Using synthetic biology to explore principles of development

Development (Cambridge)

Volumn 144, Issue 7, 2017, Pages 1146-1158

  Davies, Jamie ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Differentiation; Morphogenesis; Pattern formation; Synthetic biology; Synthetic morphology; Validation

Indexed keywords

GREEN FLUORESCENT PROTEIN;

CELL DIFFERENTIATION; CLINICAL FEATURE; DEVELOPMENTAL BIOLOGY; DROSOPHILA; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; MORPHOGENESIS; NONHUMAN; OPEN READING FRAME; PATTERNING; REVIEW; SYNTHETIC BIOLOGY; ANIMAL; EVOLUTION; HUMAN; PROCEDURES;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; CELL DIFFERENTIATION; EMBRYONIC DEVELOPMENT; HUMANS; MORPHOGENESIS; SYNTHETIC BIOLOGY;

EID: 85016413087     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.144196     Document Type: Review

References (99)

1. Akam, M. (1987). The molecular basis for metameric pattern in the Drosophila embryo. Development 101, 1-22.
2. Ang, J., Harris, E., Hussey, B. J., Kil, R. and McMillen, D. R. (2013). Tuning response curves for synthetic biology. ACS Synth. Biol. 2, 547-567.
3. Angeli, D., Ferrell, J. E.Jr and Sontag, E. D. (2004). Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems. Proc. Natl. Acad. Sci. USA 101, 1822-1827.
4. Ashe, H. L. and Briscoe, J. (2006). The interpretation of morphogen gradients. Development 133, 385-394.
5. Asimov, I. (1979). A Short History of Chemistry. New York, USA: Preager. ISBN 978-0313207693.
6. Barad, O., Hornstein, E. and Barkai, N. (2011). Robust selection of sensory organ precursors by the Notch-Delta pathway. Curr. Opin. Cell Biol. 23, 663-667.
7. Basu, S., Gerchman, Y., Collins, C. H., Arnold, F. H. and Weiss, R. (2005). A synthetic multicellular system for programmed pattern formation. Nature 434, 1130-1134.
8. Beal, J. (2015). Signal-to-noise ratio measures efficacy of biological computing devices and circuits. Front. Bioeng. Biotechnol. 3, 93.
9. Blagodatskia, A., Sergeevb, A., Kryuchkova, M., Lopatinad, Y. and Katanaevc, V. L. (2015). Diverse set of Turing nanopatterns coat corneae across insect lineages. Proc. Natl. Acad. Sci. USA 112, 10750-10755.
10. Blenkiron, M., Arvind, D. K. and Davies, J. A. (2007). Design of an irreversible DNA memory element. Nat. Comput. 6, 403-411.
11. Briscoe, J. and Ericson, J. (2001). Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11, 43-49.
12. Briscoe, J. and Small, S. (2015). Morphogen rules: design principles of gradientmediated embryo patterning. Development 142, 3996-4009.
13. Cachat, E., Liu, W., Hohenstein, P. and Davies, J. A. (2014). A library of mammalian effector modules for synthetic morphology. J. Biol. Eng. 8, 26.
14. Cachat, E., Liu, W., Martin, K. C., Yuan, X., Yin, H., Hohenstein, P. and Davies, J. A. (2016). 2-and 3-dimensional synthetic large-scale de novo patterning by mammalian cells through phase separation. Sci. Rep. 6, 20664.
15. Campos-Ortega, J. A. (1995). Genetic mechanisms of early neurogenesis in Drosophila melanogaster. Mol. Neurobiol. 10, 75-89.
16. Carbonell-Ballestero, M., Garcia-Ramallo, E., Montañez, R., Rodriguez-Caso, C. and Macía, J. (2016). Dealing with the genetic load in bacterial synthetic biology circuits: convergences with the Ohm’s law. Nucleic Acids Res. 44, 496-507.
17. Cotterell, J. and Sharpe, J. (2010). An atlas of gene regulatory networks reveals multiple three-gene mechanisms for interpreting morphogen gradients. Mol. Syst. Biol. 6, 425.
18. Crick, F. (1970). Diffusion in embryogenesis. Nature 225, 420-422.
19. Dalcq, A. (1938). Form and Causality in Early Development. Cambridge: Cambridge Univ. Press.
20. Danino, T., Mondragón-Palomino, O., Tsimring, L. and Hasty, J. (2010). A synchronized quorum of genetic clocks. Nature 463, 326-330.
21. Davies, J. A. (2008). Synthetic morphology: prospects for engineered, selfconstructing anatomies. J. Anat. 212, 707-719.
22. Davies, J. A. (2013). Mechanisms of Morphogenesis. London: Academic Press.
23. Davies, J. A. and Cachat, E. (2016). Synthetic biology meets tissue engineering. Biochem. Soc. Trans. 44, 696-701.
24. d’Espaux, L., Mendez-Perez, D., Li, R. and Keasling, J. D. (2015). Synthetic biology for microbial production of lipid-based biofuels. Curr. Opin. Chem. Biol. 29, 58-65.
25. Dessaud, E., Yang, L. L., Hill, K., Cox, B., Ulloa, F., Ribeiro, A., Mynett, A., Novitch, B. G. and Briscoe, J. (2007). Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450, 717-720.
26. Driever, W., Thoma, G. and Nüsslein-Volhard, C. (1989). Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen. Nature 340, 363-367.
27. Economou, A. D., Ohazama, A., Porntaveetus, T., Sharpe, P. T., Kondo, S., Basson, M. A., Gritli-Linde, A., Cobourne, M. T. and Green, J. B. A. (2012). Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 44, 348-351.
28. Elowitz, M. B. and Leibler, S. (2000). A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338.
29. Ferrell, J. E.Jr and Machleder, E. M. (1998). The biochemical basis of an all-ornone cell fate switch in Xenopus oocytes. Science 280, 895-898.
30. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
31. Gao, X. J. and Elowitz, M. B. (2016). Synthetic biology: precision timing in a cell. Nature 538, 462-463.
32. Gierer, A. and Meinhardt, H. (1972). A theory of biological pattern formation. Kybernetik 12, 30-39.
33. Greber, D. and Fussenegger, M. (2010). An engineered mammalian band-pass network. Nucleic Acids Res. 38, e174.
34. Grosskopf, T. and Soyer, O. S. (2014). Synthetic microbial communities. Curr. Opin. Microbiol. 18, 72-77.
35. Gurdon, J. B., Mitchell, A. and Mahony, D. (1995). Direct and continuous assessment by cells of their position in a morphogen gradient. Nature 376, 520-521.
36. Hays, S. G., Patrick, W. G., Ziesack, M., Oxman, N. and Silver, P. A. (2015). Better together: engineering and application of microbial symbioses. Curr. Opin. Biotechnol. 36, 40-49.
37. Huang, S., Guo, Y.-P., May, G. and Enver, T. (2007). Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 305, 695-713.
38. Hurley, J. M., Loros, J. J. and Dunlap, J. C. (2016). Circadian oscillators: around the transcription-translation feedback loop and on to output. Trends Biochem. Sci. 41, 834-846.
39. Hussain, F., Gupta, C., Hirning, A. J., Ott, W., Matthews, K. S., Josic, K. and Bennett, M. R. (2014). Engineered temperature compensation in a synthetic genetic clock. Proc. Natl. Acad. Sci. USA 111, 972-927.
40. Hutmacher, D. W., Holzapfel, B. M., De-Juan-Pardo, E. M., Pereira, B. A., Ellem, S. J., Loessner, D. and Risbridger, G. P. (2015). Convergence of regenerative medicine and synthetic biology to develop standardized and validated models of human diseases with clinical relevance. Curr. Opin. Biotechnol. 35, 127-132.
41. Johnson, A. D., Poteete, A. R., Lauer, G., Sauer, R. T., Ackers, G. K. and Ptashne, M. (1981). lambda Repressor and cro–components of an efficient molecular switch. Nature 294, 217-223.
42. Kauffman, S. A. (1993). The Origins of Order. Oxford, UK: Oxford University Press.
43. Kramer, B. P. and Fussenegger, M. (2005). Hysteresis in a synthetic mammalian gene network. Proc. Natl. Acad. Sci. USA 102, 9517-9522.
44. Kramer, B. P., Viretta, A. U., Daoud-El-Baba, M., Aubel, D., Weber, W. and Fussenegger, M. (2004). An engineered epigenetic transgene switch in mammalian cells. Nat. Biotechnol. 22, 867-870.
45. Kuchen, E. E., Fox, S., de Reuille, P. B., Kennaway, R., Bensmihen, S., Avondo, J., Calder, G. M., Southam, P., Robinson, S., Bangham, A. et al. (2012). Generation of leaf shape through early patterns of growth and tissue polarity. Science 335, 1092-1096
46. Kutejova, E., Briscoe, J. and Kicheva, A. (2009). Temporal dynamics of patterning by morphogen gradients. Curr. Opin. Genet. Dev. 19, 315-322.
47. Kwok, R. (2010). Five hard truths for synthetic biology. Nature 463, 288-290.
48. Leduc, S. (1912). La Biologie Synthétique, Étude de Biophysique. Paris: Poinat.
49. Lewis, J. (2003). Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr. Biol. 19, 1398-1408.
50. Liu, C., Fu, X., Liu, L., Ren, X., Chau, C. K., Li, S., Xiang, L., Zeng, H., Chen, G., Tang, L.-H. et al. (2011). Sequential establishment of stripe patterns in an expanding cell population. Science 334, 238-241.
51. MacQuarrie, K. L., Fong, A. P., Morse, R. H. and Tapscott, S. J. (2011). Genomewide transcription factor binding: beyond direct target regulation. Trends Genet. 27, 141-148.
52. Mandelbrot, B. (2012). The Fractalist: Memoir of a Scientific Maverick. New York: Pantheon.
53. Matsuda, M., Koga, M., Woltjen, K., Nishida, E. and Ebisuya, M. (2015). Synthetic lateral inhibition governs cell-type bifurcation with robust ratios. Nat. Commun. 6, 6195.
54. Monier, B., Pélissier-Monier, A. and Sanson, B. (2011). Establishment and maintenance of compartmental boundaries: role of contractile actomyosin barriers. Cell. Mol. Life Sci. 68, 1897-1910.
55. Monk, N. A. M. (2003). Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays. Curr. Biol. 13, 1409-1413.
56. Morsut, L., Roybal, K. T., Xiong, X., Gordley, R. M., Coyle, S. M., Thomson, M. and Lim, W. A. (2016). Engineering customized cell sensing and response behaviors using synthetic notch receptors. Cell 164, 780-791.
57. Müller, P., Rogers, K. W., Jordan, B. M., Lee, J. S., Robson, D., Ramanathan, S. and Schier, A. F. (2012). Differential diffusivity of Nodal and Lefty underlies a reaction-diffusion patterning system. Science 336, 721-724.
58. Niederholtmeyer, H., Sun, Z. Z., Hori, Y., Yeung, E., Verpoorte, A., Murray, R. M. and Maerkl, S. J. (2015). Rapid cell-free forward engineering of novel genetic ring oscillators. Elife 4, e09771.
59. Oates, A. C., Morelli, L. G. and Ares, S. (2012). Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 139, 625-639.
60. Park, J. S., Rhau, B., Hermann, A., McNally, K. A., Zhou, C., Gong, D., Weiner, O. D., Conklin, B. R., Onuffer, J. and Lim, W. A. (2014). Synthetic control of mammalian-cell motility by engineering chemotaxis to an orthogonal bioinert chemical signal. Proc. Natl. Acad. Sci. USA 111, 5896-5901.
61. Pascalie, J., Potier, M., Kowaliw, T., Giavitto, J.-L., Michel, O., Spicher, A. and Doursat, R. (2016). Developmental design of synthetic bacterial architectures by morphogenetic engineering. ACS Synth. Biol. 5, 842-861.
62. Pasotti, L., Politi, N., Zucca, S., Cusella De Angelis, M. G. and Magni, P. (2012). Bottom-up engineering of biological systems through standard bricks: a modularity study on basic parts and devices. PLoS ONE 7, e39407.
63. Piccolinoa, M. (1997). Luigi Galvani and animal electricity: two centuries after the foundation of electrophysiology. Trends Neurosci. 20, 443-448.
64. Potvin-Trottier, L., Lord, N. D., Vinnicombe, G. and Paulsson, J. (2016). Synchronous long-term oscillations in a synthetic gene circuit. Nature 538, 514-517.
65. Raff, M. C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
66. Raspopovic, J., Marcon, L., Russo, L. and Sharpe, J. (2014). Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 345, 566-570.
67. Rekhi, R. and Qutub, A. A. (2013). Systems approaches for synthetic biology: a pathway toward mammalian design. Front. Physiol. 4, 285.
68. Richmond, D. L. and Oates, A. C. (2012). The segmentation clock: inherited trait or universal design principle? Curr. Opin. Genet. Dev. 22, 600-606.
69. Ro, D.-K., Paradise, E. M., Ouellet, M., Fisher, K. J., Newman, K. L., Ndungu, J. M., Ho, K. A., Eachus, R. A., Ham, T. S., Kirby, J. et al. (2006). Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440, 940-943.
70. Ruder, W. C., Lu, T. and Collins, J. J. (2011). Synthetic biology moving into the clinic. Science 333, 1248-1252.
71. Sandercock, P. (2012). Negative results: why do they need to be published? Int. J. Stroke 7, 32-33.
72. Shimojo, H. and Kageyama, R. (2016). Oscillatory control of Delta-like1 in somitogenesis and neurogenesis: a unified model for different oscillatory dynamics. Semin. Cell Dev. Biol. 49, 76-82.
73. Shou, W., Ram, S. and Vilar, J. M. G. (2007). Synthetic cooperation in engineered yeast populations. Proc. Natl. Acad. Sci. USA 104, 1877-1882.
74. Sick, S., Reinker, S., Timmer, J. and Schlake, T. (2006). WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314, 1447-1450.
75. Sohka, T., Heins, R. A., Phelan, R. M., Greisler, J. M., Townsend, C. A. and Ostermeier, M. (2009). An externally tunable bacterial band-pass filter. Proc. Natl. Acad. Sci. USA 106, 10135-10140.
76. Solnica-Krezel, L. and Sepich, D. S. (2012). Gastrulation: making and shaping germ layers. Annu. Rev. Cell Dev. Biol. 28, 687-717.
77. Steinberg, M. S. (1970). Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J. Exp. Zool. 173, 395-433.
78. Stricker, J., Cookson, S., Bennett, M. R., Mather, W. H., Tsimring, L. S. and Hasty, J. (2008). A fast, robust and tunable synthetic gene oscillator. Nature 456, 516-519.
79. Swinburne, I. A., Miguez, D. G., Landgraf, D. and Silver, P. A. (2008). Intron length increases oscillatory periods of gene expression in animal cells. Genes Dev. 22, 2342-2346.
80. Teague, B. P., Guye, P., and Weiss, R. (2016). Synthetic morphogenesis. Cold Spring Harb. Perspect Biol. a023929.
81. Thompson, D. W. (1917). On Growth and form. Cambridge, UK: Cambridge University Press.
82. Todhunter, M. E., Jee, N. Y., Hughes, A. J., Coyle, M. C., Cerchiari, A., Farlow, J., Garbe, J. C., LaBarge, M. A., Desai, T. A. and Gartner, Z. J. (2015). Programmed synthesis of three-dimensional tissues. Nat. Methods 12, 975-981.
83. Traube, M. (1866). Über homogene Membranen und deren Einfluβ auf die Endosmose. Vorläufige Mitteilungen. Zentralblatt f. d. med. Wissenschaften Nr. 7 u. 8.
84. Turing, A. M. (1952). The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. 237, 37-72.
85. Unbekandt, M. and Davies, J. A. (2010). Dissociation of embryonic kidneys followed by reaggregation allows the formation of renal tissues. Kidney Int. 77, 407-416.
86. Uriu, K. (2016). Genetic oscillators in development. Dev. Growth Differ. 58, 16-30.
87. van Assen, M. A. L. M., van Aert, R. C. M., Nuijten, M. B. and Wicherts, J. M. (2014). Why publishing everything is more effective than selective publishing of statistically significant results. PLoS ONE 9, e84896.
88. Varenne, F., Chaigneau, P., Petitot, J. and Doursat, R. (2015). Programming the emergence in morphogenetically architected complex systems. Acta Biotheor. 63, 295-308.
89. Waddington, C. H. (1957). The Strategy of the Genes. London, UK: George Allen and Unwin.
90. Webster, D. P., TerAvest, M. A., Doud, D. F. R., Chakravorty, A., Holmes, E. C., Radens, C. M., Sureka, S., Gralnick, J. A. and Angenent, L. T. (2014). An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system. Biosens. Bioelectron. 62, 320-324.
91. Weintraub, P. G. (2016). The importance of publishing negative results. J. Insect. Sci. 23, 16.
92. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47.
93. Xiong, W. and Ferrell, J. E.Jr (2003). A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision. Nature 426, 460-465.
94. Yabe, T. and Takada, S. (2016). Molecular mechanism for cyclic generation of somites: lessons from mice and zebrafish. Dev. Growth Differ. 58, 31-42.
95. Yamanaka, H. and Kondo, S. (2014). In vitro analysis suggests that difference in cell movement during direct interaction can generate various pigment patterns in vivo. Proc. Natl. Acad. Sci. USA 111, 1867-1872.
96. Yang, Y., Drossopoulou, G., Chuang, P. T., Duprez, D., Marti, E., Bumcrot, D., Vargesson, N., Clarke, J., Niswander, L., McMahon, A. et al. (1997). Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development 124, 4393-4404.
97. Zhang, C.-C., Laurent, S., Sakr, S., Peng, L. and Bédu, S. (2006). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol. Microbiol. 9, 367-375.
98. Zhao, X., Cho, H., Yu, R. T., Atkins, A. R., Downes, M. and Evans, R. M. (2014). Nuclear receptors rock around the clock. EMBO Rep. 15, 518-528.
99. Zhong, W., Feder, J. N., Jiang, M.-M., Jan, L. Y. and Jan, Y. N. (1996). Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43-53.