Initial Deployment of the Cardiogenic Gene Regulatory Network in the Basal Chordate, Ciona Intestinalis

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2012 May 19

PMID 22595514

Citations 25

Authors

Arielle Woznica

Maximilian Haeussler

Ella Starobinska

Jessica Jemmett

Younan Li

David Mount

Brad Davidson

Affiliations

Soon will be listed here.

Abstract

The complex, partially redundant gene regulatory architecture underlying vertebrate heart formation has been difficult to characterize. Here, we dissect the primary cardiac gene regulatory network in the invertebrate chordate, Ciona intestinalis. The Ciona heart progenitor lineage is first specified by Fibroblast Growth Factor/Map Kinase (FGF/MapK) activation of the transcription factor Ets1/2 (Ets). Through microarray analysis of sorted heart progenitor cells, we identified the complete set of primary genes upregulated by FGF/Ets shortly after heart progenitor emergence. Combinatorial sequence analysis of these co-regulated genes generated a hypothetical regulatory code consisting of Ets binding sites associated with a specific co-motif, ATTA. Through extensive reporter analysis, we confirmed the functional importance of the ATTA co-motif in primary heart progenitor gene regulation. We then used the Ets/ATTA combination motif to successfully predict a number of additional heart progenitor gene regulatory elements, including an intronic element driving expression of the core conserved cardiac transcription factor, GATAa. This work significantly advances our understanding of the Ciona heart gene network. Furthermore, this work has begun to elucidate the precise regulatory architecture underlying the conserved, primary role of FGF/Ets in chordate heart lineage specification.

Citing Articles

Cell cycle-driven transcriptome maturation confers multilineage competence to cardiopharyngeal progenitors.

Bernadskaya Y, Kuan A, Tjarnberg A, Brandenburg J, Zheng P, Wiechecki K bioRxiv. 2024; .

PMID: 39091743 PMC: 11291048. DOI: 10.1101/2024.07.23.604718.

Gene expression and cellular changes in injured myocardium of .

Stokes S, Palmer P, Barth J, Price R, Parker B, Evans Anderson H Front Cell Dev Biol. 2024; 12:1304755.

PMID: 38544819 PMC: 10965623. DOI: 10.3389/fcell.2024.1304755.

Lhx3/4 initiates a cardiopharyngeal-specific transcriptional program in response to widespread FGF signaling.

Pickett C, Gruner H, Davidson B PLoS Biol. 2024; 22(1):e3002169.

PMID: 38271304 PMC: 10810493. DOI: 10.1371/journal.pbio.3002169.

Single-nucleotide variants within heart enhancers increase binding affinity and disrupt heart development.

Jindal G, Bantle A, Solvason J, Grudzien J, DAntonio-Chronowska A, Lim F Dev Cell. 2023; 58(21):2206-2216.e5.

PMID: 37848026 PMC: 10720985. DOI: 10.1016/j.devcel.2023.09.005.

GATA4/5/6 family transcription factors are conserved determinants of cardiac versus pharyngeal mesoderm fate.

Song M, Yuan X, Racioppi C, Leslie M, Stutt N, Aleksandrova A Sci Adv. 2022; 8(10):eabg0834.

PMID: 35275720 PMC: 8916722. DOI: 10.1126/sciadv.abg0834.

References

Lunn J, Fishwick K, Halley P, Storey K . A spatial and temporal map of FGF/Erk1/2 activity and response repertoires in the early chick embryo. Dev Biol. 2006; 302(2):536-52. DOI: 10.1016/j.ydbio.2006.10.014. View

Davidson B, Shi W, Levine M . Uncoupling heart cell specification and migration in the simple chordate Ciona intestinalis. Development. 2005; 132(21):4811-8. DOI: 10.1242/dev.02051. View

Beh J, Shi W, Levine M, Davidson B, Christiaen L . FoxF is essential for FGF-induced migration of heart progenitor cells in the ascidian Ciona intestinalis. Development. 2007; 134(18):3297-305. DOI: 10.1242/dev.010140. View

Olson E . Gene regulatory networks in the evolution and development of the heart. Science. 2006; 313(5795):1922-7. PMC: 4459601. DOI: 10.1126/science.1132292. View

R Longabaugh W . BioTapestry: a tool to visualize the dynamic properties of gene regulatory networks. Methods Mol Biol. 2011; 786:359-94. DOI: 10.1007/978-1-61779-292-2_21. View

Tsachaki M, Sprecher S . Genetic and developmental mechanisms underlying the formation of the Drosophila compound eye. Dev Dyn. 2011; 241(1):40-56. DOI: 10.1002/dvdy.22738. View

Cooley J, Whitaker S, Sweeney S, Fraser S, Davidson B . Cytoskeletal polarity mediates localized induction of the heart progenitor lineage. Nat Cell Biol. 2011; 13(8):952-7. PMC: 3149722. DOI: 10.1038/ncb2291. View

Christoffels V, Keijser A, Houweling A, Clout D, Moorman A . Patterning the embryonic heart: identification of five mouse Iroquois homeobox genes in the developing heart. Dev Biol. 2000; 224(2):263-74. DOI: 10.1006/dbio.2000.9801. View

Costantini D, Arruda E, Agarwal P, Kim K, Zhu Y, Zhu W . The homeodomain transcription factor Irx5 establishes the mouse cardiac ventricular repolarization gradient. Cell. 2005; 123(2):347-58. PMC: 1480411. DOI: 10.1016/j.cell.2005.08.004. View

10.

Reim I, Frasch M . Genetic and genomic dissection of cardiogenesis in the Drosophila model. Pediatr Cardiol. 2009; 31(3):325-34. DOI: 10.1007/s00246-009-9612-1. View

11.

Niu Z, Li A, Zhang S, Schwartz R . Serum response factor micromanaging cardiogenesis. Curr Opin Cell Biol. 2007; 19(6):618-27. PMC: 2735128. DOI: 10.1016/j.ceb.2007.09.013. View

12.

Peter I, Davidson E . Modularity and design principles in the sea urchin embryo gene regulatory network. FEBS Lett. 2009; 583(24):3948-58. PMC: 2810318. DOI: 10.1016/j.febslet.2009.11.060. View

13.

Bolouri H, Davidson E . The gene regulatory network basis of the "community effect," and analysis of a sea urchin embryo example. Dev Biol. 2009; 340(2):170-8. PMC: 2854306. DOI: 10.1016/j.ydbio.2009.06.007. View

14.

Lemaire P . Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. Dev Biol. 2009; 332(1):48-60. DOI: 10.1016/j.ydbio.2009.05.540. View

15.

Dunwoodie S . Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation. Semin Cell Dev Biol. 2007; 18(1):54-66. DOI: 10.1016/j.semcdb.2006.12.003. View

16.

Erives A . Non-homologous structured CRMs from the Ciona genome. J Comput Biol. 2009; 16(2):369-77. DOI: 10.1089/cmb.2008.20TT. View

17.

Squarzoni P, Parveen F, Zanetti L, Ristoratore F, Spagnuolo A . FGF/MAPK/Ets signaling renders pigment cell precursors competent to respond to Wnt signal by directly controlling Ci-Tcf transcription. Development. 2011; 138(7):1421-32. DOI: 10.1242/dev.057323. View

18.

Vincent S, Buckingham M . How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol. 2010; 90:1-41. DOI: 10.1016/S0070-2153(10)90001-X. View

19.

Khoueiry P, Rothbacher U, Ohtsuka Y, Daian F, Frangulian E, Roure A . A cis-regulatory signature in ascidians and flies, independent of transcription factor binding sites. Curr Biol. 2010; 20(9):792-802. DOI: 10.1016/j.cub.2010.03.063. View

20.

Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A . A cDNA resource from the basal chordate Ciona intestinalis. Genesis. 2002; 33(4):153-4. DOI: 10.1002/gene.10119. View