Synthetic biology: a new approach to study biological pattern formation

Abstract

The principles and molecular mechanisms underlying biological pattern formation are difficult to elucidate in most cases due to the overwhelming physiologic complexity associated with the natural context. The understanding of a particular mechanism, not to speak of underlying universal principles, is difficult due to the diversity and uncertainty of the biological systems. Although current genetic and biochemical approaches have greatly advanced our understanding of pattern formation, the progress mainly relies on experimental phenotypes obtained from time-consuming studies of gain or loss of function mutants. It is prevailingly considered that synthetic biology will come to the application age, but more importantly synthetic biology can be used to understand the life. Using periodic stripe pattern formation as a paradigm, we discuss how to apply synthetic biology in understanding biological pattern formation and hereafter foster the applications like tissue engineering.

Graphical abstract

References

[1] Wolpert, L. (1969) Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol., 25, 1−47

[2] Danino, T., Mondragón-Palomino, O., Tsimring, L. and Hasty, J. (2010) A synchronized quorum of genetic clocks. Nature, 463, 326−330

[3] Tabor, J. J., Salis, H. M., Simpson, Z. B., Chevalier, A. A., Levskaya, A., Marcotte, E. M., Voigt, C. A. and Ellington, A. D. (2009) A synthetic genetic edge detection program. Cell, 137, 1272−1281

[4] Levskaya, A., Chevalier, A. A., Tabor, J. J., Simpson, Z. B., Lavery, L. A., Levy, M., Davidson, E. A., Scouras, A., Ellington, A. D., Marcotte, E. M., (2005) Synthetic biology: engineering Escherichia coli to see light. Nature, 438, 441−442

[5] 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

[6] You, L., Cox, R. S. 3rd, Weiss, R. and Arnold, F. H. (2004) Programmed population control by cell-cell communication and regulated killing. Nature, 428, 868−871

[7] Elowitz, M. B. and Leibler, S. (2000) A synthetic oscillatory network of transcriptional regulators. Nature, 403, 335−338

[8] Elowitz, M. and Lim, W. A. (2010) Build life to understand it. Nature, 468, 889−890

[9] Mukherji, S. and van Oudenaarden, A. (2009) Synthetic biology: understanding biological design from synthetic circuits. Nat. Rev. Genet., 10, 859−871

[10] Held, L. I. (1992) Models for embryonic periodicity. Basel; New York: Karger. viii, 119 p. p.

[11] Nüsslein-Volhard, C. and Wieschaus, E. (1980) Mutations affecting segment number and polarity in Drosophila. Nature, 287, 795−801

[12] Lawrence, P. A. (1992) The making of a fly: the genetics of animal design. Oxford: Blackwell Scientific Publications. xiii, 228 p. p.

[13] Peel, A. D., Chipman, A. D. and Akam, M. (2005) Arthropod segmentation: beyond the Drosophila paradigm. Nat. Rev. Genet., 6, 905−916

[14] Dequéant, M. L. and Pourquié O. (2008) Segmental patterning of the vertebrate embryonic axis. Nat. Rev. Genet., 9, 370−382

[15] Schnell, S., Maini, P. K., McInerney, D., Gavaghan, D. J. and Houston, P. (2002) Models for pattern formation in somitogenesis: a marriage of cellular and molecular biology. C. R. Biol., 325, 179−189

[16] Sadler, T. W. and Langman, J. (2000) Langman's medical embryology. Philadelphia: Lippincott Williams & Wilkins. x, 504 p. p.

[17] Dubrulle, J., McGrew, M. J. and Pourquié O. (2001) FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell, 106, 219−232

[18] Pourquié O. (2003) The segmentation clock: converting embryonic time into spatial pattern. Science, 301, 328−330

[19] Finney, M. and Ruvkun, G. (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell, 63, 895−905

[20] McKearin, D. M. and Spradling, A. C. (1990) bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev., 4, 2242−2251

[21] Sussex, I. M. (1989) Developmental programming of the shoot meristem. Cell, 56, 225−229

[22] Murray, J. D. (2002) Mathematical biology. New York: Springer.

[23] Cooke, J. (1975) Control of somite number during morphogenesis of a vertebrate, Xenopus laevis. Nature, 254, 196−199

[24] Alon, U. (2007) An introduction to systems biology: design principles of biological circuits. Boca Raton, FL: Chapman & Hall/CRC. xvi, 301 p., [304] p. of plates p.

[25] May, R. M. (1976) Simple mathematical models with very complicated dynamics. Nature, 261, 459−467

[26] Wolpert, L. (1971) Positional information and pattern formation. Curr. Top. Dev. Biol., 6, 183−224

[27] Kondo, S. and Miura, T. (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science, 329, 1616−1620

[28] Hodges, A. (1983) Alan Turing: the enigma. New York: Simon and Schuster. 587 p p.

[29] Turing, A. M. (1990) The chemical basis of morphogenesis. 1953. Bull. Math. Biol., 52, 153−197, discussion 119−152 PMID:2185858.

[30] Fitzhugh, R. (1961) Impulses and Physiological States in Theoretical Models of Nerve Membrane. Biophys. J., 1, 445−466

[31] Maini, P. K., Myerscough, M. R., Winters, K. H. and Murray, J. D. (1991) Bifurcating spatially heterogeneous solutions in a chemotaxis model for biological pattern generation. Bull. Math. Biol., 53, 701−719

[32] Swindale, N. V. (1980) A model for the formation of ocular dominance stripes. Proc. R. Soc. Lond., B, Biol. Sci., 208, 243−264

[33] Murray, J. D., Oster, G. F. and Harris, A. K. (1983) A mechanical model for mesenchymal morphogenesis. J Math Biol, 17, 125−129

[34] Murray, J. D. (2002) Mathematical biology. II, Spatial models and biomedical applications. New York: Springer. xxv, 811 p. p.

[35] Meinhardt, H. and Gierer, A. (1974) Applications of a theory of biological pattern formation based on lateral inhibition. J. Cell. Sci., 15, 321−346

[36] 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

[37] Cates, M. E., Marenduzzo, D., Pagonabarraga, I. and Tailleur, J. (2010) Arrested phase separation in reproducing bacteria creates a generic route to pattern formation. Proc. Natl. Acad. Sci. U.S.A., 107, 11715−11720

[38] Fu, X., Tang, L. H., Liu, C., Huang, J. D., Hwa, T. and Lenz, P. (2012) Stripe formation in bacterial systems with density-suppressed motility. Phys. Rev. Lett., 108, 198102

[39] Liu, C., Fu, X., Liu, L., Ren, X., Chau, C. K., Li, S., Xiang, L., Zeng, H., Chen, G., Tang, L. H., (2011) Sequential establishment of stripe patterns in an expanding cell population. Science, 334, 238−241

[40] Cooke, J. and Zeeman, E. C. (1976) A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol., 58, 455−476

[41] Khalil, A. S. and Collins, J. J. (2010) Synthetic biology: applications come of age. Nat. Rev. Genet., 11, 367−379

[42] Benner, S. A. and Sismour, A. M. (2005) Synthetic biology. Nat. Rev. Genet., 6, 533−543

[43] Friedland, A. E., Lu, T. K., Wang, X., Shi, D., Church, G. and Collins, J. J. (2009) Synthetic gene networks that count. Science, 324, 1199−1202

[44] Skerker, J. M., Perchuk, B. S., Siryaporn, A., Lubin, E. A., Ashenberg, O., Goulian, M. and Laub, M. T. (2008) Rewiring the specificity of two-component signal transduction systems. Cell, 133, 1043−1054

[45] Kobayashi, H., Kaern, M., Araki, M., Chung, K., Gardner, T. S., Cantor, C. R. and Collins, J. J. (2004) Programmable cells: interfacing natural and engineered gene networks. Proc. Natl. Acad. Sci. U.S.A., 101, 8414−8419

[46] Balagaddé F. K., Song, H., Ozaki, J., Collins, C. H., Barnet, M., Arnold, F. H., Quake, S. R. and You, L. (2008) A synthetic Escherichia coli predator-prey ecosystem. Mol. Syst. Biol., 4, 187

[47] Lee, H. H., Molla, M. N., Cantor, C. R. and Collins, J. J. (2010) Bacterial charity work leads to population-wide resistance. Nature, 467, 82−85

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg