A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

Development (Cambridge)

Volumn 141, Issue 12, 2014, Pages 2462-2472

  Annunziata, Rossella ^a,b   Arnone, Maria Ina ^a  

^a STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

^b UMR 7238   (France)

Author keywords

Gene regulatory network; Intestine; Stomach

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ANTISENSE OLIGONUCLEOTIDE; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1A; BRA PROTEIN; CHOLINERGIC RECEPTOR; FORKHEAD TRANSCRIPTION FACTOR; FOXA PROTEIN; HOX PROTEIN; HOX11 PROTEIN; HOX13 PROTEIN; MESSENGER RNA; MYOSIN HEAVY CHAIN; NEUROGENIC DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CDX; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETS 4; TRANSCRIPTION FACTOR FOXA; TRANSCRIPTION FACTOR FOXD; TRANSCRIPTION FACTOR FOXP; TRANSCRIPTION FACTOR FOXY; TRANSCRIPTION FACTOR IRXB; TRANSCRIPTION FACTOR LOX; TRANSCRIPTION FACTOR NKX3.2; TRANSCRIPTION FACTOR OTX; TRANSCRIPTION FACTOR TBR; TRANSCRIPTION FACTOR XLOX; UNCLASSIFIED DRUG; WNT PROTEIN; WNT10 PROTEIN;

ANIMAL EXPERIMENT; ANTERIOR POSTERIOR AXIS; ARTICLE; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; DEUTEROSTOMIA; DNA LIBRARY; DOWN REGULATION; EMBRYO; ENDODERM; FLUORESCENCE IN SITU HYBRIDIZATION; GASTRULA; GASTRULATION; GENE CONTROL; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HOX GENE; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; INTESTINE CELL; LARVAL STAGE; MIDGUT; MORPHOGENESIS; MUSCLE CELL; NONHUMAN; PARAHOX GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA SEQUENCE; SPHINCTER; STOMACH; STRONGYLOCENTROTUS PURPURATUS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WNT SIGNALING PATHWAY;

GENE REGULATORY NETWORK; INTESTINE; STOMACH;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; INTESTINES; PROTEIN-LYSINE 6-OXIDASE; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; STOMACH; STRONGYLOCENTROTUS PURPURATUS;

EID: 84902194233     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.105775     Document Type: Article

References (62)

1. Anders, S. and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11, R106.
2. Andrikou, C., Iovene, E., Rizzo, F., Oliveri, P. and Arnone, M. I. (2013). Myogenesis in the sea urchin embryo: the molecular fingerprint of the myoblast precursors. EvoDevo 4, 33.
3. Annunziata, R., Martinez, P. and Arnone, M. I. (2013a). Intact cluster and chordate-like expression of ParaHox genes in a sea star. BMC Biol. 11, 68.
4. Annunziata, R., Perillo, M., Andrikou, C., Cole, A. G., Martinez, P. and Arnone, M. I. (2013b). Pattern and process during sea urchin gut morphogenesis: the regulatory landscape. Genesis 52, 251-268.
5. Arenas-Mena, C., Cameron, R. A. and Davidson, E. H. (2006). Hindgut specification and cell-adhesion functions of Sphox11/13b in the endoderm of the sea urchin embryo. Dev. Growth Differ. 48, 463-472.
6. Arnone, M. I., Rizzo, F., Annunciata, R., Cameron, R. A., Peterson, K. J. and Martińez, P. (2006). Genetic organization and embryonic expression of the ParaHox genes in the sea urchin S. purpuratus: insights into the relationship between clustering and colinearity. Dev. Biol. 300, 63-73.
7. Babu, D. A., Chakrabarti, S. K., Garmey, J. C. and Mirmira, R. G. (2008). Pdx1 and BETA2/NeuroD1 participate in a transcriptional complex that mediates short-range DNA looping at the insulin gene. J. Biol. Chem. 283, 8164-8172.
8. Brooke, N. M., Garcia-Fernaǹdez, J. and Holland, P. W. H. (1998). The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392, 920-922.
9. Burke, R. D. (1981). Structure of the digestive tract of the pluteus larva of dendraster excentricus (echinodermata: echinoida). Zoomorphology 98, 209-225.
10. Burke, R. D., Angerer, L. M., Elphick, M. R., Humphrey, G. W., Yaguchi, S., Kiyama, T., Liang, S., Mu, X., Agca, C., Klein, W. H. et al. (2006). A genomic view of the sea urchin nervous system. Dev. Biol. 300, 434-460.
11. Chawengsaksophak, K., de Graaff, W., Rossant, J., Deschamps, J. and Beck, F. (2004). Cdx2 is essential for axial elongation in mouse development. Proc. Natl. Acad. Sci. U.S.A. 101, 7641-7645.
12. Cole, A. G. and Arnone, M. I. (2009). Fluorescent in situ hybridization reveals multiple expression domains for SpBrn1/2/4 and identifies a unique ectodermal cell type that co-expresses the ParaHox gene SpLox. Gene Expr. Patterns 9, 324-328.
13. Cole, A. G., Rizzo, F., Martinez, P., Fernandez-Serra, M. and Arnone, M. I. (2009). Two ParaHox genes, SpLox and SpCdx, interact to partition the posterior endoderm in the formation of a functional gut. Development 136, 541-549.
14. Croce, J. C. and McClay, D. R. (2010). Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo. Development 137, 83-91.
15. Croce, J., Duloquin, L., Lhomond, G., McClay, D. R. and Gache, C. (2006). Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. Development 133, 547-557.
16. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
17. David, E.-S., Luke, N. H. and Livingston, B. T. (1999). Characterization of a gene encoding a developmentally regulated winged helix transcription factor of the sea urchin Strongylocentrotus purpuratus. Gene 236, 97-105.
18. Davidson, E. H. (2010). Emerging properties of animal gene regulatory networks. Nature 468, 911-920.
19. 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.
20. Donoghue, P. C. J. and Purnell, M. A. (2005). Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312-319.
21. Feng, R., Xiao, C. and Zavros, Y. (2012). The role of Sonic Hedgehog as a regulator of gastric function and differentiation. Vitam. Horm. 88, 473-489.
22. Gao, N., White, P. and Kaestner, K. H. (2009). Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev. Cell 16, 588-599.
23. Grainger, S., Savory, J. G. A. and Lohnes, D. (2010). Cdx2 regulates patterning of the intestinal epithelium. Dev. Biol. 339, 155-165.
24. Gustafson, T. and Wolpert, L. (1967). Cellular movement and contact in sea urchin morphogenesis. Biol. Rev. 42, 442-498.
25. Holland, P. W. H. (2013). Evolution of homeobox genes. Wiley Interdiscip. Rev. Dev. Biol. 2, 31-45.
26. Howard-Ashby, M., Materna, S. C., Brown, C. T., Chen, L., Cameron, R. A. and Davidson, E. H. (2006). Identification and characterization of homeobox transcription factor genes in Strongylocentrotus purpuratus, and their expression in embryonic development. Dev. Biol. 300, 74-89.
27. Ikuta, T., Chen, Y.-C., Annunziata, R., Ting, H.-C., Tung, C.-H., Koyanagi, R., Tagawa, K., Humphreys, T., Fujiyama, A., Saiga, H. et al. (2013). Identification of an intact ParaHox cluster with temporal colinearity but altered spatial colinearity in the hemichordate Ptychodera flava. BMC Evol. Biol. 13, 129.
28. Jacobs, I. J., Ku, W.-Y. and Que, J. (2012). Genetic and cellular mechanisms regulating anterior foregut and esophageal development. Dev. Biol. 369, 54-64.
29. Kaneto, H., Matsuoka, T.-a., Katakami, N. and Matsuhisa, M. (2009). Combination of MafA, PDX-1 and NeuroD is a useful tool to efficiently induce insulin-producing surrogate beta-cells. Curr. Med. Chem. 16, 3144-3151.
30. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
31. Lee, P. Y. and Davidson, E. H. (2004). Expression of Spgatae, the Strongylocentrotus purpuratus ortholog of vertebrate GATA4/5/6 factors. Gene Expr. Patterns 5, 161-165.
32. Lengyel, J. A. and Iwaki, D. D. (2002). It takes guts: the Drosophila hindgut as a model system for organogenesis. Dev. Biol. 243, 1-19.
33. Lhomond, G., McClay, D. R., Gache, C. and Croce, J. C. (2012). Frizzled1/2/7 signaling directs beta-catenin nuclearisation and initiates endoderm specification in macromeres during sea urchin embryogenesis. Development 139, 816-825.
34. Li, X., Chuang, C.-K., Mao, C.-A., Angerer, L. M. and Klein, W. H. (1997). Two Otx proteins generated from multiple transcripts of a single gene in Strongylocentrotus purpuratus. Dev. Biol. 187, 253-266.
35. Livi, C. B. and Davidson, E. H. (2006). Expression and function of blimp1/krox, an alternatively transcribed regulatory gene of the sea urchin endomesoderm network. Dev. Biol. 293, 513-525.
36. Luo, Y.-J. and Su, Y.-H. (2012). Opposing nodal and BMP signals regulate left-right asymmetry in the sea urchin larva. PLoS Biol. 10, e1001402.
37. Martin, B. L. and Kimelman, D. (2009). Wnt signaling and the evolution of embryonic posterior development. Curr. Biol. 19, R215-R219.
38. McClay, D. R. (2011). Evolutionary crossroads in developmental biology: sea urchins. Development 138, 2639-2648.
39. McGhee, J. D. (2007). The C. elegans intestine. WormBook, 1-36.
40. Minokawa, T., Rast, J. P., Arenas-Mena, C., Franco, C. B. and Davidson, E. H. (2004). Expression patterns of four different regulatory genes that function during sea urchin development. Gene Expr. Patterns 4, 449-456.
41. Nielsen, C. (2008). Six major steps in animal evolution: are we derived sponge larvae? Evol. Dev. 10, 241-257.
42. Offield, M. F., Jetton, T. L., Labosky, P. A., Ray, M., Stein, R. W., Magnuson, M. A., Hogan, B. L. and Wright, C. V. (1996). PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122, 983-995.
43. Oliveri, P. and Davidson, E. H. (2007). Development: built to run, not fail. Science 315, 1510-1511.
44. Oliveri, P., Carrick, D. M. and Davidson, E. H. (2002). A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev. Biol. 246, 209-228.
45. Oliveri, P., Walton, K. D., Davidson, E. H. and McClay, D. R. (2006). Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133, 4173-4181.
46. Osborne, P. W., Benoit, G., Laudet, V., Schubert, M. and Ferrier, D. E. K. (2009). Differential regulation of ParaHox genes by retinoic acid in the invertebrate chordate amphioxus (Branchiostoma floridae). Dev. Biol. 327, 252-262.
47. Peter, I. S. and Davidson, E. H. (2010). The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Dev. Biol. 340, 188-199.
48. Ransick, A., Ernst, S., Britten, R. J. and Davidson, E. H. (1993). Whole mount in situ hybridization shows Endo 16 to be a marker for the vegetal plate territory in sea urchin embryos. Mech. Dev. 42, 117-124.
49. Ransick, A., Rast, J. P., Minokawa, T., Calestani, C. and Davidson, E. H. (2002). New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev. Biol. 246, 132-147.
50. Rast, J. P., Cameron, R. A., Poustka, A. J. and Davidson, E. H. (2002). Brachyury Target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev. Biol. 246, 191-208.
51. Reece-Hoyes, J. S., Keenan, I. D. and Isaacs, H. V. (2002). Cloning and expression of the Cdx family from the frog Xenopus tropicalis. Dev. Dyn. 223, 134-140.
52. Robert, N., Lhomond, G., Schubert, M. and Croce, J. C. (2014). A comprehensive survey of wnt and frizzled expression in the sea urchin Paracentrotus lividus. Genesis 52, 235-250.
53. Roberts, D. J. (2000). Molecular mechanisms of development of the gastrointestinal tract. Dev. Dyn. 219, 109-120.
54. Sherwood, R. I., Maehr, R., Mazzoni, E. O. and Melton, D. A. (2011). Wnt signaling specifies and patterns intestinal endoderm. Mech. Dev. 128, 387-400.
55. Spence, J. R., Lauf, R. and Shroyer, N. F. (2011). Vertebrate intestinal endoderm development. Dev. Dyn. 240, 501-520.
56. Trapnell, C., Pachter, L. and Salzberg, S. L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
57. Tu, Q., Brown, C. T., Davidson, E. H. and Oliveri, P. (2006). Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev. Biol. 300, 49-62.
58. van de Ven, C., Bialecka, M., Neijts, R., Young, T., Rowland, J. E., Stringer, E. J., Van Rooijen, C., Meijlink, F., Novoa, A., Freund, J.-N. et al. (2011). Concerted involvement of Cdx/Hox genes and Wnt signaling in morphogenesis of the caudal neural tube and cloacal derivatives from the posterior growth zone. Development 138, 3451-3462.
59. van den Brink, G. R. (2007). Hedgehog signaling in development and homeostasis of the gastrointestinal tract. Physiol. Rev. 87, 1343-1375.
60. Venuti, J. M., Gan, L., Kozlowski, M. T. and Klein, W. H. (1993). Developmental potential of muscle cell progenitors and the myogenic factor SUM-1 in the sea urchin embryo. Mech. Dev. 41, 3-14.
61. Wolpert, L. (1994). The evolutionary origin of development: cycles, patterning, privilege and continuity. Dev. Suppl. 79-84.
62. Zorn, A. M. and Wells, J. M. (2009). Vertebrate endoderm development and organ formation. Annu. Rev. Cell Dev. Biol. 25, 221-251.