Systems biology of embryogenesis
Lucas B. Edelman A B E , Sriram Chandrasekaran A C and Nathan D. Price A C D FA Institute for Genomic Biology, University of Illinois, Urbana-Champaign, Urbana, IL 61801, USA.
B Department of Bioengineering, University of Illinois, Urbana-Champaign, Urbana, IL 61801, USA.
C Center for Biophysics and Computational Biology, University of Illinois, Urbana-Champaign, Urbana, IL 61801, USA.
D Department of Chemical and Biomolecular Engineering, University of Illinois, Urbana-Champaign, Urbana, IL 61801, USA.
E Present address: The Babraham Institute, University of Cambridge, Cambridge CB2 3AT, UK.
F Corresponding author. Email: ndprice@illinois.edu
Reproduction, Fertility and Development 22(1) 98-105 https://doi.org/10.1071/RD09215
Published: 8 December 2009
Abstract
The development of a complete organism from a single cell involves extraordinarily complex orchestration of biological processes that vary intricately across space and time. Systems biology seeks to describe how all elements of a biological system interact in order to understand, model and ultimately predict aspects of emergent biological processes. Embryogenesis represents an extraordinary opportunity (and challenge) for the application of systems biology. Systems approaches have already been used successfully to study various aspects of development, from complex intracellular networks to four-dimensional models of organogenesis. Going forward, great advancements and discoveries can be expected from systems approaches applied to embryogenesis and developmental biology.
Additional keywords: complex adaptive systems, computational models, development, organogenesis, regulatory networks.
Acknowledgements
The authors gratefully acknowledge insightful discussions with Leroy Hood and James Eddy, and funding from the NIH Howard Temin Pathway to Independence Award in Cancer Research (NDP).
Aboobaker, A. A. , Tomancak, P. , Patel, N. , Rubin, G. M. , and Lai, E. C. (2005). Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc. Natl Acad. Sci. USA 102, 18 017–18 022.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bantscheff, M. , Schirle, M. , Sweetman, G. , Rick, J. , and Kuster, B. (2007). Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 389, 1017–1031.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Gunderson, K. L. , Steemers, F. J. , Lee, G. , Mendoza, L. G. , and Chee, M. S. (2005). A genome-wide scalable SNP genotyping assay using microarray technology. Nat. Genet. 37, 549–554.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kashiwagi, A. , Urabe, I. , Kaneko, K. , and Yomo, T. (2006). Adaptive response of a gene network to environmental changes by fitness-induced attractor selection. PLoS One 1, e49.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lausted, C. , Hu, Z. , and Hood, L. (2008). Quantitative serum proteomics from surface plasmon resonance imaging. Mol. Cell. Proteomics 7, 2464–2474.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Quail, M. A. , Kozarewa, I. , Smith, F. , Scally, A. , Stephens, P. J. , Durbin, R. , Swerdlow, H. , and Turner, D. J. (2008). A large genome center’s improvements to the Illumina sequencing system. Nat. Methods 5, 1005–1010.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Reeves, G. T. , Muratov, C. B. , Schüpbach, T. , and Shvartsman, S. Y. (2006). Quantitative models of developmental pattern formation. Dev. Cell 11, 289–300.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Robertson, S. H. , Smith, C. K. , Langhans, A. L. , McLinden, S. E. , and Oberhardt, M. A. , et al. (2007). Multiscale computational analysis of Xenopus laevis morphogenesis reveals key insights of systems-level behavior. BMC Syst. Biol. 1, 46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rothberg, J. M. , and Leamon, J. H. (2008). The development and impact of 454 sequencing. Nat. Biotechnol. 26, 1117–1124.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Rual, J. F. , Venkatesan, K. , Hao, T. , Hirozane-Kishikawa, T. , and Dricot, A. , et al. (2005). Towards a proteome-scale map of the human protein–protein interaction network. Nature 437, 1173–1178.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sandmann, T. , Girardot, C. , Brehme, M. , Tongprasit, W. , Stolc, V. , and Furlong, E. E. M. (2007). A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 21, 436–449.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Schena, M. , Shalon, D. , Davis, R. W. , and Brown, P. O. (1995). Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Schinköthe, T. , Bloch, W. , and Schmidt, A. (2008). In vitro secreting profile of human mesenchymal stem cells. Stem Cells Dev. 17, 199–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schwab, E. D. , and Pienta, K. J. (1996). Cancer as a complex adaptive system. Med. Hypotheses 47, 235–241.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Seila, A. C. , Calabrese, J. M. , Levine, S. S. , Yeo, G. W. , Rahl, P. B. , Flynn, R. A. , Young, R. A. , and Sharp, P. A. (2008). Divergent transcription from active promoters. Science 322, 1849–1851.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Setty, Y. , Cohen, I. R. , Dor, Y. , and Harel, D. (2008). Four-dimensional realistic modeling of pancreatic organogenesis. Proc. Natl Acad. Sci. USA 105, 20 374–20 379.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Shalgi, R. , Lieber, D. , Oren, M. , and Pilpel, Y. (2007). Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLOS Comput. Biol. 3, e131.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shannon, P. , Markiel, A. , Ozier, O. , Baliga, N. S. , Wang, J. T. , Ramage, D. , Amin, N. , Schwikowski, B. , and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Shannon, P. T. , Reiss, D. J. , Bonneau, R. , and Baliga, N. S. (2006). The Gaggle: An open-source software system for integrating bioinformatics software and data sources. BMC Bioinformatics 7, 176.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shendure, J. , and Ji, H. (2008). Next-generation DNA sequencing. Nat. Biotechnol. 26, 1135–1145.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sherlock, G. , Hernandez-Boussard, T. , Kasarskis, A. , Binkley, G. , and Matese, J. C. , et al. (2001). The Stanford Microarray Database. Nucleic Acids Res. 29, 152–155.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Stelling, J. , Sauer, U. , Szallasi, Z. , Doyle, F. J. , and Doyle, J. (2004). Robustness of cellular functions. Cell 118, 675–685.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Taft, R. J. , Pheasant, M. , and Mattick, J. S. (2007). The relationship between non-protein-coding DNA and eukaryotic complexity. BioEssays 29, 288–299.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Theise, N. D. (2006). Implications of ‘postmodern biology’ for pathology: the cell doctrine. Lab. Invest. 86, 335–344.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Theise, N. D. , and d’Inverno, M. (2004). Understanding cell lineages as complex adaptive systems. Blood Cells Mol. Dis. 32, 17–20.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tomancak, P. , Berman, B. , Beaton, A. , Weiszmann, R. , Kwan, E. , Hartenstein, V. , Celniker, S. , and Rubin, G. (2007). Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 8, R145.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tomlin, C. J. , and Axelrod, J. D. (2007). Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 8, 331–340.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tsang, J. , Zhu, J. , and van Oudenaarden, A. (2007). MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 26, 753–767.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Usui-Aoki, K. , Shimada, K. , Nagano, M. , Kawai, M. , and Koga, H. (2005). A novel approach to protein expression profiling using antibody microarrays combined with surface plasmon resonance technology. Proteomics 5, 2396–2401.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Van Loo, P. , Aerts, S. , Thienpont, B. , De Moor, B. , Moreau, Y. , and Marynen, P. (2008). ModuleMiner-improved computational detection of cis-regulatory modules: are there different modes of gene regulation in embryonic development and adult tissues? Genome Biol. 9, R66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
von Dassow, G. , Meir, E. , Munro, E. M. , and Odell, G. M. (2000). The segment polarity network is a robust developmental module. Nature 406, 188–192.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Walker, D. C. , and Southgate, J. (2009). The virtual cell: a candidate co-ordinator for ‘middle-out’ modelling of biological systems. Brief. Bioinform. 10, 450–461.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Walker, D. , Wood, S. , Southgate, J. , Holcombe, M. , and Smallwood, R. (2006). An integrated agent-mathematical model of the effect of intercellular signalling via the epidermal growth factor receptor on cell proliferation. J. Theor. Biol. 242, 774–789.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wang, J. , Wang, W. , Li, R. , Li, Y. , and Tian, G. , et al. (2008). The diploid genome sequence of an Asian individual. Nature 456, 60–65.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wei, Z. , Angerer, R. , and Angerer, L. (2006). A database of mRNA expression patterns for the sea urchin embryo. Dev. Biol. 300, 476–484.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wheeler, D. A. , Srinivasan, M. , Egholm, M. , Shen, Y. , and Chen, L. , et al. (2008). The complete genome of an individual by massively parallel DNA sequencing. Nature 452, 872–876.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Xiao, Z. , Blonder, J. , Zhou, M. , and Veenstra, T. (2009). Proteomic analysis of extracellular matrix and vesicles. J. Proteomics 72, 34–45.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zhao, F. , Xuan, Z. , Liu, L. , and Zhang, M. Q. (2005). TRED: a transcriptional regulatory element database and a platform for in silico gene regulation studies. Nucleic Acids Res. 33, D103–D107.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |