Wnt5a and wnt11 are essential for second heart field progenitor development

Development

Volumn 139, Issue 11, 2012, Pages 1931-1940

  Cohen, Ethan David ^a   Miller, Mayumi F ^c   Wang, Zichao ^a   Moon, Randall T ^b   Morrisey, Edward E ^c  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cardiac development; Mouse; Progenitor; Wnt

Indexed keywords

BETA CATENIN; WNT11 PROTEIN; WNT5A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYONIC STEM CELL; HEART DEVELOPMENT; HEART STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; BLOTTING, WESTERN; HEART; HISTOLOGICAL TECHNIQUES; MICE; MICE, MUTANT STRAINS; MYOCARDIUM; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

MUS;

EID: 84860703695     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.069377     Document Type: Article

References (62)

1. Abdul-Ghani, M., Dufort, D., Stiles, R., De Repentigny, Y., Kothary, R. and Megeney, L. A. (2011). Wnt11 promotes cardiomyocyte development by caspase-mediated suppression of canonical Wnt signals. Mol. Cell. Biol. 31, 163-178.
2. Ai, D., Fu, X., Wang, J., Lu, M. F., Chen, L., Baldini, A., Klein, W. H. and Martin, J. F. (2007). Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc. Natl. Acad. Sci. USA 104, 9319-9324.
3. Baranski, M., Berdougo, E., Sandler, J. S., Darnell, D. K. and Burrus, L. W. (2000). The dynamic expression pattern of frzb-1 suggests multiple roles in chick development. Dev. Biol. 217, 25-41.
4. Biechele, T. L., Adams, A. M. and Moon, R. T. (2009). Transcription-based reporters of Wnt/beta-catenin signaling. Cold Spring Harb. Protoc. 2009, pdb prot5223.
5. Bondue, A., Lapouge, G., Paulissen, C., Semeraro, C., Iacovino, M., Kyba, M. and Blanpain, C. (2008). Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 3, 69-84.
6. Bruneau, B. G., Logan, M., Davis, N., Levi, T., Tabin, C. J., Seidman, J. G. and Seidman, C. E. (1999). Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev. Biol. 211, 100-108.
7. Brunner, E., Peter, O., Schweizer, L. and Basler, K. (1997). Pangolin encodes a Lef-1 homologue that acts downstream of Armadillo to transduce the Wingless signal in Drosophila. Nature 385, 829-833.
8. Cai, C. L., Liang, X., Shi, Y., Chu, P. H., Pfaff, S. L., Chen, J. and Evans, S. (2003). Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5, 877-889.
9. Cha, S. W., Tadjuidje, E., Tao, Q., Wylie, C. and Heasman, J. (2008). Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. Development 135, 3719-3729.
10. Cha, S. W., Tadjuidje, E., White, J., Wells, J., Mayhew, C., Wylie, C. and Heasman, J. (2009). Wnt11/5a complex formation caused by tyrosine sulfation increases canonical signaling activity. Curr. Biol. 19, 1573-1580.
11. Cohen, E. D., Wang, Z., Lepore, J. J., Lu, M. M., Taketo, M. M., Epstein, D. J. and Morrisey, E. E. (2007). Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest. 117, 1794-1804.
12. Cohen, E. D., Tian, Y. and Morrisey, E. E. (2008). Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development 135, 789-798.
13. Dyer, L. A. and Kirby, M. L. (2009). The role of secondary heart field in cardiac development. Dev. Biol. 336, 137-144.
14. Eisenberg, C. A. and Eisenberg, L. M. (1999). WNT11 promotes cardiac tissue formation of early mesoderm. Dev. Dyn. 216, 45-58.
15. Fuerer, C. and Nusse, R. (2010). Lentiviral vectors to probe and manipulate the Wnt signaling pathway. PLoS ONE 5, e9370.
16. Hardy, K. M., Garriock, R. J., Yatskievych, T. A., D'Agostino, S. L., Antin, P. B. and Krieg, P. A. (2008). Non-canonical Wnt signaling through Wnt5a/b and a novel Wnt11 gene, Wnt11b, regulates cell migration during avian gastrulation. Dev. Biol. 320, 391-401.
17. Huang, S. M., Mishina, Y. M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G. A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S. et al. (2009). Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461, 614-620.
18. Ishitani, T., Ninomiya-Tsuji, J., Nagai, S., Nishita, M., Meneghini, M., Barker, N., Waterman, M., Bowerman, B., Clevers, H., Shibuya, H. et al. (1999). The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399, 798-802.
19. Ishitani, T., Kishida, S., Hyodo-Miura, J., Ueno, N., Yasuda, J., Waterman, M., Shibuya, H., Moon, R. T., Ninomiya-Tsuji, J. and Matsumoto, K. (2003). The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol. Cell. Biol. 23, 131-139.
20. James, R. G., Conrad, W. H. and Moon, R. T. (2008). Beta-catenin-independent Wnt pathways: signals, core proteins, and effectors. Methods Mol. Biol. 468, 131-144.
21. Kispert, A., Vainio, S., Shen, L., Rowitch, D. H. and McMahon, A. P. (1996). Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122, 3627-3637.
22. Kitajima, S., Takagi, A., Inoue, T. and Saga, Y. (2000). MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 127, 3215-3226.
23. Klaus, A., Saga, Y., Taketo, M. M., Tzahor, E. and Birchmeier, W. (2007). Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis. Proc. Natl. Acad. Sci. USA 104, 18531-18536.
24. Ko, B. S., Chang, T. C., Shyue, S. K., Chen, Y. C. and Liou, J. Y. (2009). An efficient transfection method for mouse embryonic stem cells. Gene Therapy 16, 154-158.
25. Korinek, V., Barker, N., Willert, K., Molenaar, M., Roose, J., Wagenaar, G., Markman, M., Lamers, W., Destree, O. and Clevers, H. (1998). Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol. Cell. Biol. 18, 1248-1256.
26. Koyanagi, M., Haendeler, J., Badorff, C., Brandes, R. P., Hoffmann, J., Pandur, P., Zeiher, A. M., Kuhl, M. and Dimmeler, S. (2005). Non-canonical Wnt signaling enhances differentiation of human circulating progenitor cells to cardiomyogenic cells. J. Biol. Chem. 280, 16838-16842.
27. Koyanagi, M., Iwasaki, M., Haendeler, J., Leitges, M., Zeiher, A. M. and Dimmeler, S. (2009). Wnt5a increases cardiac gene expressions of cultured human circulating progenitor cells via a PKC delta activation. PLoS ONE 4, e5765.
28. Kwon, C., Arnold, J., Hsiao, E. C., Taketo, M. M., Conklin, B. R. and Srivastava, D. (2007). Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc. Natl. Acad. Sci. USA 104, 10894-10899.
29. Kwon, C., Qian, L., Cheng, P., Nigam, V., Arnold, J. and Srivastava, D. (2009). A regulatory pathway involving Notch1/beta-catenin/Isl1 determines cardiac progenitor cell fate. Nat. Cell Biol. 11, 951-957.
30. Lindsley, R. C., Gill, J. G., Kyba, M., Murphy, T. L. and Murphy, K. M. (2006). Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133, 3787-3796.
31. Lindsley, R. C., Gill, J. G., Murphy, T. L., Langer, E. M., Cai, M., Mashayekhi, M., Wang, W., Niwa, N., Nerbonne, J. M., Kyba, M. et al. (2008). Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 3, 55-68.
32. Liou, J. Y., Ko, B. S. and Chang, T. C. (2010). An efficient transfection method for mouse embryonic stem cells. Methods Mol. Biol. 650, 145-153.
33. Majumdar, A., Vainio, S., Kispert, A., McMahon, J. and McMahon, A. P. (2003). Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130, 3175-3185.
34. Malbon, C. C. (2004). Frizzleds: new members of the superfamily of G-protein-coupled receptors. Front. Biosci. 9, 1048-1058.
35. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
36. Mikels, A. J. and Nusse, R. (2006). Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 4, e115.
37. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destree, O. and Clevers, H. (1996). XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399.
38. Nagy, I. I., Railo, A., Rapila, R., Hast, T., Sormunen, R., Tavi, P., Rasanen, J. and Vainio, S. J. (2010). Wnt-11 signalling controls ventricular myocardium development by patterning N-cadherin and beta-catenin expression. Cardiovasc. Res. 85, 100-109.
39. Naito, A. T., Shiojima, I., Akazawa, H., Hidaka, K., Morisaki, T., Kikuchi, A. and Komuro, I. (2006). Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Natl. Acad. Sci. USA 103, 19812-19817.
40. Pandur, P., Lasche, M., Eisenberg, L. M. and Kuhl, M. (2002). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641.
41. Provost, E., Yamamoto, Y., Lizardi, I., Stern, J., D'Aquila, T. G., Gaynor, R. B. and Rimm, D. L. (2003). Functional correlates of mutations in beta-catenin exon 3 phosphorylation sites. J. Biol. Chem. 278, 31781-31789.
42. Riley, P., Anson-Cartwright, L. and Cross, J. C. (1998). The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat. Genet. 18, 271-275.
43. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. and Inoue, T. (1999). MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126, 3437-3447.
44. Saga, Y., Kitajima, S. and Miyagawa-Tomita, S. (2000). Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc. Med. 10, 345-352.
45. Schleiffarth, J. R., Person, A. D., Martinsen, B. J., Sukovich, D. J., Neumann, A., Baker, C. V., Lohr, J. L., Cornfield, D. N., Ekker, S. C. and Petryk, A. (2007). Wnt5a is required for cardiac outflow tract septation in mice. Pediatr. Res. 61, 386-391.
46. Schlessinger, K., Hall, A. and Tolwinski, N. (2009). Wnt signaling pathways meet Rho GTPases. Genes Dev. 23, 265-277.
47. Schneider, V. A. and Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15, 304-315.
48. Terami, H., Hidaka, K., Katsumata, T., Iio, A. and Morisaki, T. (2004). Wnt11 facilitates embryonic stem cell differentiation to Nkx2.5-positive cardiomyocytes. Biochem. Biophys. Res. Commun. 325, 968-975.
49. Thomas, T., Yamagishi, H., Overbeek, P. A., Olson, E. N. and Srivastava, D. (1998). The bHLH factors, dHAND and eHAND, specify pulmonary and systemic cardiac ventricles independent of left-right sidedness. Dev. Biol. 196, 228-236.
50. Tian, Y., Cohen, E. D. and Morrisey, E. E. (2010a). The importance of Wnt signaling in cardiovascular development. Pediatr. Cardiol. 31, 342-348.
51. Tian, Y., Yuan, L., Goss, A. M., Wang, T., Yang, J., Lepore, J. J., Zhou, D., Schwartz, R. J., Patel, V., Cohen, E. D. et al. (2010b). Characterization and in vivo pharmacological rescue of a Wnt2-Gata6 pathway required for cardiac inflow tract development. Dev. Cell 18, 275-287.
52. Torres, M. A., Yang-Snyder, J. A., Purcell, S. M., DeMarais, A. A., McGrew, L. L. and Moon, R. T. (1996). 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 development. J. Cell Biol. 133, 1123-1137.
53. Tsuchihashi, T., Maeda, J., Shin, C. H., Ivey, K. N., Black, B. L., Olson, E. N., Yamagishi, H. and Srivastava, D. (2011). Hand2 function in second heart field progenitors is essential for cardiogenesis. Dev. Biol. 351, 62-69.
54. Tzahor, E. (2007). Wnt/beta-catenin signaling and cardiogenesis: timing does matter. Dev. Cell 13, 10-13.
55. Ueno, S., Weidinger, G., Osugi, T., Kohn, A. D., Golob, J. L., Pabon, L., Reinecke, H., Moon, R. T. and Murry, C. E. (2007). Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 9685-9690.
56. Wang, Z., Shu, W., Lu, M. M. and Morrisey, E. E. (2005). Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol. Cell. Biol. 25, 5022-5030.
57. Watanabe, Y. and Buckingham, M. (2010). The formation of the embryonic mouse heart: heart fields and myocardial cell lineages. Ann. N. Y. Acad. Sci. 1188, 15-24.
58. Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223.
59. Young, C. S., Kitamura, M., Hardy, S. and Kitajewski, J. (1998). Wnt-1 induces growth, cytosolic beta-catenin, and Tcf/Lef transcriptional activation in Rat-1 fibroblasts. Mol. Cell. Biol. 18, 2474-2485.
60. Yuan, Y., Niu, C. C., Deng, G., Li, Z. Q., Pan, J., Zhao, C., Yang, Z. L. and Si, W. K. (2011). The Wnt5a/Ror2 noncanonical signaling pathway inhibits canonical Wnt signaling in K562 cells. Int. J. Mol. Med. 27, 63-69.
61. Zhang, Y., Goss, A. M., Cohen, E. D., Kadzik, R., Lepore, J. J., Muthukumaraswamy, K., Yang, J., DeMayo, F. J., Whitsett, J. A., Parmacek, M. S. et al. (2008). A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat. Genet. 40, 862-870.
62. Zhou, W., Lin, L., Majumdar, A., Li, X., Zhang, X., Liu, W., Etheridge, L., Shi, Y., Martin, J., Van de Ven, W. et al. (2007). Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat. Genet. 39, 1225-1234.