Mammalian designer cells: Engineering principles and biomedical applications

Biotechnology Journal

Volumn 10, Issue 7, 2015, Pages 1005-1018

  Xie, Mingqi ^a   Fussenegger, Martin ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Biocomputer; Cell therapy; Gene regulation; Mammalian production; Trigger inducible designer cell

Indexed keywords

BIOLOGICAL SYSTEMS; BIOLOGY; BIOTECHNOLOGY; CELLS; CYTOLOGY; DESIGN; GENE EXPRESSION; GENE THERAPY; GENES; MAMMALS; MEDICAL APPLICATIONS; MOBILE SECURITY; REMOTE CONTROL;

BIOCOMPUTER; BIOMEDICAL APPLICATIONS; BIOTECHNOLOGY INDUSTRY; CELL THERAPY; COMPLEX BIOLOGICAL SYSTEMS; ENGINEERING PRINCIPLES; INTERDISCIPLINARY FIELDS; TRANSLATIONAL MEDICINE;

CELL ENGINEERING;

NUCLEASE; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; BIOENGINEERING; BIOTECHNOLOGY; CELL ENGINEERING; CELL SURFACE; DNA BINDING; DNA SEQUENCE; GENE CONTROL; GENE TARGETING; GENETIC TRANSCRIPTION; MAMMAL CELL; PRIORITY JOURNAL; PROMOTER REGION; REPRESSOR GENE; REVIEW; RNA INTERFERENCE; SECOND MESSENGER; SYNTHETIC BIOLOGY; TRANSACTIVATION; ANIMAL; BIOLOGICAL THERAPY; GENE EXPRESSION REGULATION; MAMMAL;

MAMMALIA;

ANIMALS; BIOTECHNOLOGY; CELL ENGINEERING; CELL- AND TISSUE-BASED THERAPY; GENE EXPRESSION REGULATION; MAMMALS; SYNTHETIC BIOLOGY;

EID: 84935746483     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400642     Document Type: Review

References (111)

1. Auslander, S., Fussenegger, M., Synthetic biology. Dynamic genome engineering in living cells. Science 2014, 346, 813-814.
2. Benenson, Y., Biomolecular computing systems: Principles, progress and potential. Nat. Rev. Genet. 2012, 13, 455-468.
3. Auslander, S., Fussenegger, M., From gene switches to mammalian designer cells: Present and future prospects. Trends Biotechnol. 2013, 31, 155-168.
4. Nielsen, J., Fussenegger, M., Keasling, J., Lee, S. Y. et al., Engineering synergy in biotechnology. Nat. Chem. Biol. 2014, 10, 319-322.
5. Philp, J. C., Ritchie, R. J., Allan, J. E., Synthetic biology, the bioeconomy, and a societal quandary. Trends Biotechnol. 2013, 31, 269-272.
6. Fussenegger, M., The impact of mammalian gene regulation concepts on functional genomic research, metabolic engineering, and advanced gene therapies. Biotechnol. Prog. 2001, 17, 1-51.
7. Peralta-Yahya, P. P., Zhang, F., del Cardayre, S. B., Keasling, J. D., Microbial engineering for the production of advanced biofuels. Nature 2012, 488, 320-328.
8. Erickson, B., Singh, R., Winters, P., Synthetic biology: Regulating industry uses of new biotechnologies. Science 2011, 333, 1254-1256.
9. Keasling, J. D., Synthetic biology and the development of tools for metabolic engineering. Metab. Eng. 2012, 14, 189-195.
10. Way, J. C., Collins, J. J., Keasling, J. D., Silver, P. A., Integrating biological redesign: Where synthetic biology came from and where it needs to go. Cell 2014, 157, 151-161.
11. Kumar, N., Borth, N., Flow-cytometry and cell sorting: An efficient approach to investigate productivity and cell physiology in mammalian cell factories. Methods 2012, 56, 366-374.
12. Geering, B., Fussenegger, M., Synthetic immunology: Modulating the human immune system. Trends Biotechnol. 2014.
13. Bacchus, W., Aubel, D., Fussenegger, M., Biomedically relevant circuit-design strategies in mammalian synthetic biology. Mol. Syst. Biol. 2013, 9, 691.
14. Jakobus, K., Wend, S., Weber, W., Synthetic mammalian gene networks as a blueprint for the design of interactive biohybrid materials. Chem. Soc. Rev. 2012, 41, 1000-1018.
15. Cameron, D. E., Bashor, C. J., Collins, J. J., A brief history of synthetic biology. Nat. Rev. Microbiol. 2014, 12, 381-390.
16. Church, G. M., Elowitz, M. B., Smolke, C. D., Voigt, C. A., Weiss, R., Realizing the potential of synthetic biology. Nat. Rev. Mol. Cell Biol. 2014, 15, 289-294.
17. Auslander, S., Fussenegger, M., Synthetic biology: Toehold gene switches make big footprints. Nature 2014, 516, 333-334.
18. Lienert, F., Lohmueller, J. J., Garg, A., Silver, P. A., Synthetic biology in mammalian cells: Next generation research tools and therapeutics. Nat. Rev. Mol. Cell Biol. 2014, 15, 95-107.
19. Muller, K., Engesser, R., Timmer, J., Zurbriggen, M. D., Weber, W., Orthogonal optogenetic triple-gene control in mammalian cells. ACS Synth. Biol. 2014, 3, 796-801.
20. Folcher, M., Xie, M., Spinnler, A., Fussenegger, M., Synthetic mammalian trigger-controlled bipartite transcription factors. Nucleic Acids Res. 2013, 41, e134.
21. Muller, K., Naumann, S., Weber, W., Zurbriggen, M. D., Optogenetics for gene expression in mammalian cells. Biol. Chem. 2015, 396, 145-152.
22. Ye, H., Daoud-El Baba, M., Peng, R. W., Fussenegger, M., A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science 2011, 332, 1565-1568.
23. Tischer, D., Weiner, O. D., Illuminating cell signalling with optogenetic tools. Nat. Rev. Mol. Cell Biol. 2014, 15, 551-558.
24. Folcher, M., Oesterle, S., Zwicky, K., Thekkottil, T. et al., Mind-controlled transgene expression by a wireless-powered optogenetic designer cell implant. Nat. Commun. 2014, 5, 5392.
25. Wieland, M., Fussenegger, M., Reprogrammed cell delivery for personalized medicine. Adv. Drug Deliv. Rev. 2012, 64, 1477-1487.
26. Folcher, M., Fussenegger, M., Synthetic biology advancing clinical applications. Curr. Opin. Chem. Biol. 2012, 16, 345-354.
27. Purcell, O., Peccoud, J., Lu, T. K., Rule-based design of synthetic transcription factors in eukaryotes. ACS Synth. Biol. 2014, 3, 737-744.
28. Ramos, J. L., Martinez-Bueno, M., Molina-Henares, A. J., Teran, W. et al., The TetR family of transcriptional repressors. Microbiol. Mol. Biol. Rev. 2005, 69, 326-356.
29. Perera, I. C., Grove, A., Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators. J. Mol. Cell Biol. 2010, 2, 243-254.
30. Stanton, B. C., Siciliano, V., Ghodasara, A., Wroblewska, L. et al., Systematic transfer of prokaryotic sensors and circuits to mammalian cells. ACS Synth. Biol. 2014, 3, 880-891.
31. Khalil, A. S., Lu, T. K., Bashor, C. J., Ramirez, C. L. et al., A synthetic biology framework for programming eukaryotic transcription functions. Cell 2012, 150, 647-658.
32. Perez-Pinera, P., Kocak, D. D., Vockley, C. M., Adler, A. F. et al., RNA-guided gene activation by CRISPR-Cas9-based transcription factors. Nat. Methods 2013, 10, 973-976.
33. Wieland, M., Fussenegger, M., Engineering molecular circuits using synthetic biology in mammalian cells. Annu. Rev. Chem. Biomol. Eng. 2012, 3, 209-234.
34. Weber, W., Fussenegger, M., Engineering of synthetic mammalian gene networks. Chem. Biol. 2009, 16, 287-297.
35. Khalil, A. S., Collins, J. J., Synthetic biology: Applications come of age. Nat. Rev. Genet. 2010, 11, 367-379.
36. Tigges, M., Fussenegger, M., Recent advances in mammalian synthetic biology-design of synthetic transgene control networks. Curr. Opin. Biotechnol. 2009, 20, 449-460.
37. Gossen, M., Freundlieb, S., Bender, G., Muller, G. et al., Transcriptional activation by tetracyclines in mammalian cells. Science 1995, 268, 1766-1769.
38. Urlinger, S., Baron, U., Thellmann, M., Hasan, M. T. et al., Exploring the sequence space for tetracycline-dependent transcriptional activators: Novel mutations yield expanded range and sensitivity. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 7963-7968.
39. Shaikh, S., Nicholson, L. F., Optimization of the Tet-On system for inducible expression of RAGE. J. Biomol. Tech. 2006, 17, 283-292.
40. Kamionka, A., Bogdanska-Urbaniak, J., Scholz, O., Hillen, W., Two mutations in the tetracycline repressor change the inducer anhydrotetracycline to a corepressor. Nucleic Acids Res. 2004, 32, 842-847.
41. Krueger, M., Scholz, O., Wisshak, S., Hillen, W., Engineered Tet repressors with recognition specificity for the tetO-4C5G operator variant. Gene 2007, 404, 93-100.
42. Scholz, O., Kostner, M., Reich, M., Gastiger, S., Hillen, W., Teaching TetR to recognize a new inducer. J. Mol. Biol. 2003, 329, 217-227.
43. Krueger, C., Schmidt, A., Danke, C., Hillen, W., Berens, C., Transactivator mutants with altered effector specificity allow selective regulation of two genes by tetracycline variants. Gene 2004, 331, 125-131.
44. Daniel, R., Rubens, J. R., Sarpeshkar, R., Lu, T. K., Synthetic analog computation in living cells. Nature 2013, 497, 619-623.
45. Sauro, H. M., Kim, K. H., Synthetic biology: It's an analog world. Nature 2013, 497, 572-573.
46. Kramer, B. P., Viretta, A. U., Daoud-El-Baba, M., Aubel, D. et al., An engineered epigenetic transgene switch in mammalian cells. Nat. Biotechnol. 2004, 22, 867-870.
47. Kramer, B. P., Fischer, C., Fussenegger, M., BioLogic gates enable logical transcription control in mammalian cells. Biotechnol. Bioeng. 2004, 87, 478-484.
48. Greber, D., Fussenegger, M., An engineered mammalian band-pass network. Nucleic Acids Res. 2010, 38, e174.
49. Kramer, B. P., Fussenegger, M., Hysteresis in a synthetic mammalian gene network. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 9517-9522.
50. Burrill, D. R., Inniss, M. C., Boyle, P. M., Silver, P. A., Synthetic memory circuits for tracking human cell fate. Genes Dev. 2012, 26, 1486-1497.
51. Xie, M., Ye, H., Hamri, G. C., Fussenegger, M., Antagonistic control of a dual-input mammalian gene switch by food additives. Nucleic Acids Res. 2014, 42, e116.
52. Vannelli, T. A., Dykman, A., Ortiz de Montellano, P. R., The antituberculosis drug ethionamide is activated by a flavoprotein monooxygenase. J. Biol. Chem. 2002, 277, 12824-12829.
53. Weber, W., Schoenmakers, R., Keller, B., Gitzinger, M. et al., A synthetic mammalian gene circuit reveals antituberculosis compounds. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9994-9998.
54. Pieren, M., Tigges, M., Adjuvant strategies for potentiation of antibiotics to overcome antimicrobial resistance. Curr. Opin. Pharmacol. 2012, 12, 551-555.
55. Ye, H., Aubel, D., Fussenegger, M., Synthetic mammalian gene circuits for biomedical applications. Curr. Opin. Chem. Biol. 2013, 17, 910-917.
56. Ye, H., Fussenegger, M., Synthetic therapeutic gene circuits in mammalian cells. FEBS Lett. 2014, 588, 2537-2544.
57. Kemmer, C., Gitzinger, M., Daoud-El Baba, M., Djonov, V. et al., Self-sufficient control of urate homeostasis in mice by a synthetic circuit. Nat. Biotechnol. 2010, 28, 355-360.
58. Gaj, T., Gersbach, C. A., Barbas, C. F., 3rd, ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013, 31, 397-405.
59. Lienert, F., Torella, J. P., Chen, J. H., Norsworthy, M. et al., Two- and three-input TALE-based AND logic computation in embryonic stem cells. Nucleic Acids Res. 2013, 41, 9967-9975.
60. Muller, K., Engesser, R., Metzger, S., Schulz, S. et al., A red/far-red light-responsive bi-stable toggle switch to control gene expression in mammalian cells. Nucleic Acids Res. 2013, 41, e77.
61. Nissim, L., Bar-Ziv, R. H., A tunable dual-promoter integrator for targeting of cancer cells. Mol. Syst. Biol. 2010, 6, 444.
62. Elleuche, S., Poggeler, S., Inteins, valuable genetic elements in molecular biology and biotechnology. Appl. Microbiol. Biotechnol. 2010, 87, 479-489.
63. Auslander, S., Stucheli, P., Rehm, C., Auslander, D. et al., A general design strategy for protein-responsive riboswitches in mammalian cells. Nat. Methods 2014, 11, 1154-1160.
64. Saito, H., Kobayashi, T., Hara, T., Fujita, Y. et al., Synthetic translational regulation by an L7Ae-kink-turn RNP switch. Nat. Chem. Biol. 2010, 6, 71-78.
65. Auslander, S., Auslander, D., Muller, M., Wieland, M., Fussenegger, M., Programmable single-cell mammalian biocomputers. Nature 2012, 487, 123-127.
66. Lucks, J. B., Qi, L., Mutalik, V. K., Wang, D., Arkin, A. P., Versatile RNA-sensing transcriptional regulators for engineering genetic networks. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 8617-8622.
67. Giudice, J., Cooper, T. A., RNA-binding proteins in heart development. Adv. Exp. Med. Biol. 2014, 825, 389-429.
68. Wittmann, A., Suess, B., Engineered riboswitches: Expanding researchers' toolbox with synthetic RNA regulators. FEBS Lett. 2012, 586, 2076-2083.
69. Culler, S. J., Hoff, K. G., Smolke, C. D., Reprogramming cellular behavior with RNA controllers responsive to endogenous proteins. Science 2010, 330, 1251-1255.
70. Ipsaro, J. J., Joshua-Tor, L., From guide to target: Molecular insights into eukaryotic RNA-interference machinery. Nat. Struct. Mol. Biol. 2015, 22, 20-28.
71. Chang, A. L., Wolf, J. J., Smolke, C. D., Synthetic RNA switches as a tool for temporal and spatial control over gene expression. Curr. Opin. Biotechnol. 2012, 23, 679-688.
72. Leisner, M., Bleris, L., Lohmueller, J., Xie, Z., Benenson, Y., MicroRNA circuits for transcriptional logic. Methods Mol. Biol. 2012, 813, 169-186.
73. Deans, T. L., Cantor, C. R., Collins, J. J., A tunable genetic switch based on RNAi and repressor proteins for regulating gene expression in mammalian cells. Cell 2007, 130, 363-372.
74. Prochazka, L., Angelici, B., Haefliger, B., Benenson, Y., Highly modular bow-tie gene circuits with programmable dynamic behaviour. Nat. Commun. 2014, 5, 4729.
75. Xie, Z., Wroblewska, L., Prochazka, L., Weiss, R., Benenson, Y., Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 2011, 333, 1307-1311.
76. Tigges, M., Denervaud, N., Greber, D., Stelling, J., Fussenegger, M., A synthetic low-frequency mammalian oscillator. Nucleic Acids Res. 2010, 38, 2702-2711.
77. Lapique, N., Benenson, Y., Digital switching in a biosensor circuit via programmable timing of gene availability. Nat. Chem. Biol. 2014, 10, 1020-1027.
78. Benenson, Y., Engineering. Recombinatorial logic. Science 2013, 340, 554-555.
79. Brown, W. R., Lee, N. C., Xu, Z., Smith, M. C., Serine recombinases as tools for genome engineering. Methods 2011, 53, 372-379.
80. Garcia-Otin, A. L., Guillou, F., Mammalian genome targeting using site-specific recombinases. Front. Biosci. 2006, 11, 1108-1136.
81. Schnutgen, F., Doerflinger, N., Calleja, C., Wendling, O. et al., A directional strategy for monitoring Cre-mediated recombination at the cellular level in the mouse. Nat. Biotechnol. 2003, 21, 562-565.
82. Siuti, P., Yazbek, J., Lu, T. K., Synthetic circuits integrating logic and memory in living cells. Nat. Biotechnol. 2013, 31, 448-452.
83. Soriano, P., Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21, 70-71.
84. Hoppe, P. S., Coutu, D. L., Schroeder, T., Single-cell technologies sharpen up mammalian stem cell research. Nat. Cell. Biol. 2014, 16, 919-927.
85. Barker, N., van Es, J. H., Kuipers, J., Kujala, P. et al., Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449, 1003-1007.
86. Barker, N., Adult intestinal stem cells: Critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol. 2014, 15, 19-33.
87. Cong, L., Ran, F. A., Cox, D., Lin, S. et al., Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339, 819-823.
88. Gonzalez, F., Zhu, Z., Shi, Z. D., Lelli, K. et al., An iCRISPR platform for rapid, multiplexable, and inducible genome editing in human pluripotent stem cells. Cell Stem Cell 2014, 15, 215-226.
89. Jinek, M., East, A., Cheng, A., Lin, S. et al., RNA-programmed genome editing in human cells. eLife 2013, 2, e00471.
90. Porteus, M. H., Carroll, D., Gene targeting using zinc finger nucleases. Nat. Biotechnol. 2005, 23, 967-973.
91. Mali, P., Esvelt, K. M., Church, G. M., Cas9 as a versatile tool for engineering biology. Nat. Methods 2013, 10, 957-963.
92. Mali, P., Yang, L., Esvelt, K. M., Aach, J. et al., RNA-guided human genome engineering via Cas9. Science 2013, 339, 823-826.
93. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M. et al., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337, 816-821.
94. Kiani, S., Beal, J., Ebrahimkhani, M. R., Huh, J. et al., CRISPR transcriptional repression devices and layered circuits in mammalian cells. Nat. Methods 2014, 11, 723-726.
95. Hansen, J., Mailand, E., Swaminathan, K. K., Schreiber, J. et al., Transplantation of prokaryotic two-component signaling pathways into mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 15705-15710.
96. Kramer, B. P., Fischer, M., Fussenegger, M., Semi-synthetic mammalian gene regulatory networks. Metab. Eng. 2005, 7, 241-250.
97. Rossger, K., Charpin-El Hamri, G., Fussenegger, M., Reward-based hypertension control by a synthetic brain-dopamine interface. Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 18150-18155.
98. Heng, B. C., Aubel, D., Fussenegger, M., G protein-coupled receptors revisited: Therapeutic applications inspired by synthetic biology. Annu. Rev. Pharmacol. Toxicol. 2014, 54, 227-249.
99. Rooney, J. W., Hodge, M. R., McCaffrey, P. G., Rao, A., Glimcher, L. H., A common factor regulates both Th1- and Th2-specific cytokine gene expression. EMBO J. 1994, 13, 625-633.
100. Hogan, P. G., Chen, L., Nardone, J., Rao, A., Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003, 17, 2205-2232.
101. Burdette, D. L., Monroe, K. M., Sotelo-Troha, K., Iwig, J. S. et al., STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011, 478, 515-518.
102. Sheng, M., Dougan, S. T., McFadden, G., Greenberg, M. E., Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences. Mol. Cell Biol. 1988, 8, 2787-2796.
103. Sassone-Corsi, P., Transcription factors responsive to cAMP. Annu. Rev. Cell Dev. Biol. 1995, 11, 355-377.
104. Stanley, S. A., Gagner, J. E., Damanpour, S., Yoshida, M. et al., Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 2012, 336, 604-608.
105. Stanley, S. A., Sauer, J., Kane, R. S., Dordick, J. S., Friedman, J. M., Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 2015, 21, 92-98.
106. Danilchanka, O., Mekalanos, J. J., Cyclic dinucleotides and the innate immune response. Cell 2013, 154, 962-970.
107. Heng, B. C., Aubel, D., Fussenegger, M., An overview of the diverse roles of G-protein coupled receptors (GPCRs) in the pathophysiology of various human diseases. Biotechnol. Adv. 2013, 31, 1676-1694.
108. Auslander, D., Auslander, S., Charpin-El Hamri, G., Sedlmayer, F. et al., A synthetic multifunctional mammalian pH sensor and CO2 transgene-control device. Mol. Cell 2014, 55, 397-408.
109. Auslander, D., Eggerschwiler, B., Kemmer, C., Geering, B. et al., A designer cell-based histamine-specific human allergy profiler. Nat. Commun. 2014, 5, 4408.
110. Murtas, G., Artificial assembly of a minimal cell. Mol. Biosyst. 2009, 5, 1292-1297.
111. Barrett, D. M., Singh, N., Porter, D. L., Grupp, S. A., June, C. H., Chimeric antigen receptor therapy for cancer. Annu. Rev. Med. 2014, 65, 333-347.