BMP signaling coordinates gene expression and cell migration during precardiac mesoderm development

Developmental Biology

Volumn 340, Issue 2, 2010, Pages 179-187

  Christiaen, Lionel ^a,b   Stolfi, Alberto ^a   Levine, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Ascidian; Feedback loop; Kernel; TGF beta; Threshold response

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CHORDIN; GROWTH FACTOR; PROTEIN NK4; TOLLOID METALLOPROTEINASE; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CIONA INTESTINALIS; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; HEART DEVELOPMENT; MESODERM; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ASCIDIA;

EID: 77951205021     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.11.006     Document Type: Article

References (56)

1. Akiyama S., Katagiri T., Namiki M., Yamaji N., Yamamoto N., Miyama K., Shibuya H., Ueno N., Wozney J.M., Suda T. Constitutively active BMP type I receptors transduce BMP-2 signals without the ligand in C2C12 myoblasts. Exp. Cell Res. 1997, 235:362-369.
2. Alvarez A.D., Shi W., Wilson B.A., Skeath J.B. pannier and pointedP2 act sequentially to regulate Drosophila heart development. Development 2003, 130:3015-3026.
3. Ashe H.L., Mannervik M., Levine M. Dpp signaling thresholds in the dorsal ectoderm of the Drosophila embryo. Development 2000, 127:3305-3312.
4. 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, 134:3297-3305.
5. Chanut-Delalande H., Fernandes I., Roch F., Payre F., Plaza S. Shavenbaby couples patterning to epidermal cell shape control. PLoS Biol. 2006, e290:4.
6. Chen Y.G. Endocytic regulation of TGF-beta signaling. Cell Res. 2009, 19:58-70.
7. Chen Y.G., Hata A., Lo R.S., Wotton D., Shi Y., Pavletich N., Massague J. Determinants of specificity in TGF-beta signal transduction. Genes Dev. 1998, 12:2144-2152.
8. Christiaen L., Davidson B., Kawashima T., Powell W., Nolla H., Vranizan K., Levine M. The transcription/migration interface in heart precursors of Ciona intestinalis. Science 2008, 320:1349-1352.
9. Christiaen L., Stolfi A., Davidson B., Levine M. Spatio-temporal intersection of Lhx3 and Tbx6 defines the cardiac field through synergistic activation of Mesp. Dev. Biol. 2009, 328:552-560.
10. Davidson E.H., Erwin D.H. Gene regulatory networks and the evolution of animal body plans. Science 2006, 311:796-800.
11. Davidson B., Levine M. Evolutionary origins of the vertebrate heart: Specification of the cardiac lineage in Ciona intestinalis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:11469-11473.
12. Davidson E.H., Levine M.S. Properties of developmental gene regulatory networks. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20063-20066.
13. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., Minokawa T., Amore G., Hinman V., Arenas-Mena C., Otim O., Brown C.T., Livi C.B., Lee P.Y., Revilla R., Rust A.G., Pan Z., Schilstra M.J., Clarke P.J., Arnone M.I., Rowen L., Cameron R.A., McClay D.R., Hood L., Bolouri H. A genomic regulatory network for development. Science 2002, 295:1669-1678.
14. Davidson B., Shi W., Beh J., Christiaen L., Levine M. FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis. Genes Dev. 2006, 20:2728-2738.
15. Desplan C., Theis J., O'Farrell P.H. The Drosophila developmental gene, engrailed, encodes a sequence-specific DNA binding activity. Nature 1985, 318:630-635.
16. Fortini M.E., Bilder D. Endocytic regulation of Notch signaling. Curr. Opin. Genet. Dev. 2009, 19:323-328.
17. Furlong E.E. Integrating transcriptional and signalling networks during muscle development. Curr. Opin. Genet. Dev. 2004, 14:343-350.
18. Furthauer M., Gonzalez-Gaitan M. Endocytic regulation of Notch signalling during development. Traffic 2009, 10:792-802.
19. Gurdon J.B., Bourillot P.Y. Morphogen gradient interpretation. Nature 2001, 413:797-803.
20. Hirano T., Nishida H. Developmental fates of larval tissues after metamorphosis in ascidian Halocynthia roretzi. I. Origin of mesodermal tissues of the juvenile. Dev. Biol. 1997, 192:199-210.
21. Hoey T., Levine M. Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature 1988, 332:858-861.
22. Hopkins D.R., Keles S., Greenspan D.S. The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol. 2007, 26:508-523.
23. Imai K.S., Hino K., Yagi K., Satoh N., Satou Y. Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 2004, 131:4047-4058.
24. Imai K.S., Levine M., Satoh N., Satou Y. Regulatory blueprint for a chordate embryo. Science 2006, 312:1183-1187.
25. Kadam S., McMahon A., Tzou P., Stathopoulos A. FGF ligands in Drosophila have distinct activities required to support cell migration and differentiation. Development 2009, 136:739-747.
26. Karaulanov E., Knochel W., Niehrs C. Transcriptional regulation of BMP4 synexpression in transgenic Xenopus. EMBO J. 2004, 23:844-856.
27. Klinedinst S.L., Bodmer R. Gata factor Pannier is required to establish competence for heart progenitor formation. Development 2003, 130:3027-3038.
28. Lee K.H., Evans S., Ruan T.Y., Lassar A.B. SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer. Development 2004, 131:4709-4723.
29. Levine M., Davidson E.H. Gene regulatory networks for development. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:4936-4942.
30. Lien C.L., McAnally J., Richardson J.A., Olson E.N. Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev. Biol. 2002, 244:257-266.
31. Lien C.L., Wu C., Mercer B., Webb R., Richardson J.A., Olson E.N. Control of early cardiac-specific transcription of Nkx2-5 by a GATA-dependent enhancer. Development 1999, 126:75-84.
32. Lovegrove B., Simoes S., Rivas M.L., Sotillos S., Johnson K., Knust E., Jacinto A., Hombria J.C. Coordinated control of cell adhesion, polarity, and cytoskeleton underlies Hox-induced organogenesis in Drosophila. Curr. Biol. 2006, 16:2206-2216.
33. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
34. McGinnis W., Levine M.S., Hafen E., Kuroiwa A., Gehring W.J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 1984, 308:428-433.
35. Miyazono K. Positive and negative regulation of TGF-beta signaling. J. Cell. Sci. 2000, 113(Pt 7):1101-1109.
36. Namiki M., Akiyama S., Katagiri T., Suzuki A., Ueno N., Yamaji N., Rosen V., Wozney J.M., Suda T. A kinase domain-truncated type I receptor blocks bone morphogenetic protein-2-induced signal transduction in C2C12 myoblasts. J. Biol. Chem. 1997, 272:22046-22052.
37. Nusslein-Volhard C., Wieschaus E. Mutations affecting segment number and polarity in Drosophila. Nature 1980, 287:795-801.
38. Olson E.N. Gene regulatory networks in the evolution and development of the heart. Science 2006, 313:1922-1927.
39. Pasini A., Amiel A., Rothbacher U., Roure A., Lemaire P., Darras S. Formation of the ascidian epidermal sensory neurons: insights into the origin of the chordate peripheral nervous system. PLoS Biol. 2006, e225:4.
40. Prall O.W., Menon M.K., Solloway M.J., Watanabe Y., Zaffran S., Bajolle F., Biben C., McBride J.J., Robertson B.R., Chaulet H., Stennard F.A., Wise N., Schaft D., Wolstein O., Furtado M.B., Shiratori H., Chien K.R., Hamada H., Black B.L., Saga Y., Robertson E.J., Buckingham M.E., Harvey R.P. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 2007, 128:947-959.
41. Rhee J.M., Oda-Ishii I., Passamaneck Y.J., Hadjantonakis A.K., Di Gregorio A. Live imaging and morphometric analysis of embryonic development in the ascidian Ciona intestinalis. Genesis 2005, 43:136-147.
42. Rojas A., De Val S., Heidt A.B., Xu S.M., Bristow J., Black B.L. Gata4 expression in lateral mesoderm is downstream of BMP4 and is activated directly by Forkhead and GATA transcription factors through a distal enhancer element. Development 2005, 132:3405-3417.
43. Satou Y., Imai K.S., Satoh N. The ascidian Mesp gene specifies heart precursor cells. Development 2004, 131:2533-2541.
44. Satou Y., Satoh N. Cataloging transcription factor and major signaling molecule genes for functional genomic studies in Ciona intestinalis. Dev. Genes Evol. 2005, 215:580-596.
45. Satou Y., Kawashima T., Shoguchi E., Nakayama A., Satoh N. An integrated database of the ascidian, Ciona intestinalis: towards functional genomics. Zoolog Sci. 2005, 22:837-843.
46. Searcy R.D., Vincent E.B., Liberatore C.M., Yutzey K.E. A GATA-dependent nkx-2.5 regulatory element activates early cardiac gene expression in transgenic mice. Development 1998, 125:4461-4470.
47. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
48. Simeoni I., Gurdon J.B. Interpretation of BMP signaling in early Xenopus development. Dev. Biol. 2007, 308:82-92.
49. Smith K.A., Chocron S., von der Hardt S., de Pater E., Soufan A., Bussmann J., Schulte-Merker S., Hammerschmidt M., Bakkers J. Rotation and asymmetric development of the zebrafish heart requires directed migration of cardiac progenitor cells. Dev. Cell 2008, 14:287-297.
50. Stathopoulos A., Levine M. Genomic regulatory networks and animal development. Dev. Cell 2005, 9:449-462.
51. Tassy O., Daian F., Hudson C., Bertrand V., Lemaire P. A quantitative approach to the study of cell shapes and interactions during early chordate embryogenesis. Curr. Biol. 2006, 16:345-358.
52. von der Hardt S., Bakkers J., Inbal A., Carvalho L., Solnica-Krezel L., Heisenberg C.P., Hammerschmidt M. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 2007, 17:475-487.
53. Wharton S.J., Basu S.P., Ashe H.L. Smad affinity can direct distinct readouts of the embryonic extracellular Dpp gradient in Drosophila. Curr. Biol. 2004, 14:1550-1558.
54. Wiley H.S., Burke P.M. Regulation of receptor tyrosine kinase signaling by endocytic trafficking. Traffic 2001, 2:12-18.
55. Zaffran S., Frasch M. Early signals in cardiac development. Circ. Res. 2002, 91:457-469.
56. Zaffran S., Kuchler A., Lee H.H., Frasch M. biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev. 2001, 15:2900-2915.