RNA-aptamers-in-droplets (RAPID) high-throughput screening for secretory phenotypes

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Abatemarco, Joseph ^a   Sarhan, Maen F ^b,c   Wagner, James M ^a   Lin, Jyun Liang ^a   Liu, Leqian ^b,c   Hassouneh, Wafa ^b,c,d   Yuan, Shuo Fu ^e   Alper, Hal S ^a,e   Abate, Adam R ^b,c,d  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CHAN ZUCKERBERG BIOHUB   (United States)

^e UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SACCHAROMYCES CEREVISIAE;

APTAMER; RECOMBINANT PROTEIN; STREPTAVIDIN; TYROSINE;

BIOSYNTHESIS; FLUORESCENCE MICROSCOPY; GENETICS; HIGH THROUGHPUT SCREENING; METABOLIC ENGINEERING; METABOLISM; MICROFLUIDIC ANALYSIS; PHENOTYPE; PROCEDURES; REPRODUCIBILITY; SACCHAROMYCES CEREVISIAE;

APTAMERS, NUCLEOTIDE; HIGH-THROUGHPUT SCREENING ASSAYS; METABOLIC ENGINEERING; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, FLUORESCENCE; PHENOTYPE; RECOMBINANT PROTEINS; REPRODUCIBILITY OF RESULTS; SACCHAROMYCES CEREVISIAE; STREPTAVIDIN; TYROSINE;

EID: 85028018078     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00425-7     Document Type: Article

References (67)

1. Curran, K. A. & Alper, H. S. Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metab. Eng. 14, 289-297 (2012).
2. Sun, J. & Alper, H. S. Metabolic engineering of strains: from industrial-scale to lab-scale chemical production. J. Ind. Microbiol. Biotechnol. 42, 423-436 (2015).
3. Kosuri, S. & Church, G. M. Large-scale de novo DNA synthesis: technologies and applications. Nat. Methods 11, 499-507 (2014).
4. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).
5. DiCarlo, J. E. et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 41, 4336-4343 (2013).
6. Sander, J. D. & Joung, J. K. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355 (2014).
7. Bortesi, L. & Fischer, R. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33, 41-52 (2015).
8. Gaj, T., Gersbach, C. A. & Barbas, C. F. 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 31, 397-405 (2013).
9. Esvelt, K. M., Carlson, J. C. & Liu, D. R. A system for the continuous directed evolution of biomolecules. Nature 472, 499-503 (2011).
10. Crook, N. et al. In vivo continuous evolution of genes and pathways in yeast. Nat. Commun. 7, 13051 (2016).
11. Brophy, J. A. & Voigt, C. A. Principles of genetic circuit design. Nat. Methods 11, 508-520 (2014).
12. Nielsen, A. A. et al. Genetic circuit design automation. Science 352, aac7341 (2016).
13. Otero-Muras, I., Henriques, D. & Banga, J. R. SYNBADm: a tool for optimization-based automated design of synthetic gene circuits. Bioinformatics. 32, 3360-3362 (2016).
14. Deaner, M. & Alper, H. S. in Advances in Biochemical Engineering/Biotechnology 1-24 (Springer Berlin Heidelberg, 2016).
15. Klein-Marcuschamer, D., Yadav, V. G., Ghaderi, A. & Stephanopoulos, G. N. in Biosystems Engineering I: Creating Superior Biocatalysts (eds Christoph, W. & Rainer, K.) 101-131 (Springer Berlin Heidelberg, 2010).
16. Purnick, P. E. & Weiss, R. The second wave of synthetic biology: from modules to systems. Nature reviews. Mol. Cell Biol. 10, 410-422 (2009).
17. Deaner, M. & Alper, H. S. Systematic testing of enzyme perturbation sensitivities via graded dCas9 modulation in Saccharomyces cerevisiae. Metab. Eng. 40, 14-22 (2017).
18. Johnson, J. R. et al. GeneMill: A 21st century platform for innovation. Biochem. Soc. Trans. 44, 681-683 (2016).
19. Wang, H. H. et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894-898 (2009).
20. Shih, S. C. et al. A versatile microfluidic device for automating synthetic biology. ACS Synth. Biol. 4, 1151-1164 (2015).
21. Mahr, R., von Boeselager, R. F., Wiechert, J. & Frunzke, J. Screening of an Escherichia coli promoter library for a phenylalanine biosensor. Appl. Microbiol. Biotechnol. 100, 6739-6753 (2016).
22. Zhang, F. & Keasling, J. Biosensors and their applications in microbial metabolic engineering. Trends Microbiol. 19, 323-329 (2011).
23. Williams, T. C., Pretorius, I. S. & Paulsen, I. T. Synthetic evolution of metabolic productivity using biosensors. Trends Biotechnol. 34, 371-381 (2016).
24. Rogers, J. K., Taylor, N. D. & Church, G. M. Biosensor-based engineering of biosynthetic pathways. Curr. Opin. Biotechnol. 42, 84-91 (2016).
25. Tawfik, D. S. & Griffiths, A. D. Man-made cell-like compartments for molecular evolution. Nat. Biotechnol. 16, 652-656 (1998).
26. Aharoni, A., Amitai, G., Bernath, K., Magdassi, S. & Tawfik, D. S. High-throughput screening of enzyme libraries: thiolactonases evolved by fluorescence-activated sorting of single cells in emulsion compartments. Chem. Biol. 12, 1281-1289 (2005).
27. Miller, O. J. et al. Directed evolution by in vitro compartmentalization. Nat. Methods 3, 561-570 (2006).
28. Huebner, A. et al. Quantitative detection of protein expression in single cells using droplet microfluidics. Chem. Commun. 2007, 1218-1220, (2007).
29. Agresti, J. J. et al. Ultrahigh-throughput screening in drop-based microfluidics for directed evolution. Proc. Natl Acad. Sci. USA 107, 4004-4009 (2010).
30. Beneyton, T. et al. Droplet-based microfluidic high-throughput screening of heterologous enzymes secreted by the yeast Yarrowia lipolytica. Microb. Cell Fact. 16, 18 (2017).
31. Huang, M. et al. Microfluidic screening and whole-genome sequencing identifies mutations associated with improved protein secretion by yeast. Proc. Natl Acad. Sci. USA 112, E4689-E4696 (2015).
32. Sjostrom, S. L. et al. High-throughput screening for industrial enzyme production hosts by droplet microfluidics. Lab. Chip 14, 806-813 (2014).
33. Wang, B. L. et al. Microfluidic high-throughput culturing of single cells for selection based on extracellular metabolite production or consumption. Nat. Biotechnol. 32, 473-478 (2014).
34. Sciambi, A. & Abate, A. R. Accurate microfluidic sorting of droplets at 30 kHz. Lab. Chip 15, 47-51 (2015).
35. Paige, J. S., Nguyen-Duc, T., Song, W. & Jaffrey, S. R. Fluorescence imaging of cellular metabolites with RNA. Science 335, 1194 (2012).
36. McKeague, M. & Derosa, M. C. Challenges and opportunities for small molecule aptamer development. J. Nucleic Acids 2012, 748913 (2012).
37. Song, W., Strack, R. L. & Jaffrey, S. R. Imaging bacterial protein expression using genetically encoded sensors composed of RNA. Nat. Methods 10, 873-875 (2013).
38. Hamaguchi, N., Ellington, A. & Stanton, M. Aptamer beacons for the direct detection of proteins. Anal. Biochem. 294, 126-131 (2001).
39. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic. Acids. Res. 31, 3406-3415 (2003).
40. O'Donovan, B., Eastburn, D. J. & Abate, A. R. Electrode-free picoinjection of microfluidic drops. Lab. Chip. 12, 4029-4032 (2012).
41. Ahn, K., Agresti, J., Chong, H., Marquez, M. & Weitz, D. Electrocoalescence of drops synchronized by size-dependent flow in microfluidic channels. Appl. Phys. Lett. 88, 264105 (2006).
42. Mannironi, C., Scerch, C., Fruscoloni, P. & Tocchini-Valentini, G. P. Molecular recognition of amino acids by RNA aptamers: the evolution into an L-tyrosine binder of a dopamine-binding RNA motif. RNA. 6, 520-527 (2000).
43. Curran, K. A., Leavitt, J. M., Karim, A. S. & Alper, H. S. Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab. Eng. 15, 55-66 (2013).
44. Leavitt, J. M. et al. Biosensor-enabled directed evolution to improve muconic acid production in Saccharomyces cerevisiae. Biotechnol. J. doi: 10.1002/biot.201600687 (2017).
45. Lutke-Eversloh, T. & Stephanopoulos, G. L-tyrosine production by deregulated strains of Escherichia coli. Appl. Microbiol. Biotechnol. 75, 103-110 (2007).
46. Hartmann, M. et al. Evolution of feedback-inhibited β/α barrel isoenzymes by gene duplication and a single mutation. Proc. Natl Acad. Sci. USA 100, 862-867 (2003).
47. Luttik, M. A. et al. Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab. Eng. 10, 141-153 (2008).
48. Weber, P. C., Ohlendorf, D. H., Wendoloski, J. J. & Salemme, F. R. Structural origins of high-affinity biotin binding to streptavidin. Science 243, 85-88 (1989).
49. Schmidt, T. G., Koepke, J., Frank, R. & Skerra, A. Molecular interaction between the Strep-tag affinity peptide and its cognate target, streptavidin. J. Mol. Biol. 255, 753-766 (1996).
50. Singh, N. P. et al. A novel approach to cancer immunotherapy: tumor cells decorated with CD80 generate effective antitumor immunity. Cancer Res. 63, 4067-4073 (2003).
51. Hultman, T., Ståhl, S., Hornes, E. & Uhlén, M. Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res. 17, 4937-4946 (1989).
52. Keefe, A. D., Wilson, D. S., Seelig, B. & Szostak, J. W. One-step purification of recombinant proteins using a nanomolar-affinity streptavidin-binding peptide, the SBP-Tag. Protein Exp. Purif. 23, 440-446 (2001).
53. Wilchek, M. & Bayer, E. A. The avidin-biotin complex in bioanalytical applications. Anal. Biochem. 171, 1-32 (1988).
54. Green, N. M. Avidin and streptavidin. Methods Enzymol. 184, 51-67 (1990).
55. Sano, T. & Cantor, C. R. Expression of a cloned streptavidin gene in Escherichia coli. Proc. Natl Acad. Sci. USA 87, 142-146 (1990).
56. Wu, S. C., Hassan Qureshi, M. & Wong, S. L. Secretory production and purification of functional full-length streptavidin from Bacillus subtilis. Protein Exp. Purif. 24, 348-356 (2002).
57. Nogueira, E. S. et al. High-level secretion of recombinant full-length streptavidin in Pichia pastoris and its application to enantioselective catalysis. Protein. Expr. Purif. 93, 54-62 (2014).
58. Lim, K. H., Hwang, I. & Park, S. Biotin-assisted folding of streptavidin on the yeast surface. Biotechnol. Prog. 28, 276-283 (2012).
59. Rakestraw, J. A., Sazinsky, S. L., Piatesi, A., Antipov, E. & Wittrup, K. D. Directed evolution of a secretory leader for the improved expression of heterologous proteins and full-length antibodies in Saccharomyces cerevisiae. Biotechnol. Bioeng. 103, 1192-1201 (2009).
60. Darmostuk, M., Rimpelova, S., Gbelcova, H. & Ruml, T. Current approaches in SELEX: An update to aptamer selection technology. Biotechnol. Adv. 33, 1141-1161 (2015).
61. Najah, M. et al. Droplet-based microfluidics platform for ultra-high-throughput bioprospecting of cellulolytic microorganisms. Chem. Biol. 21, 1722-1732 (2014).
62. Colin, P. Y. et al. Ultrahigh-throughput discovery of promiscuous enzymes by picodroplet functional metagenomics. Nat. Commun. 6, 10008 (2015).
63. Terekhov, S. S. et al. Microfluidic droplet platform for ultrahigh-throughput single-cell screening of biodiversity. Proc. Natl Acad. Sci. USA 114, 2550-2555 (2017).
64. Xia, Y. & Whitesides, G. M. Soft lithography. Annu. Rev. Mater. Sci. 28, 153-184 (1998).
65. Hegemann, J. H. & Heick, S. B. Delete and repeat: a comprehensive toolkit for sequential gene knockout in the budding yeast Saccharomyces cerevisiae. Methods Mol. Biol. 765, 189-206 (2011).
66. Mumberg, D., Müller, R. & Funk, M. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768 (1994).
67. Zaccolo, M., Williams, D. M., Brown, D. M. & Gherardi, E. An approach to random mutagenesis of DNA using mixtures of triphosphate derivatives of nucleoside analogues. J. Mol. Biol. 255, 589-603 (1996).