Gene regulatory network controlling embryonic specification in the sea urchin

Current Opinion in Genetics and Development

Volumn 14, Issue 4, 2004, Pages 351-360

  Oliveri, Paola ^a   Davidson, Eric H ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

early signal; ES; gene regulatory network; GRN; M; MASO; micromeres; morpholino substituted antisense oligonucleotide; N; notch; PMC; primary mesenchyme cells; secondary mesenchyme cells; SMC

Indexed keywords

BETA CATENIN; WNT PROTEIN;

BIOLOGY; CELL LINEAGE; DEVELOPMENT; EMBRYOLOGY; ENDODERM; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC LINKAGE; GENOME; MESODERM; MODEL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SEA URCHIN; ZYGOTE;

NON-PROGRAMMATIC;

ANIMALS; CELL DIFFERENTIATION; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; MODELS, BIOLOGICAL; SEA URCHINS;

ECHINOIDEA;

EID: 3142630279     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2004.06.004     Document Type: Review

References (50)

1. Arnone M.I., Davidson E.H. The hardwiring of development: organization and function of genomic regulatory systems. Development. 124:1997;1851-1864
2. Davidson EH: Genomic Regulatory Systems. Development and Evolution. San Diego, CA: Academic Press; 2001.
3. Brown C.T., Rust A.G., Clarke P.J., Pan Z., Schilstra M.J., De Buysscher T., Griffin G., Wold B.J., Cameron R.A., Davidson E.H., et al. New computational approaches for analysis of cis-regulatory networks. Dev Biol. 246:2002;86-102
4. ••].
5. ••] we describe the identification and provide a thorough experimental analysis, in both cis and trans, of the regulatory element responsible for correct expression of the endomesoderm variant of the Otx factor. The results unequivocally demonstrate the direct regulation of the otx gene by gatae and krox genes, plus an autoregulatory loop. These specific DNA-transcription factor interactions were all correctly predicted to be direct in the GRN model.
6. Uchikawa M., Ishida Y., Takemoto T., Kamachi Y., Kondoh H. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell. 4:2003;509-519 A functional analysis of the regulatory sequence of the chicken sox2 gene shows that its apparently uniform CNS expression is regulated by five different modules, each responsible for a portion of the total expression pattern. The identified regulatory modules correspond to extragenic blocks of sequence that are conserved between chicken and mammals, highlighting the importance for success in interspecies sequence comparison of choosing the right evolutionary distance.
7. Stathopoulos A., Van Drenth M., Erives A., Markstein M., Levine M. Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. Cell. 111:2002;687-701
8. Rajewsky N., Vergassola M., Gaul U., Siggia E.D. Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics. 3:2002;30
9. Markstein M., Levine M. Decoding cis-regulatory DNAs in the Drosophila genome. Curr Opin Genet Dev. 12:2002;601-606 This review is a useful summary of recent efforts to identify the regulatory code by mainly computational means. All strategies reviewed involve searching for clusters of specific, well characterized binding sites, which are known to be key regulators of one or more genes. The review mainly considers Drosophila melanogaster.
10. Berman B.P., Nibu Y., Pfeiffer B.D., Tomancak P., Celniker S.E., Levine M., Rubin G.M., Eisen M.B. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci USA. 99:2002;757-762
11. Calzone F.J., Theze N., Thiebaud P., Hill R.L., Britten R.J., Davidson E.H. Developmental appearance of factors that bind specifically to cis-regulatory sequences of a gene expressed in the sea urchin embryo. Genes Dev. 2:1988;1074-1088
12. Nasiadka A, Dietrich BH, Krause HM: Advances in Developmental Biology and Biochemistry. Edited by M DePamphilis. Amsterdam: Elsevier; 2002:155-204.
13. ••].
14. ••] describe the first large-scale GRN for an animal developmental system, and provide the foundation for the studies reviewed here. The authors describe all the data obtained to build the initial version of the sea urchin endomesoderm GRN, the general approach used to study the GRN, the type of data necessary to build a developmental logic model, and the biological meaning of the model.
15. Bolouri H., Davidson E.H. Transcriptional regulatory cascades in development: Initial rates, not steady state, determine network kinetics. Proc Natl Acad Sci USA. 100:2003;9371-9376 The kinetics of gene regulatory cascades are here modeled in mathematical terms. Such cascades exist in developmental GRNs. Simulation is carried out using real sea urchin embryo parameters, and the models illustrate sharp transitions in regulatory state. State transitions occur long before the steady-state level of the upstream regulatory molecules is ever reached. The main causes are cooperativity between regulatory factors and the high specificity of DNA-transcription factor interaction.
16. Chuang C.K., Wikramanayake A.H., Mao C.A., Li X., Klein W.H. Transient appearance of Strongylocentrotus purpuratus Otx in micromere nuclei: cytoplasmic retention of SpOtx possibly mediated through an alpha-actinin interaction. Dev Genet. 19:1996;231-237
17. Kenny A.P., Kozlowski D., Oleksyn D.W., Angerer L.M., Angerer R.C. SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. Development. 126:1999;5473-5483
18. Oliveri P., Carrick D.M., Davidson E.H. A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev Biol. 246:2002;209-228
19. Logan C.Y., Miller J.R., Ferkowicz M.J., McClay D.R. Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development. 126:1999;345-357
20. Wikramanayake A.H., Huang L., Klein W.H. beta-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proc Natl Acad Sci USA. 95:1998;9343-9348
21. Emily-Fenouil F., Ghiglione C., Lhomond G., Lepage T., Gache C. GSK3beta/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo. Development. 125:1998;2489-2498
22. Weitzel H.E., Illies M.R., Byrum C.A., Xu R., Wikramanayake A.H., Ettensohn C.A. Differential stability of beta-catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development. 131:2004;2947-2956 The authors describe in vivo measurements of β-catenin half-life in the sea urchin embryo. They demonstrate that nuclearization of β-catenin at the vegetal pole of the embryo is a direct consequence of differential protein stability. The key player in stabilizing β-catenin at the vegetal pole is Dishevelled. This molecule is localized to the vegetal cortex and is specifically segregated predominantly to the vegetal blastomeres during the first set of cleavages.
23. Ransick A., Davidson E.H. Micromeres are required for normal vegetal plate specification in sea urchin embryos. Development. 121:1995;3215-3222
24. Oliveri P., Davidson E.H., McClay D.R. Activation of pmar1 controls specification of micromeres in the sea urchin embryo. Dev Biol. 258:2003;32-43 We experimentally tested an architectural component of the sea urchin GRN. In the micromere/PMC lineage the only transducer of maternal inputs is the regulatory system of the gene pmar1. This prediction of the network architecture has been proved by transplantation of micromeres that are unable to express their endogenous pmar1 gene, but which are able to rescue all the normal functions performed by micromeres if pmar1 mRNA has been reintroduced into them. Ectopic pmar1 mRNA has the ability to promote the micromere/PMC regulatory program in all the cells of the embryo.
25. Sweet H.C., Gehring M., Ettensohn C.A. LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development. 129:2002;1945-1955
26. Sherwood D.R., McClay D.R. LvNotch signaling plays a dual role in regulating the position of the ectoderm-endoderm boundary in the sea urchin embryo. Development. 128:2001;2221-2232
27. Ransick A., Rast J.P., Minokawa T., Calestani C., Davidson E.H. New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev Biol. 246:2002;132-147
28. Calestani C., Rast J.P., Davidson E.H. Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development. 130:2003;4587-4596 A differential screen to isolate SMC-specific genes is described in this paper. Using a perturbation of Delta/Notch signaling, the authors isolate a set of transcription factors and downstream genes that are specific for pigment cell specification. This approach led to a better understanding of SMC specification, and more specifically of the pigment cell differentiation pathway.
29. Howard E.W., Newman L.A., Oleksyn D.W., Angerer R.C., Angerer L.M. SpKrl: A direct target of beta-catenin regulation required for endoderm differentiation in sea urchin embryos. Development. 128:2001;365-375
30. Hinman V.F., Nguyen A.T., Cameron R.A., Davidson E.H. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci USA. 100:2003;13356-13361 This paper describes a comparative analysis of endomesoderm GRNs between two echinoderm species that have evolved separately for 500 million years. Conservation of a major intergenic regulatory loop was demonstrated, attesting to the functional importance of this architectural feature. Many other aspects of the respective GRNs were shown to be different, and the differences predict the respective patterns of gene expression.
31. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., Alon U. Network motifs: Simple building blocks of complex networks. Science. 298:2002;824-827
32. Davidson E.H., McClay D.R., Hood L. Regulatory gene networks and the properties of the developmental process. Proc Natl Acad Sci USA. 100:2003;1475-1480 This review of the few extant experimentally established examples considers the significance of GRN analysis, both for understanding the function of the animal genome, and for understanding the basic mechanisms of animal development. Only by GRN analysis can the genomic regulatory code underlying development be expressed in an appropriate system-level model.
33. Ettensohn CA, Ingersoll EP: Morphogenesis of the sea urchin embryo. In Morphogenesis: Analysis of the Development of Biological Structures. Edited by EF Rossomando and S Alexander. New York: Marcel Dekker press; 1992:189-263.
34. Davidson E.H., Cameron R.A., Ransick A. Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development. 125:1998;3269-3290
35. Ruffins S.W., Ettensohn C.A. A clonal analysis of secondary mesenchyme cell fates in the sea urchin embryo. Dev Biol. 160:1993;285-288
36. Ruffins S.W., Ettensohn C.A. A fate map of the vegetal plate of the sea urchin (Lytechinus variegatus) mesenchyme blastula. Development. 122:1996;253-263
37. Revilla-i-Domingo R. Davidson EH: Developmental gene network analysis. Int J Dev Biol. 47:2003;695-703
38. Takacs C.M., Amore G., Oliveri P., Poustka A.J., Wang D., Burke R.D., Peterson K.J. Expression of an NK2 homeodomain gene in the apical ectoderm defines a new territory in the early sea urchin embryo. Dev Biol. 269:2004;152-164
39. Rast J.P., Cameron R.A., Poustka A.J., Davidson E.H. brachyury Target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev Biol. 246:2002;191-208
40. Zhu X., Mahairas G., Illies M., Cameron R.A., Davidson E.H., Ettensohn C.A. A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development. 128:2001;2615-2627
41. Cavallo R., Rubenstein D., Peifer M. Armadillo and dTCF: A marriage made in the nucleus. Curr Opin Genet Dev. 7:1997;459-466
42. Jacobsen T.L., Brennan K., Arias A.M., Muskavitch M.A. Cis-interactions between Delta and Notch modulate neurogenic signalling in Drosophila. Development. 125:1998;4531-4540
43. Yeh E., Zhou L., Rudzik N., Boulianne G.L. Neuralized functions cell autonomously to regulate Drosophila sense organ development. EMBO J. 19:2000;4827-4837
44. Yeh E., Dermer M., Commisso C., Zhou L., McGlade C.J., Boulianne G.L. Neuralized functions as an E3 ubiquitin ligase during Drosophila development. Curr Biol. 11:2001;1675-1679
45. Huang L., Li X., El-Hodiri H.M., Dayal S., Wikramanayake A.H., Klein W.H. Involvement of Tcf/Lef in establishing cell types along the animal-vegetal axis of sea urchins. Dev Genes Evol. 210:2000;73-81
46. Vonica A., Weng W., Gumbiner B.M., Venuti J.M. TCF is the nuclear effector of the beta-catenin signal that patterns the sea urchin animal-vegetal axis. Dev Biol. 217:2000;230-243
47. Kenny A.P., Oleksyn D.W., Newman L.A., Angerer R.C., Angerer L.M. Tight regulation of SpSoxB factors is required for patterning and morphogenesis in sea urchin embryos. Dev Biol. 261:2003;412-425 This paper points out the importance of SoxB1 protein exclusion from the vegetal nuclei for the early specification processes, initially in micromeres and later in the endomesoderm territory. The authors compare the specificity of this SoxB1 function with that of a closely related Sox class transcription factor, SoxB2.
48. Ettensohn C.A., Illies M.R., Oliveri P., De Jong D.L. Alx1, a member of the Cart1/Alx3/Alx4 subfamily of Paired-class homeodomain proteins, is an essential component of the gene network controlling skeletogenic fate specification in the sea urchin embryo. Development. 130:2003;2917-2928 The authors describe the functional characterization of an important new transcription factor, Alx1, involved in the micromere/PMC network. The role of Alx1 in the PMC lineage is to connect the very early zygotic inputs to the downstream differentiation gene battery, controlling directly the epithelial-mesenchyme transition of these cells and their skeletogenic biosynthetic functions.
49. Kurokawa D., Kitajima T., Mitsunaga-Nakatsubo K., Amemiya S., Shimada H., Akasaka K. HpEts, an ets-related transcription factor implicated in primary mesenchyme cell differentiation in the sea urchin embryo. Mech Dev. 80:1999;41-52
50. Bolouri H., Davidson E.H. Modeling DNA sequence-based cis-regulatory gene networks. Dev Biol. 246:2002;2-13