Frs2α-deficiency in cardiac progenitors disrupts a subset of FGF signals required for outflow tract morphogenesis

Development

Volumn 135, Issue 21, 2008, Pages 3611-3622

  Zhang, Jue ^a   Lin, Yongshun ^a   Zhang, Yongyou ^a   Lan, Yongsheng ^a   Lin, Chunhong ^a   Moon, Anne M ^b   Schwartz, Robert J ^a   Martin, James F ^a   Wang, Fen ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

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

Author keywords

Cell signaling; Heart development; Mouse model; Receptor tyrosine kinase; Second heart field

Indexed keywords

ADAPTOR PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR SUBSTRATE 2; PROTEIN KINASE; UNCLASSIFIED DRUG; FGFR1 PROTEIN, MOUSE; FGFR2 PROTEIN, MOUSE; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FRS2ALPHA PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; AORTOPULMONARY SEPTAL DEFECT; ARTICLE; CELL TRANSPORT; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM; HEART DEVELOPMENT; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART MUSCLE; HEART RIGHT VENTRICLE DOUBLE OUTLET; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VENTRICLE SEPTUM DEFECT; MESENCHYME; MESODERM; MORPHOGENESIS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; BRANCHIAL ARCH; CYTOLOGY; ENDODERM; ENZYME ACTIVATION; ENZYMOLOGY; EPITHELIUM; GENETICS; HEART; HISTOLOGY; METABOLISM; MUTATION; NEURAL CREST; PRENATAL DEVELOPMENT;

ANIMALS; BODY PATTERNING; BRANCHIAL REGION; ENDODERM; ENZYME ACTIVATION; EPITHELIUM; FIBROBLAST GROWTH FACTORS; HEART; MEMBRANE PROTEINS; MESODERM; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MORPHOGENESIS; MUTATION; MYOCARDIUM; NEURAL CREST; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 57349186277     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.025361     Document Type: Article

References (62)

1. Aggarwal, V. S., Liao, J., Bondarev, A., Schimmang, T., Lewandoski, M., Locker, J., Shanske, A., Campione, M. and Morrow, B. E. (2006). Dissection of Tbx1 and Fgf interactions in mouse models of 22q11DS suggests functional redundancy. Hum. Mol. Genet. 15, 3219-3228.
2. Ai, D., Liu, W., Ma, L., Dong, F., Lu, M. F., Wang, D., Verzi, M. P., Cai, C., Gage, P. J., Evans, S. et al. (2006). Pitx2 regulates cardiac left-right asymmetry by patterning second cardiac lineage-derived myocardium. Dev. Biol. 296, 437-449.
3. 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.
4. Armstrong, E. J. and Bischoff, J. (2004). Heart valve development: endothelial cell signaling and differentiation. Circ. Res. 95, 459-470.
5. Avery, A. W., Figueroa, C. and Vojtek, A. B. (2007). UNC-51-like kinase regulation of fibroblast growth factor receptor substrate 2/3. Cell Signal. 19, 177-184.
6. Buckingham, M., Meilhac, S. and Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6, 826-835.
7. 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.
8. Chang, C. P., Neilson, J. R., Bayle, J. H., Gestwicki, J. E., Kuo, A., Stankunas, K., Graef, I. A. and Crabtree, G. R. (2004). A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 118, 649-663.
9. Choi, K. Y., Kim, H. J., Lee, M. H., Kwon, T. G., Nah, H. D., Furuichi, T., Komori, T., Nam, S. H., Kim, Y. J., Kim, H. J. et al. (2005). Runx2 regulates FGF2-induced Bmp2 expression during cranial bone development. Dev. Dyn. 233, 115-121.
10. 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.
11. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. and McMahon, A. P. (1998). Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323-1326.
12. Edmondson, D. G., Lyons, G. E., Martin, J. F. and Olson, E. N. (1994). Mef2 gene expression marks the cardiac and skeletal muscle lineages during mouse embryogenesis. Development 120, 1251-1263.
13. Enciso, J. M., Gratzinger, D., Camenisch, T. D., Canosa, S., Pinter, E. and Madri, J. A. (2003). Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J. Cell Biol. 160, 605-615.
14. Eswarakumar, V. P., Lax, I. and Schlessinger, J. (2005). Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139-149.
15. Frank, D. U., Fotheringham, L. K., Brewer, J. A., Muglia, L. J., Tristani-Firouzi, M., Capecchi, M. R. and Moon, A. M. (2002). An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 129, 4591-4603.
16. Galli, D., Dominguez, J. N., Zaffran, S., Munk, A., Brown, N. A. and Buckingham, M. E. (2008). Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed. Development 135, 1157-1167.
17. Gotoh, N., Manova, K., Tanaka, S., Murohashi, M., Hadari, Y., Lee, A., Hamada, Y., Hiroe, T., Ito, M., Kurihara, T. et al. (2005). The docking protein FRS2alpha is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol. Cell. Biol. 25, 4105-4116.
18. Grego-Bessa, J., Luna-Zurita, L., del Monte, G., Bolos, V., Melgar, P., Arandilla, A., Garratt, A. N., Zang, H., Mukouyama, Y. S., Chen, H. et al. (2007). Notch signaling is essential for ventricular chamber development. Dev. Cell 12, 415-429.
19. Guris, D. L., Fantes, J., Tara, D., Druker, B. J. and Imamoto, A. (2001). Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat. Genet. 27, 293-298.
20. Hadari, Y. R., Gotoh, N., Kouhara, H., Lax, I. and Schlessinger, J. (2001). Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways. Proc. Natl. Acad. Sci. USA 98, 8578-8583.
21. Hoch, R. V. and Soriano, P. (2006). Context-specific requirements for Fgfr1 signaling through Frs2 and Frs3 during mouse development. Development 133, 663-673.
22. Hutson, M. R. and Kirby, M. L. (2003). Neural crest and cardiovascular development: a 20-year perspective. Birth Defects Res. C Embryo Today 69, 2-13.
23. Hutson, M. R., Zhang, P., Stadt, H. A., Sato, A. K., Li, Y. X., Burch, J., Creazzo, T. L. and Kirby, M. L. (2006). Cardiac arterial pole alignment is sensitive to FGF8 signaling in the pharynx. Dev. Biol. 295, 486-497.
24. Ilagan, R., Abu-Issa, R., Brown, D., Yang, Y. P., Jiao, K., Schwartz, R. J., Klingensmith, J. and Meyers, E. N. (2006). Fgf8 is required for anterior heart field development. Development 133, 2435-2445.
25. Kelly, R. G., Brown, N. A. and Buckingham, M. E. (2001). The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1, 435-440.
26. Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., Williams, S. C., Richardson, J. A. and Yanagisawa, M. (2001). Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242.
27. Kouhara, H., Hadari, Y. R., Spivak-Kroizman, T., Schilling, J., Bar-Sagi, D., Lax, I. and Schlessinger, J. (1997). A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell 89, 693-702.
28. Lamers, W. H. and Moorman, A. F. (2002). Cardiac septation: a late contribution of the embryonic primary myocardium to heart morphogenesis. Circ. Res. 91, 93-103.
29. Larsson, H., Klint, P., Landgren, E. and Claesson-Welsh, L. (1999). Fibroblast growth factor receptor-1-mediated endothelial cell proliferation is dependent on the Src homology (SH) 2/SH3 domain- containing adaptor protein Crk. J. Biol. Chem. 274, 25726-25734.
30. Liao, J., Kochilas, L., Nowotschin, S., Arnold, J. S., Aggarwal, V. S., Epstein, J. A., Brown, M. C., Adams, J. and Morrow, B. E. (2004). Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet. 13, 1577-1585.
31. Lin, L., Cui, L., Zhou, W., Dufort, D., Zhang, X., Cai, C. L., Bu, L., Yang, L., Martin, J., Kemler, R. et al. (2007). Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc. Natl. Acad. Sci. USA 104, 9313-9318.
32. Lin, Y., Zhang, J., Zhang, Y. and Wang, F. (2007). Generation of an Frs2alpha conditional null allele. Genesis 45, 554-559.
33. Lindsay, E. A., Vitelli, F., Su, H., Morishima, M., Huynh, T., Pramparo, T., Jurecic, V., Ogunrinu, G., Sutherland, H. F., Scambler, P. J. et al. (2001). Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410, 97-101.
34. Liu, W., Selever, J., Wang, D., Lu, M. F., Moses, K. A., Schwartz, R. J. and Martin, J. F. (2004). Bmp4 signaling is required for outflow-tract septation and branchial-arch artery remodeling. Proc. Natl. Acad. Sci. USA 101, 4489-4494.
35. Ma, L., Lu, M. F., Schwartz, R. J. and Martin, J. F. (2005). Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132, 5601-5611.
36. Macian, F. (2005). NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 5, 472-484.
37. Marguerie, A., Bajolle, F., Zaffran, S., Brown, N. A., Dickson, C., Buckingham, M. E. and Kelly, R. G. (2006). Congenital heart defects in Fgfr2-IIIb and Fgf10 mutant mice. Cardiovasc. Res. 71, 50-60.
38. McDougall, K., Kubu, C., Verdi, J. M. and Meakin, S. O. (2001). Developmental expression patterns of the signaling adapters FRS-2 and FRS-3 during early embryogenesis. Mech. Dev. 103, 145-148.
39. McKeehan, W. L., Wang, F. and Kan, M. (1998). The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acid Res. Mol. Biol. 59, 135-176.
40. Mohammadi, M., Dionne, C. A., Li, W., Li, N., Spivak, T., Honegger, A. M., Jaye, M. and Schlessinger, J. (1992). Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature 358, 681-684.
41. Moon, A. M., Guris, D. L., Seo, J. H., Li, L., Hammond, J., Talbot, A. and Imamoto, A. (2006). Crkl deficiency disrupts Fgf8 signaling in a mouse model of 22q11 deletion syndromes. Dev. Cell 10, 71-80.
42. Moses, K. A., DeMayo, F., Braun, R. M., Reecy, J. L. and Schwartz, R. J. (2001). Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31, 176-180.
43. Ong, S. H., Goh, K. C., Lim, Y. P., Low, B. C., Klint, P., Claesson-Welsh, L., Cao, X., Tan, Y. H. and Guy, G. R. (1996). Suc1-associated neurotrophic factor target (SNT) protein is a major FGF- stimulated tyrosine phosphorylated 90-kDa protein which binds to the SH2 domain of GRB2. Biochem. Biophys. Res. Commun. 225, 1021-1026.
44. Ong, S. H., Guy, G. R., Hadari, Y. R., Laks, S., Gotoh, N., Schlessinger, J. and Lax, I. (2000). FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol. Cell. Biol. 20, 979-989.
45. Ornitz, D. M. (2000). FGFs, heparan sulfate and FGFRs: complex interactions essential for development. BioEssays 22, 108-112.
46. Park, E. J., Ogden, L. A., Talbot, A., Evans, S., Cai, C. L., Black, B. L., Frank, D. U. and Moon, A. M. (2006). Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133, 2419-2433.
47. Park, E. J., Watanabe, Y., Smyth, G., Miyagawa-Tomita, S., Meyers, E., Klingensmith, J., Camenisch, T., Buckingham, M. and Moon, A. M. (2008). An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 135, 3599-3610.
48. 2+ flux but not mitogenesis. Nature 358, 678-681.
49. Rosamond, W., Flegal, K., Friday, G., Furie, K., Go, A., Greenlund, K., Haase, N., Ho, M., Howard, V., Kissela, B. et al. (2007). Heart disease and stroke statistics-2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 115, e69-e171.
50. Srivastava, D. (2006). Making or breaking the heart: from lineage determination to morphogenesis. Cell 126, 1037-1048.
51. Stottmann, R. W., Choi, M., Mishina, Y., Meyers, E. N. and Klingensmith, J. (2004). BMP receptor IA is required in mammalian neural crest cells for development of the cardiac outflow tract and ventricular myocardium. Development 131, 2205-2218.
52. Trokovic, N., Trokovic, R. and Partanen, J. (2005). Fibroblast growth factor signalling and regional specification of the pharyngeal ectoderm. Int. J. Dev. Biol. 49, 797-805.
53. Trokovic, R., Trokovic, N., Hernesniemi, S., Pirvola, U., Vogt Weisenhorn, D. M., Rossant, J., McMahon, A. P., Wurst, W. and Partanen, J. (2003). FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J. 22, 1811-1823.
54. Verzi, M. P., McCulley, D. J., De Val, S., Dodou, E. and Black, B. L. (2005). The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 287, 134-145.
55. Vincentz, J. W., McWhirter, J. R., Murre, C., Baldini, A. and Furuta, Y. (2005). Fgf15 is required for proper morphogenesis of the mouse cardiac outflow tract. Genesis 41, 192-201.
56. Vitelli, F., Taddei, I., Morishima, M., Meyers, E. N., Lindsay, E. A. and Baldini, A. (2002). A genetic link between Tbx1 and fibroblast growth factor signaling. Development 129, 4605-4611.
57. Vitelli, F., Zhang, Z., Huynh, T., Sobotka, A., Mupo, A. and Baldini, A. (2006). Fgf8 expression in the Tbx1 domain causes skeletal abnormalities and modifies the aortic arch but not the outflow tract phenotype of Tbx1 mutants. Dev. Biol. 295, 559-570.
58. Ward, C., Stadt, H., Hutson, M. and Kirby, M. L. (2005). Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev. Biol. 284, 72-83.
59. Wright, T. J., Hatch, E. P., Karabagli, H., Karabagli, P., Schoenwolf, G. C. and Mansour, S. L. (2003). Expression of mouse fibroblast growth factor and fibroblast growth factor receptor genes during early inner ear development. Dev. Dyn. 228, 267-272.
60. Yamamoto, S., Yoshino, I., Shimazaki, T., Murohashi, M., Hevner, R. F., Lax, I., Okano, H., Shibuya, M., Schlessinger, J. and Gotoh, N. (2005). Essential role of Shp2-binding sites on FRS2alpha for corticogenesis and for FGF2-dependent proliferation of neural progenitor cells. Proc. Natl. Acad. Sci. USA 102, 15983-15988.
61. Yu, K., Xu, J., Liu, Z., Sosic, D., Shao, J., Olson, E. N., Towler, D. A. and Ornitz, D. M. (2003). Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074.
62. Zhang, Y., McKeehan, K., Lin, Y., Zhang, J. and Wang, F. (2008). FGFR1 tyrosine phosphorylation regulates binding of FRS2alpha but not FRS2beta to the receptor. Mol. Endocrinol. 22, 167-175.