Requirement for BMP and FGF signaling during cardiogenic induction in non-precardiac mesoderm is specific, transient, and cooperative

Developmental Dynamics

Volumn 218, Issue 2, 2000, Pages 383-393

  Barron, Matthew ^a   Gao, Ming ^a   Lough, John ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Activin A; Alkaline phosphatase; Bone morphogenetic protein; Cardiac specification; Dlx 5; Fibroblast growth factor; GATA 4; Nkx 2.5; Non precardiac mesoderm, serum response factor

Indexed keywords

ACTIVIN A; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; INSULIN; MESSENGER RNA; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EXPLANT; FOWL; HEART DEVELOPMENT; MESODERM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; TISSUE INDUCTION;

BONE MORPHOGENETIC PROTEINS; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYONIC INDUCTION; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 7; FIBROBLAST GROWTH FACTORS; GROWTH SUBSTANCES; HEART; HOMEODOMAIN PROTEINS; MESODERM; NUCLEAR PROTEINS; PHENOTYPE; PROTO-ONCOGENE PROTEINS; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; XENOPUS PROTEINS;

EID: 0034093126     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(200006)218:2<383::AID-DVDY11>3.0.CO;2-P     Document Type: Article

References (45)

1. Andree B, Duprez D, Vorbusch B, Arnold HH, Brand T. 1998. BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech Dev 70:119-131.
2. Antin PB, Yatskievych T, Dominguez JL, Chieffi P. 1996. Regulation of avian precardiac mesoderm development by insulin and insulin-like growth factors. J Cell Physiol 168:42-50.
3. Arai A, Yamamoto K, Toyama J. 1997. Murine cardiac progenitor cells require visceral embryonic endoderm and primitive streak for terminal differentiation. Dev Dyn 210:344-353.
4. Barron M, McAllister D, Smith SM, Lough J. 1998. Expression of retinol binding protein and transthyretin during early embryogenesis. Dev Dyn 212:413-422.
5. Chen CC, Schwartz RJ. 1996. Recruitment of the tinman homologue Nkx-2.5 by serum response factor activates cardiac α-actin gene transcription. Mol Cell Biol 16:6372-6384.
6. Croissant J, Kim J-H, Eichele G, Goering L, Lough J, Prywes R, Schwartz RJ. 1996. Avian serum response factor restricted primarily to muscle cell lineages is required for alpha-actin gene transcription. Dev Biol 177:250-264.
7. Crossley PH, Martin GR. 1995. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121:439-451.
8. Dyson S, Gurdon JB. 1998. The interpretation of position in a morphogen gradient as revealed by occupancy of activin receptors. Cell 93:557-568.
9. Ferrari D, Sumoy L, Gannon J, Sun H, Brown AM, Upholt WB, Kosher RA. 1995. The expression pattern of the Distal-less homeobox-containing gene Dlx-5 in the developing chick limb bud suggests its involvement in apical ectodermal ridge activity, pattern formation, and cartilage differentiation. Mech Dev 52:257-264.
10. Frasch M. 1995. Induction of visceral and cardiac mesoderm by ectodermal dpp in the early Drosophila embryo. Nature 374:464-467.
11. Galvin KM, Donovan MJ, Lynch CA, Meyer RI, Paul RJ, Lorenz JN, Fairchild-Huntress V, Dixon KL, Dunmore JH, Gimbrone MA Jr, Falb D, Huszar D. 2000. A role for smad6 in development and homeostasis of the cardiovascular system. Nat Genet 24:171-174.
12. Garcia-Martinez V, Schoenwolf GC. 1993. Primitive-streak origin of the cardiovascuclar system in avian embryos. Dev Biol 159:706-719.
13. Gordon-Thomson C, Fabian BC. 1994. Hypoblastic tissue and fibroblast growth factor induce blood tissue (haemoglobin) in the early chick embryo. Development 120:3571-3579.
14. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 38:49-92.
15. Inada M, Katagiri T, Akiyama S, Namiki M, Komaki M, Yamaguchi A, Kamoi K, Rosen V, Suda T. 1996. Bone morphogenetic protein-12 and -13 inhibit terminal differentiation of myoblasts, but do not induce their differentiation into osteoblasts. Biochem Biophys Res Comm 222:317-322.
16. Katsev S, Shi Y, Kan D, Evans, SM. 1999. The role of bone morphogenetic protein signaling cascade in xenopus cardiogenesis. Abstract 104798 of the 72d Scientific Sessions of the American Heart Association.
17. A by endoderm cultured from early embryonic chicken. Dev Biol 146:242-245.
18. Ladd AN, Yatskievych TA, Antin PB. 1998. Regulation of avian cardiac myogenesis by activin/TGFβ and bone morphogenetic proteins. Dev Biol 204:407-419.
19. Laverriere AC, MacNeill C, Mueller C, Poelmann RE, Burch JB, Evans T. 1994. GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J Biol Chem 269: 23177-23184.
20. Lough J, Barron M, Brogley M, Sugi Y, Bolender DL, Zhu X. 1996. Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. Dev Biol 178:198-202.
21. Mitrani E, Gruenbaum Y, Shohat H, Ziv T. 1990. Fibroblast growth factor during mesoderm induction in the early chick embryo. Development 109:387-393.
22. Miyama K, Yamada G, Yamamoto TS, Takagi C, Miyado K, Sakai M, Ueno N, Shibuya H. 1999. A BMP-inducible gene, Dlx-5, regulates osteoblast differentiation and mesoderm induction. Development 208:123-133.
23. Moore CS, Mjaatvedt CH, Gearhart JD. 1998. Expression and function of activin beta A during mouse cardiac cushion tissue formation. Dev Dyn 212:548-562.
24. Moss JB, McQuinn TC, Schwartz RJ. 1994. The avian cardiac alpha-actin promoter is regulated through a pair of complex elements composed of E boxes and serum response elements that bind both positive-and negative-binding factors. J Biol Chem 269:12731-12740.
25. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T. 1999. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479-482.
26. Panabieres F, Piechaczyk M, Rainer B, Dani C, Fort P, Riaad S, Marty L, Imbach JL, Jeanteur P, Blanchard JM. 1984. Complete nucleotide sequence of the messenger RNA coding for chicken muscle glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Comm 118:767-773.
27. Parker TG, Chow KL, Schwartz RJ, Schneider MD. 1992. Positive and negative control of the skeletal alpha-actin promoter in cardiac muscle. A proximal serum response element is sufficient for induction by basic fibroblast growth factor (FGF) but not for inhibition by acidic FGF. J Biol Chem 267:3343-3350.
28. Parlow MH, Bolender DL, Kokan-Moore NP, Lough J. 1991. Localization of bFGF-like proteins as punctate inclusions in the pre-septation myocardium of the chicken embryo. Dev Biol 146:139-147.
29. Riese J, Zeller R, Dono R. 1995. Nucleo-cytoplasmic translocation and secretion of fibroblast growth factor-2 during avian gastrulation. Mech Dev 49:13-22.
30. Schultheiss TM, Xydas S, Lassar AB. 1995. Induction of avian cardiac myogenesis by anterior endoderm. Development 121:4203-4214.
31. Schultheiss TM, Burch JBE, Lassar AB. 1997. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev 11:451-462.
32. Shamim H, Mason I. 1999. Expression of FGF4 during early development of the chick embryo. Mech Dev 85:189-192.
33. Sheng Z, Pennica D, Wood WI, Chien KR. 1996. Cardiotrophin-1 displays early expression in the murine heart tube and promotes cardiac myocyte survival. Development 122:419-428.
34. Stern HM, Lin-Jones J, Hauschka SD. 1997. Synergistic interactions between bFGF and a TGF-β family member may mediate signals from the neural tube. Development 124:3511-3523.
35. Stewart AF, Camoretti-Mercado B, Perlman D, Gupta M, Jakovcic S, Zak R. 1991. Structural and phylogenetic analysis of the chicken ventricular myosin heavy chain rod. J Mol Evol 33:357-366.
36. Sugi Y, Lough J. 1994. Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev Dyn 200:155-162.
37. Sugi Y, Lough J. 1995. Activin-A and FGF-2 mimic the inductive effects of anterior endoderm on terminal cardiac myogenesis in vitro. Dev Biol 169:567-574.
38. Sugi Y, Sasse J, Lough J. 1993. Inhibition of precardiac mesoderm cell proliferation by antisense oligodeoxynucleotide complementary to fibroblast growth factor-2 (FGF-2). Dev Biol 157:28-37.
39. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, McQuaid D, Moutsatsos IK, Nove J, Wozney JM. 1990. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224.
40. Yamada M, Szendro PI, Prokscha A, Schwartz RJ, Eichele G. 1999. Evidence for a role of Smad6 in chick cardiac development. Dev Biol 215:48-61
41. Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kahn AJ, Suda T, Yoshiki S. 1991. Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687.
42. Yamazaki Y, Hirakow R. 1991. Factors required for differentiation of chick precardiac mesoderm cultured in vitro. Proc Japan Acad 67:165-169.
43. Yatskievych TA, Ladd AN, Antin PB. 1997. Induction of cardiac myogenesis in avian pregastrula epiblast: the role of the hypoblast and activin. Development 124:2561-2570.
44. Zhang H, Bradley A. 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977-2986.
45. Zhu X, Sasse J, McAllister D, Lough J. 1996. Evidence that fibroblast growth factors 1 and 4 participate in regulation of cardiogenesis. Dev Dyn 207:429-438.