Differential requirement for BMP signaling in atrial and ventricular lineages establishes cardiac chamber proportionality

Developmental Biology

Volumn 328, Issue 2, 2009, Pages 472-482

  Marques, Sara R ^a,b   Yelon, Deborah ^a  

^a Center for Biology and Medicine of the Skirball Inst of Biomolecular Medicine   (United States)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

Alk8; Atrium; BMP; Chamber formation; Ventricle; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELL TYPE; CONTROLLED STUDY; EMBRYO; GENE MUTATION; HEART ATRIUM; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART SIZE; HEART VENTRICLE; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR GENE; SIGNAL TRANSDUCTION; ZEBRA FISH;

DANIO RERIO;

EID: 63549094184     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.02.010     Document Type: Article

References (78)

1. Auman H.J., Coleman H., Riley H.E., Olale F., Tsai H.J., and Yelon D. Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 5 (2007) e53
2. Bauer H., Lele Z., Rauch G.J., Geisler R., and Hammerschmidt M. The type I serine/threonine kinase receptor Alk8/Lost-a-fin is required for Bmp2b/7 signal transduction during dorsoventral patterning of the zebrafish embryo. Development 128 (2001) 849-858
3. Berdougo E., Coleman H., Lee D.H., Stainier D.Y., and Yelon D. Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development 130 (2003) 6121-6129
4. Branford W.W., Essner J.J., and Yost H.J. Regulation of gut and heart left-right asymmetry by context-dependent interactions between Xenopus lefty and BMP4 signaling. Dev. Biol. 223 (2000) 291-306
5. Brown L.A., Amores A., Schilling T.F., Jowett T., Baert J.L., de Launoit Y., and Sharrocks A.D. Molecular characterization of the zebrafish PEA3 ETS-domain transcription factor. Oncogene 17 (1998) 93-104
6. Bruneau B.G. Transcriptional regulation of vertebrate cardiac morphogenesis. Circ. Res. 90 (2002) 509-519
7. Buckingham M., Meilhac S., and Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6 (2005) 826-835
8. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., and Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5 (2003) 877-889
9. Chen J.N., and Fishman M.C. Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 122 (1996) 3809-3816
10. Chen Y., and Schier A.F. Lefty proteins are long-range inhibitors of squint-mediated nodal signaling. Curr. Biol. 12 (2002) 2124-2128
11. Chocron S., Verhoeven M.C., Rentzsch F., Hammerschmidt M., and Bakkers J. Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev. Biol. 305 (2007) 577-588
12. Délot E.C., Bahamonde M.E., Zhao M., and Lyons K.M. BMP signaling is required for septation of the outflow tract of the mammalian heart. Development 130 (2003) 209-220
13. Dick A., Meier A., and Hammerschmidt M. Smad1 and Smad5 have distinct roles during dorsoventral patterning of the zebrafish embryo. Dev. Dyn. 216 (1999) 285-298
14. Dick A., Hild M., Bauer H., Imai Y., Maifeld H., Schier A.F., Talbot W.S., Bouwmeester T., and Hammerschmidt M. Essential role of Bmp7 (snailhouse) and its prodomain in dorsoventral patterning of the zebrafish embryo. Development 127 (2000) 343-354
15. Dunwoodie S.L. Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation. Semin. Cell Dev. Biol. 18 (2007) 54-66
16. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374 (1995) 464-467
17. Fürthauer M., Thisse C., and Thisse B. A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124 (1997) 4253-4264
18. Gritsman K., Zhang J., Cheng S., Heckscher E., Talbot W.S., and Schier A.F. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97 (1999) 121-132
19. Hild M., Dick A., Rauch G.J., Meier A., Bouwmeester T., Haffter P., and Hammerschmidt M. The smad5 mutation somitabun blocks Bmp2b signaling during early dorsoventral patterning of the zebrafish embryo. Development 126 (1999) 2149-2159
20. Ho R.K., and Kane D.A. Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors. Nature 348 (1990) 728-730
21. Hochgreb T., Linhares V.L., Menezes D.C., Sampaio A.C., Yan C.Y., Cardoso W.V., Rosenthal N., and Xavier-Neto J. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 130 (2003) 5363-5374
22. Hogan B.M., Layton J.E., Pyati U.J., Nutt S.L., Hayman J.W., Varma S., Heath J.K., Kimelman D., and Lieschke G.J. Specification of the primitive myeloid precursor pool requires signaling through Alk8 in zebrafish. Curr. Biol. 16 (2006) 506-511
23. Huang C.J., Tu C.T., Hsiao C.D., Hsieh F.J., and Tsai H.J. Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228 (2003) 30-40
24. Keegan B.R., Meyer D., and Yelon D. Organization of cardiac chamber progenitors in the zebrafish blastula. Development 131 (2004) 3081-3091
25. Kelly R.G., Brown N.A., and Buckingham M.E. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1 (2001) 435-440
26. Kimmel C.B., Warga R.M., and Schilling T.F. Origin and organization of the zebrafish fate map. Development 108 (1990) 581-594
27. Kishimoto Y., Lee K.H., Zon L., Hammerschmidt M., and Schulte-Merker S. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124 (1997) 4457-4466
28. Klaus A., Saga Y., Taketo M.M., Tzahor E., and Birchmeier W. Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 18531-18536
29. Kondo M. Bone morphogenetic proteins in the early development of zebrafish. FEBS J. 274 (2007) 2960-2967
30. Lee K.H., Evans S., Ruan T.Y., and 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 131 (2004) 4709-4723
31. Liberatore C.M., Searcy-Schrick R.D., Vincent E.B., and Yutzey K.E. Nkx-2.5 gene induction in mice is mediated by a Smad consensus regulatory region. Dev. Biol. 244 (2002) 243-256
32. Lien C.L., McAnally J., Richardson J.A., and Olson E.N. Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev. Biol. 244 (2002) 257-266
33. Liu W., Selever J., Wang D., Lu M.F., Moses K.A., Schwartz R.J., and Martin J.F. Bmp4 signaling is required for outflow-tract septation and branchial-arch artery remodeling. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 4489-4494
34. Mably J.D., Mohideen M.A., Burns C.G., Chen J.N., and Fishman M.C. heart of glass regulates the concentric growth of the heart in zebrafish. Curr. Biol. 13 (2003) 2138-2147
35. Marques S.R., Lee Y., Poss K.D., and Yelon D. Reiterative roles for FGF signaling in the establishment of size and proportion of the zebrafish heart. Dev. Biol. 321 (2008) 397-406
36. Martínez-Barberá J.P., Toresson H., Da Rocha S., and Krauss S. Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene 198 (1997) 53-59
37. Meilhac S.M., Esner M., Kelly R.G., Nicolas J.F., and Buckingham M.E. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell 6 (2004) 685-698
38. Mine N., Anderson R.M., and Klingensmith J. BMP antagonism is required in both the node and lateral plate mesoderm for mammalian left-right axis establishment. Development 135 (2008) 2425-2434
39. Mintzer K.A., Lee M.A., Runke G., Trout J., Whitman M., and Mullins M.C. Lost-a-fin encodes a type I BMP receptor, Alk8, acting maternally and zygotically in dorsoventral pattern formation. Development 128 (2001) 859-869
40. Moorman A.F., and Christoffels V.M. Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83 (2003) 1223-1267
41. Müller F., Blader P., Rastegar S., Fischer N., Knöchel W., and Strähle U. Characterization of zebrafish smad1, smad2 and smad5: the amino-terminus of smad1 and smad5 is required for specific function in the embryo. Mech. Dev. 88 (1999) 73-88
42. Mullins M.C., Hammerschmidt M., Kane D.A., Odenthal J., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Haffter P., Heisenberg C.P., Jiang Y.J., Kelsh R.N., and Nüsslein-Volhard C. Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123 (1996) 81-93
43. Nakajima Y., Yamagishi T., Ando K., and Nakamura H. Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Dev. Biol. 245 (2002) 291-303
44. Nguyen V.H., Schmid B., Trout J., Connors S.A., Ekker M., and Mullins M.C. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev. Biol. 199 (1998) 93-110
45. Nusslein-Volhard C., and Dahm R. Zebrafish, A Practical Approach (2002), Oxford University Press
46. Parker L., and Stainier D.Y. Cell-autonomous and non-autonomous requirements for the zebrafish gene cloche in hematopoiesis. Development 126 (1999) 2643-2651
47. 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., and Harvey R.P. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128 (2007) 947-959
48. Pyati U.J., Webb A.E., and Kimelman D. Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132 (2005) 2333-2343
49. Pyati U.J., Cooper M.S., Davidson A.J., Nechiporuk A., and Kimelman D. Sustained Bmp signaling is essential for cloaca development in zebrafish. Development 133 (2006) 2275-2284
50. Reifers F., Walsh E.C., Léger S., Stainier D.Y., and Brand M. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development 127 (2000) 225-235
51. Reiter J.F., Verkade H., and Stainier D.Y. Bmp2b and Oep promote early myocardial differentiation through their regulation of gata5. Dev. Biol. 234 (2001) 330-338
52. Rohr S., Otten C., and Abdelilah-Seyfried S. Asymmetric involution of the myocardial field drives heart tube formation in zebrafish. Circ. Res. 102 (2008) e9-e12
53. Schlange T., Andrée B., Arnold H.H., and Brand T. BMP2 is required for early heart development during a distinct time period. Mech. Dev. 91 (2000) 259-270
54. Schoenebeck J.J., Keegan B.R., and Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev. Cell 13 (2007) 254-267
55. Schultheiss T.M., Burch J.B., and Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11 (1997) 451-462
56. Scott I.C., Masri B., D'Amico L.A., Jin S.W., Jungblut B., Wehman A.M., Baier H., Audigier Y., and Stainier D.Y. The g protein-coupled receptor agtrl1b regulates early development of myocardial progenitors. Dev. Cell 12 (2007) 403-413
57. Shi Y., Katsev S., Cai C., and Evans S. BMP signaling is required for heart formation in vertebrates. Dev. Biol. 224 (2000) 226-237
58. Smith K.A., Chocron S., von der Hardt S., de Pater E., Soufan A., Bussmann J., Schulte-Merker S., Hammerschmidt M., and Bakkers J. Rotation and asymmetric development of the zebrafish heart requires directed migration of cardiac progenitor cells. Dev. Cell 14 (2008) 287-297
59. Solloway M.J., and Robertson E.J. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126 (1999) 1753-1768
60. Stainier D.Y., Lee R.K., and Fishman M.C. Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. Development 119 (1993) 31-40
61. Stickney H.L., Imai Y., Draper B., Moens C., and Talbot W.S. Zebrafish bmp4 functions during late gastrulation to specify ventroposterior cell fates. Dev. Biol. 310 (2007) 71-84
62. Stottmann R.W., Choi M., Mishina Y., Meyers E.N., and Klingensmith J. BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131 (2004) 2205-2218
63. Sugi Y., Yamamura H., Okagawa H., and Markwald R.R. Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev. Biol. 269 (2004) 505-518
64. Thomas N.A., Koudijs M., van Eeden F.J., Joyner A.L., and Yelon D. Hedgehog signaling plays a cell-autonomous role in maximizing cardiac developmental potential. Development 135 (2008) 3789-3799
65. Tucker J.A., Mintzer K.A., and Mullins M.C. The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev. Cell 14 (2008) 108-119
66. van Wijk B., Moorman A.F., and van den Hoff M.J. Role of bone morphogenetic proteins in cardiac differentiation. Cardiovasc. Res. 74 (2007) 244-255
67. von der Hardt S., Bakkers J., Inbal A., Carvalho L., Solnica-Krezel L., Heisenberg C.P., and Hammerschmidt M. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 17 (2007) 475-487
68. Waxman J.S., Keegan B.R., Roberts R.W., Poss K.D., and Yellon D. Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev. Cell 15 (2008) 923-934
69. Wieser R., Wrana J.L., and Massagué J. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J. 14 (1995) 2199-2208
70. Xavier-Neto J., Rosenthal N., Silva F.A., Matos T.G., Hochgreb T., and Linhares V.L. Retinoid signaling and cardiac anteroposterior segmentation. Genesis 31 (2001) 97-104
71. Yelick P.C., Abduljabbar T.S., and Stashenko P. zALK-8, a novel type I serine/threonine kinase receptor, is expressed throughout early zebrafish development. Dev. Dyn. 211 (1998) 352-361
72. Yelon D., Horne S.A., and Stainier D.Y. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214 (1999) 23-37
73. Yelon D., Ticho B., Halpern M.E., Ruvinsky I., Ho R.K., Silver L.M., and Stainier D.Y. The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127 (2000) 2573-2582
74. Yin Z., and Frasch M. Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. Dev. Genet. 22 (1998) 187-200
75. Yu P.B., Hong C.C., Sachidanandan C., Babitt J.L., Deng D.Y., Hoyng S.A., Lin H.Y., Bloch K.D., and Peterson R.T. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4 (2008) 33-41
76. Zaffran S., and Frasch M. Early signals in cardiac development. Circ. Res. 91 (2002) 457-469
77. Zeng X.X., Wilm T.P., Sepich D.S., and Solnica-Krezel L. Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev. Cell 12 (2007) 391-402
78. Zhang H., and Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122 (1996) 2977-2986