Cited by 796Developmental Biology and Gene RegulationGenomics and Chromatin DynamicsGene Regulatory Network Analysis

Gene regulatory networks for development

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Levine, Michael, Davidson, Eric H.·2005·Proceedings of the National Academy of Sciences

Abstract

The genomic program for development operates primarily by the regulated expression of genes encoding transcription factors and components of cell signaling pathways. This program is executed by cis-regulatory DNAs (e.g., enhancers and silencers) that control gene expression. The regulatory inputs and functional outputs of developmental control genes constitute network-like architectures. In this PNAS Special Feature are assembled papers on developmental gene regulatory networks governing the formation of various tissues and organs in nematodes, flies, sea urchins, frogs, and mammals. Here, we survey salient points of these networks, by using as reference those governing specification of the endomesoderm in sea urchin embryos and dorsal-ventral patterning in the Drosophila embryo.

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Crossref · 10.1073/pnas.0408031102

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  • Recent evidence shows that positions where cis-regulatory modules act depend on combinatorial activator and repressor inputs, and morphogen concentrations alone do not predict target expression domains except sometimes at extreme high concentrations.

    “Much recent evidence, however, shows that the positions where these cis-regulatory modules act depend on combinatorial activator and repressor inputs15–19, and the quantitative values of these ‘morphogens’ alone do not by themselves predict the spatial expression domains of their target genes (except sometimes at the extreme positions where their concentrations are highest).”

    From Emerging properties of animal gene regulatory networks (2010) · cites this paper as [17]

  • In the syncytial Drosophila embryo, spatial stripes of dorsal/ventral and anterior/posterior regulatory gene expression are generated by parallel cis-regulatory responses to maternal and zygotic combinations of diffusing transcription factors.

    “In the syncytial embryo spatial stripes of both dorsal/ventral and anterior/posterior regulatory gene expression, which specify the future multicellular embryonic territories, are generated by parallel cis-regulatory responses to maternally localized and zygotically expressed combinations of diffusing transcription factors15–17.”

    From Emerging properties of animal gene regulatory networks (2010) · cites this paper as [17]

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  1. [1]Small, S., Blair, A. & Levine, M. (1992) EMBO J. 11, 4047–4057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. [3]Gray, S., Szymanski, P. & Levine, M. (1994) Genes Dev. 8, 1829–1838. [DOI] [PubMed] [Google Scholar]
  3. [4]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) Science 295, 1669–1678. [DOI] [PubMed] [Google Scholar]
  4. [5]Davidson, E. H., McClay, D. R. & Hood, L. (2003) Proc. Natl. Acad. Sci. USA 100, 1475–1480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. [6]Bolouri, H. & Davidson, E. H. (2002) BioEssays 24, 1118–1129. [DOI] [PubMed] [Google Scholar]
  6. [7]Oliveri, P. & Davidson, E. H. (2004) Curr. Opin. Genet. Dev. 14, 351–360. [DOI] [PubMed] [Google Scholar]
  7. [8]Ochoa-Espinosa, A., Yucel, G., Kaplan, L., Pare, A., Pura, N., Oberstein, A., Papatsenko, D. & Small, S. (2005) Proc. Natl. Acad. Sci. USA 102, 4960–4965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. [9]Stathopoulos, A. & Levine, M. (2002) Dev. Biol. 246, 57–67. [DOI] [PubMed] [Google Scholar]
  9. [10]Koide, T., Hayata, T. & Cho, K. (2005) Proc. Natl. Acad. Sci. USA 102, 4943–4948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. [11]Singh, H. & Medina, K. L. (2005) Proc. Natl. Acad. Sci. USA 102, 4949–4953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. [12]Inoue, T., Wang, M., Ririe, T., Fernandes, J. & Sternberg, P. W. (2005) Proc. Natl. Acad. Sci. USA 102, 4972–4977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. [13]Papatsenko, D. & Levine, M. (2005) Proc. Natl. Acad. Sci. USA 102, 4966–4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. [14]Istrail, S. & Davidson, E. H. (2005) Proc. Natl. Acad. Sci. USA 102, 4954–4959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. [15]Davidson, E. H., Cameron, R. A. & Ransick, A. (1998) Development (Cambridge, U.K.) 125, 3269–3290. [DOI] [PubMed] [Google Scholar]
  15. [16]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) Dev. Biol. 246, 162–190. [DOI] [PubMed] [Google Scholar]
  16. [17]Oliveri, P., Carrick, D. M. & Davidson, E. H. (2002) Dev. Biol. 246, 209–228. [DOI] [PubMed] [Google Scholar]
  17. [18]Oliveri, P., McClay, D. R. & Davidson, E. H. (2003) Dev. Biol. 258, 32–43. [DOI] [PubMed] [Google Scholar]
  18. [19]Yuh, C.-H., Dorman, E. R., Howard, M. L. & Davidson, E. H. (2004) Dev. Biol. 269, 536–551. [DOI] [PubMed] [Google Scholar]
  19. [20]Logan, C. Y., Miller, J. R., Ferkowicz, M. J. & McClay, D. R. (1999) Development (Cambridge, U.K.) 126, 345–357. [DOI] [PubMed] [Google Scholar]
  20. [21]Emily-Fenouil, F., Ghiglione, C., Lhomond, G., Lepage, T. & Gache, C. (1998) Development (Cambridge, U.K.) 125, 2489–2498. [DOI] [PubMed] [Google Scholar]
  21. [22]Weitzel, H. E., Illies, M. R., Byrum, C. A., Xu, R., Wikramanatake, A. H. & Ettensohn, C. A. (2004) Development (Cambridge, U.K.) 131, 2947–2956. [DOI] [PubMed] [Google Scholar]
  22. [23]Wikramanayake, A. H., Huang, L. & Klein, W. H. (1998) Proc. Natl. Acad. Sci. USA 95, 9343–9348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. [24]Minokawa, T.& Davidson, E. H. (2005) Dev. Biol., in press.
  24. [25]Sherwood, D. R. & McClay, D. R. (1997) Development (Cambridge, U.K.) 124, 3363–3374. [DOI] [PubMed] [Google Scholar]
  25. [26]Sherwood, D. R. & McClay, D. R. (1999) Development (Cambridge, U.K.) 126, 1703–1713. [DOI] [PubMed] [Google Scholar]
  26. [27]Sweet, H. C., Hodor, P. G.& Ettensohn, C. A. (1999) Development (Cambridge, U.K.) 126, 5255–5265. [DOI] [PubMed] [Google Scholar]
  27. [28]Revilla-i-Domingo, R., Minokawa, T. & Davidson, E. H. (2004) Dev. Biol. 274, 438–451. [DOI] [PubMed] [Google Scholar]
  28. [29]Calestani, C., Rast, J. P. & Davidson, E. H. (2003) Development (Cambridge, U.K.) 130, 4587–4596. [DOI] [PubMed] [Google Scholar]
  29. [30]Stathopoulos, A., Van Drenth, M., Erives, A., Markstein, M. & Levine, M. (2002) Cell 111, 687–701. [DOI] [PubMed] [Google Scholar]
  30. [31]Zaffran, S. & Frasch, M. (2002) Circ. Res. 91, 457–469. [DOI] [PubMed] [Google Scholar]
  31. [32]Kasai, Y., Stahl, S. & Crews, S. (1998) Gene Expression 7, 171–189. [PMC free article] [PubMed] [Google Scholar]
  32. [33]Frank, L. H. & Rushlow, C. (1996) Development (Cambridge, U.K.) 122, 1343–1352. [DOI] [PubMed] [Google Scholar]
  33. [34]Peri, F., Technau, M. & Roth, S. (2002) Development (Cambridge, U.K.) 129, 2965–2975. [DOI] [PubMed] [Google Scholar]
  34. [35]Belvin, M. P. & Anderson, K. V. (1996) Annu. Rev. Cell Dev. Biol. 12, 393–416. [DOI] [PubMed] [Google Scholar]
  35. [36]Stathopoulos, A., Tam, B., Ronshaugen, M., Frasch, M. & Levine, M. (2004) Genes Dev. 18, 687–699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. [37]Jiang, J. & Levine, M. (1993) Cell 72, 741–752. [DOI] [PubMed] [Google Scholar]
  37. [38]Kosman, D., Ip, Y. T., Levine, M. & Arora, K. (1991) Science 254, 118–122. [DOI] [PubMed] [Google Scholar]
  38. [39]Leptin, M. (1991) Genes Dev. 5, 1568–1576. [DOI] [PubMed] [Google Scholar]
  39. [40]Alberga, A., Boulay, J. L., Kempe, E., Dennefeld, C. & Haenlin, M. (1991) Development (Cambridge, U.K.) 111, 983–992. [DOI] [PubMed] [Google Scholar]
  40. [41]Rushlow, C., Colosimo, P. F., Lin, M.C., Xu, M. & Kirov, N. (2001) Genes Dev. 15, 340–351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. [42]Zhang, H., Levine, M. & Ashe, H. L. (2001) Genes Dev. 15, 261–266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. [43]Pyrowolakis, G., Hartmann, B., Muller, B., Basler, K. & Affolter, M. (2004) Dev. Cell 7, 229–240. [DOI] [PubMed] [Google Scholar]
  43. [44]Morel, V. & Schweisguth, F. (2000) Genes Dev. 14, 377–388. [PMC free article] [PubMed] [Google Scholar]
  44. [45]Cowden, J. & Levine, M. (2002) Development (Cambridge, U.K.) 129, 1785–1793. [DOI] [PubMed] [Google Scholar]
  45. [46]Nambu, J. R., Lewis, J. O., Wharton, K. A., Jr., & Crews, S. T. (1991) Cell 67, 157–167. [DOI] [PubMed] [Google Scholar]
  46. [47]Lee, C. M., Yu, D. S., Crews, S. T. & Kim, S. H. (1999) Int. J. Dev. Biol. 43, 305–315. [PubMed] [Google Scholar]
  47. [48]Golembo, M., Raz, E. & Shilo, B. Z. (1996) Development (Cambridge, U.K.) 122, 3363–3370. [DOI] [PubMed] [Google Scholar]
  48. [49]Chang, J., Kim, I. O., Ahn, J. S. & Kim, S. H. (2001) Int. J. Dev. Biol. 45, 715–724. [PubMed] [Google Scholar]
  49. [50]Zinn, K. & Sun, Q. (1999) Cell 97, 1–4. [DOI] [PubMed] [Google Scholar]
  50. [51]Golembo, M., Yarnitzky, T., Volk, T. & Shilo, B. Z. (1999) Genes Dev. 13, 158–162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. [52]Gabay, L., Scholz, H., Golembo, M., Klaes, A., Shilo, B. Z. & Klambt, C. (1996) Development (Cambridge, U.K.) 122, 3355–3362. [DOI] [PubMed] [Google Scholar]
  52. [53]von Ohlen, T. & Doe, C. Q. (2000) Dev. Biol. 224, 362–372. [DOI] [PubMed] [Google Scholar]
  53. [54]Weiss, J. B., Von Ohlen, T., Mellerick, D. M., Dressler, G., Doe, C. Q. & Scott, M. P. (1998) Genes Dev. 12, 3591–3602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. [55]Cornell, R. A., Ohlen, T. V. (2000) Curr. Opin. Neurobiol. 10, 63–71. [DOI] [PubMed] [Google Scholar]
  55. [56]Hinman, V. F., Nguyen, A., Cameron, R. A. & Davidson, E. H. (2003) Proc. Natl. Acad. Sci. USA 100, 13356–13361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. [57]Amiri, A. & Stein, D. (2002) Curr. Biol. 12, R532–R534. [DOI] [PubMed] [Google Scholar]
  57. [58]Nilson, L. A. & Schupbach, T. (1999) Curr. Top. Dev. Biol. 44, 203–243. [DOI] [PubMed] [Google Scholar]
  58. [59]Roth, S. (1994) Curr. Biol. 4, 755–757. [DOI] [PubMed] [Google Scholar]
  59. [60]Markstein, M., Zinzen, R., Markstein, P., Yee, K. P., Erives, A., Stathopoulos, A. & Levine, M. (2004) Development (Cambridge, U.K.) 131, 2387–2394. [DOI] [PubMed] [Google Scholar]
  60. [61]Podos, S. D. & Ferguson, E. L. (1999) Trends Genet. 15, 396–402. [DOI] [PubMed] [Google Scholar]
  61. [62]Halfon, M. S., Grad, Y., Church, G. M., Michelson, A. M. (2002) Genome Res. 12, 1019–1028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. [63]Lee, J. R., Urban, S., Garvey, C. F. & Freeman, M. (2001) Cell 107, 161–171. [DOI] [PubMed] [Google Scholar]
  63. [64]Raftery, L. A. & Sutherland, D. J. (2003) Trends Genet. 19, 701–708. [DOI] [PubMed] [Google Scholar]
  64. [65]Reim, I., Lee, H. H. & Frasch, M. (2003) Development (Cambridge, U.K.) 130, 3187–3204. [DOI] [PubMed] [Google Scholar]
  65. [66]Wharton, S. J., Basu, S. P. & Ashe, H. L. (2004) Curr. Biol. 14, 1550–1558. [DOI] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Levine, M., & Davidson, E. H.
Affiliations
California Institute of Technology (US)
Venue
Proceedings of the National Academy of Sciences
Published
2005-03-23
Volume
102
Issue
14
Pages
4936-4942
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2148944713
Cited by
796
References
7
Citations by year
2026: 44 · 2025: 50 · 2024: 36 · 2023: 44 · 2022: 25 · 2021: 38 · 2020: 28 · 2019: 36 · 2018: 27 · 2017: 32 · 2016: 31 · 2015: 24 · 2014: 34 · 2013: 29 · 2012: 30
FWCI
19.44
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Funders
  • National Institutes of Health (5p01hd037105-20)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01-HD037105, HD37105)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
gene regulatory networks, developmental gene regulation, cis-regulatory elements, enhancers, silencers, transcription factors, signaling pathways, endomesoderm specification, sea urchin embryo, dorsoventral patterning, Drosophila embryo, organogenesis, tissue specification
MeSH terms
Animals, Drosophila, Endoderm, Genes, Regulator, Mesoderm, Models, Genetic, Morphogenesis, Genes, Insect, Gene Expression Regulation, Developmental, Body Patterning, Strongylocentrotus purpuratus

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