BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

The art of reporter proteins in science: past, present and future applications

  • Ghim, Cheol-Min (School of Nano-Biotechnology and Chemical Engineering, Ulsan National Institute of Science and Technology) ;
  • Lee, Sung-Kuk (School of Nano-Biotechnology and Chemical Engineering, Ulsan National Institute of Science and Technology) ;
  • Takayama, Shuichi (School of Nano-Biotechnology and Chemical Engineering, Ulsan National Institute of Science and Technology) ;
  • Mitchell, Robert J. (School of Nano-Biotechnology and Chemical Engineering, Ulsan National Institute of Science and Technology)
  • Received : 2010.07.01
  • Published : 2010.07.31
Download PDF
⟨ Previous Next ⟩

Abstract

Starting with the first publication of lacZ gene fusion in 1980, reporter genes have just entered their fourth decade. Initial studies relied on the simple fusion of a promoter or gene with a particular reporter gene of interest. Such constructs were then used to determine the promoter activity under specific conditions or within a given cell or organ. Although this protocol was, and still is, very effective, current research shows a paradigm shift has occurred in the use of reporter systems. With the advent of innovative cloning and synthetic biology techniques and microfluidic/nanodroplet systems, reporter genes and their proteins are now finding themselves used in increasingly intricate and novel applications. For example, researchers have used fluorescent proteins to study biofilm formation and discovered that microchannels develop within the biofilm. Furthermore, there has recently been a "fusion" of art and science; through the construction of genetic circuits and regulatory systems, researchers are using bacteria to "paint" pictures based upon external stimuli. As such, this review will discuss the past and current trends in reporter gene applications as well as some exciting potential applications and models that are being developed based upon these remarkable proteins.

Keywords

References

  1. http://www.ncbi.nlm.nih.gov.
  2. Wood, K. V. (1995) Marker proteins for gene expression. Curr. Opin. Biotechnol. 6, 50-58. https://doi.org/10.1016/0958-1669(95)80009-3
  3. Berman, M. L. and Beckwith, J. (1979) Fusions of the lac operon to the transfer RNA gene tyrT of Escherichia coli. J. Mol. Biol. 130, 285-301. https://doi.org/10.1016/0022-2836(79)90542-4
  4. Casadaban, M. J., Chou, J. and Cohen, S. N. (1980) In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J. Bacteriol. 143, 971-980.
  5. Lis, J. T., Simon, J. A. and Sutton, C. A. (1983) New heat shock puffs and β-galactosidase activity resulting from transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell 35, 403-410. https://doi.org/10.1016/0092-8674(83)90173-3
  6. James, A. L., Perry, J. D., Ford, M., Armstrong, L. and Gould, F. K. (1996) Evaluation of cyclohexenoesculetinbeta- D-galactoside and 8-hydroxyquinoline-beta-D-galactoside as substrates for the detection of beta-galactosidase. Appl. Environ. Microbiol. 62, 3868-3870.
  7. Imagawa, M., Yoshitake, S., Ishikawa, E., Endo, Y., Ohtaki, S., Kano, E. and Tsunetoshi, Y. (1981) Highly sensitive sandwich enzyme immunoassay of human IgE with beta- D-galactosidase from Escherichia coli. Clin. Chim. Acta 117, 199-207. https://doi.org/10.1016/0009-8981(81)90039-5
  8. Craig, D., Arriaga, E. A., Banks, P., Zhang, Y., Renborg, A., Palcic, M. M. and Dovichi, N. J. (1995) Fluorescencebased enzymatic assay by capillary electrophoresis laser- induced fluorescence detection for the determination of a few beta-galactosidase molecules. Anal. Biochem. 226, 147-153. https://doi.org/10.1006/abio.1995.1202
  9. Bronstein, I., Martin, C. S., Fortin, J. J., Olesen, C. E. and Voyta, J. C. (1996) Chemiluminescence: sensitive detection technology for reporter gene assays. Clin. Chem. 42, 1542-1546.
  10. de Wet, J. R., Wood, K. V., Helinski, D. R. and DeLuca, M. (1985) Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 82, 7870-7873. https://doi.org/10.1073/pnas.82.23.7870
  11. de Wet, J. R., Wood, K. V., DeLuca, M., Helinski, D. R. and Subramani, S. (1987) Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7, 725-737. https://doi.org/10.1128/MCB.7.2.725
  12. Ow, D. W., de Wet, J. R., Helinski, D. R., Howell, S. H., Wood, K. V. and Deluca, M. (1986) Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants. Science 234, 856-859 https://doi.org/10.1126/science.234.4778.856
  13. Keller, G. A., Gould, S., Deluca, M. and Subramani, S. (1987) Firefly luciferase is targeted to peroxisomes in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 84, 3264-3268. https://doi.org/10.1073/pnas.84.10.3264
  14. Nordeen, S. K. (1988) Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6, 454-458.
  15. Brasier, A. R., Tate, J. E. and Habener, J. F. (1989) Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines. Biotechniques 7, 1116-1122.
  16. Mitchell, R. J. and Gu, M. B. (2005) Construction and evaluation of nagR-nagAa::lux fusion strains in the biosensing for salicylic acid derivatives. Appl. Biochem. Biotechnol. 120, 183-198. https://doi.org/10.1385/ABAB:120:3:183
  17. Mitchell, R. J., Ahn, J. M. and Gu, M. B. (2005) Comparison of Photorhabdus luminescens and Vibrio fischeri lux fusions to study gene expression patterns. J. Microbiol. Biotechnol. 15, 48-54.
  18. Mitchell, R. J. and Gu M. B. (2004) Construction and characterization of novel dual-stress-responsive bacterial biosensors. Biosens. Bioelectron. 19, 977-985. https://doi.org/10.1016/j.bios.2003.09.002
  19. Mitchell, R. J. and Gu M. B. (2004) An Escherichia coli biosensor capable of detecting both genotoxic and oxidative damage. Appl. Microbiol. Biotechnol. 64, 46-52. https://doi.org/10.1007/s00253-003-1418-0
  20. Gupta, R. K., Patterson, S. S., Ripp, S., Simpson, M. L. and Sayler, G. S. (2003) Expression of the Photorhabdus luminescens lux genes (luxA, B, C, D, and E) in Saccharomyces cerevisiae. FEMS Yeast Res. 4, 305-313. https://doi.org/10.1016/S1567-1356(03)00174-0
  21. Morin, J. G. and Hastings, J. W. (1971) Biochemistry of the bioluminescence of colonial hydroids and other coelenterates. J. Cell Physiol. 77, 305-312. https://doi.org/10.1002/jcp.1040770304
  22. Morin, J. G. and Hastings, J. W. (1971) Energy transfer in a bioluminescent system. J. Cell Physiol. 77, 313-318. https://doi.org/10.1002/jcp.1040770305
  23. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. and Prasher, D. C. (1994) Green fluorescent protein as a marker for gene expression. Science 263, 802-805. https://doi.org/10.1126/science.8303295
  24. Casper, S. J. and Holt, C. A. (1996) Expression of the green fluorescent protein-encoding gene from a tobacco mosaic virus-based vector. Gene 173, 69-73. https://doi.org/10.1016/0378-1119(95)00782-2
  25. Amsterdam, A., Lin, S., Moss, L. G. and Hopkins, N. (1996) Requirements for green fluorescent protein detection in transgenic zebrafish embryos. Gene 173, 99-103. https://doi.org/10.1016/0378-1119(95)00719-9
  26. http://www.clontech.com/upload/images/ WP9X2790_FP.html.
  27. Heim, R., Cubitt, A. B. and Tsien, R. Y. (1995) Improved green fluorescence. Nature 373, 663-664.
  28. Katranidis, A., Atta, D., Schlesinger, R., Nierhaus, K. H, Choli-Papadopoulou, T., Gregor, I., Gerrits, M., Buldt, G. and Fitter, J. (2009) Fast biosynthesis of GFP molecules: a single-molecule fluorescence study. Angew. Chem. Int. Ed Engl. 48, 1758-1761. https://doi.org/10.1002/anie.200806070
  29. Karin, M. (1994) Signal-transduction from the cell-surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6, 415-424. https://doi.org/10.1016/0955-0674(94)90035-3
  30. Treisman, R. (1994) Ternary complex factors: growth factor regulated transcriptional activators. Curr. Opin. Genet. Dev. 4, 96-101. https://doi.org/10.1016/0959-437X(94)90097-3
  31. Elowitz, M. B. and Leibler, S. (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338. https://doi.org/10.1038/35002125
  32. Hasty, J., McMillen, D. and Collins, J. J. (2002) Engineered gene circuits. Nature 420, 224-230. https://doi.org/10.1038/nature01257
  33. Gardner, T. S., Cantor, C. R. and Collins, J. J. (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403, 339-342. https://doi.org/10.1038/35002131
  34. Van Dyk, T. K., DeRose, E. J. and Gonye, G. E. (2001) LuxArray, a high-density, genome wide transcription analysis of Escherichia coli using bioluminescent reporter strains. J. Bacteriol. 183, 5496-5505. https://doi.org/10.1128/JB.183.19.5496-5505.2001
  35. Xiong, Y. Q., Willard, J., Kadurugamuwa, J. L., Yu, J., Francis, K. P. and Bayer, A. S. (2005) Real-time in vivo bioluminescent imaging for evaluating the efficacy of anti biotics in a rat Staphylococcus aureus endocarditis model. Antimicrob. Agents Chemother. 49, 380-387.
  36. Doyle, T. C., Burns, S. M. and Contag, C. H. (2004) In vivo bioluminescence imaging for integrated studies of infection. Cell. Microbiol. 6, 303-317. https://doi.org/10.1111/j.1462-5822.2004.00378.x
  37. Lee, S. K., Chou, H. H., Pfleger, B. F., Newman, J. D., Yoshikuni, Y. and Keasling, J. D. (2007) Directed evolution of AraC for improved compatibility of arabinose- and lactose-inducible promoters. Appl. Environ. Microbiol. 73, 5711-5715. https://doi.org/10.1128/AEM.00791-07
  38. Canton, B., Labno, A. and Endy, D. (2008) Refinement and standardization of synthetic biological parts and devices. Nat. Biotechnol. 26, 787-793. https://doi.org/10.1038/nbt1413
  39. Tabor, J. J., Salis, H. M., Simpson, Z. B., Chevalier, A. A., Levskaya, A., Marcotte, E. M., Voigt, C. A. and Ellington, A. D. (2009) A synthetic genetic edge detection program. Cell 137, 1272-1281 https://doi.org/10.1016/j.cell.2009.04.048
  40. Bennett, M. R. and Hasty, J. (2009) Microfluidic devices for measuring gene network dynamics in single cells. Nat. Rev. Genet. 10, 628-638. https://doi.org/10.1038/nrg2625
  41. Andersen, J. B., Sternberg, C., Poulsen, L. K., Bjorn, S. P., Givskov, M. and Molin, S. (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 64, 2240-2246.
  42. Simpson, M. L. (2007) A destabilized bacterial luciferase for dynamic gene expression studies. Syst. Synth. Biol. 1, 3-9. https://doi.org/10.1007/s11693-006-9001-5
  43. Kuiper, I., Lagendijk, E. L., Pickford, R., Derrick, J. P., Lamers, G. E., Thomas-Oates, J. E., Lugtenberg, B. J. and Bloemberg, G. V. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol. Microbiol. 51, 97-113. https://doi.org/10.1046/j.1365-2958.2003.03751.x
  44. Sabev, H. A., Robson, G. D. and Handley, P. S. (2006) Influence of starvation, surface attachment and biofilm growth on the biocide susceptibility of the biodeteriogenic yeast Aureobasidium pullulans. J. Appl. Microbiol. 101, 319-330. https://doi.org/10.1111/j.1365-2672.2006.03014.x
  45. Kim, J., Hahn, J. S., Franklin, M. J., Stewart, P. S. and Yoon, J. (2009) Tolerance of dormant and active cells in Pseudomonas aeruginosa PA01 biofilm to antimicrobial agents. J. Antimicrob. Chemother. 63, 129-135. https://doi.org/10.1093/jac/dkn462
  46. Marti, M., Trotonda, M. P., Tormo-Mas, M. A., Vergara- Irigaray, M., Cheung, A. L., Lasa, I. and Penades, J. R. (2010) Extracellular proteases inhibit protein-dependent biofilm formation in Staphylococcus aureus. Microbes Infect. 12, 55-64. https://doi.org/10.1016/j.micinf.2009.10.005
  47. Wood, T. K, Gonzalez Barrios A. F., Herzberg, M. and Lee, J. (2006) Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72, 361-367. https://doi.org/10.1007/s00253-005-0263-8
  48. Yang, X., Ma, Q. and Wood, T. K. (2008) The R1 conjugative plasmid increases Escherichia coli biofilm formation through an envelope stress response. Appl. Environ. Microbiol. 74, 2690-2699. https://doi.org/10.1128/AEM.02809-07
  49. http://www.che.tamu.edu/groups/Wood/biofilm%20 architecture.htm
  50. Cowan, S. E., Gilbert, E., Liepmann, D. and Keasling, J. D. (2000) Commensal interactions in a dual-species biofilm exposed to mixed organic compounds. Appl. Environ. Microbiol. 66, 4481-4485. https://doi.org/10.1128/AEM.66.10.4481-4485.2000
  51. Tomlin, K. L., Clark, S. R. and Ceri, H. (2004) Green and red fluorescent protein vectors for use in biofilm studies of the intrinsically resistant Burkholderia cepacia complex. J. Microbiol. Methods 57, 95-106 https://doi.org/10.1016/j.mimet.2003.12.007
  52. Lee, J., Jayaraman, A. and Wood, T. K. (2007) Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7, 42-56. https://doi.org/10.1186/1471-2180-7-42
  53. Lederberg, J. and Lederberg, E. M. (1952) Replica plating and indirect selection of bacterial mutants. J. Bacteriol. 63, 399-406.
  54. Lee, J. H., Mitchell, R. J., Kim, B. C., Cullen, D. C. and Gu, M. B. (2005) A cell array biosensor for environmental toxicity analysis. Biosens. Bioelectron. 21, 500-507. https://doi.org/10.1016/j.bios.2004.12.015
  55. Mitchell, R. J. and Gu, M. B. (2006) Characterization and optimization of two methods in the immobilization of 12 bioluminescent strains. Biosens. Bioelectron. 22, 192-199. https://doi.org/10.1016/j.bios.2005.12.019
  56. Xu, C. W. (2002) High-density cell microarrays for parallel functional determinations. Genome Res. 12, 482-486. https://doi.org/10.1101/gr.213002.ArticlepublishedonlinebeforeprintinFebruary2002
  57. Ingham, C., Bomer, J., Sprenkels, A., van den Berg, A., de Vos, W. and van Hylckama Vlieg, J. (2010) High-resolution microcontact printing and transfer of massive arrays of microorganisms on planar and compartmentalized nanoporous aluminium oxide. Lab Chip 10, 1410-1416. https://doi.org/10.1039/b925796a
  58. Bearinger, J. P., Dugan, L. C., Wu, L. G., Hill, H., Christian, A. T. and Hubbell, J. A. (2009) Chemical tethering of motile bacteria to silicon surfaces. Biotechniques 46, 209-216. https://doi.org/10.2144/000113073
  59. Eun, Y. J. and Weibel, D. B. (2009) Fabrication of microbial biofilm arrays by geometric control of cell adhesion. Langmuir 25, 4643-4654. https://doi.org/10.1021/la803985a
  60. Tavana, H., Jovic, A., Mosadegh, B., Yi, L. Q., Liu, X., Luker, K. E., Luker, G. D., Weiss, S. J. and Takayama, S. (2009) Nanolitre liquid patterning in aqueous environments for spatially defined reagent delivery to mammalian cells. Nat. Mater. 8, 736-741. https://doi.org/10.1038/nmat2515
  61. Tavana, H., Mosadegh, B. and Takayama, S. (2010) Polymeric aqueous biphasic systems for non-contact cell printing on cells: Engineering heterocellular embryonic stem cell niches. Adv. Mater. online. DOI: 10.1002/adma. 200904271.
  62. Kuang, Y., Biran, I. and Walt, D. R. (2004) Living bacterial cell array for genotoxin monitoring. Anal. Chem. 76, 2902- 2909. https://doi.org/10.1021/ac0354589
  63. Jovic, A., Howell, B. and Takayama, S. (2009) Timing is everything: using fluidics to understand the role of temporal dynamics in cellular systems. Microfluid. Nanofluid. 6, 717-729. https://doi.org/10.1007/s10404-009-0413-x
  64. Gachon, F., Nagoshi, E., Brown, S. A., Ripperger, J. and Schibler, U. (2004) The mammalian circadian timing system: from gene expression to physiology. Chromosoma 113, 103-112.
  65. Iwasaki, H., Williams, S. B., Kitayama, Y., Ishiura, M., Golden, S. S. and Kondo, T. (2000) A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101, 223-233. https://doi.org/10.1016/S0092-8674(00)80832-6
  66. Tsuchiya, M. and Ross, J. (2002) Advantages of external periodic events to the evolution of biochemical oscillatory reactions. Proc. Natl. Acad. Sci. U.S.A. 100, 9691-9695.
  67. Bennett, M. R., Pang, W. L., Ostroff, N. A., Baumgartner, B. L., Nayak, S., Tsimring, L. S. and Hasty, J. (2008) Metabolic gene regulation in a dynamically changing environment. Nature 454, 1119-1122. https://doi.org/10.1038/nature07211
  68. Hersen, P., McClean, M. N., Mahadevan, L. and Ramanathan, S. (2008) Signal processing by the HOG MAP kinase pathway. Proc. Natl. Acad. Sci. U.S.A. 105, 7165-7170. https://doi.org/10.1073/pnas.0710770105
  69. Mettetal, J. M., Muzzey, D., Gomez-Uribe, C. and van Oudenaarden, A. (2008) The frequency dependence of osmo- adaptation in Saccharomyces cerevisiae. Science 319, 482-484. https://doi.org/10.1126/science.1151582
  70. Dyszel, J. L., Soares, J. A., Swearingen, M. C., Lindsay, A., Smith, J. N. and Ahmer, B. M. M. (2010) E. coli K-12 and EHEC genes regulated by SdiA. PLoS One 5, e8946. https://doi.org/10.1371/journal.pone.0008946
  71. Tani, H., Maehana, K. and Kamidate, T. (2004) Chipbased bioassay using bacterial sensor strains immobilized in three-dimensional microfluidic network. Anal. Chem. 76, 6693-6697. https://doi.org/10.1021/ac049401d
  72. Guet, C. C., Elowitz, M. B., Hsing, W. and Leibler, S. (2002) Combinatorial synthesis of genetic networks. Science 296, 1466-1470. https://doi.org/10.1126/science.1067407
  73. Kim, P. M. and Tidor, B. (2003) Limitations of quantitative gene regulation models: a case study. Genome Res. 13, 2391-2395. https://doi.org/10.1101/gr.1207003
  74. Keiler, K. C., Waller, P. R. and Sauer, R. T. (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990-993. https://doi.org/10.1126/science.271.5251.990
  75. Buchler, N. E., Gerland, U. and Hwa, T. (2005) Nonlinear protein degradation and the function of genetic circuits. Proc. Natl. Acad. Sci. U.S.A. 102, 9559-9564. https://doi.org/10.1073/pnas.0409553102
  76. Ghim, C. M. and Almaas, E. (2008) Genetic noise control via protein oligomerization. BMC Sys. Biol. 2, 94. https://doi.org/10.1186/1752-0509-2-94
  77. Ghim, C. M. and Almaas, E. (2009) Two-component genetic switch as a synthetic module with tunable stability. Phys. Rev. Lett. 103, 028101. https://doi.org/10.1103/PhysRevLett.103.028101
  78. Regaldo, A. (2005) Next dream for Venter: create entire set of genes from scratch. The Wall Street Journal, June 29th, p A1.
  79. Hale, V., Keasling, J. D., Renninger, N. and Diagana, T. T. (2007) Microbially derived artemisinin: a biotechnology solution to the global problem of access to affordable antimalarial drugs. Am. J. Trop. Med. Hyg. 77, 198-202.
  80. Gibson, D. G., Glass, J. I., Lartigue, C., Noskov, V. N., Chuang, R. Y., Algire, M. A., Benders, G. A., Montague, M. G., Ma, L., Moodie, M. M., Merryman, C., Vashee, S., Krishnakumar, R., Assad-Garcia, N., Andrews-Pfannkoch, C., Denisova, E. A., Young, L., Qi, Z. Q., Segall-Shapiro, T. H., Calvey, C. H., Parmar, P. P., Hutchison, III, C. A., Smith, H. O. and Venter, J. C. (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science DOI: 10.1126/science.1190719.
  81. Khalil, A. S. and Collins, J. J. (2010) Synthetic biology: applications come of age. Nat. Rev. Genet. 11, 367-379. https://doi.org/10.1038/nrg2775
  82. Martin, L., Che, A. and Endy, D. (2009) Gemini, a bifunctional enzymatic and fluorescent reporter of gene expression. PLoS One 4, e7596. Doi:10.1371/journal. pone. 0007569.
  83. http://www.worldsciencefestival.com/blog/bioart_process.
  84. http://www.psfk.com/2009/01/pic-painting-with-fluorescentbacteria.html.
  85. http://www.binder-world.com/eu/en/company/binder-news.cfm/binder/83/laborschraenke-umweltsimulation/painting-with-bacteria.cfm.
  86. http://www.microbialart.com/contributed-art/
  87. http://faculty.washington.edu/afolch/FolchLabART.html.
  88. Levskaya, A., Chevalier, A. A., Tabor, J. J., Simpson, Z. B., Lavery, L. A., Levy, M., Davidson, E. A., Scouras, A., Ellington, A. D., Marcotte, E. M. and Voigt, C. A. (2005) Synthetic biology: engineering Escherichia coli to see light. Nature 438, 441-442. https://doi.org/10.1038/nature04405
  89. http://www.utexas.edu/features/2005/bacteria/index.html.
  90. Levskaya, A., Weiner, O. D., Lim, W. A. and Voigt C. A. (2009) Spatiotemporal control of cell signaling using a light-switchable protein interaction. Nature 461, 997-1001. https://doi.org/10.1038/nature08446

Cited by

  1. Electrochemical Measurement of the β-Galactosidase Reporter from Live Cells: A Comparison to the Miller Assay vol.5, pp.1, 2016, https://doi.org/10.1021/acssynbio.5b00073
  2. Surface glycoproteins determine the feature of the 2009 pandemic H1N1 virus vol.45, pp.11, 2012, https://doi.org/10.5483/BMBRep.2012.45.11.137
  3. A reporter system coupled with high-throughput sequencing unveils key bacterial transcription and translation determinants vol.8, pp.1, 2017, https://doi.org/10.1038/s41467-017-00239-7
  4. On-chip enzymatic assay for chloramphenicol acetyltransferase using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry vol.136, 2015, https://doi.org/10.1016/j.colsurfb.2015.09.052
  5. Comparison of IRES and F2A-Based Locus-Specific Multicistronic Expression in Stable Mouse Lines vol.6, pp.12, 2011, https://doi.org/10.1371/journal.pone.0028885
  6. The glpD gene is a novel reporter gene for E. coli that is superior to established reporter genes like lacZ and gusA vol.131, 2016, https://doi.org/10.1016/j.mimet.2016.10.015
  7. A comprehensive toolbox for the rapid construction of lacZ fusion reporters vol.91, pp.3, 2012, https://doi.org/10.1016/j.mimet.2012.09.023
  8. A fluorogenic probe for β-galactosidase activity imaging in living cells vol.9, pp.12, 2013, https://doi.org/10.1039/c3mb70269c
  9. Multicolor Whole-Cell Bacterial Sensing Using a Synchronous Fluorescence Spectroscopy-Based Approach vol.10, pp.3, 2015, https://doi.org/10.1371/journal.pone.0122848
  10. How to screen non-viral gene delivery systems in vitro? vol.154, pp.3, 2011, https://doi.org/10.1016/j.jconrel.2011.05.001
  11. Microbial linguistics: perspectives and applications of microbial cell-to-cell communication vol.44, pp.1, 2011, https://doi.org/10.5483/BMBRep.2011.44.1.1
  12. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence 2011, https://doi.org/10.1038/nrg3095
  13. Applications of flow cytometry in plant pathology for genome size determination, detection and physiological status vol.12, pp.8, 2011, https://doi.org/10.1111/j.1364-3703.2011.00711.x
  14. Virus integration and genome influence in approaches to stem cell based therapy for andro-urology vol.82-83, 2015, https://doi.org/10.1016/j.addr.2014.10.012
  15. Construction of chromosomally encodedlacZandgfpreporter strains ofEscherichia colifor the study of global regulation of metabolism vol.16, pp.7, 2016, https://doi.org/10.1002/elsc.201600056
  16. Fluorescent transgenic zebrafish as a biosensor for growth-related effects of methyl parathion vol.152, 2014, https://doi.org/10.1016/j.aquatox.2014.04.001
  17. Establishment of a melanogenesis regulation assay system using a fluorescent protein reporter combined with the promoters for the melanogenesis-related genes in human melanoma cells vol.68, 2015, https://doi.org/10.1016/j.enzmictec.2014.09.008
  18. Screening of a novel strong promoter by RNA sequencing and its application to H2 production in a hyperthermophilic archaeon vol.99, pp.9, 2015, https://doi.org/10.1007/s00253-015-6444-1
  19. Destabilized eYFP variants for dynamic gene expression studies inCorynebacterium glutamicum vol.6, pp.2, 2013, https://doi.org/10.1111/j.1751-7915.2012.00360.x
  20. Genetically modified whole-cell bioreporters for environmental assessment vol.28, 2013, https://doi.org/10.1016/j.ecolind.2012.01.020
  21. Use of Reporter Genes in the Generation of Vaccinia Virus-Derived Vectors vol.8, pp.5, 2016, https://doi.org/10.3390/v8050134
  22. Translational efficiency of BVDV IRES and EMCV IRES for T7 RNA polymerase driven cytoplasmic expression in mammalian cell lines vol.51, pp.2, 2017, https://doi.org/10.1134/S002689331702011X
  23. Fluorescent protein-based detection of φC31 integrase activity in mammalian cells vol.441, pp.2, 2013, https://doi.org/10.1016/j.ab.2013.07.024
  24. Using yeast to determine the functional consequences of mutations in the human p53 tumor suppressor gene: An introductory course-based undergraduate research experience in molecular and cell biology vol.45, pp.2, 2017, https://doi.org/10.1002/bmb.21024
  25. Application of β-glucuronidase (GusA) as an effective reporter for extremely acidophilic Acidithiobacillus ferrooxidans vol.101, pp.8, 2017, https://doi.org/10.1007/s00253-017-8116-9
  26. Protein display on the Yarrowia lipolytica yeast cell surface using the cell wall protein YlPir1 vol.48, pp.7, 2012, https://doi.org/10.1134/S0003683812070058
  27. β-Glucuronidase as a Sensitive and Versatile Reporter in Actinomycetes vol.77, pp.15, 2011, https://doi.org/10.1128/AEM.00434-11
  28. SaCas9 Requires 5′-NNGRRT-3′ PAM for Sufficient Cleavage and Possesses Higher Cleavage Activity than SpCas9 or FnCpf1 in Human Cells vol.13, pp.4, 2018, https://doi.org/10.1002/biot.201700561
  29. vol.46, pp.4, 2018, https://doi.org/10.1080/12298093.2018.1548806
  30. New Applications of Synthetic Biology Tools for Cyanobacterial Metabolic Engineering vol.7, pp.2296-4185, 2019, https://doi.org/10.3389/fbioe.2019.00033