Predicting embryonic patterning using mutual entropy fitness and in silico evolution

Development

Volumn 137, Issue 14, 2010, Pages 2385-2395

  François, Paul ^a   Siggia, Eric D ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Hox genes; In silico evolution; Mutual entropy; Systems biology

Indexed keywords

ARTICLE; BIOCHEMISTRY; COMPUTER MODEL; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE REPRESSION; GROWTH RATE; HILL REACTION; HOX GENE; PRIORITY JOURNAL;

ANIMALS; EMBRYONIC DEVELOPMENT; ENTROPY; EVOLUTION; GENE EXPRESSION; GENES, HOMEOBOX; PHENOTYPE; VERTEBRATES;

HEXAPODA; VERTEBRATA;

EID: 77954656146     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048033     Document Type: Article

References (68)

1. Aulehla, A. and Pourquié, O. (2010). Signaling gradients during paraxial mesoderm development. Cold Spring Harbor Perspect. Biol. 2, a000869.
2. Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Hox genes and the evolution of vertebrate axial morphology. Development 121, 333-346.
3. Copf, T., Schröder, R. and Averof, M. (2004). Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl. Acad. Sci. USA 101, 17711-17715.
4. Crick, F. H. and Lawrence, P. A. (1975). Compartments and polyclones in insect development. Science 189, 340-347.
5. Davidson, E. H., Rast, J. P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C.-H., Minokawa, T., Amore, G., Hinman, V., Arenas-Mena, C. et al. (2002). A genomic regulatory network for development. Science 295, 1669-1678.
6. Duboule, D. (1995). Vertebrate hox genes and proliferation: an alternative pathway to homeosis? Curr. Opin. Genet. Dev. 5, 525-528.
7. Duboule, D. and Morata, G. (1994). Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358-364. (Pubitemid 24305375)
8. Dubrulle, J., McGrew, M. J. and Pourquie, O. (2001). Fgf signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal hox gene activation. Cell 106, 219-232.
9. Duprey, P., Chowdhury, K., Dressler, G. R., Balling, R., Simon, D., Guenet, J. L. and Gruss, P. (1988). A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev. 2, 1647-1654.
10. Durston, A. J., Jansen, H. J. and Wacker, S. A. (2010). Time-space translation regulates trunk axial patterning in the early vertebrate embryo. Genomics 95, 250-255.
11. Ferrier, D. E. K. and Minguillón, C. (2003). Evolution of the hox/parahox gene clusters. Int. J. Dev. Biol. 47, 605-611.
12. Francois, P. and Hakim, V. (2004). Design of genetic networks with specified functions by evolution in silico. Proc. Natl. Acad. Sci. USA 101, 580-585.
13. Francois, P. and Siggia, E. D. (2008). A case study of evolutionary computation of biochemical adaptation. Phys. Biol. 5, 26009.
14. Francois, P., Hakim, V. and Siggia, E. D. (2007). Deriving structure from evolution: metazoan segmentation. Mol. Syst. Biol. 3, 9.
15. Gaunt, S. J. and Strachan, L. (1994). Forward spreading in the establishment of a vertebrate hox expression boundary: the expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev. Dyn. 199, 229-240.
16. Gaunt, S. J., Drage, D. and Trubshaw, R. C. (2008). Increased cdx protein dose effects upon axial patterning in transgenic lines of mice. Development 135, 2511-2520.
17. Gebelein, B., Culi, J., Ryoo, H. D., Zhang, W. and Mann, R. S. (2002). Specificity of distalless repression and limb primordia development by abdominal hox proteins. Dev. Cell 3, 487-498. (Pubitemid 35252259)
18. Gehring, W. J. and Ikeo, K. (1999). Pax 6, mastering eye morphogenesis and eye evolution. Trends Genet. 15, 371-377.
19. Gibson, G. and Gehring, W. (1988). Head and thoracic transformations caused by ectopic expression of antennapedia during Drosophila development. Development 102, 657.
20. Giudicelli, F. and Lewis, J. (2004). The vertebrate segmentation clock. Curr. Opin. Genet. Dev. 14, 407-414.
21. Goldbeter, A. and Pourquié, O. (2008). Modeling the segmentation clock as a network of coupled oscillations in the notch, wnt and fgf signaling pathways. J. Theor. Biol. 252, 574-585.
22. González-Reyes, A. and Morata, G. (1990). The developmental effect of overexpressing a ubx product in Drosophila embryos is dependent on its interactions with other homeotic products. Cell 61, 515-522.
23. Green, J. (2002). Morphogen gradients, positional information, and Xenopus: Interplay of theory and experiment. Dev. Dyn. 225, 392-408.
24. Hobert, O. (2008). Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc. Natl. Acad. Sci. USA 105, 20067-20071.
25. Horan, G. S., Wu, K., Wolgemuth, D. J. and Behringer, R. R. (1994). Homeotic transformation of cervical vertebrae in hoxa-4 mutant mice. Proc. Natl. Acad. Sci. USA 91, 12644-12648.
26. Iimura, T. and Pourquie, O. (2006). Collinear activation of hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442, 568-571. (Pubitemid 44167915)
27. Iimura, T. and Pourquie, O. (2007). Hox genes in time and space during vertebrate body formation. Dev. Growth Differ. 49, 265-275. (Pubitemid 46743866)
28. Iimura, T., Denans, N. and Pourquié, O. (2009). Establishment of hox vertebral identities in the embryonic spine precursors. Curr. Top. Dev. Biol. 88, 201-234.
29. Isaacs, H. V., Pownall, M. E. and Slack, J. M. (1998). Regulation of hox gene expression and posterior development by the Xenopus caudal homologue xcad3. EMBO J. 17, 3413-3427.
30. Kessel, M., Balling, R. and Gruss, P. (1990). Variations of cervical vertebrae after expression of a hox-1.1 transgene in mice. Cell 61, 301-308.
31. Kmita, M. and Duboule, D. (2003). Organizing axes in time and space; 25 years of colinear tinkering. Science 301, 331-333. (Pubitemid 36877058)
32. Kozmik, Z. (2005). Pax genes in eye development and evolution. Curr. Opin. Genet. Dev. 15, 430-438.
33. Lewis, E. B. (1963). Genes and developmental pathways. Am. Zool. 3, 33-56.
34. Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
35. Lewis, E. B. (1992). The 1991 Albert Lasker medical awards. Clusters of master control genes regulate the development of higher organisms. JAMA 267, 1524-1531.
36. Liu, P. Z. and Kaufman, T. C. (2005). Short and long germ segmentation: unanswered questions in the evolution of a developmental mode. Evol. Dev. 7, 629-646.
37. Lufkin, T., Mark, M., Hart, C. P., Dollé, P., LeMeur, M. and Chambon, P. (1992). Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 359, 835-841.
38. Lynch, J. A., Brent, A. E., Leaf, D. S., Pultz, M. A. and Desplan, C. (2006). Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439, 728-732.
39. Mann, R. S. and Morata, G. (2000). The developmental and molecular biology of genes that subdivide the body of Drosophila. Annu. Rev. Cell Dev. Biol. 16, 243-271.
40. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
41. McIntyre, D. C., Rakshit, S., Yallowitz, A. R., Loken, L., Jeannotte, L., Capecchi, M. R. and Wellik, D. M. (2007). Hox patterning of the vertebrate rib cage. Development 134, 2981-2989. (Pubitemid 47386909)
42. Morata, G. (1993). Homeotic genes of Drosophila. Curr. Opin. Genet. Dev. 3, 606-614.
43. Nelson, C. E., Morgan, B. A., Burke, A. C., Laufer, E., DiMambro, E., Murtaugh, L. C., Gonzales, E., Tessarollo, L., Parada, L. F. and Tabin, C. (1996). Analysis of hox gene expression in the chick limb bud. Development 122, 1449-1466. (Pubitemid 26159635)
44. Nilsson, D. E. and Pelger, S. (1994). A pessimistic estimate of the time required for an eye to evolve. Proc. Biol. Sci. 256, 53-58.
45. Olesnicky, E. C., Brent, A. E., Tonnes, L., Walker, M., Pultz, M. A., Leaf, D. and Desplan, C. (2006). A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development 133, 3973-3982. (Pubitemid 44756190)
46. Oliveri, P., Tu, Q. and Davidson, E. H. (2008). Global regulatory logic for specification of an embryonic cell lineage. Proc. Natl. Acad. Sci. USA 105, 5955-5962. (Pubitemid 351758381)
47. Pearson, J. C., Lemons, D. and McGinnis, W. (2005). Modulating hox gene functions during animal body patterning. Nat. Rev. Genet. 6, 893-904. (Pubitemid 41782157)
48. Peel, A. D. (2008). The evolution of developmental gene networks: lessons from comparative studies on holometabolous insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1539-1547.
49. Peel, A. D., Chipman, A. D. and Akam, M. (2005). Arthropod segmentation: beyond the Drosophila paradigm. Nat. Rev. Genet. 6, 905-916.
50. Pownall, M. E., Tucker, A. S., Slack, J. M. and Isaacs, H. V. (1996). efgf, xcad3 and hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 122, 3881-3892.
51. Rieke, F., Warland, D., de Ruyter van Steveninck, R. and Bialek, W. (1999). Spikes: Exploring the Neural Code. Cambridge, MA: The MIT Press.
52. Rosenberg, M. I., Lynch, J. A. and Desplan, C. (2009). Heads and tails: evolution of antero-posterior patterning in insects. Biochim. Biophys. Acta 1789, 333-342.
53. Ryan, J. F., Mazza, M. E., Pang, K., Matus, D. Q., Baxevanis, A. D., Martindale, M. Q., Finnerty, J. R. and Fay, J. (2007). Pre-bilaterian origins of the hox cluster and the hox code: evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2, e153.
54. Seo, H.-C., Edvardsen, R. B., Maeland, A. D., Bjordal, M., Jensen, M. F., Hansen, A., Flaat, M., Weissenbach, J., Lehrach, H., Wincker, P. et al. (2004). Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431, 67-71.
55. Shannon, C. E. and Weaver, W. (1998). The Mathematical Theory of Communication. Urbana, IL: University of Illinois Press.
56. Shippy, T. D., Ronshaugen, M., Cande, J., He, J., Beeman, R. W., Levine, M., Brown, S. J. and Denell, R. E. (2008). Analysis of the tribolium homeotic complex: insights into mechanisms constraining insect hox clusters. Dev. Genes Evol. 218, 127-139.
57. Tkacik, G., Callan, C. G. and Bialek, W. (2008). Information flow and optimization in transcriptional regulation. Proc. Natl. Acad. Sci. USA 105, 12265-12270.
58. Tkacik, G., Walczak, A. M. and Bialek, W. (2009). Optimizing information flow in small genetic networks. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80, 031920.
59. Tschopp, P., Tarchini, B., Spitz, F., Zakany, J. and Duboule, D. (2009). Uncoupling time and space in the collinear regulation of hox genes. PLoS Genet. 5, e1000398.
60. Tzouanacou, E., Wegener, A., Wymeersch, F. J., Wilson, V. and Nicolas, J.-F. (2009). Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev. Cell 17, 365-376.
61. van den Akker, E., Forlani, S., Chawengsaksophak, K., de Graaff, W., Beck, F., Meyer, B. I. and Deschamps, J. (2002). Cdx1 and cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129, 2181-2193.
62. Wacker, S. A., McNulty, C. L. and Durston, A. J. (2004). The initiation of hox gene expression in Xenopus laevis is controlled by brachyury and bmp-4. Dev. Biol. 266, 123-137.
63. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R. and Hollenberg, S. (1991). The myod gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766.
64. Wellik, D. M. (2007). Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 236, 2454-2463.
65. Wellik, D. M. and Capecchi, M. R. (2003). Hox10 and hox11 genes are required to globally pattern the mammalian skeleton. Science 301, 363-367.
66. Young, T., Rowland, J. E., van de Ven, C., Bialecka, M., Novoa, A., Carapuco, M., van Nes, J., de Graaff, W., Duluc, I., Freund, J.-N. et al. (2009). Cdx and hox genes differentially regulate posterior axial growth in mammalian embryos. Dev. Cell 17, 516-526.
67. Ziv, E., Nemenman, I. and Wiggins, C. H. (2007). Optimal signal processing in small stochastic biochemical networks. PLoS ONE 2, e1077.
68. Zuber, M. E., Gestri, G., Viczian, A. S., Barsacchi, G. and Harris, W. A. (2003). Specification of the vertebrate eye by a network of eye field transcription factors. Development 130, 5155-5167. (Pubitemid 37369675)