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Bottom-up approaches in synthetic biology and biomaterials for tissue engineering applications

  • Biotechnology Methods - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Synthetic biologists use engineering principles to design and construct genetic circuits for programming cells with novel functions. A bottom-up approach is commonly used to design and construct genetic circuits by piecing together functional modules that are capable of reprogramming cells with novel behavior. While genetic circuits control cell operations through the tight regulation of gene expression, a diverse array of environmental factors within the extracellular space also has a significant impact on cell behavior. This extracellular space offers an addition route for synthetic biologists to apply their engineering principles to program cell-responsive modules within the extracellular space using biomaterials. In this review, we discuss how taking a bottom-up approach to build genetic circuits using DNA modules can be applied to biomaterials for controlling cell behavior from the extracellular milieu. We suggest that, by collectively controlling intrinsic and extrinsic signals in synthetic biology and biomaterials, tissue engineering outcomes can be improved.

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References

  1. Callura JM, Cantor CR, Collins JJ (2012) Genetic switchboard for synthetic biology applications. Proc Natl Acad Sci USA 109(15):5850–5855

    Article  PubMed  Google Scholar 

  2. Chang AL, Wolf JJ, Smolke CD (2012) Synthetic RNA switches as a tool for temporal and spatial control over gene expression. Curr Opin Biotechnol 23(5):679–688

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Deans TL, Cantor CR, Collins JJ (2007) A tunable genetic switch based on RNAi and repressor proteins for regulating gene expression in mammalian cells. Cell 130(2):363–372

    Article  PubMed  CAS  Google Scholar 

  4. Fitzgerald M, Gibbs C, Shimpi AA, Deans TL (2017) Adoption of the Q transcriptional system for regulating gene expression in stem cells. ACS Synth Biol 6(11):2014–2020

    Article  PubMed  CAS  Google Scholar 

  5. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403(6767):339–342

    Article  PubMed  CAS  Google Scholar 

  6. Green AA et al (2014) Toehold switches: de-novo-designed regulators of gene expression. Cell 159(4):925–939

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Horner M, Weber W (2012) Molecular switches in animal cells. FEBS Lett 586(15):2084–2096

    Article  PubMed  CAS  Google Scholar 

  8. Kramer BP et al (2004) An engineered epigenetic transgene switch in mammalian cells. Nat Biotechnol 22(7):867–870

    Article  PubMed  CAS  Google Scholar 

  9. Mandal M et al (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113(5):577–586

    Article  PubMed  CAS  Google Scholar 

  10. Polstein LR et al (2017) An engineered optogenetic switch for spatiotemporal control of gene expression, cell differentiation, and tissue morphogenesis. ACS Synth Biol 6(11):2003–2013

    Article  PubMed  CAS  Google Scholar 

  11. Schmidl SR et al (2014) Refactoring and optimization of light-switchable Escherichia coli two-component systems. ACS Synth Biol 3(11):820–831

    Article  PubMed  CAS  Google Scholar 

  12. Weber W, Fussenegger M (2011) Molecular diversity–the toolbox for synthetic gene switches and networks. Curr Opin Chem Biol 15(3):414–420

    Article  PubMed  CAS  Google Scholar 

  13. Aulehla A, Pourquie O (2008) Oscillating signaling pathways during embryonic development. Curr Opin Cell Biol 20(6):632–637

    Article  PubMed  CAS  Google Scholar 

  14. Danino T et al (2010) A synchronized quorum of genetic clocks. Nature 463(7279):326–330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403(6767):335–338

    Article  PubMed  CAS  Google Scholar 

  16. Fung E et al (2005) A synthetic gene-metabolic oscillator. Nature 435(7038):118–122

    Article  PubMed  CAS  Google Scholar 

  17. Judd EM, Laub MT, McAdams HH (2000) Toggles and oscillators: new genetic circuit designs. BioEssays 22(6):507–509

    Article  PubMed  CAS  Google Scholar 

  18. Stricker J et al (2008) A fast, robust and tunable synthetic gene oscillator. Nature 456(7221):516–519

    Article  PubMed  CAS  Google Scholar 

  19. Tigges M et al (2009) A tunable synthetic mammalian oscillator. Nature 457(7227):309–312

    Article  PubMed  CAS  Google Scholar 

  20. Friedland AE et al (2009) Synthetic gene networks that count. Science 324(5931):1199–1202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Weber W et al (2007) A synthetic time-delay circuit in mammalian cells and mice. Proc Natl Acad Sci USA 104(8):2643–2648

    Article  PubMed  CAS  Google Scholar 

  22. Bonnet J et al (2013) Amplifying genetic logic gates. Science 340(6132):599–603

    Article  PubMed  CAS  Google Scholar 

  23. Hasty J et al (2000) Noise-based switches and amplifiers for gene expression. Proc Natl Acad Sci USA 97(5):2075–2080

    Article  PubMed  CAS  Google Scholar 

  24. Guet CC et al (2002) Combinatorial synthesis of genetic networks. Science 296(5572):1466–1470

    Article  PubMed  CAS  Google Scholar 

  25. Mukherji S, van Oudenaarden A (2009) Synthetic biology: understanding biological design from synthetic circuits. Nat Rev Genet 10(12):859–871

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Schukur L, Fussenegger M (2016) Engineering of synthetic gene circuits for (re-)balancing physiological processes in chronic diseases. Wiley Interdiscip Rev Syst Biol Med 8(5):402–422

    Article  PubMed  CAS  Google Scholar 

  27. Siuti P, Yazbek J, Lu TK (2013) Synthetic circuits integrating logic and memory in living cells. Nat Biotechnol 31(5):448–452

    Article  PubMed  CAS  Google Scholar 

  28. Auslander D et al (2014) A synthetic multifunctional mammalian pH sensor and CO2 transgene-control device. Mol Cell 55(3):397–408

    Article  PubMed  CAS  Google Scholar 

  29. Bowsher CG, Swain PS (2014) Environmental sensing, information transfer, and cellular decision-making. Curr Opin Biotechnol 28C:149–155

    Article  CAS  Google Scholar 

  30. Brenner M, Cho JH, Wong WW (2017) Synthetic biology: sensing with modular receptors. Nat Chem Biol 13(2):131–132

    Article  PubMed  CAS  Google Scholar 

  31. Daringer NM et al (2014) Modular extracellular sensor architecture for engineering mammalian cell-based devices. ACS Synth Biol 3(12):892–902

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Feng J et al (2015) A general strategy to construct small molecule biosensors in eukaryotes. Elife 4:1–23

    Google Scholar 

  33. Garcia JR et al (2009) Microbial nar-GFP cell sensors reveal oxygen limitations in highly agitated and aerated laboratory-scale fermentors. Microb Cell Fact 8:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Looger LL et al (2003) Computational design of receptor and sensor proteins with novel functions. Nature 423(6936):185–190

    Article  PubMed  CAS  Google Scholar 

  35. Saeidi N et al (2011) Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol Syst Biol 7:521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Schwarz KA et al (2017) Rewiring human cellular input-output using modular extracellular sensors. Nat Chem Biol 13(2):202–209

    Article  PubMed  CAS  Google Scholar 

  37. Slomovic S, Collins JJ (2015) DNA sense-and-respond protein modules for mammalian cells. Nat Methods 12(11):1085–1090

    Article  PubMed  CAS  Google Scholar 

  38. Smole A et al (2017) A synthetic mammalian therapeutic gene circuit for sensing and suppressing inflammation. Mol Ther 25(1):102–119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Wu F, Menn DJ, Wang X (2014) Quorum-sensing crosstalk-driven synthetic circuits: from unimodality to trimodality. Chem Biol 21(12):1629–1638

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Youk H, Lim WA (2014) Secreting and sensing the same molecule allows cells to achieve versatile social behaviors. Science 343(6171):1242782

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Auslander S et al (2012) Programmable single-cell mammalian biocomputers. Nature 487(7405):123–127

    Article  PubMed  CAS  Google Scholar 

  42. Callura JM et al (2010) Tracking, tuning, and terminating microbial physiology using synthetic riboregulators. Proc Natl Acad Sci USA 107(36):15898–15903

    Article  PubMed  Google Scholar 

  43. Ellis T, Wang X, Collins JJ (2009) Diversity-based, model-guided construction of synthetic gene networks with predicted functions. Nat Biotechnol 27(5):465–471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Gitzinger M et al (2012) The food additive vanillic acid controls transgene expression in mammalian cells and mice. Nucleic Acids Res 40(5):e37

    Article  PubMed  CAS  Google Scholar 

  45. Guido NJ et al (2006) A bottom-up approach to gene regulation. Nature 439(7078):856–860

    Article  PubMed  CAS  Google Scholar 

  46. Isaacs FJ et al (2004) Engineered riboregulators enable post-transcriptional control of gene expression. Nat Biotechnol 22(7):841–847

    Article  PubMed  CAS  Google Scholar 

  47. Kaern M, Blake WJ, Collins JJ (2003) The engineering of gene regulatory networks. Annu Rev Biomed Eng 5:179–206

    Article  PubMed  CAS  Google Scholar 

  48. Khalil AS, Collins JJ (2010) Synthetic biology: applications come of age. Nat Rev Genet 11(5):367–379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Khalil AS et al (2012) A synthetic biology framework for programming eukaryotic transcription functions. Cell 150(3):647–658

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Litcofsky KD et al (2012) Iterative plug-and-play methodology for constructing and modifying synthetic gene networks. Nat Methods 9(11):1077–1080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Weber W et al (2009) A synthetic mammalian electro-genetic transcription circuit. Nucleic Acids Res 37(4):e33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Paddon CJ et al (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496(7446):528–532

    Article  PubMed  CAS  Google Scholar 

  53. Ro DK et al (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440(7086):940–943

    Article  PubMed  CAS  Google Scholar 

  54. Danino T et al (2015) Programmable probiotics for detection of cancer in urine. Sci Transl Med 7(289):289ra284

    Article  CAS  Google Scholar 

  55. Folcher M, Fussenegger M (2012) Synthetic biology advancing clinical applications. Curr Opin Chem Biol 16(3–4):345–354

    Article  PubMed  CAS  Google Scholar 

  56. Forbes NS (2010) Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer 10(11):785–794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Higashikuni Y, Chen WC, Lu TK (2017) Advancing therapeutic applications of synthetic gene circuits. Curr Opin Biotechnol 47:133–141

    Article  PubMed  CAS  Google Scholar 

  58. Kim T et al (2015) A synthetic erectile optogenetic stimulator enabling blue-light-inducible penile erection. Angew Chem Int Ed Engl 54(20):5933–5938

    Article  PubMed  CAS  Google Scholar 

  59. Kojima R, Aubel D, Fussenegger M (2016) Toward a world of theranostic medication: programming biological sentinel systems for therapeutic intervention. Adv Drug Deliv Rev. 105(Pt A):66–76

    Article  PubMed  CAS  Google Scholar 

  60. Nissim L, Bar-Ziv RH (2010) A tunable dual-promoter integrator for targeting of cancer cells. Mol Syst Biol 6:444

    Article  PubMed  PubMed Central  Google Scholar 

  61. Rossger K, Charpin-El-Hamri G, Fussenegger M (2013) A closed-loop synthetic gene circuit for the treatment of diet-induced obesity in mice. Nat Commun 4:2825

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Xie Z et al (2011) Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science 333(6047):1307–1311

    Article  PubMed  CAS  Google Scholar 

  63. Ye H, Aubel D, Fussenegger M (2013) Synthetic mammalian gene circuits for biomedical applications. Curr Opin Chem Biol 17(6):910–917

    Article  PubMed  CAS  Google Scholar 

  64. Ye H et al (2013) Pharmaceutically controlled designer circuit for the treatment of the metabolic syndrome. Proc Natl Acad Sci USA 110(1):141–146

    Article  PubMed  CAS  Google Scholar 

  65. Ye H et al (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science 332(6037):1565–1568

    Article  PubMed  CAS  Google Scholar 

  66. Ye H, Fussenegger M (2014) Synthetic therapeutic gene circuits in mammalian cells. FEBS Lett 588(15):2537–2544

    Article  PubMed  CAS  Google Scholar 

  67. Auslander S, Fussenegger M (2016) Engineering gene circuits for mammalian cell-based applications. Cold Spring Harb Perspect Biol 8(7):1–17

    Article  CAS  Google Scholar 

  68. Deans TL (2014) Parallel networks: synthetic biology and artificial intelligence. ACM J Emerg Technol Comput Syst (JETC) 11(3):1–22

    Article  Google Scholar 

  69. Baylin SB et al (2001) Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet 10(7):687–692

    Article  PubMed  CAS  Google Scholar 

  70. Golub TR et al (1999) Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286(5439):531–537

    Article  PubMed  CAS  Google Scholar 

  71. van ‘t Veer LJ et al (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871):530–536

    Article  Google Scholar 

  72. Caddeo S, Boffito M, Sartori S (2017) Tissue engineering approaches in the design of healthy and pathological in vitro tissue models. Front Bioeng Biotechnol 5:40

    Article  PubMed  PubMed Central  Google Scholar 

  73. Guvendiren M, Burdick JA (2012) Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat Commun 3:792

    Article  PubMed  CAS  Google Scholar 

  74. van den Broek LJ et al (2014) Human hypertrophic and keloid scar models: principles, limitations and future challenges from a tissue engineering perspective. Exp Dermatol 23(6):382–386

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Anesiadis N et al (2013) Analysis and design of a genetic circuit for dynamic metabolic engineering. ACS Synth Biol 2(8):442–452

    Article  PubMed  CAS  Google Scholar 

  76. Auslander S, Wieland M, Fussenegger M (2012) Smart medication through combination of synthetic biology and cell microencapsulation. Metab Eng 14(3):252–260

    Article  PubMed  CAS  Google Scholar 

  77. Ideker T et al (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292(5518):929–934

    Article  PubMed  CAS  Google Scholar 

  78. Jeong H et al (2000) The large-scale organization of metabolic networks. Nature 407(6804):651–654

    Article  PubMed  CAS  Google Scholar 

  79. Park JH, Lee SY (2008) Towards systems metabolic engineering of microorganisms for amino acid production. Curr Opin Biotechnol 19(5):454–460

    Article  PubMed  CAS  Google Scholar 

  80. Teixeira AP, Fussenegger M (2017) Synthetic biology-inspired therapies for metabolic diseases. Curr Opin Biotechnol 47:59–66

    Article  PubMed  CAS  Google Scholar 

  81. Bloom RJ, Winkler SM, Smolke CD (2015) Synthetic feedback control using an RNAi-based gene-regulatory device. J Biol Eng 9:5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Andrianantoandro E et al (2006) Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2:1–14

    Article  Google Scholar 

  83. Basu S et al (2004) Spatiotemporal control of gene expression with pulse-generating networks. Proc Natl Acad Sci USA 101(17):6355–6360

    Article  PubMed  CAS  Google Scholar 

  84. Chen AY et al (2014) Synthesis and patterning of tunable multiscale materials with engineered cells. Nat Mater 13(5):515–523

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Farzadfard F, Perli SD, Lu TK (2013) Tunable and multifunctional eukaryotic transcription factors based on CRISPR/Cas. ACS Synth Biol 2(10):604–613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Miyamoto T et al (2013) Synthesizing biomolecule-based Boolean logic gates. ACS Synth Biol 2(2):72–82

    Article  PubMed  CAS  Google Scholar 

  87. Purcell O, Lu TK (2014) Synthetic analog and digital circuits for cellular computation and memory. Curr Opin Biotechnol 29C:146–155

    Article  CAS  Google Scholar 

  88. Roquet N, Lu TK (2014) Digital and analog gene circuits for biotechnology. Biotechnol J 9(5):597–608

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Roquet N et al (2016) Synthetic recombinase-based state machines in living cells. Science 353(6297):aad8559

    Article  PubMed  CAS  Google Scholar 

  90. Yang L et al (2014) Permanent genetic memory with > 1-byte capacity. Nat Methods 11(12):1261–1266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Chan G, Mooney DJ (2008) New materials for tissue engineering: towards greater control over the biological response. Trends Biotechnol 26(7):382–392

    Article  PubMed  CAS  Google Scholar 

  92. Deans TL, Elisseeff JH (2009) Mimicking extracellular matrix to direct stem cell differentiation. World Stem Cell Report, Genetics Policy Institute

  93. Deans TL, Elisseeff JH (2009) Stem cells in musculoskeletal engineered tissue. Curr Opin Biotechnol 20(5):537–544

    Article  PubMed  CAS  Google Scholar 

  94. Deans TL, Elisseeff JH (2010) The life of a cell: probing the complex relationships with the world. Cell Stem Cell 6(6):499–501

    Article  PubMed  CAS  Google Scholar 

  95. Cepko CL (1999) The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr Opin Neurobiol 9(1):37–46

    Article  PubMed  CAS  Google Scholar 

  96. Jones DL, Wagers AJ (2008) No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9(1):11–21

    Article  PubMed  CAS  Google Scholar 

  97. Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287(5457):1427–1430

    Article  PubMed  CAS  Google Scholar 

  98. Zon LI (2008) Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453(7193):306–313

    Article  PubMed  CAS  Google Scholar 

  99. Aamodt JM, Grainger DW (2016) Extracellular matrix-based biomaterial scaffolds and the host response. Biomaterials 86:68–82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5(1):1–13

    Article  PubMed  CAS  Google Scholar 

  101. Beachley VZ et al (2015) Tissue matrix arrays for high-throughput screening and systems analysis of cell function. Nat Methods 12(12):1197–1204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Chen FM, Liu X (2016) Advancing biomaterials of human origin for tissue engineering. Prog Polym Sci 53:86–168

    Article  PubMed  CAS  Google Scholar 

  103. Chen XD et al (2007) Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J Bone Miner Res 22(12):1943–1956

    Article  PubMed  CAS  Google Scholar 

  104. Coburn JM et al (2012) Bioinspired nanofibers support chondrogenesis for articular cartilage repair. Proc Natl Acad Sci USA 109(25):10012–10017

    Article  PubMed  Google Scholar 

  105. Crapo PM, Gilbert TW, Badylak SF (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32(12):3233–3243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Flaim CJ, Chien S, Bhatia SN (2005) An extracellular matrix microarray for probing cellular differentiation. Nat Methods 2(2):119–125

    Article  PubMed  CAS  Google Scholar 

  107. Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27(19):3675–3683

    PubMed  CAS  Google Scholar 

  108. Griffith LG (2002) Emerging design principles in biomaterials and scaffolds for tissue engineering. Ann N Y Acad Sci 961:83–95

    Article  PubMed  CAS  Google Scholar 

  109. Griffith LG, Naughton G (2002) Tissue engineering–current challenges and expanding opportunities. Science 295(5557):1009–1014

    Article  PubMed  CAS  Google Scholar 

  110. Hillel AT et al (2011) Photoactivated composite biomaterial for soft tissue restoration in rodents and in humans. Sci Transl Med 3(93):93ra67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Parmar PA et al (2015) Collagen-mimetic peptide-modifiable hydrogels for articular cartilage regeneration. Biomaterials 54:213–225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Porzionato A et al (2015) Decellularized human skeletal muscle as biologic scaffold for reconstructive surgery. Int J Mol Sci 16(7):14808–14831

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Sachlos E, Czernuszka JT (2003) Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur Cell Mater 5:29–39 (discussion 39–40)

    Article  PubMed  CAS  Google Scholar 

  114. Bashor CJ et al (2010) Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu Rev Biophys 39:515–537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Benenson Y (2012) Biomolecular computing systems: principles, progress and potential. Nat Rev Genet 13(7):455–468

    Article  PubMed  CAS  Google Scholar 

  116. Brophy JA, Voigt CA (2014) Principles of genetic circuit design. Nat Methods 11(5):508–520

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Ho P, Chen YY (2017) Mammalian synthetic biology in the age of genome editing and personalized medicine. Curr Opin Chem Biol 40:57–64

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  118. Karlsson M, Weber W (2012) Therapeutic synthetic gene networks. Curr Opin Biotechnol 23(5):703–711

    Article  PubMed  CAS  Google Scholar 

  119. Mathur M, Xiang JS, Smolke CD (2017) Mammalian synthetic biology for studying the cell. J Cell Biol 216(1):73–82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Breithaupt H (2006) The engineer’s approach to biology. EMBO Rep 7(1):21–23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Chin JW (2006) Programming and engineering biological networks. Curr Opin Struct Biol 16(4):551–556

    Article  PubMed  CAS  Google Scholar 

  122. Slusarczyk AL, Lin A, Weiss R (2012) Foundations for the design and implementation of synthetic genetic circuits. Nat Rev Genet 13(6):406–420

    Article  PubMed  CAS  Google Scholar 

  123. Evan GI, Vousden KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411(6835):342–348

    Article  PubMed  CAS  Google Scholar 

  124. Liu HS et al (1998) Lac/Tet dual-inducible system functions in mammalian cell lines. Biotechniques 24(4):624–628, 630–622

  125. Lutz R, Bujard H (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25(6):1203–1210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Bertram R, Hillen W (2008) The application of Tet repressor in prokaryotic gene regulation and expression. Microb Biotechnol 1(1):2–16

    PubMed  CAS  Google Scholar 

  127. Deuschle U, Meyer WK, Thiesen HJ (1995) Tetracycline-reversible silencing of eukaryotic promoters. Mol Cell Biol 15(4):1907–1914

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Aubel D, Fussenegger M (2010) Mammalian synthetic biology–from tools to therapies. BioEssays 32(4):332–345

    Article  PubMed  CAS  Google Scholar 

  129. Auslander S, Auslander D, Fussenegger M (2017) Synthetic biology-the synthesis of biology. Angew Chem Int Ed Engl 56(23):6396–6419

    Article  PubMed  CAS  Google Scholar 

  130. Auslander S, Fussenegger M (2013) From gene switches to mammalian designer cells: present and future prospects. Trends Biotechnol 31(3):155–168

    Article  PubMed  CAS  Google Scholar 

  131. Bacchus W, Aubel D, Fussenegger M (2013) Biomedically relevant circuit-design strategies in mammalian synthetic biology. Mol Syst Biol 9:691

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Black JB, Perez-Pinera P, Gersbach CA (2017) Mammalian synthetic biology: engineering biological systems. Annu Rev Biomed Eng 19:249–277

    Article  PubMed  CAS  Google Scholar 

  133. Cameron DE, Bashor CJ, Collins JJ (2014) A brief history of synthetic biology. Nat Rev Microbiol 12(5):381–390

    Article  PubMed  CAS  Google Scholar 

  134. Collins J (2012) Synthetic biology: bits and pieces come to life. Nature 483(7387):S8–10

    Article  PubMed  CAS  Google Scholar 

  135. Collins JJ et al (2014) Synthetic biology: how best to build a cell. Nature 509(7499):155–157

    Article  PubMed  Google Scholar 

  136. Deans TL, Grainger DW, Fussenegger M (2016) Synthetic biology: innovative approaches for pharmaceutics and drug delivery. Adv Drug Deliv Rev 105(Pt A):1–2

    Article  PubMed  CAS  Google Scholar 

  137. Dobrin A, Saxena P, Fussenegger M (2015) Synthetic biology: applying biological circuits beyond novel therapies. Integr Biol 8:409–430

    Article  Google Scholar 

  138. Greber D, Fussenegger M (2007) Mammalian synthetic biology: engineering of sophisticated gene networks. J Biotechnol 130(4):329–345

    Article  PubMed  CAS  Google Scholar 

  139. Haellman V, Fussenegger M (2016) Synthetic Biology-toward therapeutic solutions. J Mol Biol 428(5):945–962

    Article  PubMed  CAS  Google Scholar 

  140. Kobayashi H et al (2004) Programmable cells: interfacing natural and engineered gene networks. Proc Natl Acad Sci USA 101(22):8414–8419

    Article  PubMed  CAS  Google Scholar 

  141. Lienert F et al (2014) Synthetic biology in mammalian cells: next generation research tools and therapeutics. Nat Rev Mol Cell Biol 15(2):95–107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Lu TK, Khalil AS, Collins JJ (2009) Next-generation synthetic gene networks. Nat Biotechnol 27(12):1139–1150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. MacDonald IC, Deans TL (2016) Tools and applications in synthetic biology. Adv Drug Deliv Rev 105(Pt A):20–34

    Article  PubMed  CAS  Google Scholar 

  144. Ruder WC, Lu T, Collins JJ (2011) Synthetic biology moving into the clinic. Science 333(6047):1248–1252

    Article  PubMed  CAS  Google Scholar 

  145. Way JC et al (2014) Integrating biological redesign: where synthetic biology came from and where it needs to go. Cell 157(1):151–161

    Article  PubMed  CAS  Google Scholar 

  146. Weber W, Fussenegger M (2012) Emerging biomedical applications of synthetic biology. Nat Rev Genet 13(1):21–35

    Article  CAS  Google Scholar 

  147. Guye P et al (2016) Genetically engineering self-organization of human pluripotent stem cells into a liver bud-like tissue using Gata6. Nat Commun 7:10243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Saxena P et al (2016) A programmable synthetic lineage-control network that differentiates human IPSCs into glucose-sensitive insulin-secreting beta-like cells. Nat Commun 7:11247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Gordley RM, Gersbach CA, Barbas CF 3rd (2009) Synthesis of programmable integrases. Proc Natl Acad Sci USA 106(13):5053–5058

    Article  PubMed  Google Scholar 

  150. Daniel R et al (2013) Synthetic analog computation in living cells. Nature 497(7451):619–623

    Article  PubMed  CAS  Google Scholar 

  151. Ajo-Franklin CM et al (2007) Rational design of memory in eukaryotic cells. Genes Dev 21(18):2271–2276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Burrill DR et al (2012) Synthetic memory circuits for tracking human cell fate. Genes Dev 26(13):1486–1497

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Burrill DR, Silver PA (2010) Making cellular memories. Cell 140(1):13–18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Inniss MC, Silver PA (2013) Building synthetic memory. Curr Biol 23(17):R812–R816

    Article  PubMed  CAS  Google Scholar 

  155. Kotula JW et al (2014) Programmable bacteria detect and record an environmental signal in the mammalian gut. Proc Natl Acad Sci USA 111(13):4838–4843

    Article  PubMed  CAS  Google Scholar 

  156. Weinberg BH et al (2017) Large-scale design of robust genetic circuits with multiple inputs and outputs for mammalian cells. Nat Biotechnol 35(5):453–462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  157. Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7):397–405

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  158. Xie M, Haellman V, Fussenegger M (2016) Synthetic biology-application-oriented cell engineering. Curr Opin Biotechnol 40:139–148

    Article  PubMed  CAS  Google Scholar 

  159. Dow LE et al (2015) Inducible in vivo genome editing with CRISPR-Cas9. Nat Biotechnol 33(4):390–394

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  160. Fu Y et al (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32(3):279–284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  161. Gilbert LA et al (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154(2):442–451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  162. Kalhor R, Mali P, Church GM (2017) Rapidly evolving homing CRISPR barcodes. Nat Methods 14(2):195–200

    Article  PubMed  CAS  Google Scholar 

  163. Makarova KS et al (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9(6):467–477

    Article  PubMed  CAS  Google Scholar 

  164. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32(4):347–355

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Zalatan JG et al (2015) Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160(1–2):339–350

    Article  PubMed  CAS  Google Scholar 

  166. Dai WJ et al (2016) CRISPR-Cas9 for in vivo gene therapy: promise and hurdles. Mol Ther Nucleic Acids 5:e349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  167. Maeder ML, Gersbach CA (2016) Genome-editing technologies for gene and cell therapy. Mol Ther 24(3):430–446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Nelson CE et al (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351(6271):403–407

    Article  PubMed  CAS  Google Scholar 

  169. Ousterout DG et al (2015) Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun 6:6244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Perez-Pinera P, Ousterout DG, Gersbach CA (2012) Advances in targeted genome editing. Curr Opin Chem Biol 16(3–4):268–277

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  171. Savic N, Schwank G (2016) Advances in therapeutic CRISPR/Cas9 genome editing. Transl Res 168:15–21

    Article  PubMed  CAS  Google Scholar 

  172. Long C et al (2014) Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science 345(6201):1184–1188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  173. Li HL et al (2015) Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Rep 4(1):143–154

    Article  CAS  Google Scholar 

  174. Duportet X et al (2014) A platform for rapid prototyping of synthetic gene networks in mammalian cells. Nucleic Acids Res 42(21):13440–13451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  175. Inniss MC et al (2017) A novel Bxb1 integrase RMCE system for high fidelity site-specific integration of mAb expression cassette in CHO cells. Biotechnol Bioeng 114(8):1837–1846

    Article  PubMed  CAS  Google Scholar 

  176. Cech TR, Steitz JA (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157(1):77–94

    Article  PubMed  CAS  Google Scholar 

  177. Fire A et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391(6669):806–811

    Article  PubMed  CAS  Google Scholar 

  178. Bloom RJ, Winkler SM, Smolke CD (2014) A quantitative framework for the forward design of synthetic miRNA circuits. Nat Methods 11(11):1147–1153

    Article  PubMed  CAS  Google Scholar 

  179. Pitner RA, Scarpelli AH, Leonard JN (2015) Regulation of bacterial gene expression by protease-alleviated spatial sequestration (PASS). ACS Synth Biol 4(9):966–974

    Article  PubMed  CAS  Google Scholar 

  180. Hartfield RM et al (2017) Multiplexing engineered receptors for multiparametric evaluation of environmental ligands. ACS Synth Biol 6(11):2042–2055

    Article  PubMed  CAS  Google Scholar 

  181. Irvine DJ (2016) A receptor for all occasions. Cell 164(4):599–600

    Article  PubMed  CAS  Google Scholar 

  182. Morsut L et al (2016) Engineering customized cell sensing and response behaviors using synthetic notch receptors. Cell 164(4):780–791

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  183. Roybal KT et al (2016) Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell 164(4):770–779

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  184. Vonderheide RH, June CH (2014) Engineering T cells for cancer: our synthetic future. Immunol Rev 257(1):7–13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  185. Engler AJ et al (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689

    Article  PubMed  CAS  Google Scholar 

  186. Fu J et al (2010) Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 7(9):733–736

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  187. Guilak F et al (2009) Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5(1):17–26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Legant WR et al (2010) Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat Methods 7(12):969–971

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  189. McBeath R et al (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6(4):483–495

    Article  PubMed  CAS  Google Scholar 

  190. Trappmann B et al (2012) Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 11(7):642–649

    Article  PubMed  CAS  Google Scholar 

  191. Yang C et al (2014) Mechanical memory and dosing influence stem cell fate. Nat Mater 13(6):645–652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  192. Crowder SW et al (2016) Material cues as potent regulators of epigenetics and stem cell function. Cell Stem Cell 18(1):39–52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  193. Murphy WL, McDevitt TC, Engler AJ (2014) Materials as stem cell regulators. Nat Mater 13(6):547–557

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  194. Vining KH, Mooney DJ (2017) Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol 18(12):728–742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  195. Watt FM, Huck WT (2013) Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 14(8):467–473

    Article  PubMed  CAS  Google Scholar 

  196. Madl CM et al (2017) Maintenance of neural progenitor cell stemness in 3D hydrogels requires matrix remodelling. Nat Mater 16(12):1233–1242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  197. Huber MC et al (2014) Introducing a combinatorial DNA-toolbox platform constituting defined protein-based biohybrid-materials. Biomaterials 35(31):8767–8779

    Article  PubMed  CAS  Google Scholar 

  198. Winnacker M (2017) Recent advances in the synthesis of functional materials by engineered and recombinant living cells. Soft Matter 13(38):6672–6677

    Article  PubMed  CAS  Google Scholar 

  199. Abdeen AA, Saha K (2017) Manufacturing cell therapies using engineered biomaterials. Trends Biotechnol 35(10):971–982

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  200. Hiew VV, Simat SFB, Teoh PL (2018) The advancement of biomaterials in regulating stem cell fate. Stem Cell Rev 14(1):43–57

    Article  PubMed  CAS  Google Scholar 

  201. Liu Z et al (2018) Looking into the future: toward advanced 3d biomaterials for stem-cell-based regenerative medicine. Adv Mater 2:1–20

    Google Scholar 

  202. Nuttelman CR, Tripodi MC, Anseth KS (2005) Synthetic hydrogel niches that promote hMSC viability. Matrix Biol 24(3):208–218

    Article  PubMed  CAS  Google Scholar 

  203. Parisi-Amon A et al (2017) Protein-nanoparticle hydrogels that self-assemble in response to peptide-based molecular recognition. ACS Biomater Sci Eng 3(5):750–756

    Article  CAS  Google Scholar 

  204. Sawkins MJ et al (2013) Hydrogels derived from demineralized and decellularized bone extracellular matrix. Acta Biomater 9(8):7865–7873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  205. Sun F et al (2014) Synthesis of bioactive protein hydrogels by genetically encoded SpyTag-SpyCatcher chemistry. Proc Natl Acad Sci USA 111(31):11269–11274

    Article  PubMed  CAS  Google Scholar 

  206. Tibbitt MW, Anseth KS (2009) Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 103(4):655–663

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  207. Chilkoti A, Christensen T, MacKay JA (2006) Stimulus responsive elastin biopolymers: applications in medicine and biotechnology. Curr Opin Chem Biol 10(6):652–657

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  208. MacEwan SR, Chilkoti A (2010) Elastin-like polypeptides: biomedical applications of tunable biopolymers. Biopolymers 94(1):60–77

    Article  PubMed  CAS  Google Scholar 

  209. MacEwan SR, Chilkoti A (2014) Applications of elastin-like polypeptides in drug delivery. J Control Release 190:314–330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  210. Nettles DL, Chilkoti A, Setton LA (2010) Applications of elastin-like polypeptides in tissue engineering. Adv Drug Deliv Rev 62(15):1479–1485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  211. Roberts S, Dzuricky M, Chilkoti A (2015) Elastin-like polypeptides as models of intrinsically disordered proteins. FEBS Lett 589(19 Pt A):2477–2486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  212. Stayton PS et al (1995) Control of protein-ligand recognition using a stimuli-responsive polymer. Nature 378(6556):472–474

    Article  PubMed  CAS  Google Scholar 

  213. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697–715

    Article  PubMed  CAS  Google Scholar 

  214. Burdick JA, Anseth KS (2002) Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials 23(22):4315–4323

    Article  PubMed  CAS  Google Scholar 

  215. Liu JC, Heilshorn SC, Tirrell DA (2004) Comparative cell response to artificial extracellular matrix proteins containing the RGD and CS5 cell-binding domains. Biomacromol 5(2):497–504

    Article  CAS  Google Scholar 

  216. Ruoslahti E, Pierschbacher MD (1987) New perspectives in cell adhesion: RGD and integrins. Science 238(4826):491–497

    Article  PubMed  CAS  Google Scholar 

  217. Salinas CN, Anseth KS (2008) The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities. Biomaterials 29(15):2370–2377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  218. Hersel U, Dahmen C, Kessler H (2003) RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24(24):4385–4415

    Article  PubMed  CAS  Google Scholar 

  219. Morrison CJ et al (2009) Matrix metalloproteinase proteomics: substrates, targets, and therapy. Curr Opin Cell Biol 21(5):645–653

    Article  PubMed  CAS  Google Scholar 

  220. Parmar PA et al (2017) Enhanced articular cartilage by human mesenchymal stem cells in enzymatically mediated transiently RGDS-functionalized collagen-mimetic hydrogels. Acta Biomater 51:75–88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  221. Macias MJ, Wiesner S, Sudol M (2002) WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett 513(1):30–37

    Article  PubMed  CAS  Google Scholar 

  222. Foo CTWP et al (2009) Two-component protein-engineered physical hydrogels for cell encapsulation. Proc Natl Acad Sci USA 106(52):22067–22072

    Article  Google Scholar 

  223. Lupas A (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21(10):375–382

    Article  PubMed  CAS  Google Scholar 

  224. McAlinden A et al (2003) Alpha-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily. J Biol Chem 278(43):42200–42207

    Article  PubMed  CAS  Google Scholar 

  225. Armony G et al (2016) Cross-linking reveals laminin coiled-coil architecture. Proc Natl Acad Sci USA 113(47):13384–13389

    Article  PubMed  CAS  Google Scholar 

  226. Dooling LJ, Tirrell DA (2016) Engineering the dynamic properties of protein networks through sequence variation. ACS Cent Sci 2(11):812–819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  227. Danmark S, Aronsson C, Aili D (2016) Tailoring supramolecular peptide-poly(ethylene glycol) hydrogels by coiled coil self-assembly and self-sorting. Biomacromol 17(6):2260–2267

    Article  CAS  Google Scholar 

  228. Tropsha A et al (1991) Do interhelical side chain-backbone hydrogen bonds participate in formation of leucine zipper coiled coils? Proc Natl Acad Sci USA 88(21):9488–9492

    Article  PubMed  CAS  Google Scholar 

  229. Addi C et al (2017) A highly versatile adaptor protein for the tethering of growth factors to gelatin-based biomaterials. Acta Biomater 50:198–206

    Article  PubMed  CAS  Google Scholar 

  230. Reddington SC, Howarth M (2015) Secrets of a covalent interaction for biomaterials and biotechnology: SpyTag and SpyCatcher. Curr Opin Chem Biol 29:94–99

    Article  PubMed  CAS  Google Scholar 

  231. Zakeri B et al (2012) Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc Natl Acad Sci USA 109(12):E690–E697

    Article  PubMed  Google Scholar 

  232. Gao X et al (2016) Engineering protein hydrogels using SpyCatcher-SpyTag chemistry. Biomacromol 17(9):2812–2819

    Article  CAS  Google Scholar 

  233. Schoene C et al (2014) SpyTag/SpyCatcher cyclization confers resilience to boiling on a mesophilic enzyme. Angew Chem Int Ed Engl 53(24):6101–6104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  234. Liu Z et al (2014) A novel method for synthetic vaccine construction based on protein assembly. Sci Rep 4:7266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  235. Tan LL, Hoon SS, Wong FT (2016) Kinetic controlled tag-catcher interactions for directed covalent protein assembly. PLoS One 11(10):e0165074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  236. Alam MK et al (2017) Synthetic modular antibody construction by using the SpyTag/SpyCatcher protein-ligase system. ChemBioChem 18(22):2217–2221

    Article  PubMed  CAS  Google Scholar 

  237. Yumura K et al (2017) Use of SpyTag/SpyCatcher to construct bispecific antibodies that target two epitopes of a single antigen. J Biochem 162(3):203–210

    Article  PubMed  CAS  Google Scholar 

  238. Brune KD et al (2016) Plug-and-display: decoration of virus-Like particles via isopeptide bonds for modular immunization. Sci Rep 6:19234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  239. Schloss AC et al (2016) Fabrication of modularly functionalizable microcapsules using protein-based technologies. ACS Biomater Sci Eng 2(11):1856–1861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  240. Bedbrook CN et al (2015) Genetically encoded spy peptide fusion system to detect plasma membrane-localized proteins in vivo. Chem Biol 22(8):1108–1121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  241. Deans TL et al (2012) Regulating synthetic gene networks in 3D materials. Proc Natl Acad Sci USA 109(38):15217–15222

    Article  PubMed  Google Scholar 

  242. Singh A, Deans TL, Elisseeff JH (2013) Photomodulation of cellular gene expression in hydrogels. Acs Macro Lett 2(3):269–272

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge the funding from the University of Utah startup funds, a University of Utah SEED Grant [10045314], the National Science Foundation CAREER program [CBET-1554017], the Office of Naval Research Young Investigator Program [N00014-16-1-3012], and the National Institutes of Health Trailblazer Award [1R21EB025413-01].

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  1. Department of Bioengineering, University of Utah, Salt Lake City, UT, 84112, USA

    Mitchell S. Weisenberger & Tara L. Deans

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Weisenberger, M.S., Deans, T.L. Bottom-up approaches in synthetic biology and biomaterials for tissue engineering applications. J Ind Microbiol Biotechnol 45, 599–614 (2018). https://doi.org/10.1007/s10295-018-2027-3

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