Tcf7l1 proteins cell autonomously restrict cardiomyocyte and promote endothelial specification in zebrafish

Developmental Biology

Volumn 380, Issue 2, 2013, Pages 199-210

  Sorrell, Mollie R J ^a   Dohn, Tracy E ^a   D'Aniello, Enrico ^a   Waxman, Joshua S ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Cardiomyocyte development; Endothelial cell development; Tcf7l1; Wnt signaling; Zebrafish

Indexed keywords

TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR 7 LIKE 1A; TRANSCRIPTION FACTOR 7 LIKE 1B; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYOID BODY; ENDOTHELIUM CELL; GENE REPRESSION; GENETIC TRANSCRIPTION; HEART MUSCLE CELL; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; WNT SIGNALING PATHWAY;

DANIO RERIO; VERTEBRATA;

EID: 84879888802     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.05.016     Document Type: Article

References (61)

1. Alexandrovich A., Arno M., Patient R.K., Shah A.M., Pizzey J.A., Brewer A.C. Wnt2 is a direct downstream target of GATA6 during early cardiogenesis. Mech. Dev. 2006, 123:297-311.
2. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10:468-477.
3. Berdougo E., Coleman H., Lee D.H., Stainier D.Y., Yelon D. Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development 2003, 130:6121-6129.
4. Bonner J., Gribble S.L., Veien E.S., Nikolaus O.B., Weidinger G., Dorsky R.I. Proliferation and patterning are mediated independently in the dorsal spinal cord downstream of canonical Wnt signaling. Dev. Biol. (NY 1985) 2008, 313:398-407.
5. Brannon M., Brown J.D., Bates R., Kimelman D., Moon R.T. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 1999, 126:3159-3170.
6. Brannon M., Gomperts M., Sumoy L., Moon R.T., Kimelman D. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 1997, 11:2359-2370.
7. Chen V.C., Stull R., Joo D., Cheng X., Keller G. Notch signaling respecifies the hemangioblast to a cardiac fate. Nat. Biotechnol. 2008, 26:1169-1178.
8. Cohen E.D., Wang Z., Lepore J.J., Lu M.M., Taketo M.M., Epstein D.J., Morrisey E.E. Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest. 2007, 117:1794-1804.
9. de Pater E., Clijsters L., Marques S.R., Lin Y.F., Garavito-Aguilar Z.V., Yelon D., Bakkers J. Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 2009, 136:1633-1641.
10. Dohn T.E., Waxman J.S. Distinct phases of Wnt/beta-catenin signaling direct cardiomyocyte formation in zebrafish. Dev. Biol. (NY 1985) 2012, 361:364-376.
11. Dorsky R.I., Itoh M., Moon R.T., Chitnis A. Two tcf3 genes cooperate to pattern the zebrafish brain. Development 2003, 130:1937-1947.
12. Dorsky R.I., Sheldahl L.C., Moon R.T. A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev. Biol. (NY 1985) 2002, 241:229-237.
13. Gribble S.L., Kim H.S., Bonner J., Wang X., Dorsky R.I. Tcf3 inhibits spinal cord neurogenesis by regulating sox4a expression. Development 2009, 136:781-789.
14. Guner-Ataman B., Paffett-Lugassy N., Adams M.S., Nevis K.R., Jahangiri L., Obregon P., Kikuchi K., Poss K.D., Burns C.E., Burns C.G. Zebrafish second heart field development relies on progenitor specification in anterior lateral plate mesoderm and nkx2.5 function. Development 2013, 140:1353-1363.
15. Hami D., Grimes A.C., Tsai H.J., Kirby M.L. Zebrafish cardiac development requires a conserved secondary heart field. Development 2011, 138:2389-2398.
16. Hamilton F.S., Wheeler G.N., Hoppler S. Difference in XTcf-3 dependency accounts for change in response to beta-catenin-mediated Wnt signalling in Xenopus blastula. Development 2001, 128:2063-2073.
17. Houston D.W., Kofron M., Resnik E., Langland R., Destree O., Wylie C., Heasman J. Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. Development 2002, 129:4015-4025.
18. Huang C.J., Tu C.T., Hsiao C.D., Hsieh F.J., 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. 2003, 228:30-40.
19. Jin S.W., Beis D., Mitchell T., Chen J.N., Stainier D.Y. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 2005, 132:5199-5209.
20. Keegan B.R., Meyer D., Yelon D. Organization of cardiac chamber progenitors in the zebrafish blastula. Development 2004, 131:3081-3091.
21. Kengaku M., Capdevila J., Rodriguez-Esteban C., De La Pena J., Johnson R.L., Izpisua Belmonte J.C., Tabin C.J. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 1998, 280:1274-1277.
22. Kim C.H., Oda T., Itoh M., Jiang D., Artinger K.B., Chandrasekharappa S.C., Driever W., Chitnis A.B. Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 2000, 407:913-916.
23. Kwon C., Cordes K.R., Srivastava D. Wnt/beta-catenin signaling acts at multiple developmental stages to promote mammalian cardiogenesis. Cell Cycle 2008, 7:3815-3818.
24. Kwon C., Qian L., Cheng P., Nigam V., Arnold J., Srivastava D. A regulatory pathway involving Notch1/beta-catenin/Isl1 determines cardiac progenitor cell fate. Nat. Cell Biol. 2009, 11:951-957.
25. Lazic S., Scott I.C. Mef2cb regulates late myocardial cell addition from a second heart field-like population of progenitors in zebrafish. Dev. Biol. (NY 1985) 2011, 354:123-133.
26. Lekven A.C., Thorpe C.J., Waxman J.S., Moon R.T. Zebrafish wnt8 encodes two wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning. Dev. Cell 2001, 1:103-114.
27. Lewis J.L., Bonner J., Modrell M., Ragland J.W., Moon R.T., Dorsky R.I., Raible D.W. Reiterated Wnt signaling during zebrafish neural crest development. Development 2004, 131:1299-1308.
28. Liu F., Kang I., Park C., Chang L.W., Wang W., Lee D., Lim D.S., Vittet D., Nerbonne J.M., Choi K. ER71 specifies Flk-1+ hemangiogenic mesoderm by inhibiting cardiac mesoderm and Wnt signaling. Blood 2012.
29. Liu F., van den Broek O., Destree O., Hoppler S. Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/beta-catenin signalling in mesoderm development. Development 2005, 132:5375-5385.
30. Mably J.D., Mohideen M.A., Burns C.G., Chen J.N., Fishman M.C. heart of glass regulates the concentric growth of the heart in zebrafish. Curr. Biol. 2003, 13:2138-2147.
31. Mahler J., Filippi A., Driever W. DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signaling during dopaminergic neurogenesis in zebrafish. J. Neurosci.:Off. J. Soc. Neurosci. 2010, 30:16621-16635.
32. Martin B.L., Kimelman D. Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev. Cell 2012, 22:223-232.
33. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., Lassar A.B. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 2001, 15:316-327.
34. Merrill B.J., Gat U., DasGupta R., Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 2001, 15:1688-1705.
35. Merrill B.J., Pasolli H.A., Polak L., Rendl M., Garcia-Garcia M.J., Anderson K.V., Fuchs E. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 2004, 131:263-274.
36. Naito A.T., Shiojima I., Akazawa H., Hidaka K., Morisaki T., Kikuchi A., Komuro I. Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:19812-19817.
37. Oxtoby E., Jowett T. Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 1993, 21:1087-1095.
38. Paige S.L., Osugi T., Afanasiev O.K., Pabon L., Reinecke H., Murry C.E. Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 2010, 5:e11134.
39. Palencia-Desai S., Kohli V., Kang J., Chi N.C., Black B.L., Sumanas S. Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of Etsrp/Etv2 function. Development 2011, 138:4721-4732.
40. Qyang Y., Martin-Puig S., Chiravuri M., Chen S., Xu H., Bu L., Jiang X., Lin L., Granger A., Moretti A., Caron L., Wu X., Clarke J., Taketo M.M., Laugwitz K.L., Moon R.T., Gruber P., Evans S.M., Ding S., Chien K.R. The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 2007, 1:165-179.
41. Robu M.E., Larson J.D., Nasevicius A., Beiraghi S., Brenner C., Farber S.A., Ekker S.C. p53 activation by knockdown technologies. PLoS Genet. 2007, 3:e78.
42. Rochais F., Mesbah K., Kelly R.G. Signaling pathways controlling second heart field development. Circ. Res. 2009, 104:933-942.
43. Rottbauer W., Saurin A.J., Lickert H., Shen X., Burns C.G., Wo Z.G., Kemler R., Kingston R., Wu C., Fishman M. Reptin and pontin antagonistically regulate heart growth in zebrafish embryos. Cell 2002, 111:661-672.
44. Schneider V.A., Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 2001, 15:304-315.
45. Schoenebeck J.J., Keegan B.R., Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev. Cell 2007, 13:254-267.
46. Simoes F.C., Peterkin T., Patient R. Fgf differentially controls cross-antagonism between cardiac and haemangioblast regulators. Development 2011, 138:3235-3245.
47. Sokol S.Y. Maintaining embryonic stem cell pluripotency with Wnt signaling. Development 2011, 138:4341-4350.
48. Stainier D.Y., Fishman M.C. Patterning the zebrafish heart tube: acquisition of anteroposterior polarity. Dev. Biol. 1992, 153:91-101.
49. Stoick-Cooper C.L., Weidinger G., Riehle K.J., Hubbert C., Major M.B., Fausto N., Moon R.T. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134:479-489.
50. Tian Y., Yuan L., Goss A.M., Wang T., Yang J., Lepore J.J., Zhou D., Schwartz R.J., Patel V., Cohen E.D., Morrisey E.E. Characterization and in vivo pharmacological rescue of a Wnt2-Gata6 pathway required for cardiac inflow tract development. Dev. Cell 2010, 18:275-287.
51. Tzahor E. Wnt/beta-catenin signaling and cardiogenesis: timing does matter. Dev. Cell 2007, 13:10-13.
52. Tzahor E., Lassar A.B. Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev. 2001, 15:255-260.
53. Ueno S., Weidinger G., Osugi T., Kohn A.D., Golob J.L., Pabon L., Reinecke H., Moon R.T., Murry C.E. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:9685-9690.
54. Wang H., Gilner J.B., Bautch V.L., Wang D.Z., Wainwright B.J., Kirby S.L., Patterson C. Wnt2 coordinates the commitment of mesoderm to hematopoietic, endothelial, and cardiac lineages in embryoid bodies. J. Biol. Chem. 2007, 282:782-791.
55. Waxman J.S., Keegan B.R., Roberts R.W., Poss K.D., Yelon D. Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev. Cell 2008, 15:923-934.
56. Westerfield M. The Zebrafish Book: A Guide for the Labratory use of Zebrafish (Danio Rerio) 1995, University of Oregon Press. third ed.
57. Wu C.I., Hoffman J.A., Shy B.R., Ford E.M., Fuchs E., Nguyen H., Merrill B.J. Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 2012, 139:2118-2129.
58. Yelon D., Horne S.A., Stainier D.Y. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. (NY 1985) 1999, 214:23-37.
59. Yi F., Merrill B.J. Non-cell-autonomous stimulation of stem cell proliferation following ablation of Tcf3. Exp. Cell Res. 2010, 316:1050-1060.
60. Yi F., Pereira L., Hoffman J.A., Shy B.R., Yuen C.M., Liu D.R., Merrill B.J. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 2011, 13:762-770.
61. Zhou Y., Cashman T.J., Nevis K.R., Obregon P., Carney S.A., Liu Y., Gu A., Mosimann C., Sondalle S., Peterson R.E., Heideman W., Burns C.E., Burns C.G. Latent TGF-beta binding protein 3 identifies a second heart field in zebrafish. Nature 2011, 474:645-648.