Fibroblast growth factor receptor-1 phosphorylation requirement for cardiomyocyte differentiation in murine embryonic stem cells

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 8 A, 2009, Pages 1489-1498

  Ronca, Roberto ^a   Gualandi, Laura ^a   Crescini, Elisabetta ^a   Calza, Stefano ^a   Presta, Marco ^a   Dell'era, Patrizia ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Cardiomyocyte; Embryonic stem cells; FGFR

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; PHOSPHOTYROSINE; PROTEIN TYROSINE KINASE;

ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; ENZYMOLOGY; GENETIC TRANSDUCTION; HEART MUSCLE CELL; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; HUMANS; MICE; MYOCYTES, CARDIAC; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN-TYROSINE KINASES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; TRANSDUCTION, GENETIC;

LENTIVIRUS; MURINAE;

EID: 70349322845     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00805.x     Document Type: Article

References (64)

1. Mohun T, Sparrow D. Early steps in vertebrate cardiogenesis. Curr Opin Genet Dev. 1997 7 : 628 33.
2. Kattman SJ, Huber TL, Keller GM. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell. 2006 11 : 723 32.
3. Morettl A, Caron L, Nakano A, et al. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell. 2006 127 : 1151 65.
4. Wu SM, Fujlwara Y, Clbulsky SM, et al. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell. 2006 127 : 1137 50.
5. Chen K, Wu L, Wang ZZ. Extrinsic regulation of cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem. 2008 104 : 119 28.
6. Buckingham M, Meilhac S, Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet. 2005 6 : 826 835.
7. Bruneau BG, Nemer G, Schmitt J P, et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell. 2001 106 : 709 721.
8. Zaffran S, Kelly RG, Meilhac SM, et al. Right ventricular myocardium derives from the anterior heart field. Circ Res. 2004 95 : 261 268.
9. Cai CL, Liang X, Shi Y, et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell. 2003 5 : 877 889.
10. Kelly RG, Brown NA, Buckingham ME. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell. 2001 1 : 435 440.
11. Srivastava D. Making or breaking the heart: from lineage determination to morphogenesis. Cell. 2006 126 : 1037 1048.
12. Nishikawa S, Jakt LM, Era T. Embryonic stem-cell culture as a tool for developmental cell biology. Nat Rev Mol Cell Biol. 2007 8 : 502 507.
13. Desbaillets I, Ziegler U, Groscurth P, et al. Embryoid bodies: an in vitro model of mouse embryogenesis. Exp Physiol. 2000 85 : 645 651.
14. Boheler KR, Czyz J, Tweedie D, et al. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res. 2002 91 : 189 201.
15. Maltsev VA, Rohwedel J, Hescheler J, et al. Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev. 1993 44 : 41 50.
16. Sachinidis A, Kolossov E, Fleischmann BK, et al. Generation of cardiomyocytes from embryonic stem cells experimental studies. Herz. 2002 27 : 589 597.
17. Fantl WJ, Johnson DE, Williams LT. Signalling by receptor tyrosine kinases. Annu Rev Biochem. 1993 62 : 453 481.
18. Chen GJ, Forough R. Fibroblast growth factors, fibroblast growth factor receptors, diseases, and drugs. Recent Pat Cardiovasc Drug Discov. 2006 1 : 211 224.
19. Powers CJ, McLeskey SW, Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr Relat Cancer. 2000 7 : 165 197.
20. Presta M, Dell'Era P, Mitola S, et al. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005 16 : 159 178.
21. Mohammadi M, Dikic I, Sorokin A, et al. Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol Cell Biol. 1996 16 : 977 989.
22. Larsson H, Klint P, Landgren E, et al. 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. 1999 274 : 25726 25734.
23. Mohammadi M, Honegger AM, Rotin D, et al. A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor (Flg) is a binding site for the SH2 domain of phospholipase C-gamma 1. Mol Cell Biol. 1991 11 : 5068 5078.
24. Cross MJ, Lu L, Magnusson P, et al. The Shb adaptor protein binds to tyrosine 766 in the FGFR-1 and regulates the Ras/MEK/MAPK pathway via FRS2 phosphorylation in endothelial cells. Mol Biol Cell. 2002 13 : 2881 2893.
25. Cailliau K, Perdereau D, Lescuyer A, et al. FGF receptor phosphotyrosine 766 is a target for Grb14 to inhibit MDA-MB-231 human breast cancer cell signaling. Anticancer Res. 2005 25 : 3877 3882.
26. Kouhara H, Hadari YR, Spivak-Kroizman T, et al. A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell. 1997 89 : 693 702.
27. Hadari YR, Kouhara H, Lax I, et al. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol Cell Biol. 1998 18 : 3966 3973.
28. Hug H, Sarre TF. Protein kinase C isoenzymes: divergence in signal transduction? Biochem J. 1993 291 : 329 343.
29. Zhou X, Quann E, Gallicano GI. Differentiation of nonbeating embryonic stem cells into beating cardiomyocytes is dependent on downregulation of PKC beta and zeta in concert with upregulation of PKC epsilon. Dev Biol. 2003 255 : 407 422.
30. Xu X, Weinstein M, Li C, Deng C. Fibroblast growth factor receptors (FGFRs) and their roles in limb development. Cell Tissue Res. 1999 296 : 33 43.
31. Yamaguchi TP, Harpal K, Henkemeyer M, et al. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994 8 : 3032 3044.
32. Deng CX, Wynshaw-Boris A, Shen MM, et al. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994 8 : 3045 3057.
33. Ciruna BG, Schwartz L, Harpal K, et al. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development. 1997 124 : 2829 2841.
34. Deng C, Bedford M, Li C, et al. Fibroblast growth factor receptor-1 (FGFR-1) is essential for normal neural tube and limb development. Dev Biol. 1997 185 : 42 54.
35. Davidson B. Ciona intestinalis as a model for cardiac development. Semin Cell Dev Biol. 2007 18 : 16 26.
36. Beiman M, Shilo BZ, Volk T. Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev. 1996 10 : 2993 3002.
37. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature. 1995 374 : 464 467.
38. Alsan BH, Schultheiss TM. Regulation of avian cardiogenesis by Fgf8 signaling. Development. 2002 129 : 1935 1943.
39. Reifers F, Walsh EC, Leger S, et al. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development. 2000 127 : 225 235.
40. Abu-Issa R, Smyth G, Smoak I, et al. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development. 2002 129 : 4613 4625.
41. Dell'Era P, Ronca R, Coco L, et al. Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circ Res. 2003 93 : 414 420.
42. Mohammadi M, McMahon G, Sun L, et al. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science. 1997 276 : 955 960.
43. Favata MF, Horiuchi KY, Manos EJ, et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem. 1998 273 : 18623 18632.
44. Kuchera S, Barth H, Jacobson P, et al. Anti-inflammatory properties of the protein kinase C inhibitor, 3-[1-[3-(dimethylamino) propyl]-1H-indol-3-yl]- 4-(1H-indol-3-yl)-1H-pyrrole-2,5-dione monohydrochloride (GF109203X) in the PMA-mouse ear edema model. Agents Actions. 1993 39 Spec No : C169 73.
45. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 162 : 156 159.
46. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002 30 : e36.
47. Dell'Era P, Mohammadi M, Presta M. Different tyrosine autophosphorylation requirements in fibroblast growth factor receptor-1 mediate urokinase-type plasminogen activator induction and mitogenesis. Mol Biol Cell. 1999 10 : 23 33.
48. De Palma M, Naldini L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 2002 346 : 514 529.
49. Magnusson PU, Ronca R, Dell'Era P, et al. Fibroblast growth factor receptor-1 expression is required for hematopoietic but not endothelial cell development. Arterioscler Thromb Vasc Biol. 2005 25 : 944 949.
50. Kiselyov VV, Kochoyan A, Poulsen FM, et al. Elucidation of the mechanism of the regulatory function of the Ig1 module of the fibroblast growth factor receptor 1. Protein Sci. 2006 15 : 2318 2322.
51. Johnson DE, Williams LT. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res. 1993 60 : 1 41.
52. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 2005 16 : 139 149.
53. Vincentz JW, Barnes RM, Firulli BA, et al. Cooperative interaction of Nkx2.5 and Mef2c transcription factors during heart development. Dev Dyn. 2008 237 : 3809 3819.
54. Ericson J, Thor S, Edlund T, Jessell TM, Yamada T. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science. 1992 256 : 1555 1560.
55. Chapman DL, Garvey N, Hancock S, et al. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn. 1996 206 : 379 390.
56. Alessi DR, Cuenda A, Cohen P, et al. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995 270 : 27489 27494.
57. Thompson AK, Mostafapour SP, Denlinger LC, et al. The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation. J Biol Chem. 1991 266 : 23856 23862.
58. Cuenda A, Rouse J, Doza YN, et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 1995 364 : 229 233.
59. Lu CW, Yabuuchi A, Chen L, et al. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet. 2008 40 : 921 926.
60. Quinlan LR, Faherty S, Kane MT. Phospholipase C and protein kinase C involvement in mouse embryonic stem-cell proliferation and apoptosis. Reproduction. 2003 126 : 121 131.
61. Kook SH, Lee HJ, Chung WT, et al. Cyclic mechanical stretch stimulates the proliferation of C2C12 myoblasts and inhibits their differentiation via prolonged activation of p38 MAPK. Mol Cells. 2008 25 : 479 486.
62. Mohammadi M, Dionne CA, Li W, et al. Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature. 1992 358 : 681 684.
63. Besser D, Presta M, Nagamine Y. Elucidation of a signaling pathway induced by FGF-2 leading to uPA gene expression in NIH 3T3 fibroblasts. Cell Growth Differ. 1995 6 : 1009 1017.
64. Schonwasser DC, Marais RM, Marshall CJ, et al. Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol Cell Biol. 1998 18 : 790 798.