Skip to main content
Log in

Transcription Factors as Evolvable Biosensors

  • Reviews
  • Published:
Analytical Sciences Aims and scope Submit manuscript

Abstract

One of the most prominent features of genetically encoded biosensors (GEBs) is their evolvability—the ability to invent new sensory functions using mutations. Among the GEBs, the transcription factor-based biosensors (TF-biosensors) is the focus of this review. We also discuss how this class of sensors can be highly evolvable and how we can exploit it. With an established platform for directed evolution, researchers can create, or evolve, new TF-biosensors. Directed evolution experiments have revealed the TF-biosensors’ evolvability, which is based partially on their characteristic physicochemical properties.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. N. Lobsiger and W. J. Stark, Anal. Sci., 2019, 35, 839.

    Article  PubMed  Google Scholar 

  2. H. Shiku, Anal. Sci., 2019, 35, 29.

    Article  CAS  PubMed  Google Scholar 

  3. E. C. Greenwald, S. Mehta, and J. Zhang, Chem. Rev., 2018, 118, 11707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. E. A. Rodriguez, R. E. Campbell, J. Y. Lin, M. Z. Lin, A. Miyawaki, A. E. Palmer, X. Shu, J. Zhang, and R. Y. Tsien, Trends Biochem. Sci., 2017, 42, 111.

    Article  CAS  PubMed  Google Scholar 

  5. V. Marx, Nat. Methods, 2017, 14, 949.

    Article  CAS  PubMed  Google Scholar 

  6. A. Germond, H. Fujita, T. Ichimura, and T. M. Watanabe, Biophys. Rev., 2016, 8, 121.

    Article  CAS  PubMed  Google Scholar 

  7. R. Fernandez-López, R. Ruiz, F. de la Cruz, and G. Moncalián, Front. Microbiol., 2015, 6, 648.

    Article  PubMed  PubMed Central  Google Scholar 

  8. W. Saenger, P. Orth, C. Kisker, W. Hillen, and W. Hinrichs, Angew. Chem. Int. Ed., 2000, 39, 2042.

    Article  CAS  Google Scholar 

  9. J. L. Ramos, M. Martínez-Bueno, A. J. Molina-Henares, W. Terán, K. Watanabe, X. Zhang, M. T. Gallegos, R. Brennan, and R. Tobes, Microbiol. Mol. Biol. Rev., 2005, 69, 326.

    Article  CAS  PubMed  Google Scholar 

  10. U. Schmeissner, D. Ganem, and J. H. Miller, J. Mol. Biol., 1977, 109, 303.

    Article  CAS  PubMed  Google Scholar 

  11. L. G. Kleina and J. H. Miller, J. Mol. Biol., 1990, 212, 295.

    Article  CAS  PubMed  Google Scholar 

  12. G. C. Chamnes and C. D. Willson, J. Mol. Biol., 1970, 53, 561.

    Article  Google Scholar 

  13. G. L. Myers and J. R. Sadler, J. Mol. Biol., 1971, 58, 1.

    Article  CAS  PubMed  Google Scholar 

  14. F J. Poelwijk, M. G. J.. de Vos, and S. J. Tans, Cell, 2011, 146, 462.

    Article  CAS  PubMed  Google Scholar 

  15. J. Suckow, P. Markiewicz, L. G. Kleina, J. Miller, B. Kisters-Woike, and B. Müller-Hill, J. Mol. Biol., 1996, 261, 509.

    Article  CAS  PubMed  Google Scholar 

  16. M. Resch, H. Striegl, E. M. Henssler, M. Sevvana, C. Egerer-Sieber, E. Schiltz, W. Hillen, and Y. A. Muller, Nucleic Acids Res., 2008, 36, 4390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. O. Scholz, E.-M. Henßler, J. Bail, P. Schubert, J. Bogdanska- Urbaniak, S. Sopp, M. Reich, S. Wisshak, M. Köstner, R. Bertram, and W. Hillen, Mol. Microbiol., 2004, 53, 777.

    Article  CAS  PubMed  Google Scholar 

  18. A. Kamionka, Nucleic Acids Res., 2004, 32, 842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. B. L. Adams, K. K. Carter, M. Guo, H.-C. C. Wu, C.-Y. Y. Tsao, H. O. Sintim, J. J. Valdes, and W. E. Bentley, ACS Synth. Biol., 2014, 3, 210.

    Article  CAS  PubMed  Google Scholar 

  20. E.-M. Henssler, R. Bertram, S. Wisshak, and W. Hillen, FEBS J., 2005, 272, 4487.

    Article  CAS  PubMed  Google Scholar 

  21. K. Saeki, M. Tominaga, S. Kawai-Noma, K. Saito, and D. Umeno, ACS Synth. Biol., 2016, 5, 1201.

    Article  CAS  PubMed  Google Scholar 

  22. K. Ike, Y. Arasawa, S. Koizumi, S. Mihashi, S. KawaiNoma, K. Saito, and D. Umeno, ACS Synth. Biol., 2015, 4, 1352.

    Article  CAS  PubMed  Google Scholar 

  23. S. Meinhardt, M. W. Manley, N. A. Becker, J. A. Hessman, L. J. Maher, and L. Swint-Kruse, Nucleic Acids Res., 2012, 40, 11139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. D. L. Shis, F. Hussain, S. Meinhardt, L. Swint-Kruse, and M. R. Bennett, ACS Synth. Biol., 2014, 3, 645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. J. F. Juárez, B. Lecube-Azpeitia, S. L. Brown, C. D. Johnston, and G. M. Church, Nat. Commun., 2018, 9, 3101.

    Article  PubMed  PubMed Central  Google Scholar 

  26. L. Li, M. Furubayashi, S. Wang, T. Maoka, S. KawaiNoma, K. Saito, and D. Umeno, Sci. Rep., 2019, 9, 1.

    Article  Google Scholar 

  27. R. P. Dimas, B. R. Jordan, X.-L. Jiang, C. Martini, J. S. Glavy, D. P. Patterson, F. Morcos, and C. T. Y. Chan, Nucleic Acids Res., 2019, 47, 8913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Y. Yokobayashi, R. Weiss, and F. H. Arnold, Proc. Natl. Acad. Sci., 2002, 99, 16587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. N. Muranaka, V. Sharma, Y. Nomura, and Y. Yokobayashi, Nucleic Acids Res., 2009, 37, e39.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Y. Nomura and Y. Yokobayashi, J. Am. Chem. Soc., 2007, 129, 13814.

    Article  CAS  PubMed  Google Scholar 

  31. Y. Tashiro, H. Fukutomi, K. Terakubo, K. Saito, and D. Umeno, Nucleic Acids Res., 2011, 39, e12.

    Article  PubMed  Google Scholar 

  32. K. Negishi, D. Loakes, and R. M. Schaaper, Genetics, 2002, 161, 1363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Y. Tashiro, A. Katabami, K. Saito, and D. Umeno, Anal. Sci., 2012, 28, 95.

    Article  CAS  PubMed  Google Scholar 

  34. M. Eigen, Proc. Natl. Acad. Sci., 2002, 99, 13374.

    Article  CAS  PubMed  Google Scholar 

  35. M. Tominaga, K. Ike, S. Kawai-Noma, K. Saito, and D. Umeno, PLoS One, 2015, 10, e0120243.

    Article  PubMed  PubMed Central  Google Scholar 

  36. M. Tominaga, S. Kawai-Noma, I. Kawagishi, Y. Sowa, K. Saito, and D. Umeno, PLoS One, 2015, 10, e0119818.

    Article  PubMed  Google Scholar 

  37. C. H. Collins, F. H. Arnold, and J. R. Leadbetter, Mol. Microbiol., 2004, 55, 712.

    Article  Google Scholar 

  38. C. H. Collins, J. R. Leadbetter, and F. H. Arnold, Nat. Biotechnol., 2006, 24, 708.

    Article  CAS  PubMed  Google Scholar 

  39. Y. Tashiro, Y. Kimura, M. Furubayashi, A. Tanaka, K. Terakubo, K. Saito, S. Kawai-Noma, and D. Umeno, J. Gen. Appl. Microbiol., 2016, 62, 240.

    Article  CAS  PubMed  Google Scholar 

  40. S. Y. Tang, H. Fazelinia, and P. C. Cirino, J. Am. Chem. Soc., 2008, 130, 5267.

    Article  CAS  PubMed  Google Scholar 

  41. S. Y. Tang and P. C. Cirino, Angew. Chem. Int. Ed., 2011, 50, 1084.

    Article  CAS  Google Scholar 

  42. S. Y. Tang, S. Qian, O. Akinterinwa, C. S. Frei, J. A. Gredell, and P. C. Cirino, J. Am. Chem. Soc., 2013, 135, 10099.

    Article  CAS  PubMed  Google Scholar 

  43. C. S. Frei, S. Qian, and P. C. Cirino, Protein Eng. Des. Sel., 2018, 31, 213.

    Article  CAS  PubMed  Google Scholar 

  44. Y. Kimura, S. Kawai-Noma, K. Saito, and D. Umeno, ACS Synth. Biol., 2020, 9, 567.

    Article  CAS  PubMed  Google Scholar 

  45. A. J. Meyer, T. H. Segall-Shapiro, E. Glassey, J. Zhang, and C. A. Voigt, Nat. Chem. Biol., 2019, 15, 196.

    Article  CAS  PubMed  Google Scholar 

  46. J. D. Bloom, S. T. Labthavikul, C. R. Otey, and F. H. Arnold, Proc. Natl. Acad. Sci., 2006, 103, 5869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. J. D. Bloom, C. O. Wilke, F. H. Arnold, and C. Adami, Biophys. J., 2004, 86, 2758.

    Article  CAS  PubMed  Google Scholar 

  48. N. Tokuriki and D. S. Tawfik, Curr Opin. Struct. Biol., 2009, 19, 596.

    Article  CAS  PubMed  Google Scholar 

  49. A. Vannini, EMBO J., 2002, 21, 4393.

    Article  CAS  PubMed  Google Scholar 

  50. F. Jacob and J. Monod, J. Mol. Biol., 1961, 3, 318.

    Article  CAS  PubMed  Google Scholar 

  51. M. Ptashne, A. Jeffrey, A. D. Johnson, R. Maurer, B. J. Meyer, C. O. Pabo, T. M. Roberts, and R. T. Sauer, Cell, 1980, 19, 1.

    Article  CAS  PubMed  Google Scholar 

  52. K. Tsumoto, H. Sakuta, K. Takiguchi, and K. Yoshikawa, Biophys. Rev., 2020, 12, 425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. J. R. Paulson and U. K. Laemmli, Cell, 1977, 12, 817.

    Article  CAS  PubMed  Google Scholar 

  54. D. Umeno, M. Kiji, M. Murata, and M. Maeda, Polym. J., 1999, 31, 1109.

    Article  CAS  Google Scholar 

  55. T. Iwataki, K. Yoshikawa, S. Kidoaki, D. Umeno, M. Kiji, and M. Maeda, J. Am. Chem. Soc., 2000, 122, 9891.

    Article  CAS  Google Scholar 

  56. M. Maeda, C. Nishimura, D. Umeno, and M. Takagi, Bioconjug. Chem., 1994, 5, 527.

    Article  CAS  PubMed  Google Scholar 

  57. D. Umeno, M. Kawasaki, and M. Maeda, Bioconjug. Chem., 1998, 9, 719.

    Article  CAS  PubMed  Google Scholar 

  58. D. Umeno and M. Maeda, Anal. Sci., 1997, 13, 553.

    Article  CAS  Google Scholar 

  59. N. Soh, D. Umeno, Z. Tang, M. Murata, and M. Maeda, Anal. Sci., 2002, 18, 1295.

    Article  CAS  PubMed  Google Scholar 

  60. D. Umeno and M. Maeda, Chem. Lett., 1999, 28, 381.

    Article  Google Scholar 

  61. D. Umeno, M. Kawasaki, and M. Maeda, ACS Symp. Ser., 1998, 703, 202.

    Article  CAS  Google Scholar 

  62. D. Umeno, M. Kawasaki, and M. Maeda, Supramol. Sci., 1998, 5, 427.

    Article  CAS  Google Scholar 

  63. D. Umeno, Ph.D. Thesis, Kyushu Univ., 1998.

    Google Scholar 

  64. S. Boeynaems, S. Alberti, N. L. Fawzi, T. Mittag, M. Polymenidou, F. Rousseau, J. Schymkowitz, J. Shorter, B. Wolozin, L. Van Den Bosch, P. Tompa, and M. Fuxreiter, Trends Cell Biol., 2018, 28, 420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. G. A. Newby, S. Kiriakov, E. Hallacli, C. Kayatekin, P. Tsvetkov, C. P. Mancuso, J. M. Bonner, W. R. Hesse, S. Chakrabortee, A. L. Manogaran, S. W. Liebman, S. Lindquist, and A. S. Khalil, Cell, 2017, 171, 966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daisuke Umeno.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Umeno, D., Kimura, Y. & Kawai-Noma, S. Transcription Factors as Evolvable Biosensors. ANAL. SCI. 37, 699–703 (2021). https://doi.org/10.2116/analsci.20SCR12

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2116/analsci.20SCR12

Keywords

Navigation