. Weiskopf K et al (2013) Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies. Science 341:88–91
40. Weiskopf K et al (2013) Improving macrophage responses to therapeutic antibodies by molecular engineering of SIRPα variants. Oncoimmunology 2:e25773
41. Tasumi S et al (2009) High-affinity lamprey VLRA and VLRB monoclonal antibodies. Proc Natl Acad Sci U S A 106:12891–12896
42. Walker LM, Bowley DR, Burton DR (2009) Efficient recovery of high-affinity antibodies from a single-chain Fab yeast display library. J Mol Biol 389:365–375
43. Shembekar N et al (2013) Isolation of a high affinity neutralizing monoclonal antibody against 2009 pandemic H1N1 virus that binds at the “Sa” antigenic site. PLoS One 8:e55516
44. Wozniak-Knopp G et al (2010) Introducing antigen-binding sites in structural loops of immunoglobulin constant domains: Fc fragments with engineered HER2/neu-binding sites and antibody properties. Protein Eng Des Sel 23:289–297
45. Rajpal A et al (2005) A general method for greatly improving the affinity of antibodies by using combinatorial libraries. Proc Natl Acad Sci U S A 102:8466–8471
46. Boder ET, Raeeszadeh-Sarmazdeh M, Price JV (2012) Engineering antibodies by yeast display. Arch Biochem Biophys 526:99–106
47. Moore SJ, Cochran JR (2012) Engineering knottins as novel binding agents. Methods Enzymol 503:223–251
48. Gera N, Hussain M, Rao BM (2013) Protein selection using yeast surface display. Methods 60:15–26
49. Silverman AP, Kariolis MS, Cochran JR (2011) Cystine-knot peptides engineered with specificities for α(IIb)β(3) or α(IIb)β(3) and α(v) β(3) integrins are potent inhibitors of platelet aggregation. J Mol Recognit 24:127–135
50. Kimura RH, Levin AM, Cochran FV, Cochran JR (2009) Engineered cystine knot peptides that bind alphavbeta3, alphavbeta5, and alpha5beta1 integrins with low-nanomolar affinity. Proteins 77:359–369
51. Silverman AP, Levin AM, Lahti JL, Cochran JR (2009) Engineered cystine-knot peptides that bind alpha(v)beta(3) integrin with antibodylike affinities. J Mol Biol 385:1064–1075
52. Moore SJ, Leung CL, Norton HK, Cochran JR (2013) Engineering agatoxin, a cystineknot peptide from spider venom, as a molecular probe for in vivo tumor imaging. PLoS One 8:e60498
53. Kimura RH et al (2011) Functional mutation of multiple solvent-exposed loops in the Ecballium elaterium trypsin inhibitor-II cystine knot miniprotein. PLoS One 6:e16112
54. Glotzbach B et al (2013) Combinatorial optimization of cystine-knot peptides towards high-affinity inhibitors of human matriptase-1. PLoS One 8:e76956
55. Koide A, Bailey CW, Huang X, Koide S (1998) The fibronectin type III domain as a scaffold for novel binding proteins. J Mol Biol 284:1141–1151
56. Lipovsek D (2011) Adnectins: engineered target-binding protein therapeutics. Protein Eng Des Sel 24:3–9
57. Bloom L, Calabro V (2009) FN3: a new protein scaffold reaches the clinic. Drug Discov Today 14:949–955
58. Pavoor TV, Cho YK, Shusta EV (2009) Development of GFP-based biosensors possessing the binding properties of antibodies. Proc Natl Acad Sci U S A 106:11895–11900
59. Lee C-H et al (2010) Engineering of a human kringle domain into agonistic and antagonistic binding proteins functioning in vitro and in vivo. Proc Natl Acad Sci U S A 107:9567–9571
60. Gera N, Hussain M, Wright RC, Rao BM (2011) Highly stable binding proteins derived from the hyperthermophilic Sso7d scaffold. J Mol Biol 409:601–616
61. Puri V, Streaker E, Prabakaran P, Zhu Z, Dimitrov DS (2013) Highly efficient selection of epitope specific antibody through competitive yeast display library sorting. MAbs 5:533–539
62. Shusta EV, Kieke MC, Parke E, Kranz DM, Wittrup KD (1999) Yeast polypeptide fusion surface display levels predict thermal stability and soluble secretion efficiency. J Mol Biol 292:949–956
63. Kowalski JM, Parekh RN, Wittrup KD (1998) Secretion efficiency in Saccharomyces cerevisiae of bovine pancreatic trypsin inhibitor mutants lacking disulfide bonds is correlated with thermodynamic stability. Biochemistry 37:1264–1273
64. Kowalski JM, Parekh RN, Mao J, Wittrup KD (1998) Protein folding stability can determine the efficiency of escape from endoplasmic reticulum quality control. J Biol Chem 273:19453–19458
65. Shusta EV, Holler PD, Kieke MC, Kranz DM, Wittrup KD (2000) Directed evolution of a stable scaffold for T-cell receptor engineering. Nat Biotechnol 18:754–759
66. Kim Y-S, Bhandari R, Cochran JR, Kuriyan J, Wittrup KD (2006) Directed evolution of the epidermal growth factor receptor extracellular domain for expression in yeast. Proteins 62:1026–1035
67. Esteban O, Zhao H (2004) Directed evolution of soluble single-chain human class II MHC molecules. J Mol Biol 340:81–95
68. Traxlmayr MW, Obinger C (2012) Directed evolution of proteins for increased stability and expression using yeast display. Arch Biochem Biophys 526:174–180
69. Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181–191
70. Sitia R, Braakman I (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426:891–894
71. Park S et al (2006) Limitations of yeast surface display in engineering proteins of high thermostability. Protein Eng Des Sel 19: 211–217
72. Pavoor TV, Wheasler JA, Kamat V, Shusta EV (2012) An enhanced approach for engineering thermally stable proteins using yeast display. Protein Eng Des Sel 25:625–630
73. Traxlmayr MW et al (2012) Directed evolution of stabilized IgG1-Fc scaffolds by application of strong heat shock to libraries displayed on yeast. Biochim Biophys Acta 1824:542–549
74. Traxlmayr MW et al (2013) Directed evolution of Her2/neu-binding IgG1-Fc for improved stability and resistance to aggregation by using yeast surface display. Protein Eng Des Sel 26:255–265
75. Jones DS, Tsai P-C, Cochran JR (2011) Engineering hepatocyte growth factor fragments with high stability and activity as Met receptor agonists and antagonists. Proc Natl Acad Sci U S A 108:13035–13040
76. Schweickhardt RL, Jiang X, Garone LM, Brondyk WH (2003) Structure-expression relationship of tumor necrosis factor receptor mutants that increase expression. J Biol Chem 278:28961–28967
77. Buonpane RA, Moza B, Sundberg EJ, Kranz DM (2005) Characterization of T cell receptors engineered for high affinity against toxic shock syndrome toxin-1. J Mol Biol 353:308–321
78. Jones LL et al (2006) Engineering and characterization of a stabilized alpha1/alpha2 module of the class I major histocompatibility complex product Ld. J Biol Chem 281: 25734–25744
79. Weber KS, Donermeyer DL, Allen PM, Kranz DM (2005) Class II-restricted T cell receptor engineered in vitro for higher affinity retains peptide specificity and function. Proc Natl Acad Sci U S A 102:19033–19038
80. Henke E, Bornscheuer UT (1999) Directed evolution of an esterase from Pseudomonas fluorescens. Random mutagenesis by error- prone PCR or a mutator strain and identification of mutants showing enhanced enantioselectivity by a resorufin-based fluorescence assay. Biol Chem 380:1029–1033
81. Sroga GE, Dordick JS (2001) Generation of a broad esterolytic subtilisin using combined molecular evolution and periplasmic expression. Protein Eng 14:929–937
82. Stevenson BJ, Yip SH-C, Ollis DL (2013) In vitro directed evolution of enzymes expressed by E. coli in microtiter plates. Methods Mol Biol 978:237–249
83. Tawfik DS, Griffiths AD (1998) Man-made cell-like compartments for molecular evolution. Nat Biotechnol 16:652–656
84. Griffiths AD, Tawfik DS (2003) Directed evolution of an extremely fast phosphotriesterase by in vitro compartmentalization. EMBO J 22:24–35
85. Lipovsek D et al (2007) Selection of horseradish peroxidase variants with enhanced enantioselectivity by yeast surface display. Chem Biol 14:1176–1185
86. Antipov E, Cho AE, Wittrup KD, Klibanov AM (2008) Highly L and D enantioselective variants of horseradish peroxidase discovered by an ultrahigh-throughput selection method. Proc Natl Acad Sci U S A 105:17694–17699
87. Chen I, Dorr BM, Liu DR (2011) A general strategy for the evolution of bond-forming enzymes using yeast display. Proc Natl Acad Sci U S A 108:11399–11404
88. Fushimi T et al (2013) Mutant firefly luciferases with improved specific activity and dATP discrimination constructed by yeast cell surface engineering. Appl Microbiol Biotechnol 97:4003–4011
89. Han S, Zhang J, Han Z, Zheng S, Lin Y (2011) Combination of site-directed mutagenesis and yeast surface display enhances Rhizomucor miehei lipase esterification activity in organic solvent. Biotechnol Lett 33:2431–2438
90. Zhang K et al (2013) Engineering the substrate specificity of the DhbE adenylation domain by yeast cell surface display. Chem Biol 20:92–101
91. White KA, Zegelbone PM (2013) Directed evolution of a probe ligase with activity in the secretory pathway and application to imaging intercellular protein-protein interactions. Biochemistry. doi: 10.1021/bi400268m
92. Yi L et al (2013) Engineering of TEV protease variants by yeast ER sequestration screening (YESS) of combinatorial libraries. Proc Natl Acad Sci U S A 110:7229–7234
93. Steffens DL, Williams JGK (2007) Efficient site-directed saturation mutagenesis using degenerate oligonucleotides. J Biomol Tech 18:147–149
94. Cochran JR, Kim Y-S, Olsen MJ, Bhandari R, Wittrup KD (2004) Domain-level antibody epitope mapping through yeast surface display of epidermal growth factor receptor fragments. J Immunol Methods 287:147–158
95. Chao G, Cochran JR, Wittrup KD (2004) Fine epitope mapping of anti-epidermal growth factor receptor antibodies through random mutagenesis and yeast surface display. J Mol Biol 342:539–550
96. Boersma YL, Chao G, Steiner D, Wittrup KD, Plückthun A (2011) Bispecific designed ankyrin repeat proteins (DARPins) targeting epidermal growth factor receptor inhibit A431 cell proliferation and receptor recycling. J Biol Chem 286:41273–41285
97. Han T et al (2011) Fine epitope mapping of monoclonal antibodies against hemagglutinin of a highly pathogenic H5N1 influenza virus using yeast surface display. Biochem Biophys Res Commun 409:253–259
98. Mata-Fink J et al (2013) Rapid conformational epitope mapping of anti-gp120 antibodies with a designed mutant panel displayed on yeast. J Mol Biol 425:444–456
99. 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 11:127–134
100. Gai SA, Wittrup KD (2007) Yeast surface display for protein engineering and characterization. Curr Opin Struct Biol 17:467–473
101. Bidlingmaier S, Liu B (2006) Construction and application of a yeast surface-displayed human cDNA library to identify posttranslational modification-dependent proteinprotein interactions. Mol Cell Proteomics 5:533–540
102. Bidlingmaier S et al (2009) Identification of MCAM/CD146 as the target antigen of a human monoclonal antibody that recognizes both epithelioid and sarcomatoid types of mesothelioma. Cancer Res 69:1570–1577
103. Bidlingmaier S, Liu B (2007) Interrogating yeast surface-displayed human proteome to identify small molecule-binding proteins. Mol Cell Proteomics 6:2012–2020
104. Kondo A, Tanaka T, Hasunuma T, Ogino C (2010) Applications of yeast cell-surface display in bio-refinery. Recent Pat Biotechnol 4:226–234
105. Tanaka T, Yamada R, Ogino C, Kondo A (2012) Recent developments in yeast cell surface display toward extended applications in biotechnology. Appl Microbiol Biotechnol 95:577–591
106. Fujita Y et al (2002) Direct and efficient production of ethanol from cellulosic material with a yeast strain displaying cellulolytic enzymes. Appl Environ Microbiol 68:5136–5141
107. Katahira S, Mizuike A, Fukuda H, Kondo A (2006) Ethanol fermentation from lignocellulosic hydrolysate by a recombinant xylose- and cellooligosaccharide-assimilating yeast strain. Appl Microbiol Biotechnol 72:1136–1143
108. Shigechi H et al (2004) Direct production of ethanol from raw corn starch via fermentation by use of a novel surface-engineered yeast strain codisplaying glucoamylase and alpha- amylase. Appl Environ Microbiol 70:5037–5040
109. Tsai S-L, DaSilva NA, Chen W (2013) Functional display of complex cellulosomes on the yeast surface via adaptive assembly. ACS Synth Biol 2:14–21
110. Kim S, Baek S-H, Lee K, Hahn J-S (2013) Cellulosic ethanol production using a yeast consortium displaying a minicellulosome and β-glucosidase. Microb Cell Fact 12:14
111. Tsai S-L, Oh J, Singh S, Chen R, Chen W (2009) Functional assembly of minicellulosomes on the Saccharomyces cerevisiae cell surface for cellulose hydrolysis and ethanol production. Appl Environ Microbiol 75:6087–6093
112. Tsai S-L, Goyal G, Chen W (2010) Surface display of a functional minicellulosome by intracellular complementation using a synthetic yeast consortium and its application to cellulose hydrolysis and ethanol production. Appl Environ Microbiol 76:7514–7520
113. 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 68:4517–4522
114. Pan X-X et al (2012) Efficient display of active Geotrichum sp. lipase on Pichia pastoris cell wall and its application as a whole-cell biocatalyst to enrich EPA and DHA in fish oil. J Agric Food Chem 60:9673–9679
115. Kim S, Oh D-B, Kwon O, Kang HA (2010) Construction of an in vitro trans-sialylation system: surface display of Corynebacterium diphtheriae sialidase on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 88: 893–903
116. Wang H et al (2013) Yeast surface displaying glucose oxidase as whole-cell biocatalyst: construction, characterization, and its electrochemical glucose sensing application. Anal Chem 85:6107–6112
117. Ren R et al (2007) Display of adenoregulin with a novel Pichia pastoris cell surface display system. Mol Biotechnol 35:103–108
118. Jo J-H, Im E-M, Kim S-H, Lee H-H (2011) Surface display of human lactoferrin using a glycosylphosphatidylinositol-anchored protein of Saccharomyces cerevisiae in Pichia pastoris. Biotechnol Lett 33:1113–1120
119. Shibasaki S et al (2013) An oral vaccine against candidiasis generated by a yeast molecular display system. Pathog Dis 69: 262–268
120. Tamaru Y et al (2006) Application of the arming system for the expression of the 380R antigen from red sea bream iridovirus (RSIV) on the surface of yeast cells: a first step for the development of an oral vaccine. Biotechnol Prog 22:949–953
121. Wasilenko JL, Sarmento L, Spatz S, Pantin- Jackwood M (2010) Cell surface display of highly pathogenic avian influenza virus hemagglutinin on the surface of Pichia pastoris cells using alpha-agglutinin for production of oral vaccines. Biotechnol Prog 26:542–547
122. Kotrba P, Ruml T (2010) Surface display of metal fixation motifs of bacterial P1-type ATPases specifically promotes biosorption of Pb(2+) by Saccharomyces cerevisiae. Appl Environ Microbiol 76:2615–2622
123. Kuroda K, Shibasaki S, Ueda M, Tanaka A (2001) Cell surface-engineered yeast displaying a histidine oligopeptide (hexa-His) has enhanced adsorption of and tolerance to heavy metal ions. Appl Microbiol Biotechnol 57:697–701
124. Kuroda K, Ueda M (2003) Bioadsorption of cadmium ion by cell surface-engineered yeasts displaying metallothionein and hexa-His. Appl Microbiol Biotechnol 63:182–186
125. Kuroda K, Ueda M, Shibasaki S, Tanaka A (2002) Cell surface-engineered yeast with ability to bind, and self-aggregate in response to, copper ion. Appl Microbiol Biotechnol 59:259–264
126. Kuroda K, Nishitani T, Ueda M (2012) Specific adsorption of tungstate by cell surface display of the newly designed ModE mutant. Appl Microbiol Biotechnol 96:153–159
127. Kuroda K, Ueda M (2006) Effective display of metallothionein tandem repeats on the bioadsorption of cadmium ion. Appl Microbiol Biotechnol 70:458–463
128. Nishitani T, Shimada M, Kuroda K, Ueda M (2010) Molecular design of yeast cell surface for adsorption and recovery of molybdenum, one of rare metals. Appl Microbiol Biotechnol 86:641–648
129. Midelfort KS et al (2004) Substantial energetic improvement with minimal structural perturbation in a high affinity mutant antibody. J Mol Biol 343:685–701
130. Pettersen EF et al (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612