Skip to main content
SpringerLink
Log in

Prospects for the Application of Yeast Display in Biotechnology and Cell Biology (Review)

  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

The technology of the yeast cell surface display, which appeared 20 years ago and was based on the displaying of target proteins on the cell surface via fusion to an abundant cell wall protein finds broad application in basic and applied research. The main advantage of the cell surface display on the basis of eukaryotic microorganisms—yeast—is the opportunity for correct modification of mammalian proteins. The cell surface display is an important tool for the analysis and understanding of protein function and protein–protein interactions and for the screening of novel clones from peptide and protein libraries. This technology makes it possible to obtain cells with novel abilities, such as catalytic functions and affinity binding to valuable ligands, including rare and heavy metals. It provides the chance to use yeast in biotechnology and in bioremediation and biomonitoring of the environment. The review considers the methods of obtaining a cell surface display on the basis of the yeasts Saccharomyces cerevisiae, Pichia pastoris, and Yarrowia lipolytica, the properties of anchor proteins, and the main fields of yeast display technology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Pack, S.P., Park, K., and Yoo, Y.J., Biotechnol. Lett., 2002, vol. 24, no. 22, p. 1919–1925.

    Article  CAS  Google Scholar 

  2. Smith, G.P., Science, 1985, vol. 228, no. 4705, pp. 1315–1317.

    Article  PubMed  CAS  Google Scholar 

  3. Tan, Y., Tian, T., Liu, W., Zhu, Z., and Yang, C., Biotechnol. J., 2016, vol. 11, no. 6, pp. 732–745.

    Article  PubMed  CAS  Google Scholar 

  4. Francisco, J.A. and Georgiou, G., Ann. N.Y. Acad. Sci., 1994, vol. 745, pp. 372–382.

    Article  PubMed  CAS  Google Scholar 

  5. Samuelson, P., Gunneriusson, E., Nygren, P.A., and Stahl, S., J. Biotechnol., 2002, vol. 96, no. 2, pp. 129–154.

    Article  PubMed  CAS  Google Scholar 

  6. Mazmanian, S.K., Liu, G., Ton-That, H., and Schneewind, O., Science, 1999, vol. 285, no. 5428, pp. 760–763.

    Article  PubMed  CAS  Google Scholar 

  7. Stahl, S., Robert, A., Gunneriusson, E., Wernerus, H., Cano, F., Liljeqvist, S., Hansson, M., Nguyen, T.N., and Samuelson, P., Int. J. Med. Microbiol., 2000, vol. 290, no. 7, pp. 571–577.

    Article  PubMed  CAS  Google Scholar 

  8. Piard, J.C., Hautefort, I., Fischetti, V.A., Ehrlich, S.D., Fons, M., and Gruss, A., J. Bacteriol., 1997, vol. 179, no. 9, pp. 3068–3072.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Narita, J., Okano, K., Kitao, T., Ishida, S., Sewaki, T., Sung, M.H., Fukuda, H., and Kondo, A., Appl. Environ. Microbiol., 2006, vol. 72, no. 1, pp. 269–275.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Tanaka, T. and Kondo, A., Biotechnol. Adv., 2015, vol. 33, no. 7, pp. 1403–1411.

    Article  PubMed  CAS  Google Scholar 

  11. Lofblom, J., Wernerus, H., and Stahl, S., FEMS Microbiol. Letts., 2005, vol. 248, no. 2, pp. 189–198.

    Article  CAS  Google Scholar 

  12. Boder, E.T. and Wittrup, K.D., Nat. Biotechnol., 1997, vol. 15, no. 6, pp. 553–557.

    Article  PubMed  CAS  Google Scholar 

  13. Shibasaki, S., Maeda, H., and Ueda, M., Anal. Sci., 2009, vol. 25, no. 1, pp. 41–49.

    Article  PubMed  CAS  Google Scholar 

  14. Orlean, P., Genetics, 2012, vol. 192, no. 3, pp. 775–818.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Van der Vaart, J.M., te Biesebeke, R., Chapman, J.W., Toschka, H.Y., Klis, F.M., and Verrips, C.T., Appl. Environ. Microbiol., 1997, vol. 63, no. 2, pp. 615–620.

    PubMed  PubMed Central  Google Scholar 

  16. Hamada, K., Terashima, H., Arisawa, M., and Kitada, K., J. Biol. Chem., 1998, vol. 273, no. 41, pp. 26946–26953.

    Article  PubMed  CAS  Google Scholar 

  17. Tanaka, T., Yamada, R., Ogino, C., and Kondo, A., Appl. Microbiol. Biotechnol., 2012, vol. 95, no. 3, pp. 577–591.

    Article  PubMed  CAS  Google Scholar 

  18. Goossens, K. and Willaert, R., Biotechnol. Lett., 2010, vol. 32, no. 11, pp. 1571–1585.

    Article  PubMed  CAS  Google Scholar 

  19. Sato, N., Matsumoto, T., Ueda, M., Tanaka, A., Fukuda, H., and Kondo, A., Appl. Microbiol. Biotechnol., 2002, vol. 60, no. 4, pp. 469–474.

    Article  PubMed  CAS  Google Scholar 

  20. Matsumoto, T., Fukuda, H., Ueda, M., Tanaka, A., and Kondo, A., Appl. Environ. Microbiol., 2002, vol. 68, no. 9, pp. 4517–4522.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Toh-E, A., Oguchi, T., Matsui, Y., Yasunaga, S., Nisogi, H., and Tanaka, K., Yeast, 1993, vol. 9, no. 5, pp. 481–494.

    Article  PubMed  CAS  Google Scholar 

  22. Russo, P., Kalkkinen, N., Sareneva, H., Paakkola, J., and Makarow, M., Proc. Natl. Acad. Sci. U.S.A., 1992, vol. 89, no. 18, pp. 3671–3675.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Mrsa, V., Seidl, T., Gentzsch, M., and Tanner, W., Yeast, 1997, vol. 13, no. 12, pp. 1145–1154.

    Article  PubMed  CAS  Google Scholar 

  24. Castillo, L., Martinez, A.I., Garcera, A., Elorza, M.V., Valentin, E., and Sentandreu, R., Yeast, 2003, vol. 20, no. 11, pp. 973–983.

    Article  PubMed  CAS  Google Scholar 

  25. Moukadiri, I. and Zueco, J., FEMS Yeast Res., 2001, vol. 1, no. 3, pp. 241–245.

    PubMed  CAS  Google Scholar 

  26. Ecker, M., Deutzmann, R., Lehle, L., Mrsa, V., and Tanner, W., J. Biol. Chem., 2006, vol. 281, no. 17, pp. 11523–11529.

    Article  PubMed  CAS  Google Scholar 

  27. Abe, H., Ohba, M., Shimma, Y., and Jigami, Y., FEMS Yeast Res., 2004, vol. 4, nos. 4–5, pp. 417–425.

    Article  PubMed  CAS  Google Scholar 

  28. Wentz, A.E. and Shusta, E.V., Appl. Environ. Microbiol., 2007, vol. 73, no. 4, pp. 1189–1198.

    Article  PubMed  CAS  Google Scholar 

  29. Rumjantsev, A.M., Bondareva, O.V., Padkina, M.V., and Sambuk, E.V., Sci. World J., 2014, vol. 2014, article ID 743615, p. 9. https://doi.org/10.1155/2014/743615.

    Article  Google Scholar 

  30. Cereghino, G.P.L., Cereghino, J.L., Ilgen, C., and Cregg, J.M., Curr. Opin. Biotech., 2002, vol. 13, no. 4, pp. 329–332.

    Article  PubMed  Google Scholar 

  31. Heyland, J., Fu, J.A., Blank, L.M., and Schmid, A., Biotechnol. Bioeng., 2010, vol. 107, no. 2, pp. 357–368.

    Article  PubMed  CAS  Google Scholar 

  32. Celik, E. and Callk, P., Biotechnol. Adv., 2012, vol. 30, no. 5, pp. 1108–1118.

    Article  PubMed  CAS  Google Scholar 

  33. Mergler, M., Wolf, K., and Zimmermann, M., Appl. Microbiol. Biotechnol., 2004, vol. 63, no. 4, pp. 418–421.

    Article  PubMed  CAS  Google Scholar 

  34. Khasa, Y.P., Conrad, S., Sengul, M., Plautz, S., Meagher, M.M., and Inan, M., Yeast, 2011, vol. 28, no. 3, pp. 213–226.

    Article  PubMed  CAS  Google Scholar 

  35. Bankar, A.V., Kumar, A.R., and Zinjarde, S.S., Appl. Microbiol. Biotechnol., 2009, vol. 84, no. 5, pp. 847–865.

    Article  PubMed  CAS  Google Scholar 

  36. Wang, H.J., Le Dall, M.T., Wach, Y., Laroche, C., Belin, J.M., Gaillardin, C., and Nicaud, J.M., J. Bacteriol., 1999, vol. 181, no. 17, pp. 5140–5148.

    PubMed  PubMed Central  CAS  Google Scholar 

  37. Zvyagilskaya, R. and Persson, B.L., Cell. Biol. Int., 2005, vol. 29, no. 1, pp. 87–94.

    Article  PubMed  CAS  Google Scholar 

  38. Madzak, C., Gaillardin, C., and Beckerich, J.M., J. Biotechnol., 2004, vol. 109, nos. 1–2, pp. 63–81.

    Article  PubMed  CAS  Google Scholar 

  39. Bordes, F., Fudalej, F., Dossat, V., Nicaud, J.M., and Marty, A., J. Microbiol. Methods, 2007, vol. 70, no. 3, pp. 493–502.

    Article  PubMed  CAS  Google Scholar 

  40. Liu, H.H., Ji, X.J., and Huang, H., Biotechnol. Adv., 2015, vol. 33, no. 8, pp. 1522–1546.

    Article  PubMed  CAS  Google Scholar 

  41. Sekova, V.Yu., Isakova, E.P., and Deryabina, Yu.I., App. Biochem. Microbiol., 2015, vol. 51, no. 3, pp. 290–304.

    Google Scholar 

  42. Zhu, Q. and Jackson, E.N., Curr. Opin. Biotechnol., 2015, vol. 36, pp. 65–72.

    Article  PubMed  CAS  Google Scholar 

  43. Yuzbasheva, E.Y., Yuzbashev, T.V., Laptev, I.A., Konstantinova, T.K., and Sineoky, S.P., Appl. Microbiol. Biotechnol., 2011, vol. 91, no. 3, pp. 645–654.

    Article  PubMed  CAS  Google Scholar 

  44. Duquesne, S., Bozonnet, S., Bordes, F., Dumon, C., Nicaud, J.M., and Marty, A., PLoS One, 2014, vol. 9, no. 4. e95128. doi 10.1371/journal.pone.0095128

    Article  PubMed  PubMed Central  Google Scholar 

  45. Jaafar, L. and Zueco, J., Microbiology, 2004, vol. 150, no. 1, pp. 53–60.

    Article  PubMed  CAS  Google Scholar 

  46. Varfolomeev, S.D., Efremenko, E.N., and Krylova, L.P., Usp. Khim., 2010, vol. 79, no. 6, pp. 544–564.

    Article  CAS  Google Scholar 

  47. Akbas, M.Y. and Stark, B.C., J. Ind. Microbiol. Biotechnol., 2016, vol. 43, pp. 1593–1609.

    Article  PubMed  CAS  Google Scholar 

  48. Van Zyl, W.H., Bloom, M., and Viktor, M.J., Appl. Microbiol. Biotechnol., 2012, vol. 95, no. 6, pp. 1377–1388.

    Article  PubMed  CAS  Google Scholar 

  49. Su, G.D., Zhang, X., and Lin, Y., Biotechnol. Lett., 2010, vol. 32, no. 8, pp. 1131–1136.

    Article  PubMed  CAS  Google Scholar 

  50. Murai, T., Ueda, M., Yamamura, M., Atomi, H., Shibasaki, Y., Kamasawa, N., Osumi, M., Amachi, T., and Tanaka, A., Appl. Environ. Microbiol., 1997, vol. 63, no. 4, pp. 1362–1366.

    PubMed  PubMed Central  CAS  Google Scholar 

  51. Murai, T., Ueda, M., Shibasaki, Y., Kamasawa, N., Osumi, M., Imanaka, T., and Tanaka, A., Appl. Microbiol. Biotechnol., 1999, vol. 51, no. 1, pp. 65–70.

    Article  PubMed  CAS  Google Scholar 

  52. Shigechi, H., Koh, J., Fujita, Y., Matsumoto, T., Bito, Y., Ueda, M., Satoh, E., Fukuda, H., and Kondo, A., Appl. Environ. Microbiol., 2004, vol. 70, no. 8, pp. 5037–5040.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Yamakawa, S., Yamada, R., Tanaka, T., Ogino, C., and Kondo, A., Enzyme Microb. Technol., 2012, vol. 50, nos. 6–7, pp. 343–347.

    Article  PubMed  CAS  Google Scholar 

  54. Kheldt, G.V., Biokhimiya rastenii (Plant Biochemistry), Moscow: Binom. Laboratoriya znanii, 2011, pp. 21–24.

    Google Scholar 

  55. Rabinovich, M.L. and Mel’nik, M.S., Usp. Biol. Khim., 2000, vol. 40, pp. 205–266.

    CAS  Google Scholar 

  56. Inokuma, K., Hasunuma, T., and Kondo, A., Biotechnol. Biofuels, 2014, vol. 7, p. 8. doi 10.1186/1754-6834-7-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Van Zyl, W.H., Lynd, L.R., Haan, R., and McBride, J.E., Adv. Biochem. Eng. Biotechnol., 2007, vol. 108, no. 2, pp. 205–235.

    PubMed  Google Scholar 

  58. Fujita, Y., Ito, J., Ueda, M., Fukuda, H., and Kondo, A., Appl. Environ. Microbiol., 2004, vol. 70, no. 2, pp. 1207–1212.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Murai, T., Ueda, M., Kawaguchi, T., Arai, M., and Tanaka, A., Appl. Environ. Microbiol., 1998, vol. 64, no. 12, pp. 4857–4861.

    PubMed  PubMed Central  CAS  Google Scholar 

  60. Fujita, Y., Takahashi, S., Ueda, M., Tanaka, A., Okada, H., Morikawa, Y., Kawaguchi, T., Arai, M., Fukuda, H., and Kondo, A., Appl. Environ. Microbiol., 2002, vol. 68, no. 10, pp. 5136–5141.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Schwarz, W.H., Appl. Microbiol. Biotechnol., 2001, vol. 56, nos. 5–6, pp. 634–649.

    Article  PubMed  CAS  Google Scholar 

  62. Tsai, S.L., Goyal, G., and Chen, W., Appl. Environ. Microbiol., 2010, vol. 76, no. 22, pp. 7514–7520.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Spellman, P.T., Sherlock, G., Zhang, M.Q., Iyer, V.R., Anders, K., Eisen, M.B., Brown, P.O., Botstein, D., and Futcher, B., Mol. Biol. Cell, 1998, vol. 9, no. 12, pp. 3273–3297.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Rozanov, A.S., Kotenko, A.V., Akberdin, I.R., and Pel’tek, S.E., Vavilov. Zh. Genet. Selekt., 2014, vol. 18, no. 4/2, pp. 989–998.

    Google Scholar 

  65. Katahira, S., Fujita, Y., Mizuike, A., Fukuda, H., and Kondo, A., Appl. Environ. Microbiol., 2004, vol. 70, no. 9, pp. 5407–5414.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Katahira, S., Mizuike, A., Fukuda, H., and Kondo, A., Appl. Microbiol. Biotechnol., 2006, vol. 72, no. 6, pp. 1136–1143.

    Article  PubMed  CAS  Google Scholar 

  67. Ota, M., Sakuragi, H., Morisaka, H., Kuroda, K., Miyake, H., Tamaru, Y., and Ueda, M., Biotechnol. Prog., 2013, vol. 29, no. 2, pp. 346–351.

    Article  PubMed  CAS  Google Scholar 

  68. Sun, J., Wen, F., Si, T., Xu, J.H., and Zhao, H., Appl. Environ. Microbiol., 2012, vol. 78, no. 11, pp. 3837–3845.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Srikrishnan, S., Chen, W., and Da Silva, N.A., Biotechnol. Bioeng., 2013, vol. 110, no. 1, pp. 275–285.

    Article  PubMed  CAS  Google Scholar 

  70. Nakanishi, A., Bae, J.G., Fukai, K., Tokumoto, N., Kuroda, K., Ogawa, J., Nakatani, M., Shimizu, S., and Ueda, M., Appl. Microbiol. Biotechnol., 2012, vol. 94, no. 4, pp. 939–948.

    Article  PubMed  CAS  Google Scholar 

  71. Andres, I., Gallardo, O., Parascandola, P., Javier Pastor, F.I., and Zueco, J., Biotechnol. Bioeng., 2005, vol. 89, no. 6, pp. 690–697.

    Article  PubMed  CAS  Google Scholar 

  72. Yang, N., Yu, Z., Jia, D., Xie, Z., Zhang, K., Xia, Z., Lei, L., and Qiao, M., Appl. Microbiol. Biotechnol., 2014, vol. 98, no. 7, pp. 2897–2905.

    Article  PubMed  CAS  Google Scholar 

  73. Liu, G., Yue, L., Chi, Z., Yu, W., Chi, Z., and Madzak, C., Mar. Biotechnol. (New York), 2009, vol. 11, no. 5, pp. 619–626.

    Article  CAS  Google Scholar 

  74. Takagi, T., Yokoi, T., Shibata, T., Morisaka, H., Kuroda, K., and Ueda, M., Appl. Microbiol. Biotechnol., 2016, vol. 100, no. 4, pp. 1723–1732.

    Article  PubMed  CAS  Google Scholar 

  75. Kaya, M., Ito, J., Kotaka, A., Matsumura, K., Bando, H., Sahara, H., Ogino, C., Shibasaki, S., Kuroda, K., Ueda, M., Kondo, A., and Hata, Y., Appl. Microbiol. Biotechnol., 2008, vol. 79, no. 1, pp. 51–60.

    Article  PubMed  CAS  Google Scholar 

  76. Fukuda, T., Isogawa, D., Takagi, M., Kato-Murai, M., Kimoto, H., Kusaoke, H., Ueda, M., and Suye, S., Biosci. Biotechnol. Biochem., 2007, vol. 71, no. 11, pp. 2845–2847.

    Article  PubMed  CAS  Google Scholar 

  77. Abe, H., Shimma, Y., and Jigami, Y., Glycobiology, 2003, vol. 13, no. 2, pp. 87–95.

    Article  PubMed  CAS  Google Scholar 

  78. Shimma, Y., Saito, F., Oosawa, F., and Jigami, Y., Appl. Environ. Microbiol., 2006, vol. 72, no. 11, pp. 7003–7012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Lee, G.Y., Jung, J.H., Seo, D.H., Hansin, J., Ha, S.J., Cha, J., Kim, Y.S., and Park, C.S., Bioresour. Technol., 2011, vol. 102, no. 19, pp. 9179–9184.

    Article  PubMed  CAS  Google Scholar 

  80. Zhang, H.C., Bi, J.Y., Chen, C., Huang, G.L., Qi, Q.S., Xiao, M., and Wang, P.G., Biosci. Biotechnol. Biochem., 2006, vol. 70, no. 9, pp. 2303–2306.

    Article  PubMed  CAS  Google Scholar 

  81. Jaeger, K.E. and Reetz, M.T., Trends Biotechnol., 1998, vol. 16, no. 9, pp. 396–403.

    Article  PubMed  CAS  Google Scholar 

  82. Liu, W., Zhao, H., Jia, B., Xu, L., and Yan, Y., Biotechnol. Lett., 2010, vol. 32, no. 2, pp. 255–260.

    Article  PubMed  CAS  Google Scholar 

  83. Yuzbasheva, E.Y., Yuzbashev, T.V., Perkovskaya, N.I., Mostova, E.B., Vybornaya, T.V., Sukhozhenko, A.V., Toropygin, I.Y., and Sineoky, S.P., Appl. Biochem. Biotechnol., 2015, vol. 175, no. 8, pp. 3888–3900.

    Article  PubMed  CAS  Google Scholar 

  84. Shiraga, S., Kawakami, M., Ishiguro, M., and Ueda, M., Appl. Environ. Microbiol., 2005, vol. 71, no. 8, pp. 4335–4338.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Washida, M., Takahashi, S., Ueda, M., and Tanaka, A., Appl. Microbiol. Biotechnol., 2001, vol. 56, nos. 5–6, pp. 681–686.

    Article  PubMed  CAS  Google Scholar 

  86. Kato, M., Fuchimoto, J., Tanino, T., Kondo, A., Fukuda, H., and Ueda, M., Appl. Microbiol. Biotechnol., 2007, vol. 75, no. 3, pp. 549–555.

    Article  PubMed  CAS  Google Scholar 

  87. Jiang, Z.B., Song, H.T., Gupta, N., Ma, L.X., and Wu, Z.B., Protein Expr. Purif., 2007, vol. 56, no. 1, pp. 35–39.

    Article  PubMed  CAS  Google Scholar 

  88. Moura, M.V., da Silva, G.P., Machado, A.C., Torres, F.A., Freire, D.M., and Almeida, R.V., PLoS One, 2015, vol. 10, no. 10. e0141454. doi 10.1371/journal. pone.0141454

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Qiu, Z., Tan, H., Zhou, S., and Cao, L., Mol. Biotechnol., 2014, vol. 56, no. 8, pp. 726–730.

    Article  PubMed  CAS  Google Scholar 

  90. Breinig, F., Diehl, B., Rau, S., Zimmer, C., Schwab, H., and Schmitt, M.J., Appl. Environ. Microbiol., 2006, vol. 72, no. 11, pp. 7140–7147.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Ni, X., Yue, L., Li, J., Chi, Z., Liu, Z., and Madzak, C., Indian J. Biochem. Biophys., 2009, vol. 46, no. 4, pp. 294–298.

    PubMed  CAS  Google Scholar 

  92. Yu, X.J., Madzak, C., Li, H.J., Chi, Z.M., and Li, J., Appl. Microbiol. Biotechnol., 2010, vol. 87, no. 2, pp. 669–677.

    Article  PubMed  CAS  Google Scholar 

  93. Tanaka, T., Masunari, S., Ishii, J., Wakamura, K., Segawa, M., Fukuda, H., and Kondo, A., J. Biotechnol., 2010, vol. 145, no. 1, pp. 79–83.

    Article  PubMed  CAS  Google Scholar 

  94. Liu, X.Y., Chi, Z., Liu, G.L., Wang, F., Madzak, C., and Chi, Z.M., Metab. Eng., 2010, vol. 12, no. 5, pp. 469–476.

    Article  PubMed  CAS  Google Scholar 

  95. Li, P.S. and Tao, H.C., Crit. Rev. Microbiol., 2015, vol. 41, no. 2, pp. 140–149.

    Article  PubMed  CAS  Google Scholar 

  96. Pazirandeh, M., Chrisey, L.A., Mauro, J.M., Campbell, J.R., and Gaber, B.P., Appl. Microbiol. Biotechnol., 1995, vol. 43, no. 6, pp. 1112–1117.

    Article  PubMed  CAS  Google Scholar 

  97. Kuroda, K. and Ueda, M., Appl. Microbiol. Biotechnol., 2010, vol. 87, no. 1, pp. 53–60.

    Article  PubMed  CAS  Google Scholar 

  98. Sousa, C., Kotrba, P., Ruml, T., Cebolla, A., and De Lorenzo, V., J. Bacteriol., 1998, vol. 180, no. 9, pp. 2280–2284.

    PubMed  PubMed Central  CAS  Google Scholar 

  99. Kuroda, K., Shibasaki, S., Ueda, M., and Tanaka, A., Appl. Microbiol. Biotechnol., 2001, vol. 57, nos. 5–6, pp. 697–701.

    Article  PubMed  CAS  Google Scholar 

  100. Bae, W., Wu, C.H., Kostal, J., Mulchandani, A., and Chen, W., Appl. Environ. Microbiol., 2003, vol. 69, no. 6, pp. 3176–3180.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Kuroda, K., Ueda, M., Shibasaki, S., and Tanaka, A., Appl. Microbiol. Biotechnol., 2002, vol. 59, nos. 2–3, pp. 259–264.

    PubMed  CAS  Google Scholar 

  102. Kuroda, K. and Ueda, M., Appl. Microbiol. Biotechnol., 2006, vol. 70, no. 4, pp. 458–463.

    Article  PubMed  CAS  Google Scholar 

  103. Wei, Q., Zhang, H., Guo, D., and Ma, S., J. Microbiol. Biotechnol., 2016, vol. 26, no. 5, pp. 846–853.

    Article  PubMed  CAS  Google Scholar 

  104. Kotrba, P. and Ruml, T., Appl. Environ. Microbiol., 2010, vol. 76, no. 8, pp. 2615–2622.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Grunden, A.M., Ray, R.M., Rosentel, J.K., Healy, F.G., and Shanmugam, K.T., J. Bacteriol., 1996, vol. 178, no. 3, pp. 735–744.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Nishitani, T., Shimada, M., Kuroda, K., and Ueda, M., Appl. Microbiol. Biotechnol., 2010, vol. 86, no. 2, pp. 641–648.

    Article  PubMed  CAS  Google Scholar 

  107. Kuroda, K., Nishitani, T., and Ueda, M., Appl. Microbiol. Biotechnol., 2012, vol. 96, no. 1, pp. 153–159.

    Article  PubMed  CAS  Google Scholar 

  108. Kuroda, K., Ebisutani, K., Iida, K., Nishitani, T., and Ueda, M., Biomolecules, 2014, vol. 4, no. 2, pp. 390–401.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Wegner, S.V., Boyaci, H., Chen, H., Jensen, M.P., and He, C., Angew. Chem., Int. Ed. Engl., 2009, vol. 48, no. 13, pp. 2339–2341.

    Article  CAS  Google Scholar 

  110. Ito, R., Kuroda, K., Hashimoto, H., and Ueda, M., AMB Express, 2016, vol. 6, no. 1, p.88.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Takayama, K., Suye, S., Kuroda, K., Ueda, M., Kitaguchi, T., Tsuchiyama, K., Fukuda, T., Chen, W., and Mulchandani, A., Biotechnol. Prog., 2006, vol. 22, no. 4, pp. 939–943.

    Article  PubMed  CAS  Google Scholar 

  112. Fukuda, T., Tsuchiyama, K., Makishima, H., Takayama, K., Mulchandani, A., Kuroda, K., Ueda, M., and Suye, S., Biotechnol. Lett., 2010, vol. 32, no. 5, pp. 655–659.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Takayama, K., Suye, S., Tanaka, Y., Mulchandani, A., Kuroda, K., and Ueda, M., Anal. Sci., 2011, vol. 27, no. 8, pp. 823–826.

    Article  PubMed  CAS  Google Scholar 

  114. Fuhacker, M., Scharf, S., and Weber, H., Chemosphere, 2000, vol. 41, no. 5, pp. 751–756.

    Article  Google Scholar 

  115. Yasui, M., Shibasaki, S., Kuroda, K., Ueda, M., Kawada, N., Nishikawa, J., Nishihara, T., and Tanaka, A., Appl. Microbiol. Biotechnol., 2002, vol. 59, nos 2–3, pp. 329–331.

    Article  PubMed  CAS  Google Scholar 

  116. Nakamura, Y., Shibasaki, S., Ueda, M., Tanaka, A., Fukuda, H., and Kondo, A., Appl. Microbiol. Biotechnol., 2001, vol. 57, no. 4, pp. 500–505.

    Article  PubMed  CAS  Google Scholar 

  117. Shibasaki, S., Kawabata, A., Ishii, J., Yagi, S., Kadonosono, T., Kato, M., Fukuda, N., Kondo, A., and Ueda, M., Appl. Microbiol. Biotechnol., 2007, vol. 75, no. 4, pp. 821–828.

    Article  PubMed  CAS  Google Scholar 

  118. Miyashita, H., Karaki, Y., Kikuchi, M., and Fujii, I., Proc. Natl. Acad. Sci. U.S.A., 1993, vol. 90, no. 11, pp. 5337–5340.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Lin, Y., Tsumuraya, T., Wakabayashi, T., Shiraga, S., Fujii, I., Kondo, A., and Ueda, M., Appl. Microbiol. Biotechnol., 2003, vol. 62, nos. 2–3, pp. 226–232.

    Article  PubMed  CAS  Google Scholar 

  120. Jo, J.H., Im, E.M., Kim, S.H., and Lee, H.H., Biotechnol. Lett., 2011, vol. 33, no. 6, pp. 1113–1120.

    Article  PubMed  CAS  Google Scholar 

  121. Jacobs, P.P., Ryckaert, S., Geysens, S., De Vusser, K., Callewaert, N., and Contreras, R., Biotechnol. Lett., 2008, vol. 30, no. 12, pp. 2173–2781.

    Article  PubMed  CAS  Google Scholar 

  122. Nobbs, A.H., Vickerman, M.M., and Jenkinson, H.F., Eukaryot. Cell, 2010, vol. 9, no. 10, pp. 1622–1634.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Wasilenko, J.L., Sarmento, L., Spatz, S., and Pantin-Jackwood, M., Biotechnol. Prog., 2010, vol. 26, no. 2, pp. 542–547.

    PubMed  CAS  Google Scholar 

  124. Lei, H., Jin, S., Karlsson, E., Schultz-Cherry, S., and Ye, K., J. Immunol. Res., 2016, vol. 2016, p. 4131324. doi 10.1155/2016/4131324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. Tamaru, Y., Ohtsuka, M., Kato, K., Manabe, S., Kuroda, K., Sanada, M., and Ueda, M., Biotechnol. Prog., 2006, vol. 22, no. 4, pp. 949–953.

    Article  PubMed  CAS  Google Scholar 

  126. Yue, L., Chi, Z., Wang, L., Liu, J., Madzak, C., Li, J., and Wang, X., J. Microbiol. Methods, 2008, vol. 72, no. 2, pp. 116–123.

    Article  PubMed  CAS  Google Scholar 

  127. Popovic, M., Prodanovic, R., Ostafe, R., Schillberg, S., Fischer, R., and Gavrovic-Jankulovic, M., Immunol. Res., 2015, vol. 61, no. 3, pp. 230–239.

    Article  PubMed  CAS  Google Scholar 

  128. Sheehan, J. and Marasco, W.A., Microbiol. Spectr., 2015, vol. 3, no. 1. AID-0028-2014.

    Google Scholar 

  129. Van den Beucken, T., Pieters, H., Steukers, M., Van der Vaart, M., Ladner, R.C., Hoogenboom, H.R., and Hufton, S.E., FEBS Lett., 2003, vol. 546, nos. 2–3, pp. 288–294.

    Article  PubMed  CAS  Google Scholar 

  130. Graff, C.P., Chester, K., Begent, R., and Wittrup, K.D., Protein Eng. Des. Sel., 2004, vol. 17, no. 4, pp. 293–304.

    Article  PubMed  CAS  Google Scholar 

  131. Razai, A., Garcia-Rodriguez, C., Lou, J., Geren, I.N., Forsyth, C.M., Robles, Y., Tsai, R., Smith, T.J., Smith, L.A., Siegel, R.W., Feldhaus, M., and Marks, J.D., J. Mol. Biol., 2005, vol. 351, no. 1, pp. 158–169.

    Article  PubMed  CAS  Google Scholar 

  132. Wang, Z., Kim, G.B., Woo, J.H., Liu, Y.Y., Mathias, A., Stavrou, S., and Neville, D.M., Jr., Bioconjug. Chem., 2007, vol. 18, no. 3, pp. 947–955.

    Article  PubMed  CAS  Google Scholar 

  133. Hara, K., Shigemori, T., Kuroda, K., and Ueda, M., AMB Express, 2012, vol. 2, no. 1, p.63.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. Shiraga, S., Ishiguro, M., Fukami, H., Nakao, M., and Ueda, M., Appl. Microbiol. Biotechnol., 2005, vol. 68, no. 6, pp. 779–785.

    Article  PubMed  CAS  Google Scholar 

  135. Kadonosono, T., Kato, M., and Ueda, M., Appl. Microbiol. Biotechnol., 2007, vol. 75, no. 6, pp. 1353–1360.

    Article  PubMed  CAS  Google Scholar 

  136. Aoki, W., Yoshino, Y., Morisaka, H., Tsunetomo, K., Koyo, H., Kamiya, S., Kawata, N., Kuroda, K., and Ueda, M., J. Biosci. Bioeng, 2011, vol. 111, no. 1, pp. 16–18.

    Article  PubMed  CAS  Google Scholar 

  137. Zhang, K., Li, H., Bhuripanyo, K., Zhao, B., Chen, T.F., Zheng, N., and Yin, J., Chembiochem, 2013, vol. 14, no. 4, pp. 426–430.

    Article  PubMed  CAS  Google Scholar 

  138. Fushimi, T., Miura, N., Shintani, H., Tsunoda, H., Kuroda, K., and Ueda, M., Appl. Microbiol. Biotechnol., 2013, vol. 97, no. 9, pp. 4003–4011.

    Article  PubMed  CAS  Google Scholar 

  139. Zou, W., Ueda, M., and Tanaka, A., Appl. Microbiol. Biotechnol., 2002, vol. 58, no. 6, pp. 806–812.

    Article  PubMed  CAS  Google Scholar 

  140. Matsui, K., Kuroda, K., and Ueda, M., Appl. Microbiol. Biotechnol., 2009, vol. 82, no. 1, pp. 105–113.

    Article  PubMed  CAS  Google Scholar 

  141. Andreu, C. and Del Olmo, M., Appl. Microbiol. Biotechnol., 2013, vol. 97, no. 20, pp. 9055–9069.

    Article  PubMed  CAS  Google Scholar 

  142. Perpina, C., Vinaixa, J., Andreu, C., and del Olmo, M., Appl. Microbiol. Biotechnol., 2015, vol. 99, no. 2, pp. 775–789.

    Article  PubMed  CAS  Google Scholar 

  143. Shibasaki, S., Ueda, M., Ye, K., Shimizu, K., Kamasawa, N., Osumi, M., and Tanaka, A., Appl. Microbiol. Biotechnol., 2001, vol. 57, no. 4, pp. 528–533.

    Article  PubMed  CAS  Google Scholar 

  144. Sambuk, E.V., Fizikova, A.Yu., Savinov, V.A., and Padkina, M.V., Enzyme Res., 2011, vol. 2011, article ID 356093, p. 16. doi 10.4061/2011/356093

    Article  CAS  Google Scholar 

  145. Shibasaki, S., Ninomiya, Y., Ueda, M., Iwahashi, M., Katsuragi, T., Tani, Y., Harashima, S., and Tanaka, A., Appl. Microbiol. Biotechnol., 2001, vol. 57, nos. 5–6, pp. 702–707.

    PubMed  CAS  Google Scholar 

  146. Shibasaki, S., Tanaka, A., and Ueda, M., Biosens. Bioelectron., 2003, vol. 19, no. 2, pp. 123–130.

    Article  PubMed  CAS  Google Scholar 

  147. Rajagopala, S.V., Adv. Exp. Med. Biol., 2015, vol. 883, pp. 187–214.

    Article  PubMed  CAS  Google Scholar 

  148. Li, Y., Biotechnol. Lett., 2011, vol. 33, no. 8, pp. 1487–1499.

    Article  PubMed  CAS  Google Scholar 

  149. Lim, K.H., Madabhushi, S.R., Mann, J., Neelamegham, S., and Park, S., Biotechnol. Bioeng., 2010, vol. 106, no. 1, pp. 27–41.

    PubMed  CAS  Google Scholar 

  150. Kuroda, K., Matsui, K., Higuchi, S., Kotaka, A., Sahara, H., Hata, Y., and Ueda, M., Appl. Microbiol. Biotechnol., 2009, vol. 82, no. 4, pp. 713–719.

    Article  PubMed  CAS  Google Scholar 

  151. Kotaka, A., Sahara, H., Kuroda, K., Kondo, A., Ueda,M., and Hata, Y., J. Biosci. Bioeng., 2010, vol. 109, no. 5, pp. 442–446.

    Article  PubMed  CAS  Google Scholar 

  152. Matsuoka, H., Hashimoto, K., Saijo, A., Takada, Y., Kondo, A., Ueda, M., Ooshima, H., Tachibana, T., and Azuma, M., Yeast, 2014, vol. 31, no. 2, pp. 67–76.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. St. Petersburg State University, St. Petersburg, 199034, Russia

    M. V. Padkina & E. V. Sambuk

Authors
  1. M. V. Padkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. V. Sambuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. V. Padkina.

Additional information

Original Russian Text © M.V. Padkina, E.V. Sambuk, 2018, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2018, Vol. 54, No. 4.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Padkina, M.V., Sambuk, E.V. Prospects for the Application of Yeast Display in Biotechnology and Cell Biology (Review). Appl Biochem Microbiol 54, 337–351 (2018). https://doi.org/10.1134/S0003683818040105

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0003683818040105

Keywords

Search

Navigation