Home LiteratureArticle Details
PMID: 18498088 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway.

Sirbu IO, Zhao X, Duester G

Abstract

Distinct progenitor cell populations exist in cardiac mesoderm important for patterning of the heart. During heart tube formation in mouse, Tbx5 is expressed in progenitors located more laterally, whereas Isl1 and Fgf8 are expressed in progenitors located more medially. Signals that drive mesodermal progenitors into various cardiac lineages include Fgf8, which functions to induce Isl1. Studies in chick and zebrafish have shown that retinoic acid restricts the number of cardiac progenitors, but its role in mammalian cardiac development is unclear. Here, we demonstrate that Raldh2(-/-) mouse embryos lacking retinoic acid signaling exhibit a posterior expansion of the cardiac Fgf8 expression domain as well as an expansion of Isl1 expression into mesoderm lying posterior to the cardiac field. We provide evidence that retinoic acid acts specifically in the posterior-medial region of the cardiac field to establish the heart posterior boundary potentially by reducing Fgf8 expression which restricts the Isl1 domain.

MeSH Terms
Animals Body Patterning Cell Differentiation Fibroblast Growth Factor 8/metabolism Gene Expression Regulation, Developmental Heart/embryology Homeodomain Proteins/metabolism LIM-Homeodomain Proteins Mesoderm/metabolism Mice Mice, Transgenic Models, Biological Myocardium/pathology Protein Structure, Tertiary Signal Transduction Transcription Factors Tretinoin/metabolism
Chemicals
Fgf8 protein, mouse Homeodomain Proteins LIM-Homeodomain Proteins Transcription Factors insulin gene enhancer binding protein Isl-1 Fibroblast Growth Factor 8 Tretinoin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sirbu Ioan Ovidiu
Burnham Institute for Medical Research, Development and Aging Program, La Jolla, California 92037, USA.
Zhao Xianling
Duester Gregg
References (38)
38 references, click to expand
  1. RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development.
    Genes Dev. 2007 May 1;21(9):1113-24 PMID: 17473173
  2. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar).
    Development. 2000 Jan;127(2):225-35 PMID: 10603341
  3. Building the mammalian heart from two sources of myocardial cells.
    Nat Rev Genet. 2005 Nov;6(11):826-35 PMID: 16304598
  4. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse.
    Development. 2001 Apr;128(7):1019-31 PMID: 11245568
  5. Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm.
    Nat Cell Biol. 2006 Mar;8(3):271-7 PMID: 16489341
  6. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation.
    Cell. 2007 Mar 9;128(5):947-59 PMID: 17350578
  7. The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development.
    Dev Biol. 2007 Nov 15;311(2):297-310 PMID: 17900553
  8. Islet1 cardiovascular progenitors: a single source for heart lineages?
    Development. 2008 Jan;135(2):193-205 PMID: 18156162
  9. Retinoic acid deficiency alters second heart field formation.
    Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):2913-8 PMID: 18287057
  10. Gene regulatory networks in the evolution and development of the heart.
    Science. 2006 Sep 29;313(5795):1922-7 PMID: 17008524
  11. Making or breaking the heart: from lineage determination to morphogenesis.
    Cell. 2006 Sep 22;126(6):1037-48 PMID: 16990131
  12. Crkl deficiency disrupts Fgf8 signaling in a mouse model of 22q11 deletion syndromes.
    Dev Cell. 2006 Jan;10(1):71-80 PMID: 16399079
  13. Retinoid activation of retinoic acid receptor but not retinoid X receptor is sufficient to rescue lethal defect in retinoic acid synthesis.
    Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7135-40 PMID: 12782789
  14. Dynamic patterns of retinoic acid synthesis and response in the developing mammalian heart.
    Dev Biol. 1998 Jul 1;199(1):55-71 PMID: 9676192
  15. Fgf8 is required for anterior heart field development.
    Development. 2006 Jun;133(12):2435-45 PMID: 16720880
  16. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart.
    Dev Cell. 2003 Dec;5(6):877-89 PMID: 14667410
  17. Stimulation of retinoic acid production and growth by ubiquitously expressed alcohol dehydrogenase Adh3.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5337-42 PMID: 11959987
  18. Dose-dependent interaction of Tbx1 and Crkl and locally aberrant RA signaling in a model of del22q11 syndrome.
    Dev Cell. 2006 Jan;10(1):81-92 PMID: 16399080
  19. The outflow tract of the heart is recruited from a novel heart-forming field.
    Dev Biol. 2001 Oct 1;238(1):97-109 PMID: 11783996
  20. Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression.
    Development. 2005 Jun;132(11):2611-22 PMID: 15872003
  21. Induction of normal cardiovascular development in the vitamin A-deprived quail embryo by natural retinoids.
    Dev Biol. 1993 Dec;160(2):424-33 PMID: 8253275
  22. Retinoic acid signaling restricts the cardiac progenitor pool.
    Science. 2005 Jan 14;307(5707):247-9 PMID: 15653502
  23. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease.
    Cell. 2001 Sep 21;106(6):709-21 PMID: 11572777
  24. The developmental genetics of congenital heart disease.
    Nature. 2008 Feb 21;451(7181):943-8 PMID: 18288184
  25. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification.
    Cell. 2006 Dec 15;127(6):1151-65 PMID: 17123592
  26. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed.
    Development. 1999 Oct;126(20):4465-75 PMID: 10498682
  27. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field.
    Development. 2003 Nov;130(22):5363-74 PMID: 13129847
  28. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension.
    Neuron. 2003 Sep 25;40(1):65-79 PMID: 14527434
  29. Effects of retinoid deficiency on the development of the heart and vascular system of the quail embryo.
    Virchows Arch B Cell Pathol Incl Mol Pathol. 1985;50(2):135-52 PMID: 2868561
  30. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice.
    Development. 2002 May;129(9):2271-82 PMID: 11959834
  31. A robust characterization of retinoic acid response elements based on a comparison of sites in three species.
    J Steroid Biochem Mol Biol. 2005 Sep;96(5):347-54 PMID: 16081280
  32. Sequential programs of retinoic acid synthesis in the myocardial and epicardial layers of the developing avian heart.
    Dev Biol. 2000 Mar 1;219(1):129-41 PMID: 10677260
  33. Promoter of FGF8 reveals a unique regulation by unliganded RARalpha.
    J Mol Biol. 2002 Jun 7;319(3):715-28 PMID: 12054865
  34. Conotruncal myocardium arises from a secondary heart field.
    Development. 2001 Aug;128(16):3179-88 PMID: 11688566
  35. Heart field: from mesoderm to heart tube.
    Annu Rev Cell Dev Biol. 2007;23:45-68 PMID: 17456019
  36. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling.
    Development. 2006 Jun;133(12):2419-33 PMID: 16720879
  37. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis.
    Genes Dev. 1991 Aug;5(8):1333-44 PMID: 1907940
  38. Regulation of avian cardiogenesis by Fgf8 signaling.
    Development. 2002 Apr;129(8):1935-43 PMID: 11934859
Article Info
Journal
Developmental dynamics : an official publication of the American Association of Anatomists
Abbr.
Dev Dyn
ISSN
1058-8388
Published
2008-06-00
Pages
1627-35
Language
English
Region
United States
NLM ID
9201927
PMCID
PMC2614402
Subset
IM
Grants
NIGMS NIH HHS · R01 GM062848 · United States
NIGMS NIH HHS · R01 GM062848-06 · United States
NIGMS NIH HHS · GM062848 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]