Wnt signal transduction and the formation of the myocardium

Developmental Biology

Volumn 293, Issue 2, 2006, Pages 305-315

  Eisenberg, Leonard M ^a   Eisenberg, Carol A ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cardiac development; Dickkopf; Frizzled related proteins; Heart fields; Myocardium; Wnt

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FRIZZLED PROTEIN; PROTEIN INHIBITOR; WNT PROTEIN;

BIRD; DROSOPHILA; EMBRYO DEVELOPMENT; EPICARDIUM; EXPERIMENTAL MOUSE; FROG; GASTRULATION; HEART DEVELOPMENT; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; HYPOTHESIS; MAMMAL; MOLECULAR BIOLOGY; MOLECULE; MORPHOGENESIS; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPECIES COMPARISON; UPREGULATION; XENOPUS LAEVIS;

ANURA; AVES; MAMMALIA; VERTEBRATA; XENOPUS LAEVIS;

EID: 33646203964     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.02.014     Document Type: Review

References (112)

1. Ai Z.W., Fischer A., Spray D.C., Brown A.M.C., and Fishman G.I. Wnt-1 regulation of connexin43 in cardiac myocytes. J. Clin. Invest. 105 (2000) 161-171
2. Bafico A., Gazit A., Pramila T., Finch P.W., Yaniv A., and Aaronson S.A. Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J. Biol. Chem. 274 (1999) 16180-16187
3. Bafico A., Liu G., Yaniv A., Gazit A., and Aaronson S.A. Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat. Cell Biol. 3 (2001) 683-686
4. Baranski M., Berdougo E., Sandler J.S., Darnell D.K., and Burrus L.W. The dynamic expression pattern of frzb-1 suggests multiple roles in chick development. Dev. Biol. 217 (2000) 25-41
5. Bejsovec A. Wnt pathway activation: new relations and locations. Cell 120 (2005) 11-14
6. Bond J., Sedmera D., Jourdan J., Zhang Y., Eisenberg C.A., Eisenberg L.M., and Gourdie R.G. Wnt11 and Wnt7a are up-regulated in association with differentiation of cardiac conduction cells in vitro and in vivo. Dev. Dyn. 227 (2003) 536-543
7. Bouillet P., Ouladabdelghani M., Ward S.J., Bronner S., Chambon P., and Dolle P. A new mouse member of the WNT gene family, mWNT-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid. Mech. Dev. 58 (1996) 141-152
8. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol. 258 (2003) 1-19
9. Brott B.K., and Sokol S.Y. A vertebrate homolog of the cell cycle regulator Dbf4 is an inhibitor of Wnt signaling required for heart development. Dev. Cell 8 (2005) 703-715
10. 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
11. Chapman S.C., Brown R., Lees L., Schoenwolf G.C., and Lumsden A. Expression analysis of chick Wnt and frizzled genes and selected inhibitors in early chick patterning. Dev. Dyn. 229 (2004) 668-676
12. Christian J.L., and Moon R.T. Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 7 (1993) 13-28
13. Christiansen J.H., Dennis C.L., Wicking C.A., Monkley S.J., Wilkinson D.G., and Wainwright B.J. Murine wnt-11 and wnt-12 have temporally and spatially restricted expression patterns during embryonic development. Mech. Dev. 51 (1995) 341-350
14. Davidson G., Mao B., del Barco Barrantes I., and Niehrs C. Kremen proteins interact with Dickkopf1 to regulate anteroposterior CNS patterning. Development 129 (2002) 5587-5596
15. Du S.J., Purcell S.M., Christian J.L., McGrew L.L., and Moon R.T. Identification of distinct classes and functional domains of wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Mol. Cell. Biol. 15 (1995) 2625-2634
16. Duprez D., Leyns L., Bonnin M.-A., Lapointe F., Etchevers H., Robertis E.M.D., and Douarin N.L. Expression of Frzb-1 during chick development. Mech. Dev. 89 (1999) 179-183
17. Eisenberg C.A., and Eisenberg L.M. WNT11 promotes cardiac tissue formation of early mesoderm. Dev. Dyn. 216 (1999) 45-58
18. Eisenberg L.M., and Eisenberg C.A. Onset of a cardiac phenotype in the early embryo. In: Dube D.K. (Ed). Cardiovascular Molecular Morphogenesis: Myofibrillogenesis (2002), Springer Verlag, New York, NY 181-205
19. Eisenberg L.M., and Eisenberg C.A. An in vitro analysis of myocardial potential indicates that phenotypic plasticity is an innate property of early embryonic tissue. Stem Cells Dev. 13 (2004) 614-624
20. Eisenberg L.M., and Markwald R.R. Cellular recruitment and the development of the myocardium. Dev. Biol. 274 (2004) 225-232
21. Eisenberg C.A., Gourdie R.G., and Eisenberg L.M. Wnt11 is expressed in early avian mesoderm and required for the differentiation of the quail mesoderm cell line QCE6. Development 124 (1997) 525-536
22. Eisenberg L.M., Moreno R., and Markwald R.R. Multiple stem cell populations contribute to the formation of the myocardium. Ann. N. Y. Acad. Sci. 1047 (2005) 38-49
23. Esteve P., Morcillo J., and Bovolenta P. Early and dynamic expression of cSfrp1 during chick embryo development. Mech. Dev. 97 (2000) 217-221
24. Fanto M., and McNeill H. Planar polarity from flies to vertebrates. J. Cell Sci. 117 (2004) 527-533
25. Foley A., and Mercola M. Heart induction: embryology to cardiomyocyte regeneration. Trends Cardiovasc. Med. 14 (2004) 121-125
26. Garriock R.J., D'Agostino S.L., Pilcher K.C., and Krieg P.A. Wnt11-R, a protein closely related to mammalian Wnt11, is required for heart morphogenesis in Xenopus. Dev. Biol. 279 (2005) 179-192
27. Gitler A.D., Lu M.M., Jiang Y.Q., Epstein J.A., and Gruber P.J. Molecular markers of cardiac endocardial cushion development. Dev. Dyn. 228 (2003) 643-650
28. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., and Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391 (1998) 357-362
29. He X., Saint-Jeannet J.-P., Wang Y., Nathans J., Dawid I., and Varmus H. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275 (1997) 1652-1654
30. He X., Semenov M., Tamai K., and Zeng X. LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development 131 (2004) 1663-1677
31. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., and Wilson S.W. Silberblick/Wnt-11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 (2000) 76-81
32. Hoang B.H., Thomas J.T., Abdulkarim F.W., Correia K.M., Conlon R.A., Luyten F.P., and Ballock R.T. Expression pattern of two frizzled-related genes, frzb-1 and sfrp-1, during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev. Dyn. 212 (1998) 364-372
33. Huang H.C., and Klein P.S. The Frizzled family: receptors for multiple signal transduction pathways. Genome Biol. 5 (2004) 234
34. Hume C.R., and Dodd J. Cwnt-8C: a novel Wnt gene with a potential role in primitive streak formation and hindbrain organization. Development 119 (1993) 1147-1160
35. Jasoni C., Hendrickson A., and Roelink H. Analysis of chicken Wnt-13 expression demonstrates coincidence with cell division in the developing eye and is consistent with a role in induction. Dev. Dyn. 215 (1999) 215-224
36. Jaspard B., Couffinhal T., Dufourcq P., Moreau C., and Duplaa C. Expression pattern of mouse sFRP-1 and mWnt-8 gene during heart morphogenesis. Mech. Dev. 90 (2000) 263-267
37. Karasawa T., Yokokura H., Kitajewski J., and Lombroso P.J. Frizzled-9 is activated by Wnt-2 and functions in Wnt/beta-catenin signaling. J. Biol. Chem. 277 (2002) 37479-37486
38. Kawano Y., and Kypta R. Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116 (2003) 2627-2634
39. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298 (2002) 1950-1954
40. Kispert A., Vainio S., Shen L., Rowitch D.H., and McMahon A.P. Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122 (1996) 3627-3637
41. Koyanagi M., Haendeler J., Badorff C., Brandes R.P., Hoffmann J., Pandur P., Zeiher A.M., Kühl M., and Dimmeler S. Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J. Biol. Chem. 280 (2005) 16838-16842
42. Ku M., and Melton D. Xwnt-11: a maternally expressed Xenopus Wnt gene. Development 119 (1993) 1161-1173
43. Kühl M. The WNT/calcium pathway: biochemical mediators, tools and future requirements. Front. Biosci. 9 (2004) 967-974
44. 2+ signaling. Mech. Dev. 106 (2001) 61-76
45. Ladher R.K., Church V.L., Allen S., Robson L., Abdelfattah A., Brown N.A., Hattersley G., Rosen V., Luyten F.P., Dale L., and Francis-West P.H. Cloning and expression of the Wnt antagonists Sfrp-2 and Frzb during chick development. Dev. Biol. 218 (2000) 183-198
46. Lickert H., Kutsch S., Kanzler B., Tamai Y., Taketo M.M., and Kemler R. Formation of multiple hearts in mice following deletion of β-catenin in the embryonic endoderm. Dev. Cell 3 (2002) 171-181
47. Liebner S., Cattelino A., Gallini R., Rudini N., Iurlaro M., Piccolo S., and Dejana E. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J. Cell Biol. 166 (2004) 359-367
48. Lin K.M., Wang S.W., Julius M.A., Kitajewski J., Moos M., and Luyten F.P. The cysteine-rich frizzled domain of Frzb-1 is required and sufficient for modulation of Wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 11196-11200
49. Linker C., Lesbros C., Gros J., Burrus L.W., Rawls A., and Marcelle C. ß-catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of paraxis. Development 132 (2005) 3895-3905
50. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., and Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22 (1999) 361-365
51. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
52. Luo W., and Lin S.C. Axin: a master scaffold for multiple signaling pathways. NeuroSignals 13 (2004) 99-113
53. Lyons J.P., Mueller U.W., Ji H., Everett C., Fang X., Hsieh J.C., Barth A.M., and McCrea P.D. Wnt-4 activates the canonical beta-catenin-mediated Wnt pathway and binds Frizzled-6 CRD: functional implications of Wnt/beta-catenin activity in kidney epithelial cells. Exp. Cell Res. 298 (2004) 369-387
54. Mao B., and Niehrs C. Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene 302 (2003) 179-183
55. Mao B., Wu W., Li Y., Hoppe D., Stannek P., Glinka A., and Niehrs C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411 (2001) 321-325
56. Mao J., Wang J., Liu B., Pan W., Farr III G., Flynn C., Yuan H., Takada S., Kimelman D., Li L., and Wu D. Low-density lipoprotein receptor-related Protein-5 binds to axin and regulates the canonical Wnt signalling pathway. Mol. Cell 7 (2001) 801-809
57. Mao B., Wu W., Davidson G., Marhold J., Li M., Mechler B.M., Delius H., Hoppe D., Stannek P., Walter C., Glinka A., and Niehrs C. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 417 (2002) 664-667
58. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., and Lassar A.B. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 15 (2001) 316-327
59. Matsui T., Raya A., Kawakami Y., Callol-Massot C., Capdevila J., Rodriguez-Esteban C., and Izpisua Belmonte J.C. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 19 (2005) 164-175
60. Maurus D., Heligon C., Burger-Schwarzler A., Brandli A.W., and Kühl M. Noncanonical Wnt-4 signaling and EAF2 are required for eye development in Xenopus laevis. EMBO J. 24 (2005) 1181-1191
61. Maye P., Zheng J., Li L., and Wu D. Multiple mechanisms for Wnt11-mediated repression of the canonical Wnt signaling pathway. J. Biol. Chem. 279 (2004) 24659-24665
62. Mohun T., Orford R., and Shang C. The origins of cardiac tissue in the amphibian, Xenopus laevis. Trends Cardiovasc. Med. 13 (2003) 244-248
63. Monaghan A.P., Kioschis P., Wu W., Zuniga A., Bock D., Poustka A., Delius H., and Niehrs C. Dickkopf genes are co-ordinately expressed in mesodermal lineages. Mech. Dev. 87 (1999) 45-56
64. Monkley S.J., Delaney S.J., Pennisi D.J., Christiansen J.H., and Wainwright B.J. Targeted disruption of the Wnt2 gene results in placentation defects. Development 122 (1996) 3343-3353
65. Moon R.T., Campbell R.M., Christian J.L., McGrew L.L., Shih J., and Fraser S. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119 (1993) 97-111
66. Moon R.T., Brown J.D., and Torres M. WNTs modulate cell fate and behavior during vertebrate development. Trends Genet. 13 (1997) 157-162
67. Moon R.T., Kohn A.D., De Ferrari G.V., and Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat. Rev., Genet. 5 (2004) 691-701
68. Naito A.T., Akazawa H., Takano H., Minamino T., Nagai T., Aburatani H., and Komuro I. Phosphatidylinositol 3-kinase-Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical Wnt signaling. Circ. Res. 97 (2005) 144-151
69. Nakamura T., Sano M., Songyang Z., and Schneider M.D. A Wnt- and ß-catenin-dependent pathway for mammalian cardiac myogenesis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5834-5839
70. Olson E.N. Development-The path to the heart and the road not taken. Science 291 (2001) 2327-2328
71. Pandur P. What does it take to make a heart?. Biol. Cell 97 (2005) 197-210
72. Pandur P., Läsche M., Eisenberg L.M., and Kühl M. Wnt-11 activation of a non-canonical Wnt signaling pathway is required for cardiogenesis. Nature 418 (2002) 636-641
73. Park M., and Moon R.T. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol. 4 (2002) 20-25
74. Park M., Wu X., Golden K., Axelrod J.D., and Bodmer R. The Wingless signaling pathway is directly involved in Drosophila heart development. Dev. Biol. 177 (1996) 104-116
75. Pera E.M., and De Robertis E.M. A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1. Mech. Dev. 96 (2000) 183-195
76. Person A.D., Garriock R.J., Krieg P.A., Runyan R.B., and Klewer S.E. Frzb modulates Wnt-9a-mediated ß-catenin signaling during avian atrioventricular cardiac cushion development. Dev. Biol. 278 (2005) 35-48
77. Phillips H.M., Murdoch J.N., Chaudhry B., Copp A.J., and Henderson D.J. Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ. Res. 96 (2005) 292-299
78. Rattner A., Hsieh J.-C., Smallwood P.M., Gilbert D.J., Copeland N.G., Jenkins N.A., and Nathans J. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2859-2863
79. Reya T., and Clevers H. Wnt signalling in stem cells and cancer. Nature 434 (2005) 843-850
80. Rodriguez-Niedenfuhr M., Dathe V., Jacob H.J., Prols F., and Christ B. Spatial and temporal pattern of Wnt-6 expression during chick development. Anat. Embryol. 206 (2003) 447-451
81. Schneider V.A., and Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15 (2001) 304-315
82. Schroeder K.E., Condic M.L., Eisenberg L.M., and Yost H.J. Spatially regulated translation in embryos: asymmetric expression of maternal Wnt-11 along the dorsal-ventral Wnt-11 along the dorsal-ventral axis in Xenopus. Dev. Biol. 214 (1999) 288-297
83. Schubert F.R., Mootoosamy R.C., Walters E.H., Graham A., Tumiotto L., Münsterberg A.E., Lumsden A., and Dietrich S. Wnt6 marks sites of epithelial transformations in the chick embryo. Mech. Dev. 114 (2002) 143-148
84. Semenov M.V., Tamai K., Brott B.K., Kühl M., Sokol S., and He X. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11 (2001) 951-961
85. Sheldahl L.C., Park M., Malbon C.C., and Moon R.T. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9 (1999) 695-698
86. 2+ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161 (2003) 769-777
87. Shibata M., Ono H., Hikasa H., Shinga J., and Taira M. Xenopus crescent encoding a Frizzled-like domain is expressed in the Spemann organizer and pronephros. Mech. Dev. 96 (2000) 243-246
88. Skromne I., and Stern C.D. Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128 (2001) 2915-2927
89. 2+ signaling by Wnt-5A. Dev. Biol. 182 (1997) 114-120
90. Smith W.C., and Harland R.M. Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67 (1991) 753-765
91. Sokol S., Christian J.L., Moon R.T., and Melton D.A. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67 (1991) 741-752
92. Solloway M.J., and Harvey R.P. Molecular pathways in myocardial development: a stem cell perspective. Cardiovasc. Res. 58 (2003) 264-277
93. Solnica-Krezel L. Genetic control of convergent extension movements during zebrafish gastrulation. FASEB J. 15 (2001) A745
94. Tada M., and Smith J.C. Xwnt-11 is a target of Xenopus Brachyury: regulation of gastrulation movements via dishevelled, but not through the canonical Wnt pathway. Development 127 (2000) 2227-2238
95. Takada S., Stark K.L., Shea M.J., Vassileva G., McMahon J.A., and McMahon A.P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8 (1994) 174-189
96. Terami H., Hidaka K., Katsumata T., Iio A., and Morisaki T. Wnt11 facilitates embryonic stem cell differentiation to Nkx2.5-positive cardiomyocytes. Biochem. Biophys. Res. Commun. 325 (2004) 968-975
97. Terry K., Magan H., Baranski M., and Burrus L.W. Sfrp-1 and sfrp-2 are expressed in overlapping and distinct domains during chick development. Mech. Dev. 97 (2000) 177-182
98. Tolwinski N.S., and Wieschaus E. Rethinking WNT signaling. Trends Genet. 20 (2004) 177-181
99. Topol L., Jiang X., Choi H., Garrett-Beal L., Carolan P.J., and Yang Y. Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J. Cell Biol. 162 (2003) 899-908
100. Torres M.A., Yang-Snyder J.A., Purcell S.M., DeMarais A.A., McGrew L.L., and Moon R.T. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus embryos. J. Cell Biol. 133 (1996) 1123-1137
101. Ulrich F., Krieg M., Schotz E.M., Link V., Castanon I., Schnabel V., Taubenberger A., Mueller D., Puech P.H., and Heisenberg C.P. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9 (2005) 555-564
102. van den Hoff M.J.B., Kruithof B.P.T., and Moorman A.F.M. Making more heart muscle. BioEssays 26 (2004) 248-261
103. Veeman M.T., Axelrod J.D., and Moon R.T. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5 (2003) 367-377
104. Wang J., and Wynshaw-Boris A. The canonical Wnt pathway in early mammalian embryogenesis and stem cell maintenance/differentiation. Curr. Opin. Genet. Dev. 14 (2004) 533-539
105. Wang S., Krinks M., Lin K., Luyten F.P., and Moos- Jr. M. Frzb, a secreted protein expressed in the Spemann Organizer, binds and inhibits Wnt-8. Cell 88 (1997) 757-766
106. Wang S., Krinks M., and Moos- Jr. M. Frzb-1, an antagonist of Wnt-1 and Wnt-8, does not block signaling by Wnts-3a, -5a, or -11. Biochem. Biophys. Res. Commun. 236 (1997) 502-504
107. Weidinger G., and Moon R.T. When Wnts antagonize Wnts. J. Cell Biol. 162 (2003) 753-755
108. Westfall T.A., Brimeyer R., Twedt J., Gladon J., Olberding A., Furutani-Seiki M., and Slusarski D.C. Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/beta-catenin activity. J. Cell Biol. 162 (2003) 889-898
109. Wong G.T., Gavin B.J., and McMahon A.P. Differential transformation of mammary epithelial cells by Wnt genes. Mol. Cell. Biol. 14 (1994) 6278-6286
110. Yamaguchi T.P., Bradley A., McMahon A.P., and Jones S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126 (1999) 1211-1223
111. Yuasa S., Itabashi Y., Koshimizu U., Tanaka T., Sugimura K., Kinoshita M., Hattori F., Fukami S., Shimazaki T., Okano H., Ogawa S., and Fukuda K. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. 23 (2005) 607-611
112. Zakin L.D., Mazan S., Maury M., Martin N., Guenet J.L., and Brulet P. Structure and expression of Wnt13, a novel mouse Wnt2 related gene. Mech. Dev. 73 (1998) 107-116